Acessibilidade / Reportar erro

Genetic analysis of fertility traits of Holstein dairy cattle in warm and temperate climate

Análise genética de traços de fertilidade em vacas leiteiras Holstein em climas quentes e temperados

ABSTRACT

The edited data set for the estimation of heritability, genetic and phenotypic correlations of fertility traits contained up to 23,402 records from 10,894 cows calved between 2001 and 2015. Heritability estimates for success in first service (FS), gestation length (GL), number of inseminations (NI), insemination outcome (IO), calving interval (CI), calving birth weight (CBW) and days open (DO) were low and ranged between 0.016 (DO) and 0.123 (GL). Repeatability of fertility traits was estimated to vary from 0.021 (FS) to 0.411 (IO). The genetic correlations between DO × CI, DO × NI and CI × NI were positive and nearly perfect (0.98, 0.88 and 0.88, respectively), while those between DO × IO and CI × IO were negative (-0.98 and -1, respectively). Further, the phenotypic correlations between DO × CI, DO × NI, CI × NI, CBW × IO and SF × IO were 0.99, 0.83, 0.83, 0.99 and 1, respectively, while those between DO × IO, CI × IO, GL × IO and NI × IO were -0.99, -0.99, -0.99 and -1, respectively. Overall genetic parameters imply a good practical management in heat stress conditions will be essential for improving fertility efficiency.

Keywords:
heritability; repeatability; genetic correlation; phenotypic correlation; heat stress

RESUMO

Os dados editados para definir a estimativa de herdabilidade, correlações genéticas e fenotípicas de características de fertilidade continham até 23,402 registros a partir de 10,894 vacas paridas entre 2001 e 2015. As estimativas de herdabilidade para o sucesso no primeiro serviço (SF), duração da gestação (GL), número de inseminações (NI), resultado de inseminação (IO), intervalo entre partos (CI), peso ao nascer (CBW) e dias abertos (DO) foram baixas e variaram entre 0,016 (DO) e 0,123 (GL). A repetitividade das características de fertilidade foi estimada e variou entre 0,021 (SF) e 0,411 (IO). A correlação genética entre DO × CI, DO × NI e CI × NI foi positiva e quase perfeita (0,98, 0,88 e 0,88, respectivamente), enquanto que aquela entre DO × IO e CI × IO foi negativa (-0,98 e -1, respectivamente). A correlação fenotípica entre DO × CI, DO × NI, CI × NI, CBW × IO e SF × IO foi 0,99, 0,83, 0,83, 0,99 e 1, respectivamente, enquanto aquela entre DO × IO, CI × IO, GL × IO e NI × IO foi -0,99, -0,99, -0,99 e -1, respectivamente. Os parâmetros genéticos constatados implicam que será essencial uma gestão bem prática na condição de estresse por calor para melhoria da eficiência da fertilidade.

Palavras-chave:
herdabilidade; repetitividade; correlação genética; correlação fenotípica; estresse por calor

Introduction

Fertility traits are considered very important because of their impact on the economy of dairy cattle breeding. Economic losses due to fertility problems are mainly caused by low dairy yield, prolonged calving intervals, increased insemination costs, few calves per cow per year, increased culling, high replacement costs and shorter reproductive lifespans (González-Recio & Alenda, 2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.; Abe, Masuda, & Susuki, 2009Abe, H., Masuda, Y., & Susuki, M. (2009). Relationship between reproductive traits of heifers and cows and yield traits for Holsteins in Japan. Journal of Dairy Science92(8), 4055-4062.). Nonetheless, for many years, genetic improvement programs worldwide did not include reproductive performance, since the selection was mainly focused on milk yield. An exception was Scandinavia, whose selection indices included not only milk yield, but also health and reproductive traits (Miglior, Muir, & Van Doormaal, 2005Miglior, F., Muir, B. L., & Van Doormaal, B. J. (2005). Selection indices in Holstein cattle of various countries. Journal of Dairy Science88(3), 1255-1263.). Now, the increase in milk yield without considering the reproductive performance is a problem, because it produced an important decline in the reproductive efficiency over time (Pryce, Royal, Garnsworthy, & Mao, 2004Pryce, J. E., Royal, M. D., Garnsworthy, P. C., & Mao, I. L. (2004). Fertility in the high-producing dairy cow. Livestock Production Science86(1-3), 125-135.; Melendez & Pinedo, 2007Melendez, P., & Pinedo, P. (2007). The association between reproductive performance and milk yield in Chilean Holstein cattle. Journal of Dairy Science90(1), 184-192.). Fertility in lactating dairy cows is also very sensitive to season, especially in hot climates. Global warming and the breeding of selected animals that are more and more sensitive to environmental effects have made this phenomenon, named heat stress, particularly relevant even in temperate areas (Nardone, Ronchi, Lacetera, Ranieri, & Bernabucci, 2010Nardone, A., Ronchi, B., Lacetera, N., Ranieri, M. S., & Bernabucci, U. (2010). Effects of climate changes on animal production and sustainability of livestock systems. Livestock Science130(1-3), 57-69.; Ferreira, 2013Ferreira, G. (2013). Reproductive performance of dairy farms in western Buenos Aires province, Argentina. Journal of Dairy Science96(12), 8075-8080.). Decreasing heat tolerance may be another of the reasons for decline in reproductive efficiency. So, one way to counteract this decline is through genetic selection (Pszczola, Aguilar, & Misztal, 2009Pszczola, M., Aguilar, I., & Misztal, I. (2009). Short communication: Trends for monthly changes in days open in Holsteins. Journal of Dairy Science92(9), 4689-4696. ). It is difficult to determine which traits must be included in the genetic evaluation of fertility, since they have very low heritability values, i.e., close to 0.1 (Thaller, 1998Thaller, G. (1998). Genetics and breeding for fertility. Interbull Bulletin18(2), 55-61.; Jamrozik, Fatehi, Kistemaker, & Schaeffer, 2005Jamrozik, J., Fatehi, J., Kistemaker, G. J., & Schaeffer, L. R. (2005). Estimates of genetic parameters for Canadian Holstein female reproduction traits. Journal of Dairy Science88(6), 2199-2208.). However, over the last decade, reproductive traits have increasingly been included in the selection indices for reproductive traits in genetic evaluations in different countries, thus highlighting the importance of including fertility in improvement programs of dairy cattle (Miglior et al., 2005Miglior, F., Muir, B. L., & Van Doormaal, B. J. (2005). Selection indices in Holstein cattle of various countries. Journal of Dairy Science88(3), 1255-1263.). Pozveh, Shadparvar, Shahrbabak, and Taromsari (2009Pozveh, S. T., Shadparvar, A. A., Shahrbabak, M. M., & Taromsari, M. D. (2009). Genetic analysis of reproduction traits and their relationship with conformation traits in Holstein cows. Livestock Science125(1), 84-87.) estimated genetic parameters for calving interval (CI), days open (DO), and gestation length (GL) in traits collected by the Animal Breeding Center of Iran from 1980 to 2004 on a data set including fertility records from 6000 cows. However, these traits and other economically important traits, such as number of insemination (NI), insemination outcome (IO), success in first service (SF) and calving birth weight (CBW) were not considered in heat stress condition. The objectives of this study were to estimate heritability, repeatability, genetic and phenotypic correlations of fertility traits of Holstein dairy cattle in warm and temperate climate.

Material and methods

Reproductive data and editing procedure

The data were collected from Holstein dairy population located in the north of Iran. The edited data set contained up to 23,402 records from 10,894 cows calved during 2001 to 2015. Original data file for reproduction traits consisted of insemination records that were matched to pedigree, lactation, and calving performance information to calculate the traits of interest. The fertility traits selected for this study were success in first service (SF), gestation length (GL), number of inseminations (NI), insemination outcome (IO), calving interval (CI), calving birth weight (CBW) and days open (DO). The SF and IO as binary traits and the NI as categorical trait were considered whereas the GL,

CI, CBW and DO were determined as continuous traits. Insemination outcome was defined as 1 = successful if cow became pregnant at insemination time and 0 = failure. Gestation length was measured as an interval from the last insemination to subsequent calving; GL was considered between 240 and 290 d. Days open was defined as the number of days between calving and conception; DO was limited to between 45 and 350 d. Calving interval was defined as the number of days between 2 consecutive calving events. CI records were limited to be between 285 and 640 d. Number of services was defined as the number of inseminations within a lactation; If NI was greater than 10, then NI was assigned to 10. SF was a binary trait defined as 1 = successful if cow became pregnant at first insemination and 0 = failure. Also, CBW was required to be between 20 and 60 kg. Subsequently, cows without pedigree information were excluded.

Climate data

Daily climate records were obtained from the most nearby meteorological station located at the same altitude as the farm studied. The major climatic variables directly affecting livestock are temperature, humidity, air movement and radiation (Konig, Chongkasikit, & Langholz, 2005Konig, S., Chongkasikit, N., & Langholz, H. J. (2005). Estimation of variance components for production and fertility traits in Northern Thai dairy cattle to define optimal breeding strategies. Archives Animal Breeding483 233-246.). Attempts to combine environmental parameters in one single index have had limited success except for the temperature-humidity index (THI) (Kadzere, Murphy, Silanikove, & Maltz, 2002Kadzere, C. T., Murphy, M. R., Silanikove, N., & Maltz, E. (2002). Heat stress in lactating dairy cows: a review. Livestock Production Science77(1), 59-91.) A daily THI was computed using the following Equation 1 (National Research Council [NRC], 1971National Research Council. (1971). A guide to environmental research on animalsNational academic science. Washington, DC: NRC.):

where:

T is mean daily temperature in degrees centigrade and

RH is the mean daily relative humidity as a percentage.

Insemination records were merged with daily temperature-humidity index. THI on the day of the insemination, 1 d prior and 1 d after insemination were studied as independent variables.

Genetic analysis and statistical models

The reproduction traits (SF, GL, NI, CI, CBW and DO) were analyzed with the Equation 2 as follow:

Also, trait of IO was analyzed with the following Equation 3:

where:

P is the observed trait of SF, GL, NI, CI, CBW and

DO; Q is the observed trait of IO;

μ is the mean of trait;

Parity is the fixed effect of parity in 5 classes;

YS is the fixed effect of year-season of calving in 14 and 4 classes, respectively;

DYS is the fixed effect of dystocia score (1 = no problem to 5 = caesarean);

β1 and β2 are linear and quadratic regression coefficients of dependent variable (P, Q) on days in milk effect, age of calving or temperature-humidity index effect;

XDIM as continuous variable representing days in milk, in weeks ranged from 15 to 105;

XAC as age of animal at calving in months, ranged from 20 to 135;

XTHI as continuous variable representing temperature-humidity index;

Animal is the random additive genetic effect;

pe is the random permanent environmental effect and e is the random residual effect. (Co) Variance components were estimated by AI-REML in DMU software package (Madsen & Jensen, 2013Madsen, P., & Jensen, J. (2013). DMU Ver. 6, rel. 5.2. Retrieved form http://dmu.agrsci.dk/DMU/Doc/ Current/dmuv6_guide .5.2.pdf
http://dmu.agrsci.dk/DMU/Doc/ Current/dm...
) using an animal linear mixed model; univariate threshold models were also carried out for the binary traits. Heritability was estimated as the ratio of the additive genetic variance to total phenotypic variance; and repeatability, as the ratio of the sum of the additive genetic variance plus permanent environmental variance to phenotypic variance, as described by Falconer and Mackay (2001Falconer, D. S., & Mackay, T. F. C. (2001). Introduction to quantitative genetics (4st ed.). Zaragoza, ES: Acribia.), according Equation 4 and 5:

Genetic and phenotypic correlations between traits were estimated using a series of bivariate animal linear mixed models. The covariance structure for the models was defined as Equation 6 and 7:

where:

A is the numerator relationship matrix;

I was an identity matrix of appropriate order;

is the Kronecker product;

G0= variance and covariance matrix of random additive genetic effects;

σ2aii = animal additive genetic variance for trait i;

σ2ajj = additive genetic variance for trait j;

σaij = σaij = additive genetic covariance between traits i and j;

= variance and covariance matrix of random permanent environmental effects;

σ2peii = permanent environmental variance for trait i;

σ2pejj = permanent environmental variance for trait j;

σpeij = σpeji = permanent environmental covariance between traits i and j;

R0 = variance and covariance matrix of residual effects;

σ2eii = residual variance for trait i;

σ2ejj = residual variance for trait j; and

σeij = σeji = residual covariance between traits i and j.

Results and discussion

Climatic conditions in the North of Iran

Climatic conditions in the north of Iran (Sari city) could be characterized as mild, and generally warm and temperate. The rain in Sari fallen mostly in the winter, with relatively little rain in the summer. The annual rainfall averaged 690 mm. The lowest precipitation was in June, with an average of 23 mm and the highest occurred in December with an average of 98 mm. The mean of temperature and humidity of present study was 18.26 ± 7.79°C and 75.19 ± 9.29%, respectively. The THI was lowest in January and February (mean of 56), which was associated with the winter season, and highest in June through September (mean of 81), which was associated with the summer season and heat stress condition.

Descriptive statistics

In this study, the mean and standard error for DO was 140.36 days (± 76.16). Also, mean of calving interval was 415.99 days (± 79.62). In accordance to the means of DO and CI traits, average of GL was 278.2 days (± 5.58). Moreover, mean of number of inseminations in this herd was 2.73 (± 1.94). Also, the averages of SF and IO traits of herd were low (0.32 ± 0.003 and 0.31 ± 0.001, respectively). Finally, the mean of calving birth weight was 40.4 kg (± 6.08).

Heritability, repeatability and variance components

Variance components and estimated heritability and repeatability for fertility traits are shown in Table 1. Heritability of GL was higher than others. Estimated heritability for DO and SF was low. However, DO as interval trait showed greater additive genetic variance related to SF as binary trait. Estimated additive genetic variances for CI and DO (11.34 and 7.23, respectively) was much greater than other traits. Additive genetic variance for SF was the least among all assessed traits. Also, permanent environmental variance for CI and DO (11.01 and 7.47, respectively) was the highest and for SF (0.001) was the least among all traits. Likewise, estimated repeatability for DO and SF was lower and for IO was higher than others (Table 1).

Table 1
Genetic variance (σ2a), permanent environmental variance (σ2pe), residual variance (σ2e), heritability (h2) and repeatability (R) with standard error (± SE) for fertility traits.

Additive genetic and phenotypic correlations

As shown in Table 2, estimates of additive genetic correlations varied from -1 for CI and IO to 0.98 for DO and CI. Phenotype correlation estimates ranged -1 for NI and IO to +1 for SF and IO.

In the following discussion, we compare estimates of parameters from this study with means for similar traits in the literature. The heritability for DO, CI, GL, NI, SF, CBW and IO traits reported in the literature are shown in Table 3. The heritability obtained for DO in this research (0.016) was similar to this reported by Ríos-Ultrera, Calderón-Robles, Rosete-Fernández, and Lagunes-Lagunes (2010aRíos-Ultrera, A., Calderón-Robles, R., Rosete-Fernández, J., & Lagunes-Lagunes, J. (2010a). Genetic analysis of reproductive traits of Holstein cows bred in a subtropical environment. Journal Agronomía Mesoamericana21(2), 245-253.). In contrast, some authors reported very higher heritability values (Abe et al., 2009Abe, H., Masuda, Y., & Susuki, M. (2009). Relationship between reproductive traits of heifers and cows and yield traits for Holsteins in Japan. Journal of Dairy Science92(8), 4055-4062.; Pozveh et al., 2009Pozveh, S. T., Shadparvar, A. A., Shahrbabak, M. M., & Taromsari, M. D. (2009). Genetic analysis of reproduction traits and their relationship with conformation traits in Holstein cows. Livestock Science125(1), 84-87.; Sun et al., 2010Sun, C., Madsen, P., Lund, M. S., Zhang, Y., Nielsen, U. S., & Su, G. (2010). Improvement in genetic evaluation of female fertility in dairy cattle using multiple-trait models including dairy yield traits. Journal of Animal Science88(3), 871-878.; Ghiasi et al., 2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ; Pantelic, Sretenović, & Ostojić-Andrić, 2011Pantelic, V., Sretenović, L., & Ostojić-Andrić, D. (2011). Heritability and genetic correlation of production and reproduction traits of Simmental cows. African Journal of Biotechnology10(36), 7117-7121.) (Table 3). As for CI, the heritability estimates obtained in this study was 0.029. This is consistent with the results reported by Veerkamp, Koenen, and De Jong (2001Veerkamp, R. F., Koenen, E. P. C., & De Jong, G. (2001). Genetic correlations among body condition score, yield, and fertility in first-parity cows estimated by random regression models. Journal of Dairy Science84(10), 2327-2335.) and Wall, Brotherstone, Woolliams, Banos, and Coffey (2003Wall, E., Brotherstone, S., Woolliams, J. A., Banos, G., & Coffey, M. P. (2003). Genetic evaluation of fertility using direct and correlated traits. Journal of Dairy Science86(12), 4093-4102.). However, these results were lower than those obtained by Haile-Mariam, Morton, and Goddard (2003Haile-Mariam, M., Morton, J. M., & Goddard, M. E. (2003). Estimates of genetic parameters for fertility traits of Australian Holstein- Friesian cattle. Animal Science76(1), 35-42.), Demeke, Neser, and Schoeman (2004Demeke, S., Neser, F. W. C., & Schoeman, S. J. (2004). Estimates of genetic parameters for Boran, Friesian and crosses of Friesian and Jersey with the Boran cattle in the tropical highlands of Ethiopia: reproduction traits. Journal of Animal Breeding and Genetics121(1), 57-65.), Restrepo, Pizarro, and Quijano (2008Restrepo, G., Pizarro, E., & Quijano, J. H. (2008). Selection indexes and independent culling levels for two productive and reproductive traits in Holstein herd (Bos Taurus). Colombian Journal of Animal Science21(2), 239-250.), Pozveh et al. (2009Pozveh, S. T., Shadparvar, A. A., Shahrbabak, M. M., & Taromsari, M. D. (2009). Genetic analysis of reproduction traits and their relationship with conformation traits in Holstein cows. Livestock Science125(1), 84-87.), Ríos-Ultrera et al. (2010aRíos-Ultrera, A., Calderón-Robles, R., Rosete-Fernández, J., & Lagunes-Lagunes, J. (2010a). Genetic analysis of reproductive traits of Holstein cows bred in a subtropical environment. Journal Agronomía Mesoamericana21(2), 245-253.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ). Interval traits (DO and CI) may be affected by management decisions such as the length of the voluntary waiting period or estrus synchronization applied in this farm. The estimate of heritability for GL in this study (0.123) is approximately compatible with previous results in the Holstein breed by Eghbalsaied (2011Eghbalsaied, S. (2011). Estimation of genetic parameters for 13 female fertility indices in Holstein dairy cows. Tropical Animal Health and Production43(4), 811-816.). In contrast to present estimate, Pozveh et al. (2009Pozveh, S. T., Shadparvar, A. A., Shahrbabak, M. M., & Taromsari, M. D. (2009). Genetic analysis of reproduction traits and their relationship with conformation traits in Holstein cows. Livestock Science125(1), 84-87.) obtained lower values and Olson, Cassell, McAllister, and Washburn (2009Olson, K. M., Cassell, B. G., McAllister, A. J., & Washburn, S. P. (2009). Dystocia, stillbirth, gestation length, and birth weight in Holstein, Jersey, and reciprocal crosses from a planned experiment. Journal of Dairy Science92(12), 6167-6175.) and Johanson, Berger, Tsuruta, and Misztal (2011Johanson, J. M., Berger, P. J., Tsuruta, S., & Misztal, I. (2011). A Bayesian threshold-linear model evaluation of perinatal mortality, dystocia, birth weight, and gestation length in a Holstein herd. Journal of Dairy Science94(1), 450-460.) reported higher values. The heritability estimate for NI was 0.041, as were those reported by Estrada-León, Magana, and Segura-Correa (2008Estrada-León, R. J., Magana, J. G., & Segura-Correa, J. C. (2008). Genetic parameters for reproductive traits of Brown Swiss cows in the tropics of Mexico. Journal of Animal and Veterinary Advances7(2), 124-129.) in Brown Swiss cows. However, Demeke et al. (2004Demeke, S., Neser, F. W. C., & Schoeman, S. J. (2004). Estimates of genetic parameters for Boran, Friesian and crosses of Friesian and Jersey with the Boran cattle in the tropical highlands of Ethiopia: reproduction traits. Journal of Animal Breeding and Genetics121(1), 57-65.) reported higher value and Wall et al. (2003Wall, E., Brotherstone, S., Woolliams, J. A., Banos, G., & Coffey, M. P. (2003). Genetic evaluation of fertility using direct and correlated traits. Journal of Dairy Science86(12), 4093-4102.), González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Sun et al. (2010Sun, C., Madsen, P., Lund, M. S., Zhang, Y., Nielsen, U. S., & Su, G. (2010). Improvement in genetic evaluation of female fertility in dairy cattle using multiple-trait models including dairy yield traits. Journal of Animal Science88(3), 871-878.) obtained lower values. The heritability estimate obtained for SF (0.015) was in a good agreement with results from Kadarmideen, Thompson, Coffey, and Kossaibati (2003Kadarmideen, H. N., Thompson, R., Coffey, M. P., & Kossaibati, M. A. (2003). Genetic parameters and evaluations from single and multiple trait analysis of dairy cow fertility and milk production. Livestock Production Science81(2-3), 183-195.). Higher estimates (González-Recio & Alenda, 2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.; Ghiasi et al., 2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) have also been reported. The obtained heritability value for CBW (0.089) was lower to those reported by Olson et al. (2009Olson, K. M., Cassell, B. G., McAllister, A. J., & Washburn, S. P. (2009). Dystocia, stillbirth, gestation length, and birth weight in Holstein, Jersey, and reciprocal crosses from a planned experiment. Journal of Dairy Science92(12), 6167-6175.) and Johanson et al. (2011Johanson, J. M., Berger, P. J., Tsuruta, S., & Misztal, I. (2011). A Bayesian threshold-linear model evaluation of perinatal mortality, dystocia, birth weight, and gestation length in a Holstein herd. Journal of Dairy Science94(1), 450-460.). The heritability for IO obtained in this study for Holstein cattle was 0.055, which was similar to these reported by Haile-Mariam et al. (2003Haile-Mariam, M., Morton, J. M., & Goddard, M. E. (2003). Estimates of genetic parameters for fertility traits of Australian Holstein- Friesian cattle. Animal Science76(1), 35-42.), Abe, Masuda, and Susuki (2009Abe, H., Masuda, Y., & Susuki, M. (2009). Relationship between reproductive traits of heifers and cows and yield traits for Holsteins in Japan. Journal of Dairy Science92(8), 4055-4062.) and Tsuruta, Misztal, Huang, and Lawlor (2009Tsuruta, S., Misztal, I., Huang, C., & Lawlor, T. J. (2009). Bivariate analysis of conception rates and test-day milk yields in Holsteins using a threshold-linear model with random regressions. Journal of Dairy Science92(6), 2922-2930.). In contrast, Ghiasi et al. (2011) and Zambrano and Echeverri (2014Zambrano, J. C., & Echeverri, J. (2014). Genetic and environmental variance and covariance parameters for some reproductive traits of Holstein and Jersey cattle in Antioquia (Colombia). Revista Brasileira de Zootecnia43(3), 132-139.) reported higher and lower heritability values, respectively (Table 3).

Table 2
Additive genetic (above diagonal) and phenotypic (below diagonal) correlations (± SE) for all fertility traits.
Table 3
Heritability reported by several authors for fertility traits.

The low heritability in this study suggested that improvement of fertility traits in cows could be achieved by improving reproductive managements such as successful detection of heat, timely insemination, feeding practice for growing and postpartum animals and controlling heat stress. The repeatability estimate for DO in Holstein (0.034) was lower to those reported by Demeke et al. (2004Demeke, S., Neser, F. W. C., & Schoeman, S. J. (2004). Estimates of genetic parameters for Boran, Friesian and crosses of Friesian and Jersey with the Boran cattle in the tropical highlands of Ethiopia: reproduction traits. Journal of Animal Breeding and Genetics121(1), 57-65.), Estrada-León et al. (2008Estrada-León, R. J., Magana, J. G., & Segura-Correa, J. C. (2008). Genetic parameters for reproductive traits of Brown Swiss cows in the tropics of Mexico. Journal of Animal and Veterinary Advances7(2), 124-129.) and M'hamdi, Aloulou, Brar, Bouallegue, and Ben Hamouda (2010M'hamdi, N., Aloulou, R., Brar, S. K., Bouallegue, M., & Ben Hamouda, M. (2010). Phenotypic and genetic parameters of reproductive traits in Tunisian Holstein cows. Biotechnology in Animal Husbandry26(5-6), 297-307.) which were in range 0.135-0.190. Regarding CI, the repeatability value obtained (0.057) was nearly the same as reported by Ojango and Pollott (2001Ojango, J. M., & Pollott, G. E. (2001). Genetics of milk yield and fertility traits in Holstein Friesian cattle on large scale Kenyan farms. Journal of Animal Science79(7), 1742-1750.) (0.06). Nevertheless, Kadarmideen, Thompson, and Simm (2000Kadarmideen, H. N., Thompson, R., & Simm, G. (2000). Linear and threshold model genetic parameters for disease, fertility and milk production in dairy cattle. Animal Science71(3), 411-419.) obtained lower value (0.049) and some authors (Estrada-León, Magana, & Segura-Correa, 2008; M'hamdi et al., 2010; Ríos-Ultrera, Calderón-Robles, Rosete-Fernández, & Lagunes-Lagunes, 2010aRíos-Ultrera, A., Calderón-Robles, R., Rosete-Fernández, J., & Lagunes-Lagunes, J. (2010a). Genetic analysis of reproductive traits of Holstein cows bred in a subtropical environment. Journal Agronomía Mesoamericana21(2), 245-253.) report higher repeatability values (0.120-0.180). Repeatability for GL was estimated to be 0.181, which was lower than estimated repeatability by Johanson et al. (2011Johanson, J. M., Berger, P. J., Tsuruta, S., & Misztal, I. (2011). A Bayesian threshold-linear model evaluation of perinatal mortality, dystocia, birth weight, and gestation length in a Holstein herd. Journal of Dairy Science94(1), 450-460.) (0.54). For NI, the repeatability estimate was 0.115, higher than those reported by Kadarmideen et al. (2000Kadarmideen, H. N., Thompson, R., & Simm, G. (2000). Linear and threshold model genetic parameters for disease, fertility and milk production in dairy cattle. Animal Science71(3), 411-419.), Demeke et al. (2004Demeke, S., Neser, F. W. C., & Schoeman, S. J. (2004). Estimates of genetic parameters for Boran, Friesian and crosses of Friesian and Jersey with the Boran cattle in the tropical highlands of Ethiopia: reproduction traits. Journal of Animal Breeding and Genetics121(1), 57-65.), Estrada-León et al. (2008Estrada-León, R. J., Magana, J. G., & Segura-Correa, J. C. (2008). Genetic parameters for reproductive traits of Brown Swiss cows in the tropics of Mexico. Journal of Animal and Veterinary Advances7(2), 124-129.) and M'hamdi et al. (2010M'hamdi, N., Aloulou, R., Brar, S. K., Bouallegue, M., & Ben Hamouda, M. (2010). Phenotypic and genetic parameters of reproductive traits in Tunisian Holstein cows. Biotechnology in Animal Husbandry26(5-6), 297-307.) which were in a range between 0.022 and 0.08. The estimate of repeatability for SF in this study (0.021) was lower than obtained result in the Holstein breed by Jamdar and Eskandarinasab (2014Jamdar, J., & Eskandarinasab, M. P. (2014). Comparison of linear and threshold models for estimation genetic and phenotypic parameters of success of conception at first service and inseminations to conception in Holstein Cattles in East Azarbayjan province. International Journal of Advanced Biological and Biomedical Research2(5), 1593-1598.) (0.077). For IO, the repeatability value found for Holstein dairy cattle (0.411) was higher than those reported by Ríos-Ultrera, Calderón, Rosete, and Lagunes (2010bRíos-Ultrera, A., Calderón-Robles, R., Rosete-Fernández, J., & Lagunes-Lagunes, J. (2010b). Estimation of genetic parameters for fertility traits in Brown Swiss cattle under subtropical conditions in Mexico. Veterinaria Mexico Journal41(2), 117-129.) and Zambrano and Echeverri (2014Zambrano, J. C., & Echeverri, J. (2014). Genetic and environmental variance and covariance parameters for some reproductive traits of Holstein and Jersey cattle in Antioquia (Colombia). Revista Brasileira de Zootecnia43(3), 132-139.) which were 0.03 in Brown Swiss cattle and 0.076 in Holstein-Jersey, respectively. Finally, the estimated repeatability for CBW was 0.142, which was lower than 0.29 obtained by Johanson et al. (2011Johanson, J. M., Berger, P. J., Tsuruta, S., & Misztal, I. (2011). A Bayesian threshold-linear model evaluation of perinatal mortality, dystocia, birth weight, and gestation length in a Holstein herd. Journal of Dairy Science94(1), 450-460.). The low repeatability estimates obtained for most traits suggest that fertility traits are strongly influenced by temporary environmental factors. It would thus be possible to improve fertility performance through improvement in herd management. This fact suggests that in making decision for culling cows, reproduction performance should take less weight in comparison with production traits, which are considerably more repeatable. The genetic correlation between DO and CI in this study was close to 1 (0.98). This value was similar to those reported by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.), Gredler, Fürst, and Sölkner (2007Gredler, B., Fürst, C., & Sölkner, J. (2007). Analysis of new fertility traits for the joint genetic evaluation in Austria and Germany. Interbull Bulletin37(2), 152-155.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ), who reported a nearly perfect genetic correlation (0.99, 0.98, and 0.99, respectively). The genetic correlation between DO and NI was high and favorable (0.88). Nearly equivalent results were reported by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Pozveh et al. (2009Pozveh, S. T., Shadparvar, A. A., Shahrbabak, M. M., & Taromsari, M. D. (2009). Genetic analysis of reproduction traits and their relationship with conformation traits in Holstein cows. Livestock Science125(1), 84-87.): 0.94 and 0.83, respectively. The joint analysis of CI and NI indicates that the genetic correlation between these 2 traits was 0.88, consistent with those reported by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Eghbalsaied (2011Eghbalsaied, S. (2011). Estimation of genetic parameters for 13 female fertility indices in Holstein dairy cows. Tropical Animal Health and Production43(4), 811-816.) (0.89 and 0.81, respectively). These results suggest that these reproductive traits (DO × CI, DO × NI and CI × NI) are almost genetically equivalent, i.e., they are influenced by the same genes. This is known as pleiotropic effect. The genetic correlation between DO and GL was -0.2. The result obtained in this study was lower than -0.36 reported by Eghbalsaied (2011Eghbalsaied, S. (2011). Estimation of genetic parameters for 13 female fertility indices in Holstein dairy cows. Tropical Animal Health and Production43(4), 811-816.). For Holstein cows, the genetic correlation between DO and SF was estimated -0.48, which was lower than values obtained by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (-0.94 and -0.83, respectively). The genetic correlation between CI and GL was -0.04 that higher value was reported by Eghbalsaied (2011) (-0.07). The genetic correlation between GL and NI (-0.09) was lower than obtained result by Eghbalsaied (2011) (-0.88). Also, the genetic correlation of GL and CBW was obtained low and near zero (0.007), which was lower than value reported by Johanson et al. (2011) (0.52). For Holstein cattle, the genetic correlation between CI and SF that we obtained was medium and negative (-0.55), similar to the finding obtained by González-Recio and Alenda (2005), who reported a correlation of -0.59 between these 2 traits. Likewise, the genetic correlation between NI and SF was middle and negative (-0.49) that higher value was reported by Kadarmideen et al. (2003) (-0.92). The genetic correlation between NI and IO obtained in this study was nearly high and negative (-0.77), similar to the result reported by Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (-0.73). These results suggest that these traits (CI × SF, NI × SF and NI × IO) are not genetically favored, as could be logically expected. The genetic correlation of SF and IO was 0.36, whereas González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) reported higher values (0.94 and 0.83, respectively). These results suggest that these 2 reproductive traits were essentially the same indicator of fertility and may be originally the same in terms of genetic source. The genetic correlation between CI and IO was -1. The result obtained in this study is similar to those obtained by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.), Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ), who both reported a correlation of -0.99 between CI and insemination outcome. Also, the genetic correlation obtained in this study between DO and IO was high and negative (-0.98). This is consistent with the results reported by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (-0.99 in both reports). The estimated genetic correlations among CI × IO and DO × IO indicated that selection for cows with high insemination outcome could lead to shorten DO and CI. Therefore, they could be used as one of the best indicators for cow fertility. This would enable efficient selection for better reproductive performance. The phenotypic correlation between CI and DO in this study was high and positive, with value of 0.99. González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.), Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ), Eghbalsaied (2011) and Zambrano and Echeverri (2014) reported similar estimates for Holstein dairy cattle (0.91, 0.95, 0.99 and 1 respectively). Likewise, the phenotypic correlation between NI and CI was high (0.83). El Amin, Simerl, and Wilcox (1986El Amin, F. M., Simerl, N. A., & Wilcox, C. J. (1986). Genetic and enviromental effects upon reproductive performance of Holstein crossbreds in the Sudan. Journal of Dairy Science69(4), 1093-1097.), Kadarmideen et al. (2000), Ageeb and Hayes (2000Ageeb, A. G., & Hayes, J. F. (2000). Reproductive responses of Holstein Friesian cattle to the climatic conditions of central Sudan. Tropical Animal Health and Production32(4), 233-234.), González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) reported lower values (0.01, 0.69, 0.05, 0.68 and 0.70, respectively). Similarly, the result obtained in this study regarding the phenotypic correlation between NI and DO was high (0.83). This result was higher than reported by El Amin et al. (1986El Amin, F. M., Simerl, N. A., & Wilcox, C. J. (1986). Genetic and enviromental effects upon reproductive performance of Holstein crossbreds in the Sudan. Journal of Dairy Science69(4), 1093-1097.), Ríos-Ultrera, Calderón-Robles, Rosete-Fernández, and Lagunes-Lagunes (2010cRíos-Ultrera, A., Calderón-Robles, R., Rosete-Fernández, J., & Lagunes-Lagunes, J. (2010c). Genetic and phenotypic correlations between reproductive characteristics of dairy cows. Mesoamerican Journal of Agronomy21(2), 235-244.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (0.01, 0.56 and 0.73, respectively). The reason of these high correlations may be due to the high use of estrus synchronization programs in warm and temperate climate condition. The phenotypic correlation between IO and NI obtained in this study was perfect and negative (-1), and it was higher than results obtained by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (-0.75 and -0.73, respectively). The obtained higher and negative correlation may also be explained by the factor discussed above. The phenotypic correlation between IO and CI was -0.99, similar the values reported by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (-0.91 and -0.95, respectively). Likewise, the phenotypic correlation between IO and DO, the value obtained in this study was -0.99, which is consistent with the results reported by González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (-1 and -0.98, respectively), which indicate that the degree of phenotypic association between these 2 traits is high and negative. In relation to the phenotypic correlation between IO and SF, the value obtained in the present study was perfect and favorable associated, presenting 1 in the population studied. This result was higher than findings of González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) who reported 0.61 and 0.55, respectively. In relation to the phenotypic correlation between GL and CI, the value obtained in this study was 0.18, which was higher than reported value by Pozveh et al. (2009Pozveh, S. T., Shadparvar, A. A., Shahrbabak, M. M., & Taromsari, M. D. (2009). Genetic analysis of reproduction traits and their relationship with conformation traits in Holstein cows. Livestock Science125(1), 84-87.) (0.002). As for phenotypic correlation between NI and GL, the value obtained was 0.15. This result was positive and higher than obtained value by Eghbalsaied (2011Eghbalsaied, S. (2011). Estimation of genetic parameters for 13 female fertility indices in Holstein dairy cows. Tropical Animal Health and Production43(4), 811-816.) (-0.13). The phenotypic correlation between GL and DO was 0.13, unlike the lower value reported by Pozveh et al. (2009Pozveh, S. T., Shadparvar, A. A., Shahrbabak, M. M., & Taromsari, M. D. (2009). Genetic analysis of reproduction traits and their relationship with conformation traits in Holstein cows. Livestock Science125(1), 84-87.) (0.003). The phenotypic correlation between SF and NI was -0.17, which is lower than result obtained by Kadarmideen et al. (2003), González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (-0.69, -0.76 and -0.7, respectively). Also, phenotypic correlation between SF and CI was low and negative associated with value of -0.07. Kadarmideen et al. (2003), González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.) and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) reported phenotypic correlation values which were moderate and negative (-0.54, -0.54 and -0.53, respectively). Similarly, phenotypic correlation between SF and DO was low and negative (-0.09) which was lower than results of González-Recio and Alenda (2005González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.), and Ghiasi et al. (2011Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280. ) (-0.61 and -0.55, respectively). Low phenotypic correlations between SF × NI, SF × CI and SF × DO may be due to the fact that present study was carried out in region with warm and temperate climate, unlike most of the studies which were carried out in zones with a subtropical climate.

Conclusion

According to the results, this study confirms that reproductive traits present low heritability, < 10% in most cases, in Holstein dairy cattle, suggesting that fertility is affected mostly by the environment.

Therefore, good management of the fertility traits in heat stress condition must be considered in order to improve reproductive efficiency. The high and negative genetic correlations for DO × IO and CI × IO, and high and positive genetic correlations for DO × CI, DO × NI, and CI × NI in this study suggest that these reproductive traits are genetically equivalent, i.e., they are influenced by the same genes. This obviously favors the selection of these traits, as we can predict what will happen to several of the reproductive traits after performing selection on one of them. In this manner, we can integrate information on different traits to propose more efficient selection strategies.

References

  • Abe, H., Masuda, Y., & Susuki, M. (2009). Relationship between reproductive traits of heifers and cows and yield traits for Holsteins in Japan. Journal of Dairy Science92(8), 4055-4062.
  • Ageeb, A. G., & Hayes, J. F. (2000). Reproductive responses of Holstein Friesian cattle to the climatic conditions of central Sudan. Tropical Animal Health and Production32(4), 233-234.
  • Demeke, S., Neser, F. W. C., & Schoeman, S. J. (2004). Estimates of genetic parameters for Boran, Friesian and crosses of Friesian and Jersey with the Boran cattle in the tropical highlands of Ethiopia: reproduction traits. Journal of Animal Breeding and Genetics121(1), 57-65.
  • Eghbalsaied, S. (2011). Estimation of genetic parameters for 13 female fertility indices in Holstein dairy cows. Tropical Animal Health and Production43(4), 811-816.
  • El Amin, F. M., Simerl, N. A., & Wilcox, C. J. (1986). Genetic and enviromental effects upon reproductive performance of Holstein crossbreds in the Sudan. Journal of Dairy Science69(4), 1093-1097.
  • Estrada-León, R. J., Magana, J. G., & Segura-Correa, J. C. (2008). Genetic parameters for reproductive traits of Brown Swiss cows in the tropics of Mexico. Journal of Animal and Veterinary Advances7(2), 124-129.
  • Falconer, D. S., & Mackay, T. F. C. (2001). Introduction to quantitative genetics (4st ed.). Zaragoza, ES: Acribia.
  • Ferreira, G. (2013). Reproductive performance of dairy farms in western Buenos Aires province, Argentina. Journal of Dairy Science96(12), 8075-8080.
  • Ghiasi, H., Pakdel, A., Nejati-Javaremi, A., Meharabani-Yeganeh, H., Honarvar, M., González-Recio, O., ... Alenda, R. (2011). Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science139(3), 277-280.
  • González-Recio, O., & Alenda, R. (2005). Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. Journal of Dairy Science88(9), 3282-3289.
  • Gredler, B., Fürst, C., & Sölkner, J. (2007). Analysis of new fertility traits for the joint genetic evaluation in Austria and Germany. Interbull Bulletin37(2), 152-155.
  • Haile-Mariam, M., Morton, J. M., & Goddard, M. E. (2003). Estimates of genetic parameters for fertility traits of Australian Holstein- Friesian cattle. Animal Science76(1), 35-42.
  • Jamdar, J., & Eskandarinasab, M. P. (2014). Comparison of linear and threshold models for estimation genetic and phenotypic parameters of success of conception at first service and inseminations to conception in Holstein Cattles in East Azarbayjan province. International Journal of Advanced Biological and Biomedical Research2(5), 1593-1598.
  • Jamrozik, J., Fatehi, J., Kistemaker, G. J., & Schaeffer, L. R. (2005). Estimates of genetic parameters for Canadian Holstein female reproduction traits. Journal of Dairy Science88(6), 2199-2208.
  • Johanson, J. M., Berger, P. J., Tsuruta, S., & Misztal, I. (2011). A Bayesian threshold-linear model evaluation of perinatal mortality, dystocia, birth weight, and gestation length in a Holstein herd. Journal of Dairy Science94(1), 450-460.
  • Kadarmideen, H. N., Thompson, R., & Simm, G. (2000). Linear and threshold model genetic parameters for disease, fertility and milk production in dairy cattle. Animal Science71(3), 411-419.
  • Kadarmideen, H. N., Thompson, R., Coffey, M. P., & Kossaibati, M. A. (2003). Genetic parameters and evaluations from single and multiple trait analysis of dairy cow fertility and milk production. Livestock Production Science81(2-3), 183-195.
  • Kadzere, C. T., Murphy, M. R., Silanikove, N., & Maltz, E. (2002). Heat stress in lactating dairy cows: a review. Livestock Production Science77(1), 59-91.
  • Konig, S., Chongkasikit, N., & Langholz, H. J. (2005). Estimation of variance components for production and fertility traits in Northern Thai dairy cattle to define optimal breeding strategies. Archives Animal Breeding483 233-246.
  • M'hamdi, N., Aloulou, R., Brar, S. K., Bouallegue, M., & Ben Hamouda, M. (2010). Phenotypic and genetic parameters of reproductive traits in Tunisian Holstein cows. Biotechnology in Animal Husbandry26(5-6), 297-307.
  • Madsen, P., & Jensen, J. (2013). DMU Ver. 6, rel. 5.2. Retrieved form http://dmu.agrsci.dk/DMU/Doc/ Current/dmuv6_guide .5.2.pdf
    » http://dmu.agrsci.dk/DMU/Doc/ Current/dmuv6_guide .5.2.pdf
  • Melendez, P., & Pinedo, P. (2007). The association between reproductive performance and milk yield in Chilean Holstein cattle. Journal of Dairy Science90(1), 184-192.
  • Miglior, F., Muir, B. L., & Van Doormaal, B. J. (2005). Selection indices in Holstein cattle of various countries. Journal of Dairy Science88(3), 1255-1263.
  • Nardone, A., Ronchi, B., Lacetera, N., Ranieri, M. S., & Bernabucci, U. (2010). Effects of climate changes on animal production and sustainability of livestock systems. Livestock Science130(1-3), 57-69.
  • National Research Council. (1971). A guide to environmental research on animalsNational academic science. Washington, DC: NRC.
  • Ojango, J. M., & Pollott, G. E. (2001). Genetics of milk yield and fertility traits in Holstein Friesian cattle on large scale Kenyan farms. Journal of Animal Science79(7), 1742-1750.
  • Olson, K. M., Cassell, B. G., McAllister, A. J., & Washburn, S. P. (2009). Dystocia, stillbirth, gestation length, and birth weight in Holstein, Jersey, and reciprocal crosses from a planned experiment. Journal of Dairy Science92(12), 6167-6175.
  • Pantelic, V., Sretenović, L., & Ostojić-Andrić, D. (2011). Heritability and genetic correlation of production and reproduction traits of Simmental cows. African Journal of Biotechnology10(36), 7117-7121.
  • Pozveh, S. T., Shadparvar, A. A., Shahrbabak, M. M., & Taromsari, M. D. (2009). Genetic analysis of reproduction traits and their relationship with conformation traits in Holstein cows. Livestock Science125(1), 84-87.
  • Pryce, J. E., Royal, M. D., Garnsworthy, P. C., & Mao, I. L. (2004). Fertility in the high-producing dairy cow. Livestock Production Science86(1-3), 125-135.
  • Pszczola, M., Aguilar, I., & Misztal, I. (2009). Short communication: Trends for monthly changes in days open in Holsteins. Journal of Dairy Science92(9), 4689-4696.
  • Restrepo, G., Pizarro, E., & Quijano, J. H. (2008). Selection indexes and independent culling levels for two productive and reproductive traits in Holstein herd (Bos Taurus). Colombian Journal of Animal Science21(2), 239-250.
  • Ríos-Ultrera, A., Calderón-Robles, R., Rosete-Fernández, J., & Lagunes-Lagunes, J. (2010a). Genetic analysis of reproductive traits of Holstein cows bred in a subtropical environment. Journal Agronomía Mesoamericana21(2), 245-253.
  • Ríos-Ultrera, A., Calderón-Robles, R., Rosete-Fernández, J., & Lagunes-Lagunes, J. (2010b). Estimation of genetic parameters for fertility traits in Brown Swiss cattle under subtropical conditions in Mexico. Veterinaria Mexico Journal41(2), 117-129.
  • Ríos-Ultrera, A., Calderón-Robles, R., Rosete-Fernández, J., & Lagunes-Lagunes, J. (2010c). Genetic and phenotypic correlations between reproductive characteristics of dairy cows. Mesoamerican Journal of Agronomy21(2), 235-244.
  • Sun, C., Madsen, P., Lund, M. S., Zhang, Y., Nielsen, U. S., & Su, G. (2010). Improvement in genetic evaluation of female fertility in dairy cattle using multiple-trait models including dairy yield traits. Journal of Animal Science88(3), 871-878.
  • Thaller, G. (1998). Genetics and breeding for fertility. Interbull Bulletin18(2), 55-61.
  • Tsuruta, S., Misztal, I., Huang, C., & Lawlor, T. J. (2009). Bivariate analysis of conception rates and test-day milk yields in Holsteins using a threshold-linear model with random regressions. Journal of Dairy Science92(6), 2922-2930.
  • Veerkamp, R. F., Koenen, E. P. C., & De Jong, G. (2001). Genetic correlations among body condition score, yield, and fertility in first-parity cows estimated by random regression models. Journal of Dairy Science84(10), 2327-2335.
  • Wall, E., Brotherstone, S., Woolliams, J. A., Banos, G., & Coffey, M. P. (2003). Genetic evaluation of fertility using direct and correlated traits. Journal of Dairy Science86(12), 4093-4102.
  • Zambrano, J. C., & Echeverri, J. (2014). Genetic and environmental variance and covariance parameters for some reproductive traits of Holstein and Jersey cattle in Antioquia (Colombia). Revista Brasileira de Zootecnia43(3), 132-139.

Publication Dates

  • Publication in this collection
    Sept 2016

History

  • Received
    20 Mar 2016
  • Accepted
    02 May 2016
Editora da Universidade Estadual de Maringá - EDUEM Av. Colombo, 5790, bloco 40, CEP 87020-900 , Tel. (55 44) 3011-4253, Fax (55 44) 3011-1392 - Maringá - PR - Brazil
E-mail: actaanim@uem.br