Livestock Research for Rural Development 33 (1) 2021 | LRRD Search | LRRD Misssion | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
The aim of the study was to evaluate reproductive traits of Holstein cows in Morocco and to investigate non-genetic factors affecting them. A total of 9461 records, collected during 2018 and 2019, from 226 herds, were used for this study. Eight reproductive traits were studied: age at first insemination in life (AFI), gestation length (GL), days from calving to first insemination (DCFI), days open (DO), days from first insemination to conception (DFIC), calving interval (CI), number of inseminations per conception (NIC) and success of conception at first insemination (SCFI). Data were analyzed using general linear model procedure. The factors examined were herd, parity and either birth season and year, calving season and year or first insemination season and year. Results showed that the reproductive performance is poor; AFI, GL, DCFI, DO, DFIC, CI, NIC and SCFI averaged 503±61.8, 276±6.39, 95.2±49.4, 125±61.3, 65.6±37.2, 437±93.4 days, 2.10±1.47 and 0.46±0.50, respectively. Our findings indicated significant (P < 0.001) herd and year effects on all the reproductive traits. Except DO and CI, all the remaining studied reproductive traits were significantly affected by parity. In general, the average fertility of heifers was superior to that of cows. Season of birth was not significant (P > 0.05) on AFI. The traits DCFI, DO and CI were significantly (P < 0.001) influenced by season of calving, while GL, DFIC, NIC and SCFI were significantly (P < 0.001) affected by season of first insemination. Reproductive traits were in general poor in summer. It was concluded that reproduction management should be improved in order to increase the profitability of dairy farms.
Keywords: calving interval, dairy cattle, fertility, Morocco, reproduction
Reproductive performance is among the most important traits affecting profitability in dairy cattle industry. Poor fertility results in an increase in calving interval, inseminations and veterinary costs, involuntary culling rate and herd replacement cost, as well as a decrease in milk production, and hence a reduction in the herd income. Boujenane (2017) showed that 36% of cow culling reasons were attributed to reproductive problems. Worldwide and for several years, the selection objective in dairy cattle improvement was directed towards milk production. This choice has affected in a negative way reproductive traits, especially in high producing cows, because of the antagonistic genetic relationship between milk production and fertility (Pryce et al 2004; Liu et al 2007). Therefore, to halt the decline of fertility and even to improve it, the genetic improvement programs of different countries incorporated the reproductive traits as selection objectives.
Fertility is a complex trait and is highly dependent on reproduction management. Determining which trait adequately represents cow reproduction performance is complicated. Traits often used in selection programs are calving interval, days from calving to first insemination, days open, the number of inseminations per conception (Guo et al 2014). Moreover, several non-genetic factors, such as herd, parity, calving season, calving year, influence the fertility of dairy cows. Moroccan Holstein is the main exotic breed used for milk production in the country. There is currently limited information on its reproductive performance. As a consequence, a comprehensive study on fertility traits of Holstein cows in Moroccan conditions is crucial for improving the breeding efficiency and setting up the selection strategy. This requires the identification of appropriate reproductive parameters that can be used as selection criteria and the determination of various non-genetic factors influencing the reproductive performance.
Thus, the objectives of the present study were to assess the reproductive traits of Holstein cows in Morocco and to determine the effect of non-genetic factors on them. The results of this study will help the development of a routine collection of reproduction data towards an evaluation system for cow fertility.
The study was conducted in the Souss-Massa region located in South-West of Morocco. The climate is semiarid. Temperatures averaged 19°C in winter and 27°C in summer. The annual rainfall varied from 180 to 280 mm.
Data for this study were obtained from herds composed by animals imported from Europe and North America, as well as by those born locally. Cows were raised under an intensive feeding and production systems. They were fed a diet formulated to meet the nutrient requirements. The ration is in general composed by forages (green or dry), corn silage and concentrates. It varied according to body condition, stage of lactation and milk production of cows. Fresh water was available all the time. Artificial insemination (AI) was practiced by AI technicians using frozen semen imported from Europe and North America. Estrus detection was done by visual inspection twice a day; early in the morning and in the evening. Heifers were inseminated for the first time in life when their weight reached 370 kg. Cows included in this study were kept in open stalls throughout the year. All lactating cows were machine milked two times daily. Mean annual milk production of studied herds was about 7500 kg.
Data analyzed for this study were from the artificial insemination database of COPAG (Coopérative Souss d’Amélioration Génétique Bovine, Taroudant). They consisted of reproductive information for Holstein cows. Records had details on identification number, pedigree (sire and dam), parity, birth date, previous and current calving dates, as well as insemination dates. The original file included 9871 records collected during 2018 and 2019 from cows of parities 1 to 10 reared in 241 herds, i.e. distributed under different management systems in semiarid conditions. Eight reproductive traits were considered: age at first insemination in life (AFI), gestation length (GL, the period from the last insemination to the subsequent calving), days from calving to first insemination (DCFI), days open (DO, days from calving to successful artificial insemination), days from first insemination to conception (DFIC), calving interval (CI, time elapses between two consecutive calving), number of inseminations per conception (NIC, number of inseminations needed to achieve pregnancy) and success of conception to first insemination (SCFI). The original file was edited to obtain an appropriate data set for the statistical analyses. Continuous interval traits (AFI, GL, DCFI, DO, DFIC and CI) were expressed in days. If one date (birth, insemination or calving) was not available, the interval was considered a missing value. AFI was omitted if it was lower than 274 days or higher than 639 days. GL was required to be ranged from 240 to 290 days. Traits DCFI, DO and CI were edited as follows: between 30 and 300 days for DCFI, between 30 and 330 days for DO and between 300 and 720 days for CI. A DFIC less or equal to 15 days was discarded since inseminations occurring within 15 days were considered as a single insemination. The NIC was coded as an ordinal categorical variable. The SCFI was a binary trait coded as 1 if the cow became pregnant at first insemination and 0 otherwise. Moreover, herds with less than 5 records were discarded, as well as cows with calving age less than 20 months or greater than 150 months, and parities greater than 6.
The final data set consisted of 9461 records collected from 226 herds having 5 to 224 data. Age of cows included in this study averaged 48.6 months old and the mean parity was 2.40. To determine the significance of non-genetic factors, data were analyzed by least squares analysis of variance using GLM procedure (SAS 2002). Models for reproductive traits consisted of three mixed models that included the random effect of herd (226 herds), but they differed with regard to fixed effects. The statistical model of AFI included the fixed effects of year (2018 and 2019) and season of birth (winter: January to March, spring: April to June, summer: July to September and fall: October to December). Those of GL, DFIC, NIC and SCFI included the fixed effects of parity (1, 2…, 5 or greater) and year and season of first insemination (winter, spring, summer and fall), whereas those of DCFI, DO and CI included the fixed effects of parity (2, 3,…, 5 or greater) and year and season of previous calving (winter, spring, summer and fall). Interactions between effects were not tested for studied traits and hence were assumed to be negligible.
Descriptive statistics for the studied reproductive traits are shown in Table 1. The mean value for AFI was 503±61.8 days (16.5±2.03 months). It is comparable to that reported by Jamrozik et al (2005) for Canadian Holstein cows (500 days), but higher than those published by Brzakova et al (2019) in the Czech Holstein population (479 days) and Eghbalsaied (2011) in Iranian Holstein cows (482 days). The AFI reported in the present study is adequate for a first calving between 24 and 27 months that is recommended in dairy cattle since it affects lifetime milk production of the cow and its productive life. Differences in AFI of Holstein heifers could be influenced by the plane of nutrition during the pre-pubertal growth that acts on the development of reproductive organs and the onset of puberty.
Means of GL, DCFI, DO, DFIC and CI were 276±6.39 days, 95.2±49.4 days, 125±61.3 days, 65.6±37.2 days and 437±93.4 days, respectively. Mean of GL is lower than values of 278 days (Eghbalsaied 2011) and 279 days (Toghiani 2012) for Holstein dairy cows in Iran, as well as those of Holstein heifers (278 days) and cows (279 days) in USA (Norman et al 2009b). Mean of DCFI in this research is in agreement with results of Tunisian Holstein cows (93.2 days) (M’Hamdi et al 2011), higher than means of DCFI in Australian Holstein-Friesian cattle (77 days) (Haile-Mariam et al 2003) and Iranian Holstein cows (72.9 days) (Ghiasi et al 2011), but lower than value of 110 days reported by Wu et al (2012) in Chinese Holstein. The figure of this study is greater compared to those typically reported in other countries with Holstein cows. This longer DCFI may be due to reproductive problems after calving that were not observed early, to poor estrus detection or to the strategy of farmer to delay the first insemination after calving, probably to save on insemination costs. Similar results as in our case were published by Brzakova et al (2019) for DO (124 days), but M’Hamdi et al (2011) reported a higher value (151 days) and Aghajari et al (2015) published a lower value (108.3 days) in Iranian Holstein dairy cattle. The DO of the current study is longer than the ideal value of 90 days. Higher DO may result from an extended interval from first service to conception caused by poor heat detection and service inefficiency, besides poor feed quality and health care. Mean of DFIC of the present study is nearly similar to the result recorded by Liu et al (2017) (60 days), but higher than mean values of 34 days (Kadarmideen et al 2003) and 44.8 days (Ghiasi et al 2011). The high DFIC might be attributed to the fact that cows conceiving after the first insemination or having a DFIC≤15 days were not taken into consideration. Days from parturition to first insemination (95.2 days) and from first insemination to conception (65.6 days) do not sum to days open (125 days), because of high DFIC. The CI found in the present study was higher than those reported by Toghiani (2012) (395 days) and Brzakova et al (2019) (400 days), but less than the CI observed by M’Hamdi et al (2011) (444 days). It is also greater than the optimum value of 390 days recommended in dairy cattle. Longer CI is due to high DCFI caused by poor estrus detection and expertise of AI technician, as well as reproductive disorders that result in poor success rate at first insemination. Furthermore, longer CI resulted in extended lactations causing a loss in milk income, particularly for cows with a low milk yield persistency towards the end of the lactation (Muller et al 2014). Moreover, average of CI in the current study that was 437 days, is not in good conformity with the summation of DO and GL values (125 and 276 days) because the data differed.
Mean number of inseminations per conception was 2.10±1.47. The result is comparable with 2.13 published by Ghiasi et al (2011), higher than 1.94 reported by Kadarmideen et al (2003), but less than 2.55 found by M’Hamdi et al (2011). The NIC is one of parameters for measuring cow reproductive efficiency. Thus, management level of farm, including heat detection, accurate time of insemination and health care, might explain the differences observed. In order to reduce the NIC, Wondossen et al (2018) recommended the adoption of four to five checks every day to determine the onset of true standing heat that gives a better idea about the adequate time of insemination.
The average for SCFI was 0.46±0.50. This is comparable with Kadarmideen et al (2003) who found a conception rate to first service of 0.47, but higher than values of 0.42 (Ghiasi et al 2011) and 0.41 (Muller et al 2014). Environmental variations, employment of an estrus detector and expertise of the inseminator may play a greater role in success of first insemination.
Table 1. Descriptive statistics for reproductive traits of Holstein cowsa |
|||||||
Trait |
Number |
Arithmetic |
Standard |
Coefficient of |
Minimum |
Maximum |
|
AFI (days) |
2674 |
503 |
61.8 |
12.3 |
315 |
639 |
|
GL (days) |
9220 |
276 |
6.39 |
2.32 |
240 |
290 |
|
DCFI (days) |
6208 |
95.2 |
49.4 |
51.9 |
30 |
300 |
|
DO (days) |
5680 |
125 |
61.3 |
49.2 |
30 |
330 |
|
DFIC (days) |
3691 |
65.6 |
37.2 |
56.7 |
16 |
150 |
|
CI (days) |
6123 |
437 |
93.4 |
21.4 |
301 |
719 |
|
NIC |
9441 |
2.10 |
1.45 |
69.0 |
1 |
9 |
|
SCFI |
9441 |
0.46 |
0.50 |
108.7 |
0 |
1 |
|
a AFI: age at first insemination, GL: gestation length, DCFI: days from calving to first insemination, DO: days open, DFIC: days from first insemination to conception, CI: calving interval, NIC: number of inseminations per conception and SCFI: success of conception at first insemination |
The least squares means and respective standard errors for the studied reproductive traits are presented in Tables 2, 3 and 4.
Herd and year effects on reproductive traits
All reproductive traits were significantly (P < 0.001) influenced by herd and year. Management factors, in relation with estrus detection and skills of inseminator, might explain the large differences observed among herds. Similar results have been reported in the literature (M’Hamdi et al 2011; Muller et al 2014).
Except DO and CI, parity had significant (P < 0.05 - 0.001) effects on GL, DCFI, DFIC, NIC and SCFI. In general, reproductive traits got poor as parity increased, indicating that reproductive traits of heifers were superior to those of cows. Thus, when comparing cows (parity ≥ 2) and heifers (parity 1), the linear contrast for GL was equal to 0.56±0.15 days (P < 0.001), and differences among cows of parity ≥ 2 were not significant (P > 0.05). This result is in agreement with Norman et al (2009b) who reported that Holstein cows (parity ≥ 2) generally have longer gestation length than do heifers (parity 1) (279 vs. 278 days).
The NIC was lower in heifers (parity 1) compared to cows in parity ≥ 2. The linear contrast between cows (parity ≥ 2) and heifers (parity 1) was equal to 0.88±0.03 inseminations (P < 0.001). Moreover, the NIC in the present study increased linearly by 0.21±0.01 inseminations (P < 0.001) with increasing parity number. The possible cause of the high NIC for older cows may be attributed to high reproductive disorders that affect them. Jamrozik et al (2005) and Muller et al (2014) also reported an increase of NIC with increasing number of parities. In contrast, M’Hamdi et al (2011) and Wu et al (2012) mentioned that the first lactation cows required more services than older cows (2.50 at 1st lactation to 2.11 at the 8 th lactation, and 2.6 at 1st lactation to 2.1 at the lactation ≥ 4, respectively).
The DFIC increased with parity (from 57.0 days for parity 1 to 73.7 days for parities ≥ 5). The linear contrast between cows (parity ≥ 2) and heifers (parity 1) was equal to 12.4±1.54 days (P < 0.001). This result might be a consequence of parity effects on DCFI and NIC.
The decline of SCFI was also seen with increasing number of parities (from 0.68 for parity 1 to 0.39 for parities ≥ 5). When comparing cows (parity ≥ 2) and heifers (parity 1), the linear contrast was equal to -0.28±0.01 points (P < 0.001), indicating that the success of first insemination is higher in heifers than in older cows. This result is not in agreement with the finding of Wu et al (2012) who reported that first service conception rate in lactation 1 was significantly lower than for the other lactations.
Cows had longer DCFI after their first calving than after their 2 nd, 3rd or 4th calving. After the first and last calving, DCFI was 101±1.14 and 97.7±1.50 days, respectively. This result is consistent with M’Hamdi et al (2011) who reported a decrease of DCFI with the lactation number (88 to 76 days between the first and the last lactations). Moreover, Silva et al (1992) reported that days from parturition to first service decreased linearly with advancing lactation number at the rate of about 1 day per lactation. The reason for the observed longer DCFI for cows after their first calving is not clear. Nevertheless, Muller et al (2014), who mentioned the same phenomenon, explained it by the effect of physiological stress of first calving.
Table 2. Number of observations (N), least squares means (LSM) ± standard errors (SE) for reproduction traits of Holstein cowsa |
|||||||||||
Factors of variation |
GL |
DFIC |
NIC |
SCFI |
|||||||
N |
LSM±SE |
N |
LSM±SE |
N |
LSM±SE |
N |
LSM±SE |
||||
Parity |
** |
*** |
*** |
*** |
|||||||
1 |
3057 |
275±0.14b |
965 |
57.0±1.53c |
3126 |
1.38±0.03c |
3126 |
0.68±0.01a |
|||
2 |
2461 |
276±0.15a |
1014 |
64.5±1.42b |
2526 |
2.19±0.03b |
2526 |
0.43±0.01b |
|||
3 |
1810 |
276±0.17a |
841 |
70.0±1.52a |
1860 |
2.29±0.04a |
1860 |
0.40±0.01c |
|||
4 |
1006 |
276±0.22a |
470 |
69.6±1.92a |
1019 |
2.29±0.05ab |
1019 |
0.38±0.02c |
|||
5 and 6 |
886 |
276±0.23a |
401 |
73.7±2.05a |
910 |
2.25±0.05ab |
910 |
0.39±0.02c |
|||
Season of 1st insemination |
*** |
*** |
*** |
** |
|||||||
Winter |
2442 |
276±0.15a |
999 |
63.4±1.46b |
2507 |
2.03±0.03b |
2507 |
0.47±0.01a |
|||
Spring |
2411 |
276±0.15a |
784 |
66.2±1.60b |
2454 |
2.11±0.03a |
2454 |
0.47±0.01a |
|||
Summer |
1900 |
275±0.17b |
827 |
71.7±1.53a |
1956 |
2.19±0.03a |
1956 |
0.42±0.01b |
|||
Fall |
467 |
276±0.15b |
1081 |
66.5±1.41b |
2524 |
1.98±0.03b |
2524 |
0.46±0.02a |
|||
a Least-squares means within a column that do not have a common superscript (a–c) are significantly different (P < 0.05);For traits abbreviations, see footnote of Table 1 ;**P < 0.01;***P < 0.001 |
The existence of non-significant effects of parity on DO in the current study is in line with the result of Rushdi (2015), but contrasts with those of Muller et al (2014) and Wassie et al (2015) who mentioned a gradual increase in DO, and with Wondossen et al (2018) who reported a decline in DO, with the advance in parity number. Moreover, Wu et al (2012) showed that the first lactation cows took on average 6-9 weeks longer to conceive than older cows.
Parity didn’t have significant effects (P > 0.05) on CI. This result was expected since the main component of CI that is DO was not influenced by parity, and the second component that is GL didn’t change tremendously with parity. However, our finding is not in conformity with those of Norman et al (2009a) and M’Hamdi et al (2011) who mentioned that mean Holstein CI were 12 days and 99 days, respectively shorter for parity 2 than for last parities.
Table 3. Number of observations (N), least squares means (LSM) ± standard errors (SE) for reproduction traits of Holstein cowsa |
|||||||||||
Factors of variation |
DCFI |
DO |
CI |
||||||||
N |
LSM±SE |
N |
LSM±SE |
N |
LSM±SE |
||||||
Parity |
* |
NS |
NS |
||||||||
2 |
2466 |
101±1.14a |
2221 |
125±1.58 |
2406 |
436±2.27 |
|||||
3 |
1838 |
98±1.28b |
1704 |
129±1.74 |
1825 |
438±2.52 |
|||||
4 |
1004 |
97±1.63b |
921 |
128±2.21 |
995 |
439±3.22 |
|||||
5 and 6 |
900 |
99±1.71ab |
834 |
130±2.32 |
897 |
442±3.37 |
|||||
Previous calving season |
*** |
*** |
*** |
||||||||
Winter |
1607 |
101±1.37a |
1419 |
125±1.90b |
1575 |
447±2.72a |
|||||
Spring |
1127 |
102±1.56a |
1053 |
135±2.11a |
1110 |
441±3.08ab |
|||||
Summer |
1745 |
92±1.29b |
1658 |
125±1.74b |
1736 |
428±2.54c |
|||||
Fall |
1729 |
98±1.33a |
1550 |
127±1.82b |
1702 |
439±2.63b |
|||||
a
Least-squares means within a column that do not have a
common superscript (a–c) are significantly different (P <
0.05) ; For traits abbreviations, see footnote of Table 1;
NS: Not significant P > 0.05; *P < 0.05;
|
The birth season of heifers had no significant (P > 0.05) effect on AFI, i.e. heifers had the same AFI whatever the season in which they were born (Table 4). Wondossen et al (2018) explained the absence of significant effect of birth season on age at first calving (AFC) by the long time between birth date and AFC that masks the effect of birth season on AFC of heifers.
Table 4. Number of observations (N), least squares means (LSM) ± standard errors (SE) for age at first insemination (days) of Holstein heifers |
||
Factors of variation |
N |
LSM±SE |
Birth season |
NS |
|
Winter |
645 |
507±2.41 |
Spring |
450 |
512±2.71 |
Summer |
672 |
512±2.40 |
Fall |
907 |
510±2.23 |
NS: Not significant P > 0.05 |
The GL was significantly affected by the season of first insemination (P<0.001). Cows inseminated for the first time in summer and fall had in average a GL 0.66 days shorter than that of cows having their first insemination in winter and spring. Norman et al (2009b), who observed an effect of conception month on GL, explained it by the effect of temperature.
Season of first insemination had a significant (P < 0.001) effect on the NIC. Cows inseminated for the first time in summer had a higher NIC than those having their 1st insemination in fall, winter and spring. Differences were 0.16, 0.08 and 0.21 inseminations, respectively. The significant effect of the first insemination season might be attributed to the nutritional effects imposed by the reduced availability of green forage during the dry season compared to the rainy season, which influence the fertility of cows. These findings are supported by Muller et al (2014) and Wassie et al (2015), who reported that the NIC was lower in the cooler months of the year and higher in summer. Likewise, when studying four Spanish dairy herds, Lopez-Gatius (2003) found that the number of estrus cycles and the number of services per conception were lower and higher (P < 0.05), respectively, in the summer than in the winter. However, the results of the present study are in contrast with those of Wondossen et al (2018) who reported that cows inseminated for the first time during the long rainy season had higher NIC than those that were first inseminated during the other seasons. At reverse, M’Hamdi et al (2011) observed an increase in the NIC during two periods; colder and hotter when NIC reached 3.5 and 3 services, respectively.
Cows inseminated for the first time in summer had a longer DFIC than those having their 1st insemination in fall, winter and spring. The differences were 8.3, 5.5 and 5.2 days, respectively. This might be explained by the high frequency of silent heat at high temperatures of summer.
The SCFI of cows inseminated for the first time in summer was 5%, 5% and 4% lower than those first inseminated in winter, spring and fall, respectively. Cavestany et al (1985) reported that increased maximum temperature from 29.7°C during April to 33.9°C during July was associated with a decrease in conception rate on first service from 25 to 7%.
In addition, DCFI, DO and CI were significantly (P < 0.001) affected by the previous calving season. DCFI was shorter for the cows that calved in summer compared to those that calved in winter, spring and fall. Differences were 8.6, 9.5 and 6.0 days, respectively. This result might be explained by heat stress that causes metabolic changes associated with decreased feed intake, which may reduce both the length and intensity of estrus and may lead to embryonic loss. Thus, most of cows that calved in summer will re-breed during fall and winter, i.e. in good feed conditions, and hence their DCFI is short, whereas most of those that calved in winter and spring will re-breed during summer, i.e. in harsh feed conditions, and their DCFI is long. Wu et al (2012) and Muller et al (2014) also reported that calving season affected the DCFI of Chinese and South African Holstein cows, respectively. Indeed, Muller et al (2014) reported that days from calving to first service were shorter for cows that calved from January to June, i.e. summer season in South Africa (79.4±0.6 days), than for cows that calved from July to December, i.e. winter season in South Africa (82.4±0.7 days), whereas Wu et al (2012) mentioned that cows calving in autumn had shorter and those calving in summer had longer days to first service. Muller et al (2014) ascribed this effect to the rainfall pattern, because most studied herds were located in the summer rainfall area of South Africa, therefore cows calving down from October to December had to endure wet conditions and metritis problems.
Spring calvers had significantly (P < 0.05) longer DO (135 days) than cows calved in the other seasons of the year. These results are expected because cows that calved in spring will suffer shortage of high-quality green feed during forthcoming summer impacting the ovarian activity and subsequent resumption of estrus. The effect of calving season on DO is in consonance with the literature (Silva et al 1992; Wu et al 2012; Muller et al 2014; Rushdi et al 2015). Rushdi et al (2015) found that days open were longer for the cows that calved in spring and shorter in winter, summer and fall. Likewise, VanRaden et al (2004) reported that fertility traits were poorest following spring calvings and best following fall calvings. To avoid detrimental effects of heat stress and to save on the cost of semen, several authors (Silva et al 1992; Muller et al 2014) suggested a postponement of first service after calving during the hot season as well as a reluctance to conceive once inseminated.
Cows calved in winter had significantly (P < 0.05) longer (447 days) and those calved in summer had significantly (P < 0.05) shorter (428 days) calving interval than those calved in spring and fall. Calving intervals showed the same pattern as DCFI and DO. Cows calving in summer will re-breed during fall and winter, characterized by good quality feeds, therefore having shorter DCFI and DO, and hence shorter CI. The results of present study are consistent with those of Lucy (2001) who reported longer calving interval for cows calved in spring than those calved in all other seasons.
This study provides information on the reproductive traits of Moroccan Holstein cows.
The authors would like to acknowledge COPAG (Coopérative Souss d’Amélioration Génétique Bovine, Taroudant, Morocco) for providing the data.
The author have no conflict of interests regarding the research reported in this manuscript.
Aghajari Z, Ayatollahi Mehrgardi A, Tahmasbi R and Moghbeli M 2015 Genetic and phenotypic trends of productive and reproductive traits in Iranian Holstein dairy cattle of Isfahan Province. Iranian Journal of Applied Animal Science 5(4): 819-825, http://www.ijas.ir/
Boujenane I 2017 Reasons and risk factors for culling of Holstein dairy cows in Morocco. Journal of Livestock Science and Technology 5(1): 25-31, http://lst.uk.ac.ir
Brzakova M, Zavadilova L, Pribyl J, Pesek P, Kasna E and Kranjcevicova A 2019 Estimation of genetic parameters for female fertility traits in the Czech Holstein population. Czech Journal of Animal Science 64(5): 199-206, https://doi.org/10.17221/51/2018-CJAS
Cavestany D, El-Wishy A B and Foote R H 1985 Effect of season and high environmental temperature on fertility of Holstein cattle. Journal of Dairy Science 68: 1471-1478, http://jds.fass.org/
Eghbalsaied S 2011 Estimation of genetic parameters for 13 female fertility indices in Holstein dairy cows. Tropical Animal Health and Production 43: 811-816, DOI 10.1007/s11250-010-9767-z
Ghiasi H, Pakdel A, Nejati-Javaremi A, Mehrabani-Yeganeh H, Honarvar M, González-Recio O, Carabano M J and Alenda R 2011 Genetic variance components for female fertility in Iranian Holstein cows. Livestock Science 139: 277-280, www.elsevier.com/locate/livsci
Guo G, Guo X, Wang Y, Zhang X, Zhang S, Li X, Liu L, Shi W, Usman T, Wang X, Du L and Zhang Q 2014 Estimation of genetic parameters of fertility traits in Chinese Holstein cattle. Canadian Journal of Animal Science 94: 281-285
Haile-Mariam M, Morton J M and Goddard M E 2003 Estimates of genetic parameters for fertility traits of Australian Holstein-Friesian cattle. Animal Science 76: 35-42
Jamrozik J, Fatehi J, Kistemaker G J and Schaeffer L R 2005 Estimates of genetic parameters for Canadian Holstein female reproduction traits. Journal of Dairy Science 88: 2199-2208, http://jds.fass.org/
Kadarmideen H N, Thompson R, Coffey M P and Kossaibati M A. 2003 Genetic parameters and evaluations from single- and multiple-trait analysis of dairy cow fertility and milk production. Livestock Production Science 81: 183-195, www.elsevier.com/ locate / livprodsci
Liu Z, Jaitner J, Pasman E, Rensing S, Reinhardt F and Reents R 2007 Genetic evaluation of fertility traits of dairy cattle using a multiple-trait model. Interbull Bulletin 37: 134-139
Liu A, Lund M S, Wang Y, Guo G, Dong G, Madsen P and Su G 2017 Variance components and correlations of female fertility traits in Chinese Holstein population. Journal of Animal Science and Biotechnology 8: 56, DOI 10.1186/s40104-017-0189-x
Lopez-Gatius F 2003 Is fertility declining in dairy cattle? A retrospective study in northeastern Spain. Theriogenology 60: 89-99, www.journals.elsevierhealth.com/periodicals/the
Lucy M C 2001 Reproductive loss in high-producing dairy cattle: Where will it end? Journal of Dairy Science 84(6): 1277-1293, http://jds.fass.org/
M’Hamdi N, Aloulou R, Brar S K, Bouallegue M and Ben Hamouda M 2011 Phenotypic and genetic parameters of reproductive traits in Tunisian Holstein cows. Revista Científica UDO Agricola 11(1): 167-173
Muller C J C, Potgieter J P, Cloete S W P and Dzama K 2014 Non-genetic factors affecting fertility traits in South African Holstein cows. South African Journal of Animal Science 44(1): 54-63, URL: http://www.sasas.co.za
Norman H D, Wright J R, Hubbard S M, Miller RH and Hutchison JL 2009a Reproductive status of Holstein and Jersey cows in the United States. Journal of Dairy Science 92: 3517-3528, http://jds.fass.org/
Norman H D, Wright J R, Kuhn M T, Hubbard S M, Cole J B and VanRaden P M 2009b Genetic and environmental factors that affect gestation length in dairy cattle. Journal of Dairy Science 92: 2259-2269, http://jds.fass.org/
Pryce J E, Royal M D, Garnsworthy P C and Mao I L 2004 Fertility in high producing dairy cow. Livestock Production Science 86: 125-135, www.elsevier.com/locate/livprodsci
SAS 2002 SAS/STAT, User’s Guide. SAS Institute, Cary, NC, USA
Silva H M, Wilcox C J, Thatcher W W, Becker R B and Morse D 1992 Factors affecting days open, gestation length, and calving interval in Florida dairy cattle. Journal of Dairy Science 75: 288-293, http://jds.fass.org/
Toghiani S 2012 Genetic relationships between production traits and reproductive performance in Holstein dairy cows. Archiv Tierzucht 55(5): 458-468
VanRaden P M, Sanders A H, Tooker M E, Miller R H, Norman H D, Kuhn M T and Wiggans G R 2004 Development of a national genetic evaluation for cow fertility. Journal of Dairy Science 87(7): 2285-2292, http://jds.fass.org/
Wassie T, Mekuriaw G and Mekuriaw Z 2015 Reproductive performance for Holstein Friesian × Arsi and Holstein Friesian × Boran crossbred cattle. Iranian Journal of Applied Animal Science 5(1): 35-40, http://www.ijas.ir/
Wondossen A, Mohammed A and Negussie E 2018 Reproductive performance of Holstein Friesian dairy cows in a tropical highland environment. Journal of Advances Dairy Research 6: 2. 1000203, DOI: 10.4172/2329-888X.1000203
Wu J J, Wathes D C, Brickell J S, Yang L G, Cheng Z, Zhao H Q, Xu Y J and Zhang S J 2012 Reproductive performance and survival of Chinese Holstein dairy cows in central China. Animal Production Science 52: 11-19, www.publish.csiro.au/journals/an