Theriogenology 83 (2015) 444–448
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Reproductive performance of backcross Holstein Brown Swiss and their Holstein contemporaries under subtropical environmental conditions Mahmoud S. El-Tarabany*, Khairy M. El-Bayoumi Department of Animal Wealth Development, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 July 2014 Received in revised form 30 September 2014 Accepted 6 October 2014
The objective of this study was to evaluate the reproductive performance of the Holstein (HO) and their backcross HO Brown Swiss (BS) under Egyptian subtropical conditions. The backcrosses were HBH (HO sires crossed with F1 BS HO cows) and HHB (HO sires crossed with F1 HO BS cows). Several reproductive indices and health traits for different genotypes were measured, and the effect of temperature–humidity index level (THI) on reproductive performance was investigated. Reproductive indices of the HHB backcross were better than those of the HO. The conception (30.1%) and pregnancy (28.9%) rates of the HHB backcross were significantly higher than those of the HO (28.1% and 22.6%, respectively). The calving interval and the days open of the HHB backcross were significantly shorter than those of the HO. The fertility of the HHB backcross was not affected by the level of the THI. The conception and the pregnancy rate of the HO decreased from 35.8% and 29.4%, respectively, at low THI to 16.1% and 12.1%, respectively, at high THI. The HHB backcross had the significant lowest incidence of retained placenta and metritis (9.6 and 16.9, respectively). In conclusion, despite their high milk production efficiency, pure HO had retarded reproductive performance and adaptability. On the other hand, the HHB backcross had a better adaptability and fertility under Egyptian conditions. Ó 2015 Elsevier Inc. All rights reserved.
Keywords: Holstein Fertility Backcross Heat stress Temperature–humidity index
1. Introduction The ultimate goal of the dairy industry is to operate an economically efficient production system, and this depends on high reproductive efficiency of the cows [1]. Over the past several decades, genetic selection of Holstein (HO) cows greatly improved their production traits and turned them into the most popular dairy breed. However, selective breeding for productivity with ignoring other undesirable correlated traits had resulted in lowering fertility and higher health problems [2,3]. Poor fertility decreased the profit margin because of loss in milk yield, cost of replacing culled cows, and decreased calf sales per cow [4]. To
* Corresponding author. Tel.: þ20 1223668785; fax: þ20 552283683. E-mail address:
[email protected] (M.S. El-Tarabany). 0093-691X/$ – see front matter Ó 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.theriogenology.2014.10.010
overcome these problems, higher consideration must be given to improve such traits in the developing selection policies [5]. Alternatively, HO may be crossbred with another breed [6]. In the crossbred cows, the desirable trait of one breed will mask the undesirable one of the other breed. Additionally, crossbred animals often outperform their purebred parents, particularly for traits related to fertility and health [7,8]. In crossbred animals, heterosis effects are due to genes acting in a nonadditive manner and greatly affected by the genetic diversity between the parent breeds and the system of crossbreeding [9]. Many recent crossbreeding studies that used HO with different temperate breeds had resulted in crosses having higher fertility than the pure HOs, involving Brown Swiss (BS) [10–12], and European breeds such as Normande and Montbéliarde [13,14], Scandinavian Red [12–14], and Jersey [12,15–17]. Most of these trials have been conducted under
M.S. El-Tarabany, K.M. El-Bayoumi / Theriogenology 83 (2015) 444–448
temperate conditions. However, tropical or subtropical climate greatly affected the reproductive performance of the temperate breeds [18–23]. Several trials were applied to improve the reproductive ability of dairy cows under heat stress conditions [24,25]. To overcome such problems, temperate breeds have been crossbred with native breeds to produce animals with higher adaptability to tropical and subtropical conditions [26–28]. Crossbreeding HO with native breeds usually resulted in a cross that has a comparatively lower productivity than the pure HO, so an alternative method of crossbreeding HO with another highly producing temperate breed that has higher resistance to stressful environmental conditions had been performed. To our knowledge, this is one of the recent studies to investigate the reproductive performance of crosses originated from two temperate breeds and managed under subtropical conditions. The objectives of this study were to evaluate the reproductive performance of the pure HO and their HO BS backcrosses under subtropical Egyptian conditions and compare the adaptability of the backcrosses to the subtropical conditions in comparison with their pure parent HO. 2. Materials and methods This work was reviewed and approved by the Animal Care and Welfare Committee of Zagazig University, Egypt (ANWD-206). 2.1. Animals and management This study was conducted at AL-Kawther and AL-Qasem farms, Ismailia Road, Cairo. The herd consisted mainly of pure HO (1000 cows) ranging from the first to the eighth lactation. Recently, because of higher health problem and lower fertility of the HO, the breeders decided to crossbred the HO with the BS and viscera. The HO and the BS semen were imported from progeny or genetically tested bulls. The main consideration during selection of the bull was given to the calving ease index and the predicted transmitted ability for milk production. The backcross animals were produced by mating HO BS and BS HO heifers to pure HO sires. This two-breed rotational cross resulted in 116 heifers, 3/4 HO:1/4 BS, described as HHB (HO sires crossed with F1 HO BS cows) and HBH (HO sires crossed with F1 BS HO cows). All backcross heifers or cows were inseminated with HO semen. All pure HO cows and their backcrosses were housed in a free yard provided with a cooling system that consisted of a water splashing system and large fans. The cooling system was operated when the ambient temperature reached 38 C, concomitant with extreme heat stress at a temperature–humidity index (THI) value greater than 87. Cows were fed a total mixed ration, twice daily. The ration was mixed daily and modified according to milk production and body condition score of the cows. The total mixed ration was formulated to meet the predicted requirements of energy, protein, minerals, and vitamins. Its primary analysis includes crude protein (16.91%), neutral detergent fiber (24.83%), and net energy for lactation (Mcal/kg ¼ 1.76).
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Alfalfa hay was the forage used primarily. The cows were milked three times per day and supplied with pedometers. All reproductive data (calving, insemination, pregnancy diagnosis, reproductive problems, and so forth) were recorded and tracked using a commercial on-farm computer software program (AfiFarm version 4.1). 2.2. Reproductive traits According to the usual reproductive management, the breeding season extended from September to June. Parturient cows were inseminated after 60 days postpartum. Cows conjectured in heat by visual inspection or reported excessive activities recorded by the pedometer were introduced to insemination 10 to 16 hours later. Inseminated cows received a dose of GnRH at the time of insemination. Conception status was determined via ultrasound examination at 28 to 30 days after insemination, and confirmatory pregnancy diagnosis was done at 75 days after insemination. The reproductive indices such as the conception rate, the pregnancy rate, the number of insemination per parturition, the days open, and the calving interval were measured for backcross cows present in the farms between September 2010 and June 2013. The pure HO counterparts were selected to be comparable with the backcross cows in the age and lactation number (550 HOs). The conception and the pregnancy rates were calculated as the number of cows diagnosed pregnant at 28 to 30 days and 75 days after insemination, respectively, divided by the number of cows inseminated during a specific period. The embryonic losses were calculated as the number of cows diagnosed nonpregnant at 75 days after insemination divided by the number of cows diagnosed pregnant at 28 to 30 days after insemination during a specific period. 2.3. Climatic and meteorological conditions The daily relative humidity and the daily ambient temperature recorded in the farm area were collected from the nearest meteorological station (approximately 46 kilometers far away). The monthly average temperature and THI are shown in Figure 1. These data were used to calculate the daily THI according to the previously reported equation applied in New Zealand HO cows [29]. The temperature– humidity index ¼ (1.8 AT þ 32)[(0.550.0055 RH) (1.8 AT26)], where AT ¼ air temperature ( C) and RH ¼ relative humidity (%). To investigate the effect of the THI on reproductive traits, the cows in all genotypes were classified according to the THI at the day of insemination into one of three conditions. The mild conditions include the months with THI average less than 70. The moderate conditions include the months with THI average greater than 70 and less than 75. The high conditions include the months with THI average greater than 80 and up to 85. 2.4. Statistical analysis All statistical procedures were performed using SAS statistical system package v9.2 [30]. Calving interval, days open, and average insemination per parturition variables
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M.S. El-Tarabany, K.M. El-Bayoumi / Theriogenology 83 (2015) 444–448 Table 2 Least square means standard error of calving interval, days open, and average insemination per parturition in different genotypes. Genotype
Calving interval (days)
Days open
Average insemination/ parturition
HO HBH HHB
434 3.2a 457 6.3a 392 5.4b
162 3.9a 164 5.2a 119 4.6b
3.92 0.06ab 4.27 0.18a 3.28 0.16b
Values with different superscripts in the same column are significantly different (P < 0.05). Abbreviations: HBH, crossbred cows originated from Holstein sire F1 (Brown Swiss Holstein) cow; HHB, crossbred cows originated from Holstein sire F1 (Holstein Brown Swiss) cow; HO, Holstein.
3.2. Effect of THI on reproductive performance of different genotypes Fig. 1. The monthly average temperature (-) and temperature–humidity index (THI, :) in the area of the farm.
3. Results
The conception and pregnancy rates were similar for all genotypes at low THI (Table 3). The temperature–humidity index level does not have any effect on conception, pregnancy, and embryonic loss rates in the HHB backcross. Whereas, the conception and the pregnancy rate of the HO were negatively affected by higher THI level. The conception and the pregnancy rate of the HO were declined from 35.8% and 29.4%, respectively, at the low THI to 16.1% and 12.1%, respectively, at the high THI. Comparable lower estimates at the high THI were recorded in the HBH backcross (12.2% and 10.3%, respectively). In comparison with the low and the moderate THI, the high THI increased the embryonic loss rate (26.2%) in the pure HO.
3.1. General reproductive performance
3.3. Health traits
The HO and the backcross cows received 2420 and 464 inseminations, respectively. The conception and the pregnancy rates of the HHB backcross (30.1% and 28.9%, respectively) were significantly higher than those of the HO (28.1% and 22.6%, respectively). The same backcross had lower embryonic loss rate (3.8%) than that recorded in the pure HO and the other backcrosses (Table 1). The calving interval and days open of the HHB backcross (392 and 119, respectively) were significantly shorter than those of the pure HO (434 and 162, respectively). On the contrary, the HBH backcross cows had comparable estimates to the pure HO (Table 2). The average insemination per parturition in the HBH backcross cows (4.27) was significantly higher than that in the pure HO and the other backcrosses (3.92 and 3.28, respectively).
The pure HO and other backcrosses did not show any difference in the percentage of the cows that had clinical mastitis (Table 4). The HHB backcross had the significant lowest incidence of retained placenta and metritis (9.6 and 16.9, respectively), therefore suggesting an overall improvement in reproductive health traits for those backcross cows compared with their pure HO contemporaries. The incidence of retained placenta and metritis in the HBH backcross (29.6 and 33.3, respectively) was comparable to that in the pure HO.
were analyzed using one-way ANOVA through the general linear models procedure, after verifying normality using the Kolmogorov–Smirnov test. The comparison of means was carried out with the Duncan multiple range tests. The chi-square test was used to evaluate association between genotype and proportion dichotomous variables (conception, pregnancy, and embryonic loss rates). Significant results were followed by multiple z tests to compare corresponding proportions. The P value for all pairwise comparisons was adjusted using the Bonferroni correction.
Table 1 Conception, pregnancy, and embryonic loss rates in different genotypes. Genotype Insemination number
Conception (%)
Pregnancy (%)
Embryonic loss (%)
HO HBH HHB
28.1a 23.5a 30.1a
22.6b 18.9b 28.9a
19.5a 19.4a 3.8b
2420 226 238
Values with different superscripts in the same column are significantly different (P < 0.05). Abbreviations: HBH, crossbred cows originated from Holstein sire F1 (Brown Swiss Holstein) cow; HHB, crossbred cows originated from Holstein sire F1 (Holstein Brown Swiss) cow; HO, Holstein.
4. Discussion Egyptian climatic conditions are considered to be stressful for the HO cows and retarded the fertility of HO cows except in December, January, February, and March. In the present study, the HHB backcross showed better fertility especially during the months characterized by high THI, and this is in agreement with previous reports [31]. Earlier studies reported that F1 HO BS crossbreds had fewer days open (144 vs. 156 days) than did HO [10]. However, they showed that BS HO backcross cows did not differ from HO for any considered reproductive traits. Because those genotypes are reared under the same environmental and managerial conditions, these differences may be referred mainly to genetic makeup.
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Table 3 Effect of the temperature–humidity index (THI) on conception, pregnancy, and embryonic loss rates in different genotypes. Genotype
Conception (%)
Pregnancy (%)
Embryonic loss (%)
THI
Low
Moderate
High
Low
Moderate
High
Low
Moderate
High
HO HBH HHB
35.8a 33.3a 32.6a
27.2b 25.0a 33.9a
16.1c 12.2b 25.7a
29.4a 25.8a 31.4a
21.8b 21.5a 31.2a
12.1c 10.3b 23.1a
17.7b 22.7a 0.0a
19.5b 28.6a 0.0a
26.3a 33.3a 3.6a
Values with different superscripts in the same row are significantly different (P < 0.05). Low, THI less than 70; moderate, THI greater than 70 and less than 75; high, THI above 80 and up to 85. Abbreviations: HBH, crossbred cows originated from Holstein sire F1 (Brown Swiss Holstein) cow; HHB, crossbred cows originated from Holstein sire F1 (Holstein Brown Swiss) cow; HO, Holstein.
The decline in reproductive ability of purebred HO may be attributed to the state of negative energy balance that occurs after parturition and when entering the lactation. This concurrently associated with the reduced expression of estrus and lessened responses to procedures for synchronization of estrus [32]. In comparison with the HO, better fertility recorded in the HHB backcross is in agreement with previous reports [10–12]. In the present study, the recorded days open for the HO and the HBH backcross cows are comparatively higher than those reported in a recent work [11], but they are comparable with some earlier reports [10]. This may be due to different managerial and environmental conditions in which the experiments were conducted or due to the fact that the authors considered the days open up to 250 days [10,11]. Whereas, in the present study, we used the actual data without any modulation. The number of services recorded in the present study for the HO and the HHB backcross cows is comparatively higher than that reported in former studies [11]. They calculated the number of services per conception on the basis of the maximum number of services to be six, whereas in the present study, we calculated the number of services per parturition without any adjustment. Fertility of the HHB backcross was not affected by the level of the THI compared with that of the pure HO. This indicates higher heat stress tolerance. Similar findings were previously reported [31,33,34]. In other respects, earlier studies revealed that peripheral blood mononuclear cells from the HO are more tolerant to chronic heat exposure than those from the BS cows [35]. The stressful effects of heat on the reproductive performance occur at different stages beginning from folliculogenesis, steriodogenic activity of the follicle, quality of the oocytes, steroidogenic activity of the corpus luteum, embryo survival, and secretory activity of endometrium [18,20]. The ability of the
Table 4 Incidence of retained placenta, metritis, and mastitis in different genotypes. Genotype
Retained placenta
Metritis
Mastitis
HO HBH HHB
16.3ab 29.6a 9.7b
28.9a 33.3a 16.9b
41.3a 37.5a 31.2a
Values with different superscripts in the same column are significantly different at level (P < 0.05). Abbreviations: HBH, crossbred cows originated from Holstein sire F1 (Brown Swiss Holstein) cow; HHB, crossbred cows originated from Holstein sire F1 (Holstein Brown Swiss) cow; HO, Holstein.
cows to dissipate heat to the environment and retard the heat gain from surrounding stressful environment conditions controls the capability of the cow to maintain its body temperature in a physiological homeostasis and in a thermoneutral zone [36]. Food intake and the metabolic rate determined the heat gain, whereas the heat dissipating ability is affected by the character of the hair coat, the number of sweat glands, the surface area, and the fat distribution [19]. Furthermore, the presence of a distinct mechanism that involved some genes controlling the resistance to cellular heat shock was suggested [37]. From all the formerly mentioned, it is obvious that the HHB backcross has one or more of such mechanisms that improve their tolerance to heat stress. The HHB backcross investigated in the present study showed better fertility than the HO and other backcrosses either at high or at moderate THI. Different temperate crosses had better performance than the HO during the warm season [31]. Crossbreeding local breed with HO resulted in a cross that had higher ability to accommodate with heat stress conditions, and this tolerance decreased when crossbreds have higher than 87.5% HO genetic makeup [26]. The results of the present study indicate that using the F1 HO BS as a dam will improve the tolerance ability of heat stress in the backcross animals. Our results revealed an overall improvement in the reproductive health traits of HHB backcross in comparison with those of the pure HO. These findings correlated clearly with the shorter calving interval and days open in the HHB backcross. A lot of studies have shown that diseases related to the reproductive tract (dystocia, retained placenta, and metritis) are interrelated and can affect the length of calving interval, the number of days open, and the reproductive efficiency in general [38,39]. Our findings support those of Brown, et al. [32] who found that incidence of metritis in pure HO (16.9) was higher than that in their crossbreds (4.8). On the other hand, our results presented herein are in disagreement with those of previous studies involving HO BS backcrosses [40]. They concluded that health traits were similar in the pure HO and their backcrosses, suggesting no overall improvement in health for the backcross cows. In conclusion, crossbreeding the HO sires with the F1 (HO BS) dams resulted in HHB backcrosses that have higher fertility, improved health traits, and higher adaptability to Egyptian subtropical environment. Although the present study involves one of the next generation crosses, it is evident that more generations are required to completely assess the long-term differences between pure HOs and their backcross cows.
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Acknowledgments The authors wish to thank the owner of AL-Kawther and AL-Qasem farms, Ismailia Road, Cairo for allowing them to collect the data. They appreciate the great help of Dr Hany Abdalla, lecturer of theriogenology, and veterinary doctor Mohamed Hussein, the head manager of the farms, in collecting and managing the data by the AfiFarm. Competing interests None of the authors have any conflict of interest to declare.
References [1] Royal MD, Darwash AO, Flint APF, Webb R, Woolliams JA, Lamming GE. Declining fertility in dairy cattle: changes in traditional and endocrine parameters of fertility. Anim Sci 2000;70:487–501. [2] Hansen LB. Consequences of selection for milk yield from a geneticist’s viewpoint. J Dairy Sci 2000;83:1145–50. [3] Lucy MC. Reproductive loss in high-producing dairy cattle: where will it end. J Dairy Sci 2001;84:1277–93. [4] Stoat AW, Verrkamp RF, Wassell TR. The economics of fertility in the dairy herd. Anim Sci 1999;68:59–67. [5] Butler ST. Genetic control of reproduction in dairy cows. Reprod Fertil Dev 2013;26:1–11. [6] Buckley F, Lopez-Villalobos N, Heins BJ. Crossbreeding: implications for dairy cow fertility and survival. Animal 2014;8:122–33. [7] Swan AA, Kinghorn BP. Evaluation and exploitation of crossbreeding in dairy cattle. J Dairy Sci 1992;75:624–39. [8] Van Aden PM, Sanders AH. Economic merit of crossbred and purebred US dairy cattle. J Dairy Sci 2003;86:1036–44. [9] McAllister AJ. Is crossbreeding the answer to questions of dairy breed utilization. J Dairy Sci 2002;85:2352–7. [10] Dechow CD, Rogers GW, Cooper JB, Phelps MI, Mosholder AL. Milk, fat, protein, somatic cell score, and days open among Holstein, Brown Swiss, and their crosses. J Dairy Sci 2007;90:3542–9. [11] Blöttner S, Heins BJ, Wensch-Dorendorf M, Hansen LB, Swalve HH. Brown Swiss Holstein crossbreds compared with pure Holsteins for calving traits, body weight, backfat thickness, fertility, and body measurements. J Dairy Sci 2011;94:1058–68. [12] Schaeffer LR, Burnside EB, Glover P, Fatehi J. Crossbreeding results in Canadian dairy cattle for production, reproduction and conformation. Open Agric J 2011;5:63–72. [13] Heins BJ, Hansen LB, Seykora AJ. Fertility and survival of pure Holsteins versus crossbreds of Holstein with Normande, Montbeliarde, and Scandinavian Red. J Dairy Sci 2006;89:4944–51. [14] Heins BJ, Hansen LB. Short communication: fertility, somatic cell score, and production of NormandeHolstein, MontbéliardeHolstein, and Scandinavian Red Holstein crossbreds versus pure Holsteins during their first 5 lactations. J Dairy Sci 2012;95:918–24. [15] Olson KM, Cassell BG, McAllister AJ, Washburn SP. Dystocia, stillbirth, gestation length, and birth weight in Holstein, Jersey, and reciprocal crosses from a planned experiment. J Dairy Sci 2009;92: 6167–75. [16] Heins BJ, Hansen LB, Hazel AR, Seykora AJ, Johnson DG, Linn JG. Short communication: Jersey Holstein crossbreds compared with pure Holsteins for body weight, body condition score, fertility, and survival during the first three lactations. J Dairy Sci 2012;95:4130–5. [17] de Haas Y, Smolders EA, Hoorneman JN, Nauta WJ, Veerkamp RF. Suitability of cross-bred cows for organic farms based on cross-breeding effects on production and functional traits. Animal 2013;7:655–65. [18] Wolfenson D, Roth Z, Meidan R. Impaired reproduction in heatstressed cattle: basic and applied aspects. Anim Reprod Sci 2000; 61:535–47.
[19] Kadzere CT, Murphy MR, Silanikove N, Maltz E. Heat stress in lactating dairy cows: a review. Livestock Prod Sci 2002;77:59–91. [20] De Rensis F, Scaramuzzi RJ. Heat stress and seasonal effects on reproduction in the dairy cowda review. Theriogenology 2003;60: 1139–51. [21] West JW. Effects of heat-stress on production in dairy cattle. Dairy Sci 2003;86:2131–44. [22] Boni R, Perrone LL, Cecchini S. Heat stress affects reproductive performance of high producing dairy cows bred in an area of southern Apennines. Livestock Sci 2014;160:172–7. [23] Schüller LK, Burfeind O, Heuwieser W. Impact of heat stress on conception rate of dairy cows in the moderate climate considering different temperature–humidity index thresholds, periods relative to breeding, and heat load indices. Theriogenology 2014;81:1050–7. [24] Berman A. Invited review: are adaptations present to support dairy cattle productivity in warm climates? J Dairy Sci 2011;94: 2147–58. [25] Kadokawa H, Sakatani M, Hansen PJ. Perspectives on improvement of reproduction in cattle during heat stress in a future Japan. Anim Sci J 2012;83:439–45. [26] Boonkum W, Misztal I, Duangjinda M, Pattarajinda V, Tumwasorn S, Buaban S. Short communication: genetic effects of heat stress on days open for Thai Holstein crossbreds. J Dairy Sci 2011;94:1592–6. [27] Mellado M, Coronel F, Estrada A, Ríosb FG. Lactation performance of Holstein and Holstein Gyr cattle under intensive conditions in a subtropical environment. Trop Subtropical Agroecosystems 2011; 14:927–31. [28] Hailu A. Cross breeding effect on milk productivity of Ethiopian indigenous cattle: challenges and opportunities. Scholarly J Agric Sci 2013;3:515–20. [29] Kendall PE, Webster JR. Season and physiological status affects the circadian body temperature rhythm of dairy cows. Livestock Sci 2009;125:155–60. [30] SAS. SAS/STAT users guide. Cary, NC 27513, USA: SAS Institute INC; 2002. [31] Ruvuna F, McDaniel BT, McDowell RE, Johnson JC, Hollon BT, Brandt GW. Crossbred and purebred dairy cattle in warm and cool seasons. J Dairy Sci 1983;66:2408–17. [32] Brown KL, Cassell BG, McGilliard ML, Hanigan MD, Gwazdauskas FC. Hormones, metabolites, and reproduction in Holsteins, Jerseys, and their crosses. J Dairy Sci 2012;95:698–707. [33] Badinga L, Collier RJ, Thatcher WW, Wilcox CJ. Effects of climatic and management factors on conception rate of dairy cattle in subtropical environment. J Dairy Sci 1985;68:78–85. [34] Correa-Calderon A, Armstrong DV, Ray DE, DeNise SK, Enns RM, Howison CM. Productive and reproductive response of Holstein and Brown Swiss heat stressed dairy cows to two different cooling systems. J Anim Vet Adv 2005;6:572–8. [35] Lacetera N, Bernabucci U, Scalia D, Basirico’ L, Morera P, Nardone A. Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein Cows. J Dairy Sci 2006; 89:4606–12. [36] Maia ASC, daSilva RG, Battiston Loureiro CM. Sensible and latent heat loss from the body surface of Holstein cows in a tropical environment. Int J Biometeorol 2005;50:17–22. [37] Paula-Lopes FF, Chase CCJ, Al-Katanani YM, Krininger CE, Rivera RM, Tekin S, et al. Genetic divergence in cellular resistance to heat shock in cattle: differences between breeds developed in temperate versus hot climates in responses of preimplantation embryos, reproductive tract tissues and lymphocytes to increased culture temperatures. Reproduction 2003;125:285–94. [38] Erb HN, Smith RD, Oltenacu PA, Guard CL, Hillman RB, Powers PA, et al. Path model of reproductive disorders and performance, milk fever, mastitis, milk yield, and culling in Holstein cows. J Dairy Sci 1985;68:3337–49. [39] Gröhn YT, Rajala-Schultz PJ, Allore HG, DeLorenzo MA, Hertl JA, Galligan DT. Optimizing replacement of dairy cows: modeling the effects of diseases. Prev Vet Med 2003;61:27–43. [40] Bjelland DW, Weigel KA, Hoffman PC, Esser NM, Coblentz WK, Halbach TJ. Production, reproduction, health, and growth traits in backcross Holstein Jersey cows and their Holstein contemporaries. J Dairy Sci 2011;94:5194–203.