Crossbred Dairy Cattle is the Answer to Improve Environment Dependent Productive and Physiological Responses – A Review

Juan Augusto Hernández-Rivera1, Jaime Molina-Ochoa2,*, Luis Jorge García-Márquez1, Omar Francisco Prado-Rebolledo1, Rafael Julio Macedo-Barragán1, Arturo César García-Casillas1 and Muhammad Irfan Ullah3

1Facultad de Medicina Veterinaria y Zootecnia, Universidad de Colima, Tecomán, Colima 28930, Mexico

2Coordinación General de Investigación Científica, Universidad de Colima, CUIDA, Mexico

3Department of Entomology, University of Sargodha, Sargodha 40100, Pakistan

ABSTRACT

Heat stress has severe effects in organisms. Dairy cattle is susceptible to suffer behavioral, physiological and reproductive damages due heat stress. Breeding searching for tolerant heat stress genes and their incorporation in crossbreeding programs has gained interest in dairy cattlemen concerned by the global warming and greenhouse effect in the environment. This review shows and update of the crossbreeding in dairy cattle in both hemispheres. Here, is reviewed the effect of heat stress on dairy cattle; the mechanism of autoregulation; the benefits of the heterosis in crossbreeding cattle by hybridization; the body condition score in crossbred dairy cattle; the yields in crossbreds; here is also discussed that even when there have been many crossbreeding in dairy cattle, but when the producer choose a system crossbreeding in dairy cows always mostly contemplate only body weight, body condition score, dry matter intake, and feed efficiency. Is suggested to contemplate other traits like genetic potential, lactation (305 d), lactation number, fertility rate, and economic impact to observe clarity the potential of each crossbred in dairy cattle in the future.

Article Information

Received 14 March 2018

Revised 02 June 2018

Accepted 17 July 2018

Available online 11 March 2019

Authors’ Contribution

JAHR, JMO, LJGM, OFPR and RJMB wrote the initial manuscript. JAHR, JMO, ACGC, and MIU corrected the manuscript attending the reviewer’s suggestions and language of the manuscript.

Key words

Crossbreeding, Dairy cattle, Heat stress, Physiological responses, Heterosis.

DOI: http://dx.doi.org/10.17582/journal.pjz/2019.51.2.773.788

* Corresponding author: [email protected]

0030-9923/2019/0002-0773 $ 9.00/0

Copyright 2019 Zoological Society of Pakistan

Introduction

For many years, the superiority for milk yield in Holstein breed cows has limited the use of other breeds or crossbreeding in dairy farms worldwide. In the USA, fewer than 7% of dairy herds are other than purebred or grade Holsteins (McAllister, 2002; Nehring et al., 2017). However, over the past few years dairy producers have shown more interest in crossbreeding programs for dairy cattle, especially in warm climate regions. Through classical genetic improvement tools a heat tolerant gene can be introduced into a less heat tolerant breed helping cattle to better adapt to warmer environmental temperatures.

Holstein cows have outstanding production when environment temperatures ranges between 5 and 25oC and temperature-humidity index (THI) does not exceed 72 units which is considered the thermal comfort zone for dairy cows (McDowell, 1972; Akyuz et al., 2010). However, in areas subjected to warm climates Holstein cows do not fully express their potential for milk yield and have their reproductive proficiency compromised (Dikmen et al., 2009; West, 2003; De Rensis and Scaramuzzi, 2003). Cows that calve during winter months produce more milk in 305-day lactations than cows calving during hot summer months (McDaniel et al., 1967). In a study in Israel during summer Holstein cows decrease milk yield, 8 % and conception rate 70 % regarding winter (Flamenbaum and Galon, 2010). In agree, Folman et al. (1979) found only about an 8% decline in milk yield for summer conditions when the mean afternoon temperature was 39.8 °C compared with winter conditions. Studies carried in climatic chambers, described a decrease in milk yield of 14% in early lactating dairy cows (Lacetera et al., 1996) kept under heat stress conditions. Under Mediterranean climatic conditions, summer calvers produce less milk per lactation than winter calvers (Barash et al., 1996). In Po Valley, northern Italy, Speroni et al. (2006) found 16% less milk yield after the start of the hot period regarding before the star of the hot period in multiparous dairy cows under milking parlor system. Following, diverse authors have shown their preoccupation respect to heat stress topic on milk yield in different parts of the world such as Missouri, Arizona, U.S., Israel, México, etc. (Igono et al., 1987, 1992; Her et al., 1988; Flamenbaum et al., 1995; Correa et al., 2002; Avendaño et al., 2006, 2010; Adin et al., 2009). Also, St-Pierre et al. (2003) reported that heat stress greatly affected economic loss by the US dairy industry and that estimated losses ranged from $897 to $1,500 million, annually. Several strategies have been suggested to minimize the negative effect of heat stress in dairy cows, including facilities design, cooling systems, feeding and breeding strategies and genetic management (Armstrong, 1994; West, 1999; Berma, 2008).

A recent report evaluating the breed composition of the US dairy cattle identified an increased percentage of crossbred dairy herds in US from 0.4 % for cows born in 1990 to 0.7 % in 2000 and 1.6% in 2005 (Powell et al., 2008). More recently, it has been estimated the US dairy cattle population of 9.2 million of dairy cows (USDA, 2009) in which 3.3% correspond to the crossbred and 90.1% to Holstein cows. These crossbred cows in the US are responsible for 2.7 million kg of milk and 102,000 kg of milk fat. In New Zealand, the proportion of crossbred dairy cows is higher than in the US. In the New Zealand 2006/2007 season dairy cow population accounted with 3.92 million of dairy cows (LIC, 2007) in which crossbred represented 31.6% mainly formed by Jersey x Holstein cross. These crossbred cows were responsible for 15.1 billion Kg of milk and 750 million Kg of milk fat and 566 million Kg of milk protein during that season. Differently than US and New Zealand, other places in Africa and Asia uses Bos taurus x Bos indicus crossbreds for dairy propose. In Thailand, more than 95% of the dairy herd is crossbred using Holstein and Sahiwal or Thai native breeds (Boonkum et al., 2011). The benefit of this crossbreeding strategy is the introduction of heat tolerant and diseases resistant gen from Sahiwal or Thai native into a less heat tolerant and less disease resistant breed such as Holstein (Reodecha et al., 2002; Chanvijit et al., 2005). The advantage of these crossbreeding strategies is due the hybrid vigor (heterosis) observed on the hybrid offspring (Hill et al., 1983; Lopez-Villalobos et al., 2000).

Therefore, the objective of this review is to describe the main effects of the environmental heat stress on productive and physiological responses crossbred dairy cows.

 

Effect of heat stress on dairy cattle

Heat stress is a term that describes the increase of several environment conditions such as: humidity, air temperature, radiation, and air movement (Jordan, 2003). Thus, the heat stress appears when any combination of these environmental conditions causes discomfort in the animal due to inefficiency heat loss, this produces negative effects on the productive and reproductive efficiency of the dairy cattle (Armstrong, 1994; McManus et al., 2011). Heat stress compromises oocyte growth in cows by altering progesterone, the secretion of luteinizing hormone and follicle-stimulating hormone and dynamics during the oestrus cycle (Ronchi et al., 2001; Hernández et al., 2011). Also, a drop can occur in summer of about a 20–27% in conception rates (Chebel et al., 2004; Lucy, 2002; Calderón et al., 2012) or a decrease in 90-day non-return rate to the first service in lactating dairy cows (Al-Katanani et al., 1999; Das et al., 2016; Ali et al., 2018).

On the other hand, Johnson (1976) attributed that the milk yield variation was due to climatic factors is among 3-10%. In addition, dairy cows in lactation produce greater amount of metabolic heat, this combined with the heat generated by atmosphere result in the increase and gain from heat corporal (Fuquay, 1981; Krishnan et al., 2017). The heat increment for feeding in cattle is high (35-70% of metabolisable energy), depending on the balance of nutrients. Heat increment is non-useful energy and, during heat stress, must be dissipated (Polsky and von Keyserlingk, 2017; Grandl et al., 2018). As environmental temperature increases, animals require extra energy to dissipate the heat load (Al-Dawood, 2017). Reduction of fiber intake, particularly with a minimum fall in metabolizable energy, may lower the heat increment sufficiently to act as a partial protection against forecast high heat stress (Fuquay, 1981; Al-Dawood, 2017). As the result, the higher threshold in the Thai crossbred population might due to the combinations of heat-tolerance genes from Bos indicus and the lower production. Generally, Thai cattle are rarely fed to their genetic potential because of the low quality of tropical roughages (Boonkum et al., 2011). The best recognized effect of heat stress is an adaptive depression of metabolic rate associated with reduced appetite (Silanikove, 2000). Heat stress causes the rostral cooling center of the hypothalamus to stimulate the medial satiety center which inhibits the lateral appetite center and consequently lowers milk yield (Kadzere et al., 2002). The arterial plasma volatile fatty acids they are in the form of acetate. Animals under heat stress conditions the plasma acetate percent is high (69% to 77%) this would be explainable in the light of the high energy and substrate demands for milk synthesis, because acetate is the major energy source of normal fed ruminants (Chaiyabutr et al., 2008). In addition, acetate is involved in mammary gland metabolism in either de novo synthesis of short and medium-chain milk fatty acids or generation of ATP and NADPH. On the other hand, the high values of concentrations of arterial plasma β-hydroxybutyrate on animals under heat stress would be consistent with an increase in oxidation of free fatty acids (Bauman et al., 1988; Al-Dawood, 2017). A greater energy requirement due to panting of animals during heat stress, resulting in increased hepatic ketogenesis due to greater mobilization of fat reserves, might be apparent under high temperatures (Collier et al., 2017a). A simple approach to quantify heat stress is the THI which is estimated by combining environmental temperature and relative humidity (i.e. THI = [0.81 x average temperature] + relative humidity [average temperature – 14.4] + 46.4; Hahn, 1999). Using this index, heat stress in dairy cattle starts at 72 units (Armstrong, 1994). Environmental effects on milk yield are difficult to determine due to can be affected by other factors such as management nutrition which can or not be ligature to factors related to the environment (Fuquay, 1981). However, currently studies on environmental impacts of milk were assessment (De Vries and de Boer, 2010). In a study, cows were fed diets of 16%, 17.9%, 19.4% and 21.2% acid detergent fiber during warm (THI between 64 and 77) and hot weather conditions (THI between 72 and 84) (Table I). However, Thatcher et al. (1994) has divulged fat and milk yield less like result by high temperatures. Heat stress has effect negatives on the secretory function of the udder (Silanikove, 1992). In addition, when dairy cows be are on THI by 83, the milk yield can fall 53%, and total energy output fall 48% (Anzures-Olvera et al., 2015). Also, percentage of fat, protein and lactose in milk decrease 19, 13, and 9%, respectively (Joksimović-Todorović et al., 2011). In order to improve the milk yield it is major lower levels of hyperthermia by environmental manipulation. Several studies have shown different cooling strategies to decrease heat stress effects on milk yield in dairy cattle (Table II).

Autoregulation mechanism on environmental

Physiological variables on crossbred dairy cattle are shown in Table III. Heat flow occurs through processes dependent on surrounding temperature (sensible heat loss; i.e. conduction, convection, radiation) and humidity (latent heat loss; evaporation through sweating and panting) (Hansen, 2004; Allen et al., 2015; Chand et al., 2017). The rectal temperature (RT) and respiration rate (RR) are excellent indicators to predict the heat stress presence in the dairy cattle (Collier et al., 2017b). Fabris et al. (2017) reported that cows increase RT and RR from 77 units of THI. Under heat stress condition the RR can increase 64% more than normal (20 breath/min) in thermoneutral zone (Arias et al., 2018). Berman et al. (1985) found that the respiratory frequency started rising above 50–60 breaths /min at ambient temperatures higher than 25 °C).

 

Table I.- Effect of heat stress on milk yield (kg day-1) and % milk fat of cows fed diets differing in acid detergent fiber (ADF) concentrations.

Milk yield (kg day-1)			Milk fat (%)
% ADF of diet	Warm temp.a,c	Hot temp.b,d	Warm temp.a	Hot temp.b,c
16.00	32.30	24.60	3.24	3.21
17.90	32.60	25.80	3.49	3.28
19.40	31.40	26.40	3.58	3.50
21.20	28.90	22.70	3.62	3,69

a, Minimum and maximum THI was 64 and 77, respectively; b, Minimum and maximum THI was 72 and 84, respectively; c, Linear effect; d, Quadratic effect. Source, West et al. (1999).

 

Table II.- Strategies of cooling and THI on the milk yield of dairy cattle during summer.

Location	Treatment and milk yield (kg/d)		THI (Max)	Cooling time (h/d)	Reference
	NC	C
Missouri, USA	23.00	25.00*	76.00	24.00¤	Igono et al. (1987)
Israel	32.10	35.00*	87.60	4.50	Her et al. (1988)
Arizona, USA	23.00	32.00*	79.00	11.00	Igono et al. (1992)
Beit-Dagan, Israel	34.00	35.00	78.00	11.00¥	Flamenbaum et al. (1995)
Mexicali, Mex	27.00	31.00*	89.00	8.00	Correa et al. (2002)
Mexicali, Mex	20.20	22.20*	79.00	3.00	Avendaño et al. (2006)
Mexicali, Mex	19.101	21.12*	91.30	3.00	Avendaño et al. (2010)
Mexicali, Mex	17.43	18.70*	83	4	Avendaño et al. (2012)
Mexicali, Mex	16.16	16.12	83	4	Hernández et al. (2011)
Moshav Timmorim, Israel	39.30	41.40*	77.40	4.00	Adin et al., 2009
Kingdom, Saudi Arabia	52.28≠	52.20∞	80	13-14	Ortiz et al. (2015)
Pirassununga, SP, Brazil	18	22	78	24	Titto et al. (2013)
Buckeye, Arizona	29.6	31.3	80	2.25	Anderson et al. (2013)

*P<0.05; NC, Control; C, Cooling; THI, temperature-humidity index.1Cooling by one hour, cooling system ignited if the environmental were greater to >27ºC; ¥, Cooling system ignited each 2 h during 30 min. ≠, Korral Kool system (Korral Kool Inc., Mesa, AZ); ∞, FlipFan system (Schafer Ventilation Equipment LLC, Sauk Rapids, MN).

 

Table III.- Physiological variables on crossbred dairy cattle differences.

Crossbred group	Rectal temperature (°C)	Respiration rate (breaths/min)	Body condition score	Reference
Jersey x Holstein	- -	- -	2.90 ± 0.03a 2.76 ± 0.04b	Heins et al. (2008a)
Holstein
Jersey x Holstein	- -	- -	2.80 ± 0.03a	Heins et al. (2008b)
Holstein			2.71 ± 0.03b
Brahman x Holstein	39.86 ± 0.48	85.16 ± 1.37	-	Khongdee et al. (2010)
Thai x Holstein	41.21 ± 0.28	86.87 ± 0.12	-	Khongdee et al. (2006)
Jersey x Holstein	-	-	4.62 ± 0.01a 4.54 ± 0.01b	Auldist et al. (2007)
Holstein
Red Shindi x Holstein	39.37 ± 0.7	73 ± 15.67	-	Chaiyabutr et al. (2008)
Cambodian native zebu × Holstein-Friesian	40.0 ± 1.0	-	-	Bun et al. (2018)
Zebu x Holstein	38.6 ± 0.75	55 ± 2.52	-	De Paula Xavier de Andrade et al. (2017)
Gyr x Holstein	≥ 39.3	≥ 36	3.5	Da Costa et al. (2015)
Gyr x Holstein	-	65 ± 5	-	Santos et al. (2017)

Means with different superscripts within a row are significantly different (P < 0.05).

 

On the other hand, it has been observed that RR can decrease after providing cold water (Golher et al., 2015). The RT increase 0.7% more than normal (38.5 °C) (Igono et al., 1992). It has been demonstrated that under heat stress conditions RT increases, then decreases the consumption of dry matter, cud process and food passage rate (Kamal et al., 2016a, b). Consequently, milk production decreases, mainly in cows that have been exposed to high temperatures for at least 67 days (Ammer et al., 2018). It appears that there are notable differences between breeds in their abilities to regulate RT: the mean rectal temperature is higher in Bos taurus than in Bos indicus cattle (Hansen, 2004) and, as a result, B. taurus cattle are more sensitive to heat stress than their Bos indicus counterparts (Hansen, 2007). An increase in the panting and sweating by dairy cows would be the normal mechanism by which animals dissipate heat load from their body to maintain thermoregulation in hot ambient conditions (Polsky and von Keyserlingk, 2017). In fact, during heat stress, evaporative heat loss via respiration rate can be greater for European breeds respect Bos indicus (Gaughan et al., 1999). Kibler and Brody (1950) showed that Jersey cows had much higher respiration rates than Holsteins, which they attributed to the Jersey cows better ability to dissipate heat compared to Holsteins. Then it is not to be surprised that Jersey x Holstein cows had lower vaginal temperatures during much of the day than Holstein or Jerseys suggests that thermotolerance is another trait controlled by heterosis (Dikmen et al., 2009). The hair coats of cattle of different breeds vary from fine and glossy to thick and woolly, and present a range of insulation values; this will affect heat exchange by convection and evaporation of sweat. Since year 50’s we know that zebus had a higher sweating rate than European breeds (Kibler and Brody, 1952). It was not until ends 50’s and beginning 60’s when discovering that gland numbers in zebus is greater than British breeds (Ferguson and Dowling, 1955; Allen et al., 1962). In fact, studies have now been made to confirm that the rate of sweating is higher in Bos indicus (Gaughan et al., 1999). Blazquez et al. (1994) reported that increased blood flow to the skin is positively correlated to the sweating rate. Likewise, the direct relationship between the rate of skin sweating and the coat surface temperature (Silva and Maia, 2011). Jersey heifers showed a linear increase in sweating rate with increasing air and skin temperature, whereas the sweating rate of zebu heifers did not rise until skin temperature reached 35 °C and air temperature 30°C (Allen, 1962). In fact, sweating rate was greater for zebu cattle than european cattle (Hansen, 2004). Respiratory rate was also greater in the Jersey, indicating more reliance on respiratory evaporation. Sharma et al. (1983) showed that, within Bos taurus dairy cattle breeds, the Jersey was less sensitive to thermal stress than the Holstein-Friesian. Among heat-adapted cattle, the sweating rates of Bos indicus increase exponentially with rises in body temperature, but in Bos taurus, sweating rates tend to plateau after an initial increase (Finch et al., 1982). Schmidt-Nielsen (1964) reported that as the environmental temperature rose, Bos taurus cattle showed an appreciable increase in evaporation between 15 and 20 °C, with a maximum rate of evaporation being reached before 30 °C. On the contrary, Brahman cows (Bos indicus) had initially lower evaporation rates, but rapid evaporation rates occurred when temperatures were between 25 and 30 °C, and continued rising up to 40 °C. Cattle in temperate and tropical regions possess the same type of sweat glands, one to each hair follicle (Findlay and Yang, 1950). Cattle with shorter hair, hair of greater diameter and lighter coat color are more adapted to hot environments than those with longer hair coats and darker colors (Bernabucci et al., 2010). However, tropical breeds have a higher density of hair follicles (1698/ cm² for Zebu) than is the case in Bos taurus breeds (1064/ cm² for Shorthorn) (Dowling, 1955; McManus et al., 2014). The metabolic rate is greater in Bos taurus than Bos indicus cattle even 80-85% (Vercoe, 1970). Finch (1985) showed that under high heat stress, resistance to heat transfer in Brahman cattle continued to fall as the skin temperature approached the body core temperature, whereas in Shorthorn cattle there was an abrupt increase in resistance as the temperature differential reached 2 °C. As a consequence, heat storage rose rapidly in the Shorthorn.

 

Heterosis in dairy cattle

Heterosis is the added increase in performance when animals are crossbred, and usually defined as the superiority of a first cross (F1) over and above the mean of the two parental strains (Syrstad, 1985; Kelleher et al., 2017). Also, heterosis can be estimated indirectly from many different combinations of crosses, e.g. by comparing pure bred with F1 or F1 with F2. In a study, McDowell (1982) showed different types of dairy performance traits to determine whether hybridization would produce cattle of improved adaptability and production (Table IV). Over the past few years dairy producers have shown more interest in crossbreeding programs for dairy cattle especially in warm climate regions. Often Canadian and United States dairy producers have a well standpoint about crossbred importance on this topic; they can have estimated sire genetic merit on a regional and national basis until 1995 because of the expectation that genotype x region interactions may be important to know what crossbred to choose and to use advisable in his dairy farm (Boettcher et al., 2003; Norman et al., 2005). Through classical genetic improvement tools a heat tolerant gene can be introduced into a less heat tolerant breed helping cattle to better adapt to warmer environmental temperatures. Crossbreeding programs are available for dairy cattle and it has been used as one of these strategies to improve resistance to thermal stress. The first publications on the performance of Bos taurus x Bos indicus crossbred cattle appeared more than 50 years ago (Syrstad, 1985). Diverse researches have been reported performance of crossbred dairy cows exposed to heat stress (Heins et al., 2006, 2008a, b; Khongdee et al., 2010; Boonkum et al., 2011). It is known that conventional crossbreeding between breeds of Bos taurus cattle and Bos taurus with Bos indicus cattle (F1) has been a strategy to improve resistance to thermal stress; but always lowers milk yields in the F1 generation compared to the Bos taurus purebred dairy cow. In agreement, Bohmanova et al. (2005) found bulls that transmit a high tolerance to heat stress have daughters with higher pregnancy rates and a longer productive life; but lower milk yields. In addition, although these results are the answer to choose any milk crossbred, this crossbred topic could be but complicated that it seems, something difficult to explain. Because in practical terms several studies show different results on crossbred dairy cattle, whereas others factor like location, clime and year are variables very important to consider (Table V).

 

Table IV.- Range in heterosis values for different types of dairy performance traits.

Trait	Heterosis (%)
Yields	5.0–6.6
Viability (livability)	3.7–4.6
Growth	3.2–5.7
Reproduction	0.8–5.0

Source, McDowell, (1982).

 

Body condition score in crossbred

Studies indicate that the body condition score (BCS) is greater or equal between Jersey and Holstein purebred cows (Washburn et al., 2002; Rastani et al., 2001). For this reason other studies have shown that BCS is highly difference between Holstein and Jersey x Holstein having advantage crossbred on purebred cows (Heins et al., 2008a, b; Auldist et al., 2007). This difference is related with nutrition of low quality, e.g. when the pasturing like only source of nutrition is provided. It is very important provide energy supplementation in these cases. If not, consecutively they would have BCS relatively low. Also, is true that during the first days of lactation both Holstein and Jersey x Holstein cows decreased their BCS due to in this time they mobilize body fat to cover the energy demand that the metabolism high produce during the production (Britt et al., 2003). However, the Jersey x Holstein have recovery during this critical time than Holstein cows. On the other hand, some authors have observed changes to increase the BCS even 3.5 the first 4 week of lactation in crossbred Karan Fries (Aggarwal et al., 2013). Therefore, it seems that the crossbred animals are more efficient in recovering their BCS. Transition cows with high BCS lose more body weight and body condition than thinner cows (Aggarwal et al., 2008). In other study, BCS before and after calving were different between Holstein and Norwegian x Holstein cows (Rinell and Heringstad, 2018). Finally, dairy cows under heat stress conditions, decrease appetite and nutrient availability, causing low weight, negative energy balance and reduction in BCS (Rhoads et al., 2009, 2011). In fact, it has been observed that ewes with low condition, have more difficulty to eat than animals with high condition (Verbeek et al., 2012).

 

Yield in crossbreds

Usually, the responses between crossbreds and environments different on fat (%), protein (%), and milk yield are very variables such as it indicated Table VI. Like is known the milk yield in Holstein dairy cows is very greater than others crossbred or purebred cows (Touchberry, 1992; McAllister et al., 1994). Heins et al. (2006) reported statistical differences between fat and protein yield when evaluating crossbreds different, where Holstein cows (Fat=346, Protein=305 kg) producing greater amount (P<0.05) of fat and protein than Normande x Holstein (Fat=319, Protein=277 kg), and Montbeliarde x Holstein (Fat=334, Protein=293 kg) cows. However, producing significantly the same amount (P>0.05) than Scandinavian Red x Holstein (Fat=340, Protein=297 kg) due to milk produced amount. Heins et al. (2008b) found significantly different (P<0.05), and reported 223 and 238 kg protein yield, respectively to Jersey x Holstein and Holstein. Studies have shown that Jersey x Holstein cows tended (P<0.10) to less milk yield than Holstein cows, but in the end both breed cows have the same (P>0.05) milk yield (Heins et al., 2008a). The standpoint it is well, so at

 

Table V.- Sources of study.

Reference	Average THI, TZ and BGT	Location	Crossbred and percent
Heins et al. (2006)	Both	California, USA	Nomande (50) x Holstein (50)
			Montbeliarde (50) x Holstein (50)
			Scandinavian Red (50) x Holstein (50)
Heins et al. (2008a)	TZ	Minnesota, USA	Jersey (50) x Holstein (50)
Heins et al. (2008b)	TZ	Minnesota, USA	Jersey (50) x Holstein (50)
Khongdee et al. (2010)	THI= 80.13 ± 0.45	Sakol Nakhon, Thailand	Brahaman (12.5) x Holstein (87.5)
Khongdee et al. (2006)	THI=>72	Sakol Nakhon, Thailand	Thai (12.5) x Holstein (87.5)
Boonkum et al. (2011)	THI=73 all year THI=80 April to July	Pathumthani and other provinces, Thailand	Thai (6.4-12.5) x Holstein (87.5-93.6)
Auldist et al. (2007)	TZ	Gippsland, Australia	Jersey (25,50,75) x Holstein (25,50 y 75)
Dikmen et al. (2009)	THI=>72	Florida, USA	Jersey (50) x Holstein (50)
Chaiyabutr et al. (2008)	THI=81 ± 2.9	Thailand	Red Shindi (87.5) x Holstein (12.5)
Barbosa et al. (2008)	THI=>72	Pernambuco, Brazil	Gir x Holstein (25, 50, 62.5, 62.5-inter se)
Bun et al. (2018)	THI=>80	Phnom Penh, Cambodia	Cambodian native zebu (50) × Holstein-Friesian (50)
Kamila et al. (2018)	TZ	Worgule, Poland	Normande (50) x Holstein (50)
			Norwegian Red (50) x Holstein (50)
			Danish Red (50) x Holstein (50)
			Brown Swiss (50) x Holstein (50)
			Montbeliarde cattle (50) x Holstein (50)
			Simmental(50) x Holstein (50)
De Paula Xavier de Andrade et al. (2017)	THI=maximum 80	Pernambuco, Brazil	Zebu (25) x Holstein (75)
			Zebu (12.5) x Holstein (87.5)
El-Tarabany and El-Tarabany (2015)	THI=máximum 90	Cairo, Egypt	Brown Swiss (50) x Holstein (50)
Da Costa et al. (2015)	THI=>80	Ceará, Brazil	Gyr (75) x Holstein (25)
			Gyr (50) x Holstein (50)
Santos et al. (2017)	BGT=>80	Paraiba, Brazil	Gyr (12.5) x Holstein (87.5)

THI, temperature-humidity index; TZ, thermoneutral zone; BGT, black globe temperature.

 

Table VI.- Productive variables on crossbred dairy cattle differences.

Crossbred group	n	Milk lactation number and DIM	Milk yield (kg)	Fat (%)	Protein (%)	Reference
Nomande x H	245	1, 40	27.96 ± 1.66b	3.74 ± 0.08	3.24 ± 0.05	Heins et al. (2006)
Montbeliarde x H	494		30.03 ± 1.66b	3.64 ± 0.08	3.20 ± 0.05
Scandinavian Red x H	328		30.42 ± 1.66b	3.66 ± 0.08	3.20 ± 0.05
Holstein	380		31.99 ± 1.66a	3.55 ± 0.08	3.13 ± 0.05
Jersey x Holstein	24	1, 4-150	29.25 ± 1.21*	3.83 ± 0.17	3.12 ± 0.09	Heins et al. (2008a)
Holstein	17		30.96 ± 1.21*	3.59 ± 0.17	3.08 ± 0.09
Jersey x Holstein	76	1, 305	23.43 ± 1.29a	2.74 ± 0.03	2.23 ± 0.03	Heins et al. (2008b)
Holstein	73		25.26 ± 1.29b	2.77 ± 0.03	2.38 ± 0.03
Jersey x Holstein (kg/d)	378	-	26.90 ± 2.46a	4.04 ± 0.24a	3.40 ± 0.10a	Auldist et al. (2007)
Holstein (kg/d)		-	29.10 ± 2.46b	3.70 ± 0.24b	3.26 ± 0.10b
Jersey x Holstein (kg/d)	1200	1-2, 150	15.80 ± 1.2c	-	-	Dikmen et al. (2009)
Jersey (kg/d)			16.30 ± 1.1b	-	-
Holstein (kg/d)			19.40 ± 1.0a	-	-
Brahman x Holstein (day-1)	8	2 and 3,60-70	8.38 ± 0.87	3.25 ± 0.41	3.10 ± 0.28	Khongdee et al. (2010)
Thai x Holstein (head-1 day-1)	7	2 and 3, 60-70	8.28 ± 0.12	-	-	Khongdee et al. (2006)
Thai x Holstein (test-day milk yield)	-	3, 64-230	13.8 ± 5.4	-	-	Boonkum et al. (2011)
Red Shindi x Holstein(early lactation)	18	1, 68 ± 5	12.6 ± 2.5	4.04 ± 2.08	3.32 ± 0.18	Chaiyabutr et al. (2008)
Red Shindi x Holstein (mid-lactation)		1, 125 ± 11	11.8 ± 3.2	3.38 ± 0.70	3.19 ± 0.24
Red Shindi x Holstein (late lactation)		1, 210 ± 10	7.9 ± 3.1	4.00 ± 0.77	3.45 ± 0.19
Gir x Holstein (25%)	1212	-	5.34 ± 0.46	4.08 ± 0.12	-	Barbosa et al. (2008)
Gir x Holstein (50%)		-	8.61 ± 1.16	4.45 ± 0.29	-
Gir x Holstein (62.5%)		-	7.42 ± 0.39	3.87 ± 0.10	-
Gir x inter se (62.5%)ǂ		-	5.76 ± 0.46	3.89 ± 0.12	-
Normande x Holstein	10	2, 150 ± 21	18.93 ± 4.40*	3.59 ± 0.58*	4.77 ± 0.16*	Kamila et al. (2018)
Norwegian Red x Holstein	10		25.44 ± 7.71*	3.40 ± 0.15*	3.91 ± 0.63*
Danish Red x Holstein	10		20.70 ± 6.51*	3.19 ± 0.28*	4.21 ± 0.80*
Brown Swiss x Holstein	10		23.13 ± 5.00*	3.23 ± 0.27*	4.79 ± 0.68*
Montbeliarde cattle x Holstein	10		28.00 ± 3.94*	3.02 ± 0.24*	3.61 ± 0.63*
Simmental x Holstein	10		23.63 ± 4.51*	3.22 ± 0.32*	3.91 ± 1.55*
Zebu x Holstein	8	-, 80	20	-	-	De Paula Xavier de Andrade et al. (2017)
Gyr (50) x Holstein (50)	60	1, 20-30	3937 ± 87a&	-	-	Da Costa et al. (2015)
Gyr (75) x Holstein (25)	60		4262 ± 116b&

Means with different superscripts within a row are significantly different (P < 0.05). Means with same signal within a row have showed tend (P < 0.10). ǂinter se, Holstein x Zebu; &, from September to November.

 

the end of the day Holstein cows produce greater fat and protein yield, due to produce greater milk yield. Auldist et al. (2007) found that Jersey x Holstein cows (26.90 kg) had significantly (P<0.05) less milk that Holstein (29.10 kg), but breed groups did not differ for fat or protein percent. It is very common not reported statistic differences in fat and protein percent (Heins et al., 2006, 2008a, b) between crossbred and Holstein cows. In agree a study proves that Holsteins had on average 5% higher fat and protein yields in parities 1 to 3 but Norwegian Red x Holstein had higher fat and protein percentages (Ezra et al., 2016). Also, other authors agree with these same results (Heins et al., 2008b; Bryant et al., 2007; Madgwick and Goddard, 1989; Lesmeister et al., 2000). Higher concentrations of fat and protein in milk from Jersey x Holstein cows compared with Holstein cows resulted similar daily yields of fat and protein between breed groups. This is significant to Victorian herd owners, who are paid for milk based on the quantities of fat and protein supplied, with a penalty for milk volume. Dikmen et al. (2009) reported significantly differences (P<0.05) in milk yield, and not is amazing that Holstein (19.4 kg) cows produce more milk than Jersey x Holstein (15.8 kg), and Jersey (16.3 kg) cows. However, these authors explain that differences in milk yield between genotypes were small, probably because the level of nutrition did not allow Holsteins to realize their genetic potential for milk yield. Perhaps genotype differences in thermoregulatory ability would be greater than seen here if there were greater differences in milk yield between genotypes. Heterosis has been demonstrated for several traits in dairy cattle including milk yield, fat and protein percentage of the milk, incidence of diseases and reproductive traits (Sørensen et al., 2008). Several studies used crossbred dairy milk cows under heat stress and have shown less milk yield that not reach an average of 14 kg, but fat and protein percent high produce (Khongdee et al., 2010, 2006; Boonkum et al., 2011; Chaiyabutr et al., 2008; Barbosa et al., 2008). Many studies agree, also reported low milk yield in dairy milk cows under heat stress (Table II). This suggests that heat stress impact on milk yield is accumulative regarding at time (De Boer et al., 1989; Barash et al., 2001). The declining of milk yield on crossbreds cows was found at a THI of 80 (Boonkum et al., 2011). The THI threshold of 80 is higher than the thresholds of 72 to 76 reported for US Holsteins (Ravagnolo et al., 2000; Freitas et al., 2006a, b; Aguilar et al., 2009). High environment temperature cause low efficiency of energy for milk produces (Wayman et al., 1962; Habeeb et al., 2018). Suggesting, animals under heat stress the energy costs are used mostly for heat dissipation mechanism (e.g. sweating rate), and not are used for milk produce (Chaiyabutr et al., 2008). Then, if consume rate energy decrease within mammary could be affecting the activities of epithelial cells within mammary gland. In context, the transport of glucose for utilization in the mammary gland has been noted to depend on the specific glucose transporter at the mammary cell membrane (Prosser, 1988; Madon et al., 1990; Avendaño et al., 2012), and the rate-limiting step for glucose transport at the mammary cell (Chaiyabutr et al., 2007). Barbosa et al. (2008) not reported significantly different (P>0.05) milk yield and fat percent on Gir x Holstein with 25 (5.34 kg and 4.08%), 50 (8.61kg and 4.45%), 62.5 (7.42 kg and 3.87%) Holstein blood cows, and 62.5 inter se (5.76 kg and 3.89 %) Holstein and Zebu blood cows. Genetic group with 50% Holstein had shown numerically difference greater amount of milk and fat percent as expected, the maximum heterosis occurred in this genetic group and was probably determined by non-additive genetic effects. This was true even for fat percent, which normally presents high estimates of heritability (Barbosa et al., 2008). Think suggested that in hot climates the first crossbred generation, under optimum management and feeding conditions, can be used for dairy purposes (McDowell et al., 1996). Lobo et al. (1984), working in Brazil with five generations of Pitangueira breed cows reported a significant advantage in milk yield of the F1 generation regarding milk yield of other generations, although there were no important differences between the remaining generations. Animals having on average 75% Zebu, the crossbred cows are generally less productive. Syrstad (1989) concluded that there was a reduction of approximately 24% in milk yield in inter se crossbred cows, probably as a consequence of a reduction in heterozygosity from the F1 to F2 generations due to discontinuity in the combinations of the epistatic genetic effects (Syrstad, 1989). In other words, although the crossbreds usually produces less milk than Holsteins, crossbreeding improves health and fertility (Rinell and Heringstad, 2018).

 

Conclusions

The crossbred dairy cows improve considerably body condition score, respiration rate, rectal temperature, and they own higher tolerance at heat than purebred cows. Milk yield not improves regarding Holstein cows, but fat and protein percent it is greater than Holstein cows. Apparently the crossbred in dairy cattle is the answer to improve productive and physiological responses dependent upon environment, however, does not exist crossbred in dairy cattle perfect. Crossbreeding of dairy cattle is being explored mostly for its potential to improve the fertility, health, and survival of cows, and advantages for these traits might compensate for loss in production of crossbreds compared to pure Holsteins. There have been many crossbreeding programs in dairy cattle, but when the producer choose a system crossbreeding in dairy cows always mostly contemplate only body weight, body condition score, dry matter intake, and feed efficiency. Is necessary, contemplate other traits like genetic potential, lactation (305 d), lactation number, fertility rate, and economic impact to observe clarity the potential of each crossbred in dairy cattle in the future.

According to the concepts discussed in this review, we sustain that crossbreeding in dairy cattle improves certain productive and physiological responses diminishing the effect of environmental heat stress.

 

Statement of conflict of interest

Authors have declared no conflict of interest.

 

References

Adin, G., Gelman, A., Solomon, R., Flamenbaum, I., Nikbachat, M., Yosef, E., Zenou, A., Shamay, A. Feuermann, Y., Mabjeesh, S.J. and Miron, J., 2009. Effects of cooling dry cows under heat load conditions on mammary gland enzymatic activity, intake of food and water, and performance during the dry period and after parturition. Livest. Sci., 124: 189-195. https://doi.org/10.1016/j.livsci.2009.01.014

Aguilar, I., Misztal, I. and Tsuruta, S., 2009. Genetic components of heat stress in dairy cattle with multiple lactations. J. Dairy Sci., 92: 5702-5711. https://doi.org/10.3168/jds.2008-1928

Aggarwal, A., Mani, V., Kumar, P. and Kaur, H., 2008. Antioxidant status in relation to body condition score in periparturient crossbred cows. Indian J. Anim. Nutr., 25: 231-235.

Aggarwal, A., Ashutosh, Chandra, G. and Singh, A.K., 2013. Heat shock protein 70, oxidative stress, and antioxidant status in periparturient crossbred cows supplemented with alpha-tocopherol acetate. Trop. Anim. Hlth. Prod., 45: 239-245. https://doi.org/10.1007/s11250-012-0196-z

Akyuz, A., Boyaci, S. and Çayli, A., 2010. Determination of critical period for dairy cows using temperature humidity index. J. Anim. Vet. Adv., 9: 1824-1827. https://doi.org/10.3923/javaa.2010.1824.1827

Al-Dawood, A., 2017. Towards heat stress management in small ruminants - A review. Annls. Anim. Sci., 17: 59-88. https://doi.org/10.1515/aoas-2016-0068

Al-Katanani, Y.M., Webb, D.W. and Hansen, P.J., 1999. Factors affecting seasonal variation in 90-day non-return rate to first service in lactating Holstein cows in a hot climate. J. Dairy Sci., 82: 2611-2616. https://doi.org/10.3168/jds.S0022-0302(99)75516-5

Ali, I., Tariq, M.M., Waheed, A., Yousafzai, F.A., Bokhari, F.A., Rafeeq, M., Ali, M., Attique, M.A., Amin, S. and Hameed, T., 2018. Exclusive Characteristics of the Bhag Nari cattle among the other indigenous cattle breeds of Pakistan. Pakistan J. Zool., 50:1979-1982. http://dx.doi.org/10.17582/journal.pjz/2018.50.5.sc5

Allen, J.D., Hall, L.W., Collier, R.J. and Smith, J.F., 2015. Effect of core body temperature, time of day, and climate conditions on behavioral patterns of lactating dairy cows experiencing mild to moderate heat stress. J. Dairy Sci., 98: 118-127. https://doi.org/10.3168/jds.2013-7704

Allen, T.E., 1962. Responses of Zebu, Jersey, and Zebu x Jersey crossbred heifers to rising temperature, with particular reference to sweating. Aust. J. agric. Res., 13: 165-179. https://doi.org/10.1071/AR9620165

Allen, T.E., Pan, Y.S. and Hayman, R.H., 1962. The effect of feeding on evaporative heat loss and body temperature in Zebu and Jersey heifers. Aust. J. agric. Res., 14: 580-593. https://doi.org/10.1071/AR9630580

Ammer, S., Lambertz, C., Soosten, D., Zimmer, K., Meyer, U., Dänicke, S. and Gauly, M., 2018. Impact of diet composition and temperature–humidity index on water and dry matter intake of high-yielding dairy cows. J. Anim. Physiol. Anim. Nutr., 102: 103-113. https://doi.org/10.1111/jpn.12664

Anderson, S.D., Bradford, B.J., Harner, J.P., Tucker, C.B., Choi, C.Y., Allen, J.D., Hall, L.W., Rungruang, S., Collier, R.J. and Smith, J.F., 2013. Effects of adjustable and stationary fans with misters on core body temperature and lying behavior of lactating dairy cows in a semiarid climate. J. Dairy Sci., 96: 4738-4750. https://doi.org/10.3168/jds.2012-6401

Anzures-Olvera, F., Macías-Cruz, U., Álvarez-Valenzuela, F., Correa-Calderón, A., Díaz-Molina, R., Hernández-Rivera, J. and Avendaño-Reyes, L., 2015. Efecto de época del año (verano vs. Invierno) en variables fisiológicas, producción de leche y capacidad antioxidante de vacas Holstein en una zona árida del noroeste de México. Arch. Med. Vet., 47: 15-20. https://doi.org/10.4067/S0301-732X2015000100004

Arias, R.A., Herrera, C., Larraín, R., González, F., Mader, T.L. and Velásquez, A., 2018. Physiological and behavioural response of two dairy cows genotypes during summertime in the central region of Chile. Austral. J. Vet. Sci., 50: 9-14. https://doi.org/10.4067/S0719-81322018000100103

Armstrong, D.V., 1994. Heat stress interaction with shade and cooling. J. Dairy Sci., 77: 2044-2050. https://doi.org/10.3168/jds.S0022-0302(94)77149-6

Auldist, M.J., Pyman, M.F.S., Grainger, C. and Macmillan, K.L., 2007. Comparative reproductive performance and early lactation productivity of Jersey x Holstein cows in predominantly Holstein herds in a pasture-based dairying system. J. Dairy Sci., 90: 4856-4862. https://doi.org/10.3168/jds.2006-869

Avendaño, L., Álvarez, F.D., Correa, C.A., Saucedo, Q.J.S., Robinson, P.H. and Fadel, J., 2006. Effect of cooling cows during dry period on postpartum performance under heat stress conditions. Livest. Sci., 105: 198-206. https://doi.org/10.1016/j.livsci.2006.06.009

Avendaño-Reyes, L., Álvarez-Valenzuela, F.D., Correa-Calderón, Algándar-Sandoval, A.A., Rodríguez-González, E., Pérez-Velázquez, R., Macías-Cruz, U., Díaz-Molina, R., Robinson, P.H. and Fadel, J.G., 2010. Comparison of three cooling management systems to reduce heat stress in lactating Holstein cows during hot and dry ambient conditions. Livest. Sci., 132: 48-52. https://doi.org/10.1016/j.livsci.2010.04.020

Avendaño, R.L., Hernández, R.J.A., Álvarez, V.F.D., Macías, C.U., Díaz, M.R., Correa, C.A., Robinson, P.H. and Fadel, J.G., 2012. Physiological and productive responses of multiparous lactating Holstein cows exposed to short-term cooling during severe summer conditions in an arid region of Mexico. Int. J. Biometeorol., 56: 993-999. https://doi.org/10.1007/s00484-011-0510-x

Barbosa, S.B.P., Ramalho, R.P., Monardes, H.G., Dias, F.M., dos Santos, D.C. and Batista Â.M.V., 2008. Milk and fat production of crossbred Holstein-Gyr cows (Bos taurus taurus-Bos taurus indicus) in the Agreste region of the Brazilian state of Pernambuco. Genet. Mol. Biol., 31: 468-474. https://doi.org/10.1590/S1415-47572008000300012

Barash, H., Silanikove, N. and Weller, J.I., 1996. Effect of season of birth on milk, fat, and protein production of Israeli Holsteins. J. Dairy Sci., 79: 1016-1020. https://doi.org/10.3168/jds.S0022-0302(96)76453-6

Barash, H., Silanikove, N., Shamay, A. and Ezra, E., 2001. Interrelationships among ambient temperature, day length, and milk yield in dairy cows under a Mediterranean climate. J. Dairy Sci., 84: 2314-2320. https://doi.org/10.3168/jds.S0022-0302(01)74679-6

Bauman, D.E., Peel, C.J., Steinhour, W.D., Reynolds, P.J., Tyrrell, H.F., Brown, A.C.G. and Haaland, G.L., 1988. Effect of bovine somatotropin on metabolism of lactating dairy cows: influence on rates of irreversible loss and oxidation of glucose and nonesterified fatty acids. J. Nutr., 118: 1031-1040. https://doi.org/10.1093/jn/118.8.1031

Berman, A, Folman, Y., Kalm, M., Mamen, Z., Wolfenson, D., Arieli, A. and Graver, Y., 1985. Upper critical temperatures and forced ventilation effects for high yielding dairy cows in a subtropical climate. J. Dairy Sci., 68: 1488-1498. https://doi.org/10.3168/jds.S0022-0302(85)80987-5

Berma, A., 2008. Increasing heat stress relief produced by coupled coat wetting and forced ventilation. J. Dairy Sci., 91: 4571-4578. https://doi.org/10.3168/jds.2008-1175

Bernabucci, U., Lacetera, N., Baumgard, L.H., Rhoads, R.P., Ronchi, B. and Nardone, A., 2010. Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal, 4: 1167-1183. https://doi.org/10.1017/S175173111000090X

Blazquez, N.B., Long, S.E., Mayhew, T.M., Perry, G.C., Prescott, N.J. and Wathes, C.M., 1994. Rate of discharge and morphology of sweat glands in the perineal, lumbodorsal and scrotal skin of cattle. Res. Vet. Sci., 57: 277-284. https://doi.org/10.1016/0034-5288(94)90118-X

Boettcher, P.J., Fatehi, J. and Schutz, M.M., 2003. Genotype environment interactions in conventional versus pasture-based dairies in Canada. J. Dairy Sci., 86: 383-404. https://doi.org/10.3168/jds.S0022-0302(03)73617-0

Boonkum, W., Misztal, I., Duangjinda, M., Pattarajinda, V., Tumwasorn, S. and Sanpote, J., 2011. Genetic effects of heat stress on milk yield of Thai Holstein crossbreds. J. Dairy Sci., 94: 487-492. https://doi.org/10.3168/jds.2010-3421

Bohmanova, J., Misztal, I., Tsuruta, S., Norman, H.D. and Lawlor, T.J., 2005. National genetic evaluation of milk yield for heat tolerance of United States Holsteins. Interbull Bull., 33: 160-162.

Bryant, J.R., López-Villalobos, N., Pryce, J.E., Holmes, C.W., Johnson, D.L. and Garrick, D.J., 2007. Effect of environment on the expression of breed and heterosis effects for production traits. J. Dairy Sci., 90: 1548-1553. https://doi.org/10.3168/jds.S0022-0302(07)71640-5

Britt, J.S., Thomas, R.C., Speer, N.C. and Hall, M.B., 2003. Efficiency of converting nutrient dry matter to milk in Holstein herds. J. Dairy Sci., 86: 3796-3801. https://doi.org/10.3168/jds.S0022-0302(03)73987-3

Bun, C., Watanabe, Y., Uenoyama, Y., Inoue, N., Ieda, N., Matsuda, F., Tsukamura, H., Kuwahara, M., Maeda, K.I., Ohkura, S. and Pheng, V., 2018. Evaluation of heat stress response in crossbred dairy cows under tropical climate by analysis of heart rate variability. J. Vet. Med. Sci., 80: 181-185. https://doi.org/10.1292/jvms.17-0368

Calderón, A.C., Rivera, J.A.H., Reyes, L.A., Cruz, U.M., Molina, R.D., Valenzuela, F.D.Á. and Reyna, A.G., 2012. Reproductive performance and serum concentrations of progesterone of heat-stressed holstein heifers subjected to timed artificial insemination and progesterone supplementation. Turk. J. Vet. Anim. Sci., 36: 611-617.

Chaiyabutr, N., Thammacharoen, S., Komolvanich, S. and Chanpongsang, S., 2007. Effects of long term exogenous bovine somatotropin on nutrients uptake by the mammary glands of crossbred Holstein cattle in the tropics. Asian-Aust. J. Anim. Sci., 20: 1407-1416.

Chaiyabutr, N., Chanpongsang, S. and Suadsong, S., 2008. Effects of evaporative cooling on the regulation of body water and milk production in crossbred Holstein cattle in a tropical environment. Int. J. Biometeorol., 52: 575-585. https://doi.org/10.1007/s00484-008-0151-x

Chand, N., Naz, S., Maris, H., Khan, R.U., Khan, S. and Qureshi, M.S., 2017. Effect of betaine supplementation on the performance and immune response of heat stressed broilers. Pakistan J. Zool., 49: 1857-1862. http://dx.doi.org/10.17582/journal.pjz/2017.49.5.1857.1862

Chanvijit, K., Duangjinda, M., Pattarajinda, V. and Reodecha, C., 2005. Model comparison for genetic evaluation of milk yield in crossbred Holsteins in the tropics. J. appl. Genet., 46: 387-393.

Chebel, R.C., Santos, J.E.P., Reynolds, J.P., Cerri, R.L.A., Juchem, S.O. and Overton, M., 2004. Factor affecting conception rate after artificial insemination and pregnancy loss in lactating dairy cows. Anim. Reprod. Sci., 84: 239-255. https://doi.org/10.1016/j.anireprosci.2003.12.012

Collier, R.J., Renquist, B.J. and Xiao, Y., 2017a. A 100-year review: Stress physiology including heat stress. J. Dairy Sci., 100: 10367-10380. https://doi.org/10.3168/jds.2017-13676

Collier, R.J., Xiao, Y. and Bauman, D.E., 2017b. Regulation of factors affecting milk yield. In: Nutrients in dairy and their implications on health and disease. Academic Press, ISBN: 978-0-12-809762-5, pp. 3-17. https://doi.org/10.1016/B978-0-12-809762-5.00001-2

Correa, C.A., Avendaño, R.L., Rubio, V.A., Armstrong, D.V., Smith, J.F. and DeNise, S.K., 2002. Effect of a cooling system on productivity of Holstein cows under heat stress. Agrociencia, 36: 531-539.

Da Costa, A.N., Feitosa, J.V., Montezuma, Jr. P.A., de Souza, P.T. and de Araujo, A.A., 2015. Rectal temperatures, respiratory rates, production, and reproduction performances of crossbred girolando cows under heat stress in northeastern Brazil. Int. J. Biometeorol., 59: 1647-1653. https://doi.org/10.1007/s00484-015-0971-4

Das, R., Sailo, L., Verma, N., Bharti, P., Saikia, J., Imtiwati and Kumar, R., 2016. Impact of heat stress on health and performance of dairy animals: A review. Vet. World, 9: 260-268. https://doi.org/10.14202/vetworld.2016.260-268

De Boer, J.A., Weller, J.I., Gipson, T.A. and Grossman, M., 1989. Multiple analysis of milk and fat yield curves of Israeli Holsteins. J. Dairy Sci., 72: 2143-2152. https://doi.org/10.3168/jds.S0022-0302(89)79339-5

De Paula Xavier de Andrade, R., de Andrade Ferreira, M., de Azevedo, M., da Silva, E.C., Urbano, S.A., da Conceicao, M.G. and de Lima Silva, J., 2017. Feed handling of lactating crossbred cows maintained in a semi-arid region during the hot season: Physiological parameters, ingestive behavior and performance. Anim. Sci. J., 88: 166-172. https://doi.org/10.1111/asj.12618

De Rensis, F. and Scaramuzzi, R.J., 2003. Heat stress and seasonal effects on reproduction in the dairy cow. Theriogenology, 60: 1139-1151. https://doi.org/10.1016/S0093-691X(03)00126-2

De Vries, M. and de Boer, I.J.M., 2010. Comparing environmental impacts for livestock products: A review of life cycle assessments. Livest. Sci., 128: 1-11. https://doi.org/10.1016/j.livsci.2009.11.007

Dikmen, S., Martins, L., Pontes, E. and Hansen, P.J., 2009. Genotype effects on body temperature in dairy cows under grazing conditions in a hot climate including evidence. Int. J. Biometeorol., 53: 327-331. https://doi.org/10.1007/s00484-009-0218-3

Dowling, D.F., 1955. The hair follicle and apocrine gland populations of Zebu (Bos indicus L.) and Shorthorn (Bos taurus L.) cattle skin. Aust. J. agric. Res., 6: 645-654. https://doi.org/10.1071/AR9550645

El-Tarabany, M.S. and El-Tarabany, A.A., 2015. Impact of maternal heat stress at insemination on the subsequent reproductive performance of Holstein, brown Swiss, and their crosses. Theriogenology, 84: 1523-1529. https://doi.org/10.1016/j.theriogenology.2015.07.040

Ezra, E., van Straten, M. and Weller, J., 2016. Comparison of pure holsteins to crossbred holsteins with norwegian red cattle in first and second generations. Animal, 10: 1254-1262. https://doi.org/10.1017/S1751731116000239

Fabris, T.F., Laporta, J., Corra, F.N., Torres, Y.M., Kirk, D.J., McLean, D.J., Chapman, J.D. and Dahl, G.E., 2017. Effect of nutritional immunomodulation and heat stress during the dry period on subsequent performance of cows. J. Dairy Sci., 100: 6733-6742. https://doi.org/10.3168/jds.2016-12313

Ferguson, K.A. and Dowling, D.F., 1955. The functions of cattle sweat glands. Aust. J. agric. Res., 6: 640-644. https://doi.org/10.1071/AR9550640

Findlay, J.D. and Yang, S.H., 1950. The sweat glands and Ayrshire cattle. J. agric. Sci., 40: 126-133. https://doi.org/10.1017/S0021859600045573

Finch, V.A., Bennett, I.L. and Holmes, C.R., 1982. Sweating response in cattle and its relation to rectal temperature, tolerance of the sun and metabolic rate. J. agric. Sci., 99: 479-487. https://doi.org/10.1017/S0021859600031130

Finch, V.A., 1985. Comparison of non-evaporative heat transfer in different cattle breeds. Aust. J. agric. Res., 36: 497-508. https://doi.org/10.1071/AR9850497

Flamenbaum, I., Wolfenson, D., Kunz P.L., Maman, M. and Berman, A., 1995. Interactions between body condition at calving and cooling of dairy cows during lactation in summer. J. Dairy Sci., 78: 2221-2229. https://doi.org/10.3168/jds.S0022-0302(95)76849-7

Flamenbaum, I. and Galon, N., 2010. Management of heat stress to improve fertility in dairy cows in Israel. J. Reprod. Dev., 56: S36-S41. https://doi.org/10.1262/jrd.1056S36

Folman, Y., Berman, A., Herz, Z., Kaim, M., Rosenberg, M., Mamen, M. and Gordin, S., 1979. Milk yield and fertility of high-yielding dairy cows in a subtropical climate during summer and winter. J. Dairy Res., 46: 411. https://doi.org/10.1017/S0022029900017441

Freitas, M.S., Misztal, I., Bohmanova, J. and Torres, R., 2006a. Regional differences in heat stress in U.S. Holsteins. Commun. No. 01–11, In: Proc. 8th World Congr. Genet. Appl. Livest. Prod., Belo Horizonte, Brazil. Available at: http://www.wcgalp8.org.br.

Freitas, M.S., Misztal, I., Bohmanova, J. and West, J., 2006b. Utility of on- and off-farm weather records for studies in genetics of heat tolerance. Livest. Sci., 105: 223-228. https://doi.org/10.1016/j.livsci.2006.06.011

Fuquay, J.W., 1981. Heat stress as it affects animal production. J. Anim. Sci., 52: 164-174. https://doi.org/10.2527/jas1981.521164x

Gaughan, J.B., Mader, T.L., Holt, S.M., Josey, M.J. and Rowan, K.J., 1999. Heat tolerance of boran and tuli crossbred steers. J. Anim. Sci., 77: 2398-2405. https://doi.org/10.2527/1999.7792398x

Golher, D.M., Thirumurugan, P., Patel, B.H.M., Upadhyay, V.K., Sahu, S., Gaur, G.K. and Bhoite, S.H., 2015. Effect of drinking water temperature on physiological variables of crossbred dairy cattle at high altitude temperate region of Himalayas. Vet. World, 8: 1210-1214. https://doi.org/10.14202/vetworld.2015.1210-1214

Grandl, F., Zeitz, J.O., Clauss, M., Furger, M., Kreuzer, M. and Schwarm, A., 2018. Evidence for increasing digestive and metabolic efficiency of energy utilization with age of dairy cattle as determined in two feeding regimes. Animal, 12: 515-527. https://doi.org/10.1017/S1751731117001823

Habeeb, A., Gad, A., El-Tarabany, A. and Atta, M., 2018. Negative effects of heat stress on growth and milk production of farm animals. J. Anim. Husband. Dairy Sci., 2: 1-12.

Hahn, G.L., 1999. Dynamic responses of cattle to thermal heat loads. J. Anim. Sci., 77: 10-20. https://doi.org/10.2527/1997.77suppl_210x

Hansen, P., 2004. Physiological and cellular adaptations of zebu cattle to thermal stress. Anim. Reprod. Sci., 82: 349-360. https://doi.org/10.1016/j.anireprosci.2004.04.011

Hansen, P.J., 2007. Effects of environment on bovine reproduction a 2 – youngquist, robert s. In: Current therapy in large animal theriogenology, Second edition (ed. W.R. Threlfall). W.B. Saunders, Saint Louis, pp. 431-442. https://doi.org/10.1016/B978-072169323-1.50059-3

Heins, B.J., Hansen, L.B. and Seykora, A.J., 2006. Production of pure Holsteins versus crossbreds of Holstein with Normande, Montbeliarde, and Scandinavian Red. J. Dairy Sci., 89: 2799-2804. https://doi.org/10.3168/jds.S0022-0302(06)72545-0

Heins, B.J., Hansen, L.B., Seykora, A.J., Hazel, A.R., Johnson, D.G. and Linn, J.G., 2008a. Crossbreds of Jersey x Holstein compared with pure Holsteins for body weight, body condition score, dry matter intake, and feed efficiency during the first one hundred fifty days of first lactation. J. Dairy Sci., 91: 3716-3722. https://doi.org/10.3168/jds.2008-1094

Heins, B.J., Hansen, L.B., Seykora, A.J., Johnson, D.G., Linn, J.G., Romano, J.E. and Hazel, A.R., 2008b. Crossbreds of Jersey x Holstein compared with pure Holsteins for production, fertility, and body and udder measurements during first lactation. J. Dairy Sci., 91: 1270-1278. https://doi.org/10.3168/jds.2007-0564

Her, E., Wolfenson, D., Flamenbaum, I., Folman, Y., Kaim, M. and Berman, A., 1988. Thermal, productive, and reproductive responses of high yielding cows exposed to short-term cooling in summer. J. Dairy Sci., 71: 1085-1092. https://doi.org/10.3168/jds.S0022-0302(88)79656-3

Hernández, R.J.A., Álvarez, V.F.D., Correa, C.A., Macías, C.U., Fadel, J.G., Robinson, P.H. and Avendaño, R.L., 2011. Effect of short-term cooling on physiological and productive responses of primiparous Holstein cows exposed to elevated ambient temperatures. Acta Agric. Scand. A: Anim. Sci., 61: 34-39.

Hill, W.G., Edwards, M.R., Ahmed, M.K. and Thompson, R., 1983. Heritability of milk yield and composition at different levels and variability of production. Anim. Prod., 36: 59-68.

Igono, M.O., Johnson, H.D., Steevens, B.J., Krause, G.F. and Shanklin, M.D., 1987. Physiological, productive, and economic benefits of shade, spray, and fan system versus shade for Holstein cows during summer heat. J. Dairy Sci., 70: 1069-1079. https://doi.org/10.3168/jds.S0022-0302(87)80113-3

Igono, M.O., Bjotvedt, G. and Sanford-Crane, H.T., 1992. Environmental profile and critical temperature effects on milk production of Holstein cows in desert climate. Int. J. Biometeorol., 36: 77-87. https://doi.org/10.1007/BF01208917

Johnson, H.D., 1976. World climate and milk production. Int. J. Biometeorol., 6: 171-175. https://doi.org/10.1007/BF01553975

Johnson, H.D. and Vanjonack, W.J., 1976. Effects of environmental and other stressors on blood hormone patterns in lactating animals. J. Dairy Sci., 59: 1603-1617. https://doi.org/10.3168/jds.S0022-0302(76)84413-X

Joksimović-Todorović, M., Davidović, V., Hristov, S. and Stanković, B., 2011. Effect of heat stress on milk production in dairy cows. Biotechnol. Anim. Husband., 27: 1017-1023. https://doi.org/10.2298/BAH1103017J

Jordan, E.R., 2003. Effects of heat stress on reproduction. J. Dairy Sci., 86: E104-E114. https://doi.org/10.3168/jds.S0022-0302(03)74043-0

Kadzere, C.T., Murphy, M.R., Silanikove, N. and Maltz, E., 2002. Heat stress in lactating dairy cows: A review. Livest. Prod. Sci., 77: 59-91. https://doi.org/10.1016/S0301-6226(01)00330-X

Kamal, R., Dutt, T., Patel, B., Singh, G., Chandran, P., Dey, A. and Barari, S., 2016a. Effect of shade materials on rectal temperature, respiration rate and body surface temperature of crossbred calves during rainy season. Indian J. Anim. Sci., 86: 75-81.

Kamal, R., Dutt, T., Patel, M., Dey, A., Chandran, P.C., Bharti, P.K. and Barari, S.K., 2016b. Behavioural, biochemical and hormonal responses of heat-stressed crossbred calves to different shade materials. J. appl. Anim. Res., 44: 347-354. https://doi.org/10.1080/09712119.2015.1074076

Kamila, P., Ewa, B., Marcin, G., Teresa, N.T., Beata, K., Jan, S., Arkadiusz, B., Paweł, S., Małgorzata, K.S. and Tomasz, P., 2018. Effect of dairy cow crossbreeding on selected performance traits and quality of milk in first generation crossbreds. J. Fd. Sci., 83: 229-236. https://doi.org/10.1111/1750-3841.13988

Kelleher, M.M., Berry, D.P., Kearney, J.F., McParland, S., Buckley, F. and Purfield, D.C., 2017. Inference of population structure of purebred dairy and beef cattle using high-density genotype data. Animal, 11: 15-23. https://doi.org/10.1017/S1751731116001099

Khongdee, S., Chaiyabutr, N., Hinch, G., Markvichitr, K. and Vajrabukka, C., 2006. Effects of evaporative cooling on reproductive performance and milk production of dairy cows in hot wet conditions. Int. J. Biometeorol., 50: 253-257. https://doi.org/10.1007/s00484-006-0030-2

Khongdee, S., Sripoon, S., Chousawai, S., Hinch, G., Chaiyabutr, N., Markvichitr, K. and Vajrabukka, C., 2010. The effect of modified roofing on the milk yield and reproductive performance of heat-stressed dairy cows under hot-humid conditions. Anim. Sci. J., 81: 606-611. https://doi.org/10.1111/j.1740-0929.2010.00771.x

Kibler, H.H. and Brody, S., 1952. Relative efficiency of surface evaporative, respiratory evaporative, and non-evaporative cooling in relation to heat production in Jersey, Holstein, Brown Swiss and Brahman cattle, 5 to 105°F. Univ. Missouri Agric. Exp. Stat. Bull. No. 497.

Kibler, H.H. and S. Brody, S., 1950. Effects of temperature, 50 to 105°F and 50 to 90°F on heat production and cardiorespiratory activities in Brahman, Jersey and Holstein cows. Univ. Missouri Agric. Exp. Stat. Res. Bull. No. 464.

Krishnan, G., Bagath, M., Pragna, P., Vidya, M.K., Aleena, J., Archana, P.R., Sejian, V. and Bhatta, R., 2017. Mitigation of the heat stress impact in livestock reproduction. In: Theriogenology. InTech Open, pp. 63-86. https://doi.org/10.5772/intechopen.69091

Lacetera, N., Bernabucci, U., Ronchi, B. and Nardone, A., 1996. Body condition score, metabolic status and milk production of early lactating dairy cows exposed to warm environment. Riv. Agric. Subtrop. Trop., 90: 43-55.

Lesmeister, K.E., Kellogg, A.H., Brown, Jr. A.H. Johnson, Z.B. and Lane, A.G., 2000. Effects of crossbreeding and season of calving on milk production of primiparous dairy cows. J. Dairy Sci., 83(Suppl. 1): 52.

LIC, 2007. Dairy statistics 2006/2007. Livestock Improvement Corporation (LIC), Hamilton, New Zealand.

Lobo, R.B., Duarte, F.A.M., Gonçalves, A.A.M., Oliveira, J.A. and Wilcox, C.J., 1984 Genetic and environmental effects on milk yield of Pitangueiras cattle. Anim. Prod., 39: 157-163. https://doi.org/10.1017/S0003356100041787

Lopez-Villalobos, N., Garrick, D.J., Holmes, C.W., Blair, H.T. and Spelman, R.J., 2000. Profitabilities of some mating systems for dairy herds in New Zealand. J. Dairy Sci., 83: 144-153. https://doi.org/10.3168/jds.S0022-0302(00)74865-X

Lucy, M.C., 2002. Reproductive loss in farm animals during heat stress. Proc. 15th Confer. Biometeorol. Aerobiol. University of Missouri Columbia, pp. 50-53. Available: http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.615.2662&rep=rep1&type=pdf.

McAllister, A.J., Lee, A.J., Batra, T.R., Lin, C.Y., Roy, G.L., Vesely, J.A., Wauthy, J.M. and Winter, K.A., 1994. The influence of additive and non-additive gene action on lifetime yields and profitability in dairy cattle. J. Dairy Sci., 77: 2400-2414. https://doi.org/10.3168/jds.S0022-0302(94)77183-6

McAllister, A.J., 2002. Is crossbreeding the answer to questions of dairy breed utilization? J. Dairy Sci., 85: 2352-2357. https://doi.org/10.3168/jds.S0022-0302(02)74315-4

McDaniel, B.T., Miller, R.H., Corley, E.L. and Plowman, R.D., 1967. DHIA age adjustment factors for standardizing lactations to a mature basis. Dairy Herd Improv. Lett., 43: 1-7.

McDowell, R.E., 1972. Improvement of livestock production in warm climates. W.H. Freeman and Co., San Francisco, CA, USA, pp. 771.

McDowell, R.E., 1982. Crossbreeding as a system of mating for dairy production. S. Coop. Ser. Bull. No. 259. Louisiana Agricultural Experiment Station, Baton Rouge, LA, USA.

McDowell, R.E., Wilk, J.C. and Talbott, C.W., 1996. Economic viability of crosses of Bos taurus and Bos indicus for dairying in warm climates. J. Dairy Sci., 79: 1292-1303. https://doi.org/10.3168/jds.S0022-0302(96)76484-6

McManus, C., Barcellos, J., Dias, E., Pereira, G., Moojen, F. and Menegassi, S., 2014. Heat tolerance in zebu cattle. Available: https://pdfs.semanticscholar.org/df99/db69d1dc9cc947339a7424ffd4b31563953f.pdf

McManus, C., Castanheira, M., Paiva, S.R., Louvandini, H., Fioravanti, M.C.S., Paludo, G.R., Bianchini, E. and Corrêa, P.S., 2011. Use of multivariate analyses for determining heat tolerance in Brazilian cattle. Trop. Anim. Hlth. Prod., 43: 623-630. https://doi.org/10.1007/s11250-010-9742-8

Madgwick, P.A. and Goddard, M.E., 1989. Comparison of purebred and crossbred dairy cattle for Victoria: estimation of genetic effects for yield. Aust. J. exp. Agric., 29: 1-7. https://doi.org/10.1071/EA9890001

Madon, R.J., Martin, S., Davies, A., Fawcett, H.A.C., Flint, D.J. and Baldwin, S.A., 1990 Identification and characterization of glucose transport proteins in plasma membrane and golgi vesicle-enriched fractions prepared from lactating rat mammary gland. Biochem. J., 272: 99-105. https://doi.org/10.1042/bj2720099

Nehring, R., Barton, R. and Hallahan, C., 2017. The economics and productivity of us dairy farms that use crossbred vs non-crossbred breeding technology (production systems). Agric. Finance Rev., 77: 275-294. https://doi.org/10.1108/AFR-05-2016-0053

Norman, H.D., VanRaden, P.M., Powell, R., Wright, J.R. and Verboort, W.R., 2005. Effectiveness of national and regional sire evaluations in predicting future-daughter milk yield. J. Dairy Sci., 88: 812-826. https://doi.org/10.3168/jds.S0022-0302(05)72746-6

Ortiz, X.A., Smith, J.F., Villar, F., Hall, L., Allen, J., Oddy, A., Al-Haddad, A., Lyle, P. and Collier, R.J., 2015. A comparison of 2 evaporative cooling systems on a commercial dairy farm in Saudi Arabia. J. Dairy Sci., 98: 8710-8722. https://doi.org/10.3168/jds.2015-9616

Polsky, L. and von Keyserlingk, M.A.G., 2017. Invited review: Effects of heat stress on dairy cattle welfare. J. Dairy Sci., 100: 8645-8657. https://doi.org/10.3168/jds.2017-12651

Powell, R.L., Norman, H.D. and Hutchison, J.L., 2008. Breed composition of the United States dairy cattle herd. J. Dairy Sci., 91(Suppl. 1): 7.

Prosser, C.G., 1988. Mechanism of the decrease in hexose transport by mouse mammary epithelial cell caused by fasting. Biochem. J., 249: 149-154. https://doi.org/10.1042/bj2490149

Rastani, R.R., Andrew, S.M., Zinn, S.A. and Sniffen, C.J., 2001. Body composition and estimated tissue energy balance in Jersey and Holstein cows during early lactation. J. Dairy Sci., 84: 1201-1209. https://doi.org/10.3168/jds.S0022-0302(01)74581-X

Ravagnolo, O. and Misztal, I., 2000. Genetic component of heat stress in dairy cattle, parameter estimation. J. Dairy Sci., 83: 2126-2130. https://doi.org/10.3168/jds.S0022-0302(00)75095-8

Reodecha, C., 2002. Genetic evaluation of dairy cattle in Thailand. In: Proc. 7th World Congr. Genet. Appl. Livest. Prod. Montpellier, France. Available: http://www.wcgalp.org/system/files/proceedings/2002/genetic-evaluation-dairy-cattle-thailand.pdf.

Rhoads, M., Rhoads, R., VanBaale, M., Collier, R., Sanders, S., Weber, W., Crooker, B. and Baumgard, L., 2009. Effects of heat stress and plane of nutrition on lactating Holstein cows: I. Production, metabolism, and aspects of circulating somatotropin. J. Dairy Sci., 92: 1986-1997. https://doi.org/10.3168/jds.2008-1641

Rhoads, R., La Noce, A., Wheelock, J. and Baumgard, L., 2011. Alterations in expression of gluconeogenic genes during heat stress and exogenous bovine somatotropin administration. J. Dairy Sci., 94: 1917-1921. https://doi.org/10.3168/jds.2010-3722

Rinell, E. and Heringstad, B., 2018. The effects of crossbreeding with Norwegian red dairy cattle on common postpartum diseases, fertility and body condition score. Animal, 2018: 1-8. https://doi.org/10.1017/S175173111800037X

Ronchi, B., Stradaioli, G., Verini Supplizi, A., Bernabucci, U., Lacetera, N., Accorsi, P.A., Nardone, A. and Seren, E., 2001. Influence of heat stress and feed restriction on plasma progesterone, estradiol-17β LH, FSH, prolactin and cortisol in Holstein heifers. Livst. Prod. Sci., 68: 231-241. https://doi.org/10.1016/S0301-6226(00)00232-3

Santos, S.G.C.G.D., Saraiva, E.P., Pimenta Filho, E.C., Gonzaga Neto, S., Fonsêca, V.F.C., Pinheiro, A.D.C., Almeida, M.E.V. and de Amorim, M.L.C.M., 2017. The use of simple physiological and environmental measures to estimate the latent heat transfer in crossbred Holstein cows. Int. J. Biometeorol., 61: 217-225. https://doi.org/10.1007/s00484-016-1204-1

Schmidt-Nielsen, K., 1964. Desert animals: Physiological problems of heat and water. Clarendon Press, Oxford.

Sharma, A.K., Rodriguez, L.A., Mekonnen, G., Wilcox, C.J., Bachman, K.C. and Collier, R.J., 1983. Climatological and genetic effects on milk composition and yield. J. Dairy Sci., 66: 119-126. https://doi.org/10.3168/jds.S0022-0302(83)81762-7

Silanikove, N., 1992. Effects of water scarcity and hot environment on appetite and digestion in ruminants: A review. Livest. Prod. Sci., 30: 175-194. https://doi.org/10.1016/S0301-6226(06)80009-6

Silanikove, N., 2000. Effects of heat stress on the welfare of extensively managed domestic ruminants. Livest. Prod. Sci., 67: 1-18. https://doi.org/10.1016/S0301-6226(00)00162-7

Silva, R.G.D. and Maia, A.S.C., 2011. Evaporative cooling and cutaneous surface temperature of Holstein cows in tropical conditions. Rev. Brasil. Zootec., 40: 1143-1147. https://doi.org/10.1590/S1516-35982011000500028

Sørensen, M.K., Norberg, E., Pedersen, J. and Christensen, L.G., 2008. Invited review: Crossbreeding in dairy cattle: A Danish perspective. J. Dairy Sci., 91: 4116-4128. https://doi.org/10.3168/jds.2008-1273

Speroni, M., Pirlo, G. and Lolli, S., 2006. Effect of automatic milking systems on milk yield in a hot environment. J. Dairy Sci., 89: 4687-4693. https://doi.org/10.3168/jds.S0022-0302(06)72519-X

St-Pierre, N.R., Cobanov, B. and Schnitkey, G., 2003. Economic losses from heat stress by US livestock industries. J. Dairy Sci., 86(Suppl.): E52-E77. https://doi.org/10.3168/jds.S0022-0302(03)74040-5

Syrstad, O., 1985. Heterosis in Bos taurus × Bos indicus crosses. Livest. Prod. Sci., 12: 299-307. https://doi.org/10.1016/0301-6226(85)90130-7

Syrstad, O., 1989. Dairy cattle cross-breeding in the tropics: Performance of secondary cross-bred populations. Livest. Prod. Sci., 23: 97-106. https://doi.org/10.1016/0301-6226(89)90008-0

Thatcher, W.W., Staples, C.R., Danet-Desnoyers, G., Oldick, B. and Schmitt, E.J.P., 1994. Embryo health and mortality in sheep and cattle. J. Anim. Sci., 72: 16-30. https://doi.org/10.2527/1994.72suppl_316x

Titto, C.G., Negrao, J.A., Titto, E.A., Canaes Tde, S., Titto, R.M. and Pereira, A.M., 2013. Effects of an evaporative cooling system on plasma cortisol, igf-i, and milk production in dairy cows in a tropical environment. Int. J. Biometeorol., 57: 299-306. https://doi.org/10.1007/s00484-012-0554-6

Touchberry, R.W. 1992. Crossbreeding effects in dairy cattle: The Illinois experiment, 1949 to 1969. J. Dairy Sci., 75: 640-667. https://doi.org/10.3168/jds.S0022-0302(92)77801-1

USDA, 2009. Agricultural statistics, annual. U.S. Department of Agriculture, U.S. Govt. Print. Office, Washington, DC.

Verbeek, E., Waas, J.R., Oliver, M.H., McLeay, L.M., Ferguson, D. and Matthews, L.R., 2012. Motivation to obtain a food reward of pregnant ewes in negative energy balance: Behavioural, metabolic and endocrine considerations. Horm. Behav., 62: 162-172. https://doi.org/10.1016/j.yhbeh.2012.08.007

Vercoe, J.E., 1970. The fasting metabolism of Brahman, Africander and Hereford x Shorthorn cattle. Br. J. Nutr., 24: 599-606. https://doi.org/10.1079/BJN19700061

Washburn, S.P., White, S.L., Green, Jr. J.T. and Benson, G.A., 2002. Reproduction, mastitis, and body condition of seasonally calved Holstein and Jersey cows in confinement or pasture systems. J. Dairy Sci., 85: 105-111. https://doi.org/10.3168/jds.S0022-0302(02)74058-7

Wayman, O., Johnson, H.D., Merilan, C.P. and Berry, I.L., 1962. Effect of ad libitum or force-feeding of two rations on lactating dairy cows subject to temperature stress. J. Dairy Sci., 45: 1472-1478. https://doi.org/10.3168/jds.S0022-0302(62)89658-1

West, J.W., Hill, G.M., Fernandez, J.M., Mandebvu, P. and Mullinix, B.G., 1999. Effects of dietary fiber on intake, milk yield, and digestion by lactating dairy cows during cool or hot, humid weather. J. Dairy Sci., 82: 2455-2465. https://doi.org/10.3168/jds.S0022-0302(99)75497-4

West, J.W., 1999. Nutritional strategies for managing the heat-stressed dairy cow. J. Anim. Sci., 77(Suppl. 2): 21-35. https://doi.org/10.2527/1997.77suppl_221x

West, J.W., 2003. Effects of heat stress on production in dairy cattle. J. Dairy Sci., 86: 2131-2144. https://doi.org/10.3168/jds.S0022-0302(03)73803-X