The number of Gyr cows and their crossbreeding has been growing among Brazilian farmers (Embrapa, 2018, 2021), which makes this breed an important genetic resource for milk production in tropical regions (Santana et al., Reference Santana, Pereira, Bignardi, El Faro, Tonhati and Albuquerque2014). Several attributes contribute to its adaptation to production systems in different regions of the country. The genetic selection of Gyr for milk yield has improved the morphology of the mammary gland (eg reduction in thickness and length of teats) and has resulted in easier to milk docile cows (Fernandes et al., Reference Fernandes, El Faro, Filho Vercesi, Machado, Barbero, Bittar and Igarasi2019). However, there are still issues that must be explored for a better understanding of the dairy Gyr breed, to make it more competitive and sustainable.
Climate change is causing a global increase in average air temperature and reduced rainfall, putting the sustainability of the livestock production system at risk (Thornton et al., Reference Thornton, Nelson, Mayberry and Herrero2022), especially in countries such as Brazil, where air temperature averages are above the comfort threshold for dairy cattle, and pasture systems are dependent on the rainy season. Benavides et al. (Reference Benavides, Vélez Terranova, Perilla Duque, Campos Gaona and Sánchez Guerrero2022) found a significant association between climatic variables, bulk tank milk volume and milk composition in tropical pasture-based dairy systems. Even breeds adapted to tropical climates (e.g. Gyr cows) could suffer the effects of heat stress (Cardoso et al., Reference Cardoso, Peripolli, Amador, Brandão, Esteves, Sousa, França, Gonçalves, Barbosa, Montalvão, Martins, Fonseca Neto and McManus2015) resulting in changes in production and quality of milk.
As well as the thermal environment, dairy cows face other challenges, such as the transition period, when cows enter a postpartum negative energy balance. This is arguably more challenging for primiparous than multiparous cows, as primiparous cows should allocate a portion of their nutritional intake to their own growth and to milk production (Mekuriaw, Reference Mekuriaw2023). Therefore, primiparous cows need special attention as they need to recover their body condition as soon as possible.
Often, dairy farmers are not sufficiently concerned with body weight and body condition score at calving and during the lactation. When farmers do take note of these traits it is possible to determine the best diet and increase the odds of a cow being healthy, have good levels of milk yield, and reproductive success (Barletta et al., Reference Barletta, Maturana Filho, Carvalho, Del Valle, Netto, Rennó, Mingoti, Gandra, Mourão, Fricke, Sartori, Madureira and Wiltbank2017). Considering the importance of the Gyr breed for tropical pasture-based systems, our exploratory study set out to evaluate the changes in body characteristics, milk yield, and milk constituents during first lactation, and then to evaluate the relationship between thermal environment and milk yield and constituents of milk of first lactation in dairy Gyr cows managed on pasture.
Materials and methods
This study was approved by the Ethics Committee on Animal Use of the ‘Instituto de Zootecnia’ of São Paulo state under protocol number 230-16, and it was performed in accordance with the ethics of animal experimentation.
Study area and climate pattern
This study was carried from August 2013 to July 2015 at the Brazilian Association of Dairy Gyr Breeders (acronym in Portuguese: ABCGIL), Uberaba, Minas Gerais state, Southeast of Brazil (19°44′54′′ S, 47°55′55′′W). The climate of the region is characterized as subtropical (CWa) with warm and rainy summers and relatively dry winters according to the Köppen's classification (Alvares et al., Reference Alvares, Stape, Sentelhas, Gonçalves and Sparovek2013). The local microclimatic data (air temperature, relative humidity, dew point and precipitation) by hour was obtained from The National Aeronautics and Space Administration Prediction of Worldwide Energy Resources (NASA POWER) and used to determine the temperature humidity index (THI; online Supplementary Equation 1) developed by Thom (Reference Thom1959). Overall, during the dry season, the average air temperature was 23 °C, range from 19.5 to 27.8 °C while the average air temperature during rainy season was 25 °C, range from 23.8 to 27.8 °C (details are shown in online Supplementary Table S1).
Animals and management
A total of forty-five primiparous dairy Gyr cows (average age of 35.4 ± 5.3 months, range: 27–48 months) participated in this study from prepartum to 10 months of lactation (details are shown in the online Supplementary File). During the prepartum period, approximately 60 d before the expected day of calving, the primiparous cows were kept in a maternity paddock close to the milking parlor and received sorghum silage and concentrate (2 kg/cow/day) at the feeder. After calving, the primiparous cows were kept in an area of 7 ha, divided into 12 paddocks (0.6 ha) with Brachiaria brizantha cv xaraes grass. The pasture was managed by the rotational stocking method to provide three days of occupation and approximately 33 d of rest. Due to forage scarcity during the dry season (August to September), the diet of cows was supplemented with corn silage. Also, the cows received 6 kg of concentrate per day until the 35th day of lactation. After this period, the concentrate was supplied at a proportion of 1 kg per 3 l of milk produced above 10 l, during the milking. The primiparous cows were milked twice a day using a mechanical milking machine (EuroLatte 330/450 l, 50 kPa) with the presence of their calves. Until 90 d old, the calves were allowed to suckle on one teat of their dams before milking to stimulate milk ejection, and after milking to suckle the residual milk (standard management for Zebu dairy cows). After 90 d old, the calves only drank the residual milk from their mothers.
Measurement
Body weight, body condition score (BCS), subcutaneous fat thickness, milk production and milk composition were recorded monthly, from prepartum, approximately 60 d before the expected day to calving (except milk related traits), to 10 months of lactation. All these data were categorized in month of lactation (1 to 10) and grouped by lactation stage (1st stage: 1–100 d; 2nd stage: 101–200 d; and 3rd: 201–305 d). Samples for milk progesterone concentration were collected once a week from the 7th to 135th days after calving, and the data were grouped by month (1 to 5).
Body measurements
To evaluate body weight, cows were weighed using an automatic balance. BCS was evaluated as described in the online Supplementary File assigning a score range from 1 to 9 according to Ferreira et al. (Reference Ferreira, Lopes, Azevedo and Ledic2005).
Subcutaneous fat thickness
To assess subcutaneous fat thickness five ultrasound images (online Supplementary File Fig. S1) were taken using a Pie Medical Equipment B.V. (1996) and processed by the Echo Image Viewer 1.0 program. In this study, we only used the data of subcutaneous fat thickness from pelvic region (EGS2), as this region has high correlation with BCS before calving and during lactation (Miranda et al., Reference Miranda, Paz, Do Bem, Barbosa, Mercadante, Vercesi Filho, Rabelo Fernandes and El Faro2022).
Milk sampling
Individual milk yield was measured monthly and milk samples were collected for the analysis of milk components (fat percentage – F%, protein percentage – P%, lactose percentage – L%, and total solids percentage – TS%). During the dairy control performed monthly by the Brazilian Association of Zebu Breeders, milk samples were collected at the morning milking (7 a.m.) throughout lactation in a collection bottle. On the day of dairy control, the calves did not suckle their mothers and the milk production was measured from the four quarters. After milk collection, the sample was homogenized for 15 s, or until the preservative (bronopol tablet) dissolved completely. Milk components were measured by near-infrared spectroscopy (Bentley Instruments, Inc., Chaska, MN, USA). For this, the samples were identified with the cow ID and were placed in an isothermal box with recyclable ice and sent to the laboratory ‘Clínica do Leite’ at the ‘Universidade de São Paulo – ESALQ’ in Piracicaba – SP.
For the determination of progesterone concentrations in milk, individual samples were collected from the cows in Eppendorff® collection tubes (2.5 ml). The samples were collected once a week, from the 7th to 135th days after calving, totaling 20 weeks and 400 milk samples. The samples were sent to the laboratory ‘Fisiologia da Lactação da Faculdade de Zootecnia e Engenharia de Alimentos’ at the ‘Universidade de São Paulo da USP’, in Pirassununga – SP and were analyzed through kits (Progesterone Accubind Elisa Kit). The start of ovarian cycles was defined as the time when progesterone concentration exceeded the threshold of 3 ng/ml (Bulman and Lamming, Reference Bulman and Lamming1978).
Statistical analysis
All analyses (influence, descriptive (average, standard deviation, coefficient of variation, minimum and maximum), correlation and confirmatory) were performed in R (version 4.2.2) language through the software RStudio (R Core Team, 2022). The database was built with 3200 data composed of each measurement. The data of body weight, body condition score, subcutaneous fat thickness, milk yield, and milk constituents were categorized by month of lactation (1–10) and grouped into lactation stage (1st stage: 1–100 d; 2nd stage: 101–200 d; and 3rd: 201–305 d). As this is an exploratory study, first we evaluated the influence of the lactation stage on the variables of interest, and second, we performed a deep analysis within the months of lactation (1–10) to obtain more information. All data were analyzed using Generalized Linear Models (GLM) at a 95% confidence level. We used the average values ± standard deviation (sd), and range variation for the descriptive results presentation. For interpretation purposes, we used the model estimate, that represents the odds of a given event occurring in relation to the reference category and the distribution of predicted values and standard error of the milk yield, and the percentage of constituents were plotted in graphics. All details of each statistical model performed are shown in the online Supplementary File.
Results
Descriptive results of thermal environment
Overall, in the dry season the average THI was 69.2 ± 5.5 (range: 50.9–86.1) and in the rainy season the average THI was 73.5 ± 3.7 (range: 64.7–84.7). During the study period, there were hours of the day of thermal challenge for the primiparous Gyr cows (online Supplementary File Fig. S2). In all evaluated months, there were hours (30%) of the day in which values of THI was in the alert category (75–83). Emergency THI occurred in October 2014 (six consecutive days), and in January 2015 (two consecutive days), with values ranging from 84 to 86.
Descriptive results of body measurements
Overall, during the prepartum period (range: −60 to 0 d), the cows showed on average (± sd) body weight of 461.1 ± 55.5 kg (range: 343–582 kg), and BCS 6.2 ± 1.15 (range: 4–9), and subcutaneous fat of 11 ± 3.98 mm (range: 3.3–19.5 mm). During prepartum, no cows showed BCS between 1 and 3, while 50% of cows showed BCS between 4 and 6, and 50% of cows showed BCS between 7 and 9.
After calving, body measurements varied in relation to the lactation stages: body weight (1st: 418 ± 55.9 kg; 2nd: 408 ± 50.5 kg; 3rd: 435 ± 54.8 kg), subcutaneous fat thickness (1st: 7.7 ± 3.6 mm; 2nd: 4.1 ± 2.2 mm; 3rd: 4.3 ± 2.6 mm), and body condition score (1st: 5.2 ± 1.1; 2nd: 4.6 ± 1.2; 3rd: 4.5 ± 1.1). The cows lost body weight throughout the lactation; at the first stage of lactation, 81% of the cows lost body weight, while 61% of the cows lost weight by the second stage of lactation and 56% of cows lost weight during the third stage (day 201–305).
Overview of statistical model results for body measurements
There was an influence (P < 0.05) of the months of lactation on body weight and pelvic fat thickness (Fig. 1). The cows were likely to lose body weight (~5% per month; P < 0.05) up to the 6th month of lactation. Between the 8th and 10th month of lactation, the cows were likely to gain body weight (~7% per month; P < 0.05). Cows were likely to lose ~40% of subcutaneous fat in each month of lactation, concerning the first month of lactation.
Figure 1. Predicted average values for the body weight (gray solid line) and subcutaneous fat thickness (black dashed line) for all cows in each month of lactation. *Statistic influence (P < 0.05) of months of lactation in relation to the reference category (1st month) based on GLM model; NS, not significant.
Descriptive results of yield and constituents of milk
Overall, the average (± sd) milk production on 1st stage of lactation was 11.1 ± 2.6 kg (range: 3.5–15.5 kg), on 2nd stage was 10.9 ± 1.9 kg (range: 3.6–14.0 kg) and on 3rd stage was 8.1 ± 1.2 kg (range: 4.9–10.2 kg). In general, the cows lost (P < 0.05) body condition throughout lactation, while a significant decrease on milk production occurred after the seventh month of lactation (Fig. 2).
Figure 2. Predicted average values for the milk production (black dotted line) and body condition score (BCS, gray solid line) for all cows in each month of lactation. Statistic influence (P < 0.05, * = milk (kg); † = BCS) of months of lactation in relation to the reference category (1st month) based on GLM models; NS, not significant.
Overview of statistical model results of yield and constituents of milk
The details from the multilevel regression models built to determine the relationship between the lactation stage, milk production and milk constituents are shown in Table 1. As the months in lactation progressed there was a decrease (P < 0.001) in milk yield and milk lactose, but an increase (P < 0.05) in milk fat, milk protein, and milk solids (online Supplementary File Fig. S3). There was no difference (P > 0.05) in total milk yield of cows from low (11.5 ± 2.8, range: 2.2–16.6 kg), medium (9.9 ± 3.3, range: 3.3–15.2 kg), and high (10.6 ± 2.9, range: 1.7–17 kg) weight loss categories. There was a correlation (P < 0.05) between THI of the two days before milk collection, milk yield (r 2 = 0.41), and constituents of milk (lactose, r 2 = 0.43; total solids, r 2 = −0.27; fat, r 2 = −0.31; protein, r 2 = −0.32).
Table 1. Posterior estimates of the regression models with the Gamma distribution, logarithmic link function, and 95% of confidence intervals (CI) built to determine the relationship between the lactation stage (first: 1–100 d, second: 101–200 d, and third: 201–305 d), milk production, and milk constituents (% of solid, lactose, fat) of dairy Gyr cows
Model estimative represents the odds of a given event occurring in relation to the reference category.
Descriptive results of milk progesterone
Most cows presented low values of P4 (<3 ng/ml) until the fourth month of lactation (1st: 82%; 2nd: 52%; 3rd: 48%; 4th: 53%) while in the fifth month of lactation, most cows (52%) presented values higher than 4 ng/ml (online Supplementary File Fig. S4).
Discussion
Body characteristics, yield and constituents of milk were influenced by the lactation stage of the primiparous dairy Gyr cows evaluated in this exploratory study. After calving, the cows of this study lost body weight, body condition score and subcutaneous fat. This is a regular physiological process in many mammals, therefore, all cows should be expected to mobilize body fat in early lactation (NRC, 2001) to support milk production (Lee et al., Reference Lee, Cho, Park, Choi and Kim2016). Our finding indicated that BCS is affected by lactation stage, as the recovery of BCS starts when the milk production decreases at the third lactation stage. Furthermore, as the months in lactation progressed an increased ovarian activity was observed. At 30 d postpartum only 13% of cows showed ovarian activity (P4 > 3 ng/ml). This low percentage was expected due to the presence of calves during milking, and indeed most cows (52%) showed ovarian activity at the 5th month of lactation. It is already known that the tardiness on the onset of ovarian activity, occurs mainly when the offspring is present (Sinclair et al., Reference Sinclair, Molle, Revilla, Roche, Quintans, Marongiu, Sanz, Mackey and Diskin2002).
An interesting result was the positive correlation between the average THI of two days before milk collection with milk yield. This can be explained by the fact that the cows did not experience intense heat stress during the study period, combined with the lower metabolic heat generation in primiparous cows due to lower milk production (Bernabucci et al., Reference Bernabucci, Biffani, Buggiotti, Vitali, Lacetera and Nardone2014). When comparing primiparous to multiparous Holstein cows, Bernabucci et al. (Reference Bernabucci, Biffani, Buggiotti, Vitali, Lacetera and Nardone2014) found that the primiparous had the least metabolic heat generation and the largest surface area, which makes them more resistant to heat stress for milk yield than multiparous ones. Many authors have reported that heat stress negatively affects milk yield (Tao et al., Reference Tao, Orellana Rivas, Marins, Chen, Gao and Bernard2020). It is known that milk yield of high-producing dairy cows will reduce when the minimum THI of a day exceeds 65 units (Zimbelman et al., Reference Zimbelman, Rhoads, Rhoads, Duff, Baumgard and Collier2009). In this study, we used the value of 74 of THI as a threshold to determine the thermal comfort (Reis et al., Reference Reis, Ferreira, Mazocco, Souza, Pinho, Neto, Malaquias, Macena, Muller, Martins, Balbino and McManus2021), due to the cows̀ features (primiparous Zebu) of this study, and we did not find an effect of THI on milk yield.
The cows in this study showed a lactation peak in the third month, then maintained their milk yield until the 6th month and reduced from the 7th month onwards. Chaudhari et al. (Reference Chaudhari, Kapadiya, Gadariya, Gamit and Savaliya2022) evaluating Gyr cows of different parity found that milk production persisted above 90% until 7th month postpartum. Lactation persistency must be considered in dairy Gyr cows because they usually have shorter lactations and lower persistency of milk production compared with Holstein cows (Costa et al., Reference Costa, de Melo, Machado, Freitas, Packer and Cobuci2005). However, within and between dairy breeds there are variations in peak and persistency of milk yield, partially explained by dietary composition and feeding management (Caccamo et al., Reference Caccamo, Veerkamp, Licitra, Petriglieri, La Terra, Pozzebon and Ferguson2012). Cows of this study calved during the dry season, which is also a period of low quantity and quality of pasture. Because of this, the cows received corn silage and concentrate during the dry season. We need to highlight that we evaluated primiparous cows which, even with supplementation, required high levels of energy for body growth. During the whole lactation period of dairy cows, the energy partitioning between milk production and body tissue deposition may vary. In the peak lactation period, more energy is partitioned to milk yield. However, in the late lactation relatively more energy is deposited in body tissue (Zhang et al., Reference Zhang, Gasser, Yang, Yin, Zhao, Bao, Pan, Huang, Wang, Zou, Zhou, Zhao, Fang and Hu2016). We observed this fact in our study; BCS increased as milk yield decreased.
All values of milk constituents found in this study were within the standard of Brazilian regulation (Brasil, 2011), in which the minimum requirements for milk constituents are 2.9% of protein, 3% of fat and 8.4% of non-fat solids. This demonstrates that milk from Gyr cows can be competitive in quality in tropical climate regions (as in this study). The presence of Zebu genetics in tropical regions is important for the sustainability of livestock. Even Zebu breeds, which are more adapted to hot regions than Bos taurus breeds, can suffer the negative impacts of climate seasonality. As shown in our results, the milk constituents, except the lactose and milk yield, were negatively correlated with the average THI two days before milk collection. Previous studies also reported the negative effects of THI on milk constituents. Studies of Maggiolino et al. (Reference Maggiolino, Dahl, Bartolomeo, Bernabucci, Vitali, Serio, Cassandro, Centoducati, Santus and De Palo2020) on primiparous Brown Swiss cows showed that as THI rises, cows tend to produce the same volume of milk, but with lower fat and protein content. Bernabucci et al. (Reference Bernabucci, Basiricò, Morera, Dipasquale, Vitali, Piccioli Cappelli and Calamari2015) reported that the main milk components (e.g. fat, protein, total solids, and solids-not-fat), are lowest during the summer.
In conclusion, there was in general an influence of the lactation stage of the primiparous dairy Gyr on body characteristics, milk yield, and milk constituents, and the environmental factors did not negatively influence milk production. These results confirm the potential of Gyr cows for tropical regions. Also, our findings suggest that body condition score variation of primiparous Gyr cows may be more related to body development than the amount of milk produced. Due to climate change, advancing knowledge of Zebu breeds, such as dairy Gyr cows, will be necessary for the adaptation of tropical farms to the scenario of global warming. Thus, our results can help future research in the advancement of knowledge about lactation of the Gyr cows, but new studies that evaluate the productive and reproductive capacity are necessary to spread the use of dairy Gyr cows in tropical regions.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0022029924000189
Acknowledgements
We acknowledge all staffs from the Brazilian Association of Dairy Gyr Cattle Breeders (ABCGIL) for helping in the data acquisition and providing all necessary information to perform this study. We thank the São Paulo Research Foundation (FAPESP- https://fapesp.br/en; grants 2013/17.867-7, 2017/50.339-5, and 2022/12148-1) for the financial support to perform data collection, and CNPq and Capes for the scholarships granted.
