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Articles

Improvements in the behaviour of Gir dairy cows after training with brushing

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Pages 184-191 | Received 25 Sep 2018, Accepted 02 Apr 2020, Published online: 29 Apr 2020

ABSTRACT

The cow’s behaviour and temperament influence handling and productivity. Training including tactile stimuli can improve zebu cow behaviour. The aim of the study was to utilize tactile stimulation training in Gir dairy cows during 14 days and measure cow behaviour. A total of 27 cows were brushed in a squeeze chute. Behavioural parameters, respiratory rate (RR) and rectal temperature (RT) were evaluated. The temperature and humidity of the environment was recorded to calculate the temperature and humidity index (THI). The THI demonstrated that the environmental conditions did not induce thermal stress. All behavioural variables showed improvements with training over time. The ‘calm’ score increased throughout the training, corroborating the movement and displacement behavioural characteristics, regardless of the parturition order. Initially, 56.6% of the cows walked to exit a chute while others trotted or ran, and, at the end of the days of training, 96.0% of the cows exited the chute by walking. A decrease in the RT and RR was verified between the first to 7th and 14th day of training. Brushing training was effective in calming the animals and improving the interaction with humans, thereby enhancing the human animal relationship.

Introduction

Attention to animal welfare in production systems meets a demand from consumers. Knowledge of animal behaviour allows producers to identify behavioural deviations and customize systems to minimize discomfort, consequently increasing the productivity of the production system, in addition to meeting animal needs (Coelho and Franzoni Citation2012). In livestock farms with low levels of production, if investments are made in productivity improvements, increments in animal well-being take place. This outcome is due to the generalized relationship between increased production and welfare, which generates enhancements in nutrition, disease control, and the farm’s facilities (McInerney Citation2004).

Management information concerning man-animal welfare or interactions with zebu (Bos indicus) or zebu-like animals is limited in the literature. These breeds are very common in tropical countries, are managed predominantly in a pasture production system and have limited human-animal interaction, except at calving, vaccination, and weighing. These conditions generate a withdrawn animal that are more difficult to handle. Consequently, these animals are more reactive and temperamental compared with taurine animals (Burrow Citation2001; Grandin and Shivley Citation2015). Cattle with high reactivity or low docility are undesirable in a livestock farm. These animals are generally culled due to difficulty in handling, especially in dairy production systems where handlers have more direct and regular contact with animals (Kenttämies et al. Citation2006) and these animals display characteristics which can be dangerous and stressful to the animal itself and to its cohorts, as well as the human handlers.

In order to improve the relationship between human beings and cattle in the day-to-day routine of the farm, changes in market conditions or substantial investments are not required. Selection of animal handlers provides an important opportunity to improve animal welfare and productivity (Fraser et al. Citation2013). To do so, farmers only need to better understand the behaviour of the reared animals, adapting the management system and installations to the animals’ characteristics.

Cattle that have had little contact with handling, show both behavioural and physiological stress responses to handler. The perception of different senses may be involved in human–animals relationship (Waiblinger et al. Citation2006) so we could use different strategies to improve this negative response. Techniques such as gentle stroking (Lensink et al. Citation2000; Lürzel et al. Citation2016), brushing (Silva et al. Citation2017), touching (Probst et al. Citation2012), talking (Lürzel et al. Citation2016) and positive human presence (Boivin et al. Citation2000) may reduce the fear of humans and consequently avoidance distance. Thus, could reduce stress in future life (Boivin and Braastad Citation1996; Grandin Citation1997).

Therefore, we can see that tactile stimulation has been perceived as a critical management tool to improve the human-animal relationship, reducing levels of fear, favouring the establishment of animal-human bonds. And knowing the difficulty of zebuine cattle handling because of its temperament and pasture production system, the present study hypothesized that tactile stimulation in the pre-partum period entails positive benefits to animal behaviour, rendering them more relaxed and confident regarding the handler and the facilities. Therefore, the objective of this assessment was to evaluate the behavioural improvement of the animals during training with tactile stimulation through brushing.

Material and methods

Gestating purebred Gir dairy cows were evaluated at the Getúlio Vargas Experimental Field of the Minas Gerais Agricultural Research Company, in the city of Uberaba (Minas Gerais, Brazil). The location is situated at the following coordinates: Latitude 19° 44′ 545″ S, Longitude 47° 55′ 55″ W; and at an altitude of 801 m. According to the Köppen classification, the area is of *CWa subtropical climate, with hot and rainy summers and relatively dry winters.

The experiment was conducted using a total of 27 animals, comprised of 7 nulliparous, 7 primiparous, and 13 multiparous (2–4 births) females. The entire sample underwent tactile stimulation training (brushing) for 14 consecutive days (5 min/animal), which was carried out in the corral, in a squeeze chute, at 7 and 11 am The females were groomed with a brush, with and without a handle, over the entire body (head, neck, trunk, udder, front limbs, and hind limbs). Brushing was performed mainly in the udder and hindlimb regions as performed by Sutherland and Huddart (Citation2012) in their study with primiparous dairy cows, given they comprise the areas that undergo greater contact during milking. The squeeze chute was chosen as the handling facility to brush the animals for handler and animal’s safety, therefore none of the body parts were restrained.

The animals were evaluated continuously by the same people who did the brushing during 14 days of management regarding behaviour and physiological parameters. The analyzed behavioural parameters consisted of vocalization (adapted from Calviello et al. (Citation2016)), sonorization with a threatened tone (snorting), rumination, movement (adapted from Sant’Anna and Paranhos da Costa (Citation2013)), displacement, ear movement (adapted from Calviello et al. (Citation2016)), and scores regarding entrance and exit speeds in and out of the squeeze chute (adapted from Lanier and Grandin (Citation2002)). The scores were attributed to the animals as described in .

Table 1. Description of the behavioral variables and their respective scores during training with brushing.

In addition to the behavioural assessment during training, physiological indicators of animal welfare were also collected by way of the following parameters: respiratory rate (RR), determined by flank breathing movements at the beginning of each training activity, for 15 s, multiplied by four to obtain the respiratory rate per minute; and rectal temperature (RT), measured using a conventional thermometer.

During the experiment, at the time of animal handling, the ambient temperature and the values regarding relative humidity (RH) were recorded to calculate the temperature and humidity index (THI), also known as the thermal comfort index, using the formula described by Thom (Citation1959): THI={0.8×T+(%RH/100)x(T14.4)+46.4}, here: T = temperature (°C) and %RH = relative humidity in percentage. The temperature and humidity were obtained through a datalogger (AK174, AKSO®) since the animals’ arrival in the chute until the end of training when the animals were released to its pasture. The information was recorded every 10 min.

The data were initially analyzed by descriptive statistics (means, and frequencies), using the FREQ and MEANS procedures of the SAS software (SAS Institute, INC., Cary, NC). Concerning the behavioural parameters evaluated during training, the % of the animals that represented each score in each evaluated parameter on different days of training, classified as 1 (first day of brushing), 7 (seventh day of brushing), and 14 (14th day of brushing) were considered.

The analysis of variances for the behavioural traits were performed using generalized linear models using the GENMOD procedure (SAS Institute, INC., Cary, NC) and the effects included in the models comprised the classificatory effects of order of parturition (1 – nulliparous and 2 – primiparous and multiparous), the day of training (1, 7, and 14), and the effect of the cow as a repeated measure. The data distribution assumed in the analyses was determined based on Akaike information criteria (QIC and QICu), selecting the distribution that retained the lowest value for these parameters. The tested distributions were the gamma, Poisson, multinomial, binomial, and binomial negative.

Respiratory rate (RR) and rectal temperature (RT), were analyzed by mixed linear models using the MIXED procedure (SAS Institute, INC., Cary, NC) and the effects included in the models comprised the classificatory effects of order of parturition (1 – nulliparous and 2 – primiparous and multiparous), the day of training (1, 7, and 14), and the effect of the cow as a repeated measure. Initially, the THI threshold was based on crossbreeding (Bos taurus taurus x Bos taurus indicus) results of De Azevedo et al. (Citation2005). They found that THI ≤ 80 did not cause heat stress in F1 Holstein-Zebu dairy cows in the tropics. THI calculation during our experiment ranged from 52.65–78.38 and in this case, this effect was not included in the model for RR an RT. A correlation was made between respiratory rate and rectal temperature using CORR procedure (SAS Institute, INC., Cary, NC).

Results

Analyses of variance were performed on the behavioural traits taking into consideration the effect of the day of training and the order of parturition in the model (). A low frequency of vocalization, rumination, and snorting behaviour was reported. When the vocalization was performed, its purpose was communication, especially when another lot of the herd was being handled nearby. The results regarding rumination and snorting frequency happened sporadically, increasing and decreasing, throughout the training. Thus, due to the low score variation, it was unfeasible to conduct statistical analyses.

Table 2. Analysis of variance of the behavioral variables evaluated during the brushing training of Gir dairy cows. The effects of training day and order of parturition was included in the model.

The effect of the parturition order was not significant (P ≥ 0.05) for the evaluated behavioural parameters. On the other hand, the effect of the day of training was significant (P < 0.05) for all the behavioural traits analyzed (). On the seventh day, a positive effect was observed for all the behaviours when compared with the beginning of training. The same occurred when comparing the beginning (Day 1) and the end (Day 14) of training (P < 0.05). Considering the parameters measured during brushing (MOV, DISP, and EAR), it was also observed improvements when comparing the 7th and 14th days of training (P < 0.05), not only days 1 × 7 (P ≤ 0.01) and 1 × 14 (P < 0.01).

The observed behavioural percentages during tactile stimulus training on the 1st, 7th, and 14th days are shown in , illustrating the results of analysis of variance for these traits. A positive effect was noted on behaviour of the animals regarding the brushing stimulation. It was possible to see the improvement in the animal entrance over the days. At the moment of entry into the chute ((a)), on the first day of brushing, 64.2% of the animals entered walking and 35.85% came in running or trotting. On the seventh day and during the training period, a positive and continuous behavioural progression was noted, such that on the last day of observation (day 14), all the animals entered the chute walking. Throughout the observation period, some animals halted at the time of chute entry (stopped in the entrance, measured by 3 scores), either due to fear or because they were calm ((b)). However, a reduction of 52.8% on the first day to 26.0% on the last day of training was observed in animals that halted out of fear. The type of command employed to encourage the animal to enter the chute (HELP) was measured using five scores ((c)) and, even with brushing, it was not possible to rule out the use of stick to prod the animals with (scores 4 and 5). Nonetheless, the need to poke the animal with some object to assist in entering the chute decreased from 41.5% (first day) to 24.5% (seventh day) and 16.0% (last day). As of days 7 and 14, scores 1 and 2 predominated, i.e. animals entering without physical command methods (entry without stimulus or voice command) increased from 54.7% to 74.0%, when comparing the first with the last day of observation.

Figure 1. Behavioral percentages observed during training, on the 1st, 7th, and 14th days of training using tactile stimulus through brushing of Gir dairy cows: the entrance speed (a), if the animal halted at the entrance (b), if it received help to enter (c), animal movement (d), animal displacement (e), ear movement (f), and exit speed (g).

Figure 1. Behavioral percentages observed during training, on the 1st, 7th, and 14th days of training using tactile stimulus through brushing of Gir dairy cows: the entrance speed (a), if the animal halted at the entrance (b), if it received help to enter (c), animal movement (d), animal displacement (e), ear movement (f), and exit speed (g).

The behavioural parameters of movement (MOV), displacement (DISP), and ear movement (EAR) of the animal during brushing displayed positive evolution during the training performed in the chute ((d–f)), demonstrated by analysis of variance () as well. A gradual increase in score 1 (calm) was observed throughout the training period and was consistent for the three behavioural characteristics (MOV, DISP, and EAR). Although parturition order was not significant in the analysis, we could observe on the 14th day of brushing, the percentage of nulliparous cows that remained calm was higher than for the multiparous in these characteristics. Moreover, despite not possible to annul scores 2 (median agitation) and 3 (agitated), only the multiparous animals exhibited scores 2 and 3, even though a significant reduction in the frequency of these behaviours was noted (not shown in figures).

At the moment of chute exit ((g)), the increase of score 1 from 56.6% (Day 1) to 93.9% (Day 7) and 96.0% (Day 14) occurred. The percentage of animals that trotted or ran (scores 2 and 3) for EXTS when leaving the chute during training days 7 and 14, was considerably low, and it was observed only in multiparous cows.

The analysis of variance with estimated means and Pearson correlation of RR and RT evaluated during the brushing training in Gir dairy cows are shown in , considering the effect of training day (1, 7 and 14), parturition order (PO) (nulliparous and multiparous) in the model. The analysis showed the effect of day of training (P < 0.01) for both traits, but no effect of PO (P > 0.05). The results showed that both physiological parameters decrease from the first day to the other days of training (P < 0.01), however, no difference was reported between the 7th and 14th days of training (P > 0.05). A positive and significant correlation (r = 0.4, P < 0.01) was estimated between RR and RT.

Table 3. Estimated means with standard errors (SE) and respective P values for respiratory rate (RR) and rectal temperature (RT) evaluated during the brushing training of Gir dairy cows. The effects of training day (1–14) and parturition order (PO) (nulliparous and multiparous) are included.

Discussion

Animals prefer to investigate an unknown subject from nearby than by touching as it causes less fear and anxiety to them (Hirata and Arimoto Citation2018). It is well-recognized that novelty is a stimulus that induces a stress response in animals that are not habituated to human handling (Doerfler et al. Citation2016). However, tactile sensitivity is paramount in the handling of dairy cattle, but touching or brushing an animal, especially when outside its line of sight, are actions that may cause unpredictable reactions in a startled animal. Therefore, it is better to establish direct contact with the animals to desensitize them and to render handling and interaction safe.

The significant effect of training days on behavioural characteristics is fundamental evidence to prove that the training through brushing applied to the animals in the chute caused a positive evolution. At first, the animals halted at the entrance of the chute out of fear, demonstrating suspicion, but following the brushing they became less aversive regarding the facility where the training took place, less reactive to brushing, and showed greater acceptance to the close presence and physical contact with the handler, improving from a restless demeanour to calm behaviour. The results reinforce that positive tactile interaction is a strategy of handling to reduce levels of fear of humans in animals (Lensink et al. Citation2001, Citation2000; Boivin et al. Citation2003) being successful even with zebuine breeds (Becker and Lobato Citation1997). In addition, it was observed that the animals liked the brushing, and they began to enter the handling stall voluntarily, without any great need of assistance. In natural conditions, cattle find ways to scratch and groom themselves on abrasive surfaces (McConnachie et al. Citation2018) and in facilities with access to mechanical brushes they spend about fivefold more time grooming compared with those without brushes (DeVries et al. Citation2007). Moreover, we could reach points on the body where the animal does not easily reach, making them interested and motivated to the training. Another study (Fonsêca et al. Citation2019) with training protocol (gentle tactile contact, restraint habituation and food reward) was able to habituate sheep to voluntarily access a squeeze chute.

In spite of the need for some kind of physical stimulation to encourage the entry of the animal into the chute, we could observe reductions in the entry and exit speed parameters during training. It was observed that almost 100% of the animals started walking, suggesting the decrease of fear in relation to the human and, even using some type of control, did not affect their behaviour in the presence of the handler. Such occurrences indicated that these characteristics were more sensitive in detecting actual changes in the behaviour of the animals and in relation with their well-being towards some object, installation, or handler. Several measures related with speed and distance have been used to assess temperament in cattle as exit (Curley et al. Citation2006; Vetters et al. Citation2013) and flight (Sant’Anna et al. Citation2012; Sant’Anna and Paranhos da Costa Citation2013; Vetters et al. Citation2013) speed/score and avoidance/approaching distance (Waiblinger et al. Citation2003; Probst et al. Citation2013, Citation2012). A similar progression was observed in the study conducted by Néri et al. (Citation2016) with ten primiparous Holstein females, which reported a positive effect regarding tactile stimulation on animal behaviour. The animals began to move less during the training, suggesting that petting reduced the fear of the handler, enabling easier and less dangerous management. Breuer et al. (Citation2000) stated that negative handling, as well as tactile interactions, is positively correlated with the degree of restlessness of the animal in the presence of the handler. Tactile interaction can reduce the avoidance distance (Lürzel et al. Citation2016) and can harm productivity and reproductive performance (Hemsworth et al. Citation1981; Hemsworth and Barnett Citation1989), including the health of the animals (Fraser et al. Citation2013) being an important determinant of animal fear of humans.

In general, the behavioural measurements during brushing in the chute (MOV, DISP and EAR) showed a continuous improvement until the last training day (day 14). For the other characteristics measured in the entrance (ENTS, STOP, HELP) or exit velocity (EXTS), the behavioural evolution was positive, but from 7 to 14 days the estimated means did not differ. These results suggest that seven days would be sufficient to improve the ease of leading the animals through the chute and make the cattle less responsiveness to touching.

The vocalization, rumination, and snorting of the animals were little observed during the training period. Vocalization, when it took place, was always for communication, especially when another lot of the herd was being handled nearby. Rumination occurred sporadically, increasing throughout the training. This fact, of increased rumination, showed that brushing had a calming effect. In agreement, it is reported in the literature that the rumination is related to the cow’s comfort state, and is expressed in less stressed animals (Bristow and Holmes Citation2007; Kovács et al. Citation2019). Only four animals snorted as they entered the chute, a behaviour that occurred sporadically and only in the first few days, possibly because constant and positive management conveyed a non-threatening environment.

The females became calmer during brushing, but although the effect of parturition order was not significant in the analysis of variance, it was observed (not shown because of no significant difference) that few cows still remained reactive to tactile stimulus during training being mainly multiparous. The aversive behaviour multiparous to human contact may be due to the fact that they carry in their memory some trauma experienced from negative interactions in the facility itself, the latter being used for several routine husbandry practices considered to affect the animal negatively (Boissy et al. Citation2005), such as medical treatments, ear tagging, weighing, insemination and shipment/landing. In primiparous, this aversive behaviour could be caused by the limited experience of the animals with humans (Sutherland and Huddart Citation2012) and farm facilities before calving.

The nulliparous females, given they were probably experiencing a more constant and recent human-animal relationship, became calmer and more accustomed to handling, mainly since the negative treatment had not yet occurred. Néri et al. (Citation2016) inferred that conventional positive treatment generates memories in the animals, causing them, even without receiving brushing training, to maintain the positive memory of the handler, demonstrating the importance of treatment with positive and gentle interactions in daily management, mainly in young animals. In the studies of Breuer et al. (Citation2003) concluded that negative management increases the fear of heifers by humans, with a lower approximation and a stress response when human presence occurs. In addition, because they are more susceptible to positive interactions, perhaps out of curiosity, it is probably a better opportunity to improve the human-animal relationship (Lürzel et al. Citation2016). Thus, the lack of human contact in early life is specially connected with the defense behaviour of the animal (Le Neindre et al. Citation1996) and the handling at this phase will have an effect on its physiological response to stressors in future life (Grandin Citation1997; Probst et al. Citation2012).

Thus, when the animal has not yet undergone traumatic management, it becomes less aversive to enter the facility and also towards the handler. The positive interactions may reduce the animals` fear (Tanida et al. Citation1995; Lensink et al. Citation2001, Citation2000; Pedersen et al. Citation2002), increasing the human-animal approach and facilitating management. Such findings could suggest, in the future, the use of these animals as leaders to facilitate taming and the application of management activities, such as entering the milking parlour. In addition, positive management enables calm and safe handling for both the animal and the handler.

Respiratory rate is considered a physiological indicator response of the animal to the experimental procedures being used as stress indicator in several studies (Andrade et al. Citation2001; Silva et al. Citation2017; Losada-Espinosa et al. Citation2018; Mohamed et al. Citation2018) as well as rectal temperature (Ahola et al. Citation2000; Waiblinger et al. Citation2006; Burdick et al. Citation2011; Chen et al. Citation2015). When the animal is going under a stressful situation it starts a physiological response in which catecholamines are released its interaction with adrenergic receptors influences a wide variety of body systems, increasing these parameters (Chen et al. Citation2015). On the first day of training, the animals had higher RR and RT and showed a downward trend, suggesting that, as the animals become habituated with the brushing and the handling as well. That is, the animals became calmer showing lower reactive response. Similar behaviour was observed in the study by Néri et al. (Citation2016), who verified that the mean RR decreased during training, exhibiting lower values at each period (initial, intermediate, and final), suggesting that the temperatures can be used as parameters to determine the animal's level of well-being. In other study, temperament differentially affected the rectal temperature and epinephrine (Burdick et al. Citation2011). A significant difference between days occurred between the first day and the 7th day with no difference observed between day 7 and day 14. These findings suggest that 7 days should be adequate to improve the ease of leading the animals through the chute and make them less reactive to human contact.

In the present study, the environmental temperature and humidity was used to calculate the THI using the formula described by Thom (Citation1959). De Azevedo et al. (Citation2005) studied the THI in different crossbreeds (Bos taurus indicus x Bos taurus taurus). They observed that cows with higher zebuine genetic showed higher heat tolerance, estimating values of THI equal to 80, 77 and 75 for genetic groups 1⁄2, 3⁄4 and 7/8 Taurine/Zebuine, respectively. Therefore, we considered the THI threshold as 80. In this study, all the THI estimated mean values were lower than 80 (52.65–78.38), indicating that the animals were in the normal category of the thermal comfort conditions. Besides that, we have to highlight that the zebu Gir cows used in the present study are known to be resistant to heat stress of the tropics (Bó et al. Citation2003). Thus, these values confirm that the Gir animals used in the present study were not subjected to thermal stress during training and indicate that the variation in the rectal temperature and respiratory rate of the cows occurred was due to the absence or presence of fear as the most significant cause.

Treatment with positive stimulation is effective and critical at the beginning of lactation, and it is essential that the husbandry management convey positive interactions, mainly regarding animal’s reaction to the presence of humans. In addition, this form of management may reflect, in the future, on positive temperament and milk production, improving productivity and production during lactation. Finally, pre-partum training is effective, and brushing is a good practice to adapt animals to human physical contact. The positive effects were observed with 7 days of training and a total of 14 days could be considered as optimal to improve the human relationship with the Gir dairy cows.

Acknowledgements

The authors acknowledge FAPESP (process 2015/24.174-3) for financial support; EPAMIG, Finep and MCTI to support the structure for carrying out the research project; and CAPES (Finance Code 001) and CNPq, that financed the scholarships.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo [grant number 2015/24174-3] and CAPES(Finance Code 001).

References