Animal Science

Effect of natural shade on the grazing behavior of breeding ewes from Pelibuey breed

J.O. Serrano^{1  *} 
http://orcid.org/0000-0003-1710-6322

J. Martínez-Melo¹ 
http://orcid.org/0000-0003-4767-9746

Magaly Herrera² 
http://orcid.org/0000-0002-2641-1518

A. Villares¹ 

F.D. Manuel³ 
http://orcid.org/0000-0003-4247-4928

N. Fonseca⁴ 
http://orcid.org/0000-0001-6635-3165

J C. Lorenzo⁵ 
http://orcid.org/0000-0003-3610-1789

¹Facultad de Ciencias Agropecuarias, Universidad de Ciego de Ávila Máximo Gómez Báez (UNICA), Carretera a Morón km 9 ½, CP: 69450, Ciego de Ávila, Cuba

²Instituto de Ciencia Animal, Carretera Central km 47 ½, San José de las Lajas, Mayabeque, Cuba

³Instituto Superior Politécnico de Huíla (ISPH), Universidad de Mandume Ya Ndemufayo, Angola

⁴Centro de Estudio de Producción Animal (CEPA), Universidad de Granma (UDG), Carretera de Manzanillo km 17 ½ CP: 85100, Granma, Cuba

⁵Universidad de Ciego de Ávila Máximo Gómez Báez, Centro de Bioplanta. Laboratorio de mejoramiento y conservación de recursos fitogenéticos, Ciego de Ávila, 69450, Cuba

Abstract

A total of twenty-four breeding ewes from Pelibuey breed were used, divided into two treatments of 12 animals each, to determine the effect of natural shade on the behavior of these animals during grazing. In treatment one, they grazed in the system with natural shade and in treatment two, without shade. Each treatment included the three physiological states: non-pregnant cow, pregnant and lactating. Both groups grazed in two paddocks of natural grasses, of 1.3 ha: one without natural shade, and another with shade from the trees Casuarina equisetifolia (casuarina) and Samanea saman (carob tree). The grazing performance was recorded. Every 10 min., observations during six hours of grazing per day were recorded. Contingency table analysis was used to test the interaction between activities and system type, with and without shade, between activities and day session, and between activities and season for each system, with trees and without them. With the analysis of comparison of proportions (chi square), the time percentages were compared. There was interaction between the activities and the characteristics of the farms, with and without trees, and between the activities and the day session. The animals that had access to the shade of the trees spent more time grazing-walking. When they grazed with trees, they selected activities in the shade, such as rest and rumination. A higher proportion of grazing time was recorded during the morning session. In the system with trees, the highest proportions of grazing time were obtained in both seasons.

Key words: grazing; trees; animal behavior; silvopastoral system

Since the dawn of civilization, sheep have had great significance in human life, making their breeding one of the oldest activities of man. It is currently an economic activity present in almost all continents (^{Lino et al. 2016}). Sheep rearing has increased by 7 % between 2006 and 2016 (^{FAO 2020}), which highlights the importance of this industry in the world. This activity not only contributes to the gross domestic product of the countries, but also supports livelihoods in rural areas.

Climate change is a global phenomenon that, due to its effects, represents a threat to the viability and sustainability of sheep production (^{Gaughan et al. 2010}), specifically in areas located in the tropics (^{McManus et al. 2011}), subtropics and arid areas (^{Ganaie et al. 2013}). In these regions, temperatures rise during the summer, causing the homeostatic balance of animals to decrease and causing heat stress, accompanied by physiological and behavioral changes, which negatively affect productivity.

The increase in ambient temperature, relative humidity and greater exposure to solar radiation make it difficult for animals to regulate energy, thermal, water, hormonal and mineral balances (^{Al-Dawood 2017}). Sheep respond to high temperatures through behavioral or physiological mechanisms (body temperature, respiratory rate, changes in blood serum, among others) or through a combination of both (^{Al-Haidary et al. 2012} and ^{Vicente-Pérez et al. 2018}). The observation of the performance of these animals provides an early indication of their welfare. Commonly recorded behavioral attributes include resting time, feeding behavior and shade seeking, as well as the time lying down (^{Ratnakaran et al. 2017}).

The introduction of trees is one of the ways to transform the microclimate in the production of ruminants and guarantee animal welfare in an environment increasingly affected by unfavorable conditions, such as high temperatures and relative humidity (^{López-Vigoa et al. 2017}). Trees regulate solar radiation that directly affects grazing animals and favors thermal welfare (^{Sousa et al. 2015}). In Ciego de Ávila province, sheep production systems are represented by meadows with a predominance of natural grasses from different species, which may or may not be associated with naturally regenerating trees.

The objective of this study was to determine the effect of natural shade on the grazing behavior of breeding ewes from the Pelibuey breed.

Materials and Methods

The study was carried out in grazing areas of two adjoining cattle farms, in Ciego de Ávila municipality (21 52´48.6´´ N, 78 41´32.6´´ W). They have a yellow quartzitic ferralitic soil, typical leachate and are located at 53 m a.s.l., with a humid tropical climate and precipitation of 600-800 mm per year (^{CMP 2019}). The minimum and maximum environmental temperature is 19.7 and 33.4 ºC and the relative humidity is between 37 and 97 %.

For grazing the animals, two adjoining paddocks of 1.3 ha each, corresponding to two farms, were used. The first showed an average level of arborization of 12-16 trees/ha, with the species Casuarina equisetifolia (Casuarina) and Samanea saman (carob tree of the country). In the second, there was no association with trees. Both showed a botanical composition of Paspalum notatum (40 %), Bothriochloa pertusa and Dichanthium caricosum (45 %) and weed species (15 %), such as wiregrass (Sporobolus indicus) and mallows (Sida rhombifolia).

The Casuarina equisetifolia trees were distributed in the field in an agglomerated way, while those of Samanea saman were randomly distributed. They were approximately three to eight years old and 3 to 10 m tall. The canopy width and height of lower branches were 3.2 and 1.9 m for casuarina and 4.1 and 1.7 m for carob tree, respectively. The animals had access to 14.4 m² of shade per animal.

Animals and treatments. Twenty-four sheep from Pelibuey breed were used, divided into two treatments of 12 animals each. In treatment one, the sheep grazed in the system with natural shade, and in treatment two, in the system without shade. In each group, the animals were homogeneously located and randomly distributed with the different physiological states: non-pregnant (without recognized pregnancy), pregnant (between two and four months) and lactating (between 30 and 90 d of lactation).

Management. The animals were taken to the grazing area twice a day, in the morning, from 9:00 a.m. to 12:00 m., and in the afternoon from 2:00 p.m. to 5:00 p.m. The rest of the time they remained in the facilities, with a supply of 1.0 kg per animal of a mixture of Cenchrus purpureus cv. Cuba CT-169 forage and sugar cane (Saccharum officinarum), common salt and water ad libitum.

Experimental procedure. Animal behavior was measured during 12 d for the rainy (RS) and dry (DS) seasons. In the RS, the data was taken in May, July and September, and for the DS in November, January and April. Every 10 minutes the animals behavior in the different activities was recorded: grazing-walking, resting in the shade, ruminate in the shade, resting in the sun, ruminate in the sun, and others. The latter include urination, defecation, licking, scratching, attacking, moving around and browsing. The activities were carried out in the morning and afternoon sessions, at the established times, for a total of six grazing hours. A total of six observations were made per hours for each group of breeders on each observation day. During the experimentation period, the time (min.) that the animals dedicated to each activity was determined. Behavior analysis was determined by the formula described by ^{Petit (1972)}.

Statistical analysis. A contingency analysis was carried out to find out if there was an interaction between the activities and the presence of shade, the activities and the day session, the activities and the season of year, and in each season, the activities and the presence of shade. For the comparison of proportions (chi-square), ^{Duncan's test (1955)} was applied for P< 0.05 in necessary cases.

Results

There was an interaction (P<0.001) between the activities performed by the animals and the farms under study (table 1). The grazing-walking activity highlighted with a higher percentage in the farm with shade, where the animals dedicated 37 % of the min. to that activity. In the farm without trees invested 32 %. In the treatment without shade, 13.47 % of the animals rested in the sun and 2.7 ruminated in the sun. When they had access to shade, they did not prefer activities in the sun. For other activities, they spent more time on the farm where there were no trees.

Table 1 Effect of shade on the activities of discontinuous behavior 

Farms Activities	With shade		Without shade		SE± Sign.
	Observations /activity	%	Observations /activity	%
Grazing-walking	6500	37.6^a	5529	32.0^b	0.21 0.001
Ruminate in the shade	522	3.02^e	0	0^h
Ruminate in the sun	0	0^h	482	2.7^e
Rest in the shade	1430	8.2^d	0	0^h
Rest in the sun	0	0^h	2327	13.4^c
Other activities	187	1.0^g	302	1.7^f

^abcdefgh Means with different letters significantly differ to P < 0.05 (^{Duncan 1955})

P < 0.001

There was an interaction (P<0.001) between the day session and the activities (table 2). The animals spent 36 % of the time grazing-walking in the morning session. The afternoon session followed with 33.6 %. In the latter, the animals of the farm where there were no trees rested more, with 8.0 % of the min. However, ruminate in the shade and in the sun showed a similar performance in both sessions.

Table 2 Effect of the day session on the activities of discontinuous behavior 

Day sesion Activities	Morning		Afternoon		SE± Sign.
	Observations /activity	%	Observations /activity	%
Grazing-walking	6222	36.0^a	5807	33.6^b	0.21 0.000
Ruminate in the shade	254	1.4^ghi	268	1.5^gh
Ruminate in the sun	284	1.6^gh	197	1.1^hi
Rest in the shade	608	3.5^f	822	4.7^e
Rest in the sun	938	5.4^d	1389	8.0^c
Other activities	333	1.9^g	155	0.9^i

^abcdefghi Means with different letters significantly differ at P < 0.05 (^{Duncan 1955}) P < 0.001

There was an interaction (P<0.001) between the season of the year and the activities (table 3). Most of the time was spent grazing-walking. The interval in which they rested in the sun followed. The time spent resting in the shade, as well as the time spent ruminating, in the shade and in the sun, was similar for both seasons.

Table 3 Effect of the season on the activities of discontinuous behavior 

Seasons Activities	Rainy		Dry		SE± Sign.
	Observations /activity	%	Observations /activity	%
Grazing-walking	6030	34.9^a	5999	34.72^b	0.30 0.001
Ruminate in the shade	252	1.4^f	271	1.5^f
Ruminate in the sun	201	1.1^f	281	1.6^f
Rest in the shade	698	4.0^e	732	4.2^e
Rest in the sun	1224	7.0^c	1103	6.9^d
Other activities	234	1.3^c	254	1.4^f

^abcdef Means with different letters significantly differ at P < 0.05 (^{Duncan 1955}) P < 0.001

There was a similar pattern in the results of the grazing behavior of sheep, in the rainy season as well as in the dry season (table 4 and 5). The activity of grazing-walking in the farm with trees was higher than in the farm without trees, while rest in the sun was higher in the farm without trees. Likewise, rest in the shade was in the farm with trees. Rest in the sun on the farm without trees was higher than rest in the shade on the farm with trees, for both seasons.

Table 4 Effect of shade on activities in the rainy season 

Farms Activities	With trees		Without trees		SE±Sign.
	Observations /activity	%	Observations /activity	%
Grazing-walking	3275	37.9^a	2755	31.8^b	0.30 0.001
Ruminate in the shade	252	2.9^e	0	0^h
Ruminate in the sun	0	0^h	201	2.3^ef
Rest in the shade	698	8.0^d	0	0^h
Rest in the sun	0	0^h	1224	14.1^c
Other activities	94	1.0^g	140	1.6^fg

^abcdefgh Means with different letters significantly differ at P < 0.05 (^{Duncan 1955}) P < 0.001

Table 5 Effect of shade on activities in the dry season 

Farms Activities	With trees		Without trees		SE ±Sign.
	Observations /activity	%	Observations /activity	%
Grazing-walking	3225	37.3^a	2774	32.1^b	0.30 0.001
Ruminate in the shade	271	3.1^e	0	0^g
Ruminate in the sun	0	0^g	281	3.2^e
Rest in the shade	732	8.4^d	0	0^g
Rest in the sun	0	0^g	1103	12.7^c
Other activities	92	1.0^f	162	1.8^f

^abcdefg Means with different letters significantly differ at P < 0.05 (^{Duncan 1955}) P < 0.001

When performing the analysis of the effect of the farms and the activities of urinate and defecate, there was an interaction between the effects (P<0.001). Sheep spent the most time defecating on the farm without trees, with 38.8 % of animals in the activity. It was followed by urinating on the same farm with 32.2 %. It was shown that the animals in the shade spent less time urinating, with 6.9 % (table 6).

Table 6 Effect of shade on the activities of continues behavior 

Farms Activity	With trees		Without trees		SE±Sign.
	Observations /activity	%	Observations /activity	%
Urinate	41	6.9^d	190	32.2^b	1.78 0.000
Defecate	130	22.0^c	229	38.8^a

P < 0.001 ^abcd Means with different letters significantly differ at P < 0.05 (^{Duncan 1955})

There was no interaction between activities and the day session for continuous behavior (table 7). When analyzing the effect of the day session, differences were recorded (P<0.001), since in the morning the animals had a better behavior, with 68.9 %. However, between the activity to urinate and defecate, the latter was the one with the highest percentage, with 60.8 compared to the previous one.

Table 7 Performance of continues behavior , main effects 

Effects	Morning		Afternoon		SE±Sign.
Day session	Observations /activity	%	Observations/activity	%	2.06 0.001
	407	68.9	183	31.0
	Urinate		Defecate		EE±Sign.
Activity	Observations /activity	%	Observations /activity	%	2.06 0.001
	231	39.1	359	60.8

Discussion

The time dedicated by the animals to the activity of grazing-walking was superior to the rest of the activities. This indicates that they spend more on grass intake, with a higher use of grazing time to cover their dry matter intake needs. ^{Solórzano-Montilla et al. (2018)} reported similar behaviors in crossbred West African sheep, without the presence of shade and with artificial shade.

Sheep, like many herbivores, in their natural environment spend long periods of the day identifying and collecting food as part of their animal behavior. According to ^{Hinch (2017)}, food collection in sheep becomes more important when food availability is restricted or the diet is not nutritionally balanced, since sheep spend large proportions of the day taking the food. This study was influenced by the restricted grazing system, which implied higher use of grazing time to cover the dry matter intake needs. Similar results were reported by ^{Oliveira et al. (2013)} and ^{Solórzano-Montilla et al. (2018)}.

In the farm with trees, rest in the shade was the second activity to which they spent the most time. Later, ruminate followed, while these activities on the farm without trees take on a value of zero. However, during rumination and rest, both in the sun, the value becomes zero for the farm with trees, where the animals have the possibility and preference to carry out these activities in the shade. Similar results were obtained by ^{Alvarado-Canché et al. (2017)} in researches carried out with sheep in a silvopastoral system with Leucaena leucocephala and Cynodon plectostachyus, where they recorded the same behavior.

For the farm with trees, the results show that the animals prefer to rest and ruminate in the shade with respect to rest in the sun. In the farm without trees, they spent more time resting and ruminating in the sun, since they did not have shade. These results explain the importance of trees in the sheep grazing system of this study. ^{Candelaria-Martinez et al. (2015)}, ^{Alvarado-Canche et al. (2017)}, ^{Macías-Cruz et al. (2018)} and ^{Reyes et al. (2018)} state that natural or artificial shade promotes cooling mechanisms of animals. In this sense, the reduction in the time dedicated to ruminate, as well as the increase in the time in the standing position and panting, are behaviors that show reductions in thermal welfare (^{Lima et al. 2014} and ^{De et al. 2017}).

The time spent grazing-walking (table 2) was greater in the morning than in the afternoon session. These results coincide with those reported by ^{De-Oliveira et al. (2013)} and ^{Silva et al. (2015)}, who observed higher intensity of grazing in the morning and at the end of the afternoon, times that are related to the best atmospheric conditions. ^{López et al. (2015)} point out that, in response to heat stress, a reduction in food intake appears in sheep.

The activity rest in the shade as well as in the sun was greater in the afternoon than in the morning, which coincides with what was reported by ^{De et al. (2017)} and ^{Solórzano-Montilla et al. (2018)}, who state that in the afternoon session, when the temperature values are higher, the animals considerably decrease intake and spend more time resting and ruminating.

The differences in behavior by season show the changes that occur in the behavioral patterns of these sheep, such as rest and ruminate, to adapt food intake to environmental conditions. The greatest time was dedicated to grazing-walking activity, followed by the time spent resting in the sun in the rainy season (table 3). The presence of trees influenced on that intake was not affected by the incidence of solar radiation and high temperatures. Similar behaviors are described by ^{Chediak-Correa et al. (2013)}, ^{Mahjoubi et al. (2014)}, ^{Todaro et al. (2015)} and ^{Macías-Cruz et al. (2016)}.

The effect of heat stress in sheep have contrasting results, because this form of stress depends on the intensity and duration of the factors that cause it, the species and the genetic characteristics of the animal (^{Al-Haidary et al. 2012}, ^{Indu et al. 2015} and ^{Sejian et al. 2017}). The results of table 5 show the changes in the behavior of the two groups of sheep that graze with access to shade or without it, in both seasons. The greater times dedicated to the activity of grazing-walking and rest in the sun in the rainy season, can be associated with the presence of trees, which favors the thermal environment of grazing, as well as the lack of shade on the farm without trees, which forces the animals to increase their rest in the sun.

The behavior observed in both seasons (table 4 and 5), in which the animals spent more time grazing-walking on the farm with trees, and preferred rest in the shade, may be due to the effects of thermal welfare of trees, which favor the thermoregulation of grazing animals (^{Silva et al. 2015} and Macías-Cruz et al. 2016a).

Defecate and urinate activities were higher in the morning than in the afternoon session, and higher for the farm without trees compared to the farm with trees. This performance could be explained by the production system with restricted grazing, which stimulates the physiological events at the start of grazing in the morning session. The decrease in urination in the afternoon could be associated with fluid retention (^{Macías-Cruz et al. 2018}), which is an adaptation mechanism that hair sheep have to reduce body water loss and avoid dehydration under conditions of intense heat stress. Macías-Cruz et al. (2016a) in a previous study in hair sheep suggested the presence of this mechanism.

In the farm without trees, they performed more actions of urination and defecation, which is explained by the studies of ^{Macías-Cruz et al. (2013)} and ^{Macías-Cruz et al. (2016)}, who suggest that the higher tolerance that hair sheep have to heat stress conditions is the result of genetic and phenotypic adaptations, as well as the activation of physiological, metabolic and endocrinological mechanisms, which help to maintain an adequate body water balance and normothermic conditions (38.3 to 39.9 ºC), at a low energy cost.

Water loss constitutes a thermoregulatory way, associated with the thermal conditions of the relation between the animal and the environment (^{Olarte et al. 2019}). Grazing with trees caused less time to be dedicated to these activities, which could be due to physiological adjustments to try to dissipate the excess body heat load. Various studies agree in suggesting that there is an increase in water intake. (^{Vicente-Pérez et al. 2015}, ^{da Silva et al. 2017} and ^{Vicente Pérez et al. 2020}).

It is concluded that the animals that had access to the trees shade dedicated more time to the grazing-walking activity with respect to those that grazed on the farm without trees. When the sheep grazed in the tree system, shaded activities such as res and ruminate was their choice. The behavior showed a higher proportion of grazing time in the morning session. In the system with trees, the highest proportions of grazing time were obtained in both seasons.

From these results, it can be affirmed that the use of shade, and more specifically, the presence of trees in the paddocks, provides a more favorable environment for grazing sheep production.

References

Al-Dawood, A. 2017. “Towards heat stress management in small ruminants - a review”. Annals of Animal Science, 17(1): 59-88, ISSN: 2300-8733. https://doi.org/10.1515/aoas-2016-0068.

Al-Haidary, A.A., Aljumaah, R.S., Alshaikh, M.A., Abdoun, K.A., Samara, E.M., Okab, A.B. & Alfuraiji, M.M. 2012. “Thermoregulatory and physiological responses of Najdi sheep to environmental heat load prevailingin in Saudi Arabia”. Pakistan Veterinary Journal, 32(4): 515-519, ISSN: 0253-8318.

Alvarado-Canché, A.D., Candelaria-Martínez, B., Castillo-Sánchez, L.E., Piñeiro-Vázquez, A.T. & Canul-Solis, J.R. 2017. “Comportamiento productivo y alimenticio de ovinos en pastoreo en sistemas silvopastoriles con Leucaena leucocephala y Cynodon plectostachyus”. Revista Bio Ciencias, 4(6): 1-11, ISSN: 2007-3380. https://doi.org/10.15741/revbio.04.06.06.

Candelaria-Martínez, B., Flota-Bañuelos, C. & Castillo-Sánchez, L.E. 2015. “Caracterización de los agroecosistemas con producción ovina en el oriente de Yucatán, México”. Agronomía Mesoamericana, 26(2): 225-236, ISSN: 2215-3608. http://dx.doi.org/10.15517/am.v26i2.19278.

Chediak-Correa, M.P., Lima-Dallago, B.S., Rezende-Paiva, S., Andrighetto-Canozzi, M.E., Louvandini, H., Jardim-Barcellos, J. & McManus, C. 2013. “Multivariate analysis of heat tolerance characteristics in Santa Inês and crossbred lambs in the Federal District of Brazil”. Tropical Animal Health and Production, 45(6): 1407-1414, ISSN: 0049-4747. https://doi.org/10.1007/s11250-013-0378-3.

CMP. 2019. Centro provincial de meteorología Ciego de Ávila. Estación Meteorológica del Territorio (78346) Venezuela.

da Silva, W.E., Leite, J.H.G.M. & de Sousa, J.E.R., 2017. “Daily rhythmicity of the thermoregulatory responses of locally adapted Brazilian sheep in a semiarid environment”. International Journal of Biometeorology, 61(7): 1221-1231, ISSN: 1432-1254. https://dx.doi.org/10.1007/s00484-016-1300-2.

De, K., Kumar, D., Saxena, V.K., Thirumurugan, P. & Naqvi, S.M. 2017. “Effect of high ambient temperature on behavior of sheep under semiarid tropical environment”. International Journal of Biometeorology, 61: 1269-1277, ISSN: 1432-1254. https://dx.doi.org/10.1007/s00484-016-1304-y.

De-Oliveira, F.A., Turco, S.H., Aaraújo, G.G., Clemente, C.A., Voltolini, T.V. & Garrido, M.S. 2013. “Comportamento de ovinos da raça Santa Inês em ambientes com e sem disponibilidade de sombra”. Revista Brasileira de Engenharia Agrícola e Ambiental, 17(3): 346-351, ISSN: 1807-1929. https://doi.org/10.1590/S1415-43662013000300015.

Duncan, D.B. 1955. “Multiple range and multiple F test”. Biometrics 11(1): 1-42, ISSN: 1541-0420. https://doi.org/10.2307/3001478.

FAO. 2020. Livestock systems. Available: http://www.fao.org/livestock-systems/global distributions/sheep/en/ [Consulted: January 15th, 2021].

Ganaie, A.H., Ghasura, R.S., Mir, N.A., Bumla, N.A., Sankar, G. & Wani, S.A. 2013. “Biochemical and physiological changes during thermal stress in bovines: A review”. Iranian Journal of Applied Animal Science, 3(3): 423-430, ISSN: 2251-631X.

Gaughan, J.B., Mader, T.L., Holt, S.M., Sullivan, M.L. & Hahn, G.L. 2010. “Assessing the heat tolerance of 17 beef cattle genotypes”. International Journal of Biometeorology, 54: 617-627, ISSN: 1432-1254. https://doi.org/10.1007/s00484-009-0233-4.

Hinch, G.N. 2017. “Understanding the natural behaviour of sheep. In: Advances in Sheep Welfare”. Edited by: Drewe M. Ferguson, Caroline Lee and Andrew Fisher. 1-15. http://doi.org/ 10.1016/B978-0-08-100718-1.00001-7.

Indu, S., Sejian, V. & Naqvi, S.M.K. 2015. “Impact of simulated heat stress on growth, physiological adaptability, blood metabolites and endocrine responses in Malpura ewes under semiarid tropical environment”. Animal Production Science, 55: 766-776, ISSN: 1836-5787. http://dx.doi.org/10.1071/AN14085.

Lima, C.B., Costa, T.G., Nascimiento, T.L., Júnior, D.M., Silva, M.J. & Mariz, T.M. 2014. “Comportamento ingestivo e respostas fisiológicas de ovinos em pastejo no semiárido”. Journal Animal Behavior and Biometeorology, 2(1): 26-34, ISSN: 2318-1265. http://dx.doi.org/10.14269/2318-1265.v02n01a05.

Lino, D.M., Pinheiro, R.S. & Ortunho, V.V. 2016. “Benefícios do bem-estar animal na produtividade e na sanidade de ovinos”. Periódico Eletrônico Fórum Ambiental da Alta Paulista, 12(5): 124-132, ISSN: 1980-0827. http://dx.doi.org/10.17271/1980082712520161506.

López, R., Pinto-Santini, L., Perozo, D., Pineda, J., Oliveros, I., Chacón, T., Rossini, M. & Ríos de Álvarez, L. 2015. “Confort térmico y crecimiento de corderas West African pastoreando con y sin acceso a sombra artificial”. Archivos de Zootecnia, 64(246): 139-146, ISSN: 0004-0592. https://dx.doi.org/10.21071/az.v64i246.388.

López-Vigoa, O., Sánchez, T., Iglesias, J. M., Lamela, L., Soca, M., Arece, J. & Milera, M. 2017. “Los sistemas silvopastoriles como alternativa para la producción animal sostenible en el contexto actual de la ganadería tropical”. Pastos y Forrajes, 40(2): 83-95, ISSN: 2078-8452.

Macías-Cruz, U., Avendaño-Reyes, L., Álvarez-Valenzuela, F.D., Torrentera- Olivera, N.G., Meza-Herrea, C.A. & Mellado-Bosque, M. 2013. “Crecimiento y características de canal en corderas tratadas con clorhidrato de zilpaterol durante primavera y verano”. Revista Mexicana de Ciencias Pecuarias, 4(1): 1-12, ISSN: 2448-6698.

Macías-Cruz, U., Gastélum, M.A., Álvarez, F.D., Correa, A., Díaz, R., Meza-Herrera, C.A., Mellado, M. & Avendaño-Reyes, L. 2016. “Effects of summer heat stress on physiological variables, ovulation and progesterone secretion in Pelibuey ewes under natural outdoor conditions in an arid region”. Animal Science Journal, 87(3): 354-360, ISSN: 1740- 0929. https://dx.doi.org/10.1111/asj.12430.

Macías-Cruz, U., Gastélum, M.A., Avendaño, R.L., Correa, C.A., Mellado, M., Chay, C.A. & Arechiga, C.F. 2018. “Variaciones en las respuestas termoregulatorias de ovejas de pelo durante los meses de verano en un clima desértico”. Revista Mexicana de Ciencias Pecuarias, 9(4): 738-753, ISSN: 2448-6698. https://doi.org/10.22319/rmcp.v9i4.4527.

Macías-Cruz, U., López-Baca, M.A., Vicente, R., Mejia, A., Álvarez, F.D. & Correa-Calderón, A. 2016. “Effects of seasonal ambient heat stress (spring vs. summer) on physiological and metabolic variables in hair sheep located in an arid region”. International Journal of Biometeorology, 60(8): 1279-1286, ISSN: 1432-1254. https://dx.doi.org/10.1007/s00484-015-1123-6.

Mahjoubi, E., Amanlou, H., Mirzaei-Alamouti, H.R., Aghaziarati, N., Hossein Yazdi, M., Noori, G.R., Yuan, K. & Baumgard, L.H. 2014. “The effect of cyclical and mild heat stress on productivity and metabolism in Afshari lambs”. Journal of Animal Science, 92(3): 1007-1014, ISSN: 1525-3163. https://dx.doi.org/10.2527/jas.2013-7153.

McManus, C., Louvandini, H., Gugel, R., Sasaki, L.C., Bianchini, E., Bernal, F. E., Paiva, S. R. & Paim, T. P. 2011. “Skin and coat traits in sheep in Brazil and their relation with heat tolerance”. Tropical Animal Health and Production, 43: 121-126, ISSN: 0049-4747. https://dx.doi.org/10.1007/s11250-010-9663-6.

Olarte, S.M., Sánchez, S.H.R., Aréchiga, C.F.F., Bañuelos R.V. & López L.M.A. 2019. “Efecto de la radiación ultravioleta (UV) en animales domésticos. Revisión”. Revista Mexicana de Ciencias Pecuarias, 10(2): 416-432, ISSN: 2448-6698. https://dx.doi.org/10.22319/rmcp.v10i2.4648.

Oliveira, F.A. de, Turco, Silvia H.N. Aaraújo, G.G.L. de, Clemente, C.A.A., Voltolini, T.V. & Garrido, M.S. 2013. “Comportamento de ovinos da raça Santa Inês em ambientes com e sem disponibilidade de sombra”. Revista Brasileira de Engenharia Agrícola e Ambiental, 17(3): 346-351, ISSN: 1807-1929. https://dx.doi.org/10.1590/S1415-43662013000300015.

Petit, M. 1972. “Emploi du temps des tropeaux de vaches-mères et de leurs veaux sur les pâturages dʹaltitude de lʹaubrac”. Annales de Zootechnie, 21(1): 5-27, ISSN: 1297-9651. Available: https://hal.archives-ouvertes.fr/hal-00887147.

Ratnakaran, A.P., Sejian, V., Jose, V.S., Vaswani, S., Bagath, M., Krishnan, G., Beena, V., Devi, P. I., Varma, G. & Bhatta, R. 2017. “Review Article Behavioral Responses to Livestock Adaptation to Heat Stress Challenges”. Asian Journal of Animal Sciences, 11(1): 1-13, ISSN: 1819-1878. https://doi.org/10.3923/ajas.2017.1.13.

Reyes, J., Herrera, M., Marquina, J.R., Enjoy, D.D. & Pinto-Santini, L. 2018. “Ambiente físico y respuestas fisiológicas de ovinos bajo sombra en horas de máxima radiación”. Archivos de Zootecnia, 67(259): 318-323, ISSN: 0004-0592. https://doi.org/10.21071/az.v67i259.3786.

Sejian, V., Bhatta, R., Gaughan, J., Malik, P.K., Naqvi, S.M.K. & Lal, R. 2017. “Adapting sheep production to climate change”. In: Sejian V., Bhatta R., Gaughan J., Malik P., Naqvi S., Lal R. (eds) Sheep Production Adapting to Climate Change. Springer, Singapore, 1-29, https://doi.org/10.1007/978-981-10-4714-5_1.

Silva, T.P.D., Marques, C.A.T., Torreão, J.N.C., Bezerra, L.R., Araújo, M.J., Gottardi, F.P., Edvan, R.L. & Oliveira, R.L. 2015. “Ingestive behaviour of grazing ewes given two levels of concentrate”. South African Journal of Animal Science, 45(2): 180-187, ISSN: 2221-4062, http://dx.doi.org/10.4314/sajas.v45i2.9.

Solórzano-Montilla, J., Pinto-Santini, L., Camacaro-Calvete, S., Vargas-Guzmán, D. & Ríos de Álvarez, L. 2018. “Efecto de la presencia de sombra en áreas de pastoreo de ovinos. 2. Actividad animal”. Pastos y Forrajes, 41(1): 41-49, ISSN: 2078-8452.

Sousa, L.F., Maurício, R.M., Paciullo, D.S., Silveira, S.R., Ribeiro, R.S., Calsavara, L.H. & Moreira, G.R. 2015. “Forage intake, feeding behavior and bio-climatological indices of pasture grass, under the influence of trees, in a silvopastoral system”. Tropical Grasslands, 3(3): 129-141, ISSN: 2346-3775. https://dx.doi.org/10.17138/tgft(3)129-141.

Todaro, M., Dattena, M., Acciaioli, A., Bonanno, A., Bruni, G., Caroprese, M., Mele, M., Sevi A. & Marinucci, M.T. 2015. “Aseasonal sheep and goat milk production in the Mediterranean area: physiological and technical insights”. Small Ruminant Research, 126: 59-66, ISSN: 0921-4488. http://dx.doi.org/10.1016/j.smallrumres.2015.01.022.

Vicente Pérez, R., Macías C.U., Avendaño, R.L., Correa-Calderón, A., López, M. de los Á. & Lara, R.A.L. 2020. “Impacto del estrés por calor en la producción de ovinos de pelo. Revisión”. Revista Mexicana de Ciencias Pecuarias, 11(1): 205-222, ISSN: 2448-6698. https://dx.doi.org/10.22319/rmcp.v11i1.4923.

Vicente-Pérez, A., Avendaño-Reyes, L., Barajas-Cruz, R., Macías-Cruz, U., Correa-Calderón, A., Vicente-Pérez, R., Corrales-Navarro, J.L. & Guerra-Liera, J.E. 2018. "Parámetros bioquímicos y hematológicos en ovinos de pelo con y sin sombra bajo condiciones desérticas". Ecosistemas y Recursos Agropecuarios, 5(14): 259-269, ISSN: 2007-901X. https://dx.doi.org/10.19136/era.a5nl4.1544.

Vicente-Pérez, R., Avendaño-Reyes, L., Álvarez, F., Correa-Calderón, A., Meza-Herrera, C.A. & Mellado, M. 2015. “Comportamiento productivo, consumo de nutrientes y productividad al parto de ovejas de pelo suplementadas con energía en el preparto durante verano e invierno”. Archivos de Medicina Veterinaria, 47(3): 301-309, ISSN: 0301-732X. http://dx.doi.org/10.4067/S0301-732X2015000300006.

Received: May 05, 2021; Accepted: October 09, 2021

^*Email: [e-mail]

Conflict of interest: The authors declare that there is no conflict of interest between them.

Authors contribution: J. O. Serrano: Conceptualization, Investigation, Formal analysis, Writing – original draft. J. Martínez-Melo: Conceptualization, Formal analysis, Writing – original draft. Magaly Herrera: Formal analysis, Writing – original draft. A. Villares: Investigation, Formal analysis. F.D. Manuel: Investigation, Formal analysis. N. Fonseca: Conceptualization, Formal analysis. J.C. Lorenzo: Conceptualization, Investigation, Formal analysis.