
==== Front
Trop Anim Health Prod
Trop Anim Health Prod
Tropical Animal Health and Production
0049-4747
1573-7438
Springer Netherlands Dordrecht

39133338
4097
10.1007/s11250-024-04097-6
Regular Articles
Relationship between metabolic indices and milk yield in Saanen goats exposed to heat stress in semi-tropical climates
Akkaya Fatma 1
Mecitoğlu Zafer 2
Şentürk Sezgin 2
Koşum Nedim 1
Kasap Sevim 2
Takma Çiğdem 1
Taskin Turgay 1
Yalçin Murat 3
http://orcid.org/0000-0001-7378-6962
Kandemir Çağrı cagri.kandemir@ege.edu.tr

1
1 https://ror.org/02eaafc18 grid.8302.9 0000 0001 1092 2592 Faculty of Agriculture, Department of Animal Science, Ege University, İzmir, 35100 Turkey
2 https://ror.org/03tg3eb07 grid.34538.39 0000 0001 2182 4517 Faculty of Veterinary Medicine, Department of Internal Medicine, Bursa Uludağ University, Bursa, Türkiye
3 https://ror.org/03tg3eb07 grid.34538.39 0000 0001 2182 4517 Faculty of Veterinary Medicine, Department of Physiology, Bursa Uludağ University, Bursa, Türkiye
12 8 2024
12 8 2024
2024
56 7 2417 7 2023
18 7 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by/4.0/ Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
This study aimed to determine the effects of heat stress on 30 Saanen goats of different ages (young, middle-aged, and old). The average temperature and humidity values during the trial were 27.82 °C and 40.65%, respectively. Statistically significant differences in pulse rate (PR), respiratory rate (SS), and temperature humidity index (THI) were found between months (P < 0.05). Beta-hydroxybutyric acid (BHBA) values were found to be statistically significant in the young and middle-aged group (P < 0.05), with the highest in the middle-aged group obtained in June (0.65 mmol/L). Non-esterified fatty acids (NEFA) and urea (BUN) were significantly different (P < 0.05) in all age groups, whereas creatinine values showed no significant differences between groups. Significant positive relationships were found between body weight (BW) and body condition score (BCS), as well as pulse rate (PR) and daily average daily milk yield (DAMY) (P < 0.01). A positive correlation was also found between the respiratory rate (SS) and pulse rate (P < 0.01). As a result, although attempts have been made to prevent the decrease in productivity with applications for animals under heat stress, the optimal strategy may be to address the source of the problem. Issues that cause heat accumulation in the body should be identified and necessary arrangements should be made in the shelter to distribute heat to ensure that animals are less affected. Shaded areas should be provided in cases of stress caused by heat. An appropriate structural arrangement for temperature, humidification, and ventilation systems, as well as the provision of abundant fresh drinking water, would also be beneficial.

Highlights

Decreased milk yield is related to thyroid hormones which speed up metabolic processes by increasing enzyme activity.

A significant decrease in milk yield was observed in both the young and old groups in July and August, when heat stress was most prevalent.

The middle-aged group was least affected by heat stress in terms of milk yield.

Changes in creatinine levels were insignificant, only determining a significant decrease in urea levels.

Despite decreased feed intake, no rise in plasma NEFA was observed.

Keywords

Heat stress
Milk yield
Warming
NEFA
Ege UniversityOpen access funding provided by the Scientific and Technological Research Council of Türkiye (TÜBİTAK).

issue-copyright-statement© Springer Nature B.V. 2024
==== Body
pmcIntroduction

In recent years, climate change has increased the awareness of the effects of heat stress on animals (Alsharif 2022). Saanen goats are strongly affected by heat stress due to their robust milk metabolism (Kandemir et al. 2013; Yilmaz et al. 2018a; Lima et al. 2022). Recent studies have shown that heat stress has a significant effect on metabolic profiles, including energy, liver, and hormonal metabolism, which lowers milk production (Hooper et al. 2018; El-Gindy et al. 2022; Choi et al. 2021; Lima et al. 2022). To circumvent this, some scientists have focused on minimizing the heat stress experienced by animals by improving the environment in which they are maintained (Saipin et al. 2020; Choi et al. 2021; Salem et al. 2022; Hanafi et al. 2022).

In hot, dry regions where the ambient temperature may surpass the upper critical threshold of animals, environmental and climatic stressors both play a significant role in animal production. According to previous reports, goats are less susceptible to stress factors than other domesticated ruminants (Khalifa et al. 2005). Goats can adjust to hot and dry conditions because of their ability to conserve water, basal metabolic rate, high respiratory rate, high skin temperature, and constant cardiac output. However, heat stress may still impair the rumen fermentation and growth efficiency of goats (Xue et al. 2022). Indeed, research has demonstrated that exposure to heat stress reduces the number of cellulolytic bacteria and increases the abundance of bacteria that break down starch (Xue et al. 2022).

In Turkey, many residents in both urban and rural areas raise goats to address their milk needs (Daskıran et al. 2018). This study was designed to compare how heat stress affects the metabolism of dairy goats of different age groups during the summer season in Turkey, in order to devise strategies to help mitigate the effect of global warming on livestock.

Materials and methods

Animals

This study was conducted on 30 Saanen goats raised at the Farm Animal Production, Research, and Application Centre of the Faculty of Agriculture, Ege University. The goats used in this study were subjected to a general health examination before the study, and received annual preventive immunizations at regular intervals. The goats were divided into three age groups: young (average age: 1.5 y), middle-aged (average age: 3.5 y), and older (average age: 5.5 years old). The animals did not become pregnant during the experiments. All experiments were approved by the Ege University Local Animal Experiments Ethics Committee (2020-082).

Location, feeding, and management

The experimental study continued for 4 months (May–August), during which the goats were in the mid-lactation period. Izmir, where the study was conducted, is a city located on the seaside of the Aegean region of Turkey and thus has a Mediterranean climate. June, July, and August are considered the summer months. In the Aegean region, beginning in May, animals remain at a high temperature for four to five months. Therefore, these months were chosen as the optimal time to study animal heat discomfort. The daily temperature, relative humidity, and humidity index were recorded monthly. All animals were provided with 0.8 kg of pelleted feed, 2.0 kg of corn silage, 0.2 kg of wheat straw, and 0.6 kg of dry alfalfa grass daily as feed, provided using a feed-vending machine equipped with a radiofrequency identification system. The daily average milk yield (DAMY) of the goats was determined, and additional milk feed requirements were identified.

Sampling and data

Throughout the experiment, DAMY data were gathered from the herd management system. Body weight (BW) and body condition score (BCS) were measured twice a month. The heart rate of the goats was also measured between the left 3–6 costa, and the respiratory rate (RR) was calculated based on the flank’s motion. A digital thermometer (KERBL®, Ankara, Turkey) was used to measure the rectal temperature of the goats. The pulse rate (PR) (beats/min), respiratory rate (RR) (beats/min), and rectal temperature (RT) (0 C) of the goats were measured twice daily (08:00–09:00 a.m. and 2:00–3:00 p.m.) throughout the study period. Blood samples (2 ml) were collected from the jugular vein in vacuum tubes without anticoagulants twice a month. During processing, blood samples were first allowed to clot, after which they were centrifuged at 3000 rpm for 10 min at 4 0 C to obtain serum. The serum samples were the collected and stored at − 20 °C until analysis of biochemical hormonal parameters. Biochemical tests were conducted using Randox test kits (Randox Laboratories Ltd., Crumlin, UK). The enzyme aspartate aminotransferase (AST) was measured using the UV (Modified IFCC) technique (catalogue number: AS3804). The colorimetric method was applied to measure the levels of total protein (TP) (catalogue number: TP3869), beta-hydroxybutyric acid (BHBA) (catalogue number: RB1007), non-esterified fatty acids (NEFA) (catalogue number: FA115), gamma-glutamyl transferase (GGT) (catalogue number: GT8320), and lactate (LACT) (catalogue number: LC3980). Biuret and enzymatic kinetic procedures were employed to assess urea (BUN) (catalogue number: UR3825) and creatinine (CREA) (catalogue number: CR3814).

Statistical analysis

Any differences in metabolic and physiological measurements for goats of the same age according to month were analyzed using GLM univariate analysis. Tukey’s multiple comparison test was applied to perform multiple comparisons of means (SAS 1999).

Results

Descriptive statistics of the climatic data according to month are shown in Fig. 1. According to our findings, while the highest temperature (HT, °C) in May was 25.11 °C, this value increased to 39.48 °C in August, yielding a temperature rise of more than 14 °C. The average temperatures in May, June, July, and August were 21.50 °C, 27.18 °C, 31.82 °C, and 30.81 °C respectively. During the entire study period, the mean temperature overall was 27.82 °C, and the average humidity value was 40.65%. The difference between the months in terms of HT (°C), AT (°C), AH (%), and the temperature humidity index (THI) was found to be statistically significant (P < 0.05).

Fig. 1 The temperature, relative humidity, and humidity index measurements for each month of the experiment. Data shows mean ± SEM of the monthly mean of daily measurements

BW did not affect heat stress in goats of any age group, whereas BCS was found to have an impact on the young and middle-aged groups (P < 0.05). Only the middle-aged group showed a substantial impact of RR, while DAMY, RT, and PR were statistically significant in all other age groups (P < 0.05). In all groups, DAMY decreased significantly in the months with the highest heat stress, while RT, PR, and RR increased the most in August (Table 1).

Table 1 Heat stress’s physiological consequences on goats

	Young	Middle	Old	
	Ma	Ju	Jl	Au	P	Ma	Ju	Jl	Au	P	Ma	Ju	Jl	Au	P	
BW	64,31	65,99	68,50	71,23	0,36	69,77	70,12	71,64	74,03	0,68	63,16	62,66	62,85	64,18	0,99	
BCS	2,5b	2,5b	2,5b	2,75a	< 0,01	2,5a	2,5a	2,5b	2,63a	< 0,01	2,5	2,5	2,13	2,25	0,32	
DAMY	2,69 a	2,41 ab	2,24 bc	1,97 c	< 0,01	2,69 a	2,47 ab	2,27 ab	2,06 b	0,02	2,40 a	2,01 ab	1,84 b	1,60 b	< 0,01	
RT	38,90a	39,00a	39,15ab	39,30b	0,03	38,6a	38,90ab	38,90b	39,00b	0,03	38,50a	38,75ab	38,95ab	39,00b	< 0,01	
RR	29,30	31,90	30,22	36,80	0,47	24,70b	27,60b	28,00ab	31,40a	< 0,01	24,10a	28,30ac	29,30bc	32,80b	0,62	
PR	107,00a	111,50ab	117,00ab	121,50b	< 0,01	98,00a	108,00ab	116,00b	121,00b	< 0,01	79,00a	89,00ab	98,00b	104,00b	< 0,01	
a.b.c: The distinction between different letters on the same line is statistically significant; *:P < 0.05, **:P < 0.01

Ma: May; Ju: June; JL: July; Au: August; BW(kg): Bodyweight; BCS: Body condition score; DAMY(kg): Daily Average Milk Yield; RT (oC): Rectal temperature; RR(beat/min): Respiratory rate; PR(beat/min): Pulse rate; P < 0.05

The young group was the most affected by heat stress in terms of metabolic parameters. Indeed, all parameters except CREA were statistically significant in the young group (P < 0.05). Although CREA and LACT were not significant (p > 0.05) in the middle-aged group, all other parameters were statistically significant (P < 0.05). In the older group, only the TP, NEFA, and BUN values were significantly different (P < 0.05) (Table 2). Overall, a significant positive correlation was found between BW and BCS, as well as PR, and DAMY (P < 0.01) (Table 3). While a positive and significant relationship was found between RR and PR (P < 0.01), a significant negative relationship was found between RT, BHBA, and DAMY (P < 0.05). In contrast, the relationship between RR and BHBA level was negative and significant (P < 0.01). Conversely, the relationship between BUN and CREA, LACT, and DAMY were positive and significant (P < 0.01) (P < 0.05), and a positive and significant relationship was also observed between the CREA and LACT (P < 0.05).

Table 2 Related metabolic changes on by heat stress in goats

	Young	Middle	Old	
	Ma	Ju	Jl	Au	P	Ma	Ju	Jl	Au	P	Ma	Ju	Jl	Au	P	
BHBA	0,49bc	0,61a	0,53b	0,38c	< 0,01	0,49b	0,65a	0,53ab	0,46b	0,01	0,34	0,46	0,40	0,28	0,17	
TP	5,46a	4,74ab	4,35ab	3,54b	< 0,01	5,15a	4,86a	4,97a	3,38b	< 0,01	5,58a	5,55a	5,32ab	4,13b	0,02	
AST	123,9a	109,7a	104,7a	70,5b	< 0,01	119,0a	113,9a	109,7a	75,5b	< 0,01	130,9	127,2	120,1	93,6	0,07	
GGT	45,7a	37,1ab	40,4ab	30,5b	0,03	39,9 a	34,8 a	39,1 ab	27,7 b	< 0,01	41,1	38,8	36,6	30,1	0,1	
NEFA	0,10a	0,12a	0,05b	0,04b	< 0,01	0,084	0,085	0,041	0,021	< 0,01	0,07a	0,08a	0,04ab	0,04b	0,04	
BUN	27,32a	23,85ab	27,64a	19,20b	< 0,01	23,87ab	19,67bc	25,62a	16,77c	< 0,01	24,14a	20,44ab	24,69a	14,93b	< 0,01	
CREA	0,629	0,644	0,651	0,584	0,40	0,610	0,617	0,627	0,585	0,76	0,627	0,651	0,657	0,61	0,72	
LACT	14,70a	14,65a	10,66ab	8,07b	0,01	12,70	13,78	13,13	10,31	0,17	14,52	13,53	17,90	12,80	0,50	
a.b.c: The distinction between different letters on the same line is statistically significant; *:P < 0.05, **:P < 0.01

Ma: May; Ju: June; JL: July; Au: August; BHBA(mmol/L): Beta-hydroxybutyric acid; NEFA(mmol/L): Non-esterified fatty acid; AST(U/L): Aspartate aminotransferase; GGT(U/L): Gamaglutamyltransferase; TP(g/dl): Total protein; BUN(mg/dL): Urea; CREA(mg/dL): Creatinine, LACT(mg/dL): Lactate; P < 0.05

Table 3 Phenotypic correlations between physiological and biochemical parameters in goats

	BBCS	RRT	RRR	PPR	BBHBA	TTP	AAST	GGGT	NNEFA	BBUN	CCREA	LLACT	DDAMY	
BBW	,607**	-,021	,078	,239**	-,127	,094	-,101	-,141	-,035	-,101	,153	-,083	,311**	
BBCS		,062	,092	,286**	-,053	,250**	,039	-,008	,104	,021	,190*	,036	,309**	
RRT			,327**	,541**	-,125	,165	,137	,091	-,174	-,041	-,042	,144	-,215*	
RRR				,519**	-,300**	-,096	-,098	-,171	-,147	-,110	-,178	-,067	-,095	
PPR					-,217*	,025	-,037	-,087	-,092	-,097	-,066	,047	-,079	
BBHBA						,164	,125	,387**	,147	,405**	,084	,090	,235*	
TTP							,574**	,652**	,355**	,317**	,604**	,351**	,051	
AAST								,376**	,267**	,338**	,341**	,366**	-,031	
GGGT									,250**	,402**	,373**	,190*	,156	
NNEFA										,070	,158	,122	,100	
BBUN											,316**	,214*	,249**	
CCREA												,213*	,123	
LLACT													,011	
**: Correlation is significant at the 0.01 level (2-tailed). *: Correlation is significant at the 0.05 level (2-tailed)

BW: Bodyweight; BCS: Body condition score; DAMY: Daily average milk yield; RT: Rectal temperature; RR: Respiratory rate; PR: Pulse rate; BHBA: Beta-hydroxybutyric acid; NEFA: Non-esterified fatty acid; AST: Aspartate aminotransferase; GGT: Gamma glutamyl transferase; TP: Total protein; BUN: Urea; CREA: Creatinine, LACT: Lactate

Discussion

Overall, it is necessary to develop sustainable management systems that consider the effects of climate change in the livestock industry. Conserving and spreading indigenous goat breeds that are climate-robust is one of several tactics that can be used to fight the harmful consequences of climate change. Goats are one of the livestock species with the highest climate tolerance across all continents. Environmental stress can be quantified by measuring the THI and correlating it with physiological, biochemical, or behavioral responses.

Many studies have shown that physiological shifts in PR, RR, and RT are the earliest signs of heat stress (Yadav et al. 2015; Kumar et al. 2020; Srivastava et al. 2021). In regards to rater (Gaughan et al. 2000; Phulia et al. 2010; Yadav et al. 2015; Kumar et al. 2018), goats increase their RR when exposed to heat to achieve homeothermy by respiratory heat loss, thus avoiding heat stress (Berbigier and Cabello 1990). The findings of a previous study revealed that at THIs of 71.78 and 79.48, respectively, PR was the first physiological parameter to change in both the Jamunapari and Barbari goat breeds, while goats native to India’s semi-arid region responded to environmental heat stress by increasing PR (Srivastava et al. 2021). Numerous studies have found that, as the PR increases, the muscles controlling the RR become more active, which functions to further increase the RR (Gupta and Mondal 2021). These data further demonstrate that the first sign of heat stress is an increase in PR. Studies on dairy cattle conducted by Jackson and Cockcroft (2008), Zimbelman et al. (2011), Dalcin et al. (2016), and Pinto et al. (2019) have all shown that the key THI for PR falls in the range between 68 and 73. Under heat stress conditions, a cascade of biochemical changes occurs in the body. For example, the body’s energy metabolism shifts toward maintenance, ultimately resulting in a loss of production when physical and physiological heat loss mechanisms fail to maintain homeothermy. In this study, in July and August, when heat stress was most prevalent, the goats in both the young and old groups showed a significant decrease in milk yield (Table 1). One previous study showed that a THI of 79 decreased milk output in Alpine goats, but did not affect Nubian goats (Brown et al. 1988). Furthermore, while Hamzaoui et al. (2013) reported a THI of 77 to be critical for Spanish Murciano-Granadina dairy goats, El-Tarabany et al. (2017) reported that a THI of 80 was critical for goats, and Sevi et al. (2001) suggested a critical THI of 80 in sheep. However, Hamzaoui et al. (2013) reported that goats suffered severe heat exhaustion at a THI of 85. Another study showed that Saanen goats showed reductions in daily milk yield of 3% and 13% at THIs of 81 and 89, respectively, (Sano et al. 1985). In the present study, the middle-aged group was found to be the least affected by heat stress in terms of milk yield, while the younger group was more adversely affected than the older group, resulting in lower milk yields. In addition, the RT values increased during the months that experienced the most severe heat stress. While maintaining a healthy body temperature is crucial for the production of milk in conditions such as mastitis, it is believed that febrile diseases takes longer to heal and/or have a worse prognosis because of the relative rise in temperature during the summer months. However, it could be stated that the decrease in milk yield is related to this because thyroid hormones accelerate metabolic processes by increasing enzyme activity. When an animal is subjected to heat stress, blood flow is concentrates in the periphery, water loss in the body increases, and movements slow down due to increased sweating and respiration rates (Contreras-Jodar et al. 2018; Bomfim et al. 2022). Owing to the disruption in circulation, the liver and udder tissues may not receive sufficient nutrients, which decreases milk production.

The values of all blood metabolites and enzymatic activities in the current study were within the typical reference ranges (Bertoni et al. 2020). In this study, we observed significant differences in BHBA, TP, AST, GGT, NEFA, BUN, and LACT levels. The current study’s observation of the impact of THI on energy metabolism is consistent with previous findings in goats under heat stress (El-Tarabany et al. 207; Yilmaz et al. 2018b). These effects could be attributed to several factors, including (1) decreased energy intake as a result of decreased DMI, (2) increased thermoregulation costs, (3) nutrient partitioning, and (4) the negative impact of heat on gluconeogenesis as a result of the body’s endocrine adaptation to hot conditions (Sorianiet al. 2013). Despite the decreased feed intake, no increase in plasma NEFA was observed, which is consistent with the findings of other studies investigating animals under heat stress (Rhoads et al. 2009; Shwartz et al. 2009). The evaluation of hematological parameters is crucial for determining how animals react to various stressful situations, as they are reliable markers of an individual’s physiological health status (Attia 2016). To assess the general health of the animals, we assessed serum enzymatic activity. According to Duncan and Prasse (1994), heat stress decreases the plasma levels of the enzymes aspartate aminotransferase (AST) and alanine aminotransferase (ALT), albeit within normal physiological bounds. Regarding renal function outcomes, Abdel-Samee et al. (2008) found that under heat-stress conditions, the blood levels of urea and creatinine significantly decreased. Although our study showed that the changes in creatinine levels were insignificant, only a significant decrease in urea levels was observed. This may be explained by a decrease in ruminal Ammonia-N, which is offset by an increase in Urea-N absorption in the rumen, causing a decrease in blood urea levels, and an increase in urine nitrogen excretion. These findings were consistent with those reported by Fike et al. (2005). It has been shown that there were considerable variations in blood biochemical levels, which may be the result of an altered metabolism triggered by stress in the goats.

Conclusion

When the ambient temperature exceeds the range of an animal’s thermoneutral zone, a combination of environmental conditions result in a condition known as heat stress. Feed intake, growth rate, and haemato-biochemical profile of goats were all negatively impacted by heat stress. During some periods of the trial, the dairy goats used in this study experienced mild to moderate heat stress. In addition to an increase in breathing rate and rectal temperature, the physiological markers of heat stress assessed in this study demonstrated that hot conditions affected hematological variables linked to energy, protein, and enzyme activity (Kandasami et al. 2023; Kaushik et al. 2023). As a result, although attempts have been made to prevent the decrease in productivity with applications for animals under heat stress, the optimal strategy would be to mitigate the source of the problem. Issues that cause heat accumulation in the body should be identified, and necessary arrangements should be made in animal shelters to distribute heat and ensure that the animals are less affected by high temperatures. Shaded areas should be provided in case of stress caused by heat. An appropriate structural arrangement for temperature, humidification, and ventilation systems along with the provision of plenty of fresh drinking water would also be beneficial.

Acknowledgements

This study was supported by Ege University Scientific Research Projects Directorate under Grant TGA-2020-22162: The Effect of Heat Stress on Some Physiological, Biochemical Values and Hormone Levels in Saanen Goats Raised in Semi-Intensive Conditions, 2020–2022.

Author contributions

F.A. and Ç.K. conceived and designed the study, Z.M., S.Ş., S.K. and M.Y. conducted laboratory works, F.A. and T.T. performed field sampling, T.T. and Ç.K. prepared and arranged the phenotypic data, Ç.T. reviewed the manuscript, statically analyses and assisted in data interpretation. All authors read and approved the manuscript.

Funding

Open access funding provided by the Scientific and Technological Research Council of Türkiye (TÜBİTAK). This research has been funded by Ege University Scientific Research Projects Directorate under Grant (Project number: TGA-2020-22162).

Data availability

The data that support the findings of this study are available upon reasonable request from the corresponding author.

Declarations

Ethical approval

All animal procedures in the study were reviewed and approved by t Local Ethics Committee of Ege University (Approval Number: 2020082), and the authors complied with the ARRIVE guidelines.

Consent to participate

Not applicable.

Consent for publication

All authors give consent for publication.

Conflict of interest

The authors declare that they have no conflicts of interest.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
==== Refs
References

Abdel-Samee AM Abd-Alla O EL-Adawy S Nutritional treatments for alleviation of heat stress in Awassi Sheep using Acacia and Olive Pulp in Subtropics Egypt J Comp Path Clin Path 2008 21 466 477
Abdel-Samee AM, Abd-Alla O, EL-Adawy S (2008) Nutritional treatments for alleviation of heat stress in Awassi Sheep using Acacia and Olive Pulp in Subtropics. Egypt J Comp Path Clin Path 21:466–477
Alsharif I Comprehensive exploration of the molecular response, clinical signs, and histological aspects of heat stress in animals J Therm Biol 2022 10.1016/j.jtherbio.2022.103346 36462855
Alsharif I (2022) Comprehensive exploration of the molecular response, clinical signs, and histological aspects of heat stress in animals. J Therm Biol 103346. 10.1016/j.jtherbio.2022.10334636462855
Attia NES Physiological, hematological and biochemical alterations in heat stressed goats Benha Veterinary Med J 2016 31 2 56 62 10.21608/bvmj.2016.31261
Attia NES (2016) Physiological, hematological and biochemical alterations in heat stressed goats. Benha Veterinary Med J 31(2):56–62. 10.21608/bvmj.2016.31261
Berbigier P Cabello G Effect of exposure to full sunshine on temperature regulation of pregnant dwarf goats of Guadeloupe (French West Indies), and on birthweight, T3 and T4 plasma levels of newborn kids J Therm Biol 1990 15 2 109 113 10.1016/0306-4565(90)90026-E
Berbigier P, Cabello G (1990) Effect of exposure to full sunshine on temperature regulation of pregnant dwarf goats of Guadeloupe (French West Indies), and on birthweight, T3 and T4 plasma levels of newborn kids. J Therm Biol 15(2):109–113
Bertoni G, Calamari L, Trevisi E (2020) Nuovi criteri per l’individuazione dei valori di riferimento di taluni parametri ematici in bovine da latte. La Selezione Veterinaria (Suppl.):261–268
Bomfim GF Merighe GKF de Oliveira SA Negrao JA Acute and chronic effects of cortisol on milk yield, the expression of key receptors, and apoptosis of mammary epithelial cells in Saanen goats J Dairy Sci 2022 105 1 818 830 10.3168/jds.2021-20364 34756435
Bomfim GF, Merighe GKF, de Oliveira SA, Negrao JA (2022) Acute and chronic effects of cortisol on milk yield, the expression of key receptors, and apoptosis of mammary epithelial cells in Saanen goats. J Dairy Sci 105(1):818–830. 10.3168/jds.2021-2036434756435
Brown DL Morrison SR Bradford GE Effects of ambient temperature on milk production of Nubian and Alpine goats J Dairy Sci 1988 71 9 2486 2490 10.3168/jds.S0022-0302(88)79835-5
Brown DL, Morrison SR, Bradford GE (1988) Effects of ambient temperature on milk production of Nubian and Alpine goats. J Dairy Sci 71(9):2486–2490
Choi WT Nejad JG Moon JO Lee HG Dietary supplementation of acetate-conjugated tryptophan alters feed intake, milk yield and composition, blood profile, physiological variables, and heat shock protein gene expression in heat-stressed dairy cows J Therm Biol 2021 98 102949 10.1016/j.jtherbio.2021.102949 34016366
Choi WT, Nejad JG, Moon JO, Lee HG (2021) Dietary supplementation of acetate-conjugated tryptophan alters feed intake, milk yield and composition, blood profile, physiological variables, and heat shock protein gene expression in heat-stressed dairy cows. J Therm Biol 98:102949. 10.1016/j.jtherbio.2021.10294934016366
Contreras-Jodar A Salama AA Hamzaoui S Vailati-Riboni M Caja G Loor JJ Effects of chronic heat stress on lactational performance and the 28 transcriptomic profile of blood cells in lactating dairy goats J Dairy Res 2018 85 4 423 430 10.1017/S0022029918000705 30236165
Contreras-Jodar A, Salama AA, Hamzaoui S, Vailati-Riboni M, Caja G, Loor JJ (2018) Effects of chronic heat stress on lactational performance and the 28 transcriptomic profile of blood cells in lactating dairy goats. J Dairy Res 85(4):423–430. 10.1017/S002202991800070530236165
Dalcin VC Fischer V Daltro DDS Alfonzo EPM Stumpf MT Kolling GJ McManus C Physiological parameters for thermal stress in dairy cattle Revista Brasileira De Zootecnia 2016 45 458 465 10.1590/S1806-92902016000800006
Dalcin VC, Fischer V, Daltro DDS, Alfonzo EPM, Stumpf MT, Kolling GJ, McManus C (2016) Physiological parameters for thermal stress in dairy cattle. Revista Brasileira De Zootecnia 45:458–465. 10.1590/S1806-92902016000800006
Daskıran I, Savaş T, Koyuncu M, Koluman N, Keskin M, Esenbuğa N, Konyali A, Cemal İ, Gül S, Elmaz O, Kosum N, Dellal G, Bingöl M (2018) Goat production systems of Turkey: Nomadic to industrial. Small Rumin Res 163:15–20. 10.1016/j.smallrumres.2017.10.001
El-Gindy YM, Sabir SA, Zahran SM, Morshedy SA (2022) The protective effect of aqueous orange peel extract against severe heat stress on reproductive efficiency, milk yield, and antioxidant status of female rabbits. J Therm Biol 103403. 10.1016/j.jtherbio.2022.103403
El-Tarabany MS El-Tarabany AA Atta MA Physiological and lactation responses of Egyptian dairy Baladi goats to natural thermal stress under subtropical environmental conditions Int J Biometeorol 2017 61 61 68 10.1007/s00484-016-1191-2 27225437
El-Tarabany MS, El-Tarabany AA, Atta MA (2017) Physiological and lactation responses of Egyptian dairy Baladi goats to natural thermal stress under subtropical environmental conditions. Int J Biometeorol 61:61–68. 10.1007/s00484-016-1191-227225437
Fike J Saker KE Fonte-not J Veit H Effect of Tasco (a seaweed extract) and heat stress on N metabolism and meat fatty acids in wether lambs fed hays containing endophyte-infected fescue Small Rumin Res 2005 60 237 245 10.1016/j.smallrumres.2004.12.007
Fike J, Saker KE, Fonte-not J, Veit H (2005) Effect of Tasco (a seaweed extract) and heat stress on N metabolism and meat fatty acids in wether lambs fed hays containing endophyte-infected fescue. Small Rumin Res 60:237–245. 10.1016/j.smallrumres.2004.12.007
Gaughan JB, Holt S, Hahn GL, Mader TL, Eigenberg R (2000) Respiration rate: is it a good measure of heat stress in cattle? Asian-Australasian J Anim Sci 13(Supplement C): 329–332
Gupta M Mondal T Heat stress and thermoregulatory responses of goats: a review Biol Rhythm Res 2021 52 3 407 433 10.1080/09291016.2019.1603692
Gupta M, Mondal T (2021) Heat stress and thermoregulatory responses of goats: a review. Biol Rhythm Res 52(3):407–433. 10.1080/09291016.2019.1603692
Hamzaoui SAAK Salama AAK Albanell E Such X Caja G Physiological responses and lactational performances of late-lactation dairy goats under heat stress conditions J Dairy Sci 2013 96 10 6355 6365 10.3168/jds.2013-6665 23958010
Hamzaoui SAAK, Salama AAK, Albanell E, Such X, Caja G (2013) Physiological responses and lactational performances of late-lactation dairy goats under heat stress conditions. J Dairy Sci 96(10):6355–6365. 10.3168/jds.2013-666523958010
Hanafi SA Zulkifli I Ramiah SK Chung ELT Awad EA Sazili AQ Prenatal thermal stress affects acute-phase proteins, heat shock protein 70, and circulating corticosterone in developing broiler embryos and neonates J Therm Biol 2022 109 103328 10.1016/j.jtherbio.2022.103328 36195399
Hanafi SA, Zulkifli I, Ramiah SK, Chung ELT, Awad EA, Sazili AQ (2022) Prenatal thermal stress affects acute-phase proteins, heat shock protein 70, and circulating corticosterone in developing broiler embryos and neonates. J Therm Biol 109:103328. 10.1016/j.jtherbio.2022.10332836195399
Hooper HB dos Santos Silva P de Oliveira SA Merighe GKF Negrão JA Acute heat stress induces changes in physiological and cellular responses in Saanen goats Int J Biometeorol 2018 62 12 2257 2265 10.1007/s00484-018-1630-3 30368674
Hooper HB, dos Santos Silva P, de Oliveira SA, Merighe GKF, Negrão JA (2018) Acute heat stress induces changes in physiological and cellular responses in Saanen goats. Int J Biometeorol 62(12):2257–2265. 10.1007/s00484-018-1630-330368674
Jackson P, Cockcroft P (2008) Clinical examination of farm animals. Wiley, Newark
Kandasami R Sangameswaran R Rajesh G Loganathasamy K Effect of summer heat stress on physiological and haemato-biochemical characters in Kanni ADU and Kodi ADU Goat breeds of Tamil Nadu Indian J Small Ruminants (the) 2023 29 1 50 54 10.5958/0973-9718.2023.00025.9
Kandasami R, Sangameswaran R, Rajesh G, Loganathasamy K (2023) Effect of summer heat stress on physiological and haemato-biochemical characters in Kanni ADU and Kodi ADU Goat breeds of Tamil Nadu. Indian J Small Ruminants 29(1):50–54. 10.5958/0973-9718.2023.00025.9
Kandemir Ç Kosum N Taskın T The effects of heat stress on physiological traits in sheep Macedonian J Anim Sci 2013 3 25 29 10.54865/mjas1331025k
Kandemir Ç, Kosum N, Taskın T (2013) The effects of heat stress on physiological traits in sheep. Macedonian J Anim Sci 3:25–29
Kaushik R, Arya A, Kumar D, Goel A, Rout PK (2023) Genetic studies of heat stress regulation in goat during hot climatic condition. J Therm Biol 103528. 10.1016/j.jtherbio.2023.103528
Khalifa HH, Shalaby T, Abdel Khalek TM (2005) An approach to develop a biometeorological thermal discomfort index for sheep and goats under Egyptian conditions. In: Proceeding of the 17th International Congress of Biometeorology. Garmisch, Germany. pp 118–122
Kumar D Yadav B Choudhury S Kumari P Madan AK Singh SP Yadav S Evaluation of adaptability to different seasons in goat breeds of semi-arid region in India through differential expression pattern of heat shock protein genes Biol Rhythm Res 2018 49 3 466 478 10.1080/09291016.2017.1377984
Kumar D, Yadav B, Choudhury S, Kumari P, Madan AK, Singh SP, Yadav S (2018) Evaluation of adaptability to different seasons in goat breeds of semi-arid region in India through differential expression pattern of heat shock protein genes. Biol Rhythm Res 49(3):466–478. 10.1080/09291016.2017.1377984
Lima ARC, Silveira RMF, Castro MSM, De Vecchi LB, da Fernandes MHMR, Resende KT (2022) Relationship between thermal environment, thermoregulatory responses and energy metabolism in goats: a comprehensive review. J Therm Biol 103324. 10.1016/j.jtherbio.2022.103324
Phulia SK Upadhyay RC Jindal SK Misra RP Alteration in surface body temperature and physiological responses in Sirohi goats during day time in summer season Indian J Anim Sci 2010 80 4 340 342
Phulia SK, Upadhyay RC, Jindal SK, Misra RP (2010) Alteration in surface body temperature and physiological responses in Sirohi goats during day time in summer season. Indian J Anim Sci 80(4):340–342
Pinto S Hoffmann G Ammon C Amon B Heuwieser W Halachmi I Amon T Influence of barn climate, body postures and milk yield on the respiration rate of dairy cows Annals Anim Sci 2019 19 2 469 481 10.2478/aoas-2019-0006
Pinto S, Hoffmann G, Ammon C, Amon B, Heuwieser W, Halachmi I, Amon T (2019) Influence of barn climate, body postures and milk yield on the respiration rate of dairy cows. Annals Anim Sci 19(2):469–481. 10.2478/aoas-2019-0006
Rhoads ML Rhoads RP VanBaale MJ Collier RJ Sanders SR Weber WJ Baumgard LH Effects of heat stress and plane of nutrition on lactating Holstein cows: I. Production, metabolism, and aspects of circulating somatotropin J Dairy Sci 2009 92 5 1986 1997 10.3168/jds.2008-1641 19389956
Rhoads ML, Rhoads RP, VanBaale MJ, Collier RJ, Sanders SR, Weber WJ, Baumgard LH (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(5):1986–1997. 10.3168/jds.2008-164119389956
Saipin N Semsirmboon S Rungsiwiwut R Thammacharoen S High ambient temperature directly decreases milk synthesis in the mammary gland in Saanen goats J Therm Biol 2020 94 102783 10.1016/j.jtherbio.2020.102783 33292975
Saipin N, Semsirmboon S, Rungsiwiwut R, Thammacharoen S (2020) High ambient temperature directly decreases milk synthesis in the mammary gland in Saanen goats. J Therm Biol 94:102783. 10.1016/j.jtherbio.2020.10278333292975
Salem HM, Alqhtani AH, Swelum AA, Babalghith AO, Melebary SJ, Soliman SM, Abd El-Hack ME (2022) Heat stress in poultry with particular reference to the role of probiotics in its amelioration: an updated review. J Therm Biol 103302. 10.1016/j.jtherbio.2022.103302
Sano H Ambo K Tsuda T Blood glucose kinetics in whole body and mammary gland of lactating goats exposed to heat J Dairy Sci 1985 68 10 2557 2564 10.3168/jds.S0022-0302(85)81137-1 4067034
Sano H, Ambo K, Tsuda T (1985) Blood glucose kinetics in whole body and mammary gland of lactating goats exposed to heat. J Dairy Sci 68(10):2557–2564. 10.3168/jds.S0022-0302(85)81137-14067034
SAS (1999) Statistical analysis system. User’s guide: statistics. SAS Institute, Inc., Cary
Sevi A Annicchiarico G Albenzio M Taibi L Muscio A Dell’Aquila S Effects of solar radiation and feeding time on behavior, immune response and production of lactating ewes under high ambient temperature J Dairy Sci 2001 84 3 629 640 10.3168/jds.S0022-0302(01)74518-3 11286417
Sevi A, Annicchiarico G, Albenzio M, Taibi L, Muscio A, Dell’Aquila S (2001) Effects of solar radiation and feeding time on behavior, immune response and production of lactating ewes under high ambient temperature. J Dairy Sci 84(3):629–640. 10.3168/jds.S0022-0302(01)74518-311286417
Shwartz G Rhoads ML VanBaale MJ Rhoads RP Baumgard LH Effects of a supplemental yeast culture on heat-stressed lactating holstein cows J Dairy Sci 2009 92 3 935 942 10.3168/jds.2008-1496 19233786
Shwartz G, Rhoads ML, VanBaale MJ, Rhoads RP, Baumgard LH (2009) Effects of a supplemental yeast culture on heat-stressed lactating holstein cows. J Dairy Sci 92(3):935–942. 10.3168/jds.2008-149619233786
Soriani N Panella G Calamari LUIGI Rumination time during the summer season and its relationships with metabolic conditions and milk production J Dairy Sci 2013 96 8 5082 5094 10.3168/jds.2013-6620 23791488
Soriani N, Panella G, Calamari LUIGI (2013) Rumination time during the summer season and its relationships with metabolic conditions and milk production. J Dairy Sci 96(8):5082–5094. 10.3168/jds.2013-662023791488
Srivastava A Yadav P Mahajan A Anand M Yadav S Madan AK Yadav B Appropriate THI model and its threshold for goats in semi-arid regions of India J Therm Biol 2021 96 102845 10.1016/j.jtherbio.2021.102845 33627282
Srivastava A, Yadav P, Mahajan A, Anand M, Yadav S, Madan AK, Yadav B (2021) Appropriate THI model and its threshold for goats in semi-arid regions of India. J Therm Biol 96:102845. 10.1016/j.jtherbio.2021.10284533627282
Xue L Zhou S Wang D Zhang F Li J Cai L The low dose of Saccharomyces cerevisiae is Beneficial for Rumen Fermentation (both in Vivo and in Vitro) and the growth performance of heat-stressed goats Microorganisms 2022 10 10 1877 10.3390/microorganisms10101877 36296154
Xue L, Zhou S, Wang D, Zhang F, Li J, Cai L (2022) The low dose of Saccharomyces cerevisiae is beneficial for rumen fermentation (both in vivo and in vitro) and the growth performance of heat-stressed goats. Microorganisms 10(10):1877. 10.3390/microorganisms1010187736296154
Yadav B Singh G Wankar A Adaptive capability as indicated by redox status and endocrine responses in crossbred cattle exposed to thermal stress J Anim Res 2015 5 1 67 73 10.5958/2277-940X.2015.00011.X
Yadav B, Singh G, Wankar A (2015) Adaptive capability as indicated by redox status and endocrine responses in crossbred cattle exposed to thermal stress. J Anim Res 5(1):67–73. 10.5958/2277-940X.2015.00011.X
Yilmaz M Altin T Kiral F Taskin T Asici GSE Kizilkaya K Effects of the season on physiological and endocrine traits and on HSP70 in Saanen goats under Mediterranean climate conditions Med Weter 2018 74 1 39 47 10.21521/mw.5834
Yilmaz M, Altin T, Kiral F, Taskin T, Asici GSE, Kizilkaya K (2018a) Effects of the season on physiological and endocrine traits and on HSP70 in Saanen goats under Mediterranean climate conditions. Med Weter 74(1):39–47. 10.21521/mw.5834
Yilmaz M, Kayki M, AŞICI GSE, Kiral F (2018b) The mRNA gene expression profiles for Hsp60 and Hsp70 in various aged Saanen goats in different seasons. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 24(1). 10.9775/kvfd.2017.18369
Zimbelman RB, Collier RJ, Eastridge ML (2011) Feeding strategies for high-producing dairy cows during periods of elevated heat and humidity. In Tri-State Dairy Nutrition Conference, Grand Wayne Center (pp. 111–126)
