Genetic Variation in Heat Tolerance and Immunocompetence of Chickens Raised in Nigeria

Received 06 Jan, 2023

Accepted 06 Jun, 2023

Published 30 Sep, 2023

Background and Objective: Knowledge of genetic variations in heat tolerance and immunocompetence between different strains is imperative in genetic selection and enhancement of natural disease resistance in the tropics. Hence, this study compared Nera Black, Dominant Blue and Nigerian indigenous chicken strains. Materials and Methods: Heat tolerance was evaluated by measuring the pulse rate, respiratory rate, rectal temperature and heat stress index of the birds. Blood analysis was carried out to determine the blood differentials of the birds. A haemagglutination inhibition (HA/HI) test on blood samples from the birds before and after antigenic challenge with newcastle disease virus (NDV) was used to evaluate immunocompetence. Results: Nera Black had the highest means for heat tolerance traits while the Nigerian indigenous had the least. Sex significantly (p<0.05) influenced all heat tolerance traits except rectal temperature. Genotype had a significant (p<0.05) effect on the blood parameters with mean values for heterophil percentage, heterophil/lymphocyte ratio and monocyte percentage lowest for the Nigerian indigenous. The Nigerian indigenous had the highest postvaccination titer mean. Conclusion: From this study, the Nigerian indigenous chickens had higher heat tolerance and immunocompetence and were therefore better adapted to the tropics than the exotic birds studied.

INTRODUCTION

Poultry is one of the largest agricultural businesses in Nigeria, which has undergone an enormous expansion and development over time^1,2. However, heat stress is one of the most serious factors affecting overall poultry production in the tropics and diseases are big causes of loss in the poultry industry^3,4.

High environmental temperatures have deleterious effects on poultry, reducing the rate of growth, feed intake and nutrient digestibility, increasing mortality and reducing immunity^5-8. The coordination of all the systems under thermal stress is different between species and also between breeds⁹, thereby providing a possibility to select for heat tolerance¹⁰.

In the same vein, knowledge of differences in disease resistance between different strains may be valuable in genetic selection programs¹¹. Characterization and evaluation of immune parameters in various genotypes can help in enhancing natural disease resistance in tropical and subtropical environments¹².

This study was a comparative analysis of three strains of chickens in Nigeria in terms of their abilities to tolerate heat and provide natural immunity against the Newcastle disease virus.

MATERIALS AND METHODS

Experimental birds: A total of 96 birds were used for the experiment. Day-old chicks of the Nigerian indigenous chicken were obtained from the crossing of the parent stock of pure naked neck, pure normal-feathered and pure frizzle-feathered birds maintained at the Poultry Breeding Unit of the University of Agriculture, Abeokuta, while the day-old chicks of Nera Black and Dominant Blue were purchased from a commercial parent-stock breeding farm. The chicks were wing-tagged right from the hatchery. The experiment lasted between June and December, 2009.

Experimental location: The fieldwork was conducted at the Poultry Breeding Unit of the Teaching and Research Farm of the Federal University of Agriculture, Abeokuta (FUNAAB), Nigeria. Blood analysis was carried out at the Microbiology Laboratory of the College of Veterinary Medicine, FUNAAB.

Management and feeding: All chicks were subjected to the same controlled environment with conventional ventilation. Wood shaving litter was used at 3-5 cm thickness. Indoor ambient temperature was started at 34°C and then gradually decreased till the end of brooding.

At the brooder phase (0-6 weeks), the chick starter ration containing 21% crude protein and 10.88 MJ kg^–1 metabolisable energy was fed to the chicks while at the grower phase (7-12 weeks), growers mash containing 15% crude protein and 10.46 MJ kg^–1 metabolisable energy was fed to them.

Data collection
Heat tolerance traits: Rectal temperature was measured by inserting a clinical thermometer into the vent of each bird for 1 min and then taking the reading. To get the pulse rate, a stethoscope was placed under the wing vein to count the number of pulses for 15 sec. The obtained value was then multiplied by 4 to get beats/min. Respiratory rate was determined by placing the fingertips under the wing vein and counting the number of beats per minute using a stopwatch¹³. The measurements were done weekly for 20 weeks. The readings were taken twice, the averages were computed and recorded.

Heat stress index: The heat stress index was evaluated using the relationship between pulse rate and respiratory rate, with their normal averages as shown¹⁴:

Where:

	H	=	Heat stress index
	AR	=	Average respiratory rate value
	AP	=	Average pulse value
	NP	=	Normal pulse rate value
	NR	=	Normal respiratory rate

Blood parameters for heat tolerance: At 17 weeks of age, about 5 mL of blood was collected from each of the birds from the three strains, through the wing vein, 2 mL of which was dispensed into a clean Bijou bottle containing an anticoagulant (Ethylenediaminetetraacetic acid (EDTA)) and labeled accordingly. The un-coagulated blood was used to determine heterophils, lymphocytes, monocytes, basophils and eosinophils counts, using standard laboratory procedures. The heterophil/lymphocyte ratio was calculated from their counts. Serum was obtained from the remaining 3 mL of blood, from which potassium and sodium were also determined.

Blood parameters for immune response: At 17 weeks of age, blood samples were taken from the three strains. Newcastle disease vaccine (NDV) was then administered to the birds the same day. As 3 weeks later, blood samples were collected from the birds again. Both the pre-vaccination blood samples and the post-vaccination samples were analyzed for the HA/HI antibody titer.

Statistical analyses: Heat tolerance traits and blood parameters measured involved both sexes, male and female. The statistical model that was used therefore accommodated the effects of sex, genotype and their interaction. The model was as follows:

Y_ijk = μ+G_i+X_j+(GX)_ij+E_ijk

Where:

	Yijk	=	Observed value of the measurable traits of the jth sex on the ith genotype
	μ	=	Overall mean
	Gi	=	Effect of the ith genotype (i = 1,2,3)
	Xj	=	Effect of the jth sex (j = 1,2)
	(GX)ij	=	Effect of the interaction of the ith genotype and the jth sex
	Eijk	=	Er or independently and identically distributed as normal with mean zero and constant variance

The data were analyzed using the General Linear Model of SAS 9.0 while Duncan’s Multiple Range Test was used for separating the means¹⁵. The results are presented as Means±Standard Error (SE), at a 5% level of significance.

RESULTS AND DISCUSSION

The Nigerian indigenous strain had the least rectal temperature while the Nera Black had the highest (Table 1). The observed significant differences in rectal temperature agreed with the report by Finch¹⁶ that there were notable differences between breeds in their abilities to regulate rectal temperature at normal environmental conditions. It was, however, observed that the rectal temperatures were within a specific range (39.41-39.98°C) among all three strains. Heat production is affected by body weight, specie/breed, production, feed intake, feed quality and activity/exercise^7,17.

The highest mean values for respiratory rate were observed among the Nera Black chickens, with the peak at the 12th week. As Robert¹⁸ pointed out, the size of the animal affects the respiratory rate. As ambient temperature increases, the autonomic nervous system of birds triggers increased heartbeat (tachycardia), accompanied by an increase in respiratory rates, which helps in maintaining their body temperature^3,8,19.

The Nigerian indigenous chickens had the lowest mean value for pulse rate throughout the period of the study. This could be attributed to the fact that Nigerian indigenous chickens have been reported to be well-adapted to tropical and subtropical environmental conditions due to the accumulation of genes for adaptability through natural selection¹. Fayeye et al.²⁰ reported that the feather distribution gene and the feather structure gene, which are found among the local birds, were also associated with increased heat tolerance.

Table 1:

Least squares mean and standard errors for heat tolerance traits as affected by the genotype of chickens

Age (weeks)	Genotype	Number	Rectal temperature (°C)	Pulse rate (beats min–1)	Respiratory rate (breaths min–1)	Heat stress index
1	Dom. Blue	29	40.11±0.08b	311.60±2.8c	39.53±0.9a	1.19±0.02b
	Nig. Indig.	32	39.41±0.14c	309.16±1.6b	35.76±0.4b	1.17±0.01b
	Nera Black	35	40.87±0.07a	317.90±2.1a	42.86±0.4a	1.22±0.01a
4	Dom. Blue	29	39.95±0.09b	307.93±2.8c	36.20±0.6a	1.19±0.01a
	Nig. Indig.	32	39.35±0.18c	303.42±1.6b	31.29±0.3b	1.16±0.01b
	Nera Black	35	40.24±0.14a	310.67±1.2a	38.24±0.2a	1.20±0.01a
8	Dom. Blue	29	40.02±0.11b	303.66±2.7b	35.07±0.8a	1.19±0.03a
	Nig. Indig.	32	39.40±0.09b	298.53±1.9a	31.47±0.4b	1.13±0.02b
	Nera Black	35	40.98±0.07a	308.19±1.4a	39.30±0.3a	1.16±0.01ab
12	Dom. Blue	29	40.08±0.13b	324.73±2.9b	38.13±0.7a	1.17±0.04b
	Nig. Indig.	32	39.42±0.08b	313.63±1.8a	34.66±0.4a	1.13±0.01c
	Nera Black	35	40.65±0.14a	339.07±1.5ab	45.01±0.3a	1.20±0.01a
16	Dom. Blue	29	39.99±0.30b	318.40±2.8b	36.03±0.7a	1.15±0.03c
	Nig. Indig.	32	39.31±0.11c	306.37±1.5a	30.92±0.4b	1.16±0.01b
	Nera Black	35	40.33±0.08a	325.65±1.6a	40.07±0.2b	1.22±0.01a
20	Dom. Blue	29	39.82±0.16b	314.67±4.6b	34.67±0.7a	1.15±0.03b
	Nig. Indig.	32	39.24±0.07c	308.00±4.7a	30.68±0.4a	1.10±0.01c
	Nera Black	35	40.18±0.13a	320.09±2.3b	38.63±0.2a	1.17±0.01a
a,b,cMeans in the same column with different superscripts are significantly different (p<0.05)

Table 2:

Least squares mean and standard errors for heat tolerance traits as affected by sex

Age (weeks)	Sex	Number	Rectal temperature (°C)	Pulse rate (beats min–1)	Respiratory rate (breaths min–1)	Heat Stress Index
1	Male	39	39.82±0.16a	308.11±2.83b	32.58±0.90b	1.18±0.03b
	Female	57	40.15±0.10a	315. 89±1.58a	38.33±0.3a	1.22±0.01a
4	Male	39	39.75±0.27a	305.20±1.19b	30.20±0.67b	1.17±0.02b
	Female	57	40.02±0.10a	310.01±1.20a	36.78±0.20a	1.21±0.01a
8	Male	39	39.73±0.12a	298.35±2.63b	30.60±0.54b	1.14±0.02a
	Female	57	39.98±0.05a	309.34±1.40a	38.34±0.26a	1.15±0.01a
12	Male	39	39.88±0.22a	307.36±1.69b	34.78±0.70b	1.14±0.02a
	Female	57	40.31±0.12a	313.03±1.32a	39.45±0.23a	1.16±0.01a
16	Male	39	39.80±0.09a	304.40±1.87b	33.21±0.09a	1.15±0.02a
	Female	57	40.07±0.06a	310.23±1.28a	36.76±0.22a	1.19±0.03a
20	Male	39	39.75±0.19a	300.02±2.43a	30.54±0.53b	1.13±0.02a
	Female	57	39.94±0.12a	305.43±1.80a	34.45±0.24a	1.18±0.01b
a,bMeans in the same age in the same column with different superscripts are significantly different (p<0.05)

The Nera Black had the highest means for all heat tolerance traits measured throughout the period of the experiment. This indicated a sign of susceptibility to heat stress⁸. The mean values for all the strains were high in the 1st week of life, however, the highest mean was at week 12. The fluctuation in pulse rate can be associated with factors like temperature, disease conditions or intense activity by the animal²¹.

Heat stress index is defined as a function of the deviation of actual temperature from target environmental temperature and bird age²². The higher the index, the more stressed the bird²³. The Nera Black had the highest mean value, making them the most stressed of the other genotypes while the Nigerian indigenous chickens had the least, making them the least stressed. The highest heat stress index was observed at week 1, which decreased with age, an indication of adaptation to tropical environment as they advanced in age. The observed pattern of heat tolerance traits among the chicken strains is similar to that reported by Lara and Rostagno²⁴.

Sex was found to have no significant effect on rectal temperature, though the males had lower values than the females throughout the experimental period (Table 2). However, there was a significant difference between sexes for pulse rate, respiratory rate and heat stress index. This also agreed with the report of the University of Illinois Extension aforementioned. Adedeji et al.²⁵ reported a significant (p<0.05) effect among the sexes of pure and crossbred chicken progenies in response to heat tolerance traits, with the females having higher responses compared to their male counterparts.

Table 3:

Least squares mean and standard error for heat tolerance traits as affected by the interaction of genotype and sex of chickens

Age (weeks)	Gen×Sex	Rectal temperature (°C)	Pulse rate (beats min–1)	Resp rate (breaths min–1)	Heat stress index
1	Dom. Blue male	39.68±0.28bc	306.87±0.12ab	32.13±0.27bc	1.17±0.08b
	Dom. Blue female	40.22±0.32ab	316.22±0.85ab	36.86±0.17ab	1.22±0.07a
4	Local male	39.43±0.21bc	301.08±0.14b	30.82±0.19c	1.16±0.02b
	Local female	39.97±0.23bc	310.94±0.17ab	33.04±0.13bc	1.18±0.03b
	Nera male	40.12±0.43ab	308.48±0.33ab	39.10±0.15a	1.16±0.08b
	Nera female	41.02±0.21a	326.38±0.08a	42.23±0.13a	1.15±0.07b
	Dom. Blue male	39.62±0.11ab	301.67±0.48b	31.23±0.61bc	1.18±0.09a
	Dom. Blue female	40.18±0.18ab	318.79±0.22a	35.03±0.26ab	1.20±0.01a
8	Local male	39.32±0.23a	296.75±0.27c	30.03±2.10c	1.13±0.06b
	Local female	39.78±0.11b	302.68±0.16b	33.57±0.21b	1.16±0.05b
	Nera male	40.32±0.12a	306.37±0.30b	33.45±0.26b	1.18±0.05b
	Nera female	40.89±0.19a	321.28±0.19a	39.10±0.24a	1.24±0.12a
	Dom. Blue male	39.58±0.27b	312.77±0.44ab	32.70±0.26b	1.13±0.18b
	Dom. Blue female	40.26±0.31ab	318.49±0.72a	35.11±0.32ab	1.17±0.09ab
12	Local male	39.42±0.21b	295.20±0.81b	29.75±0.21c	1.13±0.09b
	Local female	39.63±0.92b	309.02±0.29ab	31.88±0.20b	1.15±0.05b
	Nera male	40.14±0.12ab	311.18±0.46a	33.95±0.21ab	1.17±0.12b
	Nera female	41.32±0.12a	316.29±0.76a	34.52±0.22ab	1.23±0.20a
	Dom. Blue male	39.63±0.45b	307.83±0.65c	38.20±0.15a	1.16±0.14b
	Dom. Blue female	40.18±0.42ab	315.87±0.25b	35.86±0.41ab	1.18±0.08ab
16	Local male	39.37±1.23bc	305.82±0.76c	25.37±0.24c	1.11±0.09b
	Local female	39.59±0.18b	312.55±0.22b	32.18±0.18bc	1.14±0.12b
	Nera male	40.34±0.46ab	315.47±0.18b	32.32±0.11bc	1.18±0.14ab
	Nera female	40.93±0.48a	343.85±0.09a	38.88±0.24a	1.21±0.09a
	Dom. Blue male	39.45±0.87ab	308.47±0.20b	32.83±0.34ab	1.16±0.02b
	Dom. Blue female	39.89±0.88a	319.91±0.33ab	34.33±0.50ab	1.19±0.07ab
20	Local male	39.23±0.45b	300.16±0.25c	28.96±0.27c	1.14±0.09b
	Local female	39.38±0.34b	311.85±0.21b	30.73±0.18b	1.15±0.03b
	Nera male	39.97±0.45ab	319.58±0.32ab	33.97±0.22ab	1.21±0.03a
	Nera female	40.26±0.66a	328.66±0.16a	39.35±0.24a	1.23±0.11a
	Dom. Blue male	39.74±0.22ab	302.37±0.67bc	30.90±0.17b	1.14±0.19b
	Dom. Blue female	40.02±0.19a	318.54±0.43b	37.50±0.48a	1.17±0.21ab
	Local male	39.23±0.34b	298.50±0.24c	29.33±0.27b	1.09±0.05ab
	Local female	39.45±0.23b	308.31±0.19bc	33.98±0.18ab	1.12±0.17b
	Nera male	39.87±0.32ab	308.22±0.54bc	32.70±0.17ab	1.16±0.09ab
	Nera female	40.45±0.67a	322.76±0.15a	37.67±0.17a	1.19±0.22a
a,b,cMeans for the same ages in the same column with different superscripts are significantly different (p<0.05)

The sex by genotype interaction was significant on heat tolerance traits in agreement with the submission of Adedeji et al.²⁵, with the Nigerian indigenous males having the lowest means. The interaction of sex by genotype on rectal temperature (Table 3) brought out the effect that was masked when the sex effect alone was considered.

The means of blood parameters for the three strains were significantly different (Table 4). Lymphocyte and eosinophil counts were significantly higher in the local birds than in the other two strains. The ratio of heterophils to lymphocytes was also found to be significantly lower for the Nigerian indigenous chickens. It has been reported that differential leucocyte count and the H/L ratio are sensitive indicators of stress responses relevant to immune function^26,27. High heterophil counts and the H/L ratio have been related to stress²⁸. The above results, therefore, demonstrated higher heat tolerance in the Nigerian indigenous strain than the Nera Black and the Dominant Bluebirds in agreement with previous reports of the superiority of local strains in this regard²⁷. According to Maxwell and Robertson²⁹, eosinophils disappeared from circulation and basophils increased in circulation during stress, particularly acute stress. The higher the eosinophils and the lower the basophils, the more heat tolerant the bird is.

Table 4:

Least squares mean and standard errors of blood parameters as affected by the genotype of chicken

Genotype	K+	Na+	H (%)	L (%)	H/L	M (%)	B (%)	E (%)
Dom. Blue	4.1±0.07a	133.5±1.76a	28.8±0.88a	64.4±0.15b	0.44±0.05b	2.33±0.33a	2.32±0.02a	3.09±0.10b
Nig. Indig.	3.9±0.07a	133.5±0.5a	25.8±1.39b	67.2±1.11a	0.38±0.04c	2.36±0.33a	2.29±0.03a	3.32±0.50a
Nera Black	3.9±0.08a	134.5±0.88a	29.6±0.67a	63.5±0.67b	0.46±0.03a	2.30±0.11a	2.45±0.02a	3.03±0.67b
a,b,cMeans in the same column with different superscripts are significantly different (p<0.05), K+: Potassium ion concentration, Na+: Sodium ion concentration, H (%): Heterophil percentage, L (%): Lymphocyte percentage, H/L: Heterophil/lymphocyte ratio, M (%): Monocyte percentage, B (%): Basophil percentage and E (%): Eosinophil percentage

Table 5:

Least squares mean and standard errors for antibody titer as affected by the genotype of chickens

Genotype	Pre-vaccination titre (log 2)	Post-vaccination titre (log 2)
Dom. Blue	0.93±0.71a	4.12±0.59b
Nig. Indig.	1.50±0.51a	4.50±0.89a
Nera Black	0.87±0.46a	3.92±0.77b
a,bMeans in the same column with different superscripts are significantly different (p<0.05)

The means of the pre-vaccination and post-vaccination antibody titers as affected by the genotype of chickens were presented in Table 5. The means of the pre-vaccination titer were not significantly different. The means of post-vaccination antibody titer were significantly higher for the Nigerian indigenous strain while Dominant Blue and Nera Black were not significantly different in means.

This showed that the Nigerian indigenous birds generated a higher immune response to the newcastle diseases virus than the other two strains. The local chickens had been said to possess genes that are believed to confer not only adaptability to the tropical climate but also disease resistance^26,30. Alvarez et al.³¹ stated that the indigenous naked neck and normal-feathered chickens seem to have better immune responses than the commercial chicken line. There are many such reports which indicate that, in general, rural chickens are resistant to many endemic diseases and stressful environments and survive better than commercial chickens under rural conditions^27,31,32. The significant difference in the blood differentials did not only reveal heat tolerance level, but it was also a measure of immune function. Reports showed that leukocyte counts also had been used as a measure of immune function in studies on sexual selection in birds^32,33.

This study showed that differences in genotype accounted for variations in heat tolerance traits, rectal temperature, respiratory rate and pulse rate as well as variations in the blood parameters measured. It also revealed that the Nigerian indigenous local chickens have higher heat tolerance as well as a higher immune response to the Newcastle disease virus, thereby possessing greater adaptability for the tropical environment.

From this study, it can be recommended that the Nigerian indigenous chicken strains be used in the genetic improvement of heat tolerance and immunocompetence in commercial strains through cross-breeding. This will provide a low-cost solution that is easier to achieve in developing countries with hot climates and endemic diseases. Also, the indigenous birds can be developed into commercial lines by raising them intensively, thereby conserving the genes they possess as well as aiding future breeding endeavours.

A limitation of this study is the fact that it only compared three strains out of many and assessed resistance to only one disease out of several that are economically important in the tropics.

CONCLUSION

The major findings of this research are the superior performances of the Nigerian indigenous chickens in terms of heat tolerance and immunocompetence (especially against the newcastle disease virus). The Nigerian indigenous birds have not been given as much credit as they deserve. As observed from this study, they have an edge over the commercial strains studied when raised intensively in the tropics.

SIGNIFICANCE STATEMENT

It is essential to assess the adaptation of our local birds in comparison with the exotic raised within our climate. Hence this study compared the genetic variations in heat tolerance and immunocompetence of Nera Black, Dominant Blue and Nigerian indigenous chickens. The major findings of this research are the superior performances of the Nigerian indigenous chickens in terms of heat tolerance and immunocompetence (against the newcastle disease virus), which showed that they have an edge over the commercial strains studied when raised intensively in Nigeria and the tropics in general.

ACKNOWLEDGMENTS

The authors wish to acknowledge Dr. Paul Akinduti of Covenant University and Dr. Babatunde Moses Ilori of the Animal Breeding and Genetics Department, Federal University of Agriculture, Abeokuta, Nigeria, for their contributions to the success of the research.

REFERENCES

1. Padhi, M.K., 2016. Importance of indigenous breeds of chicken for rural economy and their improvements for higher production performance. Scientifica, 2016: 2604685.
2. Oladeji, J.O., 2011. Sources and utilization of poultry production information among poultry farmers in Oyo State. Int. J. Livest. Prod., 2: 11-16.
3. Nawaz, A.H., K. Amoah, Q.Y. Leng, J.H. Zheng, W.L. Zhang and L. Zhang, 2021. Poultry response to heat stress: Its physiological, metabolic, and genetic implications on meat production and quality including strategies to improve broiler production in a warming world. Front. Vet. Sci., 8: 699081.
4. Xu, Y., X. Lai, Z. Li, X. Zhang and Q. Luo, 2018. Effect of chronic heat stress on some physiological and immunological parameters in different breed of broilers. Poult. Sci., 97: 4073-4082.
5. Mills, W., R. Critcher, C. Lee and C.J. Farr, 1999. Generation of an ∼2.4 Mb human X centromere-based minichromosome by targeted telomere-associated chromosome fragmentation in DT40. Hum. Mol. Genet., 8: 751-761.
6. Naseem, M.T., S. Naseem, M. Younus, C.Z. Iqbal, A. Ghafoor, A. Aslam and S. Akhter, 2005. Effect of potassium chloride and sodium bicarbonate supplementation on thermotolerance of broilers exposed to heat stress. Int. J. Poult. Sci., 4: 891-895.
7. Pawar, S.S., S. Basavaraj, L.V. Dhansing, K.N. Pandurang and K.A. Sahebrao et al., 2016. Assessing and mitigating the impact of heat stress in poultry. Adv. Anim. Vet. Sci., 4: 332-341.
8. Wasti, S., N. Sah and B. Mishra, 2020. Impact of heat stress on poultry health and performances, and potential mitigation strategies. Animals, 10: 1266.
9. Silanikove, N., 2000. The physiological basis of adaptation in goats to harsh environments. Small Ruminant Res., 35: 181-193.
10. Nawaz, A.H., S. Lin, F. Wang, J. Zheng and J. Sun et al., 2023. Investigating the heat tolerance and production performance in local chicken breed having normal and dwarf size. Animal, 17: 100707.
11. Ilaya, B.D., M.G. Raj and P. Shamsudeen, 2016. Selection methods for disease resistance in poultry-An overview. Int. J. Sci. Environ. Technol., 5: 810-815.
12. El-Safty, S.A., U.M. Ali and M.M. Fathi, 2006. Immunological parameters and laying performance of naked neck and normally feathered genotypes of chicken under winter conditions of Egypt. Int. J. Poult. Sci., 5: 780-785.
13. Femi, O.J., T.O. Mariam, E.A. Henry, A.E. Yemi, A. Onaopemipo and K. Bello, 2023. Physiological indicators and stress index of scavenging chickens at lafarge (Ewekoro) and dangote (Ibese) cement factory areas of Ogun State. J. Austrian Soc. Agric. Econ., 19: 1679-1686.
14. Amevor, Y., D. Addison and J.K. Sosu, 2022. Comparative study on thermo-tolerant and estimated breeding values of four (4) strains of indigenous chicken in the sagnarigu municipality of Ghana. World J. Pharm. Life Sci., 8: 6-13.
15. Gomez, K.A. and A.A. Gomez, 1984. Statistical Procedures for Agricultural Research. 2nd Edn., John Wiley and Sons, New York, USA, ISBN-13: 9780471870920, Pages: 704.
16. Finch, V.A., 1986. Body temperature in beef cattle: Its control and relevance to production in the tropics. J. Anim. Sci., 62: 531-542.
17. Lyde, N.A., K.B.H. Wenceslas, F. Nambaté and A.G.A. Béatrice, 2018. Effect of genotype on morphometric traits and body temperature of three genotypes of chicken (Gallus gallus domesticus) raised in the humid tropical stressful environment. Int. J. Adv. Res., 5: 1489-1498.
18. Robert, A.V., 1994. Raising Healthy Goats Under Primitive Conditions. Christian Veterinary Mission, Lynnwood, Washington, United States, ISBN-10: 1886532044, Pages: 156.
19. Teyssier, J.R., G. Brugaletta, F. Sirri, S. Dridi and S.J. Rochell, 2022. A review of heat stress in chickens. Part II: Insights into protein and energy utilization and feeding. Front. Physiol., 13: 943612.
20. Fayeye, T.R., K.L. Ayorinde, V. Ojo and O.M. Adesina, 2006. Frequency and influence of some major genes on body weight and body size parameters of Nigerian local chickens. Livest. Res. Rural Dev., 18.
21. Bello, S.A., O.G. Akintunde, A.O. Sonibare and E.B. Otesile, 2016. Effect of sex, age and time of the day on vital parameters of apparently healthy west African dwarf goats in Abeokuta, Nigeria. Alexandria J. Vet. Sci., 49: 18-23.
22. Ryder, A.A., J.J.R. Feddes and M.J. Zuidhof, 2004. Field study to relate heat stress index to broiler performance. J. Appl. Poult. Res., 13: 493-499.
23. Wang, Y., P. Saelao, K. Chanthavixay, R. Gallardo and D. Bunn et al., 2018. Physiological responses to heat stress in two genetically distinct chicken inbred lines. Poult. Sci., 97: 770-780.
24. Lara, L.J. and M.H. Rostagno, 2013. Impact of heat stress on poultry production. Animal, 3: 356-369.
25. Adedeji, T.A., O.T. Aderoju,, A.M. Adebimpe and B. Matheuw, 2015. Genotype-sex interaction in relation to heat tolerance attributes of pure and crossbred chicken progenies. J. Biol. Agric. Healthcare, 5: 43-49.
26. Atansuyi, A.J., T.Z. Ogunribido and C.A. Chineke, 2019. Haematological and serum biochemical characteristics of four chicken genotypes in South-Western, Nigeria. Niger. J. Anim. Sci., 21: 9-16.
27. Shini, S., 2003. Physiological responses of laying hens to the alternative housing systems. Int. J. Poult. Sci., 2: 357-360.
28. El-Safty, S.A.R., 2012. Comparative study on some immunological traits in two different genetic groups of chicken. Vet. World, 5: 645-650.
29. Maxwell, M.H. and G.W. Robertson, 1998. The avian heterophil leucocyte: A review. World's Poult. Sci. J., 54: 155-178.
30. Haunshi, S., D. Sharma, L.M.S. Nayal, D.P. Singh and R.V. Singh, 2002. Effect of naked neck gene (NA) and frizzle gene (F) on immunocompetence in chickens. Br. Poult. Sci., 43: 28-32.
31. Alvarez, M.T., N. Ledesma, G. Téllez, J.L. Molinari and P. Tato, 2003. Comparison of the immune responses against Salmonella enterica serovar Gallinarum infection between naked neck chickens and a commercial chicken line. Avian Pathol., 32: 193-203.
32. Dufva, R. and K. Allander, 1995. Intraspecific variation in plumage coloration reflects immune response in great tit (Parus major) males. Funct. Ecol., 9: 785-789.
33. Johnsen, T.S. and M. Zuk, 1998. Parasites, morphology, and blood characters in male red jungle fowl during development. Condor, 100: 749-752.