Abstract
The aim of this study was to determine the effects of 6 h/day cold (35.0 °C) acclimatization between the 9th and 15th days of incubation of Japanese quail embryos on hatchability, livability, chick quality, developmental stability, fear response, live weight, and slaughter-carcass characteristics. Two homologous incubators and a total of 500 hatching eggs were used in the study. Randomly selected half of the eggs were exposed to cold according to the eggshell temperature. The cold acclimation of Japanese quail embryos had no adverse effects on all mentioned traits, except for chick quality. Chicks in the control group had higher Tona scores (99.46) than those exposed to cold (99.00) (P < 0.05). In addition, there were differences among the treatment groups in terms of the parameters of mature weight (β0), instantaneous growth rate (β2), and inflection point coordinates of the Gompertz growth model (P < 0.05 for all). It was found that exposing embryos to cold during the incubation changed the shape of the growth curve. As the development of embryos exposed to cold slows down, a compensatory growth occurs in the early posthatch period. Thus, the growth rate increased in the period before the inflection point of the growth curve.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Interested readers can get it by special request from the authors.
References
Afsarian O, Shahir MH, Akhlaghi A, Lotfolahian H, Hoseini A, Lourens A (2016) Periodical low eggshell temperatures during incubation and post hatch dietary arginine supplementation: effects on performance and cold tolerance acquisition in broilers. Poult Sci J 95:2427–2434. https://doi.org/10.3382/ps/pew193
Afsarian O, Shahir MH, Lourens A, Akhlaghi A, Lotfolahian H, Hoseini A, Mousavi N (2018) Eggshell temperature manipulations during incubation and in ovo injection of thyroxine are associated with a decreased incidence of cold-induced ascites in broiler chickens. Poult Sci 97(1):328–336. https://doi.org/10.3382/ps/pex302
Akbaş Y, Oğuz I (1998) Growth curve parameters of lines of Japanese quail (Coturnix coturnix japonica), unselected and selected for four-week body weight. Archiv Fuer Gefluegelkunde 62(3):104–109
Akşit M, Yalçın S, Siegel PB, Yenisey Ç, Özdemir D, Özkan S (2013) Broilers respond to cooler ambient temperatures after temperature acclimation during incubation and early postnatal age. J Appl Poultry Res 22(2):298–307. https://doi.org/10.3382/japr.2012-00675
Alkan S, Narinç D, Karslı T, Karabağ K, Balcıoğlu MS (2012) Effects of thermal manipulations during early and late embryogenesis on growth characteristics in Japanese quails (Coturnix cot japonica). Archiv für Geflügelkunde 76(3):184–190. https://doi.org/10.7482/0003-9438-56-078
Babacanoğlu E, Güler HC, Yalçın S (2006) Effect of timing of acclimation of broiler breeder eggs during incubation on embryo and chick development. In Proceeding Book of XII European Poultry Conference, Verona, Italy, 10–14 September 2010, p 482
Baghbanzadeh A, Decuypere E (2008) Ascites syndrome in broilers: physiological and nutritional perspectives. Avian Pathol 37(2):117–126. https://doi.org/10.1080/03079450801902062
Benoff FH, Siegel PB (1976) Genetic analysis of tonic immobility in young Japanese quail (Coturnix cotunix japonica). Anim Learn Behav 4(2):160–162. https://doi.org/10.3758/bf03214027
Bonos EM, Christaki EV, Florou-Paneri PC (2010) Performance and carcass characteristics of Japanese quail as affected by sex or mannan oligosaccharides and calcium propionate. S Afr J Anim Sci 40(3):173–184. https://doi.org/10.4314/sajas.v40i3.2
Brannan KE, Livingston ML, Wall B, Livingston KA, van Rensburg CJ (2021) Embryonic thermal manipulation and dietary fat source during acute heat stress: 2. Effect on broiler carcass characteristics and breast muscle myopathies. J Appl Poult Res 30(3):100174. https://doi.org/10.1016/j.japr.2021.100174
Decuypere E (1984) Incubation temperature in relation to postnatal performance in chickens. Archiv Fur Experimentelle Veterinarmedizin 38(3):439–449
Flores R, Penna M, Wingfield JC, Cuevas E, Vásquez RA, Quirici V (2019) Effects of traffic noise exposure on corticosterone, glutathione and tonic immobility in chicks of a precocial bird. Conserv Physiol 7(1):coz061. https://doi.org/10.1093/conphys/coz061
Geers R, Michels H, Nackaerts G, Konings F (1983) Metabolism and growth of chickens before and after hatch in relation to incubation temperatures. Poult Sci 62(9):1869–1875. https://doi.org/10.3382/ps.0621869
Halle I, Tzschentke B, Henning M, Köhler P (2012) Influence of temperature stimulation during the last 6 days of incubation on hatching results and later performance in Pekin ducks. Archiv Für Geflügelkunde 76(3):176–183. https://doi.org/10.1080/00071660903186570
Joseph NS, Lourens A, Moran ET Jr (2006) The effects of suboptimal eggshell temperature during incubation on broiler chick quality, live performance, and further processing yield. Poult Sci 85(5):932–938. https://doi.org/10.1093/ps/85.5.932
Kaplan S, Gürcan EK (2018) Comparison of growth curves using non-linear regression function in Japanese quail. J Appl Anim Res 46(1):112–117. https://doi.org/10.1080/09712119.2016.1268965
Karabağ K, Alkan S, Karslı T, Balcıoğlu MS (2017) Genetic changes in growth curve parameters in Japanese quail lines divergently selected for body weight. Eur Poult Sci 81(1):1–10. https://doi.org/10.1399/eps.2017.205
Kühn ER, Decuypere E, Colen LM, Michels H (1982) Posthatch growth and development of a circadian rhythm for thyroid hormones in chicks incubated at different temperatures. Poult Sci 61(3):540–549. https://doi.org/10.3382/ps.0610540
Lotfi E, Zerehdaran S, Azari MA (2011) Genetic evaluation of carcass composition and fat deposition in Japanese quail. Poult Sci 90(10):2202–2208. https://doi.org/10.3382/ps.2011-01570
Lourens A, Van den Brand H, Meijerhof R, Kemp B (2005) Effect of eggshell temperature during incubation on embryo development, hatchability, and posthatch development. Poult Sci 84(6):914–920. https://doi.org/10.1093/ps/84.6.914
Miri B, Ghasemi HA, Hajkhodadadi I, Farahani AHK (2022) Effects of low eggshell temperatures during incubation, in ovo feeding of L-arginine, and posthatch dietary guanidinoacetic acid on hatching traits, performance, and physiological responses of broilers reared at low ambient temperature. Poult Sci 101:101548. https://doi.org/10.1016/j.psj.2021.101548
Molenaar R, Van den Anker I, Meijerhof R, Kemp B, Van den Brand H (2011) Effect of eggshell temperature and oxygen concentration during incubation on the developmental and physiological status of broiler hatchlings in the perinatal period. Poult Sci 90(6):1257–1266. https://doi.org/10.3382/ps.2010-00684
Moraes VMB, Malheiros RD, Bruggeman V, Collin A, Tona K, Van As P, Onagbesan OM, Buyse J, Decuypere E, Macari (2003) Effect of thermal conditioning during embryonic development on aspects of physiological responses of broilers to heat stress. J Therm Biol 28(2):133–140. https://doi.org/10.1016/S0306-4565(02)00049-9
Narinç D, Aksoy T (2012) Effects of mass selection based on phenotype and early feed restriction on the performance and carcass characteristics in Japanese quails. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 18(3):425–430. https://doi.org/10.9775/kvfd.2011.5619
Narinç D, Aydemir E (2021) Chick quality: an overview of measurement techniques and influencing factors. Worlds Poult Sci J 77(2):313–329. https://doi.org/10.1080/00439339.2021.1892469
Narinç D, Genç BA (2021) Genetic parameter estimates of fear, growth, and carcass characteristics in Japanese quail. Turkish J Vet Anim Sci 45(2):272–280. https://doi.org/10.3906/vet-2007-43
Narinç D, Sabuncuoğlu K (2022) Comparison of growth and developmental stability traits of japanese quails reared in conventional and enriched cages. Ankara Üniversitesi Veteriner Fakültesi Dergisi 69:33–41. https://doi.org/10.33988/auvfd.796045
Narinç D, Karaman E, Fırat MZ, Aksoy T (2010) Comparison of non-linear growth models to describe the growth in Japanese quail. J Anim Vet Adv 9(14):1961–1966. https://doi.org/10.3923/javaa.2010.1961.1966
Narinç D, Karaman E, Aksoy T, Fırat MZ (2014a) Genetic parameter estimates of growth curve and reproduction traits in Japanese quail. Poult Sci 93(1):24–30. https://doi.org/10.3382/ps.2013-03508
Narinç D, Karaman E, Aksoy T (2014b) Effects of slaughter age and mass selection on slaughter and carcass characteristics in 2 lines of Japanese quail. Poult Sci 93(3):762–769. https://doi.org/10.3382/ps.2013-03506
Narinç D, Erdoğan S, Tahtabiçen E, Aksoy T (2016) Effects of thermal manipulations during embryogenesis of broiler chickens on developmental stability, hatchability and chick quality. Animal 10(8):1328–1335. https://doi.org/10.1017/s1751731116000276
Narinç D, Narinç NÖ, Aygün A (2017) Growth curve analyses in poultry science. Worlds Poult Sci J 73(2):395–408. https://doi.org/10.1017/S0043933916001082
Nichelmann M, Tzschentke B (2002) Ontogeny of thermoregulation in precocial birds. Comp Biochem Physiol a: Mol Integr Physiol 131(4):751–763. https://doi.org/10.1016/S1095-6433(02)00013-2
Nord A, Nilsson JA (2021) Low incubation temperature slows the development of cold tolerance in a precocial bird. J Exp Biol 224(1):jeb237743. https://doi.org/10.1242/jeb.237743
Nyuiadzi D, Berri C, Dusart L, Travel A, Méda B, Bouvarel I, Guilloteau LA, Chartrin P, Coustham V, Praud C, Le Bihan-Duval E, Tona K, Collin A (2020) Short cold exposures during incubation and postnatal cold temperature affect performance, breast meat quality, and welfare parameters in broiler chickens. Poult Sci 99(2):857–868. https://doi.org/10.1016/j.psj.2019.10.024
Özkan S, Plavnik I, Yahav S (2006) Effects of early feed restriction on performance and ascites development in broiler chickens subsequently raised at low ambient temperature. J Appl Poultry Res 15(1):9–19. https://doi.org/10.1093/japr/15.1.9
Özkan S, Malayoğlu HB, Yalçın S, Karadaş F, Koçtürk S, Cabuk M, Oktay G, Ozdemir S, Ozdemir E, Ergül M (2007) Dietary vitamin E (α-tocopherol acetate) and selenium supplementation from different sources: performance, ascites-related variables and antioxidant status in broilers reared at low and optimum temperatures. Br Poult Sci 48(5):580–593. https://doi.org/10.1080/00071660701593951
Piestun Y, Druyan S, Brake J, Yahav S (2013) Thermal manipulations during broiler incubation alter performance of broilers to 70 days of age. Poult Sci 92(5):1155–1163. https://doi.org/10.3382/ps.2012-02609
Shinder D, Rusal M, Giloh M, Yahav S (2009) Effect of repetitive acute cold exposures during the last phase of broiler embryogenesis on cold resistance through the life span. Poult Sci 88(3):636–646. https://doi.org/10.3382/ps.2008-00213
Swaddle JP, Witter MS (1997) On the ontogeny of developmental stability in a stabilized trait. Proc R Soc Lond Ser B: Biol Sci 264(1380):329–334. https://doi.org/10.1098/rspb.1997.0047
Tona K, Bamelis F, De Ketelaere B, Bruggeman V, Moraes VM, Buyse J, Onagbesan O, Decuypere E (2003) Effects of egg storage time on spread of hatch, chick quality, and chick juvenile growth. Poult Sci 82(5):736–741. https://doi.org/10.1093/ps/82.5.736
Veterany L, Hluchy S, Jedlıcka J, Cervenanova E (2005) Effect of the use of synthetic sound during incubation in chicken. J Agric Sci 50(2):131–138. https://doi.org/10.2298/JAS0502131V
Walita KZ, Tanganyika J, Mussah SR (2017) Effect of sex, type of feed and age at slaughter on carcass yield characteristics of Japanese quails (Coturnix Japonica) in Malawi. Int J Avian Wildl Biol 2(2):50–53. https://doi.org/10.15406/ijawb.2017.02.00015
Walstra I, Ten Napel J, Kemp B, Van Den Brand H (2010) Temperature manipulation during layer chick embryogenesis. Poult Sci 89(7):1502–1508. https://doi.org/10.3382/ps.2009-00568
Wijnen HJ, Van den Brand H, Lammers A, van Roovert-Reijrink IAM, van der Pol CW, Kemp B, Molenaar R (2020) Effects of eggshell temperature pattern during incubation on primary immune organ development and broiler immune response in later life. Poult Sci 99(12):6619–6629. https://doi.org/10.1016/j.psj.2020.09.088
Willemsen H, Kamers B, Dahlke F, Han H, Song Z, Pirsaraei ZA, Tona K, Decuypere E, Everaert N (2010) High-and low-temperature manipulation during late incubation: effects on embryonic development, the hatching process, and metabolism in broilers. Poult Sci 89(12):2678–2690. https://doi.org/10.3382/ps.2010-00853
Yahav S, Collin A, Shinder D, Picard M (2004) Thermal manipulations during broiler chick embryogenesis: effects of timing and temperature. Poult Sci 83(12):1959–1963. https://doi.org/10.1093/ps/83.12.1959
Yahav S, Tzschentke B (2006) Perinatal thermal manipulations in poultry, does it cause long-lasting thermo regulatory memory. Proceedings of the 12th European Poultry Conference, 10–14 September 2006, Verona, Italy
Yalçın S, Siegel PB (2003a) Developmental stability of broiler embryos in relation to length of egg storage prior to incubation. J Poult Sci 40(4):298–308. https://doi.org/10.2141/jpsa.40.298
Yalçın S, Siegel PB (2003b) Exposure to cold or heat during incubation on developmental stability of broiler embryos. Poult Sci 82(9):1388–1392. https://doi.org/10.1093/ps/82.9.1388
Yalçın S, Oğuz İ, Ötleş S (1995) Carcase characteristics of quail (Coturnix coturnix japonica) slaughtered at different ages. Br Poult Sci 1995 36(3):393–399. https://doi.org/10.1080/00071669508417786
Yalçın S, Settar P, Özkan S, Cahaner A (1997) Comparative evaluation of three commercial broiler stocks in hot versus temperate climates. Poult Sci 76(7):921–929. https://doi.org/10.1093/ps/76.7.921
Yalçın S, Özkan S, Çabuk M, Buyse J (2005) Pre-and postnatal conditioning induced thermotolerance on body weight, physiological responses and relative asymmetry of broilers originating from young and old breeder flocks. Poult Sci 84(6):967. https://doi.org/10.1093/ps/84.6.967
Yalçın S, Çabuk M, Bruggeman V, Babacanoğlu E, Buyse J, Decuypere E, Siegel PB (2008) Acclimation to heat during incubation: 3. Body weight, cloacal temperatures, and blood acid-base balance in broilers exposed to daily high temperatures. Poult Sci 87(12):2671–2677. https://doi.org/10.3382/ps.2008-00164
Yalçın S, Babacanoğlu E, Güler HC, Akşit M (2010) Effects of incubation temperature on hatching and carcass performance of broilers. Worlds Poult Sci J 66(1):87–94. https://doi.org/10.1017/S0043933910000097
Yalçın S, Özkan S, Siegel P, Yenisey C, Akşit M (2012) Manipulation of incubation temperatures to increase cold resistance of broilers: influence on embryo development, organ weights, hormones and body composition. J Poult Sci 49(2):133–139. https://doi.org/10.2141/jpsa.011117
Funding
This study was carried out with the support of the TUBITAK (The Scientific and Technological Research Council of Turkey) 2209A project.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interest.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Karakelle, H., Özçalişan, G., Şahin, F. et al. The effects of exposure to cold during incubation on developmental stability, fear, growth, and carcass traits in Japanese quails. Int J Biometeorol 67, 1303–1310 (2023). https://doi.org/10.1007/s00484-023-02497-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-023-02497-1