Embryonic thermal manipulation has short and long-term effects on the development and the physiology of the Japanese quail

Abstract

In vertebrates, the embryonic environment is known to affect the development and the health of individuals. In broiler chickens, the thermal-manipulation (TM) of eggs during the incubation period was shown to improve heat tolerance at slaughter age (35 days of age) in association with several modifications at the molecular, metabolic and physiological levels. However, little is known about the Japanese quail (Coturnix japonica), a closely related avian species widely used as a laboratory animal model and farmed for its meat and eggs. Here we developed and characterized a TM procedure (39.5°C and 65% relative humidity, 12 h/d, from days 0 to 13 of incubation) in quails by analyzing its short and long-term effects on zootechnical, physiological and metabolic parameters. Heat-tolerance was tested by a heat challenge (36°C for 7h) at 35 days of age. TM significantly reduced the hatching rate of the animals and increased mortality during the first four weeks of life. At hatching, TM animals were heavier than controls, but lighter at 25 days of age for both sexes. Thirty-five days after hatching, TM decreased the surface temperature of the shank in females, suggesting a modulation of the blood flow to maintain the internal temperature. TM also increased blood partial pressure and oxygen saturation percentage at 35 days of age in females, suggesting a long-term modulation of the respiration physiology. Quails physiologically responded to the heat challenge, with a modification of several hematologic and metabolic parameters, including an increase in plasma corticosterone concentration. Several physiological parameters such as beak surface temperature and blood sodium concentration revealed that TM birds responded differently to the heat challenge compared to controls. Altogether, this first comprehensive characterization of TM in Japanese quail showed durable effects that may affect the response of TM quails to heat.

Fig 1. Experimental protocol of thermal manipulation in quail.

Cons DD quail eggs were incubated in control (C) conditions, i.e. maintained at 37.8°C and 56% relative humidity (RH) during the whole incubation period (upper graph), or thermo-manipulated (TM) with a cyclic increase of incubation temperature at 39.5°C and 65% RH for 12 h/d from incubation days I0 to I13 (lower graph). Hatching corresponds to both I17 and D1. Red boxes under arrows indicate the heat challenge performed at D35 (36°C for 7h).

Fig 2. Effect of thermal manipulation on mortality during the first four weeks of age (from day 1 to day 28).

C: control; TM: thermal manipulation during embryonic incubation. The bold parts of the bars represent the surviving quails and the light parts, the dead ones. ***: p-value < 0.001. Individual data are presented in S2 Table.

Fig 3

Effect of thermal manipulation on quail weight (g) from day 1 (D1) to D35. C: control; TM: thermal manipulation during egg incubation; D: day. Impact of the TM on quails of each sex and at D1, D25 or D35. The dots correspond to the mean. *: p-value ≤ 0.05, **: p-value ≤ 0.01, ***: p-value ≤ 0.001. Individual data are presented in S3 Table.

Fig 4. Effect of thermal manipulation and sex on shank surface temperature, oxygen saturation (O₂sat) and partial pressure (pO₂) at day 35.

C: control; TM: thermal manipulation during egg incubation. The dots correspond to the mean and the range of the lines correspond to the confidence interval of the mean. Different letters indicate significant differences (p-value ≤ 0.05). Individual data are presented in S3 Table.

Fig 5. Effect of thermal manipulation, heat challenge and sex on beak surface temperature and plasma Na⁺ concentration at day 35.

C: control; TM: thermal manipulation during egg incubation; RT: non-challenged birds; HC: heat-challenged birds. The dots correspond to the mean and the range of the lines correspond to the confidence interval of the mean. Different letters indicate significant differences (p-value ≤ 0.05). Individual data are presented in S3 Table.

Fig 6

Effect of heat challenge on temperature (A), blood parameters (B) and hormone (C) and metabolite (D) concentrations at day 35. RT: non-challenged birds; HC: heat-challenged birds. TCO₂: total carbon dioxide; K⁺: ion potassium; iCa: ion calcium; HCO₃-: ion bicarbonate; Beb: base excess in blood; Beecf: base excess in extra-cellular fluid; T4: thyroxine. The dots correspond to the mean and the range of the lines correspond to the confidence interval of the mean. Different letters indicate significant differences (p-value ≤ 0.05). Individual data are presented in S3 Table.