Ventilation changes associated with hatching and maturation of an endothermic phenotype in the Pekin duck, Anas platyrhynchos domestica

Abstract

Precocial birds begin embryonic life with an ectothermic metabolic phenotype and rapidly develop an endothermic phenotype after hatching. Switching to a high-energy, endothermic phenotype requires high-functioning respiratory and cardiovascular systems to deliver sufficient environmental oxygen to the tissues. We measured tidal volume (VT), breathing frequency (ƒ), minute ventilation (V̇e), and whole-animal oxygen consumption (V̇o2) in response to gradual cooling from 37.5°C (externally pipped paranates, EP) or 35°C (hatchlings) to 20°C along with response to hypercapnia during developmental transition from an ectothermic, EP paranate to endothermic hatchling. To examine potential eggshell constraints on EP ventilation, we repeated these experiments in artificially hatched early and late EP paranates. Hatchlings and artificially hatched late EP paranates were able to increase V̇o2significantly in response to cooling. EP paranates had high ƒ that decreased with cooling, coupled with an unchanging low VT and did not respond to hypercapnia. Hatchlings had significantly lower ƒ and higher VT and V̇e that increased with cooling and hypercapnia. In response to artificial hatching, all ventilation values quickly reached those of hatchlings and responded to hypercapnia. The timing of artificial hatching influenced the temperature response, with only artificially hatched late EP animals, exhibiting the hatchling ventilation response to cooling. We suggest one potential constraint on ventilatory responses of EP paranates is the rigid eggshell, limiting air sac expansion during inhalation and constraining VT Upon natural or artificial hatching, the VT limitation is removed and the animal is able to increase VT, V̇e, and thus V̇o2, and exhibit an endothermic phenotype.

Keywords: endothermy; hypercapnia; minute ventilation; tidal volume; ventilation.

Fig. 1.

Representative trace of inflow and outflow oxygen measurements. The trace shows oxygen percentage of inflow oxygen and respiratory chamber outflow from one animal, switching every 120 s and subsampling from the multiplexer at rate of ∼100 ml/min.

Fig. 2.

Pekin duck whole animal oxygen consumption (A), cloacal/eggshell temperature (B), ventilation rate (breaths/min) (C), tidal volume (μl/breath) (D), and minute ventilation (ml/min) (E) in response to cooling during external pipping (●) and the first day of post-hatch life (■). Animals were cooled at a rate of 9.2^°C/h. Hatchling temperature was measured in the cloaca, and externally pipped embryo body surface temperature was measured just under the shell. Open symbols represent significant differences from the value at the highest air temperature for the age at P < 0.05. The dashed line in B represents the line of thermal equality. Shell temperature of cooling infertile eggs are included in B (gray line; n = 4). Horizontal lines above a temperature indicate a significant difference between the externally pipped and hatchling values at that temperature. Data are presented as means ± SD; n = 7 externally pipped paranates and five hatchlings, except for V̇o₂ where n = 4 hatchlings.

Fig. 3.

Breathing pattern of day old hatchlings in response to exposure to increased CO₂. Ventilation rate (breaths/min) (A), tidal volume (μl/breath) (B), and minute ventilation (ml/min) (C) are shown. Open symbols represent significant difference from the value at 0% CO₂ at P < 0.05; n = 4. Data are presented as means ± SD.

Fig. 4.

Breathing pattern response to exposure to 0% and 4% CO₂ at 37.5°C in animals as externally pipped paranates and then after artificial hatching by removing the animal from the eggshell. Whole animal oxygen consumption (ml/min) (A), ventilation rate (breaths/min) (B), tidal volume (μl/breath) (C), and minute ventilation (ml/min) (D). Values with different letters are significantly different from each other at P < 0.05. Data points express means ± SD; n = 7. Gray lines indicate individual responses.

Fig. 5.

Examples of individual oxygen consumption (ml/min) from externally pipped paranates at various stages of hatching in response to gradual cooling.

Fig. 6.

Oxygen consumption of early externally pipped paranates during cooling in a 40% oxygen environment. Open symbols represent significant differences from the value at the highest air temperature at P < 0.05. Data presented as means ± SD; n = 8.

Fig. 7.

Oxygen consumption, body temperature, and breathing pattern responses to cooling of animals after artificial hatching by removing the animal from the eggshell during the externally pipped stage (EP). Externally pipped paranates were helped out of the eggshell with either a small star fracture (early EP, ■) or larger hole in the eggshell (late EP, ●). Whole animal oxygen consumption (ml/min) (A), ventilation rate (breaths/min) (B), tidal volume (μl/breath) (C), and minute ventilation (ml/min) (D). Open symbols represent significant difference from the value at 37.5°C within an age group at P < 0.05. Horizontal lines above a temperature denote significant differences between the late EP and early EP response at that temperature. Data points express means ± SD; n = 5 early EP and 7 late EP. Gray lines indicate individual responses.