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Extreme hypoxia and high lactate concentrations in early chicken embryos show that cutaneous oxygen uptake is limited by diffusion and metabolism is partially anaerobic

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Abstract

Respiratory gas exchange in avian embryos progresses through three stages inside the egg. During the first 3–5 days of incubation, the chicken embryo has no specialised respiratory organs and is not reliant on blood circulation. At this stage, it obtains oxygen mainly by diffusion through the eggshell, albumen, amniotic fluid and embryonic tissues. In the second stage, gas exchange relies on diffusion through the shell in the gas phase and convection by blood circulation through the chorioallantoic membrane and body. Day 19 starts the third stage, the transition from chorioallantoic to pulmonary gas exchange, which is complete when the chick hatches on day 20. Metabolism is thought to be aerobic throughout incubation, although the early embryo is covered by fluids (albumen and amniotic fluid) which would greatly resist oxygen diffusion. This study uses fibre-optic sensors to measure oxygen partial pressure (Po2) near, and inside of, the embryo during days 3–5, and relates the data to total body lactate levels. The study shows that fluids surrounding the embryo greatly impede oxygen diffusion, with Po2 becoming severely hypoxic near the embryo, occasionally almost anoxic inside it. Meanwhile, lactate rises to high levels, and the stored lactate can be later oxidised by the embryo when the chorioallantois takes over and metabolism becomes entirely aerobic.

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Data availability

Raw data are available from Researchgate:www.researchgate.net/profile/Roger_Seymour.

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Funding

Research supported by the University of Adelaide.

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Authors and Affiliations

  1. School of Biological Sciences, University of Adelaide, Adelaide, South Australia, 5005, Australia

    Sarah Rola-Wojciechowski Barrett & Roger S. Seymour

Authors
  1. Sarah Rola-Wojciechowski Barrett
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  2. Roger S. Seymour
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Contributions

Both authors contributed to the study conception and design. SB made all of the measurements, collected the data, ran statistical tests, drew draft figures and wrote her thesis. RSS checked the data, ran additional statistics, drew final figures and largely wrote the final drafts.

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Correspondence to Roger S. Seymour.

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Authors declare no conflict of interests or competing interests.

Ethical approval

Research approved by the University of Adelaide Animal Ethics Committee (S-2015-094).

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Communicated by E. Polymeropoulos.

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Barrett, S.RW., Seymour, R.S. Extreme hypoxia and high lactate concentrations in early chicken embryos show that cutaneous oxygen uptake is limited by diffusion and metabolism is partially anaerobic. J Comp Physiol B 191, 1007–1016 (2021). https://doi.org/10.1007/s00360-021-01372-y

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