Oxygen supply limits the heat tolerance of avian embryos

Abstract

Physiologists have primarily focused on two potential explanations for heat stress in animals—the classic model of molecular stability and an alternative model of oxygen limitation. Although the classic model has widespread support, the oxygen-supply model applies to many aquatic animals and some terrestrial ones. In particular, the embryonic stage of terrestrial animals seems most susceptible to oxygen limitation because embryos acquire oxygen from the atmosphere by diffusion rather than ventilation. We report experiments confirming the two conditions of the oxygen-supply model in Japanese quail embryos, Coturnix coturnix . Hypoxia (12% O 2 ) greatly reduced the chance of survival at 47.5°C, and hyperoxia greatly improved the chance of survival at 48.5°C. This finding expands the scope of the oxygen-supply model to a terrestrial, endothermic species, suggesting that oxygen supply generally limits the heat tolerance of embryos.

Latitudinal embryonic thermal tolerance and plasticity shape the vulnerability of oviparous species to climate change

“…For example, a growing number of researchers suggest embryonic heat tolerance is related to oxygen limitation at extremely high temperatures in reptile and avian species (Vimmerstdt et al. 2015, Hall and Warner 2019 a ). Such mechanistic knowledge can help us to understand the proximate and evolutionary factors that results in the variations in EAHT, and what is more important to predict survival probability under ongoing climate warming with adaptation and evolution (Huey et al.…”

Thermal sensitivity of lizard embryos indicates a mismatch between oxygen supply and demand at near‐lethal temperatures

“…These data implicate a mismatch between oxygen demand and supply as a cause for death at high temperatures (Gangloff & Telemeco, 2018; Wittmann et al, 2008). Indeed, other studies find that hypoxic and hyperoxic incubation conditions decrease or increase, respectively, the thermal tolerance of reptile embryos (e.g., Liang, Sun, Ma, & Du, 2015; Smith et al, 2015; Vimmerstedt, Padilla Pérez, Angilletta, & VandenBrooks, 2019); however, these have used chronic oxygen and/or temperature conditions. Thus, they demonstrate the positive correlation between oxygen supply and the lethal temperature but fail to unearth mechanisms that link the two.…”

Integrative developmental biology in the age of anthropogenic change

“…This hypothesis states that at temperatures near a species' thermal extremes, metabolic demand for oxygen outpaces oxygen supply, pushing cells into a state of hypoxia and molecular distress. Although originally developed for adult, marine ectotherms (Frederich & Pörtner, 2000; Portner, 2010; Portner & Farrell, 2008), this hypothesis has since been tested in terrestrial organisms and their embryos (Camacho et al, 2018; Campbell‐Staton et al, 2018; Hall & Warner, 2020; Smith et al, 2015; Vimmerstedt et al, 2019).…”

“…At later stages, during the period of rapid growth, the increased demand for oxygen must be met through delivery by the circulatory system. Without knowledge of developmental staging or embryonic physiology, these stage‐specific effects may confound the clear interpretation of embryonic respirometry studies (Camacho et al, 2018; Campbell‐Staton et al, 2018; Hall & Warner, 2020; Smith et al, 2015; Vimmerstedt et al, 2019). Furthermore, incubation times vary widely among squamates (Birchard & Marcellini, 1996; Birchard, 2001) and reptilian eggs are laid at dramatically different stages (e.g., early cleavage stages vs. the early stages of morphogenesis; Deeming & Ferguson, 1990; Diaz et al, 2019; Sanger et al, 2008; Tokita & Kuratani, 2001).…”