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Ventilatory, metabolic, and thermoregulatory responses of Damaraland mole rats to acute and chronic hypoxia

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Abstract

Damaraland and naked mole rats are the only eusocial mammalian species and live in densely populated, poorly ventilated underground burrows, within which they likely experience intermittent periods of hypoxia. Naked mole rats are the most hypoxia-tolerant mammal and do not exhibit a hypoxic ventilatory response to acute or chronic hypoxia but instead rely upon a robust hypoxic metabolic response to tolerate reduced environmental O2. Conversely, physiological responses to hypoxia have not been explored in Damaraland mole rats but given their social and environmental similarities to naked mole rats, we hypothesized that they would exhibit similar physiological responses to hypoxia. We predicted that they would rely primarily on metabolic rate depression when O2 is limited and would not exhibit ventilatory responses to acute or chronic hypoxia. To test this hypothesis, we exposed Damaraland mole rats to normoxia (21% O2) or progressive hypoxia (12–5% O2), before and after acclimation to chronic hypoxia (8–10 days at 10% O2), and measured ventilatory, metabolic, and thermoregulatory responses. We found that ventilation increased up to fourfold with progressive hypoxia and body temperature decreased ~ 2 °C; however, a hypoxic metabolic response was absent. Following acclimation to chronic hypoxia, ventilation in 21% O2 was ~ twofold higher than in control animals, indicating the occurrence of ventilatory plasticity to hypoxia, and body temperature and metabolic rate were elevated. However, ventilation was not further augmented in acute hypoxia following acclimation to chronic hypoxia, indicating that ventilatory acclimatization to hypoxia was atypical of other mammals. These results refute our hypothesis and we conclude that Damaraland and naked mole rats have divergent physiological responses to hypoxia.

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Abbreviations

ACR:

Air convection requirement

CSH:

Chronic sustained hypoxia

eO2%:

Oxygen extraction percentage

f R :

Breathing frequency

\({\text{P}}{{\text{a}}_{{{\text{O}}_2}}}\) :

Partial pressure of arterial O2 tension

RFID:

Radio frequency identification

T a :

Ambient temperature

T b :

Body temperature

\({\dot {V}_{\text{E}}}\) :

Minute ventilation

\({\dot {V}_{{{\text{CO}}_2}}}\) :

Carbon dioxide production rate

\({\dot {V}_{{{\text{O}}_2}}}\) :

Oxygen consumption rate

V T :

Tidal volume

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Acknowledgements

We would like to thank the uOttawa animal care and veterinary services team for their assistance in animal handling and husbandry. We would also like to thank Yvonne Dzal for her clever assistance in preparing our manuscript.

Funding

This work was supported by an NSERC Discovery Grant, an NSERC Canada Research Chair (Tier II), and a Parker B Francis PDF to MEP.

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Authors

Contributions

MEP conceived of and designed the study and wrote the manuscript. SYZ performed and analyzed the experiments. All the authors gave final approval of the published version and agree to be accountable for all content therein.

Corresponding author

Correspondence to Matthew E. Pamenter.

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We have no competing interests.

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Communicated by H. V. Carey.

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Zhang, S.Y., Pamenter, M.E. Ventilatory, metabolic, and thermoregulatory responses of Damaraland mole rats to acute and chronic hypoxia. J Comp Physiol B 189, 319–334 (2019). https://doi.org/10.1007/s00360-019-01206-y

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  • DOI: https://doi.org/10.1007/s00360-019-01206-y

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