ABSTRACT The critical oxygen partial pressure (Pcrit), typically defined as the PO2 below which an animal's metabolic rate (MR) is unsustainable, is widely interpreted as a measure of hypoxia tolerance. Here, Pcrit is defined as the PO2 at which physiological oxygen supply (α0) reaches its maximum capacity (α; µmol O2 g−1 h−1 kPa−1). α is a species- and temperature-specific constant describing the oxygen dependency of the maximum metabolic rate (MMR=PO2×α) or, equivalently, the MR dependence of Pcrit (Pcrit=MR/α). We describe the α-method, in which the MR is monitored as oxygen declines and, for each measurement period, is divided by the corresponding PO2 to provide the concurrent oxygen supply (α0=MR/PO2). The highest α0 value (or, more conservatively, the mean of the three highest values) is designated as α. The same value of α is reached at Pcrit for any MR regardless of previous or subsequent metabolic activity. The MR need not be constant (regulated), standardized or exhibit a clear breakpoint at Pcrit for accurate determination of α. The α-method has several advantages over Pcrit determination and non-linear analyses, including: (1) less ambiguity and greater accuracy, (2) fewer constraints in respirometry methodology and analysis, and (3) greater predictive power and ecological and physiological insight. Across the species evaluated here, α values are correlated with MR, but not Pcrit. Rather than an index of hypoxia tolerance, Pcrit is a reflection of α, which evolves to support maximum energy demands and aerobic scope at the prevailing temperature and oxygen level.
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Oxygen supply capacity in animals evolves to meet maximum demand at the current oxygen partial pressure regardless of size or temperature
The capacity to extract oxygen from the environment and transport it
to respiring tissues in support of metabolic demand reportedly has
implications for species’ thermal tolerance, body size, diversity and
biogeography. Here, we derived a quantifiable linkage between
maximum and basal metabolic rate and their oxygen, temperature
and size dependencies. We show that, regardless of size or
temperature, the physiological capacity for oxygen supply precisely
matches the maximum evolved demand at the highest persistently
available oxygen pressure and this is the critical PO2 for the maximum
metabolic rate, Pcrit-max. For most terrestrial and shallow-living marine
species, Pcrit-max is the current atmospheric pressure, 21 kPa. Any
reduction in oxygen partial pressure from current values will result
in a calculable decrement in maximum metabolic performance.
However, oxygen supply capacity has evolved to match demand
across temperatures and body sizes and so does not constrain
thermal tolerance or cause the well-known reduction in mass-specific
metabolic rate with increasing body mass. The critical oxygen
pressure for resting metabolic rate, typically viewed as an indicator
of hypoxia tolerance, is, instead, simply a rate-specific reflection of the
oxygen supply capacity. A compensatory reduction in maintenance
metabolic costs in warm-adapted species constrains factorial aerobic
scope and the critical PO2 to a similar range, between ∼2 and 6,
across each species’ natural temperature range. The simple new
relationship described here redefines many important physiological
concepts and alters their ecological interpretation.
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- Award ID(s):
- 1459243
- NSF-PAR ID:
- 10220136
- Date Published:
- Journal Name:
- Journal of experimental biology
- Volume:
- 223
- ISSN:
- 0022-0949
- Page Range / eLocation ID:
- jeb210492
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1101/701417
