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First published online June 11, 2007
Journal of Experimental Biology 210, 2146-2153 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.005389
Oxygen consumption rates in hovering hummingbirds reflect substrate-dependent differences in P/O ratios: carbohydrate as a `premium fuel'
1 Department of Ecology, Evolution and Marine Biology, University of
California, Santa Barbara, CA 93106-9610, USA
2 Department of Biology, University of California, Riverside, CA 92521,
USA
* Author for correspondence (e-mail: k_welch{at}lifesci.ucsb.edu)
Accepted 10 April 2007
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O2, should
decline as the respiratory quotient, RQ
(CO2/O2),
increases from 0.71 to 1.0 as hummingbirds transition from a fasted to a fed
state. Here, we show that hovering
O2 values in
rufous (Selasphorus rufus) and Anna's hummingbirds (Calypte
anna) are significantly greater when fats are metabolized (RQ=0.71) than
when carbohydrates are used (RQ=1.0). Because hummingbirds gained mass during
our experiments, making mass a confounding variable, we estimated
O2 per unit
mechanical power output. Expressed in this way, the difference in
O2 when
hummingbirds display an RQ=0.71 (fasted) and an RQ=1.0 (fed) is between 16 and
18%, depending on whether zero or perfect elastic energy storage is assumed.
These values closely match theoretical expectations, indicating that a
combination of mechanical power estimates and `indirect calorimetry', i.e. the
measurement of rates of gas exchange, enables precise estimates of ATP
turnover and metabolic flux rates in vivo. The requirement for less
oxygen when oxidizing carbohydrate suggests that carbohydrate oxidation may
facilitate hovering flight in hummingbirds at high altitude.
Key words: P/O ratio, carbohydrate, fatty acid, hummingbird, oxygen consumption
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O2) are
accounted for by mitochondrial respiration in locomotory muscles
(Suarez, 1992
;
Taylor, 1987). For decades, it
has been recognized by physiologists that conversion of such
O2 values to the
equivalent values of energy expenditure in watts or joules requires
consideration of the metabolic substrate(s) used (e.g.
Kleiber, 1961;
Schmidt-Nielsen, 1990). On the
other hand, biochemists have empirically determined mitochondrial P/O ratios
(moles ATP phosphorylated per mole oxygen atom consumed) and found that these
depend upon the nature of the substrates oxidized. The latest estimates, based
on a combination of empirical data and theoretical considerations, reveal an
15% higher cellular P/O ratio when glucose is oxidized compared with
fatty acid oxidation (Brand,
1994; Brand, 2005).
This substrate-dependent difference in the efficiency of aerobic ATP
production has been observed in isolated, perfused hearts that, when provided
with fatty acids to oxidize, elevate their
O2 above rates
obtained when oxidizing glucose (Korvald
et al., 2000; Neely and
Morgan, 1974). Such differences in P/O ratios have also been
observed in vitro using mitochondria isolated from hummingbird flight
muscles (Suarez et al.,
1986). At one or more stages in their education, biologists are often required to memorize P/O ratios and other stoichiometric relationships in biochemistry. Apart from turning a fascinating subject into a dry exercise in memorization, the relevance of stoichiometric relationships to the lives of real animals is often presented as a matter of faith, i.e. a matter that cannot be subjected to empirical test, except in cell-free extracts. So, an important question that we address here is whether substrate-dependent P/O ratios influence whole animal performance and whether they have any relevance to behavioral ecology.
Hummingbirds offer a unique opportunity to determine whether the substrate
dependence of P/O ratios is manifested in whole animals and what the
significance of this might be. Their flight muscles consist exclusively of
fast-twitch, oxidative fibers (Grinyer and
George, 1969; Suarez et al.,
1991; Suarez,
1992). Thus, >90% of their
O2 during flight
is accounted for by mitochondrial respiration in a single cell type. In
addition, it is possible to alter the relative contributions of carbohydrate
and fat to the fueling of mitochondrial respiration through manipulation of
their dietary status. Fasted hummingbirds rely heavily on fatty acid oxidation
and rapidly switch to carbohydrate oxidation when dietary sucrose becomes
available, oxidizing newly ingested sucrose almost exclusively to fuel
foraging flight (Suarez et al.,
1990; Welch et al.,
2006). All else being equal, the mechanical power requirements for
hovering flight should remain constant irrespective of the fuel oxidized. In
biochemical terms, the ATP turnover (i.e. synthesis = hydrolysis) rate
required for a unit mass of bird to hold itself aloft should be independent of
the nature of the fuel oxidized. Assuming a negligible contribution of protein
to the support of metabolism (Vaillancourt
et al., 2005), RQ
(=CO2/O2)
may be used to infer the relative contributions of carbohydrate and fat to the
support of metabolism, with an RQ of 0.71 indicating exclusively fat oxidation
and an RQ of 1.0 indicating exclusively carbohydrate oxidation. The difference
in P/O ratio between carbohydrate and fat oxidation leads to the hypothesis
that O2 should
decline by 15% as the RQ increases from 0.71 to 1.0.
Recently reported mismatches between heat production rates predicted from
indirect calorimetry, determined through measurement of rates of whole-animal
gas exchange, and those measured by `direct calorimetry' have raised doubt
concerning the validity of indirect calorimetry as a means by which to
estimate metabolic rate (Walsberg and
Hoffman, 2005). However, rates of metabolic heat production are
not predictive of rates of ATP turnover, nor are they useful for estimating
flux rates through the pathways of substrate oxidation. Here, we consider the
results of indirect calorimetry in terms of the biochemical meaning of the
term `metabolic rate'. We demonstrate how this, in combination with estimates
of mechanical power output, leads to novel insights concerning the energetics
of hummingbird hovering flight.
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)
and housed at the UCSB Aviary in individual outdoor, wire-mesh enclosures
measuring 1.8 m tall x 0.6 m wide x 2.4 m long. Birds were fed
ad libitum on a 13% (w/v) solution of Nektar-Plus (Guenter Enderle,
Tarpon Springs, FL, USA) supplemented with beet sugar (5% w/v). Birds were
subjected to natural photophase and ambient weather conditions. Capture,
housing and experimental protocols were approved by the University of
California, Santa Barbara Institutional Animal Care and Use Committee
(Protocol 672).
Experiments were performed in an enclosure measuring 0.92 m wide x
0.54 m high x 0.51 m deep, in the laboratory at a mean temperature of
23.9±0.4°C. Data collection took place between April and August
2006 between 06.00 h and 11.00 h. Prior to the experiment, each hummingbird
was fasted overnight to ensure that it would be oxidizing primarily fat at the
beginning of the hour-long period of data collection
(Suarez et al., 1990;
Welch et al., 2006) as well as
to ensure that it would be motivated to feed. Hummingbirds were active and
sporadically hovering for a period of at least 20 min prior to the beginning
of data collection. Experiments were repeated using each individual
approximately 1–2 weeks later, with the exception of the two male Anna's
hummingbirds (C. anna). Hummingbirds were offered the Nektar-Plus and
beet sugar solution for a period of one hour. Oxygen consumption
(O2) and carbon
dioxide production
(CO2) rates were
determined by open-flow respirometry during the first hour of access to feeder
solution following the overnight fast. The respirometric system used follows
one described elsewhere (Bartholomew and
Lighton, 1986; Suarez et al.,
1990; Welch et al.,
2006). Briefly, we constructed the feeder such that birds had to
hover and insert their heads into a plastic tube (that functioned as a mask)
to gain access to the end of a 20 ml disposable syringe, filled with feeder
solution. Plastic tubing was attached to the side of the mask, allowing
incurrent air to be drawn and then passed through a column of DrieriteTM
(W. A. Hammond Drierite, Xenia, OH, USA) to scrub water vapor before entering
the carbon dioxide analyzer (CA-2A; Sable Systems International, Las Vegas,
NV, USA). After leaving the carbon dioxide analyzer, air passed through a
DrieriteTM–AscariteTM–DrieriteTM column (Ascarite
II; Arthur H. Thomas, Philadelphia, PA, USA), to scrub any carbon dioxide and
additional water from the line, and then into the oxygen analyzer (FOXBOX;
Sable Systems International). Air flow was maintained by a mechanism internal
to the FOXBOX (thus, after the removal of water vapor) at a rate of 1200 ml
min–1. The presence of the hummingbird's head inside the mask
was detected by interruption of an infrared beam crossing the front edge of
the mask. The only available perch in the cage was placed on top of a balance,
allowing recording of bird mass. Mass was estimated for each feeding event as
the average of mass values immediately prior to and following that feeding
event. Oxygen analyzer, carbon dioxide analyzer, flow rate, infrared beam and
balance analog output were converted into a digital signal (Universal
Interface II; Sable Systems International), which was then fed to a computer.
Data were recorded at 0.05-s intervals for 1 h using Expedata software (v.
1.0.17; Sable Systems International).
Immediately before data collection, the oxygen analyzer was calibrated with well-mixed ambient air drawn through the mask in the absence of a hummingbird. The carbon dioxide analyzer was calibrated with CO2-free nitrogen gas (zero gas) and 0.5% CO2 in nitrogen gas (Praxair, Danbury, CT, USA). In each case, tubing was removed directly downstream of the mask and held inside a small reservoir into which flowed the calibration gas at a rate in excess of the flow rate of air pulled through the respirometry system.
Rates of oxygen consumption
(O2) and carbon
dioxide production
(CO2) were
determined from raw oxygen and carbon dioxide traces as described previously
(Suarez et al., 1990;
Welch et al., 2006).
STP-corrected oxygen depletion and carbon dioxide enrichment associated with
each feeding event were determined by first correcting the traces by
subtracting baseline values (determined as the linear extrapolation of points
directly before and after the feeding event in question). These
baseline-corrected data were then converted to ml of gas by application of
standard equations (Withers,
1977). Rates of gas consumption or production were determined by
dividing the volume of gases respired by the time the hummingbird's head was
inside the mask (estimated as the period of time that the infrared beam was
occluded). All feeding events that lasted for less than 1 s in duration were
excluded from analysis. All means are reported ± s.d.
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O2/Mb)
varies significantly (1-way ANOVA analysis; data not shown) in relation to RQ.
However, it is important to note that each bird gained mass during the hour
(C. anna, 0.33±0.15 g, range=0.16–0.57 g, N=6;
S. rufus, 0.28±0.11 g, range=0.16–0.47 g,
N=12).
Aerodynamic theory predicts that mass-specific power output requirements
for hovering should vary as a complex function of the mass being lifted
(Ellington, 1984a;
Ellington, 1984b;
Ellington, 1984c;
Ellington, 1984d;
Ellington, 1984e;
Ellington, 1984f). Total
hovering power requirements are a function of the individual component power
requirements, including the energy required to overcome profile drag forces on
the wings [profile power (Ppro)], the energy required to
move sufficient air in order to overcome the downward pull of gravity [induced
power (Pind)] and the energy necessary to accelerate the
wings during the first half of a half-stroke [inertial power
(Pacc)]. If the kinetic energy of the wings during the
first half of each half-stroke can be completely stored as elastic strain
energy during the second half of the half-stroke and then released at the
beginning of the following stroke (perfect elastic storage), then
Pacc will be zero and total hovering power requirement
(Pper) will equal
Ppro+Pind. Instead, if none of the
kinetic energy of the wings is recovered for subsequent strokes (zero elastic
storage), then total hovering power requirement (Pzero)
will equal (Ppro+Pind+
Pacc)/2. Actual hovering power requirements are not
empirically known for hovering hummingbirds but are likely to be somewhere
between estimated Pper and Pzero
values. We estimated Pper and Pzero
using equations in Ellington (Ellington,
1984f). Body mass was measured for each bird during each feeding
event (as described above) whereas other morphological and kinematic
parameters required for power estimates were taken from average species- and
gender-specific values of rufous
(Altshuler, 2006;
Altshuler and Dudley, 2003) and
Anna's hummingbirds (D.L.A., unpublished data).
We controlled for the chain effects of Mb on muscle
power requirements and therefore on
O2 by dividing
mass-specific O2
(O2/Mb)
by mass-specific mechanical power requirements for hovering assuming perfect
elastic energy storage (Pper). This correction, oxygen
consumption rate per unit hovering power output assuming perfect elastic
energy storage in ml O2 h–1 W–1,
is summarized as follows:
 | (1) |
O2/Mb is
in ml O2 g–1 h–1 and
Pper is in W g–1. To obtain oxygen
consumption rate per unit hovering power output assuming zero elastic energy
storage in ml O2 h–1 W–1, we
simply substituted Pzero for Pper, as
follows:
 | (2) |
O2/Mb
is in ml O2 g–1 h–1 and
Pzero is in W g–1. The effect of
variations in mechanical power output assuming either perfect or zero elastic
energy storage on carbon dioxide production rate can similarly be removed by
using mass-specific carbon dioxide production rate
(CO2/Mb)
in place of
O2/Mb
in Eqns 1 and 2 to solve for carbon dioxide production rate per unit hovering
power output
(CO2/Wper
and
CO2/Wzero).
There was no significant effect of trial day on
O2/Wper
and
O2/Wzero
or
CO2/Wper
and
CO2/Wzero
in either Anna's
(O2/Wper:
F1,3=0.0081, P=0.9287, ANOVA;
O2/Wzero:
F1,3=0.0082, P=0.9281, ANOVA;
CO2/Wper:
F1,3=0.0058, P=0.9395, ANOVA;
CO2/Wzero:
F1,3=0.0028, P=0.9576, ANOVA) or rufous
hummingbirds
(O2/Wper:
F5.5=0.4030, P=0.8456, ANOVA;
O2/Wzero:
F5,5=0.4024, P=0.8460, ANOVA;
CO2/Wper:
F5,5=0.2425, P=0.9425, ANOVA;
CO2/Wzero:
F5,5=0.2439, P=0.9418, ANOVA). The data for each
individual from the two trial days were therefore combined for further
analysis. Table 1 shows results
of a linear model of the effect of RQ on oxygen consumption rate per unit
hovering power output and carbon dioxide production rate per unit hovering
power output for both Anna's and rufous hummingbirds. For Anna's hummingbirds,
with individual hummingbird as a random effect within a linear model, the
effect of metabolic substrate, as indicated by RQ, on
O2/W and
CO2/W was highly
significant (P<0.0001) when either perfect or zero elastic storage
was assumed (Table 1). There
was no difference in the relationship of either
O2/W or
CO2/W to RQ
between Anna's hummingbirds (RQ x individual interaction term;
P>0.9052; see Table
1), indicating that the nature of the effect of metabolic
substrate on oxygen consumption or carbon dioxide production rate was constant
across individuals. Results were similar for rufous hummingbirds
(Table 1). With individual
hummingbird as a random effect within a linear model, the effect of metabolic
substrate, as indicated by the RQ, on
O2/W and
CO2/W was also
highly significant (P<0.0001) assuming either perfect or zero
elastic storage (Table 1). As
with Anna's hummingbirds, there was no difference in the relationship of
either O2/W or
CO2/W to RQ
between rufous hummingbirds (RQ x individual interaction term;
P>0.1063; see Table
1), indicating that the nature of the effect of metabolic
substrate on oxygen consumption or carbon dioxide production rate was also
constant across individuals within this taxon.
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Linear functions describing the relationship of
O2/Wper
or
O2/Wzero
to RQ for each hummingbird (Figs
2,
3) can be used to determine the
mass-corrected oxygen consumption rate when burning solely fat (RQ=0.71) or
carbohydrate (RQ=1.0). The relative difference between these values can then
be compared to the relative difference in P/O ratios
(Brand, 2005) under these two
conditions. Table 2 shows the
predicted
O2/Wper
and
O2/Wzero
values as a function of metabolic substrate for each individual. For Anna's
hummingbirds, percentage differences between the predicted
O2/W values at
an RQ of 0.71 and 1.0 averaged 18.0±0.6% (N=4) when perfect
elastic storage (Pper) was assumed and 16.4±0.8%
(N=4) when zero elastic storage (Pzero) was
assumed. For rufous hummingbirds, percent differences between the predicted
O2/W values at
an RQ of 0.71 and 1.0 averaged 16.8±1.7% (N=6) when
Pper was assumed and 16.2±2.1% (N=6) when
Pzero was assumed.
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) as well as the latest consensus values calculated for whole
cells (Brand, 2005).
Detection of substrate-dependent variation in the P/O ratio is feasible in
hovering hummingbirds in large part because they so rapidly shift from
displaying an RQ near 0.71, indicating primarily fat oxidation, to an RQ near
1.0, indicating primarily carbohydrate oxidation. Hummingbirds store excess
energy primarily by converting ingested sugars into fat
(Carpenter et al., 1993;
Odum et al., 1961). As Frayn
details (Frayn, 1983), the RQ
associated with carbon fixation and the oxidation of fuels to provide the ATP
necessary to convert sugars into lipids is approximately 5.6. Thus, if
lipogenesis is activated shortly after sugar ingestion, it is possible that
the RQ that a hummingbird displays during repeated hover-feeding may be
elevated by both carbohydrate oxidation (to fuel hovering flight) and the
metabolic processes associated with lipogenesis. However, the effect of
lipogenesis on hovering hummingbird RQ is likely to be relatively small
because >90% of hovering metabolic rate is due to flight muscles
(Suarez, 1992;
Taylor, 1987). In addition,
Welch et al. show a remarkably strong correlation between the rise in RQ
towards 1.0 and the approach of the carbon isotope signature of expired
CO2 towards the value of recently ingested sugars
(Welch et al., 2006),
suggesting that the shift in RQ is due mainly to the increased oxidation of
dietary sugar. Further, because there is oxygen consumption associated with
lipogenesis, as hummingbirds shift from the fasted to the fed state and
lipogenesis is activated, oxygen consumption should increase. Instead, we find
that after we correct for slight differences in mechanical power output over
the course of the experiment, oxygen consumption declines more than would be
predicted solely by consideration of the proton stoichiometry associated with
the metabolic substrate in use, not less.
Indeed, regardless of the assumption of perfect or zero elastic storage,
the estimate of the difference in P/O ratio between glucose and palmitate
oxidation for Anna's hummingbirds is significantly greater
(Pper, t3=10.3333, P=0.0019;
Pzero, t3=3.9294, P=0.0293)
than the theoretical 14.9% difference estimated by Brand
(Brand, 2005). The difference
in P/O ratio between glucose and palmitate oxidation for rufous hummingbirds
is significantly different from 14.9% when perfect elastic storage is assumed,
but not when zero elastic storage is assumed (Pper,
t5=2.7676, P=0.0395; Pzero,
t5=1.4760, P=0.2000). These discrepancies may
simply be due to estimation or measurement error. For the former, it should be
noted that the power estimates for flight contain several assumptions that
have yet to be evaluated, although we did use an empirically derived value for
the profile drag coefficient (Altshuler et
al., 2004a). However, the extremes of zero and perfect elastic
energy storage almost certainly bracket the true values for mechanical power
requirements. For the latter, it is worth noting that the difference in P/O
ratio between glycogen and palmitate oxidation is 18.7%
(Brand, 2005). How glucose and
fructose are metabolized in hummingbirds prior to oxidation during hovering
flight has not been established. However, mammalian studies reveal that
dietary fructose is converted to glucose by the liver
(Delarue et al., 1993); blood
fructose concentration is low and skeletal muscles display low capacities for
fructose oxidation (Kristiansen et al.,
1997; Kristiansen et al.,
1996). Irrespective of the details concerning the metabolism of
ingested sucrose, our estimates fall within the range predicted by all
possible scenarios and support the hypothesis that carbohydrate oxidation
yields a higher P/O ratio than fatty acid oxidation. As neither RQ values nor
the current stable carbon isotope results allow discrimination between glucose
and glycogen use, we plan to employ in vivo 13C-nmr
spectroscopy to resolve this issue in future studies.
Another potential contributor to the slightly larger than expected
difference in O2
between carbohydrate and fatty acid oxidation might be the latter's activation
of mitochondrial proton leak. In hummingbirds, a mitochondrial uncoupling
protein (UCP) homologue has been found that is most abundant in flight muscles
and, when expressed in yeast, stimulates mitochondrial proton leak
(Vianna et al., 2001). Fatty
acid oxidation results in production of reactive oxygen species
(St-Pierre et al., 2002) that,
in turn, activate avian UCP (Talbot et
al., 2004). Thus, it is possible that some degree of mitochondrial
uncoupling, leading to decreased P/O ratio, may occur during fatty acid-fueled
hummingbird flight. Rolfe et al. (Rolfe et
al., 1999) suggest that proton leak might be responsible for a
non-trivial proportion of oxygen consumption in electrically stimulated rat
leg muscles. However, the extent to which such futile cycling of protons leads
to elevated oxygen consumption in hovering hummingbirds remains unknown.
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O2 values
reflect substrate-dependent differences in P/O ratios, then
O2 values can be
used to estimate ATP turnover rates after properly correcting for the effect
of metabolic substrate. Using Anna's hummingbird 3 as an example
(Fig. 4), there is a
significant negative relationship between whole-animal oxygen consumption rate
and RQ (F1,22=10.4134, P=0.0039). Thus,
whole-body O2
declines despite the gain in body mass as repeated feeding occurs and RQ
climbs from 0.7 to 1.0. Upon correction for the effect of metabolic substrate
on P/O ratio and for the effect of small differences in mass on mechanical
power requirements, the resulting estimates of whole-animal ATP turnover rate
per unit power output display no significant relationship to RQ (assuming
Pper, F1,22=1.8537, P=0.1871;
assuming Pzero, F1,22=1.1524,
P=0.2947). Thus, the bird used a constant amount of ATP per unit
mechanical power output during hovering as it went from the fasted to the fed
state. This illustrates the utility of indirect calorimetry for the estimation
of ATP turnover rate. In addition, the well-established stoichiometric
relationships between moles of substrate oxidized and moles of O2
consumed allow straightforward estimates of the flux rates through catabolic
pathways. Assuming that palmitate is the substrate oxidized while the RQ is
0.71, and based on the regression of oxygen consumption rate (ml O2
h–1) as a function of RQ
(Fig. 4), fatty acid oxidation
would occur at a rate of 4.14 µmol min–1 in bird no. 3 as
it hovers in the fasted state. Assuming that glucose is oxidized when the RQ
is 1.0, glycolytic flux (and glucose oxidation) would occur in this bird at a
rate of 13.93 µmol min–1 during hovering in the fed state.
Rather than being a flawed technique for the estimation of `metabolic rates'
in animals, we show here a set of circumstances in which indirect calorimetry
serves as the method of choice.
Suarez and colleagues (Suarez et al.,
1990; Suarez and Gass,
2002) proposed that hummingbirds maximize net energy gain by
engaging in short foraging bouts while oxidizing dietary carbohydrate. Flying
short distances for short durations while foraging results in reliance upon
dietary sugar as the main oxidative substrate. This prevents the need to
deplete fat stores but also avoids the inefficiency of investing energy into
the synthesis of fat and then using fat to fuel foraging. Hochachka and
colleagues (Hochachka et al.,
1991; McClelland et al.,
1998) hypothesized that a preference for carbohydrate oxidation,
resulting in lower O2 requirements, may have evolved as an
evolutionary adaptation to hypobaric hypoxia. Our evidence of
substrate-dependent P/O ratios in hummingbirds and, in particular, the reduced
requirement for O2 during carbohydrate oxidation provides support
for Hochachka's hypothesis. Hummingbird flight performance has been repeatedly
studied in physically variable gas mixtures, most commonly in normoxic heliox.
In these density-reduction trials, hummingbirds compensate for increased
flight requirements by substantially increasing the stroke amplitude of their
wings and only moderately increasing the wingbeat frequency
(Altshuler and Dudley, 2003;
Chai and Dudley, 1995). This
suggests that neuromuscular adjustments to increase stroke amplitude during a
bout of hovering may incur lower muscle power expenditures than increases in
contractile frequency. In oxygen-reduction experiments, hummingbirds
accordingly decreased wingbeat frequency during sustained hovering, without a
concomitant increase in stroke amplitude
(Altshuler and Dudley, 2003).
Substantial increases in wingbeat frequency have only been seen during
transient load-lifting trials, which are brief and probably anerobic
(Altshuler and Dudley, 2003;
Chai, 1997;
Chai et al., 1997). These
kinematic studies collectively suggest that oxygen delivery to flight muscle
mitochondria may limit muscle performance during sustained flight (more than
several seconds) at ecologically relevant elevations. Many species of
hummingbirds have been observed to forage at high elevation
(Altshuler, 2006;
Altshuler et al., 2004b). Under
these conditions, significant benefits to hummingbird flight performance would
be gained through the O2-sparing effect of carbohydrate oxidation.
The combined benefits of oxidizing carbohydrate qualify it as a premium fuel
for hummingbird flight.
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O2
CO2
CO2/O2)
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References |
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