Cardiorespiratory adjustments of homing pigeons to steady wind tunnel flight
Department of Biological Sciences, Duquesne University, Pittsburgh, PA 15282, USA
* Author for correspondence at University of Pittsburgh, Center for Computational Biology and Bioinformatics, Biomedical Science Tower
Accepted 14 June 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: blood gas, metabolism, cardiac output, stroke volume, heart rate
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Over the years, much has been learned about the many aspects of the
cardiorespiratory responses of birds to treadmill exercise (Bevan et al.,
1994,
1995
) and resting hypoxic
stress (Maginniss et al.,
1997
; Novoa et al.,
1991
). Other studies have investigated various aspects of avian
flight physiology that include metabolism and biochemistry
(Christensen et al., 1994
;
George and John, 1993
;
Schwilch et al., 1996
),
thermoregulation and water balance (Adams
et al., 1997
; Carmi et al.,
1993
,
1994
;
Hissa et al., 1995
;
Giladi et al., 1997
), and wing
cycle and ventilation (Boggs et al.,
1997a
,b
).
However, only one in-depth cardiorespiratory study on an avian species during
steady flight has been reported (Butler et
al., 1977
). Consequently, this central aspect of avian physiology
remains poorly understood.
Two reasons for the scarcity of detailed avian flight cardiorespiratory data are the need for specialized equipment (e.g. a wind tunnel) and chronic vascular cannulation techniques, which provide access to the bird's circulatory system while allowing normal behavior of the bird. Accordingly, the two primary objectives of this study were: (1) to develop chronic cannulation techniques and blood sampling procedures for the pigeon in order to routinely obtain arterial and mixed venous blood samples from both resting and flying birds, and (2) to comprehensively characterize the basic cardiorespiratory parameters of our population of homing pigeons at calm rest and during steady wind tunnel flight under defined conditions.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Screening and familiarization
Resting studies
The birds were first screened to determine whether they were behaviorally
acceptable for use in the resting experiments. Screening involved placing the
bird inside an open-circuit metabolic chamber (described below) for 1 h while
its rate of carbon dioxide production was continuously recorded. Quiet,
resting birds produced little variation in carbon dioxide production. These
birds were chosen as potential candidates for resting studies. Birds passing
this screening test were further familiarized to the chamber during three 1 h
sessions on consecutive days before being scheduled for surgery.
Flight studies
After an initial screening for wind tunnel flight competence, birds showing
promise were included in the daily training schedule. Each bird was trained to
fly in a horizontal wind tunnel for 7 min at a constant air speed of 18.4 m
s1 and an ambient air temperature of 1012°C,
while carrying the devices required for a specific experiment (e.g. metabolism
mask and tube, blood pressure transducer, or pieces of heavy string simulating
cannula extension lines). The trained bird was then scheduled for surgery.
Experimental apparatus
Metabolic chamber
Resting measurements were made from each bird as it sat quietly in a
darkened, open-circuit Plexiglas® metabolic chamber (40
cmx20 cmx20 cm L:W:H). This chamber was placed inside an
environmental chamber set at 15°C to prevent thermal hyperventilation
during the experiment. The environmental chamber kept the internal temperature
of the metabolic chamber at 18.0±0.9°C, as monitored by a YSI
Scanning tele-thermometer (Model 47, YSI, Yellow Springs, OH, USA) and
thermistor probe (Model 427).
Wind tunnel
All flight experiments were performed in a 6.6 m long open-circuit
horizontal wind tunnel (Aerolab, Laurel, MA, USA) with test section dimensions
and air flow properties that have been described elsewhere
(Thomas et al., 1984). All
training and each wind tunnel experiment was carried out at an air speed of
18.4 m s1, and an ambient temperature of 1012°C
to keep the bird from overheating.
Vascular surgery
Resting and flight studies
Surgery was performed on the day before an experiment using 2% Halothane
anesthetic metered by a vaporizer (Flurothane, Model FR, Pittsburgh, PA, USA)
and carried in a 2:1 ratio of oxygen and nitrous oxide. The total flow rate
through the vaporizer was 1.5 l min1. Mixed venous blood
samples were obtained from a silastic cannula (0.030 cm i.d.x0.064 cm
o.d.; Dow Corning, Midland, MI, USA) placed in the bird's right atrium through
the cervical cutaneous branch of the jugular vein. The position of the
cannula's tip in the right atrium was verified by autopsy after completion of
the experiments. Data from birds having the cannula tip located outside the
right atrium were discarded. Arterial blood samples were obtained from a
second silastic cannula (Dow Corning, 0.051 cm i.d.x0.094 cm o.d.)
placed in the bird's right ischiadic artery. An 80% solution of
polyvinylpyrrolidone (PVP-40T; Sigma, St Louis, MO, USA) in aqueous heparin
[1000 U ml1; Elkins-Sinns, Inc., Cherry Hill, NJ, USA
(hereafter called `PVPheparin')] was used to maintain cannulae patency
prior to an experiment.
Measurements
Metabolism
Resting studies. Conventional open circuit methods and equation 2
from Tucker (1968) were used
to determine the oxygen consumption rate
(
O2) of each
bird. A mass flow controller (Model FM-4587, Linde-Union Carbide, Danbury, CT,
USA) maintained a constant air flow rate of 0.80±0.01 l
min1 (STPD) through the metabolic chamber. The
composition of gas entering and leaving the metabolic chamber was continuously
sampled by a pump (Model R-2, Applied Electrochemistry, Pittsburgh, PA, USA)
and monitored by oxygen and carbon dioxide analyzers (Applied
Electrochemistry, Models S-3A-N-22M and CD-38, respectively). Analyzers were
calibrated with dry air and a carbon dioxide (5.00% CO2 in
nitrogen) Primary Standard grade gas mixture (Linde-Union Carbide, Jackson
Welding, Pittsburgh, PA, USA). Individual oxygen consumption rates were
calculated from the mean values of the oxygen and carbon dioxide gas analyzers
while blood samples were being drawn.
Flight studies. The rate of oxygen consumption for five pigeons
was determined using the open-circuit method and flight training procedures
similar to those previously described by Thomas et al.
(1984). Briefly, the birds
were trained to fly in the wind tunnel for 7 min wearing a custom-fit
celluloid mask and molded latex hood. A vacuum source was connected to the
mask by a flexible tube that trailed below the flying bird and pulled room air
through the mask at a rate of 13.1 l min1 (STPD).
Composition of the expired gas was continuously measured as described above,
and the oxygen consumption rate was calculated using mean data from the sixth
minute of each flight.
To detect if leakage of expired gas occurred from the mask at the flow rate
that was to be used for the flight oxygen consumption experiments, several
lower flow rates were used during preliminary tests on each bird, and the rate
of oxygen consumption
(O2) calculated.
These tests revealed that no unintended mask leakage occurred (i.e. there was
no decrease in the bird's apparent
O2) until the
flow rate was reduced to 16% below the flow rate used in the actual
O2 flight
experiments.
The flight mass-specific oxygen consumption rate
(O2
kg1) of each homing pigeon used in the cardiovascular series
of measurements was calculated from the mean mass-specific oxygen consumption
rate measured from a different but equivalent group of homing pigeons
(N=5). These were separate experiments carried out during the same
times of the day (09:00 h11:30 h), months of the year (summer) and wind
tunnel conditions used for the cardiorespiratory measurements (i.e. horizontal
flight at 18.4 m s1 and 1012°C). This two-group
approach was used to increase wind tunnel training success. Switching back and
forth between normal flight and training a given pigeon to fly with the mask
(oxygen consumption measurements) and the pressure transducer back pack (heart
rate measurements) confused most birds, and resulted in substantially lower
training success rates.
Body temperature
Resting and flight studies. Body temperature was measured to the
nearest 0.1°C by inserting a thermistor probe (YSI, Model 427) 5 cm into
the bird's cloaca. The probe was calibrated immediately before each experiment
using a thermostatically controlled water bath (Isotemp Bath Model 8000,
Fisher, Hanover Park, IL, USA) and a precision mercury thermometer (Fisher,
15-000A).
Blood gas tension, total oxygen content and pH
Resting and flight studies. Arterial (a) and mixed venous
() blood samples were analyzed for
oxygen tension (PaO2,
P
O2) carbon
dioxide tension (PaCO2,
P
CO2) and pH
(pHa, pH
) using a blood gas analyzer
(Instrumentation Laboratories Model 1306, Lexington, MA, USA). Total oxygen
content (CaO2,
C
O2) for the
arterial and mixed venous blood samples was measured using a Model K analyzer
(Lex-O2-Con, Chestnut Hill, MA, USA). Oxygen and carbon dioxide
tensions and pH values were corrected using the measured cloacal temperature
and equations supplied in the blood gas analyzer manual. Blood samples were
stored in glass syringes (Model 1750-LTN, Hamilton Gastight®,
Reno, NV, USA) and chilled in an icewater slurry to quench the red
cells' metabolism before analysis. Hematocrit (Hct) was measured for each
blood sample to determine if contamination had occurred by saline admixing.
Arterial and mixed venous blood gas tensions and pH analyses were completed
within 5 min after the sample was collected. Total oxygen content analyses
were completed within 7 min after the sample was collected.
Heart rate
Resting studies. Heart rate (fH) was recorded
during the blood sampling period with silver cutaneous electrodes connected to
a heart monitor equipped with a chart recorder (Model 1700, Mennen Medical,
Trevose, PA, USA).
Flight studies. Heart rate during flight was determined from the arterial pressure waveform measured with a small (3.0 cmx4.2 cmx1.3 cm W:L:H) 9.4 g pressure transducer (NAMIC, Glens Falls, NY, USA) attached to the bird's back with VelcroTM patches. The transducer's output was recorded by a MacLab analog-to-digital converter controlled by a Macintosh computer running MacLab Chart software.
Experimental protocols
Resting studies
On the day of the experiment, the venous cannula was cleared of the
PVPheparin solution, and the bird systemically heparinized with 0.3 ml
of heparinized saline (50 U ml1) through the venous cannula.
The venous cannula was then attached to a saline-filled extension line (0.051
cm i.d.x0.150 cm o.d.x90 cm L; S-54-HL, Tygon, Akron, OH, USA)
connected to one port of a saline-filled three-way manifold. A Tuberculin
syringe used to remove saline from the extension line before collecting the
blood sample, and a Hamilton syringe used to collect the blood sample, were
each attached to the remaining two manifold ports by 1.3 cm lengths of
silastic tubing (Dow Corning, 0.051 cm i.d.x0.094 cm o.d.). The arterial
cannula was prepared the same way, except that 0.3 ml of saline was used in
place of the heparinized saline. After the electrocardiographic leads were
attached to the bird it was placed inside the metabolic chamber that was
placed inside the environmental chamber.
After a 45 min equilibration period, heart rate and carbon dioxide readouts
were monitored for stability to determine an appropriate time for blood sample
collection. Just before collecting the blood samples, the extension lines were
simultaneously cleared of saline using the Tuberculin syringes. The silastic
segments of the Tuberculin syringes were clamped and a 0.5 ml sample of
arterial and mixed venous blood was collected simultaneously in each Hamilton
syringe over 3 min while heart rate and metabolic rate information were
simultaneously recorded. Immediately after collecting the blood samples, the
extension lines were clamped near the manifolds, the silastic tubing segments
on the Hamilton syringes were clamped and separated from the manifolds, then
immersed in an icewater slurry to quench the red cells' metabolism. The
3 min sampling period was chosen because preliminary tests revealed that
faster blood sampling rates were detected by the birds as indicated by higher
heart rates and increased oxygen consumption values. Total oxygen content
analyses were completed within 7 min after sample collection, and arterial and
mixed venous blood gas tensions and pH were completed within 5 min after
sample collection. Deep body temperature was measured within 1 min after
sample collection was completed. Cardiac output
() and stroke volume
(VS) were calculated for each experiment using the Fick
equation.
Flight studies
Blood sampling and blood gas measurements. For these experiments,
the arterial and venous cannulae were first prepared as described above. The
three-way manifold, Tuberculin syringe, and the Hamilton glass sample syringe
associated with each cannula's 90 cm long extension line were secured to a
custom-built `dual-sampling device' that allowed all four syringes to be
filled by using a single hand. By applying small clamps to the appropriate
silastic tubing segments during the flight, a single researcher could first
simultaneously clear saline from the lines into the Tuberculin syringes and
then draw arterial and venous blood samples into the Hamilton glass syringes.
During an experiment, the sampling device was held in a position 0.5 m
downstream from the flying bird by a researcher lying on top of the wind
tunnel with his arms protruding through snug-fitting arm holes in the ceiling
of the wind tunnel's test section. Arterial and mixed venous blood (0.5 ml)
was collected simultaneously in each Hamilton syringe during the sixth minute
of flight. As soon as the bird landed on a perch lowered to signal the end of
the flight, the extension lines were clamped near the manifolds, the silastic
tubing segments on the Hamilton syringes were clamped and separated from the
manifolds, and then submersed in an icewater slurry to quench the red
cells' metabolism prior to analysis. Blood gas tension and pH analyses were
completed within 5 min after sample collection, and total oxygen content
analyses were completed with in 7 min after sample collection. Deep body
temperature was measured within 1 min after the bird landed by the previously
described procedure. Cardiac output and stroke volume were calculated for each
experiment using the Fick equation.
Heart rate measurements. Measurement of a bird's heart rate during flight was made on the day following the blood gas sampling experiment using the same wind tunnel conditions (horizontal flight at 18.4 m s1 and ambient temperature of 1012°C). The PVPheparin solution was removed from the arterial cannula and the bird systemically heparinized as previously described. The arterial cannula was then connected to the pressure transducer attached to the back of the bird with a Velcro® square. The heart rate reported for each bird is the mean value calculated from data collected throughout the sixth minute of flight, to coincide with the same time in the flight when blood samples were collected.
After these measurements were completed, the bird was killed and the position of the tip of the venous cannula in the right atrium was checked. The heart was then excised, its chambers were open and blotted free of blood and the mass of the heart was (MH) was determined to the nearest 0.01 g using a Mettler balance.
Assessment of protocols used for collecting and storing whole blood samples
These tests were carried out for two reasons: (1) to learn the best method
of preserving the blood gas tensions of whole blood samples during collection
and temporary storage, and (2) to determine whether whole blood metabolism
and/or tubing permeability were factors to consider in reporting final blood
gas tensions and pH values.
Collection of blood samples and extension line permeability
Mixed venous pigeon blood (0.5 ml) was collected in a Hamilton syringe at
room temperature (22°C) and a sample immediately injected into the blood
gas analyzer for analysis. The Hamilton syringe was then attached to an
extension line of equal length and composition used in the resting
experiments. The extension line was filled with blood and its free end was
clamped to prevent contaminating the blood with room air. Samples of blood
from the free tip of the extension line were then injected into the analyzer
every 5 min until the syringe was empty. This procedure was repeated at
12°C (i.e. the ambient temperature of the environmental chamber and wind
tunnel). Oxygen tension data were plotted against time and the slope was
calculated for both temperatures.
Whole blood metabolism and storage
A 0.5 ml sample of mixed venous pigeon blood collected in a Hamilton
syringe was immediately injected into the blood gas analyzer for assay. After
sealing off the syringe's needle with a short segment of silastic tubing, the
syringe was submersed in an icewater slurry. Injections were repeated
every 5 min until the syringe was empty. This procedure was carried out at the
temperatures of 22 and 12°C, and with the Hamilton syringe submersed in
the ice-water slurry (1°C) during injections. Oxygen tension results were
plotted against time and the slope was calculated for each temperature.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
During both resting and flight experiments, preservation of the oxygen
tension of blood samples during collection is seen by the notable reduction of
the PO2 rate in going from 22°C to
12°C (Table 1). This
reduction in blood temperature takes place as the blood passes through the
extension line, which acts as a heat exchanger and brings the blood into
thermal equilibrium with the air of environmental chamber or wind tunnel,
preserving the oxygen tension of each arterial and mixed venous blood sample
used in our results.
Using an icewater slurry for storage of blood samples prior to analysis proved to be the most effective method of preserving the oxygen tension of blood samples (Table 1).
Although not measured, we would expect similar drifts in the carbon dioxide tension and pH values of whole blood samples using the methods of collection and storage described here.
In summary, these preliminary tests indicated that under the sampling and temporary storage conditions used in this study, the influences of cannula extension line permeability and whole blood metabolism prior to analysis on the blood gas tensions and pH of analyzed samples was negligible. Accordingly, no attempt was made to correct the final measured values for these influences.
Resting and flight cardiorespiratory data Resting and flight data are presented in Tables 2, 3 and 4.
Adjustments of pigeons to flight
Our pigeons satisfied their 17.4-fold increase in
O2 with a
7.4-fold increase in cardiac output (
)
and a 2.4-fold increase in blood oxygen extraction (EB).
Cardiac output was increased primarily by an increase in the heart rate
(fH) (sixfold), and stroke volume (VS)
increased only modestly (Table
2). The similarity of the resting and flight
PaO2 and CaO2
values indicates a close matching of respiratory adjustments and metabolic
requirements (Table 3). The
fall in PaCO2 and the associated respiratory
alkalosis that accompanied flight, however, indicate hyperventilation during
flight (Table 3). These data
suggest some exchange limitations for oxygen during flight that required the
higher relative ventilation to maintain
PaO2.
|
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Aside from these two studies, all other cardiorespiratory studies on flying
birds have been of limited scope in the sense that they did not
directly measure all of the Fick equation parameters needed to fully
assess a given animal's cardiorespiratory performance
(Bishop, 1997;
Bishop and Butler, 1995
). To
circumvent this problem, various researchers have combined data from
incomplete studies on different avian species flying at disparate flight
conditions in order to derive allometric equations for estimating the various
Fick equation parameters for a generalized bird
(Bishop, 1997
;
Bishop and Butler, 1995
). In
the second part of our discussion, we will evaluate how accurately Bishop's
allometric equations (Bishop,
1997
) can estimate the cardiorespiratory parameters that we
measured from our flying pigeons.
Because of their different evolutionary histories, birds and mammals use
different cardiorespiratory designs and resources to satisfy their metabolic
requirements. Nevertheless, the maximal aerobic capabilities
(O2max) of
flying birds and bats are essentially the same, but are about twice those of
running mammals of similar size (Thomas,
1975
). This is because flying vertebrates combine the
O2max-enhancing
influences of small body size (allometric variation) and an athletic lifestyle
(adaptational variation), whereas similar-sized non-flying mammals (e.g. mice
and rats) have consistently adapted `non-athletic' lifestyles. Only after body
size exceeds about 2 kg do examples of `highly athletic' running mammals begin
to appear. Finally in our discussion, we consider what Fick parameter
adaptations and adjustments distinguish our exercising pigeons from those of
running mammals of various sizes. Particular attention will be given to how
the heart-mass-specific stroke volumes, cardiac outputs and cardiac work
capabilities of our flying pigeons compare with those of exercising mammals of
different body masses and aerobic capabilities.
Comparison of the current resting and flight data with previous studies
Resting data
Resting data from the present study (`PS') are compared in
Table 4 with corresponding
pigeon data reported by Butler et al.
(1977) (`B'). As is readily
apparent from the PS/B ratios, the resting
O2/Mb,
/Mb,
fH and VS/Mb
values of our pigeons are substantially lower than those reported by Butler.
One important reason for this discrepancy is the difference in `resting'
conditions that were used. While Butler's resting data were obtained from
masked pigeons perched inside a wind tunnel, our data were collected from
birds quietly resting in a darkened chamber to which they were previously
familiarized. Consistent with this interpretation are the
O2/Mb
and
/Mb values
reported by Grubb (1982
) for
pigeons resting at conditions similar to those of the present study. Grubb's
values agree to within 3% and 12%, respectively with our values. A second
probable reason for discrepancies in these PS/B ratios is that the
O2/Mb
value used by Butler in his 1977 study to calculate resting
/Mb and
VS/Mb came from his earlier study
(Butler, 1970
), which used
resting conditions different from those in his later study. Finally, the
different hematocrit values measured in these two studies are an important
factor accounting for the observed CaO2 and
C
O2
discrepancies, as indicated by the similarity of the PS/B ratios for Hct,
CaO2,
C
O2 and
CaO2C
O2
(Table 4). The hematocrit value
reported by Butler's group is substantially lower than the weighted mean value
of 55.2% that we calculated from data reported for a total of 293 pigeons by
five different groups of investigators
(Gayathri and Hegde, 1994
;
Kalomenopolou and Koliakos, 1989; Viscor et al., 1985;
Bond and Gilbert, 1958
;
Kaplan, 1954
). In summary,
differences in resting conditions used, methodologies concerning the source of
the oxygen consumption value used in the Fick equation, and very different
hematocrit values, appear to be primary factors contributing to the observed
PS/B ratio discrepancies observed in these two studies (Tables
4 and
5).
|
Flight data
The flight
O2/Mb
of our pigeons was about 1.6 times that of Butler's pigeons
(Table 4). A reason for this
difference could be the substantially different wind tunnel air speeds used in
the current study (18.4 m s1) and Butler's study (10 m
s1). Most birds, however, show little change in oxygen
consumption over the range of air speeds at which they fly in a wind tunnel
(Ellington, 1991
). Grippler
and Grivuni strains of pigeons show only a 10% change in
O2/Mb
over a range of wind tunnel flight speeds from 8 to 14 m s1
(Rothe et al., 1987
). These
investigators reported a
O2/Mb
value of 310 ml (kg min)1 for their pigeons flying at 10 m
s1, a value 1.6 times greater than Butler's value despite
the same air speed, but essentially the same as that measured from our pigeons
flying at 18 m s1.
Concerning flight speed, pigeons have been reported flying in nature at
speeds of 16.1 m s1
(LeFebvre, 1964), 18.3 m
s1 (Skutch,
1991
), 19.1 m s1
(Polus, 1985
), and 19.7 m
s1 (Levy,
1986
). Record-holding homing pigeons have achieved average flight
speeds of 22 m s1 during long distance races in calm air
(Levy, 1986
). Thus, the air
speed used in the current study (18.4 m s1) is within the
range of air speeds that pigeons normally fly at in nature. The highest speeds
that unencumbered Grippler pigeons will fly at in a wind tunnel is 18 m
s1 (Rothe and
Nachtigall, 1987
). Our birds, however, were equipped with a mask
and associated gas sampling tubes (metabolic determinations), or pressure
transducers (heart rate determinations), or cannula extension lines (blood
sampling), which contributed extra drag during these measurements. Based on
determinations from other species of flying vertebrates
(Thomas, 1975
), we assume that
the metabolic rates of our pigeons may have been about 10% to 15% higher than
those expected during unencumbered flight at the same air speed, but may
approximate the metabolic requirements of unencumbered flight at the higher
speeds that these bird sometimes achieve in nature
(Levy, 1986
).
There are reasons to believe that the flight
O2 value
reported in Table 2 for our
pigeons is near the maximal value that these birds are capable of achieving in
nature. The flight
O2 of our birds
is only 10% less than the highest specific
O2 that Rothe et
al. (1987
) were able to
measure from their somewhat smaller sized Grippler and Grivuni strains of
pigeons during flight at their maximum encumbered speed (14 m
s1). Also, most of our pigeons would only fly steady for a
maximum period of about 10 min while carrying the various types of measuring
and blood sampling equipment. Accordingly, we will hereafter assume that our
homing pigeons were operating either very close to, or at their
O2max
capability, and the flight cardiorespiratory data we obtained represent the
maximal, or very near the maximal, values that these birds are capable of.
Flight fH, VS, CaO2CO2 and
Despite the substantially higher flight
O2/Mb
of our pigeons, the flight fH,
VS/Mb and thus, the specific
of our birds, are generally similar
to those of Butler's birds (Table
4). This relationship appears to be primarily attributable to the
higher hematocrits (Hct) of our birds, as previously discussed, that allow
them to achieve a much higher CaO2
(Table 4). This, along with
their somewhat lower
C
O2, allowed
our pigeons to deliver 1.6 times more oxygen to their tissues per unit blood
flow compared to Butler's pigeons (Table
4). Thus, our pigeons' higher
CaO2C
O2
value allowed them to satisfy their substantially higher flight
O2/Mb
with approximately the same
/Mb as Butler's
pigeons.
Pigeon flight/rest ratio data
How do the factors by which our pigeons increase their resting
cardiorespiratory parameters to accommodate the increased metabolic
requirement of flight compare with those of Butler's pigeons? Flight/Rest
(F/R) ratios for these two studies are summarized in
Table 5. As expected from the
foregoing relationships, each Fick parameter F/R ratio shown in
Table 5 is higher for our birds
than for those in Butler's study (Butler
et al., 1977).
Comparison of cardiorespiratory data obtained in the current study to those predicted from allometric equations
Allometric equations are a powerful tool for understanding fundamental
relationships between the physiological capabilities and the morphological
dispositions and design constraints of different animals
(Taylor and Weibel, 1991).
Bishop (1997
) has recently
published a very comprehensive allometric evaluation of the maximum
cardiorespiratory capabilities of exercising birds and mammals. He concluded
that avian heart muscle has the same biomechanical performance as that of a
terrestrial animal. Accordingly, by making some simplifying assumptions about
the magnitude of the
CaO2C
O2
term in the Fick equation, Bishop
(1997
) showed that heart mass
(MH) and
O2max data from
mammals could be used to calculate reasonable estimates of a flying bird's
O2max.
Bishop (1997) presented two
different methods for predicting a flying bird's
O2max. Method 1
takes a hierarchical approach, and has the reader use his allometric equations
to estimate fH from Mb (equation 3)
and VS from MH (equation 6), if they
are not known, and to estimate
CaO2C
O2
from blood hemoglobin concentration (Hgb). Bishop's Method 2 simply assumes
that
max is a function of
MH and that there is no difference between birds and
mammals during maximal cardiac performance. Thus, for both birds and mammals,
Bishop's equation 10 (Bishop,
1997
) is used to calculate
max from the animal's
MH, and
CaO2C
O2
is estimated from Hgb as in Method 1. How precisely do Bishop's Method 1 and
Method 2 allometric equations (Bishop,
1997
) estimate the cardiorespiratory parameters that we directly
measured from our flying pigeons?
Heart rate (Method 1)
The flight fH from our pigeons our pigeons is about 12%
greater than the predicted value (Table
6, Row 1). This underestimation is expected, since Bishop's
equation 3 is from an earlier study (equation 9 of
Bishop and Butler, 1995), which
summarized the minimum metabolic requirements of flying birds, and which
included some low-quality (e.g. non steady-state, non
O2max avian
fH data. Bishop pointed out that the data he used to
formulate equation 3 may not represent true maximal fH
values, but he assumed that hey were close to maximal values for the purpose
of his analysis since better data were unavailable
(Bishop, 1997
). Some of this
discrepancy may also reflect real inter-species differences in maximum heart
rate, and that pigeons may be a species with a high maximum. Using Bishop's
Mb exponent and adjusting its coefficient to be consistent
with our data, yields the following relationship between
Mb (kg) and maximum fH (beats
min1) for highly athletic birds like pigeons flying at
O2max
conditions:
![]() | (1) |
|
Heart mass
Most of Bishop's allometric equations
(Bishop, 1997) relate the
cardiorespiratory parameter to heart mass, rather than to body mass, so
MH is an important attribute to consider
(Table 6). Bishop's equation
11, in turn, lets one calculate a mean population MH of a
bird from its Mb. The calculated MH
for our pigeons is more than 20% less than the measured value
(Table 6, Row 2). Concerning
our MH value Magnan
(1922
), in his comprehensive
study of birds, reported a mean pigeon MH of 1.294% of
Mb, which corresponds to a mean MH of
4.57 g for the 0.353 kg flying pigeons we studied. This differs by only 2%
from our measured MH value
(Table 6).
The large discrepancy between allometrically calculated and measured
MH for a bird like a homing pigeon is not surprising for
the following reasons. Heart mass is importantly influenced by adaptive
specialization. As Bishop's study (Bishop,
1997) clearly demonstrates, you need to know an animal's
MH before any reliable predictions can be made. Homing
pigeons are clearly a `highly athletic' species of bird since they can fly for
over 10 h a day at very high speeds (Levy,
1986
). Thus, homing pigeons share with other highly athletic birds
(e.g. humming birds, swifts, starlings and wild ducks) disproportionately
large specific heart masses (Hartman,
1961
; Magnan,
1922
). In formulating equation 11, Bishop used data from Magnan's
comprehensive study (Magnan,
1922
) that included both athletic and substantially less athletic
species of birds. Accordingly, his equation tends to underestimate the
MH of highly athletic avian species. Using the same
Mb exponent that Bishop used in his equation 11, and
adjusting its coefficient to fit our data, yields the following relationship
between Mb (kg) and MH for our pigeons
(and perhaps other highly athletic birds):
![]() | (2) |
Stroke volume
Bishop's equation 6 (Bishop,
1997) predicts a flying bird's maximal VS from
MH. Substituting our pigeon's mean measured
MH into this equation yields a predicted
VS that is almost 20% higher than our measured value
(Table 6, Row 3). What are the
reasons for this discrepancy? Bishop's equation 6
(Bishop, 1997
) also comes
directly from an earlier study (Bishop and
Butler, 1995
) that used VS data for pigeons
flying at minimum power speed (Bishop et al., 1977) to estimate the
coefficient of this equation. As was discussed previously, even though the
flight
O2 of
Butler's pigeons was only about two-thirds that of our birds, their
Fick-calculated VS value was about 6% higher than our
value because of their low CaO2 value, which in
turn, resulted from the abnormally low Hct values in their birds
(Table 4). Accordingly, only
part of the observed 20% discrepancy is explained by the
VS value that Bishop and Butler used to determine their
equation's coefficient.
Because Butler et al.
(1977) did not measure the
MH of their pigeons, Bishop and Butler
(1995
) assumed their
MH was 1.1% of Mb, as reported by
Grubb (1982
). This value is
lower than the 1.23% we measured from our birds. Accordingly, the lower
MH that Bishop and Butler
(1995
) used to formulate the
coefficient of their flight VS equation resulted in a
higher coefficient magnitude, which results in an overestimation of
VS when our (higher) measured pigeon
MH value is substituted into Bishop's equation 6. In
summary, the higher VS value and the lower
MH value that Bishop and Butler
(1995
) used to formulate their
avian flight VS equation both contribute to its
overestimation of our pigeons flight VS value
(Table 6, Row 3). Based on our
data, a more appropriate form of Bishop's equation 6 that relates maximum
flight VS (ml beat1) to
MH (g) is:
![]() | (3) |
Arteriovenous oxygen content difference (Method 1 and Method 2)
In the absence of actual flight
CaO2CO2
measurements (remembering that only pigeon values are currently available),
Bishop used blood hemoglobin concentration data ([Hgb]; g
ml1) to estimate blood oxygen carrying capacity
([Hgb]x1.36 ml O2 ml1 blood). When [Hgb]
data were unavailable, Bishop assumed the mean value of 0.1513 g
ml1 reported by Prinzinger and Miscovic
(1994
) from a comprehensive
survey of birds. Bishop then estimated CaO2 by
assuming that the arterial blood of a bird flying at
O2max conditions
was 94% saturated with oxygen, which is the mean value reported for seven
species of mammals (mostly of large body size) running at
O2max conditions
(Bishop, 1997
). Bishop
estimated the flying bird's
C
O2 by assuming
a value of 0.038 ml O2 ml1, which again is the
mean value for seven species of mammals running at
O2max
conditions. These assumptions are embedded in the two methods Bishop used for
estimating the
O2max of a
flying bird. How closely do these largely mammalian-based assumptions and the
resulting
CaO2C
O2
estimates correspond to those measured from our homing pigeons flying at what
we assume are
O2max
conditions?
While we did not measure [Hgb] for our birds, McGrath
(1971) reported a mean blood
hemoglobin of 15.6 g% for his pigeons whose mean Hct was similar to our value
(i.e. 52.6% vs 51% in our study). Proportional scaling and units
conversion indicates a [Hgb] of 0.151 g ml1 for our birds,
which is in excellent agreement with the default avian [Hgb] that Bishop
assumes in his equations (see above). According to Bishop's assumptions, this
[Hgb] would translate to an estimated flight
CaO2 of 0.193 ml O2
ml1 for our pigeons, which is only slightly higher than our
measured value of 0.188 ml O2 ml1
(Table 3). Finally, our finding
that the CaO2 values of our resting and flying
pigeons are almost the same (Table
3) indicates that arterial blood saturation does not fall as these
birds go from quiet rest to heavy exercise.
Based on Bishop's assumptions, our pigeons should be capable of an
estimated flight
CO2 of 0.038 ml
O2 ml1; a value about 20% lower than the measured
value (Table 3). Again, it is
not known whether this difference reflects the possibility that our pigeons
were not flying at
O2max conditions
(as we have assumed) or the possibility that flying birds, for
thermoregulatory or other reasons, may be incapable of achieving
C
O2 values as
low as highly athletic exercising larger-size mammals. In summary, the
predicted
CaO2C
O2
measured from our pigeons flying at
O2max is about
10% lower than the calculated value (Table
6, Row 4).
Cardiac output (Method 1 and Method 2)
Method 1: Our measured is
18% lower than the value predicted by multiplying our measured
fH by the VS value estimated from
Bishop's equation 6 (Bishop,
1997
; i.e. Method 1, see Table
6, Row 5). Surprisingly, our measured
is more accurately predicted by
multiplying the fH value estimated from Bishop's equation
3 by the VS value estimated from his equation 6. In the
latter case, our measured
is only
about 8% lower than the predicted value. These overestimates of
are primarily attributable to the
previously discussed fact that Bishop's equation 6
(Bishop, 1997
) overestimates
the VS of our pigeons
(Table 6, Row 3).
Method 2: Bishop's Method 2 (equation 10;
Bishop, 1997), however, very
precisely predicts the flight
of our
pigeons (Table 6, Row 5).
Accordingly, our
data provide strong
support for Bishop's assumption that
max is simply a function of
MH (Bishop,
1997
).
Maximum rate of oxygen consumption (Method 1 and Method 2)
How accurately do Bishop's two methods
(Bishop, 1997) estimate the
mean
O2max value
we determined for our flying pigeons? Our measured
O2max value is
about 18% less than the value predicted by Bishop's Method 1 when our
MH value was used to estimate VS, and
all other variables were estimated by Method 1 procedures. Our measured
O2max value is
only about 11% less than that predicted by Bishop's Method 2, however
(Table 6, Row 6). This level of
agreement is quite good considering all the variables that can influence
O2max. This
discrepancy might reflect an inaccuracy in our assumption that our pigeons
were flying at
O2max
conditions, or inaccuracies in one or more of the previously discussed
assumptions or relationships that Bishop used to formulate his equation 10.
These relationships support Bishop's
(Bishop, 1997
) suggestion that
his Method 2 is the preferred way to estimate a flying bird's
O2max.
Relations between cardiorespiratory parameters measured in the current study and those predicted by allometric equations for running mammals
How do the cardiorespiratory parameters of our flying pigeons compare with
those predicted by Bishop's allometric equations for a mammal of this size
running at O2max
conditions (Bishop, 1997
)?
These relationships are summarized in Table
7 and the findings are reported below.
|
Fick parameters
The O2max of
our pigeons was about 1.5x that predicted for an athletic running mammal
of the same size (Table 7, Row
6). Of course, very few (if any) running mammals of this size are athletic, so
this
O2max
differential is usually significantly greater when a typical small running
mammal is compared to our pigeons. For example, the mass-specific
O2max of our
pigeons is more than 3x greater than that of a trained running rat
(Gleeson et al., 1983
).
The higher (1.5-fold)
O2max of our
pigeons is associated with a disproportionately larger (1.8-fold) heart mass,
and Q (1.7-fold) compared to values predicted for an athletic running
mammal of this size (Table 7,
Row 5). The higher
of our pigeons
results from its ability to achieve fH and
VS values that are both about 20% higher than those
expected for a running mammal of the same size
(Table 7, Rows 1 and 3). The
fact that the ratio of `present study/predicted' for MH
and
in
Table 7 are generally similar
supports Bishop's assumption that MH is a valid indicator
of an animal's maximum
capability
(Bishop, 1997
).
In summary, the superior blood oxygen convection capabilities of our pigeons over running mammals of equivalent size are primarily attributable to their ability to achieve higher heart rates and greater stroke volumes simultaneously from their larger size hearts.
Heart mass-specific cardiorespiratory performances of flying pigeons and exercising mammals
As stated previously, a primary underlying assumption of Bishop's
comprehensive analysis was that avian heart muscle has the same maximal
physiological performance capability as mammalian heart muscle
(Bishop, 1997). In this final
part of our discussion, we will examine how closely the heart mass-specific
cardiac performances of our flying pigeons correspond to those reported for
certain non-athletic and highly athletic mammals exercising at or near
O2max
conditions.
It has been known for some time that high Mb-specific
heart mass (MH/Mb) distinguishes
highly athletic animals from their less athletic counterparts. The 4.6-fold
MH/Mb difference between the pigeon
and the exercise-trained rat is particularly striking
(Table 8), and reflects the
fact that the body mass-specific
O2max of our
pigeons is more than three times greater than that of a rat
(Gleeson et al., 1983
).
Although MH/Mb is generally similar in
highly athletic mammals of very different body sizes, our pigeons' value is
the highest of any of the animals shown in
Table 8.
|
The relatively high flight fH of our pigeons compared to a flying bird or a running mammal of the same size has been discussed previously (Tables 6 and 7). The latter relationship is further supported by the fact that our pigeon's flight fH exceeds the running rat's maximum value despite the latter's substantially smaller body mass (Table 8).
Data summarized in Table 8
show no consistent relationship between athletic ability or body size and
MH-specific VS
(VS/MH). Since available data indicate
that running mammals and flying birds have similar mean systemic arterial
blood pressures (Bishop, 1997),
the data in Table 8 suggest
that the maximum MH-specific stroke work capability of our
pigeons is somewhat less than that of a running rat. Perhaps this is a
trade-off that pigeons have had to accept in gaining the advantages of having
a relatively large size heart that can achieve a relatively high
fH.
Due in part to the inverse relationship between maximum
fH and body mass, MH-specific
(
/MH) decreases
with increasing body mass (Table
8). Accordingly, the most valid
/MH comparisons
are between animals of generally similar body mass. There is reasonably close
correspondence between the pigeon's
/MH value and that
reported for the running rat or estimated for two species of flying bats
(Table 8). Since flying birds
and running mammals have similar mean systemic arterial blood pressures
(Bishop, 1997
), the
MH-specific cardiac work rate capabilities
(WH/MH) of birds and smaller size
mammals also appear to be generally similar. In summary,
/MH data from our
pigeons provide additional direct support for one of Bishop's central
assumptions, that avian heart muscle has the same maximal physiological and
biomechanical performance as that from terrestrial mammals. Particularly
impressive to us is the ability of 1 g of pigeon myocardium to achieve a
/MH value that
approaches that of a running rat, even though this bird is operating at a
/Mb level during
flight that is about four times greater than that of the running rat. The
physiological mechanisms that enable homing pigeons to achieve such a high
level of cardiovascular performance are still not completely understood. Some
important contributing factors, however, may be the robust plasma
catecholamine response that accompanies pigeon flight
(Liang and Thomas, 1994
), and
the possibility that flying pigeons maintain advantageous phase relationships
between their cardiac and pectoral muscle (wing-beat) cycles
(Thomas et al., 1996
).
![]() |
List of symbols |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
![]() |
Acknowledgments |
---|
![]() |
Footnotes |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Adams, N. J., Pinshow, B. and Gannes, L. Z. (1997). Water influx and efflux in free-flying pigeons. J. Comp. Physiol. B 167,444 -450.
Bevan, R. M., Woakes, A. J., Butler, P. J. and Boyd, I. L.
(1994). The use of heart rate to estimate oxygen consumption for
free-ranging black-browed albatrosses Diomedea melanophrys. J. Exp.
Biol. 193,119
-137.
Bevan, R. M., Woakes, A. J., Butler, P. J. and Croxall, J. P. (1995). Heart rate and oxygen consumption of exercising gentoo penguins. Physiol. Zool. 68,855 -877.
Bishop, C. M. (1997). Heart mass and the maximum cardiac output of birds and mammals: implications for estimating the maximum aerobic power output of flying animals. Phil. Trans. R. Soc. Lond. B 352,447 -456.[CrossRef]
Bishop, C. M. and Butler, P. J. (1995). Physiological modeling of oxygen consumption in birds during flight. J. Exp. Biol. 198,2153 -2163.[Medline]
Boggs, D. F., Jenkins, F. A., Jr and Dial, K. P.
(1997a). The effects of the wing beat cycle on respiration in
black-billed magpies (Pica pica). J. Exp.
Biol. 200,1403
-1412.
Boggs, D. F., Seveyka, J. J., Kilgore, D. L. and Dial, K. P.
(1997b). Coordination of respiratory cycles with wing beat cycles
in the black-billed magpie (Pica pica). J. Exp.
Biol. 200,1413
-1420.
Bond, C. F. and Gilbert, P. W. (1958).
Comparative study of blood volume in representative aquatic and non-aquatic
birds. Am. J. Physiol.
194,519
-521.
Butler, P. J. (1970). The effect of progressive hypoxia on the respiratory and cardiovascular system of the pigeon and duck. J. Physiol. Lond. 201,527 -538.
Butler, P. J., West, N. H. and Jones, D. R. (1977). Respiratory and cardiovascular responses of the pigeon to sustained level flight in a wind tunnel. J. Exp. Biol. 71, 7-26.
Carmi, N., Pinshow, B., Horowitz, M. and Bernstein, M. H. (1993). Birds conserve plasma volume during thermal and flight-incurred dehydration. Physiol. Zool. 66,829 -846.
Carmi, N., Pinshow, B. and Horowitz, M. (1994). Plasma volume conservation in pigeons: effects of air temperature during dehydration. Am. J. Physiol. 267,R1449 -R1453.[Medline]
Carpenter, R. E. (1985). Flight physiology of flying foxes, Pteropus poliocephalus. J. Exp. Biol. 114,619 -647.
Christensen, M., Hartmund. T. and Gesser, H. (1994). Creatine kinase, energy rich phosphates and energy metabolism in heart muscle of different vertebrates. J. Comp. Physiol. 164B,118 -123.
Ellington, C. P. (1991). Limitations on animal flight performance. J. Exp. Biol. 160, 71-79.
Gayathri, K. L. and Hegde, S. N. (1994) Sexual differences in blood values of the pigeon, Columba livia. Comp. Biochem. Physiol. 109B,219 -224.[CrossRef]
George, J. C. and John, T. M. (1993). Flight effects on certain blood parameters in homing pigeons Columba livia.Comp. Biochem. Physiol. 106,707 -712.[CrossRef]
Giladi, I., Goldstein, D. L., Pinshow, B. and Gerstberger,
R. (1997). Renal function and plasma levels of arginine
vasotocin during free flight in pigeons. J. Exp. Biol.
200,3203
-3211.
Gleeson, T. T., Mullin, W. J. and Baldwin, K. W.
(1983). Cardiovascular responses to treadmill exercise in rats:
effects of training. J. Appl. Physiol.
54,789
-793.
Grubb, B. R. (1982). Cardiac output and stroke
volume in exercising ducks and pigeons. J. Appl.
Physiol. 53,207
-211.
Hartman, F. A. (1961). Motor mechanisms of birds. Smithson. Misc. Coll. 143, 1-91.
Hissa, R., John, M. T., Palo, B., Viswanathan, M. and George, J. C. (1995). Noradrenaline-induced hypothermia is suppressed in the vagotomized cold-exposed pigeon. Comp. Biochem. Physiol. 111A,89 -97. 71.[CrossRef]
Jones, J. H., Longworth, K. E., Lindholm, A., Conley, K. E.,
Karas, R. H., Kayar, S. R. and Taylor, C, R. (1989).
Oxygen transport during exercise in large mammals. I. Adaptive variation in
oxygen demand. J. Appl. Physiol.
67,862
-870.
Kalomenopoulou, M. and Koliakos, G. (1989). Total body haematocrit iron kinetics and erythrocyte life span in pigeons (Columba livia). Comp. Biochem. Physiol. 92A,215 -218.[CrossRef]
Kaplan, H. M. (1954). Sex differences in the packed cell volume of vertebrate blood. Science 120, 1044.
Karas, R. H., Taylor, C. R., Rosler, K. and Hoppeler, H. (1987). Adaptive variation in the mammalian respiratory system in relation to energetic demand. V. Limits to oxygen transport by the circulation. Resp. Physiol. 69, 65-79.[CrossRef]
LeFebvre, E. A. (1964). The use of D2O18 for measuring energy metabolism in Columba livia at rest and in flight. Auk 81,403 -416.
Levy, W. M. (1986). The Pigeon. Sumter, SC: Levi Publishing.
Liang, W. and Thomas, S. P. (1994). Heart rate and plasma catecholamine responses to flight in pigeons. Physiologist 35,236 .
Maginniss, L. A., Bernstein, M. H., Deitch, M. L. and Pinshow, B. (1997). Effects of chronic hypobaric hypoxia on blood oxygen binding in pigeons. J. Exp. Zool. 277,293 -300.[CrossRef]
Magnan, A. (1922). Les caracteristiques des oiseauz suivant le mode de vol. Ann. Nat. Sci. 10,125 -334.
McGrath, J. J. (1971). Acclimation response of
pigeons to simulated high altitudes. J. Appl. Physiol.
31,274
-276.
Novoa, F. F., Rosenmann, M. and Bozinovic, F. (1991). Physiological responses of four passerine species to simulated altitudes. Comp. Biochem. Physiol. 99A,179 -183.[CrossRef]
Polus, M. (1985). Quantitative and qualitative respiratory measurements on unrestrained free-flying pigeons by AMACS (airborne measuring and control systems). In BIONA Report 3, Akada Wiss Mainz (ed. W. Nachtigall), pp.293 -301. Stuggart, Germany: G. Fisher.
Prinzinger, R. and Miscovic, A. (1994). Vogelblut-eine allornetrische Ubersicht der Bestandteile. J. Orn. 135,133 -165.[CrossRef]
Rothe, H. J. and Nachtigall, W. (1987). Pigeon flight in a wind tunnel. I. Aspects of wind tunnel design, training methods and flight behavior of different pigeon races. J. Comp. Physiol. B 157,91 -98.
Rothe, H. J., Biesel, W. and Nachtigall, W. (1987). Pigeon flight in a wind tunnel. II. Gas exchange and power requirements. J. Comp. Physiol. B 157,99 -109.
Schwilch, R., Jenni, L. and Jenni, E. S. (1996). Metabolic responses of homing pigeons to flight and subsequent recovery. J. Comp. Physiol. B 166, 77-78.
Skutch, A. (1991) Life of a Pigeon. Ithaca, NY: Cornell University Press.
Taylor, C. R. and Weibel, E. R. (1991). The Lung: Scientific Foundations. New York: Raven Press.
Thomas, S. P. (1975). Metabolism during flight in two species of bats, Phyllostomus hastatus and Pteropus gouldii. J. Exp. Biol. 63,273 -293.[Abstract]
Thomas, S. P. (1987). In Recent Advances in the Study of Bats (ed. M. B. Fenton, P. Racey and J. Rayner), pp. 75-99. New York: Cambridge University Press.
Thomas, S. P., Lust, M. R. and Van Riper, H. J. (1984). Ventilation and oxygen extraction in the bat (Phyllostomus hastatus) during rest and steady flight. Physiol. Zool. 57,237 -250.
Thomas, S. P., Rigoni, J. A., Mascilli, A. D., Schnepp, R. W. and Peters, G. W. (1996). Coordination between wing beat and cardiac cycle of flying pigeons. Physiology 39, A-22.
Tucker, V. A. (1968). Respiratory exchange and evaporative water loss in the flying pigeon. J. Exp. Biol. 48,67 -87.
Visor, G., Marques, M. S. and Polemic, J. (1985). Cardiovascular and organ weight adaptations as related to flight activity in birds. Comp. Biochem. Physiol. 82A,597 -599.[CrossRef]