Terrestrial locomotion does not constrain venous return in the American alligator, Alligator mississippiensis
Department of Ecology and Evolutionary Biology, University of California, 321 Steinhaus Hall, Irvine, CA 92697, USA
* Author for correspondence at present address: School of Veterinary and Biomedical Sciences, James Cook University, Townsville, QLD 4811, Australia (e-mail: suzy.munns{at}jcu.edu.au)
Accepted 22 June 2005
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Summary |
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Key words: exercise, hemodynamics, intra-abdominal pressure, locomotion, oxygen consumption, reptile, venous return, ventilation, central venous pressure, heart rate
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Introduction |
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Locomotion increases intra-abdominal pressure (IAP) in Varanus
exanthematicus (Munns et al.,
2004). High IAP (
20 mmHg; 1 mmHg=133.3 Pa), both at rest and
during exercise, was associated with decrements in post caval blood flow
(
PC) via decreases
in transmural pressure. Elevated IAP associated with decrements in
PC have also been measured
during exercise in Iguana iguana
(Farmer and Hicks, 2000
).
Elevated IAP can act to limit venous return when IAP exceeds central venous
pressure, causing partial or complete collapse of the main veins in the
abdominal compartment. Systemic venous return and ventricular preload are
major determinants of cardiac output, and thus reductions in venous return
have important impacts on oxygen delivery during exercise.
In contrast to the sprawling gait used by lizards
(Farley and Ko, 1997),
crocodilians use a semi-erect posture during locomotion (`high walk') in which
the body is held in an intermediate position between a sprawling and an erect
gait (Reilly and Blob, 2003
;
Reilly and Elias, 1998
).
Despite the differences in gait between lizards and crocodilians, both groups
experience a substantial degree of lateral trunk bending during locomotion
(Farley and Ko, 1997
;
Reilly and Elias, 1998
). In
addition, crocodilians possess significantly different ventilatory mechanics
compared with lizards. In crocodilians, the lateral and ventral portions of
the liver are attached to the pelvis by a diaphragmaticus muscle (Gans and
Clark, 1976b; Naifeh et al.,
1970a
,
1971
). Contraction of the
diaphragmaticus muscle retracts the liver caudally, increasing pleural cavity
volume and thus effecting lung inflation
(Farmer and Carrier, 2000a
;
Gans and Clark, 1976
;
Grigg and Gans, 1993a
). The
intercostal musculature is also active during inspiration
(Gans and Clark, 1976
), as are
the ischiopubis and ischiotruncus muscles, which act to expand the abdomen by
expansion of the ribs and ventral rotation of the pubic bones, respectively
(Farmer and Carrier, 2000a
).
By contrast, expiration is caused by contractions of the superficial
intercostal (Gans and Clark,
1976
), the transverse abdominal
(Farmer and Carrier, 2000a
;
Gans and Clark, 1976
) and the
rectus abdominius muscles (Farmer and
Carrier, 2000a
), which move the liver anteriorly and reduce the
volume of the abdominal cavity (Farmer and
Carrier, 2000a
; Grigg and
Gans, 1993a
). Thus, both inspiration and expiration are active in
crocodiles (Farmer and Carrier,
2000a
; Naifeh et al.,
1971
), and lung ventilation can be effected solely by use of the
hepatic piston pump (Gans and Clark,
1976
) or by use of costal ventilation
(Hartzler et al., 2004
) or by
a combination of both (Farmer and Carrier,
2000a
).
An important consequence of the ventilatory mechanics in alligators is the
separation of the muscles used for ventilation and locomotion. Activity of the
diaphragmaticus, transversus abdominius, rectus abdominius and ischiopubis
muscles is tightly correlated with the respiratory cycle in exercising
alligators, but these muscles are only intermittently active or are inactive
during locomotion (Farmer and Carrier,
2000a). Thus, despite alligators engaging in lateral bending of
the trunk during locomotion and having a similar posture to that of lizards
(factors predisposing them to ventilatory limitations during exercise),
alligators retain the ability to run and breathe at the same time
(Farmer and Carrier, 2000a
).
The lack of axial constraint in alligators may result in the generation of
lower abdominal pressures and a reduced venous flow limitation during
exercise.
The aim of this study was to determine the effects of treadmill exercise on aspects of the cardiovascular and respiratory systems in the American alligator, Alligator mississippiensis. We hypothesized that, due to the absence of axial constraint in crocodilians, any increase in IAP will be exceeded by elevations in central venous pressure, resulting in no suppression of venous return during exercise.
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Materials and methods |
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Surgical procedure, blood flow, intra-abdominal pressure and blood pressure
The surgical procedures used in this study are presented in detail for
Savannah monitor lizards (Varanus exanthematicus) in Munns et al.
(2004) and are briefly
described below. Alligators were lightly anesthetized by placing them in a
sealed container with gauze dampened with isofluorane (Isoflo; Abbott
Laboratories, North Chicago, IL, USA). Alligators were then intubated and
artificially ventilated (SAR-830; CWE Inc., Ardmore, PA, USA) with room air
that had been passed through a vaporizer (Dräger, Lubeck, Germany). The
vaporizer was initially set at 34% and was then reduced to 12%
for the majority of the surgery. A 35 cm ventral incision was made in
the abdomen, and two loose-fitting ultrasonic blood flow probes (2R; Transonic
System Inc., Ithaca, NY, USA) were placed around each post caval vein
(homologous to the mammalian inferior vena cava). In Alligator
mississippiensis, the two post caval veins carrying blood from the
hindlimbs, tail and pubic region do not fuse prior to entry into the liver;
instead, each post caval vein enters ipsilateral lobes of the liver directly.
Each ultrasonic blood flow probe was placed around one post caval vein
anterior to the kidney but posterior to its entry into the liver. The
intestinal, lienogastric, gastric and abdominal veins fuse to form the hepatic
portal vein, which enters the left lobe of the liver
(Schaffner, 1998
). Thus, the
venous return measured in this study comprises venous drainage from the
hindlimbs and tail but excludes drainage from the gastrointestinal tract,
which enters the liver anterior to the location of the blood flow probe. IAP
was measured using a pressure transducer (Millar Mikrotip; Millar Instruments,
Inc., Houston, TX, USA) sutured to connective tissue adjacent to the flow
probes. The probes were exteriorized through the lateral body wall
approximately 5 cm anterior to the pelvis and secured using 3-0 silk sutures
on the dorsal surface of the tail.
The femoral artery was cannulated in order to measure arterial blood pressure. A 12 cm incision was made in the ventral surface of the hindlimb. The femoral artery was exposed using blunt dissection techniques, and the artery cannulated with polyethylene tubing (I.D. 0.023 cm, O.D. 0.038 cm; Harvard Apparatus, Inc., Holliston, MA, USA) and secured using 3-0 sutures. Blood pressure was measured using disposable pressure transducers (model MLT0670; ADInstruments, Colorado Springs, CO, USA). The contralateral femoral vein was also cannulated to facilitate measurement of central venous pressure. A 3.5F pressure transducer (Millar Mikrotip; Millar Instruments, Inc.) was introduced into the femoral vein and advanced 810 cm into the central venous circuit.
All incisions were closed with interrupted sutures and treated with cyanoacrylate tissue adhesive (Vetbond; 3M, St Paul, MN, USA). Artificial ventilation with room air was continued until the alligator regained consciousness and reinitiated spontaneous breathing. Intramuscular injections of the antibiotic enrofloxican (Baytril; Bayer Corporation, Shawnee Mission, KS, USA) and the analgesic flunixin meglumine (Flunixamine; Fort Dodge, Madison, NJ, USA) were given at the conclusion of surgery. Enrofloxican injections were repeated every second day after surgery. A minimum recovery period of two days was given before commencement of experimentation.
Lung ventilation and gas exchange
Ventilation was measured using a mask constructed from the base of a 50 ml
polypropylene centrifuge tube (Corning Inc. Life Sciences, Acton, MA, USA).
Flexible tubing was attached via two ports drilled into the mask. The
mask was attached over the alligator's nostrils, and the mouth sealed closed
with a dental polyether impression material (Impregum F; 3M). Fresh room air
was drawn through the mask using a sealed aquarium air pump at a constant flow
rate of 1.21.7 l min1 (depending on the size of the
alligator). Care was taken to ensure that the flow rate though the mask
exceeded the rate of inspiration, thus minimizing the possibility of
rebreathing. Air flow through the mask was controlled with rotameters (Brooks
Instruments, Hatfield, PA, USA). Alterations in airflow due to ventilation
were measured using a pneumotachograph (8311; Hans Rudolph, Inc., Kansas City,
MO, USA) placed upstream of the mask, such that expirations caused an increase
in airflow and inspiration caused a decrease in airflow. Pressure gradients
induced by alterations in airflow across the pneumotachograph were monitored
using a differential pressure transducer (MP-45-1-871; Validyne, Northridge,
CA, USA). The signal from the differential pressure transducer was calibrated
by injecting and withdrawing known volumes of gas from the sealed mask and was
integrated to obtain tidal volumes. Gas from the mask was sub-sampled and
passed through Drierite® (anhydrous calcium sulfate) before
being passed through CO2 (CD-3A; Applied Electrochemistry, Inc.,
Sunnyvale, CA, USA) and O2 (S-3A; Applied Electrochemistry, Inc.)
analyzers. The rates of oxygen consumption
(O2) and carbon dioxide
production (
CO2) were
determined using a technique previously described
(Bennett and Hicks, 2001
;
Farmer and Hicks, 2000
;
Wang et al., 1997
). Briefly,
O2 and
CO2 of single breaths were
determined as the area below
(
O2) or above
(
CO2) the baseline signal
for room air. Exhalations were simulated by injecting known volumes of known
gas mixtures (21% O2, 79% N2; 100% N2; 15%
O2, 5% CO2, 80% N2) into the mask to
establish the relationship between this area and gas exchange. Minute
ventilation and tidal volume are reported at BTPS (body temperature and
pressure, saturated) and metabolic gas values at STPD (standard temperature
and pressure, dry).
Experimental protocol
Alligators were accustomed to walking and running on the treadmill in a
series of `training' bouts for a minimum of 3 months prior to experimentation.
Training bouts consisted of alligators repeatedly walking and running on the
treadmill at each of the experimental speeds (0.75, 1.0 and 1.5 km
h1) until exhaustion. Training bouts occurred three times a
week and continued until all alligators were able to maintain 4 min of
consistent locomotion at each treadmill speed (non consecutive). Alligators
were fasted for 7 days prior to surgery and were held at the experimental
temperature (30°C) for 23 days prior to experimentation. A mask was
attached over the alligator's nostrils and the alligator was placed on the
treadmill belt. The alligator was left on the stationary treadmill belt for at
least one hour before the treadmill was started to obtain pre-exercise
`resting' measurements. All alligators rested quietly on the treadmill during
the pre-exercise period. The exercise regime consisted of 4 min exercise bouts
at each of three treadmill speeds; 0.75, 1.0 and 1.5 km h1;
each 4 min exercise bout was separated by a minimum of 1 h at rest (during
which all experimental parameters returned to pre-exercise values). Locomotion
was initiated by gently tapping the treadmill belt behind the alligator or by
lightly touching the alligator's tail. Ventilatory and cardiovascular
parameters reached a steady state by 3 min of treadmill exercise at each
speed.
Data collection, analysis and statistics
All signals were collected on a computer at 100 Hz using Acknowledge data
acquisition software (Biopac, Goleta, CA, USA). Due to the intermittent and
variable nature of reptilian ventilation and the low breathing frequencies
employed at rest, ventilatory and cardiovascular parameters and
intra-abdominal pressure were calculated from the last 10 min of the
pre-exercise period prior to commencement of each exercise bout. Ventilation,
O2,
CO2, IAP, central venous
pressure (CVP) and
PC were
calculated from the last minute of treadmill exercise at each speed. Mean
arterial blood pressure and heart rate for the exercise period were calculated
from the first 10 s of the recovery period after each treadmill speed to avoid
any interference caused by the alligator's locomotion. All recovery period
data were calculated from a 60 s window 2 min after exercise ceased. Total
PC was calculated from the
sum of the left and right post caval flows.
The effect of increasing treadmill speed on all parameters was determined using paired Dunnett's tests with the rest period as the control (P<0.05). Comparisons of the recovery period with the maximal treadmill speed were performed using a paired t-test (P<0.05). All data presented are means ± S.E.M.
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Results |
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Treadmill exercise induced a rapid increase in
PC
(Fig. 3). Maximal
PC was achieved
within the first 20 s after the onset of exercise at 0.75 km
h1, after which there was no further significant increase in
PC. Maximal
PC was achieved
within 40 s after the onset of exercise at both 1.0 and 1.5 km
h1.
PC decreased slowly
during the recovery period after exercise and was still significantly elevated
compared with resting levels 10 min into the recovery period.
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Discussion |
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Respiratory cycle variations in venous return, IAP and CVP have not been
previously investigated in reptiles. Mammalian studies demonstrate that
inspiration causes opposing alterations in intrathoracic and intra-abdominal
pressure and hence have differing effects on regional venous blood flow.
Although some studies on locomoting mammals demonstrate a decrease in gastric
pressure during inspiration (Ainsworth et
al., 1989), most studies show that the caudal translation of the
diaphragm during inspiration results in compression of the viscera, increasing
IAP and collapsing the inferior vena cava
(Decramer et al., 1984
;
Guyton and Adkins, 1954
;
van den Berg et al., 2002
;
Wexler et al., 1968
). Collapse
of the inferior vena cava during inspiration decreases venous return from the
lower extremities and is associated with a decrease in splanchnic blood flow
(Abel and Waldhausen, 1969
;
Rabinovici and Navot, 1980
;
Willeput et al., 1984
). Left
ventricular stroke volume can also be reduced during inspiration in mammals
(Charlier et al., 1974
;
Hoffman et al., 1965
;
Ruskin et al., 1973
;
Schrijen et al., 1975
) due to
a fall in effective ejection pressure of the left ventricle
(Olsen et al., 1985
).
Contraction of the abdominal muscles during expiration aids venous return in
mammals (Abel and Waldhausen,
1969
; Youmans et al.,
1963
). In contrast to the inspiratory increase in IAP,
intrathoracic and right atrial pressures decrease during inspiration in
mammals, increasing blood flow in the veins located near the thorax, such as
the jugular and hepatic veins and the superior vena cava
(Abu-Yousef, 1992
;
Brecher and Hubay, 1955
;
Brecher and Mixter, 1953
;
Mixter, 1953
;
Moreno et al., 1967
;
Osada et al., 2002
;
Takata et al., 1992
;
Teichgraber et al., 1997
;
Willeput et al., 1984
).
Venous return is proportional to the ratio of the pressure gradient between
CVP and right atrial pressure. A decrease in right atrial pressure during
inspiration increases the pressure gradient between the central venous circuit
and the right atria, promoting venous return. In addition, venous return is
inversely related to venous resistance. In collapsible vessels, such as the
reptilian post caval vein, vessel cross-sectional area is largely determined
by PTRANS (Katz et
al., 1969; Kresh and
Noordergraaf, 1972
; Moreno et
al., 1970
). When IAP exceeds CVP, PTRANS
becomes negative, resulting in venous vessel collapse and an increase in the
viscous resistance to blood flow (Badeer
and Hicks, 1992
). Thus, increments in IAP during inspiration
decrease venous return. The variable effects of inspiration on venous return
are the result of the integration of the effects of intrathoracic pressure and
IAP on venous blood flow.
Unlike mammals, reptiles do not possess a muscular diaphragm. Crocodilians
do possess a sheath of connective tissue that connects the liver to the body
wall and creates separate thoracic and abdominal cavities
(Grigg and Gans, 1993a;
Hughes, 1973
). Crocodilians
are aspiration breathers, creating negative pressures within the thoracic
cavity to inflate the lungs. At the same time, caudal translation of the
visceral organs causes an increase in IAP. Thus, in alligators, a pressure
gradient is generated between the thoracic and abdominal cavities, similar to
that created during ventilation in mammals. Negative intrathoracic pressures
act to decrease right atrial pressures and increase the pressure gradient,
driving venous return, while increases in IAP act to compress the abdominal
veins (if IAP>CVP). Thus, the effects of inspiration on venous return are
complex and are the result of interactions between intrathoracic pressure,
IAP, right artial pressure and CVP.
Tidal volume increased in response to exercise in alligators, and
increments in treadmill speed were positively correlated with increasing tidal
volume (Fig. 6). The resting
tidal volumes measured in this study were equivalent to those measured in
previous studies (Farmer and Carrier,
2000b; Hicks and White,
1992
), although the maximum tidal volumes induced by exercise in
this study (55 ml kg1) were lower than those previously
presented at the same treadmill speed (85 ml kg1;
Farmer and Carrier, 2000b
).
The significant increments in tidal volume and minute ventilation that were
measured in response to increasing treadmill speed indicate that tidal volume
limitations during exercise were not present in alligators. By contrast,
costal tidal volumes decrease or remain unaltered with increasing treadmill
speed in Varanus exanthematicus
(Carrier, 1987
;
Munns et al., 2004
;
Wang et al., 1997
). Minute
ventilation during exercise was maintained in Varanus exanthematicus
due to the contribution of the gular pump, an accessory ventilatory mechanism
that forces air from the gular region into the lungs
(Munns et al., 2004
;
Owerkowicz et al., 1999
,
2001
). However, it is
important to note that the use of gular pumping during exercise is not
universal among varanid species. Varanus gouldi and Varanus
spenceri do not use gular pumping and increase tidal volumes during
exercise (Frappell et al.,
2002b
; Schultz et al.,
1999
).
Gular pumping is not present in alligators
(Brainerd, 1999;
Farmer and Carrier, 2000a
).
Some movement of air in and out of the buccal region in alligators was
measured in this (Fig. 1) and
other studies; however, these volumes do not contribute to gas exchange
(Farmer and Carrier, 2000b
;
Gans and Clark, 1976
; Naifeh
et al.,
1970a
,b
,
1971
). In contrast to the
positive correlation between treadmill speed and both minute ventilation and
tidal volume, rates of oxygen consumption and carbon dioxide production did
not increase with treadmill speed (Fig.
6). The low maximal rates of oxygen consumption measured during
exercise in alligators are indicative of the low aerobic capacity of this
species.
IAP and CVP increased during treadmill exercise in alligators; however, CVP
exceeded IAP at all treadmill speeds (Fig.
4), resulting in elevations in both PTRANS and
PC
(Fig. 5). By contrast,
elevations in IAP in varanid lizards resulted in a reduction in
PTRANS below zero, causing post caval vein collapse and a
52% reduction in
PC
(Munns et al., 2004
).
Elevations in IAP and reductions in
PC have also been
found during exercise in iguanid lizards
(Farmer and Hicks, 2000
).
During exercise in varanid lizards, elevated IAP resulted in the collapse of
the post caval vein and a pooling of blood in the peripheral circulation.
During the recovery period immediately after exercise ceased, IAP fell and
blood pooling in the periphery reentered the circulation, causing an increase
in
PC and MAP above
exercise values (Munns et al.,
2004
). Peak MAP and
PC occurred during
exercise in alligators and not during the recovery period, as was the case in
varanid lizards. This, in combination with the increase in
PTRANS, indicates that collapse of the post caval vein did
not occur during exercise in alligators.
Alligators had lower IAP at rest (5.90±1.78 mmHg) compared with
varanid lizards (11.09±2.14 mmHg)
(Munns et al., 2004). The
differences in IAP between varanids and alligators at rest may be due to a
number of factors, including the degree of gastrointestinal filling,
functional residual capacity of lungs, and resting body posture.
Interestingly, exercise induced increases in IAP of similar magnitude in
varanid lizards and American alligators (up to 170% and 150% of resting value,
respectively). The marked differences in the effects of IAP on
PC were the result of
the interactions of IAP, CVP and right atrial pressure. The large increases in
CVP (270%) in alligators were able to maintain positive
PTRANS during exercise, and thus prevent the inferior vena
caval collapse that limited
PC in exercising
varanid lizards. Thus, the key factor determining
PC during exercise is
not absolute IAP but rather the interaction of CVP and IAP, and the
maintenance of positive PTRANS. The high CVP generated
during exercise in alligators may be due to a number of factors. Movement of
the liver and elevated IAP during the inspiration act to impede venous return
and increase CVP, especially at high tidal volumes. In addition,
exercise-induced peripheral vasodilation may act to increase CVP, and the
liver may provide significant resistance to the flow of blood, thus increasing
the resistance to venous return and increasing CVP. While high CVP values
during locomotion have been measured in this study, the mechanisms underlying
this increase are outside the scope of this study.
Increments in treadmill speed did not correlate with additional increases
in heart rate, CVP, IAP, MAP (Fig.
4) or PC
(Fig. 3) in alligators. Similar
results were measured in varanid lizards, in which increments in treadmill
speed caused no further increase in heart rate
(Gleeson et al., 1980
;
Munns et al., 2004
;
Wang et al., 1997
), systemic
blood flow (Wang et al.,
1997
),
PC
(Munns et al., 2004
) or stroke
volume (Frappell et al.,
2002a
). Thus, in contrast to the graded respiratory responses to
exercise in both alligators (Fig.
6) and varanid lizards (Munns
et al., 2004
; Owerkowicz et
al., 1999
; Wang et al.,
1997
), the maximal cardiovascular response may be reached early in
the exercise period, reflecting an `all or nothing' response at the tested
treadmill speeds. In fact, peak
PC in alligators
occurred within the first 2040 s after the onset of exercise
(Fig. 3). In contrast to the
all-or-nothing cardiovascular response to exercise in reptiles, the graded
responses are seen in response to feeding, with incremental increases in heart
rate, stroke volume and cardiac output occurring during the first 2448
h after feeding (Hicks et al.,
2000
; Secor et al.,
2000
). It remains probable that the cardiovascular system in both
alligators and varanid lizards may demonstrate graded responses to exercise at
lower intensities and that the treadmill speeds used in this and other studies
may not be low enough to elicit sub-maximal cardiovascular responses. Thus,
under the experimental conditions used to date, cardiovascular responses in
reptiles appear to be flexible and dependent on the type of physiological
stress.
In conclusion, alligators retain the ability to ventilate their lungs
during locomotion, an ability lacking in some lizards. A significant increase
in IAP was associated with exercise in alligators; however, a nearly 2-fold
increase in CVP maintained positive PTRANS, preventing
both the collapse of the post caval vein and inhibition of venous return.
Thus, despite both alligators and varanid lizards experiencing lateral bending
of the trunk and similar elevations in IAP during exercise, the high CVP
induced in alligators prevented the collapse of abdominal veins that was
apparent during exercise in varanid lizards. Hemodynamic responses to exercise
were rapid with peak values attained within 2040 s after the onset of
exercise. Furthermore, hemodynamic responses to exercise were not graded,
showing no correlation with increments in treadmill speed. IAP, CVP and
PC also varied during
each respiratory cycle, and data suggest that while the tonically elevated IAP
during exercise does not limit venous return, phasic fluctuations in IAP may
act to reduce
PC
during the respiratory cycle at high tidal volumes.
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Acknowledgments |
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References |
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