Role of the post-hepatic septum on breathing during locomotion in Tupinambis merianae (Reptilia: Teiidae)
1 Institut für Zoologie, Universität Bonn, Poppelsdorfer Schloss,
53115 Bonn, Germany
2 Departamento de Zoologia, Universidade Estadual Paulista Rio
Claro, c.p. 199, 13506-900 Rio Claro, SP, Brazil
* Author for correspondence (e-mail: kleinwilfried{at}web.de)
Accepted 24 March 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: Tupinambis merianae, lizard, post-hepatic septum, locomotion, ventilation, breathing mechanics
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Teiid lizards of the genus Tupinambis are ecologically similar to
the savannah monitor but their lungs and pattern of internal septation are
fundamentally different. They possess single-chambered lungs with
homogeneously distributed parenchyma
(Duncker, 1978;
Perry, 1983
). Teiids are also
characterised by a well-developed post-hepatic septum (PHS)
(Broman, 1904
;
Duncker, 1978
), which
incompletely divides the body cavity into two parts. The cranial part contains
the liver and the lungs, which are fixed in the body cavity by dorsal
mesopneumonia, while the caudal part contains the remaining viscera
(Klein et al., 2000
). The
morphology of the PHS varies in teiid lizards. It is best developed, almost
completely closed, in Crocodilurus and Tupinambis, whereas
the PHS in smaller teiids, such as Ameiva and Cnemidophorus,
only attaches to the ventro-lateral part of the body wall
(Klein et al., 2000
).
Morphological diffusing capacity has been shown to be similar in the
savannah monitor and the tegu, T. teguixin (earlier T.
nigropunctatus; Avila-Pires,
1995) (Perry,
1983
) but ventilation of tegus has not yet been measured during
exercise or interpreted in terms of breathing strategies. Furthermore, the
deep, densely partitioned lung parenchyma of tegu lungs is well suited for a
sedentary life-style of a sit-and-wait predator, which does not need to
support a high rate of oxygen consumption for prolonged periods
(Perry, 1998
). An actively
foraging life-style as in the savannah monitor, on the other hand, favours a
convective gas-exchange strategy to provide high levels of gas exchange during
activity (Perry, 1998
).
Accordingly, the savannah monitor shows a more shallow and less densely
partitioned parenchyma, which can be ventilated with low work of breathing
(Perry, 1983
). In the tegu,
also a highly active lizard, only the lung parenchyma directly exposed to the
lung lumen is accessible for convective gas exchange, whereas gas exchange in
the deep faveolar parenchyma depends mainly on diffusion and contraction of
smooth muscle to remove the used air. Furthermore, tegu lungs are of low
compliance (Klein et al.,
2003
) and require a high work of breathing to ventilate them
(Perry and Duncker, 1980
).
Given these differences between savannah monitors and tegus, the tegu lizard
appears to demonstrate a mismatch between form and function, as its
low-compliance, energy-expending respiratory system has several disadvantages
for a lifestyle as an actively foraging predator.
Because the tegu shows the best developed PHS of all teiid lizards, we suspect that this septum may reduce the axial constraint to lung ventilation during exercise at moderate speeds and compensate for the limitations set by the diffusion-dominated lungs. This hypothesis was tested by measuring oxygen uptake and ventilatory parameters of tegus with and without post-hepatic septum on a motorised treadmill.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ventilation and gas exchange
Ventilation was studied using the mask technique of Glass et al.
(1978), modified by Wang and
Warburton (1995
). For
ventilation measurements during the night, a plastic mask enclosing the entire
head and containing a pneumotachometer was employed. For the locomotion
experiments the tip of the tegu's snout, including nares and closing the mouth
tightly, was covered with a small plastic mask, which was connected to a
pneumotachometer by a short piece of Tygon® tubing. In both cases the mask
was connected by the tubing to a pressure transducer (Sable PT-100; Las Vegas,
USA) and an O2 analyser (Applied Electrochemistry S-3 A/L;
Pittsburgh, USA). Flow through the mask was generated by a suction pump
(Ametek, Paoli, USA; flow control R1) placed downstream from the O2
analyser. To remove water vapour and CO2 from the expired air, a
tube containing silica gel and Ascarite® was placed upstream to the
O2 analyser. For ventilation measurements at night, flow rate was
kept constant at 200 ml min-1, whereas flow rate was 300 ml
min-1 for ventilation measurements on the treadmill. These flow
rates allowed breath-by-breath analysis, although the signal from the oxygen
analyser was delayed for 23 s. The signals from the pressure transducer
and oxygen analyser were recorded through a computerised data-acquisition
system (DAC, Sable System). To calibrate the masks, a plaster cast of a tegu's
head was made, placed into the mask and sealed with latex rubber. The masks
were calibrated with simulated breaths of known volume and gas composition.
The relationship between the electrical signal generated and volume and
composition of gas could be accurately described by linear regressions
(r2>0.9 in all cases).
Surgery
Septum removed (SR)-tegus
To remove the PHS, tegus were anaesthetised with CO2
(Wang et al., 1993). When the
animal no longer reacted to pinching of the skin, it was fixed with rubber
bands in a supine position on an operation table and a constant low
CO2-flow was provided to the nostrils. The belly was disinfected
with tincture of iodine before surgery. A 1.52.5 cm incision was made
on the ventro-lateral body wall caudal to the last long rib. The fat-body,
stomach and intestine were retracted, the PHS was exposed and completely
ruptured in a stepwise fashion beginning at the lateral part of the body wall
and moving to the dorsal midline and ventrally, approaching the abdominal vein
as close as possible. The caudal part of the hepatic ligament was also
ruptured. A similar rupture of the PHS was also carried out on the other side
of the animal. The cuts were closed with suture, disinfected with iodine and
BaytrilTM was injected intraperitoneally to prevent infections after the
surgery. Tegus were then allowed to recover for at least 3 months before
experimentation.
Sham-operated (SO)-tegus
The procedure for the sham-operated animals was the same as for the
SR-tegus, except that the PHS was not ruptured.
Experimental protocol
Experiments were performed with 5 SR-tegus (body mass, 855±343 g;
snoutvent length, 278±28 mm) and 5 SO-tegus (body mass,
712±234 g; snoutvent length, 266±28 mm) after they had
been allowed to recover for at least 3 months following surgery. Ventilation
of resting animals, determined during the inactive period at night, was
determined 3 weeks before the treadmill experiments. At least 24 h before
making the recordings, the masks were attached to the tegus, sealed around the
neck with latex rubber and secured with adhesive tape. The tegus were then
placed into a climatic chamber at 35°C and ventilatory parameters were
recorded during the following night between 00:00 h and 04:00 h. Before
experimentation, food was withheld for at least 4 days.
The masks for the treadmill experiment were fixed on the tegu's snout the day before the experiment and tegus were kept overnight in a climatic chamber at 35°C. The next day, the animal was placed on the treadmill and the mask was connected to the experimental set-up. Room temperature was 2830°C and a lamp over the treadmill maintained a temperature of 35°C on the belt. The belt of this custom-made motorised treadmill was 65 cmx78 cm (widthxlength); a cardboard box frame was used to prevent the animal from escaping.
Treadmill protocol
After an acclimatisation period of approximately 5 min, tegus were made to
walk at a belt speed of 0.17 m s-1 for 5 min. They were then left
undisturbed for 5 min, made to locomote at 0.28 m s-1 until
exhaustion and then left undisturbed for 30 min. Tegus were motivated to run
by pinching or tapping the tail. Running experiments were stopped when tegus
could no longer be motivated with 10 consecutive stimuli (at 1
s-1). These speeds were chosen for experiments on sustained
locomotion, because tegus only show sprints of high speeds and short duration
when chased or attacked (W.K., personal observation). Freely ranging tegus
maintained in the outdoor pens moved at moderate speeds and foraged for
prolonged periods (W.K., personal observation). Furthermore the effect of the
PHS is expected to be greater at elevated aerobic states rather than during
anaerobic sprints.
Endurance
Test of locomotor endurance of SO- and SR-tegus were measured 2 weeks
before ventilatory measurements. Tegus that were not wearing masks were made
to walk on the treadmill at either 0.17 m s-1 or 0.28 m
s-1 until exhaustion. Measurements were repeated the next day at
the same speed. The animals were tested at the other speed on two consecutive
days. The greatest value of each speed obtained for a given animal were used
to determine its endurance.
Data handling and statistics
For the animals resting at night, a period of 5 min or at least 30
consecutive breaths was analysed. This period was chosen to reflect a regular
steady-state breathing pattern under this condition. From the treadmill
experiment the following parts of the breathing trace were analysed: (1) 1 min
before starting exercise (pre-exercise), (2) the last minute of the exercise
periods (0.17 m s-1 and 0.28 m s-1, respectively), (3)
the first and the last min of the recovery period following exercise at 0.17 m
s-1, and (4) for 1 min immediately after exercising at 0.28 m
s-1, and 5, 10, 20 and 30 min later.
In all cases, we determined breathing frequency (fR), tidal volume
(VT), duration of total respiratory movements
(TTOT), oxygen uptake per breath
(VBO2), and oxygen extraction coefficient
(EO2). From these measurements the rate of
oxygen consumption
(O2), total
ventilation rate (
E) and air
convection requirement for O2
(
E/
O2)
were calculated. Data were transformed to STPD conditions following
Dejours (1981
).
To detect differences between previously defined parts of the breathing
trace, a one-way repeated-measures analysis of variance (ANOVA) was used,
followed by a paired multiple comparison procedure
(StudentNewmanKeuls) to identify the group or groups that
differed from each other. SO- and SR-tegus were compared using a paired
t-test. A difference was considered significant at a level of
P0.05. If the test for normality failed, data were
log10 transformed and reanalysed.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
Ventilation at night and day
In SO-tegus all ventilatory parameters investigated, except VT,
showed significant differences (P0.05) between the recordings
during the night and during the day. This was also the case for most of the
parameters investigated in SR-tegus, but in this group
TTOT and
O2 also showed
no significant differences between day and night. In general the length of a
respiratory cycle was longer during the night. In addition fR,
E,
O2 and
E/
O2
were smaller during the night whereas VBO2 and
EO2 were greater during the night than during
the day.
Ventilation during the activity
TTOT before exercise was 1.73 s for SO-tegus and 1.92 s
for SR-tegus but decreased in both groups during exercise to the shortest
TTOT values recorded
(Fig. 2A).
VT in SO-tegus during pre-exercise was only significantly
different from the values during walking at 0.17 m s-1 and in the
first minute of recovery from either speed
(Fig. 2C). VT in
SR-tegus showed no significant differences between rest and exercise at both
speeds. Exercising at 0.17 m s-1 increased
E significantly (P
0.05)
compared with pre-exercise values, both in SO- and in SR-tegus
(Fig. 2D). This change was due
to a significant increase in VT in SO-tegus and fR in
SR-individuals. At this speed SO- and SR-tegus also differed in fR
and VT (P=0.048 and 0.0102, respectively), but not in
E (P=0.0621). In the first
minute after exercise at 0.17 m s-1
E decreased significantly
(P
0.05). fR also decreased to pre-exercise values in
both groups, but VT remained at the level reached during exercise
(18.76 and 19.89 ml kg-1, respectively) in SO-tegus. In SR-tegus
VT increased from 11.6 to 16.1 ml kg-1. 5 min after
exercising at 0.17 m s-1, fR, VT and
E returned to pre-exercise values in
both groups. At 0.28 m s-1, fR, VT and
E increased significantly
(P
0.05) compared to the preceding resting phase, with the
exception of SR-tegus, in which VT was only slightly increased above
the resting values. The high
E in
SO-tegus was a result of an increase in VT together with a small
decrease in fR. VT 1 min after 0.28 m s-1 was
significantly (P=0.0117) lower in SR-tegus than in SO-tegus.
As a result of exercise, EO2 decreased when
compared to daytime resting values (Fig.
3A). SO- and SR-tegus showed the lowest
EO2 during fast walking at 0.28 m
s-1 and during the first minute of this recovery period and
returned towards resting values 30 min after exercise. SO- and SR-tegus
decreased VBO2 during exercise compared with
the preceding phase. The highest values for oxygen uptake per breath were
reached in the first min after walking at 0.17 m s-1 in both
groups. O2, on
the other hand, was high both during exercising at 0.17 m s-1 and
the following first minute of recovery
(Fig. 3C). Only SO-tegus showed
a tendency to increase VBO2 and
O2 in the first
minute after 0.28 m s-1, which was not significantly different from
the pre-exercise value.
E/
O2
did not differ significantly between SO- and SR-tegus under any of the
conditions investigated; however,
E/
O2
in SO-tegus was significantly different from the pre-exercise value during the
first minute after exercising at 0.28 m s-1. In addition, SO-tegus
showed a significantly greater
E/
O2
at 0.28 m s-1 compared to the preceding recovery period.
Endurance
There was a large individual variation in the endurance of SO-tegus,
ranging from 4.2 to 142.5 min at 0.17 m s-1 and from 2.3 to 70.3
min at 0.28 m s-1. SR-tegus also showed a great variation at 0.17 m
s-1 (3.5109.7 min) and 0.28 m s-1 (1.517.9
min). Because of this great spread in values, no significant differences
between group means for SO- and SR-tegus were found at either speed, but in
both groups endurance at 0.28 m s-1 was significantly less than at
0.17 m s-1 (two-way repeated-measures ANOVA, P0.05).
On average, however, SO-tegus could keep up with the lower belt speed for 47.6
min and the greater speed for 18.3 min, which was greater than in SR-tegus.
Thus, endurance was 36.5 min at 0.17 m s-1 and 5.2 min at 0.28 m
s-1 (Fig. 4).
|
Because of the large variation, the median value appeared the more attractive indicator of central tendency for this parameter. The median was greater in SR-tegus exercising at 0.17 m s-1 compared with SO- animals (29.7 and 19.2 min, respectively) but at 0.28 m s-1 endurance was greater in SO- than in SR-tegus (6.3 and 2.6 min, respectively; Fig. 4).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Tupinambis teguixin (earlier T. nigropunctatus;
Avila-Pires, 1995) attain a
maximum speed of 5.1 m s-1 during quadrupedal and 4.3 m
s-1 during bipedal running
(Urban, 1965
). In general,
however, lizards are only capable of maintaining such high velocities for
short periods of time. Metabolism during these sprint events is largely
anaerobic (Bennett, 1972
,
1973
; Bennett and Dawson, 1972;
Bennett and Licht, 1972; Farmer and Hicks,
2000
). Iguana iguana, for instance, reaches
O2max between
0.06 and 0.14 m s-1 (Mitchell
et al., 1981
) and
O2 declines
between 0.28 and 0.56 m s-1
(Wang et al., 1997
), which is
only a small fraction (6.3%) of their maximum running speed. The greater speed
for T. merianae in the present study (0.28 m s-1)
represents approximately 5% of their maximum running velocity. To match the
lower speed (0.17 m s-1), tegus did not even need to walk
continuously, but sometimes rested until they reached the end of the belt and
then started to walk or run until they reached the other end of the box, when
they again rested. To match the faster speed (i.e. 0.28 m s-1),
however, they had to walk continuously. This upper speed lies at the threshold
at which
O2
reaches maximum and starts to decline with increasing velocity. The increased
metabolic demands are subsequently covered by increasing anaerobic metabolism
(Bennett, 1972
,
1973
; Bennett and Dawson, 1972;
Bennett and Licht, 1972; Farmer and Hicks,
2000
). The measured endurance indicates the importance of this
speed range in tegus, as they are capable of sustaining 0.17 m s-1
for approximately 20 min, even without PHS. Endurance time at 0.28 m
s-1 is greatly reduced in both groups and the high mean in SO-tegus
is mainly based on one specimen, which showed a threefold greater endurance
than the others. Therefore, the speed of 0.17 m s-1 reflects the
performance of tegus with respect to mainly aerobic activity, where a
sustained efficiency of lung ventilation is necessary. At 0.28 m
s-1, on the other hand,
O2 still
contributes greatly to the overall energy requirements, but anaerobic
metabolism plays a more significant role.
Role of the post-hepatic septum
Tegus with intact PHS increased VT during light exercise, whereas
SR-tegus were not able to increase VT while walking on the treadmill.
In contrast, SR-tegus showed the highest VT directly after exercise.
This implies that the PHS helps maintain a minimum space for lungs and that
this volume can be increased by costal movements during low-speed treadmill
locomotion. In tegus without PHS the viscera are displaced cranially
(Klein et al., in press)
especially during exercise, when the lateral undulation of the trunk induced
by abdominal muscles causes greater pressures in the body cavity
(Farmer and Hicks, 2000
).
According to Carrier (1987b
), a
mechanical constraint on the hypaxial muscles prevents lizards from breathing
and running simultaneously. This limitation in ventilation, however, becomes
more severe at greater speeds than the ones tested in this study and therefore
E may decrease in tegus running at
greater velocities as a result of the speed dependent axial constraint. At
0.28 m s-1, SO-tegus already showed a lower VT than at
0.17 m s-1, indicating that the axial constraint may play a
significant role at higher velocities in running tegus. Due to the increase in
fR, however,
E also
increased. During exercise, SR-tegus partially compensated for their generally
low VT by increasing fR to a greater extent than in the
SO-tegus, but still could not attain the
E of the latter group.
SR-tegus and SO-tegus showed nearly identical values for
E/
O2.
This was due to lower values for both
E and
O2 in SR-tegus
compared with SO-animals. Despite a lack of significant differences in
E/
O2
between SR- and SO-tegus, the data suggest that without PHS, tegus are limited
in their ability to respond to elevated metabolic demands. The SR-animals also
needed longer to recover from exercise. The latter was indicated by the rise
in VBO2 after exercising at 0.28 m
s-1. Even 30 min after exercise, this value was greater than in the
pre-exercise condition.
During resting conditions at night, VBO2
tended to be lower (P=0.0959) in SR-tegus than in SO-tegus. The lack
of the PHS possibly affected oxygen uptake negatively in tegus, but their
endurance seemed to be unaffected. It is conceivable that chronic aerobic
insufficiency increases the ability to sustain anaerobic activity in this
group. This could be coupled with compensation through an increase in
breathing frequency, an increase in pulmonary perfusion, or both. Furthermore,
a reduction in lung volumes, which accompanies the removal of the PHS
(Klein et al., 2003) could
reduce the dead space of the lungs, while the volume and surface area of the
gas exchange tissue remain unchanged.
Breathing pattern during rest and activity
The ventilatory pattern of Tupinambis, resting at night, consisted
of regular breaths of long duration and constant frequency. The values for
fR and VT obtained in this study (fR=3.6 breaths
min-1; VT=10.5 ml kg-1) differ somewhat from
those of Hlastala et al.
(1985) for T.
teguixin (earlier T. nigropunctatus;
Avila-Pires, 1995
;
fR=8.21 breaths min-1; VT=9.6 ml kg-1)
and Abe (1987
) for T.
merianae (earlier T. teguixin;
Avila-Pires, 1995
;
fR=4.9 breaths min-1; VT=6.3 ml kg-1),
as fR in the former study is greater whereas in the latter
VT is less than in the present study. The differences may be due to
differences in handling of the animals, to different mask techniques or could
represent species differences.
During exercise, breathing pattern was altered in SO- and SR-tegus and was
characterised by breaths of high flow velocities and shorter duration. These
findings are consistent with those of Carrier
(1987a) and Wang et al.
(1997
). SO-tegus nearly
doubled VT at 0.17 m s-1, and even while exercising at
0.28 m s-1 they were able to increase VT. These results
contrast with those for V. exanthematicus and I. iguana
(Wang et al., 1997
), where
VT showed no difference during exercise compared to pre-exercise
values, but increased significantly during the recovery from speeds of 0.28 m
s-1 and greater.
Gular pumping as additional breathing mechanism during locomotion was not
observed in tegus as has been described for Varanus
(Owerkowicz et al., 1999).
Instead, the present results are consistent with the hypothesis that the PHS
serves as a breathing aid during locomotion, and even after rupture of this
structure the animals are not capable of evoking other mechanisms for
supporting aerobic activity.
Tegus with intact PHS showed the greatest
O2 during
exercise at 0.17 m s-1 and in the first minute of recovery from
both speeds tested. The air convection requirement for oxygen, however,
revealed a marked hyperventilation during both running events as well as at
the beginning of the recovery period after exercising at 0.28 m
s-1. Following walking at 0.17 m s-1, however, air
convection requirements immediately returned to pre-exercise values. There is
reason to believe that
0.17 m s-1 is a reasonably approximation
of the speed used by tegus when they are foraging (W. K., personal
observation). At 0.28 m s-1 or faster, even the large observed
increase in
E may not be sufficient to
match the high aerobic demands, and thus the
EO2 falls. The increase in
O2 and
E directly after
E/
O2
to pre-exercise values and the greatly reduced endurance are also consistent
with this hypothesis. However, as flow rate was relatively low, the
possibility of rebreathing exists, and would also be indicated by a low oxygen
consumption and marked hypoventilation. More studies on the locomotor
performance together with measurements of lactate production and lactate
removal of tegus with and without PHS are needed to test the hypothesis that
intact tegus recover faster from strenuous exercise.
Work of breathing
A change in minute ventilation can be produced in three different ways: (1)
a change only in fR, (2) a change only in VT or (3) a
combination of changes in fR and VT. Elastic work of
breathing () is defined as:
![]() | (1) |
In conclusion, the PHS plays an important role in the breathing system in
Tupinambis. It acts as a mechanical barrier to separate the lungs
from the viscera, thereby increasing the efficiency of costal breathing.
Especially during activity the PHS is essential for increasing
E by a combined increase in
fR and VT, whereas tegus without a PHS rely solely on an
increase in fR to cope with the increasing metabolic demands during
activity. Whether the PHS directly affects physiological parameters such as
ventilation-perfusion ratio further remains to be elucidated.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Abe, A. S. (1987). Ventilação, trocas gasosas, tensão de gases e pH do sangue no teiú, Tupinambis teguixin: efeitos da temperatura (Reptilia Teiidae).UNESP Rio Claro . Tese apresentada ao Concurso do Livre Docente, pp. 123.
Avila-Pires, T. C. S. (1995). Lizards of Brazilian Amazonia (Reptilia; Squamata). Zool. Verh. Leiden 299,1 -706.
Bennett, A. F. (1972). The effect of activity on oxygen consumption, oxygen debt, and heart rate in the lizards Varanus gouldii and Sauromalus hispidus. J. Comp. Physiol. 79,259 -280.
Bennett, A. F. (1973). Ventilation of two species of lizards during rest and activity. Comp. Biochem. Physiol. 46A,653 -671.[CrossRef]
Bennett, A. F. and Dawson, W. R. (1972a). Aerobic and anaerobic metabolism during activity in the lizard Dipsosaurus dorsalis. J. Comp. Physiol. 81,289 -299.
Bennett, A. F. and Licht, P. (1972b). Anaerobic metabolism during activity in lizards. J. Comp. Physiol. 81,277 -288.
Broman, I. (1904). Die Entwicklungsgeschichte der Bursa omentalis und ähnlicher Rezessbildungen bei Entwicklungsgeschichtliche Monographien. pp.611 . den Wirbeltieren.
Carrier, D. R. (1987a). Lung ventilation during walking and running in four species of lizards. Exp. Biol. 47,33 -42.[Medline]
Carrier, D. R. (1987b). The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiol. 13,326 -341.
Cragg, P. A. (1978). Ventilatory patterns and variables in rest and activity in the lizard, Lacerta. Comp. Biochem. Physiol. 60A,399 -410.[CrossRef]
Crosfill, M. L. and Widdicombe, J. G. (1961). Physical characteristics of the chest wall and lungs and the work of breathing in different mammalian species. J. Physiol. 158, 1-14.
Dejours, P. (1981). Principles of Comparative Respiratory Physiology. Second edition, pp.265 . Amsterdam: Elsevier/North-Holland Biomedical Press.
Duncker, H.-R. (1978). Coelom-Gliederung der Wirbeltiere Funktionelle Aspekte. Verh. Anat. Ges. 72,91 -112.[Medline]
Farmer, C. G. and Hicks, J. W. (2000).
Circulatory impairment induced by exercise in the lizard Iguana
iguana. J. Exp. Biol.
203,2691
-2697.
Glass, M. L., Burggren, W. W. and Johansen, K. (1978). Ventilation in an aquatic and a terrestrial chelonian reptile. J. Exp. Biol. 72,165 -179.[Abstract]
Hlastala, M. P., Standaert, T. A., Pierson, D. J. and Luchtel, D. L. (1985). The matching of ventilation and perfusion in the lung of the tegu lizard, Tupinambis nigropunctatus. Respir. Physiol. 60,277 -294.[CrossRef][Medline]
Hopkins, S. R., Hicks, J. W., Cooper, T. K. and Powell, F. L. (1995). Ventilation and pulmonary gas exchange during exercise in the savannah monitor lizard Varanus exanthematicus. J. Exp. Biol. 198,1783 -1789.[Medline]
Klein, W., Böhme, W. and Perry, S. F. (2000). The mesopneumonia and the post-hepatic septum of the Teiioidea (Reptilia: Squamata). Acta Zoologica (Stockholm) 81,109 -119.[CrossRef]
Klein, W., Abe, A. S. and Perry, S. F. (2003). Static lung compliance and body pressures in Tupinambis merianae with and without post-hepatic septum. Respir. Physiol. Neurobiol. 135,73 -86.[CrossRef][Medline]
Klein, W., Abe, A. S., Andrade, D. V. and Perry, S. F. (in press). Structure of the post-hepatic septum and its influence on visceral topology in the tegu lizard, Tupinambis merianae (Teiidae: Sauria: Reptilia). J. Morphol.
Lopes, H. R. and Abe, A. S. (1999). Biologia reprodutiva e comportamento do teiu, Tupinambis merianae, em cativeiro (Reptilie, Teiidae). In Manejo y Conservación de Fauna Silvestre en América Latina (ed. T. G. Fang, O. L. Montenegro and R. E. Bodmer), p. 259. La Paz, Bolivia: Instituto de Ecología.
Milsom, W. K. and Vitalis, T. Z. (1984). Pulmonary mechanics and work of breathing in the lizard, Gekko gecko. J. Exp. Biol. 113,187 -202.
Mitchell, G. S., Gleeson, T. T. and Bennett, A. F. (1981). Pulmonary oxygen transport during activity in lizards. Respir. Physiol. 43,365 -375.[CrossRef][Medline]
Owerkowicz, T., Farmer, C. G., Hicks, J. W. and Brainerd, E.
L. (1999). Contribution of gular pumping to lung ventilation
in monitor lizards. Science
284,1661
-1663.
Perry, S. F. (1983). Reptilian Lungs. Functional anatomy and evolution. Adv. Anat. Embryol. Cell Biol. 79,1 -81.[Medline]
Perry, S. F. (1998). Lungs: Comparative anatomy, functional morphology, and evolution. In Biology of the Reptilia (ed. C. Gans and A. S. Gaunt), pp.1 -80. Ithaca, New York: Society for the Study of Amphibians and Reptilians.
Perry, S. F. and Drucker, H. R. (1980). Interrelationship of static mechanical factors and anatomical structure in lung evolution. J. Comp. Physiol. B 138,321 -334.
Urban, E. K. (1965). Quantitative study of locomotion in teiid lizards. Anim. Behav. 13,513 -529.[Medline]
Wang, T., Fernandes, W. and Abe, A. S. (1993). Blood pH and O2 homeostasis upon CO2 anaesthesia in the rattlesnake (Crotalus durissus). The Snake 25, 21-26
Wang, T. and Warburton, S. J. (1995). Breathing pattern and cost of ventilation in the American alligator. Respir. Physiol. 102,29 -37.[CrossRef][Medline]
Wang, T., Carrier, D. R. and Hicks, J. W.
(1997). Ventilation and gas exchange in lizards during treadmill
exercise. J. Exp. Biol.
200,2629
-2639.
Wood, S. C., Johansen, K., Glass, M. L. and Maloiy, G. M. O. (1978). Aerobic metabolism of the lizard Varanus exanthematicus: effects of activity, temperature, and size. J. Comp. Physiol. B 127,331 -336.
Related articles in JEB: