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First published online March 14, 2008
Journal of Experimental Biology 211, 1141-1147 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015339
Recruitment of the diaphragmaticus, ischiopubis and other respiratory muscles to control pitch and roll in the American alligator (Alligator mississippiensis)
Department of Biology, 257 South 1400 East, University of Utah, Salt Lake City, UT 84112, USA
e-mails: uriona{at}biology.utah.edu; farmer{at}biology.utah.edu
Accepted 4 February 2008
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Summary |
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Key words: pitch, roll, aquatic locomotion, lung, alligator, Alligator mississippiensis, archosaur, crocodilian, diaphragm, diaphragmaticus, ischiopubis, rectus abdominis, intercostalis, buoyancy, metacentric height, evolution, ventilation, ventilatory mechanics, pelvic aspiration
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Maneuverability in water depends upon the generation of lift and drag, two
velocity-dependent forces. Thus the ability to maneuver and control posture is
much more difficult at slow speeds than at high speeds, a fact that underlies
the importance of gas inclusions or lungs to slow swimming organisms
(Alexander, 1990;
Webb, 2002). Aquatic organisms
that have a lung, or some other buoyancy device, can experience a torque if
the center of mass and center of buoyancy are not in the same location, and
this torque can change the angle of the long axis of the body (a change in
pitch) or cause a roll about the long axis.
Whipple (Whipple, 1906)
suggested that the musculoskeletal complex of the ypsiloid apparatus of
Urodele amphibians functions to shift air in the lungs and thereby change the
direction of the long axis of the body in the absence of swimming motions
(Whipple, 1906). The basis of
this apparatus consists of the cartilago ypsiloides, a y-shaped cartilage
dorsal to the rectus abdominis muscle, the stem of the y articulating with the
pubes in a mobile joint. Whipple hypothesized that contraction of the M.
ypsiloideus posterior, a fan-shaped muscle originating on the pubes and
inserting on the arms and stem of the cartilage, as well as other muscles
associated with the cartilage, pull the ypsiloid cartilage dorsad and thereby
squeeze air out of caudal and into cranial portions of the lung, raising the
cranial body and lowering the caudal body
(Whipple, 1906).
In crocodilians, the part of the musculoskeletal system that enables pelvic
aspiration is in many ways remarkably similar to the ypsiloid apparatus. The
crocodilian pubes articulate with the ischia in a moveable joint. Fan shaped
muscles originating on the ventral, posteriolateral margin of the ischia
extend forward and attach to the cranial margin of the pubes, which are
expanded paddle-shaped bones completely excluded from the acetabulum. The
cranial edges of the pubes are mechanically connected to the gastralia
anteriorly through a fibrous sheet and laterally by ligamentous bands
(Farmer and Carrier, 2000a).
This musculoskeletal complex is mechanically connected with the
diaphragmaticus muscle, which originates laterally on the illia, ventrally on
the hindermost gastralia and inserts ventrally on the pericardium and a
fibrous membrane that encapsulates the liver, and dorsally on an aponeurosis
that binds the esophagus to the liver
(Reese, 1915). The lungs are
mechanically connected to the liver. Thus, contraction of the ischiopubis and
diaphragmaticus muscles causes the pubes to rotate ventrocaudad and the
viscera to shift ventrocaudad (Farmer and
Carrier, 2000a; Gans and
Clark, 1976). Although documented to assist ventilation, the liver
piston results in a pronounced shift of the lungs and other viscera along the
long axis of the body (Brainerd,
1999; Claessens,
2004) (Fig. 1);
thus, the muscles and bones that make diaphragmatic and pelvic aspiration
possible could plausibly be employed in an aquatic setting to control posture
and contribute to maneuverability. If this is true it raises the possibility
that the primitive function for this musculoskeletal complex is locomotion,
arising when the Crocodylomorpha assumed a more aquatic lifestyle, and that
the complex was secondarily recruited for ventilation. Such a scenario implies
that the ancestral Archosauromorpha overcame Carrier's constraint
(Carrier, 1987) by evolving an
upright posture and employing cuirassal breathing
(Carrier and Farmer, 2000)
rather than relying on the diaphragmaticus. We used electromyography on
juvenile American alligators to test the hypothesis that the following
muscles, which are known to play a role in respiration
(Farmer and Carrier, 2000a;
Gans and Clark, 1976), are
recruited for aquatic locomotion: M. diaphragmaticus, M. ischiopubis, M.
rectus abdominis, M. intercostalis internus, M. transversus abdominis.
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MATERIALS AND METHODS |
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Surgery
Animals were lightly anaesthetized by enclosure in a box containing a rag
soaked with isoflurane. Once drowsy, the animals were intubated and ventilated
with a small animal ventilator (CWE Inc., Ardmore, PA, USA) using air that had
passed through an isoflurane vaporizer (Drager, Lubeck, Germany). The level of
anesthesia was initially set at 4%, but was reduced to 0.5% for the majority
of the surgery. All surgeries were performed using sterile technique. With the
animal in the supine position, the belly and sides were disinfected with
betadine and then draped with a sterile cloth. Prior to making the incision,
lidocaine was injected just under the skin in the area of the incision. To
place electrodes over the diaphragmaticus, the rectus abdominis and the
transverses abdominis, an incision was made along the ventral midline of the
animal, caudal to the last long rib and cranial to the last gastralia. The
ventral portion of the diaphragmaticus muscle was located along both the right
and left sides of the body and a patch electrode was secured over the muscle,
perpendicular to the muscle fiber orientation. In the same fashion, a patch
electrode was sutured in place perpendicular to the muscle fiber orientation
on the rectus abdominis and the transverses abdominis muscles. For placement
of a patch electrode over the ischiopubis muscle, a small incision was made on
the ventral midline of the animal at the location of the hind legs and the
patch electrode was placed over the ischiopubis in the same fashion as the
above-mentioned muscles. To place a patch electrode over the intercostalis
internus a small incision was made perpendicular to the third long rib at the
level of the shoulder. The electrode was then placed between the third and
fourth long rib between the two layers of intercostal muscles and facing the
intercostalis internus muscles. A ground electrode was placed inside the
abdominal cavity and all electrodes were tunneled out the dorsal side of the
body wall. At the exit point, the leads were fed through a rubber tube and the
tube was filled with silicone. The leads were anchored against mechanical
strain by suturing the rubber tube to the back of the animal. All incisions
were sutured and all the animals were treated with a topical antibiotic until
the incisions had healed. During healing the animals were housed in a dry
enclosure.
Data collection and analysis
Analog signals from the patch electrodes were amplified 5000 times and
filtered above 1000 Hz and below 30 Hz. The analog signals from the electrodes
and the inclinometer were converted to a digital form using an analog to
digital converter (Biopac Systems, Goleta, CA, USA) and stored on a Macintosh
computer. Signals were sampled at a rate of 2000 Hz and analyzed with
Acqknowledge software (Biopac Systems, Goleta, CA, USA). The muscle activity
signals were rectified and analyzed in two ways. First, a dive–surface
cycle consisting of a dive underwater immediately followed by a return to the
original pitch angle was divided into one hundred equal bins
(Fig. 2). The muscle activity
within each bin was then integrated and averaged. For each animal, at least
two non-weighted dive cycles were analyzed, and respective bins averaged. The
muscle activity within each bin was divided by the average integrated signal
for all the bins in order to obtain a relative muscle activity for each bin.
For all the animals, the relative muscle activity for respective bins was
averaged and the standard error obtained in order to characterize the timing
and magnitude of muscle activity for each muscle over the course of a
dive–surface cycle (Ritter et al.,
2001). Second, muscle activity during dives, for the three
treatments, was divided by the change in pitch over the dive in order to get a
relative muscle activity for a change in pitch angle. This value was then
averaged for all the dives in each treatment. Only dives that had a change in
pitch greater than 45° and little change in the roll were used for this
analysis. A one-way ANOVA was used to check for a statistically significant
treatment effect (P
0.05).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Gans and Clark,
1976). Activity in the diaphragmaticus was also observed in a
non-respiratory capacity when the animals were diving underwater. Muscle
activity was seen during nearly every dive and was always correlated with
changes in pitch where the cranial body rotated ventrally along the long axis
of the body. The magnitude of muscle activity during these maneuvers was, at
times, equal to that observed during quiet breathing at the surface of the
water. Most dives were preceded by an inspiration, whereupon the
diaphragmaticus remained active until the maximum difference in pitch angle
was reached (at around 50% of the dive–surface cycle). Under this
condition, the maximum average muscle intensity was reached at about 20% of a
dive–surface cycle. When all the dives for each animal were averaged
together the beginning of muscle activity associated with diving was obscured
by the ventilation activity that preceded the dive
(Fig. 3). When a breath did not
precede a dive, again the muscle only remained active until the maximum
difference in pitch angle was reached. However, a full cycle of muscle
activity was observed, and the maximum average muscle intensity was reached
slightly later than that obtained in the cycles preceded by a breath (example
of this can be seen in Fig. 2).
When the animals were weighted with 2.5% of their body mass under the jaw, the
average integrated area of the electromyographic (EMG) signal for a given
change in pitch during a dive was significantly smaller then when the same
weight was placed on the base of the tail. This was true for all but one of
the animals. When the weight was placed on the head of this animal it would
not make a head-down dive and would sink with the body parallel to the
horizontal plane. However, for this animal the average integrated area of the
EMG signal for a given change in pitch during a dive was significantly larger
when the weight was placed on the tail than when no weight was added to the
animal. In general, the activity of the diaphragmaticus was greatest for a
given change in pitch when the weight was placed on the tail and least when
the weight was placed under the jaw, with the trials where no weight was added
falling between the other two (Fig.
4). We also observed that the diaphragmaticus had the ability to
become active differentially on either side of the body. If the animal were to
roll hard to one side during a dive, the muscle on the side leading the roll
would become active, whereas activity on the opposite side could be seen to
diminish or stop (Fig. 5).
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M. ischiopubis
Like the diaphragmaticus, activity in the ischiopubis was consistent with
that observed in other studies, with the muscle showing phasic activity
associated with quiet ventilation on land and in the water
(Farmer and Carrier, 2000a).
However, the magnitude of activity was greatly reduced, or at times absent
during ventilation in the water. The ischiopubis was also like the
diaphragmaticus in that the muscle showed activity associated with the animal
diving underwater. Again, muscle activity was seen during almost every dive
and was always correlated with changes in pitch, which rotated the cranial
body of the animal ventrally. The magnitude of muscle activity during these
maneuvers was greater than that observed during quiet breathing at the surface
of the water. Because of this, the initial average activity level for this
muscle during the start of a dive was reduced in relation to the maximum
intensity, despite the fact that most of the dives were preceded by an
inspiration. The ischiopubis remained active for less time than the
diaphragmaticus and finished firing at about 45% of a dive–surface
cycle. The maximum average muscle intensity for all the animals showed two
peaks at about 17 and 25% of a dive–surface cycle
(Fig. 3). When the animals were
weighted under the jaw and on the tail, the same general trends were observed
for the average integrated EMG activity for a given change in pitch as that
observed for the diaphragmaticus. A statistically significant treatment effect
was observed when comparing the values for weight under the jaw with weight
added to the tail, with the largest values observed when the weight was on the
tail (Fig. 4).
M. rectus abdominis
As reported previously, the rectus abdominis was active during exhalation
when breathing on land (Farmer and Carrier,
2000a). However, in this study it was never active during
exhalation while the animal was breathing on the surface of the water. This
muscle, like the diaphragmaticus and the ischiopubis, was active when the
animal dived underwater. Activity was seen during almost every dive and was
always correlated with changes in pitch, which rotated the cranial body of the
animal ventrally. The muscle became active at the start of a dive and the
maximum intensity was reached around 30% of the dive–surface cycle. The
muscle remained active for a longer period than that observed with the
diaphragmaticus or ischiopubis, and was finished firing at
about 55% of a dive–surface cycle
(Fig. 3). When the animals were
weighted under the jaw and on the tail, the same trends were observed for the
average integrated EMG activity for a given change in pitch as was observed
for the diaphragmaticus and ischiopubis. A statistically significant treatment
effect was observed when comparing the values for weight under the jaw with
weight added to the tail, with the largest values observed when the weight was
on the tail (Fig. 4). Like the
diaphragmaticus, the rectus abdominis appears to become active independently
on each side during a dive when the animal was rolling to one side or the
other (Fig. 5).
M. intercostalis internus
Activity in the intercostalis internus muscle was observed during
exhalation when the animal was on land. However, this muscle was not active
during exhalation when the animal was breathing on the surface of the water.
The internal intercostals showed activity associated with the animal diving.
Muscle activity was seen during almost every dive and was always correlated
with a change in pitch in which the cranial body rotated ventrally. Activity
in this muscle was initiated before the start of a dive, reached its maximal
average intensity between 10 and 20% of the dive cycle, and was quieted by 60%
of a dive–surface cycle (Fig.
3).
M. transversus abdominis
Like the rectus abdominis and in accordance with what has been previously
reported, this muscle was active during exhalation when the animal was on land
(Farmer and Carrier, 2000a).
However, this muscle was inactive during exhalation when the animal was
breathing at the surface of the water. This muscle showed no activity when the
animals were diving or surfacing from a dive.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). In
addition, inspiration is facilitated when ischiopubis muscles rotate the pubes
and the gastralia caudoventrad while the diaphragmaticus muscle pulls the
liver–lung complex caudad (Farmer and
Carrier, 2000a; Gans and
Clark, 1976). The rectus abdominis and transversus abdominis
contract during exhalation to squeeze the liver and other viscera craniad
(Farmer and Carrier, 2000a;
Gans, 1976). With large
breaths, the liver–lung complex undergoes very large craniocaudal
displacements (Brainerd, 1999;
Claessens, 2004). On land this
form of breathing shifts the center of mass largely fore and aft (personal
observations). However, in water, movement of the liver-piston will move the
center of buoyancy as well as the center of mass.
The relative position of the center of mass and the center of buoyancy is a
principle determinant of the stability and maneuverability of the organism
(Webb, 2002). A torque will be
exerted along the long axis of the body if the center of buoyancy is either
cranial or dorsal to the center of mass. Similarly, if the center of buoyancy
is ventral to the center of mass the animal can easily roll. Although a highly
maneuverable design, this situation is also unstable
(Webb, 2002). By shifting the
center of buoyancy with respect to the center of mass, crocodilians could
control posture, pitch and rolls. Thus we analyzed the activity of several
muscles that have the capacity to shift the center of buoyancy.
When pivoting about the long axis of the body so that the head tilts down
and the tail up, we measured electrical activity in the diaphragmaticus, the
ischiopubis, the rectus abdominis and the internal intercostals. Although the
rectus abdominis and the intercostal muscles are important in movements of the
trunk in lizards (Carrier,
1990), the ischiopubis and diaphragmaticus have little if any
mechanical ability to bend the trunk. During exercise on land the transversus
abdominis, rectus abdominis and ischiopubis muscles have only low-level, and
often intermittent activity during locomotion but they have a strong phasic
pattern of activity tightly correlated with ventilation
(Farmer and Carrier, 2000a).
During ventilation the diaphragmaticus and ischiopubis muscles move the lung
ventrocaudad. Therefore, we think that when these muscles are employed in an
aquatic setting they increase the relative buoyancy of the caudal body while
decreasing the relative buoyancy of the cranial body, and thereby change
pitch. Furthermore, when we made this maneuver more difficult by adding a
weight to the base of the tail, or easier by adding a weight to the head, the
activity of these muscles changed in a manner that is consistent with the
hypothesis, that is, more activity was measured when the weight was on the
tail than when the head was weighted.
With rolling maneuvers we measured differences in the levels of activity of the right and left diaphragmaticus and rectus abdominis muscles. When the animals rolled clockwise around the long axis of rotation (the right side of the body moving ventrad) activity in the right moiety of these muscles increased whereas activity in the left moiety decreased. A counterclockwise roll was accompanied by an increase in the activity of the left moieties and a decrease in the right moieties (see Fig. 5). Prior to this study we know of no studies showing unilateral activity in the right and left side of the diaphragmaticus. This high degree of neural sophistication associated with the ability to control ones position from side to side in water further highlights the importance of this muscle to aquatic locomotion.
Evolutionary implications
The evolutionary history of the breathing mechanisms of amniotes is a
central chapter in what is arguably one of the most exciting stories in the
history of life, the water–land transition. The common ancestor of
tetrapods used the mouth, the buccal pump, to ventilate both gills and lungs
(Gans, 1970). The rise of
novel breathing mechanisms that eventually replaced buccal ventilation has
long been of interest (Brainerd,
1999; Perry et al.,
2005). How and when did novel respiratory muscles, such as the
diaphragmaticus, evolve? Our results may provide new insight into the origin
of the crocodilian diaphragmaticus in offering a plausible and logical
scenario for the sequence of events giving rise to this new muscle.
We observed that alligators activate the rectus abdominis and the
diaphragmaticus in synchrony when diving in water, despite the fact that the
rectus abdominis is used for exhalation and the diaphragmaticus for inhalation
during ventilation. Both the rectus abdominis and the diaphragmaticus were
probably originally derived from the same muscle-group in alligators
(Carrier and Farmer, 2000;
Keith, 1905) and the primitive
function of the rectus muscle was almost certainly locomotion rather than
ventilation. To have a favorable function in aquatic locomotion just one
innovation would have been required, a change of the site of insertion of a
portion of the rectus from the sternum to the liver. By contrast, to evolve
this muscle for the purpose of respiration requires two evolutionary
innovations to occur, a deviation of the site of insertion of part of the
rectus from the sternum to the liver and the development of new motor
recruitment patterns. Thus, the most parsimonius explanation for the origin of
the diaphragmaticus is that it arose first for controlling movement in the
water and was later recruited for ventilation.
Early crocodilians appear to have been fully terrestrial animals. In the
Triassic period (approximately 245 million years ago) they were small (about
the size of a cat), slender animals with traits indicative of a capacity for
agile locomotion, such as a parasagittal limb posture and reduced numbers of
digits on long slender limbs (Parrish,
1987; Walker,
1970). It is in the Cretaceous (roughly 145 million years ago)
that the lineage became amphibious and acquired many features associated with
a life in water (e.g. the dorsoventrally flattened skull, short limbs and
expanded tail) (Sill, 1968).
Although it has been suggested that both cuirassal inspiration and a
diaphragmaticus supplemented costal inspiration in the Triassic forms
(Carrier and Farmer, 2000;
Farmer and Carrier, 2000a), the
data of this study support the origin of this muscle in the Cretaceous with
the assumption of an aquatic lifestyle
(Paul, 2002). If this is true,
then cuirassal breathing and upright posture may have been the primary
mechanisms by which early archosaurs overcame Carrier's constraint on
simultaneous costal ventilation and locomotion
(Carrier, 1987).
Inferences of the evolutionary history of the crocodilian diaphragmaticus
will be strengthened with further studies of similar muscles that have been
convergently acquired because convergent evolution is one of the most robust
lines of evidence for the adaptive significance of traits. Diaphragm-like
muscles have been identified in some frogs (Xenopus laevis and
Pipa pipa) (Keith,
1905; Snapper et al.,
1974), and some testudines (e.g. Trionix)
(Gaunt and Gans, 1969;
George and Shah, 1959) and
prior studies implicate a respiratory or gastrointestinal function in these
lineages (Pickering et al.,
2004; Pickering and Jones,
2002; Snapper et al.,
1974). However, electrical activity of the amphibian diaphragm
suggests a role for this muscle in aquatic locomotion
(De Jongh, 1972) and we have
measured electrical activity in the chelonian diaphragmaticus that is
coincident with changes in pitch and roll during aquatic locomotion (T.J.U.
and C.G.F., personal observations). The anuran diaphragm has no relationship
to the ypsiloid apparatus of salamanders, which is yet again an independently
evolved but analogous mechanism for adjusting the center of buoyancy
(Whipple, 1906). Finally, the
diaphragms of Sirenia are highly derived in a way that could allow the lungs
to be used to control pitch and roll
(Rommel and Reynolds, 2000).
Thus, there may be at least six examples of innovations that enable the gases
in the lungs to be manipulated to control posture, pitch and roll in
tetrapods, suggesting there is strong positive selection for this function. We
find this ability to be quite remarkable, with implications related to aquatic
locomotion in many vertebrates that possess a lung or gas bladder.
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Acknowledgments |
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significant
treatment effect when comparing dives where no weighted was added to tail
weighted dives (P