JOURNAL OF MORPHOLOGY 271:438–450 (2010)
Abdominal Muscle and Epipubic Bone Function During
Locomotion in Australian Possums: Insights to Basal
Mammalian Conditions and Eutherian-Like Tendencies
in Trichosurus
Stephen M. Reilly,1* Eric J. McElroy,2 Thomas D. White,3
Audrone R. Biknevicius,4 and Michael B. Bennett5
1
Department of Biological Sciences, Ohio Center for Ecology and Evolutionary Studies,
Ohio University, Athens, Ohio 45701
2
Department of Biology, College of Charleston, Charleston, South Carolina 29401
3
Biology Department, Buffalo State College, Buffalo, New York 14222
4
Department of Biomedical Sciences, College of Osteopathic Medicine, Ohio University, Athens, Ohio 45701
5
School of Biomedical Sciences, University of Queensland, St. Lucia, Queensland 4072, Australia
ABSTRACT Mammals have four hypaxial muscle layers
that wrap around the abdomen between the pelvis, ribcage, and spine. However, the marsupials have epipubic
bones extending anteriorly into the ventral hypaxial
layers with two additional muscles extending to the ventral midline and femur. Comparisons of South American
marsupials to basal eutherians have shown that all of the
abdominal hypaxials are active bilaterally in resting ventilation. However, during locomotion marsupials employ
an asymmetrical pattern of activity as the hypaxial
muscles form a crosscouplet linkage that uses the epipubic bone as a lever to provide long-axis support of the body
between diagonal limb couplets during each step. In basal
eutherians, this system shifts off the femur and epipubic
bones (which are lost) resulting in a shoulder to pelvis
linkage associated with shifts in both the positions and activity patterns of the pectineus and rectus abdominis
muscles during locomotion. In this study, we present data
on hypaxial function in two species (Pseudocheirus
peregrinus and Trichosurus vulpecula) representing the
two major radiations of possums in Australia: the Pseudocheiridae (within the Petauroidea) and the Phalangeridae. Patterns of gait, motor activity, and morphology in
these two Australian species were compared with previous work to examine the generality of 1) the crosscouplet
lever system as the basal condition for the Marsupialia
and 2) several traits hypothesized to be common to all
mammals (hypaxial tonus during resting ventilation,
ventilation to step synchrony during locomotion, and
bilateral transversus abdominis activity during locomotor
expiration). Our results validate the presence of the crosscouplet pattern and basic epipubic bone lever system in
Australian possums and confirm the generality of basal
mammalian patterns. However, several novelties
discovered in Trichosurus, reveal that it exhibits an
evolutionary transition to intermediate eutherian-like
morphological and motor patterns paralleling many other
unique features of this species. J. Morphol. 271:438–450,
2010. Ó 2009 Wiley-Liss, Inc.
KEY WORDS: locomotion;
marsupial;
mammals;
hypaxial; eutherian; epipubic bone; mammal evolution
Ó 2009 WILEY-LISS, INC.
INTRODUCTION
Mammals, like all tetrapods, have the four basic
abdominal hypaxial muscle layers that wrap
around the abdomen between the pelvis, ribcage,
and spine (external oblique, internal oblique,
transverses abdominis, rectus abdominis; Fig. 1).
However, marsupials have two additional muscle
layers that are associated with the epipubic bones.
The pyramidalis muscles in marsupials span the
epipubic bones medially and extend obliquely forward to meet on the midline. The marsupial pectineus muscle extends from the femur to the base of
the epipubic bone. During locomotion in South
American marsupials, it has been shown that each
epipubic bone is retracted like a lever by the pectineus muscle and femur as part of a ‘‘crosscouplet’’
pattern of primary activity in abdominal muscles
(Fig. 1A) that provides long-axis support of the
body between diagonal limb couplets (Reilly and
White, 2003, 2009).
In eutherian mammals, the epipubic bones are
absent so that the pectineus muscle attaches
instead on the lateral aspect of the ilium and pubis
where it takes on a swing phase limb-adductor
Contract grant sponsor: U.S. National Science Foundation; Contract grant number: IOB 0520100; Contract grant sponsor: Ohio
University Research Challenge Grant.
*Correspondence to: Steve Reilly, Department of Biological
Sciences, Ohio University, 107 Irvine Hall, Athens, OH 45701.
E-mail: [email protected]
Received 22 June 2009; Revised 17 September 2009;
Accepted 23 September 2009
Published online 27 October 2009 in
Wiley InterScience (www.interscience.wiley.com)
DOI: 10.1002/jmor.10808
HYPAXIAL FUNCTION IN AUSTRALIAN MARSUPIALS
439
Fig. 1. Patterns of abdominal anatomy and function in mammals inferred from comparisons of South American marsupials and
basal eutherians. For simplicity muscles are labeled only on one side of the body. A: Didelphid marsupial hypaxial muscles and epipubic lever system. The sequence of muscles figured illustrates the asymmetrical pattern of muscle activity in the crosscouplet linkage shown previously in the three South American marsupials Monodelphis, Philander, and Didelphis (Reilly and White, 2003;
Reilly et al., 2009) that stiffens the body across diagonal couplets during trotting steps. B: Extant basal eutherian mammals retain
the four basic abdominal hypaxial layers, but have lost the epipubic bones, the pyramidalis muscles are vestigial and the pectineus
has retreated to the lateral aspect of the pubis as a femoral adductor. The eutherian abdominal muscles form a shoulder-to-pelvis
linkage used unilaterally during each step (Reilly et al., 2009). The key motor pattern differences in eutherians is a shift to bilateral rectus abdominis activity dominant on the forelimb side and the shift from stance to swing phase activity of the pelvic pectineus. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]
function (Reed, 1951). The pyramidalis is a small
or vestigial muscle that, when present, spans the
front of the pubis and has no locomotor function.
In basal eutherians, the forces transmitted from
the four remaining hypaxial muscles are no longer
transmitted to the contralateral femur but are
instead transmitted to the midline and pelvis
proper in what we termed a shoulder-to-pelvis
linkage (Fig. 1B; Reilly et al., 2009). The loss of
the epipubic lever system in basal eutherians had
little effect on the function of the remaining four
hypaxial muscles except for the rectus abdominis
muscle. Morphologically, the rectus abdominis
muscle pair is separate in most marsupials but
conjoined along the midline in eutherians (White,
1990). Furthermore, it shifts from unilateral hindlimb-side activity with the crosscouplet in marsupials to unilateral shoulder-side activity in basal
eutherians at slow speeds (see Fig. 1). At higher
speeds, the hindlimb-side rectus abdominis is
recruited to develop a bilateral but asymmetrical
pattern of activity in the muscle pair.
Comparisons across South American marsupials
and eutherians revealed several traits that appear
Journal of Morphology
440
S.M. REILLY ET AL.
sums but reveal an interesting evolutionary transition to an intermediate eutherian-like morphological and motor pattern in Trichosurus that parallels
many other novel features of this species.
MATERIALS AND METHODS
Fig. 2. Phylogenetic positions of our study species within the
Australian marsupials based on the molecular phylogenies of
Beck (2008) and Phillips and Pratt (2008). Generalized possums
are found in the Pseudocheiridae and the Phalangeridae.
to be common to all mammals (Reilly et al., 2009): 1)
all of the hypaxial layers (but not the pectineus) exhibit mild continuous bilateral tonus during resting
ventilation, 2) a 1:1 couplet step to ventilation synchrony is maintained during locomotion, and 3) as
expected from its widespread prevalence in tetrapods (Brainerd, 1999), the transversus abdominis is
bilaterally active during expiration during locomotion. These results are significant because they
show that the 1) loss of the epipubic bones is associated with shifts of muscles to the pelvis proper and
2) a shift in rectus abdominis activity and a shift in
pectineus function from stance epipubic-lever-retractor to swing limb-adductor are the only motor
pattern differences observed with the loss of the epipubic lever system in basal eutherians.
A key question remaining, that we examine in
this study, is how the Australian marsupials fit
into this picture. Given the similarities of three
South American marsupial species, we concluded
that the crosscouplet lever system is a general feature of the didelphid marsupials (Reilly et al.,
2009). Furthermore, based on the presence of epipubic bones and associated muscles in Australian
species, we proposed that they too should possess
the crosscouplet lever system, and therefore, it
would represent the basal condition for the Marsupialia (Reilly and White, 2003, 2009). The goal of
this study was to test these hypotheses with data
on hypaxial muscle function in Australian marsupials. Hypaxial anatomy, muscle function and locoventilatory integration were studied in representative species from two of the major radiations of
possums in Australia: the Pseudocheiridae (within
the Petauroidea) and the Phalangeridae (the sister
group to the kangaroos, Fig. 2). Our results validate the presence of the crosscouplet pattern and
basic epipubic bone lever system in Australian posJournal of Morphology
Representatives of the two major radiations of Australian
possums were studied (see Fig. 2). Overall, five Pseudocheirus
peregrinus (ringtailed possums, Pseudocheiridae, 0.737–0.893
kg, two females, three males) and seven Trichosurus vulpecula,
Phalangeridae, 1.77–2.25 kg, three females, four males) were
used in kinematic studies with subsamples of these individuals
used in videoflouroscopy and electromyographical (EMG) studies (generic names are used herein). Animals were collected
under a Queensland Environmental Protection Agency Scientific Purposes Permit and used under a University of Queensland Animal Ethics Approval Certificate.
All animals were run on a speed-controlled treadmill (70 3
27 cm2) for EMG and gait studies and a 3 3 0.35 m2 trackway
(for gait studies) to accustom them to the experimental procedure prior to data collection. Stride patterns (gaits) used by
these mammals were sampled over a range of trackway (400
Hz, JVC camera) and treadmill matched speeds recorded during
the EMG experiments (500 Hz NAC Camera). The timing of
footfalls for each stride quantified from lateral views of numerous strides of the animals moving over the widest range of
speeds we could obtain in both trackway and treadmill locomotion. Gaits were described following Hildebrand (1976) by plotting limb phase (portion of stride duration that the forefoot follows the ipsilateral hind foot) versus duty factor (portion of
stride duration that the hind foot is on the substrate).
To examine the relationship between ventilation, epipubic
bone movements, and stride timing, we used videoflouroscopy
(Toshiba Fluorex unit) to film (60 Hz) one individual of each
species (males) moving on the treadmill at speeds between 0.01
and 0.5 m/s. From the videoflouroscopy recordings the coordination of footfalls, epipubic bone movements and diaphragmatic
movements (craniocaudal displacement cycles of the apex of the
diaphragm imaged laterally) were noted at different speeds.
Locomotor ventilation and epipubic bone retraction patterns
from the videoflouroscopy were later related to abdominal EMG
patterns via their relationship to stride cycles. Breathing patterns could also be inferred from patterns of EMG activity in
the transversus abdominis muscles which are known to be
active during exhalation in mammals (Reilly et al., 2009).
Muscle activity was recorded in two Pseudocheirus (one 833 g
female and one 861 g male) and four Trichosurus (one 1,770 g
female and three males, from 1,970 to 2,250 g) using standard
fine-wire EMG (Reilly et al., 2009). EMG recordings were made
from tiny (0.05-mm diameter) bipolar stainless steel electrodes
implanted percutaneously or via small incisions directly into
each muscle layer while the animals were under anesthesia (ketamine). The bared metal tips of each electrode were 0.25 mm
(Pseudocheirus) or 0.5-mm long (Trichosurus). The bundle of
electrodes was glued together, passing laterally around the abdomen to a suture point on the skin on the midline anterior to
the pelvis. Animals completely recovered from anesthesia
within 2 hours and synchronized EMG and kinematic data
were sampled for initial resting breathing, during several bouts
of locomotion, and then resting breathing after locomotion. Animals were rested (about 5–10 min) between bouts of locomotion
(lasting 40 s maximum). EMG signals were amplified 10,000
times using AM Systems model 1700 differential AC amplifiers
with a bandpass of 100–3,000 Hz (and a 60 Hz notch filter), and
then recorded on a Cambridge Electronics MICRO 1401 analog
to digital converter that generated a synchronization pulse
simultaneously recorded on the video frames. EMG data were
recorded and analyzed using the Cambridge Electronics SPIKE
5.0 software with sample rate for each channel set at 10,000 Hz
to obtain reliable recordings of EMG burst patterns (Jayne
HYPAXIAL FUNCTION IN AUSTRALIAN MARSUPIALS
TABLE 1. Electromyographical sampling of abdominal muscles
for marsupials used in this study
Number of individuals sampled
(right/left sides)
Muscle
Rectus abdominis
Internal oblique
External oblique
Transversus abdominis
Pyramidalis
Pectineus superficial
Pectineus deep
Pseudocheirus
(n 5 2)
Trichosurus
(n 5 4)
2/2
1/1
2/1
2/1
2/2
1/2
4/3
3/3
4/2
2/2
4/4
3/2
1/2
et al., 1990). EMG profiles were inspected for possible patterns
revealing crosstalk. Immediately following data collection, each
animal was euthanized by overdose of anesthetic (nembutol)
and electrode position was then confirmed by dissection. Only
individual preparations in which the electrode lay completely
within the muscle were used in the analysis.
We attempted to record bilateral motor patterns in each of
the four abdominal hypaxial layers (rectus abdominis, transversus abdominis, external and internal obliques) and the pyramidalis and pectineus muscles in each individual. Dissection of
fresh specimens prior to EMG work revealed that Trichosurus
has two pectineus bellies: a superficial belly (essentially identical to the single femur-to-epipubic bone pectineus in Pseudocheirus) and a deep belly medial to the former extending to the
lateral pubis, see results later). Thus, we attempted to record
from both bellies in Trichosurus. Samples sizes realized are
indicated in Table 1. Each individual was subjected to a series
of treadmill bouts in which they were carefully brought up to a
given speed and a sample of 10–20 s of EMG recording was
made as they matched that given speed. Speed effects on locoventilatory integration were observed by relating footfalls to diaphragmatic movements (videoflouroscopy) and transversus abdominis bursts over the range of steady state speeds we could
obtain from each animal. To examine the relationship between
muscle activation bursts and stride timing, footfall timing patterns digitized from videos were aligned with simultaneous
EMG recordings for multiple strides from each individual. Unilateral versus bilateral patterns of muscle activity could easily
be identified from the presence of either one or two bursts of
EMG activity per stride.
To better compare the details of hypaxial muscle and epipubic
bone variation among these two species, five of each were dissected (Trichosurus: four EMG animals plus one road kill specimen; Pseudocheirus: two EMG animals plus three road kill
specimens). Gross anatomy of muscles and their attachments
were noted and epipubic bone dimensions, body mass and
snout-vent length were taken. Epipubic length was the longest
length of the bone, from the medial edge of the proximal (articular) base to the distal tip. The width was measured along the
proximal base of the bone along its articulation with the pelvis.
To quantify differences in the single pectineus belly in Pseudocheirus compared with the double bellies in Trichosurus, several
variables were taken from the left limb of each specimen with
the femur held perpendicular from the body axis. For each belly
the total (maximum) length and the midbelly width and depth
muscle were measured with digital calipers to the nearest 0.1
mm (the muscles were flatly elliptical in cross-section). These
linear measures were scaled to body length (snout-vent length).
For a rough comparison of the force generating capacity of the
muscles between the species (assuming similar fiber organization), the cross-sectional area of the pectineus was calculated as
the product of the midbelly width and depth (mm) divided by
body mass (kg). Species means were compared using Bonferroni
corrected t-tests.
441
To further examine the relative size of epipubic bones in Trichosurus, we compared epipubic scaling in a larger sample of
species from the families of our study species and New World
didelphids. In addition to our study individuals, we used taxa
available in White (1989) and from additional samples of Australian taxa we measured from skeletal collections at the
Queensland Museum. Epipubic length and width were measured as indicated earlier and scaled to total pelvis length
because body mass and length data were not available on many
of the museum specimens.
RESULTS
Gaits
During treadmill locomotion both Trichosurus
and Pseudocheirus matched treadmill speeds only
between 0.1 and 0.4 m/s and only used diagonalcouplets dominated gaits (Fig. 3). In trackway locomotion, both species tended to move faster (Pseudocheirus 0.38–1.97 m/s; Trichosurus, 0.31–2.17 m/
s) using diagonal couplet dominated gaits trending
toward trotting and diagonal-sequence gaits at the
higher speeds (Fig. 3). Pseudocheirus tended to
transition to diagonal-sequence singlefoot gaits at
the highest speeds. At high speeds both species
also switched to asymmetrical gaits but the two
species differed in their propensity to use them.
On the trackways Pseudocheirus used halfbounds
or gallops 6.2 6 3.0 (SE) % of the time (n 5 66,
individual percentages: 0–16.7%) versus 32.9 6 8
(SE) % in Trichosurus (n 5 80, individual percentages: 7.7–71.4%). Because only symmetrical gaits
were obtained on the treadmill, all EMG data are
matched with these gaits.
Muscle Variation
Exploratory dissections in preparation for EMG
studies revealed similarity in the insertions, origins and general relative positions of the four of
the abdominal muscles (transversus abdominis,
pyramidalis and internal and external obliques
excepted as noted later). However, the epipubic/
pelvic insertions of the other two muscles differed
in the two species.
The rectus abdominis muscle was wide and
inserted all along the medial surfaces of the epipubic bones in Pseudocheirus similar to the position
observed in didelphids. Only a few fibers attached
to the pelvis between the epipubic bones. In Trichosurus the rectus abdominis muscles narrowed
posteriorly between the epipubic bones, to insert
only on the posterior one-third of the medial surface of the epipubic bones. About two-thirds of the
Trichosurus rectus abdominis muscle attached to
the pelvis between the epipubic bones and deeper
on the pubis.
The pectineus of Pseudocheirus extended from
its tubercle on the base of the epipubic bone to
insert on the middle third of the shaft of the femur
and is similar to that of didelphids (Fig. 4, top).
Journal of Morphology
442
S.M. REILLY ET AL.
single head of Pseudocheirus. Thus, the entire pectineus was smaller in Trichosurus and based on
cross-sectional areas of the two heads, Trichosurus
had 60.3% of the influence of the pectineus has
moved off of the epipubic bone to the pelvic pubis.
Epipubic Bone Variation
The size of the epipubic bones also differs in the
two species (Table 1). The epipubic bones of Trichosurus were significantly shorter in both absolute
length (25% shorter) and relative to body length
(65% shorter). In absolute width, Trichosurus have
wider epipubic bones but when scaled to body size
their epipubic bones are 20% narrower at the base
than Pseudocheirus. Because length differences
Fig. 3. Locomotor gaits observed in our study species over
the range of speeds they used in treadmill (0.1–0.4 m/s, filled
symbols) and trackway (0.31–2.17 m/s, open symbols). Duty factor is the portion of the stride time that the hind foot is on the
ground and Limb phase is the portion of stride duration that
the fore footfall follows the ipsilateral hind foot-fall. Comparative gait spaces are from White (1990; Didelphis, Dasyurus),
Parchman et al. (2003; Monodelphis), Reilly et al. (2009; Philander and eutherians), and Lemelin et al. (2003; Caluromys).
All data are from level substrate studies.
Trichosurus, however, was found to have two pectineus bellies (Fig. 4, bottom). The superficial belly
was in the same position of the single muscle in
Pseudocheirus (hereafter referred to as the epipubic head). A newly identified deep belly (hereafter
the pelvic head) was present extending from the
pelvis lateral and medially deep to the epipubic
joint, to the shaft of the femur distal to the outer
belly. The two bellies in Trichosurus were easily
observed by simply pulling on the outer belly.
Table 2 presents comparative data for the pectineus muscles in the two species. Clearly the pectineus of Trichosurus has moved partially off of the
epipubic bone forming a new slip to the pelvic
pubis. Although Trichosurus was significantly
larger in body size, its epipubic head was significantly smaller than the entire pectineus in Pseudocheirus (in length, width, and depth) in both
absolute size (23, 9, and 18% smaller, respectively)
and relative to body size (71, 53, and 56% smaller,
respectively). Accordingly, compared with the pectineus of Pseudocheirus, the smaller epipubic head
in Trichosurus resulted in about one-third the
mass-adjusted estimate of cross-sectional area
(Table 2) that can influence the epipubic bone. The
pelvic head in Trichosurus was shorter, but was
significantly wider (25%) and tended to be thicker
(25%, P 5 0.097) which results in an estimated
cross-sectional area that is about 65% greater than
its epipubic head. The summed cross-sectional
area of the two heads of the pectineus in Trichosurus was less than the cross-sectional area of the
Journal of Morphology
Fig. 4. Variation in the pectineus muscle in the study species. In Pseudocheirus and many other marsupials the pectineus extends from the base of the epipubic bone to the middle
third of the femoral shaft. In Trichosurus the pectineus muscle
has adjacent but independent, side-by-side superficial and deep
bellies. The superficial belly (epipubic head) is in the same position as the entire pectineus muscle of Pseudocheirus. The deep
belly (pelvic head) extends from pelvic pubis to the distal third
of the femur. Epipubic bones are highlighted by dashed outlines. Scale bar on the right indicate 1 cm. [Color figure can
be viewed in the online issue, which is available at www.
interscience.wiley.com.]
HYPAXIAL FUNCTION IN AUSTRALIAN MARSUPIALS
TABLE 2. Comparison of pectineus muscles and epipubic bones
in Pseudocheirus and Trichosurus
Trichosurus
Mass (kg)
Snout-vent length (SVL, mm)
Pectineus epipubic head
Length (mm)
(% SVL)
Width (mm)
(% SVL)
Depth (mm)
(% SVL)
Mass adjusted cross-sectional
Area (mm2 /kg)
Pectineus pelvic head (% SVL)
Length (mm)
(% SVL)
Width (mm)
(% SVL)
Depth (mm)
(% SVL)
Mass adjusted cross-sectional
Area (mm2 /kg)
Pectineus total cross-section
Area (mm2 /kg)
Epipubic bone length (mm)
(% SVL)
Epipubic bone width (mm)
(% SVL)
Pseudocheirus
a
2.002 6 0.073
433 6 9.9a
47.3
10.9
5.73
1.3
3.8
0.9
6
6
6
6
6
6
1.7b
0.23b
0.1
0.03
0.3
0.09
10.9 6 0.8
37.8
8.8
7.2
1.7
4.6
1.0
0.764 6 0.061
313 6 27.2
58.1
18.6
6.2
2.0
4.5
1.4
32.5 6 2.8a
—
61.0
6 0.29
6 0.4b
6 0.12b
6 0.4
6 0.10
—
—
16.55 6 2.3b
27.44
26.80
6.6
14.7
3.4
6
6
6
6
6
2.4
2.1
0.41
0.6
0.02
6 4.7a
6 0.12a
6 0.4a
6 0.03a
60.4a
6 0.06a
—
36.75
34.34
10.9
12.9
4.1
6
6
6
6
6
3.5a
3.1a
0.07a
1.2
0.01a
Data are means 6 SE for five individuals per species. Significantly larger measures (t-tests, P < 0.05) are indicated for
between speciesa and between Trichosurus pectineus heads.b
were greater than width differences, Trichosurus
was found to have, on average, 37% lower lengthto-width ratios compared with Pseudocheirus (see
outlines of epipubic bones in Fig. 4).
Thoracic Ventilatory Movements at Rest and
During Locomotion
During resting ventilation and locomotion both
species exhibited observable diaphragmatic movements under videoflouroscopy. Resting diaphragmatic cycle rates were around 1.5 Hz in Pseudocheirus and 1 Hz in Trichosurus. During locomotion on the treadmill, all strides for both species
(roughly 100 each for each of the two individuals
per species) exhibited one cycle of diaphragmatic
movement per diagonal couplet step (two breaths
per stride). Thus, a 1:1 pattern of limb couplet cycling and diaphragmatic ventilation was characteristic of locomotion over the 0.1–0.4 m/s speed
range.
Abdominal Motor Patterns at Rest
Hypaxial EMG at rest revealed that both species
exhibited continuous low-amplitude activity in all
of the hypaxial muscles, including the pyramidalis
(see Fig. 5). The pattern of bilateral, continuous
tonus of the abdominal muscles was maintained
over many thoracic ventilatory cycles (externally
443
observed as visible movements of the abdomen/
thorax assumed to reflect diaphragm movements).
Thus, at rest, constant low intensity abdominal
tonus was maintained in the face of continuous
cycles of contraction and relaxation of the diaphragm. The pectineus was silent in both species
at rest except when the limbs occasionally shifted
position. After bouts of locomotion both species
returned to the abdominal tonus pattern observed
before locomotion.
The Crosscouplet Pattern in Both Species
The relationship between the movements of epipubic bones and hindlimbs was obtained using videoflouroscopy at treadmill speeds of 0.1–0.4 m/s.
Under these conditions, each epipubic bone was
found to retract together with its ipsilateral femur
and then rapidly protract in early swing phase
during each stride. Both species were observed to
use diagonal couplet dominated gaits over the
speeds attained on the treadmill (Fig. 3).
Abdominal motor patterns during locomotion
showed that both species exhibited the crosscouplet motor pattern: The internal and external
oblique muscles of the forelimb side fired in concert with the rectus abdominis, pyramidalis, and
pectineus muscles of the hindlimb side (see Fig. 6).
The transversus abdominis was active bilaterally
during each couplet step firing in synchrony with
the exhalation phase of each ventilatory cycle. As
speed increased the couplet step rate and ventilatory rate (transversus abdominis burst rate and by
inference the diaphragm cycle rate) maintained a
1:1 relationship at all speeds possible on the treadmill (up to about 0.4 m/s). However, within the experimental setup both species preferred moderate
speeds between about 0.15 and 0.3 m/s and trotting gaits (see Fig. 3).
‘‘Novel’’ Motor Patterns in Trichosurus
Rectus abdominis. Motor patterns in the rectus abdominis and the pelvic head of the pectineus
of Trichosurus consistently exhibited differences
from Pseudocheirus. In Trichosurus (Fig. 6B), the
rectus abdominis usually exhibited a strong burst
with the ipsilateral hindlimb stance phase as
expected in the diagonal pattern associated with
the crosscouplet lever system (as exemplified by
Pseudocheirus, Fig. 6A). However, the rectus abdominis also consistently exhibited a contralateral
burst with each step (present in all strides across
individuals). This contralateral burst (e.g., right
rectus abdominis firing with the left hindlimb
retraction) maintained the same level of asymmetry within the series of strides sampled at a given
speed in a recording bout but appeared to increase
in duration with speed. Generally, at slower speeds
the swing burst was weaker as illustrated in FigJournal of Morphology
444
S.M. REILLY ET AL.
Fig. 5. Abdominal hypaxial motor patterns in Australian marsupials during resting breathing. Electromyograms for both species over several respiratory cycles illustrate the maintenance
of constant, low amplitude muscle activity indicating bilateral tonus in all four hypaxial muscles
and the pyramidalis but not in the pectineus. Exhalation and inhalation timing is indicated
with bars at the top of each panel.
ure 6B (in about two-thirds of strides sampled),
but it was variably equal to or sometimes greater
in intensity than the crosscouplet burst as speed
increased (in about one-third of the strides). With
the narrow speed range sampled and the large
variation in rectus abdominis bursts it was impossible to quantify the speed effects statistically.
However, it appeared that the ipsilateral couplet
burst remained constant while contralateral burst
increased in amplitude with speed. Clearly, the
rectus abdominis motor pattern of Trichosurus has
shifted to a variable, bilateral pattern of activity.
Motor patterns in the Trichosurus pectineus. The two heads of the Trichosurus pectineus
muscle exhibit different motor patterns. The epipubic head exhibits the same motor pattern
observed in Pseudocheirus and other marsupials
with large amplitude bursts correlated with epipubic bone retraction when the limb retracts (Fig.
Journal of Morphology
6B). This is coincident with the rest of the diagonal array of muscles firing in the crosscouplet
lever system.
During locomotion the pelvic head of the pectineus usually exhibits a continuous, moderate-amplitude tonic background pattern with obvious
increases in amplitude during swing phase (Fig.
6B, pectineus, pelvic head, slow). Activity in the
pelvic head increased at higher speeds (Fig. 6B,
fast). Accordingly, the larger amplitudes occur out
of phase with the crosscouplet pattern observed in
the epipubic head. When the animal was standing
or turning around the low amplitude tonus in the
pelvic head continued but it variably increased
and decreased in amplitude. After reviewing the
videos, it was clear the varying amplitude of the
tonus has related to postural movements when the
animals changed positions on the treadmill. Thus,
the new pectineus head functions as a hip stabi-
HYPAXIAL FUNCTION IN AUSTRALIAN MARSUPIALS
445
DISCUSSION
Basal Conditions for Mammals Confirmed
Fig. 6. Crosscouplet and novel patterns of abdominal motor
activity during locomotion in Australian marsupials. Pseudocheirus (A) shows the diagonal pattern of unilateral muscle contraction with each diagonal couplets step that illustrates the
crosscouplet epipubic lever system spanning from one shoulder
to the opposite hindlimb as in South American marsupials.
Trichosurus (B) exhibits the same crosscouplet pattern except
for the addition of a bilateral rectus abdominis burst and the
advent of primarily swing phase function in its new pelvic head
of the pectineus. Exhalation and inhalation timing and footfall
(gait) patterns indicated with bars at the top and bottom of
each panel.
lizer and variably ramps up intensity as a swing
phase femoral adductor/protractor during locomotion.
Our results confirm that the Australian marsupials possess the three functional traits related to
hypaxial abdominal muscle function that were previously hypothesized to be basal for mammals (see
Fig. 1) based on comparisons across South American marsupials and eutherians (Reilly et al.,
2009).
The first trait involves the bilateral activity of
the transversus abdominis during expiration during locomotion. This finding was expected based on
its widespread prevalence across tetrapods (Brainerd, 1999).
The second functional trait, involves all of the
hypaxial layers (including the pyramidalis in marsupials) but not the pectineus. These muscles show
continuous mild activity, during resting breathing.
This tonic activity has been hypothesized to
increase intra-abdominal pressure and rigidity to
aid the initial passive recoil of the diaphragm during exhalation (Reilly and White, 2009). In erectlimbed cursorial mammals, tonic activity in the abdominal hypaxial layers is observed in resting
breathing but it is highly variable in muscles
involved both within and among species. The
external oblique has been reported to sometimes
exhibit a resting tonus in humans (De Troyer
et al., 1990) and dogs (De Troyer et al., 1989; Farkas et al., 1989; Ainsworth et al., 1996; Deban and
Carrier, 2002), and dogs also exhibit tonus in the
transversus abdominis at rest, although activity
ceases during each inhalation (De Troyer et al.,
1989). In dogs and humans, the primitive pattern
of resting tonus in abdominal muscles is only
observed in low-energy states. Sustained tonus is
seldom observed because these species have a low
threshold for the active recruitment of bilateral expiratory bursts in the transversus abdominis, rectus abdominis, and the external oblique at rest
and during locomotion (De Troyer et al., 1990;
Deban and Carrier, 2002). Active exhalation
involving the hypaxial muscles functions to
increase the rate of exhalation and to increase
tidal volume beyond the passive end-expiratory
volume (Ainsworth et al., 1989; DeTroyer et al.,
1989). The Australian possums did not exhibit any
evidence of active or accessory recruitment of the
hypaxial muscles in ventilation when coming out
of anesthesia, at rest, or post exercise. However,
some of the didelphid marsupials do exhibit accessory hypaxial recruitment during locomotion
(Monodelphis) or under high oxygen demand (postanesthesia and immediately after fast locomotion,
Philander) before returning to resting tonus. Marsupials that use bilateral ventilatory motor patterns appear to have a relatively higher threshold
than eutherians for using active bilateral hypaxial
ventilation (Reilly et al., 2009). Overall, comparing
Journal of Morphology
446
S.M. REILLY ET AL.
across marsupials and eutherians shows a generalized mammalian condition with a consistent pattern of tonus in all of the hypaxial musculature
during resting ventilation. However, some mammals rely more heavily on active recruitment of
hypaxial musculature to aid in ventilation at rest
and during locomotion.
Finally, a 1:1 breath-to-step cycling pattern (the
third functional trait) was characteristic of the
Australian marsupials when they used symmetrical gaits. Coupling limb cycling to ventilation cycling is widely thought to enhance sustained aerobic locomotor capacity by minimizing the conflicts
between the locomotor and ventilatory functions of
the limbs (Carrier et al., 2008) and trunk (Bramble
and Carrier, 1983; Lee and Banzett, 1997). Locoventilatory integration and gaits of these Australian marsupials (this study), didelphids (Reilly and
White, 2009), basal eutherians (Reilly et al., 2009),
and cursorial eutherians (Bramble and Carrier,
1983) confirm that the slow speed pattern of one
breath per step with symmetrical gaits appears to
be the plesiomorphic and dominant condition for
mammals. With the demands for higher speed,
many mammals including marsupials transition to
a one breath per stride at higher speeds associated
with asymmetrical gaits (Pridmore, 1992; Fischer
et al., 2002; Schilling and Hackert, 2006). Pseudocheirus and Trichosurus both shifted to asymmetrical gaits (half-bounds, gallops) at high speeds.
Thus, it appears that a high speed one breath per
stride coupling is present in marsupials and
eutherians and may also be a basal characteristic
for mammals that need to transition to higher
speeds.
The Crosscouplet Pattern is Basal
for Marsupials
Patterns of motor activity in hypaxial muscles
and pectineus in both Australian opossum species
were found to be consistent with the crosscouplet
lever system observed in other marsupials. The diagonal array of forelimb-side obliques firing with
hindlimb side rectus abdominis, pyramidalis, and
pectineus (epipubic head in Trichosurus) was evident during couplet dominated steps in both species. In addition, each couplet step was associated
with the unilateral retraction and then protraction
of each epipubic bone together with its ipsilateral
femur (as visualized with videoflouroscopy). This
provides further support for the hypothesis that
the crosscouplet lever system represents the basal
condition for the Marsupialia (Reilly and White,
2003, 2009). Pseudocheirus universally exhibited
the cross couplet pattern in these muscles essentially identical to those of Monodelphis, Didelphis,
and Philander (Reilly and White, 2003; Reilly
et al., 2009). Trichosurus exhibited the same pattern but with some differences in the bilateral naJournal of Morphology
ture of the rectus abdominis and pectineus contractions discussed later.
Eutherian-Tendencies in Trichosurus
In eutherians, the shoulder-to-pelvis linkage is
the result of the morphological shift of the rectus
abdominis and pectineus muscles onto the pelvis
proper with the loss of the epipubic bones and
changes in the timing of motor patterns of these
muscles (see Fig. 1). Although Trichosurus utilizes
the crosscouplet motor pattern and associated epipubic bone retraction movements during locomotion, it has novel characteristics of the rectus abdominis, the pectineus, and the epipubic bones
that clearly parallel some of the key transitions
involved in the change to the basal eutherian
condition.
Transitional Rectus Abdominis
One of the main consequences of losing epipubic
bones in eutherians is the shift of the rectus abdominis muscles from medial surfaces of the epipubic bones onto the anterior and medial surfaces of
the pubis. Comparing South American marsupials
to basal eutherians revealed a shift in the rectus
abdominis motor pattern as well (Reilly et al.,
2009). In the basic marsupial step (Figs. 1A and
6A), the hindlimb-side rectus abdominis fires unilaterally as part of the crosscouplet linkage. However, in basal eutherians, the rectus abdominis has
shifted to a forelimb-side-dominant bilateral firing
pattern during each couplet step that becomes
more balanced as speed increases (Fig. 1B). Trichosurus is in between these two conditions: its rectus
abdominis attaches about one-third on the epipubic bones and two-thirds pubis proper. In addition,
it has a bilateral motor pattern that retains the
hindlimb-side dominance of the crosscouplet system but ramps up to a balanced or even forelimbside dominant (eutherian-like) pattern at high
speeds. Thus, in Trichosurus appears to be moving
the attachment of the rectus abdominis off of the
epipubic bones and onto the pelvis which is complemented by a shift to a bilateral, speed-related
motor pattern that shifts a majority of this
muscle’s effect from the crosscouplet linkage onto
the pelvis instead of the contralateral femur.
Transitional Pectineus
Compared with the normal marsupial condition,
exemplified by Pseudocheirus, the pectineus muscle of Trichosurus has shifted more than half of
the muscle cross-sectional area onto the pubis
proper (Fig. 3, Table 2). The function of the pectineus is transitional as well. The epipubic head
retains the marsupial motor pattern, firing with
the ipsilateral hindlimb stance phase. The varying
HYPAXIAL FUNCTION IN AUSTRALIAN MARSUPIALS
low amplitude tonic pattern of the pelvic head
shows that it is acting as a general hip joint stabilizer while standing and during locomotion.
Increasing amplitudes during the swing phase
show that the pelvic head is serving as a locomotor
limb adductor and/or flexor, as well.
The eutherian pectineus muscle has been
neglected in terms of EMG study of its activity
during locomotion. Based on the muscles attachments most authors agree that it is primarily a
hip adductor with some function in femoral flexion
(Reed, 1951; Woodburne, 1960; Johnson et al.,
2008). Takebe et al. (1974) recorded EMG in
humans and concluded that pectineus works as a
hip stabilizer and in swing phase limb flexion. Evidence for the hip stabilizer function also comes
from the common assumption in dogs and cats
that the pectineus can contribute to hip dysplasia
(Remedios and Fries, 1995). When the muscle is
underdeveloped (too short or weak), it allows the
head of the femur to ride upward out of the acetabulum (Ihemelandu, 2007). Indeed, the pectineus
is often surgically removed in older dysplastic dogs
to eliminate the pain associated with the muscles
usual adductive/stabilizing role that pulls the femoral head into the now arthritic dorsal acetabulum
(Remedios and Fries, 1995). In both humans
(Takebe et al., 1974) and dogs (Bowen, 1974) data
are not presented in relation to limb movements
during locomotion. However, the motor patterns
illustrated show continuous tonic activity patterns
like those exhibited by the pelvic head of the pectineus in Trichosurus.
The transitional pectineus in Trichosurus provides some insights into how the eutherian pectineus may have evolved. The eutherian pectineus
has long been considered a composite muscle
because it originates from both ventral (obturator
innervation) and dorsal (femoral innervation) muscle masses (Patterson, 1891; Woodburne, 1960;
Lance Jones, 1979). Thus, the two portions of the
eutherian pectineus can, by position, be functionally associated with the ventral (adductor) and anterior (femoral flexion) compartments of the thigh.
If we assume that the pelvic and epipubic heads of
Trichosurus represent the ventral and dorsal components of the eutherian pectineus then we can
make several inferences (the epipubic head was innervated by the femoral nerve, but we did not ascertain the innervation of the pelvic head). First, it
appears that the ventral (adductor) component of
the Trichosurus pectineus has made the transition
to the eutherian condition with a shift in position
and a motor pattern shift from focused stance
phase bursts to a generalized adductor/flexor
motor pattern. Second, the epipubic head would
also have to make the same positional and motor
pattern changes with the reduction and loss of the
epipubic bones. Detailed EMGs of eutherian pectineus muscle activity during locomotion are needed
447
to test these hypotheses and quantify the function
of the pectineus muscles in eutherian mammals.
Transitional Epipubic Bone Morphology
One of the most obvious differences between
marsupials and extant eutherian mammals is the
presence of epipubic bones articulating with the
anterior aspect of the pubis. Mammals either have
epipubic bones or they do not but within marsupials they vary in size (White, 1989). The epipubic
bones in Trichosurus were about 25% smaller in
absolute size than Pseudocheirus. Given the much
larger body size of Trichosurus, this equates to epipubic bones that are smaller by about 60% of their
relative length. To further examine the relative
size of epipubic bones in Trichosurus we compared
epipubic length and width in a sample of species
from the families of our study species, museum
specimens and the didelphids (see Fig. 7). This
revealed that Trichosurus has relatively shorter
(but not narrower) epipubic bones than the other
phalangerids, the didelphids and all of the pseudocheirids except Petauroides volans. Thus, it
appears that Trichosurus is phasing out the epipubic bones. Although reduction of the epipubic bone
in Petauroides is consistent with the tendency for
gliders to have rudimentary epipubic bones (Reilly
et al., unpublished data), the reduced epipubic
bones in Trichosurus appear to be unique for a
generalized quadrupedal marsupial.
Functional and Evolutionary Inferences
About Novel Conditions in Trichosurus
Altogether the combination of transitional morphologies and motor patterns in Trichosurus
appears to be a surprisingly good example of an intermediate condition between the typical marsupial and eutherian conditions and is similar to
what may have occurred in the shift from the
crosscouplet linkage (marsupials) to shoulderto-pelvis linage (eutherians). Differences in the
anatomy and motor patterns in the rectus abdominis and pectineus in Trichosurus relative to other
marsupials are associated with a reduction in epipubic bone size. Functionally, the shift in muscle
effects from the epipubic bones (and thus, from the
crosscouplet linkage to the femur) to the pelvis
proper means that both the marsupial and eutherian conditions are working in Trichosurus. However, the epipubic bones of Trichosurus have shortened and appear to reflect a decrease in leverage
associated with the decreased insertion of the rectus abdominis medially and the decrease in the
amount of pectineus muscle on the epipubic bone
laterally. Trichosurus was also different in that the
transversus abdominis muscle does not attach to
the epipubic bones and the fibers of the internal
Journal of Morphology
448
S.M. REILLY ET AL.
Fig. 7. Patterns of epipubic bone size scaling in the Pseudocheiridae, Phalangeridae, and didelphid marsupials. Among the
pseudocheirids, Pseudocheirus peregrinus is indicated with
slash marks. Data from Queensland Museum specimens and
White (1989).
oblique do not extend medially to the side of the
rectus abdominis as in other marsupials.
Trichosurus also exhibits several other unique
traits compared with its sister taxa within the
phalangeridae and the petauroidean possums.
First, its diet and feeding habits are more terrestrial. The cuscuses (sister group to Trichosurus)
and pseudocheirids are arboreal and considered to
be slow deliberate climbers specializing on a highly
folivorous (eucalypt) diet (Rasmussen and Sussman, 2007). In contrast, the members of the genus
Trichosurus are dietary (Wellard and Hume, 1981)
and locomotor generalists (Statham, 1984) and
wide foragers that feed on the ground on average
23% of each night (Freeland and Winter, 1975).
Trichosurus appears to be losing its tolerance of
eucalyptus toxins (Freeland and Winter, 1975) and
increasing its tolerance of grassland plants toxins
(Mead et al., 1979). It has longer loops of Henle
and renal urine concentrations closer to wombats
than other possums (Reid, 1977). Thus, Trichosurus is physiologically and ecologically more terrestrial than other possums.
Second, the hands of petauroids and phalagerids
are indistinguishable in multivariate morphospace
(Weisbecker and Warton, 2006), which is congruent with their general anatomical and ecological
similarities (Aplin and Archer, 1987). However, the
genus Trichosurus is unique among these taxa in
having lost zygodactyly (Goldfinch and Molnar,
1978) and it has the narrowest hand of any Australian possum (Weisbecker and Warton, 2006). It
has been suggested that hand shape is related to
differences in locomotor behavior (Taylor, 1974;
Hildebrand and Goslow, 2001) and the shifts in
the Trichosurus hand reflect its secondary evolution toward more terrestrial and perhaps more
asymmetrical locomotion.
Journal of Morphology
Third, Trichosurus is trending to be somewhat
different in locomotor gaits as well. While most
tetrapods use primarily trotting gaits with a tendency for the forefoot of each swinging couplet to
land first (lateral sequence gaits, Hildebrand,
1966; Reilly and Biknevicius, 2003) Pseudocheirus
and Trichosurus trended toward the diagonal
sequence gaits with the hind foot leading each couplet step (see Fig. 3). Both species used trotting
gaits and diagonal sequence strides over a range
of slow to moderate speeds, but Trichosurus had a
greater tendency to use higher limb phase strides
(see Fig. 3). Also, Pseudocheirus appeared to maintain symmetrical gaits at higher speeds rather
than switching to asymmetrical gaits (6.2%) compared with Trichosurus which more readily (33%)
switched to asymmetrical gaits like many cursorial
mammals. Among mammals, a tendency toward
diagonal sequence gaits is characteristic of most
primates (Hildebrand, 1967; Cartmill et al., 2007;
Young et al., 2007). However, our two Australian
species add to the growing list of nonprimates
employing higher limb phases (African dik dik,
Madoqua, Hildebrand, 1966; wooly opossum,
Caluromys, Lemelin et al., 2003; slender loris,
Loris, Schmitt and Lemelin, 2004).
Much has been said about the compelling similarities of many arboreal phalangerids to primitive primates (Rasmussen and Sussman, 2007) and the utility of comparing arboreal didephids and primates to
understanding primate evolution (Lemelin and
Schmitt, 2007). However, Trichosurus is clearly contrary to the fine-branch primates in many ways and
may be an informative model for parallels in the evolution of large branch/trunk and terrestrial primates.
Trichosurus is easy to work with and is one of the few
marsupials actually thriving in Australia, and
unfortunately, New Zealand. It is quite terrestrial
with great success in little forested, rocky, urban and
grassland habitats in Australia and it has invaded
most of New Zealand’s farmland and grasslands. It
has been described as having a primate head on a
possum body (Rasmussen and Sussman, 2007). Trichosurus appears to have relatively longer hindlimbs
and a more upright limb posture than Pseudocheirus
giving it more of the erect hindlimb and may have a
tendency toward hindlimb dominance patterns seen
in terrestrial primates. It has shifted to narrower and
nonzygodactylous hands and it readily uses symmetrical and asymmetrical gaits which are probably
facilitated by the suite of eutherian tendencies in its
abdominal function discussed earlier.
Finally, we were fortunate that our two taxon sample provided so much confirmation and novelty.
Except for its tendency toward diagonal sequence
gaits (probably related to fine branch arboreality),
Pseudocheirus was very similar to didelphid marsupials. These lineages diverged 80 million years ago in
the Cretaceous (Beck, 2008) and their similarity
today illustrates that the marsupial bauplan has held
HYPAXIAL FUNCTION IN AUSTRALIAN MARSUPIALS
up well to arboreality and the test of time and competition with the Eutheria. Trichosurus and Pseudocheirus shared a common ancestor about 50 million
years ago (Beck, 2008) and represent taxa that sustained the ‘‘possum’’ lifestyle while their kangaroo
relatives invaded the grasslands. However, Trichosurus appears to be changing ecology, function and bauplan. As pointed out by Phillips and Pratt (2008) it is
interesting that, in contrast to the rest of the Petauroidea and Phalangeridae that are specialized arboreal forms, Trichosurus occupies the ecospace and
body size that lies between the purely arboreal
possums and the purely terrestrial wombats and kangaroos. Dendrolagus (the tree kangaroos), are undergoing similar ecological and morphological shifts
(Newell, 1999; Phillips and Pratt, 2008), but Trichosurus is transitioning down out of the trees while the
tree kangaroos are transitioning up into them.
SUMMARY
Hypaxial anatomy and function during rest and
locomotion and locoventilatory integration are
described for two Australian marsupials. As in
other marsupials, the Australian species exhibited
functional patterns consistent with the crosscouplet epipubic bone lever system supporting the hypothesis that this locomotor pattern represents the
basal condition for the Marsupialia. The Australian species also exhibited three functional traits
posited to be basal patterns for the Mammalia: 1)
tonic resting activity in all the hypaxial muscles
during resting breathing, 2) bilateral transversus
abdominis activity consistent with an exhalitory
function during locomotion, and 3) a 1:1 breath to
step cycling pattern during locomotion during symmetrical gaits. Finally, Trichosurus exhibited a series of intermediate ‘‘eutherian-like’’ characteristics in the hypaxial muscles, epipubic bones, and
pectineus muscles that are discussed in relation to
other Trichosurus novelties (in diet, gait, foraging
mode, loss of zygodactyly, physiology, and hindlimb
dominance) that appear to be related to an evolutionary transition from fine branch to terrestrial
lifestyle.
ACKNOWLEDGMENTS
The authors thank Kristen Stover for assistance
in the video analysis of gaits, Susan Williams and
Biren Patel for discussions about the work, and
Angela Horner for critical manuscript review.
They also thank the Queensland Museum staff for
their hospitality and access to incredible collection
materials, and Dr. Steve van Dyck, Senior Curator
of Mammals and Heather Janetzki, Collection
Manager, Mammals and Birds. All procedures followed approved U.S. and Australian animal collection, care and use protocols.
449
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