AMER. ZOOL., 29:287-301 (1989)
The Avian Shoulder: An Experimental Approach1
G. E. GOSLOW, JR.
Department of Biological Sciences, Northern Arizona University,
Flagstaff, Arizona 86011
AND
K. P. DIAL AND F. A. JENKINS, JR.
Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology,
Harvard University, Cambridge, Massachusetts 02138
SYNOPSIS. This essay is in two parts. The first describes functional studies of the shoulder
in modern vertebrates that led to the formulation of the hypotheses that motor patterns
of homologous muscles have been maintained during the evolution of the tetrapod shoul-
der, and that a primitive organization of the neural control components has persisted in
derived groups.
The second part of this essay focuses upon a longstanding question in vertebrate evo-
lution: what neuromuscular and musculoskeletal changes in the tetrapod shoulder accom-
panied the evolution of flight in birds? The lack of empirical data on shoulder function
in extant birds limited our insight into this question, and prompted our initiation of
experimental studies. Preliminary kinematics of the furcula and humerus of European
starlings (Sturnus vulgaris) flying in a wind tunnel, as revealed by high speed cineradiog-
raphy, are presented. The two halves of the furcula, which contact the coracoids dorsally,
are bent laterally during downstroke and medially during upstroke by as much as 60% of
the intrafurcular resting distance. High speed film and electromyographic studies of free-
flying pigeons (Columba livia) reveal that the supracoracoideus muscle is strongly activated
during wing elevation and, as predicted from studies of Varanus and Didelphis, an additional
activation burst occurs at mid-downstroke in 48% of the recordings.
INTRODUCTION tigations, which relied principally on cine-
We recently began a series of studies that radiography and electromyography, the
center around an analysis of the musculo- movements of the shoulder of the Savan-
skeletal and neuromuscular components of nah Monitor lizard {Varanus exanthemati-
the shoulder in birds. Why undertake such cus) and the Virginia opossum {Didelphis
an analysis? The objective of this essay is virginiana) were analyzed together with the
not only to answer this question, but in activity patterns of the shoulder muscles.
doing so, to recount the observations, These species were selected because each
background search and thought processes possesses postural features thought to be
that led us to this project. In addition, we representative of a generalized reptile and
present some preliminary findings from our mammal. The conceptual basis for the two
studies of free-flying pigeons {Columba livia) studies was straightforward: to explore
and starlings {Sturnus vulgaris) flying in a the musculoskeletal and neuromuscular
wind tunnel. changes that accompanied the transition
The idea of studying the bird wing was from reptiles to mammals.
a logical extension of observations made in Why was the shoulder emphasized and
two earlier studies of a quadrupedal reptile not the rest of the forelimb? During the
and mammal (Jenkins and Weijs, 1979; evolution from reptiles to mammals, the
Jenkins and Goslow, 1983). In those inves- skeletal changes in the shoulder were most
extensive and appear to form the basis of
the postural and locomotor differences that
1 From the Symposium on Vertebrate Functional Mor-exist in these groups. This fact was rec-
phology: A Tribute to Milton Hildebrand presented at theognized by two early morphologists, A. B.
Annual Meeting of the American Society of Zoolo- Howell and A. S. Romer. Each made a series
gists, 27-30 December 1986, at Nashville, Tennessee.
2 Present address: Division of Biological Sciences, of carefully prepared comparative anatom-
University of Montana, Missoula, MT 59812. ical studies of the tetrapod shoulder which
287
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288 G. E. GOSLOW, JR. ET AL.
FIG. 1. Stages in the evolutionary development of the shoulder girdle in birds and mammals. At the left is
a lateral view of the shoulder girdle elements of a primitive reptile (Gephyrostegus) to illustrate the ancestral
form (after Carroll, 1970). Compsognathus, a coelurosaurian theropod reptile from the Late Jurassic period,
is representative of an intermediate stage (after Ostrom, 1978) in the evolution of birds (above). Although
the clavicle is as yet unknown in Compsognathus, it is present in related forms. Thrinaxodon, a mammal-like
reptile from the Triassic (after Jenkins, 1971), is representative of an intermediate stage in the evolution of
mammals (below). Didelphis modified from Jenkins and Weijs (1979). ac—anterior coracoid; cl—clavicle; ic—
interclavicle; pc posterior coracoid; sc—scapula.
formed an important background for our shallow, ventrally facing glenoid for artic-
studies (Romer, 1922, 1944;Howell, 1936, ulation with the humeral head.
1937rt, b). Major skeletal changes occurred
in the shoulder during the transition from
reptilian ancestors to modern birds and to INITIAL REASONS FOR A STUDY OF
therian mammals (Fig. 1). The evolution BIRD FLIGHT
of modern birds resulted in loss of the pos- Conserved motor patterns
terior coracoid, elongation of the anterior Similar motor patterns for diverse species,
coracoid, fusion of the interclavicle and Varanus and Didelphis. In previous studies
clavicles to form the furcula, and elonga- of Varanus and Didelphis, attention was
tion of the scapula together with its align- focused on the dynamics of the musculo-
ment parallel to the thoracic vertebrae. The skeletal system. In each study, the move-
transition to therian mammals involved loss ments of the forelimb (i.e., changes in joint
of the anterior coracoid, reduction of the angles, excursions of the bones) during
posterior coracoid into a beak-like process, walking on a treadmill were recorded by
loss of the interclavicle, appearance of a cineradiography. Simultaneously, electro-
supraspinous fossa, establishment of a myograms (EMGs) of the muscles sur-
mobile clavicle, and the development of a rounding the shoulder were recorded.
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AVIAN SHOULDER FUNCTION 289
lottssimus dorsi
(posterior)
deltoid (spinal)
deitoideus scopuioris pectorolis(posienor;
deltoid (acromial)
deltotdeus clovtculoris
pectoralis (superficial)
pectorohs
supraspinatus
infraspmatus
Varanus Didelphis
Fie. 2. Selected shoulder muscles of the Savannah monitor lizard (Varanus exanthematkus) and Virginia
opossum (Didelphis virginiana). Some of the presumed homologous muscles acting on the shoulder of the two
species are similar in anatomical configuration (deltoids, latissimus dorsi, pectoralis), whereas others are
distinctly different (supracoracoideus versus supraspinatus-infraspinatus complex). Above—lateral views of
the superficial shoulder muscles of V. exanthematkus and D. virginiana, respectively. The deltoids arise from
the clavicle and scapula, span the glenoid, and insert on the deltopectoral crest of the proximal humerus.
The latissimus dorsi arises from the spinous processes of posterior thoracic and anterior lumbar vertebrae,
and converges to a strong tendon which inserts on the proximal humerus. Three heads of the pectoralis are
recognized in both species, but the bulk of the muscle arises from the sternal elements of the midline and
inserts on the deltopectoral crest of the proximal humerus. Below—lateral view of the supracoracoideus (V.
exanthematkus), and supraspinatus and infraspinatus (D. virginiana), respectively. The supracoracoideus lies
ventral to the glenoid and arises broadly from the coracoid. It inserts by a short, broad tendon into the
proximal margin of the deltopectoral crest of the humerus. The supraspinatus lies dorsal to the glenoid, arises
from the supraspinous fossa of the scapula and inserts on the anterior surface of the greater tuberosity of
the proximal humerus; the infraspinatus also lies dorsal to the glenoid and arises primarily from the infraspinous
fossa and inserts on the lateral surface of the greater tuberosity of the proximal humerus. (Modified from
Jenkins and Weijs, 1979; Jenkins and Goslow, 1983.)
While analyzing the data from Varanus, we with the substrate, and a swing phase, dur-
were somewhat surprised when these ing which the foot is free of the substrate.)
results were comparable to those from the That is, for homologous sets of muscles,
Didelphis study. We noted that many the onset, relative duration and cessation
homologous muscles of the shoulder of EMG activity were equivalently timed
showed similar timing patterns of electrical within the stride cycle.
activity within a stride. (A stride may be Consider, for example, the anatomy (Fig.
defined as a single, complete cycle of limb 2) and EMG profile (Fig. 3) of several mus-
movement and is comprised of a propulsive cles of Varanus and their presumed homo-
phase, during which the foot is in contact logues in Didelphis (Jenkins and Goslow,
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290 G. E. GOSLOW, JR. ET AL.
Reptile Mammal
(Varanus exanthemoticus) (Didelphis virginiona)
I Propulsion i Swing I I Propulsion » Swing
Deltoids
Latissimus
Pectoralis
Supracoracoideus
(Infraspinatus)
(Suprospinotus)
FIG. 3. Electromyographic activity of homologous muscles. EMG profiles for selected shoulder muscles during
walking are shown for muscles presumed to be homologous in V. exanthematicus and D. virginiana. Bars represent
the most consistent activity; wavy line intermittent activity. Downward arrow depicts footstrike and onset of
the propulsive phase; upward arrow is coincident with foot liftoff which begins the swing phase. Mammalian
homologues of the Varanus supracoracoideus are the infraspinatus and supraspinatus. Note the similarity in
the timing patterns of these four muscles. (Data from Jenkins and Weijs, 1979; Jenkins and Goslow, 1983.)
1983). Some of these homologous sets (e.g., These observations led us to speculate,
deltoids, latissimus dorsi, pectoralis) clearly first, that the transition from a primitive
share similar anatomical attachments in the musculoskeletal design of the tetrapod
two species, and their similar activity pat- shoulder to a more specialized state may
terns with respect to the phases of a stride have occurred with little change in the basic
might be expected. Other muscles (e.g., motor pattern that controls the shoulder.
supracoracoideus) in Varanus and their Lauder and Shaffer (1988) discuss this issue
putative homologues in Didelphis do not as it relates to the ontogeny of feeding sys-
share similar musculoskeletal configura- tems in salamanders. Secondly, it seemed
tions; thus, their similar motor patterns conceivable that the organization of the
were not expected. The supracoracoideus neural control components of the shoulder
of Varanus, for example, takes its origin at the reptilian level of organization might
entirely from the coracoid and inserts on provide evolutionary opportunities on the
the proximal margin of the deltopectoral one hand but constraints on the other.
crest of the humerus (Fig. 2). In contrast, Quite naturally, we were intrigued by the
the infraspinatus and supraspinatus of prospect of describing an evolutionary
Didelphis arise entirely from the scapula phenomenon that not only explained what
(infraspinous and supraspinous fossae, we observed, but also might lend itself to
respectively). The infraspinatus inserts on further testing.
the lateral surface of the greater tuberosity It is probably clear by now why we
of the humerus, whereas the supraspinatus decided to examine birds in flight. Of the
inserts on the anterior surface of the tu- major groups of higher tetrapods, birds
berosity. Although the activity pattern of possess the most highly specialized shoul-
these muscles is biphasic, it appears that der region. If the motor output system for
these muscles are of greatest importance the muscles controlling the shoulder move-
for stabilization of the glenohumeral joint ments of tetrapods is evolutionarily con-
during the propulsive phase. It should be servative, a functional analysis of the shoul-
emphasized that in both species, the EMG der of birds in flight might provide insight
burst coincident with the propulsive phase into its constraints and plasticity.
is more intense (i.e., product of spike ampli-
tude x frequency) than the burst that Related studies that support the hypothesis of
occurs in the swing phase. motor control conservatism. A first step wasto compare the Varanus and Didelphis activ-
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AVIAN SHOULDER FUNCTION 291
Supracorocotdtufl
Dorsal Cord
/
Loii»itnua
Savannah monitor lizard Palm-Nut Vulture Domestic cat
(Voronus exonthemoticus) (Gypohierax anaolensis) (Fehs domesticus)
SEGMENT
rostral caudal
13 14 15 16
Biceps
Flexor digitorum superficial -
Latissimus dorsi posterior —
Triceps
Extensor metacarpi ulnaris -
Pectoralis
FIG. 4. Neural basis for muscle homology. A. Diagrammatic representation of the brachial plexus (ventral
view) of a reptile (Varanus exanthematicus), bird {Gypohierax angolensis) and mammal (Felis domesticus), taken
from a classic comparative study by Harris (1939) to illustrate nerve branching patterns. Although plasticity
of peripheral nerve innervation occurs within each class, study of nerve distributions is a useful indicator of
muscle homologies across taxa. For example, note the relatively consistent emergence of the nerves to the
triceps and latissimus dorsi from the dorsal cord, and the nerves to the supracoracoideus (supraspinatus and
infraspinatus), biceps and pectoralis from the ventral cord. B. Diagrammatic transverse section of the spinal
cord at the level of segment 15 (left) of the chick (Gallus sp.) to illustrate motoneuron pool location in the
lateral motor column. Rostral-caudal distribution of each motor pool transcends more than one segment
(right). Motor pools of each muscle were located by retrograde filling of the respective nerves with an
anatomical tracer, horseradish peroxidase. Note the medio-lateral segregation (broken line) of motoneurons
innervating muscles derived from ventral and dorsal embryonic muscle masses. The spatial location of motor
pools within the spinal cord across taxa is also useful for the establishment of muscle homologies. (Modified
after Straznicky and Tay, 1983.)
ity patterns to similar data available in work of conserved motor patterns. It
the literature for quadrupedal amphibians seemed reasonable that if the development
and the more specialized mammals. Numer- and organization of these systems were
ous similarities were seen in data from similar from one group to the next, the
two amphibian species, Triturus cristatus presence of a conserved motor pattern in
(Szekely et al., 1969) and Ambystoma macu- diverse phylogenies would not be unex-
latum (Edwards, 1981), and the domestic pected.
cat (English, 1978) and dog (Tokuriki, Determining muscle homologies is to
1973; Goslow et al., 1981). Thus the avail- some degree a speculative enterprise, but
able data, although limited, supported our the cautious use of peripheral nerve inner-
hypothesis. vation patterns can provide a starting point
At this point, it was necessary to evaluate for establishing homologies (Fig. 4A). The
the available literature concerning the number of nerves associated with the limb
organization and development of the neu- of any tetrapod is high, however, and the
romuscular and musculoskeletal systems of patterns of innervation vary to some degree
the tetrapod shoulder within the frame- across species. Additional data that relate
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292 G. E. GOSLOW, JR. ET AL.
to development and spinal cord organiza- (1902), Howell (1937a), Hudson and Lan-
tion are therefore important. All tetrapod zillotti (1955) and George and Berger
limbs arise from dorsal and ventral pre- (1966). In addition, general biomechanical
muscle masses of the limb bud which sub- principles that relate to wing movement
sequently subdivide and separate into indi- have been discussed by Bock (1969). Sev-
vidual limb muscles (see Chen, 1935; eral workers have provided interpretive
Romer, 1944; Cheng, 1955; Sullivan, 1962; analyses of various aspects of flight, includ-
Shellswell and Wolpert, 1977). Each mus- ing Sy (1936), Fisher (1957), Savile (1957),
cle of the shoulder receives innervation Hartman (1961), Greenewalt (1962, 1975),
from specific levels of the spinal cord. All Brown (1963), Pennycuick (1968, 1975),
of the motoneurons that innervate the limb and Simpson (1983). From such studies has
muscles are located within the lateral motor been derived the generally accepted inter-
columns (Lamina IX) of the spinal cord pretation of wing muscles in terms of their
(Fig. 4B). The population of motor neu- actions (summarized by Raikow, 1985).
rons that innervate a given muscle com- Features of wing movement have also been
prises the motor pool for that muscle. elegantly demonstrated through the use of
Motor pool maps have been obtained for high speed photography {e.g., Riippell,
selected tetrapod species using both ana- 1977; Nachtigall, 1980).
tomical tracing (retrograde transport of In the paleontological literature the
horseradish peroxidase) and electrophys- ancestry of birds and the origin of flight
iological methods. In the tetrapods that are two persistently recurring themes (for
have been examined, the majority of moto- review see Hecht e/ al., 1985;Padian, 1986).
neurons belonging to a given motor pool The phylogenetic origin of birds is pres-
tend to be situated close to one another, ently unresolved. Ostrom (1975, 1976a)
although in amphibians (Szekely and Czeh, summarized the evidence that the closest
1967; Cruce, 1974; Lamb, 1976) neurons relatives of birds are to be found among
belonging to different motor pools tend to the coelurosaurian dinosaurs. Walker
be intermingled more than in birds (1972) has argued for a thecodont ances-
(Landmesser and Morris, 1975; Hollyday, tory, and other workers (Whetstone and
l980a,b) and mammals (Romanes, 1951, Martin, 1979; Martin et al, 1980) have
1964; Weeks and English, 1987). Although adduced evidence of a close (sister group)
numerous details of development of the relationship between birds and crocodiles.
tetrapod forelimb remain to be deter- The question has been extensively debated
mined, we concluded that the general sim- (Tarsitano and Hecht, 1980; McGowan and
ilarities from one group to the next noted Baker, 1981; Martin, 1983; Steadman,
here are consistent with the conserved 1983), but the preponderance of evidence
motor pattern hypothesis. favors a relationship to coelurosaurs (Gau-
thier, 1986). A second problem concerns
Evolution of flight the origin of flight itself. Numerous sce-
Our decision to pursue an analysis of the narios have been proposed over the last
avian shoulder during flight was also hundred years, and each of these theories
directed toward answering a longstanding reconstructs a somewhat different loco-
and major morphological problem in ver- motor and behavioral intermediate stage.
tebrate evolution: the interpretation of the There are two major hypotheses: "arbo-
musculoskeletal features that developed real" and "cursorial" (reviewed by Ostrom,
during the transition from terrestrial loco- 1974, 1979, 1986; Martin, 1983; Hecht et
motion to flight. al, 1985; Bock, 1986). Regardless of whichparticular behavioral-ecological pathway is
Anatomical correlates of bird flight: A long
history. The musculoskeletal structures correct, a central issue in the origin of flightcontroversy is the difficulty of postulating
related to avian flight have been exten- a set of transitional stages of the shoulder
sively studied; detailed treatments of the and forelimb that are adaptive at each evo-
skeleton are available (Bellairs and Jenkin, lutionary level.
1960). Particularly useful descriptions of
musculature are given by Fiirbringer Archaeopteryx, represented by six skele-
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AVIAN SHOULDER FUNCTION 293
tal specimens from the Late Jurassic rocks erally, thereby permitting unrestricted
of Germany, documents one stage in the transverse (up and down) movements of
reptilian-avian transition. Some aspects of the forelimb; 2) development of an
its anatomy provide insight into the prob- enlarged buttress at the level of the glenoid
able evolutionary pathways to flight, but to brace the furcula, thereby ensuring
others are controversial. For example, proper transverse separation of the shoul-
Archaeopteryx did not possess an ossified keel der sockets, and 3) raising the levels of
on its sternum. On the basis of the struc- humeral extension and forearm flexion by
ture of the sternum and shoulder girdle, elevating the sites of origin of the cora-
Ostrom (1974, 1979) concluded that pow- cobrachialis and biceps. Figure 5B is taken
ered flight was not possible at this evolu- from Ostrom (19766) to illustrate these
tionary stage; others, however, hold a dif- proposed changes in coracoid morphology
ferent opinion (cf. Olson and Feduccia, from Archaeopteryx to a modern bird like
1979; Feduccia, 1980; Martin, 1983; Pen- the turkey vulture (Cathartes).
nycuick, 1986). Although it is unlikely that Implicit in Ostrom's argument, as well
the intermediate stages that led to avian as that of others, is the assumption that the
flight may be found in the fossil record, flight muscles of birds have undergone
speculation about the accompanying struc- some fundamental alterations from the
tural changes helps us to formulate ques- primitive tetrapod pattern in phasic activ-
tions that can be addressed in extant rep- ity or function with respect to limb move-
tilian and avian systems. ment. In our estimation, our ability to eval-
In modern birds, the supracoracoideus uate the various reconstructions of the
retains its primitive position deep to the evolutionary stages in the origin of the
pectoralis but its tendon of insertion avian flight apparatus, and the debate over
attaches to the dorsal aspect of the humerus whether Archaeopteryx could fly, is limited
(Fig. 5A) rather than to its anterior aspect by our lack of an understanding of the
as in reptiles. After arising from parts of functional anatomy of the avian shoulder
the sternum, coracoid and coracoclavicu- in flight. For this reason we initiated stud-
lar membrane, its fibers converge dorsally ies on the function of the shoulder of
on a tendon that passes upward through pigeons {Columba livia) in free flight and
the foramen triosseum (formed by the cor- European starlings (Sturnus vulgaris) flying
acoid laterally, furcula anteriorly and scap- in a wind tunnel.
ula posteriorly). Various explanations of
how this arrangement may have evolved FUNCTIONAL ANALYSIS OF THE
could be given, but here we present BIRD SHOULDER
Ostrom's (19766) thoughtful outline which As so often happens, many of our pre-
is based on the premise that Archaeopteryx liminary observations were unexpected and
was not capable of powered flight. He pro- opened numerous possibilities for future
posed that subsequent to the Archaeopteryx research. Some of our early results are con-
stage of evolution, the shape of the cora- sidered relevant to an assessment of 1) the
coid underwent extensive change. This hypothesis that the motor pattern of shoul-
change was accompanied by alteration of der muscles has remained relatively con-
the position and function of the principal servative throughout tetrapod evolution,
humeral extensor (coracobrachialis crani-
alis) and forearm flexor (biceps brachii) and 2) an interpretation of the musculo-
which, in turn, converted the function of skeletal features that accompanied the
the supracoracoideus from a humeral transition from terrestrial locomotion to
depressor to an elevator. Ostrom further flight.
proposed that the upward expansion of the Supracoracoideus and pectoralis
avian coracoid (to form the acrocoracoid), activity patterns
an event basic to his hypothesis, may have
occurred as a result of 1) elevation of the Our initial EMG studies focused upon
anterior part of the glenoid and rotation the supracoracoideus, the primary elevator
of the shoulder socket to face directly lat- of the humerus during wing upstroke, and
the pectoralis, the major humeral depres-
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294 G. E. GOSLOW, JR. ET AL.
left corocoid
A ocrocoracoid
supracoracoideus
tendon
right humerus
supracoracoideus
acrocoracoid
tendon alignment
muscle
belly
alignment
Cathartes Archaeopteryx
FIG. 5. Hypothetical transitional stages in supracoracoideus orientation from a primitive bird {Archaeopteryx)
to a modern bird (Cathartes). A. Orientation of the supracoracoideus in a modern bird; note the elongate
coracoid, the acrocoracoid process, and the pulley-like arrangement of the supracoracoideus tendon as it
passes through the foramen triosseum to insert on the dorsal aspect of the humerus. The pectoralis has been
removed. B. Arrow depicts the proposed orientation of the belly of the supracoracoideus and the line of pull
of its tendon on the humerus of Archaeopteryx (right), hypothetical intermediates, and a modern bird, Cathartes
(left). Note that the elongation of the coracoid and development of the acrocoracoid process facilitate the
conversion of the supracoracoideus from a humeral protractor to a humeral elevator. (Modified after Ostrom,
1976ft.)
sor. The muscle fascicles of the pectoralis 16 mm film (64-200 fps). Two electrode
originate on the anterolateral surface of configurations and implantations were
the clavicle, along the entire surface of the employed: 1) paired, Teflon-coated, 18-
sternal carina (keel), and from portions of stranded, stainless steel wires (0.28 mm
the sternal body. Its fascicles converge to diam.; 0.5 mm bared surface; intertip dis-
insert on the cranial surface of the delto- tances 0.5 mm), and 2) paired, silver elec-
pectoral crest of the humerus. A complete trodes (100 Mm diam.; 0.5 mm bared tips;
description of the anatomy of the supra- intertip distances < 0.5 mm). Electrodes
coracoideus and pectoralis in pigeons is were sutured to muscle fascia and directed
found in George and Berger (1966). subcutaneously to an exit point between
Methods. We recorded EMGs in the pec- the scapulae and connected to an
toralis and supracoracoideus from six adult Amphenol plug. EMGs were recorded by
pigeons during level, flapping flight. Flight both telemetry and direct wire connections
behavior was recorded synchronously on to the plug, amplified and stored on FM
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AVIAN SHOULDER FUNCTION 295
Pectoralis
Supracoracoideus }0.5mV
t 100 ms
Fie. 6. Patterns of muscle activity during flapping flight. Silhouettes illustrate positions of the wing during
a complete wingbeat cycle of the pigeon (Columba hvia). Arrows designate the initiation of downstroke
(downward arrow) and upstroke (upward arrow). The pectoralis begins activity in late upstroke and continues
into the downstroke. The supracoracoideus exhibits a biphasic pattern. The major burst associated with wing
elevation begins in late downstroke and continues into upstroke. A second, and more variable burst, occurs
during the middle of the downstroke.
tape at 15 ips. Subsequently, these signals brought downward and forward to provide
were played back at either 15/16 or 15 / power and lift, and a complicated upstroke
32 ips tape speed and bandpass filtered phase that apparently imparts little lift but
(effective band widths 120-2,000 Hz). The repositions the wing for the subsequent
birds were trained to fly approximately 18 downstroke. At the beginning of down-
m down a hallway to a landing perch. Post- stroke (Fig. 6, downward arrow), the prox-
operatively, each bird was given 10,000 imal leading edge of the wing has been
units/kg of penicillin daily. elevated to a nearly vertical position, the
Results. Typical activity patterns for a elbow and wrist joints are fully extended,
flapping pigeon in level flight (8 m/sec) are and the bird appears to be reaching high
presented with reference to the phases of above its back. During the downstroke, the
the flight cycle (Fig. 6). Detailed accounts humerus is depressed to bring the wing
of wing movements described from light into a horizontal position. During the sec-
films during takeoff (Simpson, 1983) and ond half of the downstroke, the wings con-
flapping flight (Brown, 1951, 1963) of the tinue to move downward and forward until
pigeon are available, but only the general they lie parallel and in front of the body.
features of wing movement are described The wrist and elbow remain extended.
here. The two basic phases of flapping flight Upstroke (Fig. 6, upward arrow) is char-
are the downstroke, when the wing is acterized by three subphases. The first third
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296 G. E. GOSLOW, JR. ET AL.
of the upstroke is marked by a reversal of The supracoracoideus in birds is a
the humeral movement that occurs in the humeral elevator, and appears to function
last part of the downstroke and flexion of differently from its homologue in living
the elbow and wrist. A backward flick comes reptiles and, presumably, in the early
next and is characterized by the rapid Mesozoic reptiles from which birds arose.
retraction and elevation of the humerus Certainly the putative supracoracoideus
while the elbow and wrist remain flexed. homologues in mammals, the supraspina-
The final phase of upstroke is character- tus and infraspinatus, function differently;
ized by maximum wing elevation and they serve to stabilize the glenohumeral
extension. joint during the propulsive phase (in con-
As intuitively expected, electrical activ- trast to birds, where the supracoracoideus
ity of the pectoralis is most pronounced lifts the humerus in the upstroke, which is
during the downstroke, while the supra- comparable to the swing or non-propulsive
coracoideus is most active in upstroke (Fig. phase). How could the supracoracoideus in
6). Note, however, that activity in the pec- an ancestral tetrapod have given rise to
toralis begins during late upstroke before such contrasting systems in birds and mam-
the wing reaches its highest position and mals? Can muscles change their function?
begins its downward movement. Similarly, Obviously this is possible through altera-
the largest burst of the supracoracoideus tion of the musculoskeletal system which
commences in late downstroke prior to wing is a framework of mechanical struts, levers
upstroke. In addition, the electrical activity and pulleys. However, another and often
in the supracoracoideus is often biphasic. overlooked aspect must change as well: the
A second, relatively small, burst begins in timing of a muscle's activity in the loco-
late upstroke and continues into the early motor cycle. In cases where a muscle's
part of downstroke. This second burst was activity is biphasic, there exists the possi-
clearly measurable in 48% of our record- bility that in the course of evolution of the
ings and is coincident with the largest EMG musculoskeletal system, one or the other
burst of the pectoralis. The double burst phase in a muscle's activity may assume a
pattern is variable; in some cases it appears critical function. Such appears to have been
and then disappears within a single flight the case for the supracoracoideus and its
sequence, whereas in others it is consis- homologues in higher tetrapods. Through
tently present or absent. No relation of the a process that we may call "neuromuscular
double burst to flight speed, body angle, canalization," the upstroke (=swing) com-
or wingbeat amplitude was evident. ponent of the biphasic activity cycle for the
supracoracoideus is most important in
Discussion. In the following discussion, we birds, whereas the propulsive ^down-
will be equating the "upstroke" and stroke) component of the homologous
"downstroke" phases of flight to the supraspinatus and infraspinatus muscles is
"swing" and "propulsive" phases respec- essential in mammals. Yet in both birds and
tively of terrestrial locomotion. The onset mammals the primitive organization of the
of the contraction of the pectoralis and neural control components still persists, for
supracoracoideus (as indicated by the EMG in both groups we find evidence of a
records) prior to the point where the mus- biphasic pattern.
cle shortens to move the humerus is not
unlike the pattern of contraction measured Although our conclusions on this issue
in the flexors and extensors of various ver- are only tentative (because the data are as
tebrate limbs during terrestrial locomo- yet so few), we may pose some additional
tion. The pattern has implications for our questions. Do the motoneurons which
understanding of muscle mechanics in reflect the biphasic activity pattern seen in
oscillating limb systems and also for the the EMG represent one population or two?
energetics of cyclic motion. In the case of If two, is one population only active during
pigeon flight, this issue has been discussed the swing phase, and the other only during
by Dial ^ a/. (1987). propulsion? This might be the case, as evi-
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AVIAN SHOULDER FUNCTION 297
dence is now available that the sartorius
muscle of the domestic cat hindlimb is
controlled by three populations of moto-
neurons, each programmed for a specific
locomotor task (Hoffer et al, 1987). Alter- D
natively, does each supracoracoideus
motoneuron undergo two periods of exci-
tation during each locomotor cycle? Dur-
ing the evolution from ancestral to derived
forms, does the amplification of one of the
two bursts {i.e., in swing phase) and the
diminution of the other (i.e., propulsive
phase) reflect a change in the number or
kinds of motoneurons in the pool, or a
change in synaptic connectivity? Why did
we only observe a distinct biphasic pattern
in the pigeon in 48% of the recordings? At
present we can only speculate about answers
to these questions; much work needs to be
done.
SKELETAL DYNAMICS DURING FLIGHT
In order to pursue some of the above
questions and to further our insight into
the general features of wing evolution
among birds, we constructed a wind tun-
nel. A wind tunnel undoubtedly induces
certain constraints on the performance of
a flying bird (Butler et al, 1977), but the
benefits of recording a series of successive
wingbeats are many. Critical to our anal-
yses is a clear understanding of wing move-
ments in relation to muscle activity. There-
fore we employed the wind tunnel in
conjunction with a cineradiographic sys-
tem which records X-ray images of a bird's
skeleton. The demands of the cineradio-
graphic apparatus are such that the size of
the flight chamber of the wind tunnel is
restricted to a relatively small volume.
Hence, because pigeons are slightly large FIG. 7. Movement of the furcula during flight. Dor-
for the wind tunnel, we have begun studies sal view of the furcula (stippled) of the starling (Stur-
on a relatively small bird, the European nus vulgaris) during a wingbeat cycle. From the begin-ning (A) to the end (C) of downstroke the dorsal ends
starling (Sturnus vulgaris), for which some of the furcula spread laterally. Simultaneously the
preliminary results are available. scapulae pivot medially (arrows). These movements
are reversed during upstroke (D).
Methods. Four starlings were trained to
fly in the variable speed wind tunnel. The
plexiglass flight box measured 61 cm square markers (ca. 0.5 mm wide, 2.5 mm long)
and 91.5 cm long. Birds flew from 9 to 20 were implanted in deeply anesthetized (25
m/sec. The visibility of bony landmarks on mg/kg ketamine; 2 mg/kg xylazine) birds
radiographic film was enhanced by the as follows: one in the deltopectoral crest of
insertion of tiny metallic markers. The the humerus, one each in the acrocoracoid
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298 G. E. GOSLOW, JR. ET AL.
; 20
60S
1
16 i
3
o
13
12
i 2 5 m s i
FIG. 8. Displacement of the furcula during flight of Sturnus vulgaris. Instantaneous distances between the
two dorsal ends of the furcula are shown for three wingbeats. Resting distance is shown as a dashed line.
Upward arrows indicate the beginning of wing upstroke, downward arrows the beginning of downstroke.
Two sets of vertical calibrations are provided. The left scale is in absolute millimeters. The right scale illustrates
the percentage of displacement relative to resting distance.
processes of each of the coracoids, and two tion of the humeral axis with respect to a
along the keel of the sternum. A marker horizontal plane through the shoulder
1 cm in length was glued between the scap- joint.
ulae for scale. Results. Our observations reveal that the
Siemens cineradiographic apparatus, dorsal ends of the "V" shaped furcula,
including a grid-controlled tube with 0.06 which contact the coracoids dorsally, shift
mm focal spot and a 27.94 cm Sirecon laterally during the downstroke (Fig. 7). In
image intensification system, was posi- the subsequent upstroke they move medi-
tioned for lateral or dorsoventral projec- ally, presumably by elastic recoil. At rest,
tion radiography. An Eclair GV16 high the distance between the dorsal ends of the
speed cine camera, mounted on the image furcula is typically about 11-12 mm. At a
intensifier and operated at approximately flight speed of 17 m/sec, intrafurcular dis-
200 fps, recorded each sequence on 16 mm tance is maximal (20 mm) at the end of
Kodak Plus-X Reversal film at the same downstroke (Fig. 8).
time that the image was monitored on a 43 Discussion. The furcula is such a unique
cm television screen. Approximately seven structure that biologists have speculated as
hundred feet of film was taken of each bird; to its function. For example, Ostrom
analysis with a Vanguard M-CIIP Film (19766) suggested that the furcula serves
Analyzer is in progress. The data pre- to maintain a set distance between the
sented here are selective. shoulders, whereas Norberg (1985) men-
As an aid to kinematic analysis, the birds tioned the furcula's potential role for
with marker implants were injected with energy storage. The furcula may, in fact,
T-61 (Euthanasia Solution) and their skel- serve both these functions but heretofore
etons mounted to duplicate structural rela- there simply has been no way to make direct
tions observed radiographically. This pro- observations of its movements. Our initial
cedure permitted verification of the kinematic analysis of some mechanical
following: 1) lateral and medial displace- properties of isolated furculae provide
ment of the acrocoracoids, as well as the indirect support for an additional hypoth-
dorsal ends of the furcula (wishbone), mea- esis which relates to respiration (Jenkins et
sured from the sagittal plane; 2) antero- al., 1988). Coupled with movements of the
posterior excursion of the humerus, mea- sternum that also occur with each wing-
sured at the intersection of the humeral beat, the furcula may play a role in cycling
axis (which bisects the humeral head and air between the air sacs and lungs during
a line between the epicondyles) and the flight. Such a pattern might serve the
sagittal plane; and 3) elevation or depres- increased demands of flight. Clearly, addi-
sion of the humerus, measured by the loca- tional observations and experimental
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AVIAN SHOULDER FUNCTION 299
manipulations are necessary in order to Butler, P. J., N. H. West, and D. R. Jones. 1977.
clarify the furcula's role not only in star- Respiratory and cardiovascular responses of the
lings, but in other species of birds with pigeon to sustained, level flight in a wind-tunnel.J. Exp. Biol. 71:7-26.
varying flight modes and furcular geome- Carroll, R. L. 1970. The ancestry of reptiles. Phil.
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Chen, H. K. 1935. Development of the pectoral limb
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motion. Numerous evolutionary pathways hindlimb motoneurons in the lumbar spinal cord
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and function of the forelimb of the reptil- Jenkins, Jr. 1987. The structure and neural con-
ian ancestor, protobird, or modern bird trol of the pectoralis in pigeons: Implications for
capable of flight. We are fortunate at last flight mechanics. Anat. Rec. 218:284-287.
to possess the kind of technology necessary Edwards, J. L. 1981. An electromyographic analysisof the forelimb muscles of the spotted salaman-
for precise documentation of tetrapod limb der, Ambystoma maculatum. Amer. Zool. 21:938.
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ACKNOWLEDGMENTS Gauthier, J. 1986. Saurischian monophyly and the
origin of birds. In K. Padian (ed.), The origin of
We thank L. L. Meszoly for illustrations, birds and the evolution of flight, pp. 1-55. California
A. H. Coleman for photography, and L. L. Academy of Sciences, San Francisco.
W. Maloney for secretarial assistance. We George, J. C. and A. J. Berger. 1966. Avian myology.
also extend our appreciation to S. R. Kap- Academic Press, New York.
lan for technical assistance and to K. Hep- Goslow, G. E.,Jr., H. J. Seeherman, C. R. Taylor, M.N. McCutchin, and N. C. Heglund. 1981. Elec-
worth for the use of his camera. This work trical activity and relative length changes of dog
was supported by N.S.F. Grant BSR85- limb muscles as a function of speed and gait. J.
11867 and by the Northern Arizona Uni- Exp. Biol. 94:15-42.
versity Organized Research Committee. Greenewak, C. H. 1962. Dimensional relationships
for flying animals. Smithsonian Misc. Coll. 144(2):
1-46.
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