Received: 29 December 2021 | Revised: 29 April 2022 | Accepted: 20 May 2022

DOI: 10.1002/jmor.21486

RESEARCH ARTICLE

Wing osteology, myology, and function of Rhea americana

(Aves, Rheidae)

Gastón E. Lo Coco1 | Matías J. Motta1 | Federico L. Agnolín1,2 |

1
Fernando E. Novas

1
Laboratorio de Anatomía Comparada y
Evolución de los Vertebrados, Museo
Argentino de Ciencias Naturales “Bernardino
Rivadavia”, Consejo Nacional de
Investigaciones Científicas y Técnicas –
CONICET, Buenos Aires, Argentina
2
Departamento de Ciencias Naturales y
Antropología, Fundación de Historia Natural
“Félix de Azara”, Universidad Maimónides,
Buenos Aires, Argentina
Correspondence
Gastón E. Lo Coco, Laboratorio de Anatomía
Comparada y Evolución de los Vertebrados,
Museo Argentino de Ciencias Naturales
“Bernardino Rivadavia”, Av Ángel Gallardo
470, C1405DJR Buenos Aires, Argentina.
Email: gastonlococo@gmail.com
Abstract
The Greater Rhea (Rhea americana, Rheidae) is a flightless paleognath with a wide
geographical distribution in South America. The morphology of its shoulder girdle
and wings are different from those of flying birds and some characteristics are similar
to basal birds and paravian theropods. We present a detailed osteological,
myological, and functional study of the shoulder and the wing of the Greater Rhea.
Particular features of the anatomy of the pectoral girdle and wing of Rhea include
the lack of triosseal canal, reduced origin area of the mm. pectoralis p. thoracica and
supracoracoideus and the lack of a propatagium. The wing muscle mass is markedly
reduced, reaching only 0.89% of total body mass (BM). Forelimb muscles mass
values are low compared to those of flying birds and are congruent with the non‐use
of wings for active locomotion movements. R. americana does not flap the wings
dorso‐ventral as typical for flying birds, but predominantly in cranio‐caudal direction,
following a craniolateral to caudomedial abduction–adduction arc. When the wings
are fully abducted, they are inverted L‐shaped, with the inner surface caudally faced,
and when the wings are folded against the body, they do not perform the complete
automatic wing folding nor the circumduction of the manus, a movement performed
by extant volant birds. This study complements our knowledge of the axial
musculature of the flightless paleognaths and highlights the use of the Greater Rhea
as a model, which may help understand the evolution of Palaeognathae, as well as
the origin of flapping flight among paravian theropods.

KEYWORDS
automatic wing folding, circumduction, flightless, Palaeognathae, wing movements

1 | INTRODUCTION
Living Palaeognathae includes 13 species of terrestrial flightless birds, the
paraphyletic ratites (Yonezawa et al., 2017), and 46 species of flying birds
(Tinamiformes), which are currently dispersed across continents of the
southern hemisphere (Gill & Donsker, 2020). Within the Palaeognathae,
the order Rheiformes includes two species, the ñandú or Greater Rhea
(Rhea americana) and the choique or Lesser Rhea (Rhea pennata),
distributed in South America (Gill & Donsker, 2020). The Greater Rhea is
the largest terrestrial bird on the continent; it has a wide distribution
range, inhabiting open areas in Argentina, Uruguay, Bolivia, Paraguay,
and Brazil (Gasparri, 2016; Gill & Donsker, 2020).
R. americana, like other non‐tinamid paleognaths, has cursorial
adaptations (except Apteryx; Fürbringer, 1888, 1902; Gadow, 1885;
Gasparri, 2016; Lowe, 1928; Muñíz, 1885; Pycraft, 1900), including a
large body size (except Apteryx), forelimb reduction (including bones
and musculature), lack of furcula, sternum without keel, pectoral
girdle lacking triosseal canal, and feather simplification (Lowe, 1928).

J. Morphol. 2022;1–33. wileyonlinelibrary.com/journal/jmor © 2022 Wiley Periodicals LLC. | 1

2 |
The first works describing the osteology and myology of
paleognaths were those from the end of the 19th century and first
decades of the 1900s, including anatomical descriptions of
different species (e.g., Cunningham, 1871; Fürbringer, 1888, 1902;
Gadow, 1885; Haughton, 1864; Lowe, 1928; Pycraft, 1900). These
studies mainly addressed the particular morphology of the
shoulder girdle and sternum, the lack of furcula, and the
“atrophied” musculature linked to the impossibility of flapping
flight, among other characteristics.
Since then, few works have been published regarding different
osteological and myological aspects of the “ratite” wing (Jasinoski
et al., 2006; Maxwell & Larsson, 2007; McGowan, 1982; Wustinger
et al., 2006). In the last decades, studies on Greater Rhea have
focused on the hind limbs (Picasso, 2010, 2015; Picasso et al., 2012)
and pelvic girdle (Picasso et al., 2020), with respect to its importance
in locomotion.
Although R. americana is a flightless bird, it has the most
extensive wing among “ratites,” being similar in some aspects to
Struthio, tinamids, and neognath birds, and unlike Casuariiformes and
Apteryx that exhibit a reduced forelimb (Cho et al., 1984). Remark-
ably, the wings of Rhea move predominantly cranio‐caudally,
following a craniolateral to caudomedial abduction–adduction arc,
instead of dorsoventrally movement as in flying birds (Novas
et al., 2020).
Thus, when the Greater Rhea laterally extends the wing, the
forearm hangs more or less perpendicularly to the ground, with the
wrist pointing to the ground and the inner wing surface pointing
caudally (Figure 1a; Novas et al., 2020; Raikow, 1968). This is in sharp
contrast to flying birds, in which the inner wing surface points
ventrally during flapping flight or gliding (Dial et al., 1991; Novas
et al., 2020; Raikow, 1968). Wing function of R. americana is limited
to thermoregulation, and to exposure when threatened, during
courtship behavior and when they run in zigzags, spreading their
wings alternately for balance (Cho et al., 1984; Gasparri, 2016;
Muñíz, 1885; Novas et al., 2020).
It is important to note that except for general mentions about
Greater Rhea's wing movement (see Cho et al., 1984; Fürbringer,
1888, 1902; Gadow, 1885; Gasparri, 2016; Haughton, 1864;
Lowe, 1928; Muñíz, 1885; Novas et al., 2020, 2021; Pycraft, 1900),
F I G U R E 1 (a) Wing posture of Rhea americana albescens with the
humerus totally abducted. Photograph taken by Ramón Moller
Jensen. (b) R. americana albescens, right pectoral girdle and wing in
lateral view. Scale bar: 10 cm. cm, carpometacarpus; fe, femur;
h, humerus; r, radius; sco, scapulocoracoid; st, sternum; u, ulna.
LO COCO ET AL.
and specific research on the movements of the elbow, wrist and
digits in Struthio (Hutson & Hutson, 2012, 2014, 2018), no
previous studies addressed in detail the movements observed
between the pectoral girdle and wing elements in flightless
paleognaths.
The aim of this study is to present an exhaustive description of
wing and pectoral girdle osteology, myology, and wing movements,
essentially focusing on the musculature linked to wing movements.
Such information may become useful for comparative osteological,
myological, and for morpho‐functional studies among extant birds,
and may also serve in the analysis of postural activities of the
forelimbs in basal paravians (Agnolín et al., 2019; Novas
et al., 2020, 2021).
2 | M A T E R I A L S AN D M E T H O D S
2.1 | Specimens
Five skeletons and two fresh specimens of R. americana (Linnaeus,
1758) from Buenos Aires province, Argentina, were studied (see
Supporting Information: SI 1). The specimens were collected dead
and were incorporated into the Colección de Ornitología of Museo
Argentino de Ciencias Naturales “Bernardino Rivadavia” (MACN‐
Or), Buenos Aires, Argentina. The specimens were manipulated
when they were fresh and then, were frozen until dissection
without the addition of any kind of preservative liquid (e.g.,
formaldehyde; see below).
2.2 | Data collection
For the osteological description, we used five skeletons of R. americana
(Supporting Information: SI 1). For comparisons, different taxa of
paleognaths (Struthio; Casuarius; Dromaius; Apteryx; Nothoprocta;
and Eudromia), neognaths (Gallus; Numida; Chauna; Geranoaetus;
Buteogallus; Vultur; Tyto; and Bubo), non‐Avialae Paraves (Buitreraptor;
Deinonychus; and Bambiraptor), and non‐Ornithothoraces Avialae
(Sapeornis; Archaeopteryx) were used (Supporting Information: SI 1
and SI 2). A protractor was used to measure the scapular girdle
principal angles and the torsion angle of the wing elements.
Other paleognath and neognath specimens were also dissected
for myological comparisons (see Supporting Information: SI 1).
The fresh specimens were stored frozen for less than 6 months
and only those muscles and body parts that were in good condition
were considered for the description and weighing. Before dissection,
each specimen was defrosted in the fridge (4–5°C). We dissected the
muscles from both body sides. Each muscle was carefully removed
and weighed (both the fleshy and tendinous components) with a
digital scale with 0.01 g accuracy. Among birds, data on muscle mass
are useful to interpret the main role that muscles perform on wing
movements (Lo Coco et al., 2020; Picasso & Mosto, 2018), consider-
ing that the muscle mass is proportional to maximum muscle power
LO COCO ET AL.
output (Biewener & Roberts, 2000). The percentage of individual
muscle masses with respect to the total mass of wing muscles and
total BM was calculated. Entire BM was obtained from the specimens
dissected. Following a classical anatomical approach of describing
wing musculature, we documented the origin and insertion sites of
each muscle as well as their general features and appearances. The
descriptions followed the order of appearance from proximal to distal
and superficial to deep muscles. We manipulated the muscles
individually, with the aim to observe and infer the type of movement
they produce on the bony elements. Based on their topography,
origin and insertion sites, and fiber direction, we determined the
individual muscle function, following the contributions of Raikow
(1985) and Jasinoski et al. (2006).
For the description of the scapular girdle and forelimb elements
and muscles, we used the natural positional orientation of the wing of
R. americana, based on the humerus position in maximum abduction.
Knowing that the functional orientation of the pectoral girdle and
elements of the R. americana wings are different from those of
tinamids and neognath birds, we prefer to employ the classical
orientation of flying birds to facilitate the reading and understanding
of the present paper.
2.3 | Wing movements
First, direct observations on the wing movement of living paleog-
naths (e.g., R. americana and Struthio camelus) were carried out at the
Fundación Temaikèn. The observation was carried out outside the
enclosure where the specimens live and they were made under
uncontrolled conditions without human intervention. Attention was
paid to the recording of wing movements while the individuals were
performing daily actions such as walking, feeding, and during
intraspecific interactions. The aim of these observations was to
confirm the typical wing movement performed by both paleognath
birds (Rhea and Struthio), previously indicated by Muñíz (1885), Cho
et al. (1984), Gasparri (2016), and Novas et al. (2020).
The fresh specimens of R. americana used in the myological
dissections (see Supporting Information: SI 1) were manipulated with
the aim to contrast them with the observations of live specimens.
This resulted in final description of wing movements, as well as the
particular movements of each wing element.
To determine the range of motion of the arm, each complete
specimen was fixed to a metal structure to keep the vertebral column
in a parallel position to the ground and with the hindlimbs folded,
resting on a flat surface. As a result, the wing was free to perform any
movement. Three digital cameras (Nikon D5200, Canon EOS Rebel
T1i, and GoPro Hero3 silver edition) were used to film the
movements in cranial, dorsal, and lateral views. To manipulate the
cadaveric specimens, all wing feathers were removed to see each
element well and the distal end of the humerus was held with a
thread to be able to move it and not interfere with the recordings.
Thus, the humerus was manipulated in such a way as to describe a
wide range of movements, reaching the maximum ranges. Finally, the
| 3
elbow excursion during the movements of the typical abduction/
adduction arc performed by R. americana was recorded.
To quantify the maximum range of movements of the humerus,
the videos were processed in all views using the freely available
software Tracker (version 5.1.5). In each video an “x, y, z” coordinate
axis was determined, where the intersection point (e.g., x = 0; y = 0;
z = 0) was positioned in the glenoid fossa of the left pectoral girdle. In
cranial and dorsal views, the latero‐medial axis was kept as the “x”
axis. In cranial and lateral views, the dorso‐ventral axis was
designated as the “y” axis, while in lateral and dorsal views the
cranio‐caudal axis was indicated as the “z” axis.
The skin of the elbow was marked to be traced by the Tracker
program and its “x, y, z” position was recorded throughout its
displacement. The position was recorded at 0.067 s. For each view,
the maximum points reached by the elbow throughout its movement
were plotted. In addition, the elbow excursion in the typical
abduction–adduction arc (n = 4) was plotted in cranial, lateral, and
dorsal views. The recordings of the elbow position were made at
0.067 s.
To determine the range of maximal forearm movements, the arm
was fixed in a position of lateral extension. Photographs were taken
perpendicular to the inner surface of the arm when the forearm was
fully flexed and fully extended. The photographs were taken with
Canon EOS Rebel T1i. Adobe Photoshop was used to superimpose
the photograph of the forearm in maximum flexion and extension,
thus being able to measure the angle formed between the long axis of
the arm with the long axis of the forearm.
To determine the range of maximal manus movements, the arm
was fixed in lateral extension. Photographs were taken perpendicular
to the inner surface of the wing in two positions. The maximum
flexion and extension of the manus was recorded when the forearm
was fully flexed and when it was fully extended. Adobe Photoshop
was used to superimpose the photograph of the manus in maximum
flexion and extension in the two forearm positions previously
indicated. Thus, it was possible to measure the angles formed
between the long axis of the forearm and the long axis of the manus.
Following the nomenclature proposed by Gill and Donsker
(2020), we refer to the Greater Rhea as R. americana albescens
(Lynch & Holmberg, 1878). The anatomical nomenclature follows
Baumel et al. (1993), and the abbreviations used in text are: lig.
(ligament), m. (muscle), mm. (muscles), and p. (pars).
Photographs of the bones and muscles were taken using a Nikon
D5200 digital camera and the figures were processed using Adobe
Photoshop.
3 | RESULTS
3.1 | Osteology of pectoral girdle and wing
The pectoral girdle of the Greater Rhea (R. americana) is formed by
the fusion of scapula and coracoid, forming a scapulocoracoid
(Lowe, 1928), and a sternum without a keel (Figures 2, 3, and 5).
4 | LO COCO ET AL.

F I G U R E 2 Rhea americana albescens, scapular girdle in cranial (a), dorsal (b), and right lateral (c) views. Scale bar: 3 cm. ci, costae incompletae;
co, corpus coracoidei; cst, costa sternalis; cv, costa vertebralis; pu, processus uncinatus; s, scapular blade; st, sternum; syn, synsacrum; t1, first
thoracic vertebra; t2, second thoracic vertebra; t3, third thoracic vertebra.

F I G U R E 3 Rhea americana albescens, right scapulocoracoid of juvenile (a) and adult (b–e) in cranial (a, b), lateral (c), and caudal (e) views.
Detail of the glenoid fossa in lateral (d) view. Scale bar: 3 cm. aco, acrocoracoid process; acr, acromion process; co, corpus coracoidei;
col, coracoidal glenoid lip; com, coracoid membrane; fnsc, foramen nervi supracoracoidei; fon, fossae pneumaticae; gl, glenoid fossa; li, linea
intermedialis; pco, procoracoid process; s, scapular blade; scc, supracoracoidal canal; scs, scapulocoracoid suture; sgf, subglenoid fossa;
sl, scapular glenoid lip.

A distinctive feature is that the pectoral girdle lacks a clavicle or
furcula (Figure 2). In natural position, the main axis of the coracoid is
oriented caudodorsally (Figure 2c), giving the pectoral girdle a
distinctive orientation in contrast to the craniodorsal orientation of
flying birds. The wings of R. americana have developed all bony
elements (Figure 1b).
3.1.1 | Ossa cinguli membri thoracici
Scapulocoracoid
The scapulocoracoid of Rhea is fused in adults, as occurs in other
flightless paleognaths (Lowe, 1928). The suture between the coracoid
and the scapula is retained in juveniles and embryos (Figure 3a).
The coracoid of R. americana is strut‐like, with the sternal end
transversally expanded (Figure 3) and a narrow omal end. The cranial
surface of the coracoid is convex, while the caudal surface is concave.
The lateral surface of the coracoid is relatively narrow and longitudinally
concave. The subglenoid fossa is subtriangular in contour and is poorly
defined; it is located ventral to the glenoid fossa (Figure 3c). The bone
becomes narrower toward its sternal margin. In cranial view, the
coracoid shows a subvertically oriented linea intermedialis that separates
the sites of origins of the mm. pectoralis p. thoracica and supracoracoideus
(Figures 3b, 12, 16a). The linea intermedialis extends from the processus
acrocoracoideus to the distal third of the bone, and disappears toward the
sternal end of the bone.
The medial surface of the coracoid is thin, and connects the
procoracoid process through the coracoid membrane (com; see
LO COCO ET AL. | 5

Figures 3a, 15c,d, 16a; Fürbringer, 1888). Usually, this membrane
becomes partially ossified, forming sharp bony keels that widen
toward the procoracoid process and form the foramen for the
passage of the supracoracoid nerve.
The facies articularis sternalis is slightly convex cranially and
lateromedially compressed, having an irregular edge (Figure 3). In its
natural position, the main axis of the coracoid conforms to a
perpendicular angle with the facies articularis sternalis in cranial and
lateral views (Figure 4a,b). The sternal end of the coracoid presents
abundant pneumatic foramina on its caudal surface (Figure 3e).
The processus acrocoracoideus is poorly developed, being repre-
sented by a craniolaterally facing bump of small size, with a rounded
external surface. This process is located cranioventrally with respect
to the glenoid fossa, being close to the coracoidal glenoid lip
(Bledsoe, 1988; Figure 3d).
The acrocoracoid process presents a rugose surface for the m. biceps
brachii attachment (Fürbringer; 1888) while the lateral edge is smooth,
subtriangular in contour and has an elongated surface, representing the
attachment site for the m. coracobrachialis cranialis (see Figure 16a,b).
The sulcus supracoracoideus or supracoracoidal canal is a broad
depression, between the processus acrocoracoideus and the processus
acromialis (Fürbringer, 1888), and extends ventrally through the
foramen nervi supracoracoidei (Figure 3b). A smooth ridge connects
the processus acrocoracoideus with the acromion process.
The acromion process forms a bulk prominence, with a rounded
and rugose surface that faces laterocranially. It is located at the
center of the cranial surface of the scapulocoracoid, between the
glenoid fossa and the medial edge of the cranial end of the scapular
blade and the procoracoid process (Figure 3). The acromion process is
located dorsal and craniomedial to the acrocoracoid process and
glenoid fossa. A small ligament, the lig. acrocoracoacromialis, connects
both the acrocoracoid and acromion processes. This ligament is
attached to these processes without leaving distinctive marks, and
delimits dorsally the sulcus supracoracoideus, as was mentioned by
Novas et al. (2021).
The procoracoid process is well developed and presents an
elongated subtriangular shape. It is located ventral to the acromion
process, and ventrolaterally contacts the coracoid membrane
(Figure 3). Its cranial surface shows a thick ridge that runs from the
acromion process to the distal end of the procoracoid process. The
caudal surface of the procoracoid process is flat to shallow concave.
The glenoid fossa is concave and has an oval outline. The
scapular glenoid lip is more developed than the coracoidal one
(Figure 3d). Both scapular and coracoidal areas of the glenoid fossa
are symmetric and similar in size (Figure 3).
The glenoid fossa is ovoidal in contour, subvertically inclined, and
laterocaudally oriented (Figure 3), as was indicated by many authors
(Agnolín et al., 2019; Bledsoe, 1988; Novas et al., 2020). The angle of
inclination of the main axis of the fossa is about 34° with respect to
the dorso‐ventral axis in a scapulocoracoid natural position
(Figure 4d). The main axis of the glenoid fossa is obliquely oriented
with respect to the main axis of the coracoid body, forming an angle
of about 140° in lateral view (Figure 4d).
The scapular blade is flat and slender, lateromedially wider at the
distal end and at its connection with the corpus coracoidei. In juvenile
or sub‐adult specimens, the distal end of the scapular blade is
subtriangular in contour and cartilaginous. In lateral view, the
scapular blade is curved at the first proximal third, forming an angle

F I G U R E 4 Rhea americana albescens, right scapular girdle in natural position (a,b) and scapulocoracoid in anatomical view (c,d) in cranial (a), lateral
(b), craniodorsal (c), and caudolateral (d) views. Vultur gryphus, right scapulocoracoid in anatomical lateral view (e). Scale bar: 3 cm. The complete lines
and black dash lines indicate the angles between the main axis of the corpus coracoidei and the main axis of the facies articularis sternalis (a,b); between
the proximal and distal end of the scapula (c); between the scapular blade and the main axis of the corpus coracoidei (d,e); and between the main axis of
the glenoid fossa and the main axis of the corpus coracoidei (d,e). The complete blue line and black dash lines indicate the angle (α and β) between the
main axis of the glenoid and the dorso‐ventral axis (d,e). co, corpus coracoidei; s, scapular blade; st, sternum.
6 |
of about 140° between both ends (Figure 4c). In R. americana, the
angle formed between the corpus coracoidei and the scapular blade is
obtuse, reaching about 130° (Figure 4c).
Sternum
The sternum of R. americana has a subrectangular shape in ventral
view, being narrower at its caudal end. The corpus sterni is ventrally
convex, while the visceral surface is concave, forming a wide fossa
that nests the heart. The sternum lacks a sternal keel, fenestrae,
trabeculae, foramina, rostrum sterni and intermuscular lines.
The sulcus articularis coracoideus (Figures 5b,c and 14b,d) are shallow
and concave, in accordance with the poor development of bounding
margins (i.e., labri internum and externum). The processus craniolateralis
sterni is subtriangular‐shaped, is notable, and craniolaterally projected.
On the lateral edges of the sternum, immediately caudal to the
processus craniolateralis sterni, three loculus costalis are observed
receiving the fourth, fifth, and sixth costa sternalis (Figure 5;
Pycraft, 1900). The caudal area of the corpus sterni has a semicircular
margin, which in young specimens is enlarged by a cartilaginous
wedge that extends caudally.
3.1.2 | Ossa alae
Although one of the main characteristics of the non‐tinamid
paleognaths is the reduction of the forelimb, probably due to their
specialization as exclusive runners, R. americana has the least reduced
wing among flightless paleognaths.
3.1.3 | Skeleton brachii
Humerus
In the Greater Rhea, the humerus is longer than the bones of the
forearm (radius‐ulna/humerus ratio around 3/4) as occurs in other
F I G U R E 5 Rhea americana albescens, sternum in ventral (a), internal (b), cranial (c), and right lateral (d) views. Scale bar: 3 cm. crst, corpus
sterni; cst, costa sternalis; lc, loculus costalis; pcrl, processus craniolateralis sterni; sac, sulcus articularis coracoideus.
LO COCO ET AL.
non‐volant paleognaths and also observed in tinamids and volant
neognaths (radius‐ulna/humerus ratio around 1/1). The humerus
of the Greater Rhea is longer than the manus (carpometacarpus/
humerus ratio between 1/2 and 1/3) as was reported by Pycraft
(1900) and Bledsoe (1988), and it is about 25%–30% longer than
the femur.
The humeral head is oval‐shaped in proximal view, with the major
diameter in the dorsal‐ventral direction (Figures 6 and 7a). It is
continuous with the tuberculum ventrale (internal tuberosity in
theropods), since there is no incisura capitis (Figures 6 and 7a). The
tuberculum ventrale has a rounded conical shape and it is more
prominent and expanded than the tuberculum dorsalis (external
tuberosity in theropods, e.g., Deinonychus; Ostrom, 1969), which is
a poorly defined prominence.
F I G U R E 6 Rhea americana albescens, right humerus in cranial
(a) and caudal (b) views. Scale bar: 3 cm. cb, crista bicipitalis; cdp, crista
deltopectoralis; ch, caput humeri; cnd, condylus dorsalis; cnv, condylus
ventralis; epd, epicondylus dorsalis; epv, epicondylus ventralis; f Br,
fossa m. brachialis; fo, fossa olecrani; i LDCa, impressio m. latissimus
dorsi p. caudalis; ii, incisura intercondylaris; l HT, linea m. humerotriceps;
l LDCa, linea m. latissimus dorsi p. caudalis; l LDCr, linea m. latissimus
dorsi p. cranialis; pf, processus flexorius; psd, processus supracondylaris
dorsalis; s ST, sulcus m. scapulotriceps; td, tuberculum dorsale;
tsv, tuberculum supracondylaris ventrale; tv, tuberculum ventrale.
LO COCO ET AL. | 7

F I G U R E 7 Rhea americana albescens, right humerus in proximal (a) and distal (b) views. The blue line indicates the orientation of the largest
diameter of caput humeri while the red line (b) indicates the orientation of the largest diameter of distal end. The angle of humerus torsion
(pronatory twist) is shown between the two lines. Scale bar: 1 cm. cb, crista bicipitalis; cdp, crista deltopectoralis; ch, caput humeri; cnd, condylus
dorsalis; cnv, condylus ventralis; epd, epicondylus dorsalis; epv, epicondylus ventralis; fo, fossa olecrani; ii, incisura intercondylaris; pf, processus
flexorius.

On the cranial surface of the proximal end of the humerus, the
deltopectoral crest and the bicipital crest extend distally for the same
length (Figure 6a). The deltopectoral crest is continuous with
the tuberculum dorsalis whereas the bicipital crest is dorsal to the
tuberculum ventralis (Fürbringer, 1888; see Figure 6). Between both
crests there is a subtriangular and shallow fossa on the cranial surface
of humerus, which receives the m. coracobrachialis cranialis (see
Figure 18a).
On the caudal surface of the proximal end of the humerus is a
slightly concave surface, located between the tuberculum dorsalis and
tuberculum ventralis without a sign of a pneumotricipital fossa (see
Figure 6b).
The corpus humeri is sigmoid in shape, with a dorsoventral
curvature. The caudal surface of the corpus presents two conspicu-
ous subparallel muscular lines that extend proximo‐distally: the linea
muscularis latissimus dorsi p. cranialis, being dorsal and proximal to
the linea muscularis humerotriceps (Livesey & Zusi, 2007). The former
became a crest at the mid of the corpus humeri, while the latter
develops a crest on the distal third of the corpus humeri (Figure 6b).
There is a narrow groove between these crests.
On the cranial surface of the distal end of the humerus is a
small concave fossa for the m. brachialis (see Figure 18a). Both
condylus dorsalis (radialis) and ventralis (ulnaris) are ovoid in shape;
the condylus dorsalis is slightly larger than the condylus ventralis.
There is a deep and oblique incisura intercondylaris that separates
the two condyles. The condylus dorsalis is more dorsodistally
ventrocranially inclined and slightly overlaps the condylus ventralis
proximally. The opposite is true for the ventral condyle, which
extends slightly distally (Figure 6a).
The processus dorsalis and the epicondylus dorsalis are small
bump‐like tubercles, less developed than the processus flexorius
(ventralis) and epicondylus ventralis. The processus flexorius is well
developed and digitiform, extending further distally than the
condyles (Figures 6b and 7b). In distal view, the distal end of the
humerus has a deep and well‐developed intercondylar incisura on
its cranial half, while the caudal margin is straight. A deep incisura
separates the condylus ventralis from the processus flexorius
(Figure 7b).
In its proximodistal extension, the humerus has an appreciable
twist of the longitudinal axis. Therefore, the major axes of both
proximal and distal ends of the humerus intersect at an angle of
approximately 52° (pronator torsion), generating a dorsal‐to‐cranial
twist (Figure 7). This direction and degree of twist between the two
ends of the humerus causes the main axis of the distal end and the
condyles to be positioned perpendicular to the dorso‐ventral axis
when the humerus is extended craniolaterally (full abduction). Thus,
the elbow joint points dorsally and, therefore, the forearm will move
in the dorso‐ventral axis when the arm is fully abducted. Conse-
quently, the twisting of the humerus of R. americana contributes to
the inverted L‐shaped wing posture when it is extended (Figure 1a).
3.1.4 | Skeleton antebrachii
The radius and the ulna of R. americana are parallel to each other. The
ulna is more robust and slightly longer than the radius, and its
proximal and distal ends are larger than those of the radius.
Ulna
The ulna is sigmoid‐shaped in dorsal view, being dorsoventrally
flattened and more voluminous at the proximal and distal ends
(Figure 8). The olecranon projects proximally and extends distally and
8 |
caudally forming a discernible ridge in the first third of the ulna
(Figure 8), being deeper proximally. In proximal view, the olecranon is
a thick and transversely narrow keel (Figure 9b). The cotyla humeralis
is concave in proximal view and falciform, located dorsodistally to the
olecranon. The cotyla humeralis occupies half the area of the proximal
end; it is demarcated by the condylus dorsalis and the condylus
ventralis (Figures 8 and 9; Baumel et al., 1993; Livesey & Zusi, 2007).
R. americana has a sole articulation to receive the humerus (the
proper cotyla humeralis; Figure 9b), which articulates only with the
condylus ventralis of the humerus.
F I G U R E 8 Rhea americana albescens, right radius and ulna in
dorsal (a) and ventral (b) views. Scale bar: 3 cm. ch, cotyla humeralis;
cncr, condylus os carpi radialis; cnd, condylus dorsalis; cnm, condylus
metacarpalis; cnv, condylus ventralis; ct, capital tuberosity; ecn,
external condyle; far, facies articularis radialis; fau, facies articularis
ulnaris; i BB, impressio m. biceps brachii; icn, internal condyle;
ol, olecranon; tb, tuberculum bicipitale radii; tlcv, tuberculum lig.
collateralis ventralis.
F I G U R E 9 Rhea americana albescens, right radius (a,c) and ulna (b,d) in proximal (a,b) and distal (c,d) views. Scale bar: 1 cm. ch, cotyla
humeralis; cnd, condylus dorsalis; cncr, condylus os carpi radialis; cnm, condylus metacarpalis; cnv, condylus ventralis; ct, capital tuberosity;
ecn, external condyle; fau, facies articularis ulnaris; icn, internal condyle; ol, olecranon; tb, tuberculum bicipitale radii.
LO COCO ET AL.
The development of the olecranon caudal ridge generates a
mostly flat surface on the dorsal side and a slightly concave surface
on the ventral side, the facies caudodorsalis and the facies
caudoventralis, respectively (Baumel et al., 1993). The former surface
is the site of origin of the m. ectepicondylo‐ulnaris while no muscles
originate or insert on the facies caudoventralis (see Figure 20a).
However, the cranial surface has a subtriangular and slightly concave
surface, which is the insertion site for several muscles (see details
below) and ligaments of the elbow arthrology (Baumel et al., 1993),
including the lig. collateralis ventralis that leave a small tubercle
(Figure 8b). The corpus ulnae is cylindrical in shape and does not
present the characteristic papillae remigales caudales (also known as
quill knobs).
The distal end of the ulna expands cranio‐caudally, maintaining a
subtriangular shape in distal view (Figure 9d). On the cranial surface
of the distal end, the external condyle is prominent on the ventral
edge, while the internal condyle is prominent on the caudal edge
(Figure 9d). In ventral view, and near the internal condyle, there is a
slightly concave surface, the facies articularis ulnaris, which is the site
of articulation with the os carpi ulnaris (Figures 8b and 9d).
In dorsal view, the surface of the distal end of the ulna has a
relatively flat surface, with the distal edge slightly concave
(Figure 8a). In cranial view, the distal end of the ulna presents the
facies articularis radialis (cotyla radialis), which articulates with the
radius and, in distal view, present the condylus carpi radialis which
articulates with the os carpi radialis, that has an oval shape and is
dorso‐ventrally oriented. Caudal to this joint is the condylus
metacarpalis (facies articularis metacarpalis), which articulates with
the carpometacarpus and is also oval in shape, but in this case its
main axis is cranio‐caudally oriented (Figure 9d).
LO COCO ET AL.
The distal border of the ulna of R. americana has an S‐shape in
ventral view (Figure 8), it is slightly convex in its cranial half (condylus
carpi radialis) and slightly concave in its caudal half (condylus
metacarpalis). In addition, the facies articularis ulnaris of the ventral
side of the distal end of the ulna is concave (Figure 8b) and articulates
with the os carpi ulnaris. The dorsal surface of the distal end of the
ulna has a poorly developed articular edge, the labrum condyli, which
has a slightly convex surface.
The major axes of the proximal and the distal ends of the ulna
intersect at an angle, which does not exceed 5°, indicating a slight
torsion in a dorso‐medial direction. Therefore, the forearm does not
contribute significantly to the characteristic position of the wing of R.
americana in full abduction.
Radius
The radius of R. americana is straight and rod‐shaped in dorsal view,
being slightly curved at the distal end, and mostly flattened in the
cranio‐caudal axis (Figure 8). Its proximal end is more voluminous
than the distal one. The proximal end presents a concave, oval‐
shaped, and wide cotyla humeralis, showing well‐developed dorsal
and ventral edges (Figure 9a). The proximal end has a protrusion at
the dorsocaudal edge, the capital tuberosity, which serves as
anchorage of ligaments of the elbow (Baumel et al., 1993). On the
caudal surface of the proximal end of the radius, there is a well‐
developed and oval tuberculum bicipitale radii, which is the mark left
by the insertion of the m. biceps brachii tendon (Figures 9a and 20b).
The corpus radii is oval in cross section with smooth surfaces. The
distal end of the radius widens dorsoventrally and forms a blunt
wedge that curves laterodistally, forming the cotyla carpi radialis
(Figure 9c). The cotyla carpi radialis lies on the caudal aspect and
articulates with the os carpi radialis.
3.1.5 | Skeleton manus
The autopodium of R. americana consists of two carpals (i.e., os carpi
radialis and os carpi ulnaris), the corpus carpometacarpi (i.e., fused
distal carpal and metacarpals I, II, and III), and the phalanges of digiti
alulae, digiti majoris, and digiti minoris (Figure 10).
Os carpi radialis
In the Greater Rhea, the os carpi radialis is larger than the os carpi
ulnaris. The element is subrectangular in contour when it is observed
in dorsal/ventral view. The os carpi radialis has a caudal concavity, the
facies carpometacarpalis, which allows articulation with the trochlea
carpalis of the carpometacarpus. It has two articulations with the
bones of the forearm. The first one is on its cranial surface (facies
radialis) and serves for the articulation with the distal end of the
radius and is formed by a concavity with a deep medial sulcus that is
deeper in its proximal part. This concavity opens cranially, and does
not enclose the radius distally. A second wide and concave facet on
the proximal surface of the os carpi radialis (facies ulnaris) articulates
with the distal end of the ulna.
| 9
F I G U R E 10 Rhea americana albescens, right carpometacarpus and
digits of a subadult in dorsal (a) and ventral (b) views. Scale bar: 3 cm.
cra, os carpi radialis; cul, os carpi ulnaris; fi, fossa intermetacarpalis;
omm, os metacarpi majoris; ommi, os metacarpi minoris; pa, processus
alulae; pda, phalanx digiti alulae; pddm,phalanx distalis digiti majoris;
pdmi, phalanx digiti minoris; pe, processus extensorius; pi, processus
intermetacarpale; ppdm, phalanx proximalis digiti majoris; si, spatium
intermetacarpali; tc, trochlea carpometacarpi; u, ulna; un, ungueal.
Os carpi ulnaris
The os carpi ulnaris does not present a well‐defined U‐shape because
the metacarpalis incisura tends to be flattened and the rami ventralis
and dorsalis are not as well developed. The element has a
subtriangular contour when it is observed in dorsal view. This carpal
has two articulations: the facies ulnaris and the incisura metacarpalis. It
is important to mention their orientation because the proximal facies
ulnaris contacts the ventral surface of the distal end of the ulna while
the craniodorsal incisura metacarpalis contacts the ventrocaudal area
of the trochlea carpalis of the carpometacarpus. The particular shape
of the os carpi ulnaris allows it to maintain a ventral position on the
wrist, in both flexion and extension of the manus. Accordingly, the
shapes of the distal ulna and the os carpi ulnaris in R. americana do not
allow the full flexion and circumduction of the manus.
Carpometacarpus
The carpometacarpus of the R. americana has an elongate and fused
metacarpal II and III, separated by an intermetacarpal space. The
proximal end of the carpometacarpus has a wide carpometacarpal
trochlea, formed by the medial (ventral) and lateral (dorsal) condyles
or rings (Figure 10). The articular surface of the trochlea carpometa-
carpi is almost convex in dorsal view, and the facies articularis
radiocarpalis and ulnocarpalis are well‐differentiated (Figure 11). The
condyli are subparallel to each other, with the condylus lateralis being
larger and cranio‐caudally more extensive than the condylus medialis
(Figure 11).
The cranial end of the condylus lateralis extends distally and
ventrally, forming a prominent edge that results in a processus
10 | LO COCO ET AL.

F I G U R E 11 Rhea americana albescens, right carpometacarpus in proximal (a) and distal (b) views. The blue line indicates the orientation of the
largest diameter of trochlea carpometacarpi while the red line (b) indicates the orientation of the largest diameter of the distal end of the
carpometacarpus. The angle of carpometacarpus torsion (supinatory twist) is shown between the two lines. Scale bar: 1 cm. cnl, condylus lateralis;
cnm, condylus medialis; fadm, faceta digiti majoris; fadmi, faceta digiti minoris; omm, os metacarpi majoris; ommi, os metacarpi minoris; pa, processus
alulae; pe, processus extensorius; pi, processus intermetacarpale; tc, trochlea carpometacarpi.

extensorius (Figure 11). This process is poorly developed and rounded
in contour. In proximal view, this process is cranioventrally oriented
with respect to the main axis of the trochlea carpometacarpi
(Figure 11). It shows a small and concave facies articularis digiti alulae
on its tip.
At the proximal end of the carpometacarpus, the dorsal surface
has a convex area formed by the os metacarpale majus. The processus
intermetacarpale is located caudal to the processus extensorius and
processus alulae and is dorsocaudally oriented (Figure 10a). In
contrast, the ventral surface of the proximal end of the carpometa-
carpus shows a wide and concave fossa intermetacarpalis. This is
probably due to the fact that the processus pisiformis is absent, a
distinctive feature of flightless birds (Livezey & Zusi, 2007).
The os metacarpale majus is stouter and straighter than the os
metacarpale minor; it also exhibits a pronounced caudal curvature,
cranially concave. Both metacarpals fuse distally, defining a long
spatium intermetacarpale, which becomes cranio‐caudally distally
wider. At the distal end, there are two joints, the facies articularis
digiti majoris (cranially) and digiti minoris (caudally). The facies
articularis digiti majoris is wider and cylindrical in shape, and
articulates with the proximal phalanx of digit II. The facies articularis
digiti minoris is subcircular in shape and articulates with the phalanx
1‐III (Figure 11b).
The carpometacarpus of R. americana is notably twisted. It
shows a dorsal‐to‐caudal direction (supinator) torsion, forming an
angle of ~68° between the major axis of its proximal and distal
ends (Figure 11). The marked twisting of the manus of R.
americana results in an inclination of the primary feathers and
does not have the same plane with respect to the secondary
feathers of the forearm.
Digit I, or alular digit, is long and exceeds half the length of the
carpometacarpus. It is composed of two phalanges. Phalanx 1‐I is
elongate and rod‐shaped. The ungual is long and slightly curved
(Figure 10).
Digit II, has two phalanges, both dorsoventrally flattened, the
proximal one being wider than the distal one. Phalanx proximalis digiti
majoris is subquadrangular in contour, whereas phalanx distalis digiti
majoris is subtriangular in shape. Both phalanges show a notably
thickened cranial edge, flattening caudally.
Digit III has a single phalanx. The phalanx digiti minoris is
subtriangular in shape and dorsoventrally flattened. It is similar to the
phalanx distalis digiti majoris, although much smaller in size.
3.2 | Myology of pectoral girdle and wing
Probably due to the loss of flight, some muscles of non‐tinamid
paleognath birds are reduced. While in volant neognaths around
50 muscles are observed in the pectoral girdle and wing (Baumel
et al., 1993; Raikow, 1985), in R. americana we found 41 muscles.
Different authors, including Fürbringer (1888), Hudson et al.
(1972), McGowan (1982), Raikow (1985), and Baumel et al.
(1993), reported that the absence of many pectoral girdle muscles
and suggested that it related to flightless of paleognaths, including
R. americana (Lowe, 1928; Suzuki et al., 2014). In accordance with
those authors, we noted the absence of five muscles in the
pectoral girdle (mm. pectoralis propatagialis, deltoideus propatagialis,
deltoideus minor, coracobrachialis p. caudalis and serratus super-
ficialis p. metapagialis [=cutaneous costohumeralis]), and the
absence of four muscles in the forearm and manus (mm. flexor
LO COCO ET AL.
digitorum superficialis, entepicondylo‐ulnaris, extensor digitorum
communis, and extensor longus digiti majoris p. proximalis).
3.2.1 | Topographic anatomy of muscles
The m. latissimus dorsi has two independent bellies, p. cranialis and p.
caudalis. The p. cranialis (LDCr, Figures 12b, 13a, 18b) is a band‐
shaped muscle that has an aponeurotic origin on the neural spines of
the second and third thoracic vertebrae. It has a fleshy insertion on
the medial portion of the corpus humeri, its insertion is marked by a
small osseous ridge. Its function is to retract and slightly elevate the
humerus and abduct the wing.
The p. caudalis (LDCa, Figures 12a, 13a, 18b) has a wide
aponeurotic origin from the ribs of the third and fifth thoracic
vertebrae. This band‐shaped belly does not reach the thoracic
vertebrae. The insertion is tendinous on a small area on the medial
part of the corpus humeri, proximal to the insertion of m. latissimus
dorsi p. cranialis. Its principal function is to retract the humerus.
The m. deltoideus major (DM, Figures 12, 13, 16a, 17, 18) is a
bulky muscle. It has a wide fleshy and tendinous origin in the proximal
cranial surface of the scapula, reaching the sulcus supracoracoideus,
between the acromion and the glenoid fossa. It runs along the first
half of the humerus and is inserted into the dorsal margin. The
topography of them. deltoideus major allows it to elevate the
humerus.
The m. rhomboideus superficialis (RS, Figures 12, 16a,c) is a single
thin band‐shaped muscle that originates aponeurotically from the last
cervical vertebra and the first and second thoracic vertebrae, not
contacting the neural spines. The m. rhomboideus superficialis
originates cranially to m. latissimus dorsi p. cranialis and partially
F I G U R E 12 Rhea americana albescens,
photographs and schematic drawings of
superficial muscles of right shoulder and
proximal humerus in lateral (a) and
craniolateral (b) views. Scale bar: 3 cm. BB, m.
biceps brachii; DM, m. deltoideus major; LDCa,
m. latissimus dorsi p. caudalis; LDCr, m.
latissimus dorsi p. cranialis; PT, m. pectoralis p.
thoracica; RS, m. rhomboideus superficialis; SC,
m. supracoracoideus; sco, scapulocoracoid;
SSCa, m. serratus superficialis p. caudalis; st,
sternum. The bones were colored gray, the
muscles yellow, and the ligaments orange.
| 11
covers the cranial part of the m. serratus profundus. It is inserted in the
medial edge of the scapular blade, in the procoracoid process, and in
the coracoid membrane, homologous to the sternocoracoclavicularis
membrane of neognaths (Baumel et al., 1993; Livezey & Zusi, 2007).
The m. rhomboideus superficialis protrudes the scapulocoracoid.
The m. rhomboideus profundus (RP, Figures 13a, 16a,c) is a flat
muscle that has an aponeurotic and tendinous origin in the area of
the third, fourth, and fifth thoracic vertebrae, without reaching the
neural spines. Close to the scapular blade, it is associated with the
two cranial layers of the m. serratus profundus. The m. rhomboideus
profundus inserts on the medial surface of the distal end of the
scapular blade, reaching the dorsal edge; it protracts the scapular
blade.
The m. scapulohumeralis has two bellies, the cranialis (SHCr,
Figures 15b, 16c, 18b) and the caudalis (SHCa, Figures 13, 15a,b,
16a,c, 17a, 18). The m. scapulohumeralis p. cranialis is a tiny, tubular
and fleshy muscle that originates on the inner edge of the scapular
blade on its medial surface, being dorsal to the glenoid fossa. It is
inserted tendinously into the caudal surface of the humerus, slightly
dorsal to the tuberculum ventrale. Functionally, it could retract and
pronate the humerus.
The m. scapulohumeralis p. caudalis is a broad, fan‐shaped, and
fleshy belly that originates with an aponeurosis on a large area of the
inner edge of the scapular blade. The insertion is broad and
tendinous, occupying the entire distal edge of the tuberculum ventrale
of the humerus. The m. scapulohumeralis p. caudalis retracts and
pronates the humerus.
The m. supracoracoideus (SC, Figures 12, 13a, 16a,e, 17a, 18a) is a
fleshy and flattened muscle that covers a large area of the pectoral
girdle. It has a fleshy origin from a small area of the cranioventral
surface of the sternum, in the craniomedial surface of the coracoid, in
12 | LO COCO
the coracoid membrane, and in the cranial surface of the procoracoid
process. The size of this muscle and the extension of its origin varies
in the two specimens. In one specimen, the origin on the sternum is
much smaller than indicated in Figure 16e.
Because R. americana does not have a triosseal foramen, the m.
supracoracoideus is sharpened and channeled through the supracor-
acoidal canal (Figure 3b), which in this species is well delimited by the
acromion and the acrocoracoid process, and roofed by the lig.
acrocoracoacromialis (Novas et al., 2021). When the m. supracoracoi-
deus passes the supracoracoidal canal it inserts with a tendon in the
dorsal edge of the proximal end of the humerus. When the muscle
was manipulated, the humerus was protruded and secondarily slightly
elevated. In contrast to neognath birds, a rotation of the humerus has
not been observed during these movements.
The m. pectoralis has only one belly, the p. thoracica (PT,
Figures 12, 16a, 18a), in contrast to the two bellies that Jasinoski
et al. (2006) described for Struthio. It is a strap‐shaped muscle that
originates fleshy on the craniolateral surface of coracoideum, without
any origin on the sternum and on the ribs (Lowe, 1928), and does not
overlap the m. supracoracoideus. Close to the acrocoracoid process,
the m. pectoralis p. thoracica surrounds the m. biceps brachii, and
extends to the proximal end of the humerus, where it has a double
tendinous insertion. In turn, it is inserted into the cranial surface of
the crista deltopectoralis and, on the other hand, it is inserted over the
crista bicipitalis. The latter insertion is associated with the arm skin.
The function of the m. pectoralis p. thoracica is to protract and slightly
depress the humerus and abduct the wing.
The m. biceps brachii (BB, Figures 12, 16a,b, 17, 19b–d, 20b) is a
large muscle that exhibits two bellies with two different origins
ET AL.
F I G U R E 13 Rhea americana albescens,
photographs and schematic drawings of
superficial (a) and deep muscles (b) of right
shoulder and proximal humerus in dorsolateral
view. Scale bar: 3 cm. DM, m. deltoideus major;
h, humerus; LDCa, m. latissimus dorsi p.
caudalis; LDCr, m. latissimus dorsi p. cranialis;
RP, m. rhomboideus profundus; s, scapular
blade; SC, m. supracoracoideus; sco,
scapulocoracoid; SHCa, m. scapulohumeralis
p. caudalis; SPCa, m. serratus profundus p.
caudalis; SPCr, m. serratus profundus p.
cranialis; ST, m. scapulotriceps; t1, first thoracic
vertebra; t2, second thoracic vertebra; t3, third
thoracic vertebra.
(Lowe, 1928). One belly is mainly tendinous; it originates on the top
of the acrocoracoid process, and is located dorsal and cranial to the
m. coracobrachialis cranialis origin. The other belly is fleshy and
tendinous on the lateral edge of the coracoid, and is also cranially
located with respect to the m. coracobrachialis cranialis origin.
The bellies of m. biceps brachii merge when they reach the
proximal humerus area and they are surrounded by the m. pectoralis
p. thoracica, as mentioned above. The strong grip between the skin
and the humerus occurs throughout the crista deltopectoralis, being
dorsal to the insertion of the m. pectoralis p. thoracica, in its cranial
part; and being dorsal to the m. deltoideus major, in its caudal
surface.
Distal to the fusion of the bellies, the m. biceps brachii extends
longitudinally along the cranial surface of the humerus reaching the
forearm. Its insertion is double and tendinous. It is inserted into the
proximal end of the radius and the ulna. The function of the m. biceps
brachii in R. americana is to flex the forearm and protract the humerus
(Novas et al., 2021).
The m. scapulotriceps (ST, Figures 13a, 16a, 17, 19a, 20a) has a
tendinous origin on the proximal end of the scapular blade. It
extends along the humerus on its caudal surface and attaches
strongly to the m. humerotriceps in their distal third. The arthrology
of the elbow is complex and involves the m. scapulotriceps and the
m. humerotriceps. The tendon of each muscle passes through the
caudodistal end of the humerus, through the sulcus scapulotriceps
(dorsal) and sulcus humerotriceps (ventral). Both tendons are
distally joined and inserted into the ventral base of the olecranon,
at the ulna. The m. scapulotriceps extends the forearm and retracts
the humerus.
LO COCO ET AL. | 13

F I G U R E 14 Rhea americana albescens, photographs and schematic drawings of superficial (a) and deep muscles (b–d) of right shoulder and
proximal humerus in lateral (a–c) and craniolateral (d) views. In (b), the scapulocoracoid is disarticulated, showing its caudal surface. In (d), the
scapulocoracoid was removed. Scale bar: 3 cm. CBCr, m. coracobrachialis cranialis; ci2, second costae incompletae; CS, m. costosternalis; cv3, third
costae vertebralis; cv4, fourth costae vertebralis; h, humerus; pcrl, processus craniolateralis sterni; sac, sulcus articularis coracoideus; SBC, m.
subcoracoideus; sco, scapulocoracoid; SSCa, m. serratus superficialis caudalis; SSCr, m. serratus superficialis cranialis; st, sternum.

The m. subcoracoideus (SBC, Figures 14c, 15c, 16a,b,e, 18b) is a
small and fleshy muscle. It has a fleshy and aponeurotic origin in the
processus craniolateralis sterni, in the lateral and distal edge of the
coracoid, and in the tendinous structures (ts; see Figure 15d)
between this process and the whole lateral edge of the os
coracoideum. It inserts with a tendon on the proximal end of the
humerus, in the tuberculum ventrale. The m. subcoracoideus adducts
the humerus.
The m. subscapularis (SBS, Figures 15a,b, 16c, 18b) is a broad,
fan‐shaped muscle. It has a fleshy and aponeurotic origin on the
caudal surface of the scapulocoracoid reaching the coracoid
membrane, the procoracoid process, and the ventral surface of the
scapular blade. It inserts with a thick tendon on the caudal surface of
the proximal end of the humerus, being dorsal to the insertion of the
m. subcoracoideus. In some specimens, the m. subscapularis and m.
subcoracoideus tendons join before reaching the humerus, maintain-
ing independent insertions. The m. subscapularis helps to retract the
humerus.
In R. americana, a single belly of m. coracobrachialis, the p. cranialis
(CBCr, Figures 14c, 16b, 17a, 18a) is observed. The m. coracobra-
chialis p. cranialis is a bulky and fusiform muscle that has a fleshy and
tendinous origin from the lateral subtriangular surface of the omal
end of the scapulocoracoid and associated tendinous tissue, over-
lapping the m. subcoracoideus. The area of m. coracobrachialis p.
cranialis origin is caudal and larger than the area of m. biceps brachii
origin. In R. americana, the m. coracobrachialis p. cranialis insertion is
fleshy and tendinous; it is located in the cranial surface of the
proximal end of the humerus, in the area between the crista
deltopectoralis and the crista bicipitalis. The insertion site is different
from that observed in neognath birds (Baumel et al., 1993; Lo Coco
et al., 2020; Picasso & Mosto, 2018). The function is to protract and
depress the humerus.
The m. sternocoracoideus (Stc, Figures 15d, 16a,c,e) is a small
muscle with a tendinous and fleshy origin on the processus
craniolateralis sterni, on its cranial surface. Its insertion is fleshy and
tendinous, and it adheres to the caudolateral surface of the sternal
end of the scapulocoracoid. It participates in respiratory movements
(Raikow, 1985).
The m. serratus superficialis cranialis (SSCr, Figures 14b, 16c,d) is a
fusiform muscle that originates fleshy on the cranial edge and lateral
surface of the distal end of the costae incompletae of the third
thoracic vertebra. Its insertion is tendinous onto the ventral side of
the proximal end of the scapular blade, leaving a small linear mark. Its
function is to move the scapula caudoventrally.
The m. serratus superficialis caudalis (SSCa, Figures 12a, 14a,
16c,d) is a flat muscle with many tendon fibers. It has an aponeurotic
origin on the processus uncinatus of the ribs of the fourth, fifth, and
sixth thoracic vertebrae, extending also over the caudal edge of the
14 | LO COCO ET AL.

F I G U R E 15 Rhea americana albescens, photographs and schematic drawings of deep muscles of right scapulocoracoid and proximal humerus
in caudal (a,b) and cranial (c,d) views. Scale bar: 3 cm. co, corpus coracoidei; com, coracoid membrane; fnsc, foramen nervi supracoracoidei;
h, humerus; pcrl, processus craniolateralis sterni; SBC, m. subcoracoideus; SBS, m. subscapularis; sco, scapulocoracoid; SHCa, m. scapulohumeralis
p. caudalis; SHCr, m. scapulohumeralis p. cranialis; st, sternum; Stc, m. sternocoracoideus; ts, tendinous structure.
LO COCO ET AL. | 15

F I G U R E 16 Rhea americana albescens, muscular maps showing the sites of origin (red) and insertion (blue) of right coracoid in cranial (a),
lateral (b), and caudal (c) views; rib cage and scapular girdle in right lateral (d) view; sternum in ventral (E) view. Scale bars 3 cm. Abbreviations.
com, coracoid membrane; gl, glenoid fossa; pcrll, processus craniolateralis sterni; sco, scapulocoracoid; t3–t6, thoracic vertebrae; BB, m. biceps
brachii; CBCr, m. coracobrachialis cranialis; DM, m. deltoideus major; PT, m. pectoralis p. thoracica; RP, m. rhomboideus profundus; RS, m.
rhomboideus superficialis; SBC, m. subcoracoideus; SBS, m. subscapularis; SC, m. supracoracoideus; SHCa, m. scapulohumeralis p. caudalis; SHCr, m.
scapulohumeralis p. cranialis; SP, m. serratus profundus; SSCa, m. serratus superficialis caudalis; SSCr, m. serratus superficialis cranialis; ST, m.
scapulotriceps; Stc, m. sternocoracoideus.

F I G U R E 17 Rhea americana albescens, photographs and schematic drawings of superficial muscles of right humerus in lateral (a) and medial
(b) views. Scale bar: 3 cm. h, humerus; s, scapular blade; sco, scapulocoracoid; BB, m. biceps brachii; CBCr, m. coracobrachialis cranialis; DM, m.
deltoideus major; HT, m. humerotriceps; SC, m. supracoracoideus; SHCa, m. scapulohumeralis p. caudalis; ST, m. scapulotriceps.

rib of the fourth thoracic vertebra. It has a tendinous insertion on the
ventral surface of the distal end of the scapular blade, being dorsal to
the insertion of the m. scapulohumeralis p. caudalis. Them. serratus
superficialis caudalis moves the scapula ventrally.
The m. serratus profundus (SP, Figure 16a,c) is composed of two
flat bellies, the p. cranialis (SPCr, Figure 13b) and the p. caudalis (SPCa,
Figure 13b), which have a common insertion in the scapular blade.
The m. serratus profundus p. cranialis is a small muscle with a fleshy
and tendinous origin on the proximal end of the rib of the first
thoracic vertebra and the intercostal space between it and the
second thoracic vertebra. Its origin does not reach the neural spine.
The m. serratus profundus p. caudalis is larger and more extensive than
the m. serratus profundus p. cranialis, originating with a tendon on the
caudal edge of the proximal end of the second thoracic vertebra rib
and aponeurotically from the intercostal space between it and the
proximal end of the third thoracic vertebra rib. In some specimens, an
aponeurotic union was observed between these muscles and the mm.
intertransversarii. Reaching the scapular blade, both muscles fuse and
insert into the middle of the medial surface of the scapular blade. The
function of the m. serratus profundus is to protract the scapular blade.
The m. costosternalis or sternocostalis (CS, Figure 14d) is a
fusiform and fleshy muscle that has a tendinous origin on the inner
16 | LO COCO ET AL.

side of the sternum (Baumel et al., 1993), in the lateral side of the
labrum internum, which forms the sulcus articularis coracoideus.
It inserts with a tendon on the medial surface of the distal end of
the costae incompletae of the second thoracic vertebra. The m.
costosternalis participates in respiration function.
The m. humerotriceps (HT, Figures 17b, 18b, 19a) is a large muscle
that has a fleshy origin on the caudal surface of the humerus, becoming
tendinous distally. As described above, in the elbow area the tendons of
m. humerotriceps and the m. scapulotriceps fuse and insert on the ventral
base of the olecranon, in the ulna. This muscle extends the forearm.

F I G U R E 18 Rhea americana albescens, muscular maps showing

the sites of origin (red) and insertion (blue) of right humerus in cranial
(a) and caudal (b) views. Scale bar: 3 cm. Br, m. brachialis; CBCr, m.
coracobrachialis cranialis; DM, m. deltoideus major; ECR, m. extensor
carpi radialis; ECU, m. extensor carpi ulnaris; EU, m. ectepicondylo‐
ulnaris; FCU, m. flexor carpi ulnaris; HT, m. humerotriceps; LDCa, m.
latissimus dorsi p. caudalis; LDCr, m. latissimus dorsi p. cranialis; PT, m.
pectoralis p. thoracica; PP, m. pronator profundus; PS, m. pronator
superficialis; SBC, m. subcoracoideus; SBS, m. subscapularis; SC, m.
supracoracoideus; SHCa, m. scapulohumeralis p. caudalis; SHCr, m.
scapulohumeralis p. cranialis; Su, m. supinator.
F I G U R E 20 Rhea americana albescens, muscular maps showing
the sites of origin (red) and insertion (blue) of right radius‐ulna in
dorsal (a) and ventral (b) views. Scale bar: 3 cm. BB, m. biceps brachii;
Br, m. brachialis; ELA, m. extensor longus alulae; EU, m. ectepicondylo‐
ulnaris; FCU, m. flexor carpi ulnaris; FDP, m. flexor digitorum profundus;
HT, m. humerotriceps; PP, m. pronator profundus; PS, m. pronator
superficialis; ST, m. scapulotriceps; Su, m. supinator; UD, m.
ulnometacarpalis dorsalis; UV, m. ulnometacarpalis ventralis.

F I G U R E 19 Rhea americana albescens, photographs and schematic drawings of superficial (a, c) and deep muscles (b, d) of right radius‐ulna in
dorsal (a, b) and ventral (c, d) views. Scale bar: 3 cm. h, humerus; r, radius; u, ulna; BB, m. biceps brachii; Br, m. brachialis; ECR, m. extensor carpi
radialis; ECU, m. extensor carpi ulnaris; ELA, m. extensor longus alulae; EU, m. ectepicondylo‐ulnaris; FCU, m. flexor carpi ulnaris; FDP, m. flexor
digitorum profundus; HT, m. humerotriceps; PP, m. pronator profundus; PS, m. pronator superficialis; ST, m. scapulotriceps; Su, m. supinator; UD, m.
ulnometacarpalis dorsalis; UV, m. ulnometacarpalis ventralis.
LO COCO ET AL. | 17

F I G U R E 21 Rhea americana albescens, photographs and schematic drawings of superficial muscles of right manus in dorsal (a) and ventral
(b) views. Scale bar: 3 cm. al, phalanx digiti alulae; c ra, os carpi radialis; cm, carpometacarpus; pddm, phalanx distalis digiti majoris; pdmi, phalanx
digiti minoris; ppdm, phalanx proximalis digiti majoris; r, radius; u, ulna; AbA, m. abductor alulae; AbDM, m. abductor digiti majoris; AdA, m. adductor
alulae; EBA, m. extensor brevis alulae; ECR, m. extensor carpi radialis; ECU, m. extensor carpi ulnaris; ELA, m. extensor longus alulae; ELDM, m.
extensor longus digiti majoris; FA, m. flexor alulae; FCU, m. flexor carpi ulnaris; FDMi, m. flexor digiti minoris; FDP, m. flexor digitorum profundus; ID,
m. interosseus dorsalis; IV, m. interosseus ventralis; UD, m. ulnometacarpalis dorsalis; UV, m. ulnometacarpalis ventralis.

F I G U R E 22 Rhea americana albescens, muscular maps showing
the sites of origin (red) and insertion (blue) of right carpometacarpus
and digits in dorsal (a) and ventral (b) views. Scale bar: 3 cm. c ra, os
carpi radialis; c ul, os carpi ulnaris; u, ulna; AbA, m. abductor alulae;
AbDM, m. abductor digiti majoris; AdA, m. adductor alulae; EBA, m.
extensor brevis alulae; ECR, m. extensor carpi radialis; ECU, m. extensor
carpi ulnaris; ELA, m. extensor longus alulae; ELDM, m. extensor longus
digiti majoris; FA, m. flexor alulae; FCU, m. flexor carpi ulnaris; FDMi, m.
flexor digiti minoris; FDP, m. flexor digitorum profundus; ID, m.
interosseus dorsalis; IV, m. interosseus ventralis; UD, m.
ulnometacarpalis dorsalis; UV, m. ulnometacarpalis ventralis.
The m. extensor carpi radialis (ECR, Figures 18a, 19a,c, 21b, 22b)
has a single belly. It is a bulky fusiform muscle that is firmly
connected to the skin on the dorsal side of the forearm. It has a fleshy
and tendinous origin on the processus supracondylaris dorsalis, on the
cranial surface of the distal end of the humerus. In its distal portion, it
becomes tendinous and passes through a dorsocranial cartilaginous
channel, in the wrist joint, cranial to the os carpi radialis. Having
crossed the wrist, it turns ventral and it divides into two tendons; the
smaller one is inserted into the ventral side of the processus
extensorius, while the larger one is inserted ventral into the proximal
end of the os metacarpale minus, that is, into the proximoventral side
of the spatium intermetacarpale. Its function is not only to extend, but
also to supinate the manus.
The m. brachialis (Br, Figures 18a, 19a–c, 20b) is a small fleshy
muscle that originates on the cranial surface of the distal end of the
humerus, in the fossa brachialis. Its insertion is fleshy and thin onto
the cranial surface of the proximal end of the ulna, flexing the
forearm.
The m. supinator (Su, Figures 18b, 19a, 20) is a fleshy muscle that
originates tendinous on the caudal surface of the distal end of the
humerus. It has a fleshy insertion on the first half of the radius, mainly
on its cranio‐dorsal side. Its function is to flex the elbow.
The m. ectepicondylo‐ulnaris (EU, Figures 18b, 19a, 20a) is a
fleshy muscle with a strong tendon that originates on the caudal‐
dorsal side of the distal end of the humerus, being distal to the origin
of the m. supinator. Toward the elbow joint, it covers the origin of the
m. extensor carpi ulnaris and is inserted fleshly in the first half of the
ulna, in its dorsal surface. The function of the m. ectepicondylo‐ulnaris
is to extend the forearm.
The m. extensor carpi ulnaris (ECU, Figures 18b, 19a, 21a, 22a) is a
thin fusiform muscle that has a tendinous origin in the dorsocaudal
surface of the distal end of the humerus¸ distal to the m.
ectepicondylo‐ulnaris origin. The m. extensor carpi ulnaris occupies
the spatium between the radius and ulna, becomes tendinous distally,
and passes through a tendinous channel, in the ulna, cranially to the
18 | LO COCO
origin of the m. ulnometacarpalis dorsalis. It inserts dorsal on the
processus intermetacarpale of the carpometacarpus and is partially
covered by the m. extensor longus digiti majoris. The m. extensor carpi
ulnaris extends the carpometacarpus.
The m. pronator superficialis (PS, Figures 18b, 19c, 20b) and the
m. pronator profundus (PP, Figures 18b, 19c, 20b) are closely related,
remaining undifferentiated over much of their length and sharing
origin and insertion. Both bellies originate tendinously at the distal
and ventral surface of the humerus, proximal to the epicondylus
ventralis. These muscles have two insertions, one proximal into the
cranio‐ventral surface in the proximal end of the ulna. The other
insertion, more distal, is fleshy and reaches the proximal and medial
area of the radius, into its ventro‐caudal surface, leaving a small notch
in its proximal portion. These muscles flex the forearm.
The m. flexor carpi ulnaris (FCU, Figures 18b, 19a,c, 20b, 21b,
22b) is intimately linked to the skin in all its extension, mainly in the
caudo‐ventral margin of the forearm where the secondary feathers
are attached. It has a tendinous origin on the caudal surface of the
distal end of the humerus and two origins in the proximal end of the
ulna, one is tendinous and originates on the cranio‐ventral surface,
and the other is aponeurotic origin on the caudal edge. There is also
an aponeurosis on the distal end of the humerus and the proximal
end of the ulna, linked to elbow arthrology. In the middle of the ulna
the m. flexor carpi ulnaris is bifurcated in two bellies as was indicated
by Lowe (1928), each with an independent insertion. The most cranial
belly is more conspicuous and has a small tendon that is inserted into
the proximal‐caudal part of the os carpi ulnaris. The caudal belly is
fleshy and extends distally linked to the skin of the forearm, until it
reaches the caudal edge skin of the manus, reaching the area of
insertion of the m. ulnometacarpalis dorsalis, but without inserting
itself into the carpometacarpus. This muscle participates in flexing
the carpometacarpus.
The m. extensor longus alulae (ELA, Figures 19, 20, 21, 22b) is a
fleshy muscle located between the radius and the ulna. It has two
points of origin, one is fleshy and aponeurotic at the cranial edge of
the ulna, in its proximal two thirds. The other is fleshy on the caudal
edge of the half radius, without reaching the proximal and distal ends.
Distally it becomes fusiform, tendinous and passes dorsally to the
wrist, through its cranial side, being caudal to the m. extensor carpi
radialis tendon. It is inserted in the ventral surface of the processus
extensorius, in the carpometacarpus, being cranial to the m. extensor
carpi radialis insertion. This muscle could extend and slightly supinate
the manus.
The m. flexor digitorum profundus (FDP, Figures 19d, 20b, 21b,
22b) is a single fleshy muscle that originates on the distal half of the
ulna, on its ventral surface, contrary to what has been described for
volant neognath birds, in which it originates in the ventral surface of
the proximal half of the ulna (Lo Coco et al., 2020; Picasso &
Mosto, 2018). Distally, it becomes a tendon that passes ventrally
through a cartilaginous channel, in the wrist area. As the processus
pisiformis is not developed in R. americana, the m. flexor digitorum
profundus passes through the ventral surface of the carpometacarpus
without generating any kind of pulley. Distally, the m. flexor digitorum
ET AL.
profundus presents two insertions, a small one located at the distal
end of the carpometacarpus, in its cranio‐ventral surface. The second
one is larger and is located on the phalanx distalis digiti majoris, along
the cranio‐ventral border. The function of the m. flexor digitorum
profundus is to extend and slightly supinate the carpometacarpus and
the digiti majoris.
The m. ulnometacarpalis ventralis (UV, Figures 19c,d, 20b, 21b,
22a) presents a fleshy and aponeurotic origin on the cranio‐ventral
surface of the distal end of the ulna. Distally, it becomes tendinous
and passes cranially through a cartilaginous channel in the os carpi
radialis, changing its orientation and inserting into the cranio‐dorsal
surface of the proximal end of the carpometacarpus. This muscle
could extend and slightly protract the manus.
The m. ulnometacarpalis dorsalis (UD, Figures 19a,b, 20a, 21a,
22b) presents a fleshy and tendon‐like origin on the dorsal surface of
the distal end of the ulna, leaving a small scar. It has a fleshy insertion
into the proximal and caudal edge of the os metacarpale minus of the
carpometacarpus, proximal to the m. flexor digiti minoris origin. The m.
ulnometacarpalis dorsalis flexes the manus.
The m. abductor alulae (AbA, Figures 21b and 22) and the m.
flexor alulae (FA, Figures 21b and 22) are strongly connected, so it is
impossible to separate them. However, it should be noted that the
location of the m. abductor alulae would be more cranial than that of
the m. flexor alulae. This small muscle complex has a fleshy origin on
the cranial border and ventral surface of the proximal end of the
carpometacarpus. It has two insertions on the phalanx of digiti alulae,
one fleshy on the cranio‐ventral border and the other tendinous on
the proximo‐ventral end. The mm. abductor alulae and flexor alulae
extend the digiti alulae.
The m. extensor brevis alulae (EBA, Figures 21a and 22a) is a
fleshy, conspicuous muscle that originates with a small aponeurosis
on the cranio‐dorsal side of the carpometacarpus, reaching the base
of the digiti alulae, among the m. abductor alulae, m. flexor alulae, and
m. extensor longus digiti majoris origin area. It has a fleshy insertion on
the cranio‐dorsal edge of the phalanx digiti alulae, being closely
related to the m. abductor alulae and m. flexor alulae, in its proximal
portion. The m. extensor brevis alulae extends the digiti alulae.
The m. extensor longus digiti majoris (ELDM, Figures 21a and 22a)
is a fleshy muscle that has a single developed belly, the p. distalis. Its
origin is established only in the carpometacarpus, while there is no
origin in the radius or ulna. It originates from a large area of the
carpometacarpus that occupies the dorsal surface from the proximal
end to the distal end of the os metacarpale majus. It has two
insertions, one on the articular region of the phalanx proximalis digiti
majoris with a strong tendinous union with the m. interosseus dorsalis.
The other is by a small tendon on the distal end of the phalanx distalis
digiti majoris. The function of them. extensor longus digiti majoris is to
extend the digiti majoris.
The m. interosseus dorsalis (ID, Figures 21 and 22a) is a fleshy,
large and conspicuous muscle that originates on the entire cranial
edge of the os metacarpale minus and on the caudo‐proximal edge of
the os metacarpale majus. It occupies and covers all of the spatium
intermetacarpale. Distally, a thin tendon joins with the m. extensor
LO COCO ET AL.
longus digiti majoris tendon and inserts on the articular region of the
os metacarpale majusand phalanx proximalis digiti majoris, and the
cranial border of the phalanx distalis digiti majoris. It is involved in the
extension of the digiti majoris.
The m. adductor alulae (AdA, Figures 21 and 22b) is a small fleshy
muscle that originates on the cranio‐ventral border of the os
metacarpale majus, in the carpometacarpus. It has a fleshy insertion
on the inner edge of the phalanx digiti alulae. Its function is to flex the
digiti alulae.
The m. abductor digiti majoris (AbDM, Figures 21b and 22b) is a
fleshy muscle that originates on almost the entire ventral side of the
os metacarpale majus, in the carpometacarpus. It inserts on the
proximo‐ventral area of the phalanx proximalis digiti majoris. The m.
abductor digiti majoris extends and depresses the digiti majoris.
The m. interosseus ventralis (IV, Figures 21b and 22) is a thin
muscle with a fleshy origin on the cranio‐distal border of the os
metacarpale minus and on the caudo‐distal border of the os
metacarpale majus, covering the spatium intermetacarpale. Distally it
becomes tendinous and spreads dorsally, is encapsulated in the
proximal area of the phalanx proximalis digiti majoris, and is inserted
dorsally into the base of the phalanx distalis digiti majoris. This muscle
could flex and slightly elevate the digiti majoris.
The m. flexor digiti minoris (FDMi, Figures 21b and 22b) shows a
fleshy origin on the caudo‐ventral border of the os metacarpale minus,
of the carpometacarpus. It is inserted fleshy and tendinous into the
caudo‐ventral border of the digiti minoris. The function of this muscle
is to flex the digiti minoris.
3.3 | Muscle mass
In R. americana, the total muscle mass of the wing with respect to
BM is low, just 0.88% (Table 1). The masses of individual wing
muscles ranged from 0.001% to 0.106% of the BM and from 0.07%
to 11.96% of the total wing muscle mass (WM).
The muscles of the pectoral girdle and proximal upper arm have
the largest mass values and there is a decrease as they locate more
distally toward the manus (Table 1). In comparison, the muscles from
the pectoral girdle represented 82.18% of the WM, the muscles of
the forearm reached 15.92% of the WM, and the muscles of the
manus reached 1.90% of the WM (Table 2).
The six largest muscles (mm. deltoideus major, supracoracoideus,
pectoralis p. thoracica, humerotriceps, subscapularis, and latissimus dorsi
p. caudalis) belong to the pectoral girdle and distal humerus module.
These muscles represent about half of the wing mass (48.87% WM),
and only 0.43% of the BM (Table 1).
The largest muscle, the m. deltoideus major, is 9.25% heavier than
the m. supracoracoideus, and 45.8% heavier than the m. pectoralis p.
thoracica (Table 1). Otherwise, the m. supracoracoideus is larger and
heavier than m. pectoralis p. thoracica, being around 33.45% heavier
(Table 1).
On the distal humerus and forearm, the mm. flexor carpi ulnaris,
extensor carpi radialis and extensor longus alulae are the largest
| 19
muscles, reaching more than half of the total weight of the forearm
module (Table 1; supplementary online material SI 3).
On the distal forearm and manus, the mm. ulnometacarpalis
dorsalis and interosseus dorsalisare the largest muscles, representing
almost half of the total weight of the manus module (Table 1;
Supporting information: SI 3). Here, the smallest muscle is the m.
interosseus ventralis, which represents 0.07% of the WM and 6.04
E−6% of the BM (Table 1).
3.4 | Wing movements
The Greater Rhea has a particular resting position and wing
movements (Cho et al., 1984; Gasparri, 2016; Muñíz, 1885; Novas
et al., 2020). When the wing is attached to the body in resting
position, the humerus is positioned subparallel to the vertebral
column and the forearm hangs subperpendicular or perpendicular to
the ground.
The most striking and distinctive feature of R. americana is that,
as soon as the humerus is abducted latero‐cranially, the orientation of
the forearm is always vertical or subvertically oriented, resulting in an
inverted L‐shaped wing posture, as originally noted by Lowe (1928).
This configuration allows the orientation of the inner surface of the
wing to be caudally faced in full abduction, as was noted by Raikow
(1968). In addition, when the specimen is standing the inner surface
of the wing never faces ventrally, no matter the movement it
performs.
As expressed in several contributions (Cho et al., 1984;
Gasparri, 2016; Muñíz, 1885; Novas et al., 2020), the Greater Rhea
does not perform the classical wing beat cycle of volant birds. In fact,
the wings extend laterally asynchronously and even asymmetrically
while the animal runs or ascends slopes (Novas et al., 2020).
The typical movement of the wings of Greater Rhea follows a
laterocranial‐mediocaudal arc, maintaining the inner wing surface
medially pointing in fully adduction, and caudally faced, in fully
abduction (Novas et al., 2020; see Figure 1a).
Another type of arm movement in Rhea is when the wings follow
a dorsocranial‐ventrocaudal trajectory, elevating the humerus close
to the body (subparallel to the vertebral column), without extending it
too much laterally. In this trajectory the orientation of the inner
surface of the wing varies from medial (folded to the body) to caudal.
Manipulation of R. americana cadaveric specimens showed that
the range of movements of the arm (humerus) is ample (Figure 23).
During the common abduction–adduction arc, in the dorso‐
ventral plane (cranial view), the maximum range of movements of the
humerus varies about 70° (Figure 23). At maximum abduction, the
range of movements of the humerus reaches 144° in the dorso‐
ventral axis (Figure 24b). It is interesting to note that when the
humerus is elevated more than 90°, the bone rotates longitudinally,
thus changing the orientation of the inner wing surface from caudally
faced to medially oriented.
Particularly, the maximum range of movements of the arm in
latero‐medial plane (dorsal view) is about 100°, from a subparallel
20 | LO COCO ET AL.

T A B L E 1 Wing muscles of Rhea americana albescens, the mean muscular mass (g), standard deviation (SD), percentage of wing mass (%WM),
and body mass (%BW), in brackets, the BM

MACN‐Or 9428 MACN‐Or 9583 Mean Mean Mean

Wing muscles Abbreviation (11,500 g) (15,200 g) mass (g) SD %WM %BM

M. deltoides major DM 12.21 15.90 14.06 1.85 11.96 0.106

M. supracoracoideus SC 11.25 14.48 12.87 1.61 10.94 0.097

M. pectoralis thoracica PT 8.19 11.09 9.64 1.45 8.20 0.073

M. humerotriceps HT 6.09 8.34 7.22 1.13 6.14 0.054

M. subscapularis SBS 6.07 7.68 6.88 0.81 5.85 0.052

M. latissimus dorsi caudalis LDCa 5.83 7.78 6.81 0.98 5.79 0.051

M. scapulotriceps ST 5.04 6.77 5.91 0.87 5.02 0.045

M. biceps brachi BB 4.85 6.60 5.73 0.88 4.87 0.043

M. scapulohumeralis caudalis SHCa 4.82 6.22 5.52 0.70 4.70 0.042

M. latissimus dorsi cranialis LDCr 4.63 6.07 5.35 0.72 4.55 0.040

M. rhomboideus superficialis RS 3.77 5.30 4.54 0.76 3.86 0.034

M. flexor carpi ulnaris FCU 2.71 4.72 3.72 1.01 3.16 0.028

M. extensor carpi radialis ECR 2.75 4.51 3.63 0.88 3.09 0.027

M. coracobrachialis cranialis CBCr 2.86 4.03 3.45 0.59 2.93 0.026

M. extensor longus alulae ELA 2.24 4.13 3.19 0.95 2.71 0.024

M. subcoracoideus SBC 1.91 2.81 2.36 0.45 2.01 0.018

M. serratus profundus SP 1.98 2.61 2.30 0.32 1.95 0.017

M. serratus superficialis caudalis SSCa 1.83 2.65 2.24 0.41 1.91 0.017

M. ectepicondilo ulnaris EU 1.95 2.05 2.00 0.05 1.70 0.015

M. pronator superficialis + profundus PS + PP 1.61 2.02 1.82 0.21 1.54 0.014

M. rhomboideus profundus RP 1.33 1.79 1.56 0.23 1.33 0.012

M. supinator Su 1.00 1.15 1.08 0.08 0.91 0.008

M. brachialis Br 0.71 1.08 0.90 0.19 0.76 0.007

M. serratus superficialis cranialis SSCr 0.67 0.91 0.79 0.12 0.67 0.006

M. extensor longus digiti majoris ELDM 0.42 0.83 0.63 0.21 0.53 0.005

M. ulnometacarpalis dorsalis UD 0.48 0.75 0.62 0.14 0.52 0.005

M. flexor digitorum profundus FDP 0.41 0.52 0.47 0.06 0.40 0.004

M. extensor carpi ulnaris ECU 0.49 0.33 0.41 0.08 0.35 0.003

M. interosseus dorsalis ID 0.39 0.41 0.40 0.01 0.34 0.003

M. extensor brevis alulae EBA 0.33 0.36 0.35 0.02 0.29 0.003

M. flexor alulae + M. abductor alulae FA + AbA 0.25 0.42 0.34 0.09 0.28 0.003

M. abductor digiti majoris AbDM 0.18 0.21 0.20 0.02 0.17 0.001

M. ulno‐metacarpalis ventralis UV 0.17 0.19 0.18 0.01 0.15 0.001

M. scapulohumeralis cranialis SHCr – 0.15 0.15 – 0.13 0.001

M. adductor alulae AdA 0.12 0.15 0.14 0.02 0.11 0.001

M. flexor digiti minoris FDMi 0.09 0.16 0.13 0.04 0.11 0.001

M. interosseus ventralis IV 0.05 0.11 0.08 0.03 0.07 0.001

Total 99.68 135.28 117.56 100.00 0.887

LO COCO ET AL. | 21

position to the vertebral column to a subperpendicular position, in
total abduction (Figure 24a).
In the elbow joint, the movements between the arm and forearm
reached a maximum range of movements about 168°, varying between
5° in total flexion and 173° in total extension (Figure 24c). Although
the elbow movements are generally performed in the same plane,
maximum expansion could vary by 25°, being the lateral expansion
about 17°. In natural movements, when the humerus is adducted, the
forearm flexes and tilts cranio‐lateroventrally, reaching about 35–45°
between the humerus and forearm. When the humerus is abducted,
the forearm hangs perpendicular to the humerus and to the ground.
In Greater Rhea, the movements of the wrist joint are more
restricted than those of the elbow joint. The maximum range of
movements of the manus is about 130°, being 171° in maximum
extension and 41° in maximum flexion, and are achieved when the
forearm is totally flexed (Figure 24c). When the forearm is extended
beyond ~80°, the flexion capacity of the manus is markedly reduced,
preventing it from flexing less than 70–75°. At maximum forearm
extension, the manus reaches 108° of maximum extension
(Figure 24c). Consequently, it is important to note that since the
manus cannot be flexed beyond 41°, circumduction cannot be
performed.
The wrist movements are performed in the forearm‐manus plane,
between 41° to ~90°, while a supination rotation can be observed
when the manus is extended more than ~90° (Figure 25a,b).
Consequently, the palm surface of the manus rotates until it is close
to 90° when reaching the maximum extension and moves from a
parallel position to the inner surface of the forearm to a sub
perpendicular position (Figure 25).
The movements of the digits are more limited than those of the
arm, forearm, and manus. The digit with the greatest range of
movements is the alular one, performing mainly flexion and extension
movements, varying from 14° to 67°, respectively, with respect to
the axis formed by the os metacarpale majus. In relation to the os
metacarpale majus, the phalanx digiti alulae performs these move-
ments with a ventrodistal inclination.
The phalanges of digiti majoris do not show wide flexion‐
extension or abduction–adduction movements. These movements
were not measured.
As for the phalanx digiti minoris, it has a minor flexion and
extension capability, being related with the movement of the phalanx
proximal digiti majoris.
With all the information gathered from the manipulation of fresh
specimens of R. americana, we could affirm that a complete automatic

T A B L E 2 Mean % wing for the three

Mean % wing
modules (pectoral girdle, forearm and Muscle Rhea Tyto Caracara Milvago Milvago
manus) of Rhea americana albescens, Tyto modules americana furcataa plancusb chimangob chimachimab
furcata (Lo Coco et al., 2020), Caracara
plancus (Picasso & Mosto, 2018), Milvago Pectoral girdle 82.18 84.79 88.39 89.49 90.25
chimango (Picasso & Mosto, 2018), Forearm 15.92 13.64 10.45 9.87 9.13
Milvago chimachima (Picasso &
Manus 1.90 1.04 1.13 0.64 0.60
Mosto, 2018)
a
Lo Coco et al. (2020).
b
Picasso and Mosto (2018).

F I G U R E 23 Rhea americana albescens, maximum range of movements of the right humerus (light blue) and the typical abduction–adduction
arc movement (blue dots) in cranial (a), lateral (b), and dorsal (c) views. Scale bar: 3 cm. “x”, latero‐medial axis; “y”, dorso‐ventral axis; “z”,
cranio‐caudal axis; axes scale 5 cm.
22 | LO COCO
wing folding is missing and the circumduction of the manus does not
occur. Only the m. biceps brachii could flex the arm–forearm when
the humerus folds over the body, and its flexion does not reach the
maximum. However, the mm. scapulotriceps and humerotriceps could
participate in a small extension of the arm–forearm during full
abduction of the arm.
When flexing/extending the arm–forearm, the manus does not
perform substantial movements of flexion/extension, respectively,
keeping an almost permanent perpendicular position with respect to
the forearm. When the forearm was fully extended, the manus
restricted its flexion angle but increased its extension angle. These
changes can be explained by the shape of the wrist joint itself, tendon
and muscle action, which generate a smaller amplitude than when the
forearm is flexed (see Figure 24c).
4 | DISC US SION
4.1 | Comparison of the pectoral girdle and wing
osteology
The pectoral girdle of R. americana shares with others flightless
paleognath birds (Struthio, Casuarius, Dromaius, and Apteryx), non‐
avian theropods, and early birds a fused scapulo‐coracoid
(Feduccia, 1986; Lowe, 1928; Wang et al., 2018) and an obtuse
angle between the main shafts of coracoid and scapula (e.g., ~130° in
R. americana, Figure 4d; Agnolín et al., 2019; Feduccia, 1986; Novas
et al., 2021; Olson, 1973). Both features distinguish the pectoral
girdle of flightless paleognaths from that of the tinamids and
neognaths, which present an articulated scapulo‐coracoid and acute
ET AL.
F I G U R E 24 Rhea americana albescens,
maximum range of movements of the right
wing. Maximum range of craniolateral‐
caudomedial arc of the right humerus in dorsal
(a) view. Maximum range of elevation‐
depression of the right humerus in total
extension in cranial (b) view. Maximum range
of extension‐flexion of the right forearm and
manus in cranial (c) view. Scale bar: 3 cm.
angle between these elements (e.g., ~50° in Vultur gryphus, Figure 4e;
see Novas et al., 2021).
The pectoral girdle of Rhea, Struthio, and Apteryx lacks a clavicle
or furcula, different from adult specimens of Dromaius and embryonic
Casuarius, which exhibit two rudimentary “clavicles” (Lowe, 1928;
Pycraft, 1900), and from tinamids and neognaths that show a well‐
developed furcula.
As in other paleognaths and neognaths, R. americana has a strut‐
like coracoid. The main characteristic of this element is the low and
bump‐shaped acrocoracoid process. Unlike the strong dorsocranial
and medial projections of the acrocoracoid process observed in
tinamids and neognath birds, in R. americana this process is
cranioventrally located with respect to the glenoid fossa. This
condition is also shared with Struthio, Casuarius, Dromaius,
and Apteryx, basal paravians and early birds (e.g., Archaeopteryx,
Buitreraptor, Sapeornis, and Confuciusornis; Novas et al., 2021).
The proximity between the acrocoracoid process and the glenoid
fossa in R. americana bounds an elongated subtriangular‐shaped
subglenoid fossa, as seen in other flightless paleognaths. This
condition does not occur in tinamids and neognath birds, but it is
present in basal paravians (e.g., Buitreraptor, Sapeornis, Confuciusornis,
Archaeopteryx, and Anchiornis; Novas et al., 2021).
The lateral and medial border of the coracoid has strong tendinous
structures (Figure 15c,d). The medial one is the coracoid membrane
(com; see Figures 3a, 15d, 16a; Fürbringer, 1888), which delimits the
foramen nervi supracoracoidei. Considering that R. americana lacks a
furcula, this membrane would be homologous to the sternocoracocla-
vicularis membrane, which is present in neognath birds and is located
between the medial margin of the coracoid and the lateral surface of
the furcula (Baumel et al., 1993; Livezey & Zusi, 2007).
LO COCO ET AL.
The scapular blade of R. americana presents a curvature that
results in that the distal end of the bone orientates subparallel to the
main axis of the vertebral column (see Figures 2b and 4c). This strong
curvature is exclusive to R. americana, whereas other non‐tinamid
paleognaths present a shallow curvature (Struthio and Apteryx) or
show a nearly straight blade (Casuariiformes).
The acromion process is located in the center of the cranial
surface of the scapulocoracoid as occurs in Struthio, Casuarius,
Dromaius, and Apteryx. However, R. americana is unique in that the
acromion process is more prominent and bulk‐shaped and it is
oriented laterocranially. This is not observed either in extant tinamids
and neognaths in which it has a cranial or craniomedial prolongation
of the dorsal edge of the scapular blade. The same is true for basal
paravians and basal birds (e.g., Buitreraptor, Sapeornis, Confuciusornis,
Archaeopteryx, and Anchiornis) in which the acromion process projects
cranially or craniomedially (Novas et al., 2021).
The position and shape of the acromion and acrocoracoid
processes in R. americana result in a concave surface or coracoid
sulcus on the cranial surface of coracoid, forming the sulcus
supracoracoideus or supracoracoidal canal (Figure 3b), which is deeper
than in other extant flightless paleognaths. This canal delimits the
passage of the m. supracoracoideus. In all extant flightless paleognaths
the supracoracoidal canal is oriented cranially as occurs in basal
paravians and basal birds (Novas et al., 2021) and contrary to that
observed in volant birds, which present a medial orientation due to
the great development of the acrocoracoid process.
Although flightless paleognaths does not show a complete
triosseal canal, the lig. acrocoracoacromialis present in R. americana,
join the acrocoracoid and acromion processes and providing a roof
for the m. supracoracoideus (Novas et al., 2021).
In R. americana and extant flightless paleognaths, the glenoid
fossa is oriented mostly in lateral or laterocaudal direction, and its
main axis is dorsocaudally oriented (e.g., ~34° in R. americana,
Figure 4d; Agnolín et al., 2019; Feduccia, 1986; Novas
et al., 2020, 2021). In contrast, in tinamids and neognath volant
birds the glenoid fossa is almost cranio‐caudally inclined and oriented
mostly in lateral or laterodorsal direction (e.g., ~70° in V. gryphus,
Figure 4e; Agnolín et al., 2019; Gatesy & Baier, 2005; Jenkins, 1993;
Novas et al., 2020, 2021). This allows the characteristic and complex
dorso‐ventral arch movements of the humerus. The shape and
inclination of Rhea glenoid fossa is similar to that of basal paravians
and basal birds (e.g., Buitreraptor, Saurornitholestes, Sapeornis, Con-
fuciusornis, Archaeopteryx, and Anchiornis; Novas et al., 2020, 2021).
In sum, the osteology of pectoral girdle and wing in R. americana
and other flightless paleognaths, shows muscle points of origin,
trajectories, force vectors, and humerus articulation that differ
distinctly from those of flying birds and, consequently, result in
different wing movements.
The sternum of R. americana has a prominent processus
craniolateralis sterni being proportionally larger than in other non‐
tinamid paleognaths with the exception of Dromaius (e.g., Struthio;
Livezey & Zusi, 2007). Other interesting characters are the lack of
sternal keel, fenestrae, trabeculae, foramina, rostrum sterni and
| 23
intermuscular lines; all these features are present in tinamids and
neognath birds (Baumel et al., 1993). In some flightless paleognaths,
like Struthio and Apteryx, the trabeculae are present.
The wings of R. americana has all bony elements (Figure 1b),
similar to Struthio, tinamids and neognath volant birds, whereas in
other non‐tinamid paleognath (Cho et al., 1984) like Casuariiformes
(Maxwell & Larsson, 2007), Apteryx (McGowan, 1982), Dinornithi-
formes and Aepyornithiformes (Worthy & Scofield, 2012), the wing
elements are reduced or some are missing.
The humerus of Rhea is longer than the forearm, the manus, and
the femur, as observed in Struthio, and contrary to what we observed
in Dromaius, Casuarius, and Apteryx. The humerus of R. americana and
other flightless paleognaths, shows a poorly developed deltopectoral
crest and a bicipital crest, being less prominent than in volant birds.
The reduction of the deltopectoral crest is probably correlated to the
low muscle volume, and therefore, the smaller force generated by the
mm. pectoralis p. thoracica and supracoracoideus. In this way, it is
probably correlated to the loss of flight.
In volant birds, the large deltopectoral crest provides a wide area
for the insertion of the mm. pectoralis p. thoracica, supracoracoideus,
and deltoideus major. In basal paravians the development of the
deltopectoral crest (and the corresponding muscle development)
could be correlated with strong‐arm movements probably related to
capture preys (e.g., Bambiraptor, Deinonychus) or flapping ability (e.g.,
Archaeopteryx, Confuciusornis; Chiappe et al., 1999; Senter, 2006).
The bicipital crest of volant birds provides large areas for the origin of
m. biceps brachii (on its cranial surface), and insertion of the m.
scapulohumeralis p. caudalis (on its caudal surface) which are also
lacking in R. americana. The humerus of Rhea lacks the pneumo-
tricipital fossa, as occurs in Struthio and Apteryx, but differing from
Casuariiformes and several volant birds (Bledsoe, 1988;
Mindell, 1997).
As in flying birds, the tuberculum ventrale of the humerus is
prominent in R. americana. In neognaths, it constitutes the site of
insertion of the mm. subscapularis, subcoracoideus and coracobrachialis
p. caudalis (Raikow, 1985; Woolley, 2000). However, in R. americana,
contrasting with volant birds it is not caudoventrally oriented. As
pointed out by Chiappe (1996) and Woolley (2000), the development
and caudoventral orientation of the tuberculum ventrale of the
humerus are associated with keeled sternum and the antagonic
function of the mm. coracobrachialis p. caudalis and pectoralis p.
thoracica in Enantiornithes and Ornithurae.
In R. americana and Struthio, the corpus humeri has two distinctive
caudal ridges: one is the site of insertion of the m. latissimus dorsi p.
cranialis and the second one is a crest left by the m. humerotriceps.
Only the m. latissimus dorsi p. cranialis crest is observed in Casuarius
and some neognaths, while in other extant flightless paleognaths
(e.g., Dromaius and Apteryx) none of these ridges are present. In basal
paravians, the site of insertion of these muscles can be referred to as
a groove close to the base of the deltopectoral crest (e.g.,
Deinonychus, Buitreraptor, and Archaeopteryx) indicating that the
mm. latissimus dorsi p. cranialis and humerotriceps were proportionally
small in basal paravians (Jasinoski et al., 2006).
24 | LO COCO
The shape and inclination of the condylus dorsalis and ventralis of
Rhea are similar to those of tinamids and neognaths. While the
incisura intercondylaris present in the aforementioned birds is absent
in Apteryx and Aepyornis.
In R. americana, the epicondyles of the distal end of the humerus,
as well as the processus supracondylaris dorsalis, and the fossa
brachialis, are less developed than in tinamids and neognaths. In
contrast, the processus flexorius is extended distally and slightly
ventrally, resulting in an oblique inclination of the condyles, differing
from other non‐tinamid paleognaths (Figure 6). These features are
variously observed among basal birds, neognaths and paleognaths.
The humerus of R. americana and Struthio exhibits a longitudinal
pronator torsion (e.g., the epicondylus dorsalis of the distal end is
craniodorsally inclined). As was mentioned above, the direction and
range of twist of the humerus results in that the major axis of the
distal end (major axis along the condyles), is positioned almost
perpendicular to the dorso‐ventral axis in full abduction (Figure 7b).
This morphology is observed in Rhea and Struthio, which contributes
to explain the distinctive inverted L‐shaped wing posture (Figure 1a).
This marked torsion is not observed in Casuarius and Dromaius.
Apteryx shows high variability in the humerus shape and therefore its
torsion is uncertain. As mentioned by Fürbringer (1888) and Baumel
et al. (1993) for volant neognaths, and as is also present in tinamids,
the main axis of the caput humeri and the distal condyles of the
humerus remain subparallel, thus indicating that they lack longitudi-
nally twist. This arrangement contributes to the fact that these birds
have a ventral orientation of the inner wing surface when the
humerus is fully extended.
The ulna of Rhea and other flightless paleognaths has a unique
surface to receive the humerus, the cotyla humeralis, unlike the two
cotyla (i.e., dorsalis and ventralis) present in neognath birds (Baumel
et al., 1993). The cotyla humeralis of flightless paleognaths might be
homologous to the cotyla ventralis of the neognath birds. In R.
americana, the cotyla humeralis articulates with the condylus ventralis
of the humerus, while in neognaths, the cotyla dorsalis articulates with
condylus dorsalis of the humerus and the cotyla ventralis articulates
with the condylus ventralis of the humerus (Baumel et al., 1993;
Vazquez, 1994).
The quill knobs present in volant neognath birds and some
extinct theropods (Forster et al., 1998; Turner et al., 2007) are not
present in R. americana. As was mentioned by Baumel et al. (1993)
and Livezey and Zusi (2007), in neognath birds these quill knobs are
the site of insertion of the ligaments of the follicles of the secondary
flight feathers. Although the feathers of Rhea are simplified, they
have a well‐developed calamus, therefore, the lack of quills seems to
be related to the active function of the ligaments of the follicles
during synchronous secondary flight feathers movement.
In the distal end of the ulna, the condylus metacarpalis of R.
americana is slightly concave distally, as opposed to the convex shape
that present neognath birds (Baumel et al., 1993; Vazquez, 1992) and
tinamids, resulting in a different articulation between the forearm and
the manus. In turn, the ulna of R. americana does not present the
convex and inclined articular dorsal ridge that Vazquez (1992)
ET AL.
described for neognaths, and therefore, the os carpi ulnaris cannot
slide over it in proximal direction. As was mentioned by
Vazquez (1992, 1994), the function of this articular edge in flying
neognath birds is to allow hyperflexion of the manus and avoid
dislocation of the wrist during downstroke (when the bird's wing
receives greater force in the ventro‐dorsal direction). In R. americana,
this last function ceased to be fundamentally necessary.
In volant birds, this wrist joint allows two essential characteristics
in the performance of active flapping flight: a greater flexion and
ability of circumduction of the manus (see Vazquez, 1992). The
anatomical features observed in the ulna of R. americana do not allow
the circumduction movement that volant neognath birds present, and
therefore, wing folding is different in both groups of birds. These
anatomical features of the wrist are also observed in Struthio, as was
observed by Hutson and Hutson (2014), indicating that the lack of
circumduction movement could be a widespread condition among
non‐tinamid paleognaths as well.
The os carpi radialis in R. americana is larger than the os carpi
ulnaris, in contrast to neognath birds in which it is shorter. The os
carpi ulnaris articulates with the radius, ulna and carpometacarpus,
allowing movements in the cranio‐caudal plane and avoiding dorso‐
ventral movements, as occurs in tinamids and neognath birds. The os
carpi radialis of R. americana do not wrap distally and cranially the
distal tip of the radius because the articular surface for the radius is a
cranially opened concavity. In contrast, in neognath birds, the os carpi
radialis covers the distal tip of the radius. In addition, it should be
noted that the area of articulation with the ulna in R. americana is
proportionally larger than that described by Vazquez (1992) for
neognath birds. This difference results in changes during the
automatic folding movement in paleognaths and neognaths.
In Rhea, the os carpi ulnaris has a subtriangular‐shape and is
located at the ventral surface of the carpometacarpus, articulating
with the ulna and carpometacarpus, as described by Suzuki et al.
(2014) for the tinamid Eudromia elegans. We observed that the os
carpi ulnaris maintains a ventral position on the wrist, prevents
ventral movements of the manus and limits its flexion in Rhea. In
contrast, the os carpi ulnaris of neognath birds has a “U”‐shape and
wraps the carpometacarpus, participating in the hyperflexion of the
manus and the consequent circumduction (Vazquez, 1992). There-
fore, the os carpi ulnaris of Rhea would not participate in the
movement of the manus in the same way that Vazquez (1994)
described for neognath birds.
The general shape of the carpometacarpus of the Greater Rhea is
similar to that of Struthio, tinamids and neognath birds in having
elongate and fused metacarpal II and III, separated by an inter-
metacarpal space. This is different from Casuarius, Dromaius, and
Apteryx (Lowe, 1928; Maxwell & Larsson, 2007), in which the
metacarpals are completely fused and with a narrow (some
specimens of Casuarius) or absent intermetacarpal space (Dromaius,
Apteryx and some specimens of Casuarius).
One of the most striking features of the carpometacarpus of R.
americana and other non‐volant paleognaths is the poor development
of the processus extensorius and the lack of the pisiform process. Both
LO COCO ET AL.
extensorius and pisiform processes are absent in non‐avian paravians
(such as Deinonychus, Buitreraptor; Novas et al., 2018; Ostrom, 1969)
and basal birds including Sapeornis and Confuciusornis (Chiappe
et al., 1999; Zhou & Zhang, 2003). These may be correlated to the
reduction of the force of the muscles that are attached in these areas
(mm. extensor carpi radialis, extensor longus alulae, and abductor digiti
majoris) and could be a key trait that explains the lack of automatic
wing folding in R. americana.
The proximo‐distal torsion of the carpometacarpus observed in
R. americana (e.g., ~68°) is more pronounced than in Struthio and
Dromaius, Most neognaths and tinamids present a lower cranial to
dorsal torsion (e.g., ~48° in Bubo virginianus). In this way, when the
manus of Rhea is fully extended, the plane of the wing surface of the
manus is almost perpendicular to the plane of the forearm, in
contrast to what occurs in extant volant birds where the manus is
held in the same plane as the forearm and the wing surface remains
in the same plane.
4.2 | Comparison of the pectoral girdle and wing
myology
R. americana and other non‐volant paleognaths are cursorial forms
with reduced wings that greatly modified their musculature (volume,
area of origin, and/or insertion), differentiating them from their flying
ancestors (for more details see Sackton et al., 2019; Yonezawa
et al., 2017).
The musculature associated with the patagium (mm. pectoralis
propatagialis and deltoideus propatagialis), and several muscles of the
pectoral girdle (mm. deltoideus minor, coracobrachialis p. caudalis and
serratus superficialis p. metapagialis) and of the forearm/manus (mm.
flexor digitorum superficialis, entepicondylo‐ulnaris, extensor digitorum
communis, and extensor longus digiti majoris p. proximalis) are absent in
R. americana (Fürbringer, 1888; Haughton, 1864; Lowe, 1928;
Pycraft, 1900). In contrast with Suzuki et al. (2014), the m.
entepicondylo‐ulnaris was not found in any specimens of R. americana
studied here.
These nine muscles are also absent in other flightless paleog-
naths (Struthio, Casuarius, Dromaius, and Apteryx; see Beddard, 1898;
Jasinoski et al., 2006; Maxwell & Larsson, 2007; McGowan, 1982)
and all of them are also present in tinamous (Hudson et al., 1972;
Suzuki et al., 2014).
4.2.1 | Topographic anatomy of muscles
In Rhea, the site of origin of the m. latissimus dorsi p. caudalis is more
caudal than Struthio, tinamids and neognath birds, which may
generate a caudal movement of the humerus. This action differs
from the caudo‐dorsal movement indicated by Raikow (1969) for
flying birds.
The m. rhomboideus superficialis in Rhea does not overlap the m.
rhomboideus profundus, like Struthio (Jasinoski et al., 2006), and both
| 25
muscles have smaller origin area than neognath birds (Baumel
et al., 1993) in which the m. rhomboideus superficialis overlap the m.
rhomboideus profundus. According to Pycraft (1900), the m. rhomboi-
deus superficialis in Rhea and Struthio arises as in neognath birds, but
its insertion is more extensive than tinamids and neognaths, reaching
the omal end of the scapula, the procoracoid, and the coracoid
membrane (Figure 16a, c). The m. rhomboideus profundus is associated
with the two cranial layers of the m. serratus profundus close to the
scapular blade, similar to the condition described by Beddard (1898)
for Casuarius, and its insertion area is wider than that of neognaths
and other paleognath birds.
In tinamids and volant neognath birds the m. pectoralis has a
larger volume and origin than the m. supracoracoideus, which overlaps
(Baumel et al., 1993); however, in R. americana, the m. pectoralis has a
smaller volume and a smaller origin area than the m. supracoracoideus,
and they do not overlap (Figure 12).
The m. pectoralis has only one belly, the p. thoracica, in contrast
to the two bellies that Jasinoski et al. (2006) described for Struthio. In
agreement with Lowe (1928), no individual was observed to have an
origin on the sternum and on the ribs, as seen in the neognath birds
(Baumel et al., 1993; Lo Coco et al., 2020).
The site and the small origin area of mm. pectoralis p. thoracica
and supracoracoideus observed in Rhea and Struthio (Jasinoski
et al., 2006), when compared with those of tinamids (Suzuki
et al., 2014) and neognaths (Baumel et al., 1993), indicate that in
non‐volant paleognaths these muscles are not as predominant in
wing movement as they are in volant birds. Further, the main elevator
muscles in R. americana are the mm. deltoides major and latissimus
dorsi p. cranialis, whereas the m. supracoracoideus and the m.
latissimus dorsi p. caudalis do not have an important role as a
humerus/wing elevator. In neognaths and tinamids, the m. supracor-
acoideus is the main elevator muscle.
It is interesting to note that the coracoid membrane of R.
americana increases the area of origin for the m. supracoracoideus, a
similar situation to that observed in volant birds since the m.
pectoralis p. thoracica originates in an important area of the
sternocoracoclavicular membrane, which connects the coracoid with
a well‐developed furcula (Olson & Feduccia, 1979). Mayr (2017)
analyzed the development of the m. supracoracoid along the early
evolution of birds indicating that the main origin of this muscle
shifted from the coracoid onto the sternum. Nevertheless, the m.
supracoracoideus of R. americana originates on the coracoid bone but
also on this membrane. Therefore should be considered when
studying the origin and evolution of this muscle in basal birds,
because it is possible that the development of the membrane has
allowed to increase the origin area and, consequently, in the size and
volume of this muscle.
While the site and the insertion area of the m. supracoracoideus
do not vary among paleognaths and neognaths, the m. pectoralis p.
thoracica of the Greater Rhea has another site of insertion on the
crista bicipitalis. This double insertion allows a unified movement of
the humerus and avoids the pronounced pronation that performs
tinamids and volant neognaths.
26 | LO COCO
The m. biceps brachii in R. americana has a tendinous origin in the
acrocoracoid process like all birds (Baumel et al., 1993; Livezey &
Zusi, 2007), but has another belly that originates along the lateral
edge of the coracoid, and contributes to the cranioventral movement
of the humerus, as was mentioned by Lowe (1928). As described for
Struthio (Jasinoski et al., 2006), in Rhea the m. biceps brachii does not
have a second joint at the proximal end of the humerus, in contrast to
tinamids (Hudson et al., 1972) and some neognaths (Baumel
et al., 1993; Jasinoski et al., 2006; Lo Coco et al., 2020; Picasso &
Mosto, 2018).
As occurs in other birds, including Rhea and tinamids (Baumel
et al., 1993; Lo Coco et al., 2020; McGowan, 1982; Picasso &
Mosto, 2018), the m. biceps brachii has two sites of insertion. This
contrasts with Struthio in which only one insertion into the proximal
end of the radius was observed by Jasinoski et al. (2006).
The large development of the m. biceps brachii of R. americana as
well as the presence of an extra belly, confer on this muscle the main
function of flexing the forearm (as in Struthio, tinamids and
neognaths; Baumel et al., 1993; Jasinoski et al., 2006), as well as
abduction and protraction of the arm (Novas et al., 2021).
Unlike what Beddard (1898), Fürbringer (1902), and Jasinoski
et al. (2006) suggested for paleognaths, and particularly what Suzuki
et al. (2014) indicated for Rhea, we confirm the presence of the m.
scapulohumeralis p. cranialis in Greater Rhea (Figure 15b). This is
congruent with the presence of this muscle in Struthio (as indicated
by Suzuki et al., 2014). We propose that the absence of the m.
scapulohumeralis p. cranialis in Rhea suggested by Suzuki et al. (2014),
or its absence in Struthio as indicated by Jasinoski et al. (2006), may
be explained by the fact that: (1) this muscle was not observed
because it is small in comparison with m. scapulohumeralis p. caudalis;
(2) because it was fused with the m. scapulohumeralis p. caudalis; or
(3) this muscle was not fully developed in some individuals, assuming
that there is intraspecific variability or a probable gradual loss of this
muscle in these species.
In contrast to neognaths (Baumel et al., 1993; Lo Coco
et al., 2020) and tinamids (Suzuki et al., 2014), the m. scapulohumeralis
p. caudalis does not cover the entire lateral surface of the scapular
blade. Instead, it is confined to the ventral edge, as occurs in Struthio
(Jasinoski et al., 2006) leaving the major lateral surface of the scapular
blade free of muscle attachments (Figure 16a).
The m. subscapularis of Rhea is composed by a single belly, as was
also indicated by Beddard (1898), McGowan (1982), and Jasinoski
et al. (2006) for neognaths and Hudson et al. (1972) and Suzuki et al.
(2014) for tinamous. In Rhea, it occupies a large area on the caudal
surface of the scapula and coracoid, covering the caudal side of the
foramen nervi supracoracoidei, unlike what Jasinoski et al. (2006)
described for Struthio. The mass of the m. subscapularis is greater than
that of the m. subcoracoideus (muscle with adjacent insertion); thus it
might generate a greater force to move the humerus.
R. americana has a single belly of m. coracobrachialis, the p.
cranialis, as was indicated by McGowan (1982) and Jasinoski et al.
(2006) for Apteryx and Struthio, respectively. The m. coracobrachialis
p. cranialis of R. americana originates on the subglenoid fossa
ET AL.
(Novas et al., 2021), and lateral surface of the coracoid, as was
indicated by Jasinoski et al. (2006) for Struthio and Maxwell and
Larsson (2007) for Dromaius. However, in neognath birds and
tinamous the m. coracobrachialis p. cranialis originates on the top of
the well‐developed acrocoracoid process. This differentiation of the
origin among flying birds and flightless paleognaths suggests a
different function in each group. In R. americana and allies, the
function of this muscle is to protract and depress the humerus while
in flying birds the m. coracobrachialis p. cranialis extends cranially the
humerus (Novas et al., 2021).
In R. americana, the m. extensor carpi radialis is constituted by a
single belly, as Hudson et al. (1972) and Suzuki et al. (2014) described
for tinamids and unlike that Baumel et al. (1993) indicated for
neognath birds. The most notable difference with extant volant birds
is observed on the wrist, where the tendon passes through a dorso‐
cranial cartilaginous channel, cranially to the os carpi radialis and
becomes ventral. In Rhea, the insertion of the m. extensor carpi radialis
turns ventrad to insert via two tendons onto the ventral surface of
the processus extensorius and the proximoventral side of the spatium
intermetacarpale (Figure 22b), whereas in tinamids the insertion
occurs on the dorsal surface of the proximal end of the phalanx digiti
alulae (Suzuki et al., 2014), and in neognaths it occurs in the processus
extensorius (Baumel et al., 1993). The condition in R. americana allows
it to generate mainly the extension and supination of the manus, as
well as a slightly dorsal movement of the forearm.
In Rhea, the mm. pronator profundus and pronator superficialis
cannot be separated and share the same origin and insertion. The
area of insertion of both pronator muscles in Rhea is larger than that
of neognaths (Lo Coco et al., 2020) and tinamids (Suzuki et al., 2014),
which would imply a greater participation in forearm flexion. The m.
ectepicondylo‐ulnaris presents a greater area of insertion in the ulna
than tinamids and neognaths, which could imply greater power in the
flexion movement of the forearm.
The m. flexor carpi ulnaris of Greater Rhea has the particularity of
having three different areas of origin, one at the end of the humerus
like the tinamids (Suzuki et al., 2014) and neognaths (Baumel
et al., 1993; Lo Coco et al., 2020), and the other two origins on the
proximal end of the ventral surface of the ulna, one is tendinous and
the other has an aponeurotic origin. An outstanding feature is that
this muscle divides into two bellies in the distal third of the ulna
(Lowe, 1928), unlike the single belly present in Apteryx
(McGowan, 1982), and tinamids (Suzuki et al., 2014). One belly
inserted tendinous into the os carpi ulnaris, as was described for
neognath birds (Lo Coco et al., 2020; Picasso & Mosto, 2018) and the
other is associated with the skin of the caudal border of the manus
(Figure 21b) and, therefore, with the primary remiges (Baumel
et al., 1993).
The m. extensor longus alulae has a broad origin in the internal
border of the radius and the ulna, greater than that described for
tinamids (Suzuki et al., 2014) and for neognath birds (Lo Coco
et al., 2020; Picasso & Mosto, 2018). It is inserted in the reduced
processus extensorius of the carpometacarpus like neognaths (Lo Coco
et al., 2020; Picasso & Mosto, 2018), differing from the insertion into
LO COCO ET AL.
the proximal end of the alula that was indicated by Suzuki et al.
(2014) for tinamids.
The origin of m. flexor digitorum profundus of Rhea is located more
distally on the ulna than described for tinamous (see Suzuki
et al., 2014) and neognaths (see Lo Coco et al., 2020; Picasso &
Mosto, 2018). This position of the origin might result in less muscle
strength and less tendon excursion. It is important to mention that in
Rhea, the tendons of m. flexor digitorum profundus are not calcified as
occurs in other neognath birds (Lo Coco et al., 2020; Picasso &
Mosto, 2018). These tendons pass ventrally through a cartilaginous
channel, in the wrist area, the only place where it pivots, due to the
absence of the pisiform process. This feature does not generate the
same manus flexion that occurs in flying birds.
The origin of the m. ulnometacarpalis ventralis of Rhea covers a
smaller and more distally located area than that described for
neognath birds (Baumel et al., 1993; Lo Coco et al., 2020; Picasso &
Mosto, 2018). In both groups, the tendon of this muscle passes
through the juncturae carpi and inserts dorsally at the proximal end of
the carpometacarpus.
In the Greater Rhea, the mm. abductor alulae and flexor alulae
originate on the cranial border and ventral surface of the proximal
end of the carpometacarpus, in a larger area than that observed in
tinamids (Suzuki et al., 2014) and neognaths (Lo Coco et al., 2020;
Picasso & Mosto, 2018), probably due to the relatively larger size of
the digiti alulae and to the lack of the pisiform process.
As was mentioned above, the single belly of the m. extensor
longus digiti majoris in Rhea is the p. distalis, which is different from
tinamids (Suzuki et al., 2014) and neognath birds, where both bellies,
i.e., the p. cranialis and distalis (Baumel et al., 1993; Lo Coco
et al., 2020; Picasso & Mosto, 2018), are present. It is interesting that
in Rhea, the origin area covers the dorsal surface of the os
metacarpale majus and is greater than in tinamids and neognaths,
where this surface, does not present any muscular attachment
(Baumel et al., 1993; Lo Coco et al., 2020; Picasso & Mosto, 2018).
The m. abductor digiti majoris, of Greater Rhea, has a broad origin
on the ventral side of the os metacarpale majus, as occurs in tinamids
(Hudson et al., 1972; Suzuki et al., 2014) unlike what other authors
indicated for neognaths (Lo Coco et al., 2020; Picasso &
Mosto, 2018).
The two interosseous muscles together (m. interosseus dorsalis
and m. interosseus ventralis) occupy all the spatium intermetacarpale,
similar to what Suzuki et al. (2014) indicates for tinamids. In contrast
to other birds (Lo Coco et al., 2020; Picasso & Mosto, 2018; Suzuki
et al., 2014), the m. interosseus ventralis does not originate on the
proximal margin of the spatium intermetacarpale, only it does on the
distal margins.
4.3 | Muscle mass
The Greater Rhea, as a specialized runner and large paleognath
flightless bird, has reduced and light wing muscles in comparison with
leg musculature. The total wing muscle mass with respect to the
| 27
BM does not reach 1% (Table 1), in contrast to what occurs in flying
birds (e.g., ~10% in Polyborinae and Tyto furcata; see Lo Coco
et al., 2020; Picasso & Mosto, 2018). Although R. americana does not
employ its wings in an active locomotor function, the muscle mass is
particularly relevant for understanding its wing movements, consid-
ering that the mass of a muscle is related to its force capacity, as in
flying birds (Biewener & Roberts, 2000; Roberts, 2001).
The module of the pectoral girdle and proximal humerus has the
highest percentage of the wing musculature (82.18% WM), followed
by the module of distal humerus and forearm (15.92% WM) and distal
forearm and manus (1.90% WM), maintaining the same order of
importance of each module as also observed in volant birds (Lo Coco
et al., 2020; Picasso & Mosto, 2018). However, the mass percentage
of the pectoral girdle of Rhea presents a lower percentage than that
described for volant birds (e.g., Polyborinae, Tyto furcata; Lo Coco
et al., 2020; Picasso & Mosto, 2018), and on the contrary, the mass
percentage of the forearm and manus present higher values inRhea
than in these volant birds (Table 2). This is mainly due to the lower
percentage of the WM of them. pectoralis p. thoracica in Rhea, as
opposed to more than 50% of the WM in flying neognaths
(Supporting Information: SI 3). Therefore, the m. pectoralis p.
thoracica of Rhea would not contribute as much to the %WM of
the pectoral module and causing the other two modules to increase
(see Supporting Information: SI 3).
The six muscles with largest mass were those associated with the
pectoral girdle and proximal humerus, which act in all basic
movements of the wing (protraction, retraction, abduction, and
adduction). The m. deltoideus major would act as a principal elevator,
the mm. supracoracoideus and pectoralis p. thoracica would act
principally as a protractor, while the mm. latissimus dorsi p. caudalis
and subscapularis would participate as a retractor of the humerus, and
the m. humerotriceps extend the forearm.
In contrast to volant birds, the mm. pectoralis p. thoracica and
supracoracoideus of R. americana have a smaller origin area and a
small mass. In R. americana, the m. pectoralis p. thoracica is not the
largest muscle, and this reveals that its role is less relevant than in
volant birds. In addition, the main function of the m. pectoralis p.
thoracica in the Greater Rhea is to protract the humerus and, when it
depresses it, it does not do so in the same way as volant birds
perform during flapping flight (Dial, 1992).
The m. pectoralis p. thoracica represents more than 50% of the
total wing muscle weight in neognaths (Lo Coco et al., 2020; Picasso
& Mosto, 2018) while in R. americana it has only 8.20% WM (see
Supporting Information: SI 3). Although the muscle mass of the m.
pectoralis p. thoracica is reduced, the percentage of the pectoral girdle
module and the proximal humerus of the wing musculature (82.18%
WM) remains similar to that of flying birds (84.79%–90.25% WM; see
Table 2). This is due to the fact that other muscles of the pectoral
girdle have greater relative size. For example, the m. deltoideus major
in some neognaths represents 4.71%–5.31% of the WM (Lo Coco
et al., 2020; Picasso & Mosto, 2018), while in R. americana it has
11.96% WM. This pattern is repeated with the mass of most of the
pectoral and wing muscles including the mm. supracoracoideus,
28 | LO COCO
subscapularis + subcoracoideus, rhomboideus superficialis + rhomboideus
profundus, as these are triple the value observed in flying birds.
Particularly, in R. americana, the m. supracoracoideus is larger and
heavier than the m. pectoralis p. thoracica, supporting greater
participation and strength in the movements of the humerus. We
would like to emphasize the cranioventral position of its origin with
respect to the glenoid fossa, the orientation of the supracoracoidal
canal and, therefore, the force vector exerted by the tendon of the m.
supracoracoideus, allows its function to be that of protraction. The m.
supracoracoideus of R. americana does not generate the elevation or
supination of the humerus that was described by Dial (1992) and
Poore et al. (1997) for flying birds during the upstroke.
The muscles of the distal humerus and forearm, that is, the mm.
flexor carpi ulnaris, extensor carpi radialis, and extensor longus alulae are
the largest muscles like in volant birds (Lo Coco et al., 2020; Picasso
& Mosto, 2018). The function of the m. flexor carpi ulnaris is to flex
the carpometacarpus while the latter two muscles extend and slightly
supinate the manus.
On the distal forearm and manus, the m. ulnometacarpalis dorsalis
is the largest muscle like in volant birds (Dial, 1992; Lo Coco
et al., 2020; Picasso & Mosto, 2018). This muscle acts as a flexor of
the carpometacarpus.
The relatively high percentage of muscle mass of the forearm
and, in particular, of the manus could be related to the fleshy shape of
the muscles and, ultimately, to the low specialization of movement by
tendons and pulleys as observed in flying birds.
4.4 | Wing movements
The Greater Rhea has a characteristic posture and distinctive way of
moving its wings, similar to Struthio but markedly different from
those of flying birds (Novas et al., 2020). The characteristic flapping
cycle of different volant birds (Baier et al., 2013; Dial et al., 1991;
Dial, 1992; Gatesy & Baier, 2005; Heers et al., 2016; Tobalske
et al., 2007), is not performed by living Rhea and Struthio individuals
(Cho et al., 1984; Gasparri, 2016; Muñíz, 1885; Novas et al., 2020)
nor during the manipulation of the cadaveric specimens of Rhea.
When the wings of R. americana are extended, they assume an
inverted L‐shape and their inner surface faces caudally
(Raikow, 1968), similar to Struthio. This is in clear contrast to tinamids
and neognaths, in which the inner wing surface faces ventrally when
they fully extend their wings during different behaviors (e.g., flapping
flight, soaring, and gliding; see Poore et al., 1997). In the Greater
Rhea, the common wing movement is a craniolateral‐caudomedial arc
with the inner surface oriented caudally, as does the Ostrich, a
movement that is generally executed asynchronously and asymme-
trically, especially during its zigzag running (Gasparri, 2016;
Muñíz, 1885; Novas et al., 2020).
R. americana is also unable to carry out the Wing Assisted Incline
Running (WAIR; Novas et al., 2020), that is, the wings do not
cooperate aerodynamically with the hindlimbs to ascend inclined
ET AL.
planes, they only extend laterally and separately, as a reflex action or
to stabilize the body (Novas et al., 2020).
Manipulation of R. americana cadaveric specimens indicates that
the range of movements of the humerus is ample (Figure 23) and
wider in cranio‐caudal plane (dorsal view) than that exhibited by
flying birds such as neognaths (e.g., Gallus gallus domesticus, Tyto
furcata) and tinamous (e.g., Nothoprocta cinerascens). Accordingly, the
trajectory of the Rhea elbow during its usual wing movements
(Figure 23) is markedly different from that exhibited by extant volant
birds during flapping flight, as was described by Dial (1992), Poore
et al. (1997), Gatesy and Baier (2005), Heers et al. (2016), among
other authors.
The movement of the humerus may be explained by the
inclination of the ovoidal and cup‐shaped glenoid fossa (Agnolín
et al., 2019; Novas et al., 2020). The shape of the glenoid fossa of R.
americana and flightless paleognaths prevents the dorso‐ventral
movements of the humerus performed by volant birds (see Poore
et al., 1997). In addition, the origin of the three relevant muscles (mm.
pectoralis p. thoracic, supracoracoideus, and coracobrachialis p.
cranialis) is cranioventral to the glenoid fossa. The absence of a
well‐developed acrocoracoid process, of the triosseal canal and the
particular origin and insertion of these muscles, allows them to
generate mainly a protractive action (Novas et al., 2021). In turn, the
m. pectoralis p. thoracica in Rhea has a %WM significantly lower than
those of flying birds while the mm. supracoracoideus and coracobra-
chialis p. cranialis have a %WM higher than those of flying birds (see
Supporting Information: SI 3). Thus, the m. supracoracoideus mainly
protrudes the humerus and the m. pectoralis p. thoracica protracts and
abducts the wing. Finally, the m. supracoracoideus does not markedly
rotate the humerus when it is manipulated and thus does not
generate a change in orientation of the inner wing surface that flying
birds perform during upstroke. Moreover, the origin of the m.
latissimus dorsi p. caudalis and its muscle mass suggest the relevance
of this muscle for humeral retraction.
All these osteological and myological traits present in the
scapular girdle and wing of R. americana explain the wide
craniolateral‐caudomedial movement range and the lack of the
dorso‐ventral arm movement.
It is possible to infer that the humerus of “ratites” and also
probably non‐avian theropods (see Novas et al., 2020, 2021), may
have had more freedom of movement, and was less channeled than
those in tinamids and neognaths.
The articulation of the humerus and radius/ulna show some traits
that distinguish R. americana from neognaths. The proximal and distal
axis of articular surfaces of the humerus are sub‐perpendicular (e.g.,
~68°), and thus the distal end is cranioventrally oblique with respect
to the proximal one (Figure 7). This twist between the proximal
articulation with the distal one make, in lateral abduction of the
humerus, the forearm ventrally oriented. Thus, the palm of the manus
is oriented caudally caudoventrally. However, in neognaths, the
articular axis of the humeral head is subparallel with respect to the
main distal articular axis and thus, when the humerus is fully
LO COCO ET AL.
extended, the forearm directs cranially and with the palm of the
manus ventrally oriented.
The movements between the arm and forearm in Rhea (e.g., ~168°)
are wider than those described in Struthio (e.g., 98–149°; see Hutson &
Hutson, 2012 and in neognaths and tinamids (e.g., ~125°; see
Vazquez, 1994). This could be explained by the fact that in maximum
flexion, the bulky muscles of the arm and forearm of flying birds touch
each other, avoiding a greater flexion (Vazquez, 1992), while Rhea does
not present such voluminous muscles in the arm and forearm. In turn,
during the maximum extension of the forearm in flying birds, there are
opposing forces generated by the presence of the propatagium and
associated muscles, while in Rhea, since there is no propatagium, these
forces are absent and do not prevent a wide extension.
When flexing/extending the forearm, the manus does not perform
substantial movements of flexion/extension, keeping an almost perma-
nent perpendicular position with respect to the forearm. The absence of
propatagium in Rhea causes the manus not to extend automatically
beyond 80° because in volant birds, the propatagium contributes to the
automatic extension of the manus during the extension of the forearm
(Vazquez, 1992). The lack of the propatagium and the lack of the
automatic wing folding mechanism in Rhea can be extrapolated to other
non‐volant paleognaths, like Struthio and Casuarius, because these species
have similar shoulder, elbow, and wrist joints, and also lack a propatagium.
Particularly, when the manus extends more than 80°, the palm
surface acquires a sub‐perpendicular position to the ventral surface
of the forearm. This position is mainly explained by the torsion of the
carpometacarpus, by the articulation with the ulna, and by the
supination function of the m. extensor carpi radialis. This differs from
that of volant birds, which maintain the same orientation between
the ventral surface of the forearm and the inner surface of the manus,
allowing the primary remiges feathers to be oriented caudally.
The circumduction of the manus performed by flying birds (see
Vazquez, 1994) is neither observed in living Rhea nor by manipulating
the fresh cadaveric specimens. This is explained by the fact that the
concave shape of the condylus metacarpalis of the ulna of Rhea
reduces the angle of movement of the manus, preventing its
hyperflexion. Likewise, Hutson and Hutson (2014) also pointed out
the bounded range of movement of the manus of Struthio.
With regard to the movements of the digits, the largest range of
movements is performed by the alular digit. In this case, between the
flexion and extension movements, 53° are reached with respect to
the axis formed by the os metacarpale majus, being similar to that
reported by Hutson and Hutson (2018) for Struthio (e.g., 15–66°).
The two phalanges of digit II mainly perform abduction–adduction
movements, while the phalanx of digit III has a low flexion and extension
capability. The movements of the phalanx digiti minoris are related with
the movements of the phalanx proximalis digiti majoris.
4.4.1 | Automatic wing folding
The modern flying birds have an efficient mechanism to perform
flapping flight: the automatic wing folding. This is a synchronic wing
| 29
movement in which the bird extends or flexes the forearm and manus
automatically due to the complementary action of tendons and
muscles, and particular osteological features present in the articula-
tion of the elbow and the wrist (see Vazquez, 1992, 1994). This
movement is important during flight because it coordinates the
upstroke and downstroke of the wing (Vazquez, 1992, 1994).
Manipulation of cadaveric R. americana, indicates that a complete
automatic wing folding is missing, probably because it lacks several of
the osteological and myological requirements as indicated by
Vazquez (1994).
Vazquez (1994) distinguishes two distinct joints between the
forearm and manus of neognath birds. The first one involves the
movement of the radius, os carpi ulnaris, os carpi radialis, and
the manus with respect to the ulna. The second one involves the
movement of the manus with respect to the ulna, radius, and both
carpals.
In neognaths, during the flexion of the forearm, the distal
displacement of the radius relative to the ulna pushes the os carpi
radialis distally which pushes the carpometacarpus and the os carpi
ulnaris caudally. During this displacement of the radius, the manus is
automatically flexed with respect to the ulna (Figure 25;
Vazquez, 1992, 1994). This is possible because during flexion of
the forearm, the dorsal condyle of the humerus pushes the radius
distally. The dorsal condyle is larger and cranially extended compared
to the ventral condyle, generating an unequal articulation with the
radius and ulna, respectively (Vazquez, 1992). R. americana has a
different condition, with the ventral condyle of the humerus being
larger than the dorsal one. Although this may indicate that the radius
cannot be displaced during the flexion of the forearm in Rhea, a slight
radius displacement occurs when the cadaveric specimen is manipu-
lated. Nevertheless, this radial displacement is minimal and notably
lower than in volant birds.
Additionally to the displacement of the radius, two morphological
traits in the wrist of neognaths are important to perform the
automatic wing folding: First, the os carpi radialis have a deep
proximal concavity for the articulation with the radius (see
Vazquez, 1992). This concavity overlaps the distal end of the radius
and articulates with it during all flexion and extension movements of
the wing (Figure 25). In R. americana, however, the os carpi radialis
have a cranial articular concavity that is only in contact with the
caudal surface of the distal end of the radius (Figure 25). Second, the
contact of articulation between the os carpi radialis and the ulna is
narrow in Rhea, while it is notably wider in neognaths (Vazquez, 1992;
Figure 25).
The second articulation or joint described by Vazquez (1994) is
made up exclusively by muscles, although some osteological traits are
also evidenced. Below, we discuss each muscular and osteological
trait involved in this articulation:
1. The propatagial tendons are important for the automatic exten-
sion of the manus in volant birds (Carpenter, 2002;
Vazquez, 1994). When the forearm is extended, these tendons
pull the wrist and extend the manus at the same time.
30 | LO COCO
The absence of the propatagium and associated muscles (mm.
pectoralis propatagialis and deltoideus propatagialis) in R. americana
is an important trait that supports the lack of automatic wing
folding.
2. During the flapping flight, the m. flexor carpi ulnaris of volant birds
plays an important role for the automatic flexion of the manus
(Carpenter, 2002; Vazquez, 1994). This muscle, complemented by
the action of the humeroulnar pulley of the ulna pulls proximally
the os carpi ulnaris of the wrist. Although in R. americana this
muscle shows some similarities with volant neognaths and
tinamids, it is notable that the m. flexor carpi ulnaris cannot
perform the automatic flexion of the wrist. It is possible that the
conformation of the forearm/wrist articulation is a limiting factor
for flexion of the manus, as was mentioned above. The shape and
the caudoventral position in the wrist joint (not caudally as in
neognaths) of the os carpi ulnaris and the concave facies articularis
ulnaris of the distal end of the ulna do not allow the hyperflexion
and the circumduction of the manus exhibited by neognaths.
3. The m. extensor carpi ulnaris (m. extensor metacarpi ulnaris, sensu
Vazquez, 1994) is a muscle that flexes the manus in neognaths
(although it derives from a extensor group of muscles, hence its
name; George & Berger, 1966). In R. americana, the m. extensor
carpi ulnaris originates from the dorsocaudal surface of the distal
end of the humerus, passes distally through a tendinous channel in
the wrist, and inserts dorsally in the processus intermetacarpale of
the carpometacarpus. The carpometacarpus is extended when
this muscle is contracted and, therefore, does not contribute to
ET AL.
F I G U R E 25 Movements of the right
manus of Rhea americana (a,b) and Tyto furcata
(c,d) during flexion (a,c) and extension (b,d).
Movements of the radius, os carpi radialis and
os carpi ulnaris are indicated in black arrow.
Movements of the carpometacarpus are
indicated in white arrow, and the gray arrow
shows the marked supination (b). Scale
bar: 3 cm.
automatic flexion of the manus, contrary to neognaths. This
movement is in concordance with that reported by Wustinger
et al. (2006) for Struthio and probably the same occurs in other
flightless paleognaths.
4. In neognaths, the m. extensor digitorum communis is an important
muscle that extends the manus with the extension of the elbow.
This muscle is absent in R. americana.
5. The m. extensor carpi radialis extends the carpometacarpus during
the forearm extension, during the transition of upstroke‐
downstroke movement of volant bird (Dial, 1992; Vazquez, 1994).
In Rhea, this muscle could extend and supinate the carpometa-
carpus, and is not clearly related to forearm extension.
These traits preclude the automatic wing folding and circumduc-
tion in the Greater Rhea. This is consistent with features of the
extensor and flexor muscles of the manus, which are more fleshy, less
tendinous, and have a relatively high percentage of the WM than
volant birds (in Rhea the forearm/manus muscles represent almost
2% of WM, while in raptors it is 0.60%–1.04% of WM; Table 2). This
high percentage of muscle mass in the manus of Rhea could be
related to the lack of tendon insertion that facilitates automatic
flexion/extension of the manus.
In summary, the osteological, myological, and experimental
observations on the wing of Rhea explain the lack of automatic wing
folding and lack of circumduction. Due to the similarities of the
pectoral girdle and wing morphology between Greater Rhea and
basal paravians, this information could be important to elucidate the
LO COCO ET AL.
arm movements and the capabilities of flight in basal birds and non‐
avian theropods.
Although there are no osseous features of the wing that might
infer wing folding movements in extinct taxa (nonavian paravians and
non‐Ornithothoraces Avialae), we believe that some osteological
features (e.g., humerus with a well‐developed condylus dorsalis more
proximally extended than the condylus ventralis; ulna and radius
subequal in length; well‐developed processus extensorius in the
carpometacarpus) are indicative of automatic flexion/extension
movements. In fossils where the presence of muscles and/or
ligaments forming the propatagium is observed, the idea of automatic
flexion/extension gains strong support (see Chimento et al., 2017).
5 | C ONC LUS I ON S
The present contribution provides detailed information about the
osteology, myology, and wing movements of the South American
paleognath R. americana. Forelimb anatomy shows several traits
shared with other flightless paleognaths as well as several unique
characters. We support here that the pectoral girdle of R. americana,
and other flightless paleognaths, share features with basal paravians
and basal birds, as was proposed by Feduccia (1986), Agnolín et al.
(2019), and Novas et al. (2021).
The obtuse angle formed between the scapula and coracoid, the
lack of triosseal canal, the shape and inclination of the major axis of
the glenoid fossa, the reduced size of the cristae deltopectoralis and
bicipitalis of the humerus, the proximo‐distal torsion of the humerus,
the presence of only one cotyla humeralis of the ulna, the concave
shape of the condylus metacarpalis of the ulna, the processus
extensorius reduced and the absence of the processus pisiformis of
the carpometacarpus, are some of the distinctive features of Greater
Rhea's pectoral girdle and wings. Similar features are shared with
flightless paleognaths (e.g., Struthio), non‐avian paravians (e.g.,
Buitreraptor), and basal birds (e.g., Archaeopteryx), being different
from the conditions present in flying neognath birds (e.g., G. gallus).
Dissection of R. americana specimens shows the lack of nine
muscles of the wing, including the propatagium, and the reduction in
size and mass of pectoral muscles. Further, the particular topography,
reduction of the origin area and %WM mass of the mm. pectoralis p.
thoracica, supracoracoideus, and coracobrachialis p. cranialis are
notably different from flying birds. These features probably are
related to the lack of flight capabilities in flightless paleognaths.
Manipulation of the wing of cadaveric specimens of Greater
Rhea shows a wide extension of the arm–forearm and an absence of
the automatic wing folding. This could be explained by the lack of the
propatagium, and associated muscles (e.g., mm. pectoralis propatagialis
and deltoideus propatagialis). Further, Greater Rhea is unable to
perform circumduction of the distal end of the wing. The particular
concave shape of the condylus metacarpalis and the osteological
conformation of the wrist of R. americana prevents the hyperflexion
of the manus, contrasting with volant birds.
| 31
The osteological and the myological analysis presented here are in
congruence with previous studies (Agnolín et al., 2019; Novas
et al., 2020, 2021) that describe the movement of the wing of R.
americana. The Greater Rhea does not flap the wings dorso‐ventrally
as typical for flying birds, but predominantly in cranio‐caudal direction,
following a craniolateral to caudomedial abduction–adduction arc.
When the wings are fully abducted, they are inverted L‐shaped, with
the inner surface caudally faced, and when the wings are folded
against the body, they do not perform the complete automatic wing
folding nor the circumduction of the manus, a movement performed
by extant volant birds.
This study complements our knowledge of the axial musculature
of the flightless paleognaths and highlights the use of the Greater
Rhea as a model, which may help in understanding the evolution of
Palaeognathae, as well as the origin of flapping flight among the
paravian theropods.
The novel information about flightless birds should be taken into
account, particularly when analyzing the movements of fossil basal
birds, non‐avian theropods, or Aves. Further, it sustains previous
claims that suggest that flightless birds may be more suitable for
understanding wing movements to basal birds and non‐avian
theropods than flying neognath birds.
ACKNOWLEDGME NT S
The authors thank Yolanda Davies (Ornithology curator, MACN) for
her help during the dissection of the specimens. The authors
acknowledge Darío Lijtmaer, Pablo Tubaro (Ornithology curators,
MACN), Joel L. Cracraft, and Paul Sweet (Ornithology curators,
AMNH) for the access to the collections under their care. Special
thanks to M. Alicia de la Colina and crew of Fundación Temaikèn, for
allowing access to study the behavior of several bird species. The
authors are deeply grateful to Marcelo Isasi, Mauro Aranciaga
Rolando, Sebastián Rozadilla, Jordi García Marsà, Mauricio Cerroni,
Federico Brissón Egli, Julia D'Angelo, Adriel Gentil, Santiago Miner,
Gerardo Álvarez‐Herrera, Germán Stoll, Ricardo Stoll, and Gonzalo
Muñóz, all from LACEV, for their help during the dissections, their
comments and fruitful discussion of the manuscript. The authors
acknowledge Clelia Mosto and Mariana Picasso for their suggestions
on methodology. Finally, the authors appreciate the improvements
for the English language carried out by Bruce Peterson through the
Association of Field Ornithologists program of editorial assistance.
DATA AVAILABILITY STATEMENT
Data available in article supplementary material special issue:
Muscles and bones: evolution, development, epigenetics, pathologies,
and variations edit.
ORC I D
Gastón E. Lo Coco https://orcid.org/0000-0002-9250-8746
Matías J. Motta https://orcid.org/0000-0002-5424-935X
Federico L. Agnolín https://orcid.org/0000-0001-5073-561X
Fernando E. Novas https://orcid.org/0000-0002-6901-8677
32 | LO COCO
REFERENCES
Agnolín, F. L., Motta, M. J., Brissón Egli, F., Lo Coco, G., & Novas, F. E.
(2019). Paravian phylogeny and the dinosaur‐bird transition: An
overview. Frontiers in Earth Science, 6, 252. https://doi.org/10.3389/
feart.2018.00252
Baier, D. B., Gatesy, S. M., & Dial, K. P. (2013). Three‐dimensional, high‐
resolution skeletal kinematics of the avian wing and shoulder during
ascending flapping flight and uphill flap‐running. PLOS ONE, 8(5),
e63982. https://doi.org/10.1371/journal.pone.0063982
Baumel, J. J., King, S. A., Breazile, J. E., Evans, H. E., & Vanden Berge, J. C.
(1993). Handbook of avian anatomy: Nomina anatomica avium.
Publication 23 of Nuttall Ornithological Club.
Beddard, F. E. (1898). The structure and classification of birds. Longmans,
Green, and Company.
Biewener, A. A., & Roberts, T. J. (2000). Muscle and tendon contributions
to force, work and elastic energy savings: A comparative perspec-
tive. Exercise and Sport Sciences Reviews, 2803, 99–107.
Bledsoe, A. H. (1988). A phylogenetic analysis of postcranial skeletal
characters of the ratite birds. Annals of Carnegie Museum, 57, 73–90.
Carpenter, K. (2002). Forelimb biomechanics of nonavian theropod
dinosaurs in predation. Senckenbergiana lethaea, 82(1), 59–75.
https://doi.org/10.1007/BF03043773
Chiappe, L. M. (1996). Late Cretaceous birds of Southern South America:
Anatomy and systematics of Enantiornithes and Patagopteryx deferrariisi.
Münchner Geowissenschaftliche Abhandlungen, 30(A), 203–244.
Chiappe, L. M., Ji, S. A., Ji, Q., & Norell, M. A. (1999). Anatomy and
systematics of the Confuciusornithidae (Theropoda, Aves) from the
late Mesozoic of northeastern China. Bulletin of the American
Museum of Natural History, 242, 1–89.
Chimento, N. R., Agnolín, F. L., Novas, F. E., Ezcurra, M. D., Salgado, L.,
Isasi, M. P., Suárez, M., De La Cruz, R., Rubilar‐Rogers, D., &
Vargas, A. O. (2017). Forelimb posture in Chilesaurus diegosuarezi
(Dinosauria, Theropoda) and its behavioral and phylogenetic
implications. Ameghiniana, 54(5), 567–575. https://doi.org/10.
5710/AMGH.11.06.2017.3088
Cho, P., Brown, R., & Anderson, M. (1984). Comparative gross anatomy of
ratites. Zoo Biology, 3(2), 133–144. https://doi.org/10.1002/zoo.
1430030205
Cunningham, R. O. (1871). Notes on some points in the osteology of Rhea
americana and Rhea darwini. Proceedings of the Zoological Society of
London, 105–110.
Dial, K. P. (1992). Activity patterns of the wing muscles of the pigeon
(Columba livia) during different modes of flight. Journal of
Experimental Zoology, 262(4), 357–373. https://doi.org/10.1002/
jez.1402620402
Dial, K. P., Goslow, G. E., Jr. & Jenkins, F. A. Jr. (1991). The functional
anatomy of the shoulder in the European starling (Sturnus vulgaris).
Journal of Morphology, 207(3), 327–344. https://doi.org/10.1002/
jmor.1052070309
Feduccia, A. (1986). The scapulocoracoid of flightless birds: A primitive
avian character similar to that of theropods. Ibis, 128(1), 128–132.
https://doi.org/10.1111/j.1474-919X.1986.tb02099.x
Forster, C. A., Sampson, S. D., Chiappe, L. M., & Krause, D. W. (1998). The
theropod ancestry of birds: New evidence from the Late Cretaceous
of Madagascar. Science, 279(5358), 1915–1919. https://doi.org/10.
1126/science.279.5358.1915
Fürbringer, M. (1888). Untersuchungen zur Morphologie und Systematik der
Vögel: zugleich ein Beitrag zur Anatomie der Stütz‐und Bewegungsor-
gane (Vol. 15). T. J. Van Holkema.
Fürbringer, M. (1902). Zur vergleichenden Anatomie des Brustschulter‐
apparates undder Schultermuskeln: Vögel. 5 Teil. J. Z. Nat., 36,
289–763.
Gadow, H. (1885). On the anatomical differences in the three species
of Rhea. Proceedings of the Zoological Society of London, 53(2),
308–322.
ET AL.
Gasparri, B. (2016). El Ñandú, Rhea americana. Fundación de Historia
Natural Félix de Azara.
Gatesy, S. M., & Baier, D. B. (2005). The origin of the avian flight stroke:
A kinematic and kinetic perspective. Paleobiology, 31(3), 382–399.
https://doi.org/10.1666/0094-8373(2005)031[0382:TOOTAF]2.0.CO;2
George, J. C., & Berger, A. J. (1966). Avian myology. Academic Press.
Gill, F., & Donsker, D. (2020). IOC world bird list (v10.1). https://doi.org/10.
14344/IOC.ML.10.1
Haughton, S. (1864). Notes on animal mechanics: No. 11. On the muscular
anatomy of the Rhea (Struthio rhea). Proceedings of the Royal Irish
Academy (1836–1869), 9, 497–504.
Heers, A. M., Baier, D. B., Jackson, B. E., & Dial, K. P. (2016). Flapping
before flight: High resolution, three‐dimensional skeletal kinematics
of wings and legs during avian development. PLoS ONE, 11(4),
e0153446. https://doi.org/10.1371/journal.pone.0153446
Hudson, G. E., Schreiweis, D. O., Wang, S. C., & Lancaster, D. A. (1972).
A numerical study of the wing and leg muscles of tinamous
(Tinamidae). Northwest Science, 46, 207–255.
Hutson, J. D., & Hutson, K. N. (2012). A test of the validity of range of
motion studies of fossil archosaur elbow mobility using repeated‐
measures analysis and the extant phylogenetic bracket. Journal of
Experimental Biology, 215(12), 2030–2038. https://doi.org/10.1242/
jeb.069567
Hutson, J. D., & Hutson, K. N. (2014). A repeated‐measures analysis of the
effects of soft tissues on wrist range of motion in the extant
phylogenetic bracket of dinosaurs: Implications for the functional
origins of an automatic wrist folding mechanism in crocodilia. The
Anatomical Record, 297(7), 1228–1249. https://doi.org/10.1002/ar.
22903
Hutson, J. D., & Hutson, K. N. (2018). Retention of the flight‐adapted
avian finger‐joint complex in the ostrich helps identify when wings
began evolving in dinosaurs. Ostrich, 89(2), 173–186. https://doi.
org/10.2989/00306525.2017.1422566
Jasinoski, S. C., Russell, A. P., & Currie, P. J. (2006). An integrative
phylogenetic and extrapolatory approach to the reconstruction of
dromaeosaur (Theropoda: Eumaniraptora) shoulder musculature.
Zoological Journal of the Linnean Society, 146(3), 301–344. https://
doi.org/10.1111/j.1096-3642.2006.00200.x
Jenkins, F. A. Jr. (1993). The evolution of the avian shoulder joint.
American Journal of Science, 293(A), 253–267
Livezey, B. C., & Zusi, R. L. (2007). Higher‐order phylogeny of modern birds
(Theropoda, Aves: Neornithes) based on comparative anatomy. II.
Analysis and discussion. Zoological Journal of the Linnean Society,
149(1), 1–95. https://doi.org/10.1111/j.1096-3642.2006.00293.x
Lo Coco, G. E., Motta, M. J., Mosto, M. C., & Picasso, M. B. (2020). Wing
and tail myology of Tyto furcata (Aves, Tytonidae). Journal of
Morphology, 281(4–5), 450–464. https://doi.org/10.1002/jmor.
21111
Lowe, P. R. (1928). Studies and observations bearing on the phylogeny of
the ostrich and its allies. Proceedings of the Zoological Society of
London, 98(1), 185–247.
Maxwell, E. E., & Larsson, H. C. (2007). Osteology and myology of the
wing of the Emu (Dromaius novaehollandiae), and its bearing on the
evolution of vestigial structures. Journal of Morphology, 268(5),
423–441. https://doi.org/10.1002/jmor.10527
Mayr, G. (2017). Pectoral girdle morphology of Mesozoic birds and the
evolution of the avian supracoracoideus muscle. Journal of
Ornithology, 158(3), 859–867. https://doi.org/10.1007/s10336-
017-1451-x
McGowan, C. (1982). The wing musculature of the Brown kiwi Apteryx
australis mantelli and its bearing on ratite affinities. Journal of
Zoology, 197(2), 173–219. https://doi.org/10.1111/jzo.1982.197.
2.173
Mindell, D. P. (1997). Avian molecular evolution and systematics. Academic
Press.
LO COCO ET AL.
Muñíz, F. J. (1885). El ñandú o avestruz pampeano. In D. F. Sarmiento
(Ed.), Vida y Escritos del Coronel Dr. Francisco J. Muñiz. F. Lajouane.
Novas, F. E., Agnolín, F., Brissón Egli, F., & Lo Coco, G. E. (2020). Pectoral
girdle morphology in early‐diverging paravians and living ratites:
Implications for the origin of flight, Pennaraptoran theropod
dinosaurs: Past progress and new frontiers. Bulletin of American
Museum of Natural History (Vol. 440, pp. 345–353).
Novas, F. E., Brissón Egli, F., Agnolín, F. L., Gianechini, F. A., & Cerda, I.
(2018). Postcranial osteology of a new specimen of Buitreraptor
gonzalezorum (Theropoda, Unenlagiidae). Cretaceous Research, 83,
127–167. https://doi.org/10.1016/j.cretres.2017.06.003
Novas, F. E., Motta, M. J., Agnolín, F. L., Rozadilla, S., Lo Coco, G. E., &
Brissón Egli, F. (2021). Comments on the morphology of basal
paravian shoulder girdle: New data based on unenlagiid theropods
and paleognath birds. Frontiers in Earth Science, 9, 662167. https://
doi.org/10.3389/feart.2021.662167
Olson, S. L. (1973). Evolution of the rails of the South Atlantic islands
(Aves: Rallidae). Smithsonian. Contributions to Zoology, 152, 1–53.
https://doi.org/10.5479/si.00810282.152
Olson, S. L., & Feduccia, A. (1979). Flight capability and the pectoral girdle
of Archaeopteryx. Nature, 278(5701), 247–248. https://doi.org/10.
1038/278247a0
Ostrom, J. H. (1969). Osteology of Deinonychus antirrhopus, an unusual
theropod from the Lower Cretaceous of Montana. Peabody Museum
Bulletin, 30, 1–165.
Picasso, M. B., Monti, A., Mosto, M. C., & Morgan, C. C. (2020).
Ontogenetic shape changes in the pelvis of the Greater Rhea (Aves,
Palaeognathae) and their relationships with cursorial locomotion: A
geometric morphometric approach. Journal of Anatomy, 236(6),
1137–1145. https://doi.org/10.1111/joa.13158
Picasso, M. B., & Mosto, M. C. (2018). Wing myology of Caracaras (Aves,
Falconiformes): Muscular features associated with flight behavior.
Vertebrate Zoology, 68(2).
Picasso, M. B., Tambussi, C. P., Mosto, M. C., & Degrange, F. J. (2012).
Crecimiento de la masa muscular del miembro posterior del Ñandu
Grande (Rhea americana) durante la vida postnatal. Revista Brasileira
de Ornitologia, 20, 1–7.
Picasso, M. B. J. (2010). The hindlimb muscles of Rhea americana (Aves,
Palaeognathae, Rheidae). Anatomia, Histologia, Embryologia, 39(5),
462–472. https://doi.org/10.1111/j.1439-0264.2010.01017.x
Picasso, M. B. J. (2015). Ontogenetic scaling of the hindlimb muscles of
the Greater Rhea (Rhea americana). Anatomia, Histologia,
Embryologia, 44(6), 452–459. https://doi.org/10.1111/ahe.12158
Poore, S. O., Ashcroft, A., Sanchez‐Haiman, A., & Goslow, G. E. Jr. (1997).
The contractile properties of the M. supracoracoideus in the pigeon
and starling: A case for long‐axis rotation of the humerus. The
Journal of Experimental Biology, 200(23), 2987–3002. https://doi.
org/10.1242/jeb.200.23.2987
Pycraft, W. P. (1900). The morphology and phylogeny of the Palaeog-
nathae (Ratitae and Crypturi) and the Neognathae (Carinatae).
Transactions of the Zoological Society of London, 15, 149–290.
Raikow, R. J. (1968). Maintenance behavior of the Common Rhea. The
Wilson Bulletin, 80(3), 312–319.
Raikow, R. J. (1969). Sexual and agonistic behavior of the Common Rhea.
The Wilson Bulletin, 81(2), 196–206.
Raikow, R. J. (1985). Locomotor system. In A. S. King & J. McLelland (Eds.),
Form and function in birds (Vol. 3, pp. 57–147). Academic Press.
Roberts, T. J. (2001). Muscle force and stress during running in dogs and
wild turkeys. Bulletin of the Museum of Comparative Zoology at
Harvard College, 156, 283–295.
Sackton, T. B., Grayson, P., Cloutier, A., Hu, Z., Liu, J. S., Wheeler, N. E.,
Gardner, P. P., Clarke, J. A., Baker, A. J., Clamp, M., & Edwards, S. V.
(2019). Convergent regulatory evolution and loss of flight in
Paleognathous birds. Science, 364(6435), 74–78. https://doi.org/
10.1126/science.aat7244
| 33
Senter, P. (2006). Comparison of forelimb function between Deinonychus
and Bambiraptor (Theropoda: Dromaeosauridae). Journal of
Vertebrate Paleontology, 26(4), 897–906. https://doi.org/10.1671/
0272-4634(2006)26[897:COFFBD]2.0.CO;2
Suzuki, D., Chiba, K., VanBuren, C. S., & Ohashi, T. (2014). The
appendicular anatomy of the elegant crested Tinamou (Eudromia
elegans). Bulletin of the Kitakyushu Museum of Natural History and
Human History, Series A (Natural History), 12, 1–48. https://doi.org/
10.34522/kmnh.12.0_1
Tobalske, B. W., Warrick, D. R., Clark, C. J., Powers, D. R., Hedrick, T. L.,
Hyder, G. A., & Biewener, A. A. (2007). Three‐dimensional
kinematics of hummingbird flight. Journal of Experimental Biology,
210(13), 2368–2382. https://doi.org/10.1242/jeb.005686
Turner, A. H., Makovicky, P. J., & Norell, M. A. (2007). Feather quill knobs
in the dinosaur Velociraptor. Science, 317(5845):1721. https://doi.
org/10.1126/science.1145076
Vazquez, R. J. (1992). Functional osteology of the avian wrist and the
evolution of flapping flight. Journal of Morphology, 211(3), 259–268.
https://doi.org/10.1002/jmor.1052110303
Vazquez, R. J. (1994). The automating skeletal and muscular mechanisms
of the avian wing (Aves). Zoomorphology, 114(1), 59–71. https://doi.
org/10.1007/BF00574915
Wang, M., Stidham, T. A., & Zhou, Z. (2018). A new clade of basal Early
Cretaceous pygostylian birds and developmental plasticity of the
avian shoulder girdle. Proceedings of the National Academy of Sciences
of the United States of America, 115(42), 10708–10713. https://doi.
org/10.1073/pnas.1812176115
Woolley, J. D. (2000). The functional morphology of the avian flight
muscle M. coracobrachialis posterior. Journal of Experimental Biology,
203(11), 1767–1776. https://doi.org/10.1242/jeb.203.11.1767
Worthy, T. H., & Scofield, R. P. (2012). Twenty‐first century advances in
knowledge of the biology of moa (Aves: Dinornithiformes): A new
morphological analysis and moa diagnoses revised. New Zealand
Journal of Zoology, 39(2), 87–153. https://doi.org/10.1080/
03014223.2012.665060
Wustinger, J., Jaśko, D., Dróżdż, D., Basińska, M., & Pospieszny, N. (2006).
Muscles of thoracic limb of African ostrich (Struthio camelus L.).
Electronic Journal of Polish Agricultural Universities. Series Veterinary
Medicine, 9(2).
Yonezawa, T., Segawa, T., Mori, H., Campos, P. F., Hongoh, Y., Endo, H.,
Akiyoshi, A., Kohno, N., Nishida, S., Wu, J., Jin, H., Adachi, J.,
Kishino, H., Kurokawa, K., Nogi, Y., Tanabe, H., Mukoyama, H.,
Yoshida, K., Rasoamiaramanana, A., … Hasegawa, M. (2017).
Phylogenomics and morphology of extinct paleognaths reveal the
origin and evolution of the ratites. Current Biology, 27(1), 68–77.
https://doi.org/10.1016/j.cub.2016.10.029
Zhou, Z., & Zhang, F. (2003). Anatomy of the primitive bird Sapeornis
chaoyangensis from the Early Cretaceous of Liaoning, China.
Canadian Journal of Earth Sciences, 40(5), 731–747. https://doi.org/
10.1139/e03-011
SUPP ORTING INFO RM ATION
Additional supporting information can be found online in the
Supporting Information section at the end of this article.
How to cite this article: Lo Coco, G. E., Motta, M. J., Agnolín,
F. L., & Novas, F. E. (2022). Wing osteology, myology, and
function of Rhea americana (Aves, Rheidae). Journal of
Morphology, 1–33. https://doi.org/10.1002/jmor.21486