Anatomia, Histologia, Embryologia
ORIGINAL ARTICLE
Ontogenetic Scaling of the Hindlimb Muscles of the Greater Rhea (Rhea americana) M. B. J. Picasso* n Paleontologıa Vertebrados, Museo de La Plata, Facultad de Ciencias Naturales y Museo-Universidad Nacional de La Address of author: Divisio Plata, Paseo del Bosque s/n, La Plata, B1900FWA, Buenos Aires, Argentina; CONICET, Consejo Nacional de Investigaciones Cientı´ficas y Tecnicas,
*Correspondence: e-mail: [email protected] With 2 figures and 3 tables Received April 2014; accepted for publication October 2014 doi: 10.1111/ahe.12158
Summary The greater rhea (Rhea americana) is the largest South American bird. It is a cursorial, flightless species with long powerful legs and reduced forelimbs. The goal of this study was to explore how hindlimb muscles scale with body mass during postnatal growth and to analyze whether the specialized locomotion of this species affects the growth of muscle masses. The mass of 19 muscles and body mass were weighed in 21 specimens ranging from 1-month-old individuals to adults. Seventeen muscles scaled with positive allometry with respect to body mass, whereas two muscles scaled isometrically. The predominance of positive allometric growth in hindlimb muscles results in a limb with massive and powerful muscles specialized to support a large body mass and to attain relatively high running speeds. Analysis of muscle mass scaling is a simple and useful way to compare possible differences between locomotor styles, and it is valuable in studies that reconstruct the paleobiology of extinct taxa.
Introduction Birds are exclusively bipedal because their forelimb functions as a wing during flight, while the hindlimbs are responsible for terrestrial movement (Hutchinson and Gatesy, 2001). Given that flight is the most striking locomotor mode, terrestrial locomotion has received relatively little attention, despite the fact that for many birds, locomotion on land plays an important ecological role (Verstappen et al., 2000). The morphology of the pelvic limbs vary according to the proportions of their skeletal elements (Gatesy and Middleton, 1997), the presence or absence of certain muscles (George and Berger, 1966) and the proportional development of these muscles relative to body mass (Hartman, 1961). Several studies have found that variations of hindlimb morphology can be correlated with different behaviours and habitats (Hartman, 1961; Bennett, 1996; Barbosa and Moreno, 1999; Zeffer et al., 2003). In general, the wide morphological variation is largely produced during ontogeny (Klingerberg, 1996; Jones and German, 2005). Also, during ontogeny, various traits may develop at different rates with respect to other body regions, a process known as ontogenetic allometry. This process
452
may provide information on morpho-functional and adaptive aspects (Cardini and O’Higgins, 2005) as the deviations from isometry are often correlated with functional demands on the musculoskeletal system (Bennett, 1996). The greater rhea (Rhea americana) is the largest (1.50 m tall and 25 kg body mass) palaeognathous bird of South America; rheas, together with the emu (Dromaius novaehollandiae), cassowary (Casuarius casuarius, C. benetti, C. unappendiculatus), ostrich (Struthio camelus) and kiwi (Apteryx australis, A. owenii, A. haastii) form the taxon Ratitae (Slack et al., 2007; Bourdon et al., 2009; but see Smith et al., 2013). The Ratitae are flightless birds with powerful, elongated and massive hindlimbs and, with the exception of kiwis, present a specialized locomotor behaviour known as cursoriality (Coombs, 1978; Gatesy and Biewener, 1991; Abourachid and Renous, 2000). They are able to attain high running speeds (ranging between 50 and 70 km/h, depending on the species; Folch, 1992). Such a specialized locomotor behaviour may affect limb morphology throughout ontogeny (Lammers and German, 2002). For example, in the greater rhea some hindlimb bones, such as the tarsometatarsus, show positive allometric growth during the © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
Leg muscles scaling of Greater Rhea
M. B. J. Picasso
postnatal development, possibly related to cursoriality (Picasso, 2012). A long tarsometatarsus enables a longer stride which, in turn, favours an increase in locomotor speed (Gatesy and Biewener, 1991; Wolff, 1991; Abourachid and Renous, 2000). However, no information is available regarding the scaling of hindlimb muscle mass in this species, and for other birds, such data are relatively scarce and often limited in terms of the number of muscles examined (Helmi and Cracraft, 1977; Carrier and Leon, 1990; Bennett, 2008). As muscle mass is proportional to the maximum muscle power output (Alexander, 1974; Biewener and Roberts, 2000; Roberts, 2001), the purpose of this study is to document the scaling patterns of the hindlimb muscles of the greater rhea using the muscle mass as a simple way to obtain information about the potential power of a muscle available during locomotion (Hartman, 1961).
Table 1. Muscles studied, and their main functions
Hip Muscles
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
Main functions
M. ambiens
Hip flexor, knee extensor Hip extensor Hip extensor Hip extensor Hip flexor Hip flexor and abductor Hip flexor and adductor Hip flexor and abductor Hip extensor Hip flexor abductor Hip extensor, adductor Pelvic girdle stabilization, adduction Knee extensor Knee flexor, hip extensor Ankle extensor Ankle extensor Ankle flexor Digits extensor
M. M. M. M. M. M. M. M. M. M. M. Knee and ankle muscles
caudofemoralis flexor cruris groupa iliotibialis lateralis iliotibialis cranialis iliotrocantericus caudalis iliotrocantericus medialis iliotrocantericus cranialis ischiofemoralis iliofemoralis externus puboischiofemoralis obturatorius medialisb
M. femorotibialis groupc M. iliofibularis M. gastrocnemius M. fibularis longus M. tibialis cranialis M. extensor digitorum longus M. flexor perforans et perforatus digiti II M. flexor perforans et perforatus digiti III M. flexor perforatus digiti II M. flexor perforatus digiti IIId M. flexor perforatus digiti IV M. flexor hallucis longus M. flexor digitorum longus
Materials and Methods Specimens and data collection A total of 21 healthy specimens of greater rhea obtained from various commercial farms located in Buenos Aires province, Argentina were studied. Specimens ranged from immature birds of 1–8 months of age (467 g–5 kg) to 2-year-old adult birds (10.5–22 kg). The birds were obtained from a slaughterhouse, and the birds were reared in accordance with Argentinean regulations for rhea farming. Body mass was measured using a digital scale (Denver Instrument, 0.01 g accuracy, 600 g capacity) for 1-monthold birds, and a hand-held scale (500 g accuracy, 50 kg capacity) for the remaining individuals, except specimens MLP 882 and 883 that were weighed using a digital scale (Sensotonic SE-500) with 100 g accuracy and 50 kg capacity (see Table 2). Functionally, muscles and tendons are intimately integrated, and their mechanical abilities as a unit far exceed the capabilities of the component alone (Roberts, 2002). Considering this, it was decided to weigh the muscles including both fleshy portions and their tendons. The muscles of one limb of each individual were carefully removed from their sites of origin and insertion and weighed with a digital scale (with 0.01 g accuracy and 600 g capacity). Table 1 shows the nineteen muscles that were studied, and their functions. Muscles that shared a similar function were weighed together (Table 1). The small muscles of the hindlimb (M. popliteus, M. obturatorius medialis and M. iliofemoralis internus and short muscles of the tarsometatarsus and digits) were not included in this study. Myological nomenclature follows Vanden Berge and Zweers (1993), and the identification of hindlimb muscles of the greater rhea was done according to Picasso (2010) (Fig. 1).
Muscle
Digital flexor group
a
M. flexor cruris medialis and M. flexor cruris were weighed together. Precise role is unknown. c M. femorotibialis lateralis, M. femorotibialis medialis and M. femorotibialis internus were weighed together. d All these muscles were weighed together. b
Ontogenetic scaling Body mass, the mass of each muscle and the total muscle mass of the hindlimb (i.e. the sum of all individual muscle masses) were log10-transformed and analyzed using the allometric equation: log y = log a + b log x, where b is the slope or allometric exponent that represents the ratio of specific growth rates (Huxley, 1932), a is the y-intercept, y is the muscle mass and x is the body mass. This equation derives from the growth function y = a xb first proposed by Huxley (1932) and Huxley and Teissier (1936). Expected coefficients under isometry are equal to 1, and deviations where b < 1 or b > 1 represent negative and positive allometry, respectively. These analyses were carried out by reduced major axis (RMA) regression using the software SMATR (v.2.0) (Falster et al., 2006). This method is a useful tool to describe how size
453
Leg muscles scaling of Greater Rhea
M. B. J. Picasso
(a)
variables are related because it assesses the relationship between x and y (Warton et al., 2006). Allometry was detected when 1.0 was not included in the 95% confidence interval of the regression slope (b). Possible differences between sexes were not evaluated due to the relatively small number of sexed specimens, which did not allow adequate statistical analysis, so the analyses were performed using pooled data.
(b)
Fig. 1. Schematic drawing of the main hindlimb muscles of the greater rhea; (a) lateral view, (b) medial view. Scale bar: 10 cm.
Fig. 1). Other muscles, such as the muscles M. iliotrochantericus caudalis, M. iliofibularis, M. femorotibialis, M. extensor digitorum longus and M. gastrocnemius showed moderate positive allometric exponents (values ~1.20). Total muscular mass showed a positive allometric relationship with body mass (slope 1.18, Table 3).
Discussion Muscle actions To produce a movement (or pattern of movements), muscles can act independently, concurrently or in sequence (Kardong, 2012). Thus, for the purposes of this study, muscle actions were simplified into extensor – flexor and adductor – abductor categories regarding limb movements during terrestrial locomotion. The interpretation of the main role of the muscles during terrestrial locomotion follows the works of Jacobson and Hollyday (1982), Gatesy (1999) and Smith et al. (2006) (Table 1). Results All the measurements obtained are listed in Table 2. Figure 2 and Table 3 show the results of the regression analyses for each muscle and for the total muscular mass of the hindlimb. R2-values ranged from 0.89 to 0.99, while b values ranged between 1.04 and 1.43. Except for M. tibialis cranialis and M. puboischiofemoralis, which showed isometric growth relative to body mass, all other muscles exhibited positive allometric growth patterns (Table 3). The M. iliotibialis lateralis, M. flexor cruris, M. fibularis longus and M. obturatorius medialis showed strong positive allometry with relatively high coefficients (range 1.30–1.43) (see also
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Scaling of the hindlimb muscle mass as a whole As a whole, the total hindlimb muscular mass of the greater rhea showed a positive allometric growth pattern (b = 1.18). In contrast, for the closely related ostrich, Smith et al. (2006) found an isometric relationship (b = 1.06) between the total hindlimb muscle mass and body mass. This disparity could be due to the use of different age ranges between the two studies. Smith et al. (2006) analyzed ostriches that ranged between 24 and 43 weeks of age, but birds younger than 6 months were not included. By contrast, this study utilized a broader range of ages because birds younger than 6 months were included. Regarding other not closely related birds, the hindlimb muscle mass of the non-cursorial ducks (Anatidae, Anseriformes) selected primarily for market weight, scaled with negative allometry (b = 0.70–0.87) (Maruyama et al., 1999). However, positive allometry (b = 1.18) between total hindlimb muscle mass and body mass has been found for neonates of non-cursorial geese and ducks (Anseriformes), shore birds (Charadriformes, Scolopacidae), gulls and terns (Laridae and Sternidae) and some non-anseriform aquatic birds (Rallidae, Podicipedidae) (Visser and Rikclefs, 1995). This pattern of growth in neonate precocial and semiprecocial birds is associated © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
15 500
10 500
19 000
18 000
20 000
22 000
5000
5000
4000
5000
3000
3000
4000
3000
484.72
618.85
544.98
466.90
2424.27
1154.52
2742.37
2707.74
3467.42
3825.12
1632.17
600.96
667.68
743.63
502.92
700.41
264.40
336.83
384.63
293.02
41.50
54.39
46.24
38.27
39.97
tmm.
4.47
1.85
6.63
5.54
8.05
8.34
5.25
1.67
2.47
2.29
1.46
2.00
0.76
0.72
0.84
0.97
0.13
0.13
0.10
0.07
0.10
am.
2.11
2.77
2.63
2.26
2.02
110.82
32.63
104.48
103.48
152.30
162.80
84.90
25.11
26.07
27.05
15.66
29.53
14.42
16.80
18.03
12.99
cf.
238.1
56.62
210.71
228.64
304.58
329.97
144.6
45.44
52.57
51.80
36.37
56.91
2.19
27.75
30.47
19.56
3.05
4.06
3.65
2.74
3.03
fcr.
4.27
5.62
5.11
0.56
4.17
344.82
118.89
417.71
409.74
488.06
588.56
246.18
104.70
92.8
99.17
69.76
99.57
34.36
41.81
45.49
32.91
ill.
133.74
50.43
118.03
141.9
174.91
217.23
85.20
28.96
34.06
35.48
20.67
33.46
14.16
22.69
21.94
15.04
2.60
3.63
3.03
3.20
2.43
ilc.
1.69
2.27
1.98
1.83
1.85
105.26
48.08
115.85
109.2
141.4
163.92
59.19
26.03
21.77
25.09
15.82
23.18
12.39
15.03
17.53
13.14
ic.
5.01
5.05
7.50
7.13
10.64
10.64
3.03
2.46
1.42
1.29
1.41
1.52
1.01
1.13
1.25
0.92
0.16
0.24
0.15
0.14
0.18
im.
8.24
5.15
9.42
11.7
15.25
13.95
5.050
2.70
2.96
3.62
1.61
3.16
1.61
1.84
2.61
1.63
0.24
0.33
0.23
0.20
0.26
icr.
18.36
9.12
18.66
14.11
20.87
19.06
9.16
5.76
3.17
4.54
3.31
4.41
2.12
2.97
2.81
2.48
0.42
0.51
0.43
0.28
0.32
isc.
10.28
7.60
9.96
8.88
15.42
11.55
5.87
2.46
2.79
2.53
1.96
2.10
1.20
0.94
1.29
1.23
0.25
0.22
0.19
0.19
0.16
iex.
32.93
27.56
24.73
30.22
39.66
48.09
15.69
12.76
9.94
8.40
8.26
9.13
5.39
5.63
6.35
5.68
1.06
1.42
1.10
1.01
1.02
pic.
109.68
30.62
122.03
103.80
190.84
164.53
58.76
25.84
25.79
24.23
16.69
27.11
9.18
12.86
15.11
10.11
0.97
1.32
0.99
0.91
0.90
om.
5.25
7.12
6.00
5.29
4.93
254.32
151.93
276.38
319.07
418.09
393.62
182.40
96.42
82.59
98.98
69.01
90.10
38.63
44.62
48.29
43.21
ft.
3.403
4.91
3.86
3.96
3.05
195.54
164.49
235.30
242.03
311.03
374.00
134.70
37.07
64.73
71.65
47.25
63.85
23.18
32.25
34.78
25.30
if.
417.05
205.25
580.84
476.01
583.02
636.32
313.44
88.13
115.15
145.03
94.10
120.83
51.04
55.17
67.29
53.71
7.73
9.51
7.83
7.59
7.54
gs.
2.13
3.09
2.35
1.98
1.97
178.81
86.89
247.40
251.33
273.45
299.1
126.11
26.51
53.20
59.53
38.47
54.26
16.93
18.29
23.72
16.75
fl.
1.91
2.41
2.09
1.94
1.85
66.38
41.54
96.79
70.52
91.63
102.38
41.89
20.71
20.73
28.95
19.46
23.6
10.97
10.79
15.1
10.87
tc.
25.4
13.69
27.63
22.47
29.07
32.72
14.77
5.73
6.99
7.08
4.6
7.76
2.74
3.18
3.97
3.01
0.45
0.61
0.54
0.42
0.41
edl.
158.88
91.15
219.97
146.23
189.80
240.20
92.36
40.53
46.44
44.92
35.51
46.34
21.24
21.65
26.60
22.51
3.49
4.02
3.84
3.45
3.59
df.
Muscle abbreviations bm.: body mass, tmm: total muscle mass. MLP: osteological appended collection of the Division Paleontologıa Vertebrados, Museo de La Plata, Argentina. am. (M. ambiens), cf. (M. caudofemoralis), fcr. (M. flexor cruris group), ill. (M. iliotibialis lateralis), ilc. (M. iliotibialis cranialis), ic. (M. iliotrocantericus caudalis), im. (M. iliotrocantericus medialis), icr. (M. iliotrocantericus cranialis), isc. (M. ischiofemoralis), iex. (M. iliofemoralis externus), pic.(M. puboischiofemoralis), om.(M. obturatorius medialis), ft. (M. femorotibialis group), if. (M. iliofibularis), gs. (M. gastrocnemius), fl. (M. fibularis longus), tc. (M. tibialis cranialis), edl. (M. extensor digitorum longus), df. (M. digital flexor group). a Approximate age.
Adult
MLP 880
8 month
MLP 882
Adult
5 months
MLP 887
Adult
5 months
MLP 886
MLP 879
5 months
MLP 885
MLP 878
5 months
MLP 884
Adult
3 months
MLP 891
Adult
3 months
MLP 890
MLP 897
3 months
MLP 889
MLP 877
9600
3 months
MLP 888
8 montha
1 month
MLP 896
Adult
1 month
MLP 895
MLP 883
1 month
MLP 894
MLP 876
4900
1 month
MLP 893
491.1
1 month
MLP 892
bm.
Age
Specimen
Table 2. Raw measurements (g) for each specimen studied
M. B. J. Picasso Leg muscles scaling of Greater Rhea
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Leg muscles scaling of Greater Rhea
M. B. J. Picasso
(a) 3.0
flexor cruris
Table 3. Results of allometric analyses for each muscle and total muscle mass
iliotibialislateralis
2.5
iliotibialiscranialis iliotrochanterichuscaudalis
2.0
Muscles and Total muscle mass
R2
b
b lower CI
b upper CI
0.97 0.98 0.89 0.95 0.98 1.00
1.18 1.12 1.30 1.43 1.12 1.17
1.09 1.05 1.12 1.28 1.05 1.13
1.29 1.20 1.51 1.58 1.19 1.21
4.19 2.70 3.16 3.39 2.61 2.91
0.98
1.08
1.02
1.15
3.74
0.99
1.08
1.03
1.13
3.53
0.99 0.98 0.99 0.99
1.09 1.14 0.97 1.37
1.03 1.07 0.92 1.30
1.15 1.21 1.02 1.45
3.39 3.82 2.61 3.73
0.99 0.99 0.99 0.99 0.99 0.99
1.14 1.21 1.18 1.31 1.04 1.14
1.10 1.15 1.13 1.24 1.00 1.10
1.19 1.27 1.23 1.38 1.08 1.18
2.33 2.71 2.32 3.22 2.52 3.42
1.00 0.99
1.10 1.18
1.06 1.14
1.13 1.22
2.43 1.59
a
puboischiofemoralis
1.5
obturatoriusmedialis
1.0 0.5 0.0 –0.5 2.6
2.8
3.0
3.2
3.4
3.6
3.8
4.0
4.2
4.4
4.6
(b) 3.0
femorotibialis iliofibularis
2.5
gastrocnemius
2.0
tibialiscranialis
1.5
flexoresdigitii extensordigitorumlongus
1.0 0.5 0.0 –0.5 –1.0 2.6
2.8
3.0
3.2
3.4
3.6
3.8
4.0
4.2
4.4
4.6
Fig. 2. Linear regressions of log-transformed data describing the relationships between body mass and muscle mass; (a) pelvic muscles, (b) femoral and tibiotarsal muscles. For a better understanding of the figure, only pertinent muscles have been included.
with the generation of heat by shivering of the leg muscles (Choi et al., 1993). Unfortunately, no data have been published so far documenting whether this positive allometric relationship between leg muscles and body mass in these birds is maintained throughout postnatal life. In this regard, the deviation from isometry that characterizes the entire postnatal life of the greater rhea might be related to the functional demands of a larger body size and a specialized locomotion. Similar results have been found in other vertebrates such as mammalian bipedal hoppers (Alexander et al., 1981; Bennett and Taylor, 1995; McGowan et al., 2008). These studies of static allometry show a positive allometric scaling of hindlimb muscle mass with respect to body mass, whereas in quadrupeds, this relationship is isometric. Also, bipedal mammals tend to have larger leg muscles than quadrupeds (Alexander et al., 1981; Pollock and Shadwick, 1994). The same can be seen in the greater rhea, in which the hindlimb muscles tend to represent a large portion of body mass which may be as a consequence of the positive allometric growth of both extensor and flexors muscles. Leg muscles of the greater rhea represent between 8.5% and 15.8% of the body mass according to age (Picasso et al., 2012), and similar value were reported also for adults of the ostrich (Smith et al., 2006) and the emu (Patak and Baldwin, 1998). In this sense, positive allometric scaling of leg muscle mass in the
456
Hip muscles M. ambiens M. caudofemoralis M. flexor cruris M. iliotibialis lateralis M. iliotibialis cranialis M. iliotrocantericus caudalis M. iliotrocantericus medialis M. iliotrocantericus cranialis M. ischiofemoralis M. iliofemoralis externus M. puboischiofemoralisa M. obturatorius medialis Knee and ankle muscles M. femorotibialis M. iliofibularis M. gastrocnemius M. fibularis longus M. tibialis cranialisa M. extensor digitorum longus M. digital flexor group Total muscle mass CI, 95% confidence interval. Indicates isometry.
a
greater rhea could be one of the factors that contribute to maintain running performance with increasing body mass. However, further studies on muscular architecture and its scaling with body mass will be useful to complement and extend these inferences. Studies on these aspects in adult ostrich or in bipedal hoppers, like kangaroos, show that the hindlimb muscle architecture is optimized for maximizing force production and to support the body mass (Smith et al., 2006; McGowan et al., 2008). Allometric growth could also be related to locomotor parameters. Smith et al. (2010) found that in ostriches, as body mass increases with age, differences arise in kinematic parameters during locomotion, such as an increase in stride length. As ratite birds usually present similar kinematic parameters during locomotion (Gatesy and Biewener, 1991; Abourachid and Renous, 2000), it is plausible that the positive allometry of muscle masses in the greater rhea might be related to a shift in kinematic parameters as the animal grows and perfects its motion. Unfortunately, no kinetic or kinematics studies have been performed to date on R. americana. © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
Leg muscles scaling of Greater Rhea
M. B. J. Picasso
Scaling of individual muscles: a comparison with other birds Interesting questions arise when the allometric exponents for specific muscles of this species are compared with the same muscles in other birds. For example, the M. gastrocnemius (an antigravity muscle) of non-running birds such as the californian gull (Larus californicus) and the black noddy (Anous minutus) show an isometric growth pattern with respect to body mass during postnatal growth (Carrier and Leon, 1990; Bennett, 2008), whereas in the greater rhea, this muscle scaled positively with body mass. This pattern could be reflecting differences in locomotor style: in running birds such as the greater rhea, increasing speed is achieved by increase of their stride length (Gatesy and Biewener, 1991; Abourachid and Renous, 2000), and for this, extension of the ankle joint is key, because it lengthens the limb and propels the body forward (Smith et al., 2006). Thus, the extensor muscles of this joint have a particularly important role in providing the power required for effective high speed locomotion (Smith et al., 2006). This is reflected by the positive allometry observed. The M. iliofibularis, which flexes the knee joint and is a hip extensor, scaled positively with body mass both in the greater rhea and the chicken (Gallus gallus) (Helmi and Cracraft, 1977). This might be associated with the evolution of bird bipedalism, in which the movement of the hindlimb became knee-dominated in contrast with the femoral retraction pattern observed in crocodilians and limbed lepidosaurs (Gatesy, 1990; Hutchinson, 2002). The M. puboischiofemioralis and M. tibialis cranialis grew isometrically. Helmi and Cracraft (1977) found a similar pattern of growth in the M. puboischiofemoralis of the chicken, the mass of this muscle remained isometric with increasing body mass, but the length of this muscle presented positive allometry. Unfortunately, there is no information about postnatal scaling of M. tibialis cranialis. The isometric growth pattern of muscle mass might possibly reflect their more general function in avian hindlimb, not related to a specific adaptation. Nevertheless, further studies on muscle architecture of these muscles will contribute to explore the scaling patterns of other features such as fascicle length and physiological cross sectional area, and to understand their relationship with functional aspects. As a large running bird, the greater rhea presents allometric growth of the hindlimb musculoskeletal system. This positive allometry found for almost all muscles, together with that of the bones, such as tarsometatarsus length (Picasso, 2012), results in a long limb with massive and powerful muscles, specialized to support a large body mass and to attain relatively high running speeds.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
Final conclusions and future directions Muscle mass data are simple to obtain and can be used to explore the relative functional importance of individual muscles or muscle groups in the maintenance of posture, joint movements and locomotor performance. In addition, the information derived from modern species can be usefully applied to paleontological studies in which muscle mass cannot be measured, but can be reconstructed (e.g. Hutchinson, 2004a,b; Hutchinson et al., 2011). Birds are an extant clade of theropod dinosaurs (Gauthier, 1986; Farlow et al., 2000), a group characterized by bipedal locomotion and digitigrady. Thus, studies of morpho-functional aspects of bipedalism in extant birds become essential to understand non-avian theropod locomotion (Farlow et al., 2000; Hutchinson, 2004a,b). Further research that focuses on growth patterns of hindlimb muscle masses of birds with different terrestrial locomotor styles is needed to shed light on the variation of muscular growth patterns. In addition, studies on muscle architecture and kinetics, and on the kinematics of the greater rhea, will also contribute to the knowledge of myological specializations for cursorial locomotion and will expand and enhance the present findings. Acknowledgements The author thanks F.J. Degrange for his friendship, help and support during the dissections and C.C. Morgan for her useful comments. C.C. Morgan and C. Mosto improved the English version of this paper.
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ORIGINAL ARTICLE
Ontogenetic Scaling of the Hindlimb Muscles of the Greater Rhea (Rhea americana) M. B. J. Picasso* n Paleontologıa Vertebrados, Museo de La Plata, Facultad de Ciencias Naturales y Museo-Universidad Nacional de La Address of author: Divisio Plata, Paseo del Bosque s/n, La Plata, B1900FWA, Buenos Aires, Argentina; CONICET, Consejo Nacional de Investigaciones Cientı´ficas y Tecnicas,
*Correspondence: e-mail: [email protected] With 2 figures and 3 tables Received April 2014; accepted for publication October 2014 doi: 10.1111/ahe.12158
Summary The greater rhea (Rhea americana) is the largest South American bird. It is a cursorial, flightless species with long powerful legs and reduced forelimbs. The goal of this study was to explore how hindlimb muscles scale with body mass during postnatal growth and to analyze whether the specialized locomotion of this species affects the growth of muscle masses. The mass of 19 muscles and body mass were weighed in 21 specimens ranging from 1-month-old individuals to adults. Seventeen muscles scaled with positive allometry with respect to body mass, whereas two muscles scaled isometrically. The predominance of positive allometric growth in hindlimb muscles results in a limb with massive and powerful muscles specialized to support a large body mass and to attain relatively high running speeds. Analysis of muscle mass scaling is a simple and useful way to compare possible differences between locomotor styles, and it is valuable in studies that reconstruct the paleobiology of extinct taxa.
Introduction Birds are exclusively bipedal because their forelimb functions as a wing during flight, while the hindlimbs are responsible for terrestrial movement (Hutchinson and Gatesy, 2001). Given that flight is the most striking locomotor mode, terrestrial locomotion has received relatively little attention, despite the fact that for many birds, locomotion on land plays an important ecological role (Verstappen et al., 2000). The morphology of the pelvic limbs vary according to the proportions of their skeletal elements (Gatesy and Middleton, 1997), the presence or absence of certain muscles (George and Berger, 1966) and the proportional development of these muscles relative to body mass (Hartman, 1961). Several studies have found that variations of hindlimb morphology can be correlated with different behaviours and habitats (Hartman, 1961; Bennett, 1996; Barbosa and Moreno, 1999; Zeffer et al., 2003). In general, the wide morphological variation is largely produced during ontogeny (Klingerberg, 1996; Jones and German, 2005). Also, during ontogeny, various traits may develop at different rates with respect to other body regions, a process known as ontogenetic allometry. This process
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may provide information on morpho-functional and adaptive aspects (Cardini and O’Higgins, 2005) as the deviations from isometry are often correlated with functional demands on the musculoskeletal system (Bennett, 1996). The greater rhea (Rhea americana) is the largest (1.50 m tall and 25 kg body mass) palaeognathous bird of South America; rheas, together with the emu (Dromaius novaehollandiae), cassowary (Casuarius casuarius, C. benetti, C. unappendiculatus), ostrich (Struthio camelus) and kiwi (Apteryx australis, A. owenii, A. haastii) form the taxon Ratitae (Slack et al., 2007; Bourdon et al., 2009; but see Smith et al., 2013). The Ratitae are flightless birds with powerful, elongated and massive hindlimbs and, with the exception of kiwis, present a specialized locomotor behaviour known as cursoriality (Coombs, 1978; Gatesy and Biewener, 1991; Abourachid and Renous, 2000). They are able to attain high running speeds (ranging between 50 and 70 km/h, depending on the species; Folch, 1992). Such a specialized locomotor behaviour may affect limb morphology throughout ontogeny (Lammers and German, 2002). For example, in the greater rhea some hindlimb bones, such as the tarsometatarsus, show positive allometric growth during the © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
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postnatal development, possibly related to cursoriality (Picasso, 2012). A long tarsometatarsus enables a longer stride which, in turn, favours an increase in locomotor speed (Gatesy and Biewener, 1991; Wolff, 1991; Abourachid and Renous, 2000). However, no information is available regarding the scaling of hindlimb muscle mass in this species, and for other birds, such data are relatively scarce and often limited in terms of the number of muscles examined (Helmi and Cracraft, 1977; Carrier and Leon, 1990; Bennett, 2008). As muscle mass is proportional to the maximum muscle power output (Alexander, 1974; Biewener and Roberts, 2000; Roberts, 2001), the purpose of this study is to document the scaling patterns of the hindlimb muscles of the greater rhea using the muscle mass as a simple way to obtain information about the potential power of a muscle available during locomotion (Hartman, 1961).
Table 1. Muscles studied, and their main functions
Hip Muscles
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Main functions
M. ambiens
Hip flexor, knee extensor Hip extensor Hip extensor Hip extensor Hip flexor Hip flexor and abductor Hip flexor and adductor Hip flexor and abductor Hip extensor Hip flexor abductor Hip extensor, adductor Pelvic girdle stabilization, adduction Knee extensor Knee flexor, hip extensor Ankle extensor Ankle extensor Ankle flexor Digits extensor
M. M. M. M. M. M. M. M. M. M. M. Knee and ankle muscles
caudofemoralis flexor cruris groupa iliotibialis lateralis iliotibialis cranialis iliotrocantericus caudalis iliotrocantericus medialis iliotrocantericus cranialis ischiofemoralis iliofemoralis externus puboischiofemoralis obturatorius medialisb
M. femorotibialis groupc M. iliofibularis M. gastrocnemius M. fibularis longus M. tibialis cranialis M. extensor digitorum longus M. flexor perforans et perforatus digiti II M. flexor perforans et perforatus digiti III M. flexor perforatus digiti II M. flexor perforatus digiti IIId M. flexor perforatus digiti IV M. flexor hallucis longus M. flexor digitorum longus
Materials and Methods Specimens and data collection A total of 21 healthy specimens of greater rhea obtained from various commercial farms located in Buenos Aires province, Argentina were studied. Specimens ranged from immature birds of 1–8 months of age (467 g–5 kg) to 2-year-old adult birds (10.5–22 kg). The birds were obtained from a slaughterhouse, and the birds were reared in accordance with Argentinean regulations for rhea farming. Body mass was measured using a digital scale (Denver Instrument, 0.01 g accuracy, 600 g capacity) for 1-monthold birds, and a hand-held scale (500 g accuracy, 50 kg capacity) for the remaining individuals, except specimens MLP 882 and 883 that were weighed using a digital scale (Sensotonic SE-500) with 100 g accuracy and 50 kg capacity (see Table 2). Functionally, muscles and tendons are intimately integrated, and their mechanical abilities as a unit far exceed the capabilities of the component alone (Roberts, 2002). Considering this, it was decided to weigh the muscles including both fleshy portions and their tendons. The muscles of one limb of each individual were carefully removed from their sites of origin and insertion and weighed with a digital scale (with 0.01 g accuracy and 600 g capacity). Table 1 shows the nineteen muscles that were studied, and their functions. Muscles that shared a similar function were weighed together (Table 1). The small muscles of the hindlimb (M. popliteus, M. obturatorius medialis and M. iliofemoralis internus and short muscles of the tarsometatarsus and digits) were not included in this study. Myological nomenclature follows Vanden Berge and Zweers (1993), and the identification of hindlimb muscles of the greater rhea was done according to Picasso (2010) (Fig. 1).
Muscle
Digital flexor group
a
M. flexor cruris medialis and M. flexor cruris were weighed together. Precise role is unknown. c M. femorotibialis lateralis, M. femorotibialis medialis and M. femorotibialis internus were weighed together. d All these muscles were weighed together. b
Ontogenetic scaling Body mass, the mass of each muscle and the total muscle mass of the hindlimb (i.e. the sum of all individual muscle masses) were log10-transformed and analyzed using the allometric equation: log y = log a + b log x, where b is the slope or allometric exponent that represents the ratio of specific growth rates (Huxley, 1932), a is the y-intercept, y is the muscle mass and x is the body mass. This equation derives from the growth function y = a xb first proposed by Huxley (1932) and Huxley and Teissier (1936). Expected coefficients under isometry are equal to 1, and deviations where b < 1 or b > 1 represent negative and positive allometry, respectively. These analyses were carried out by reduced major axis (RMA) regression using the software SMATR (v.2.0) (Falster et al., 2006). This method is a useful tool to describe how size
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(a)
variables are related because it assesses the relationship between x and y (Warton et al., 2006). Allometry was detected when 1.0 was not included in the 95% confidence interval of the regression slope (b). Possible differences between sexes were not evaluated due to the relatively small number of sexed specimens, which did not allow adequate statistical analysis, so the analyses were performed using pooled data.
(b)
Fig. 1. Schematic drawing of the main hindlimb muscles of the greater rhea; (a) lateral view, (b) medial view. Scale bar: 10 cm.
Fig. 1). Other muscles, such as the muscles M. iliotrochantericus caudalis, M. iliofibularis, M. femorotibialis, M. extensor digitorum longus and M. gastrocnemius showed moderate positive allometric exponents (values ~1.20). Total muscular mass showed a positive allometric relationship with body mass (slope 1.18, Table 3).
Discussion Muscle actions To produce a movement (or pattern of movements), muscles can act independently, concurrently or in sequence (Kardong, 2012). Thus, for the purposes of this study, muscle actions were simplified into extensor – flexor and adductor – abductor categories regarding limb movements during terrestrial locomotion. The interpretation of the main role of the muscles during terrestrial locomotion follows the works of Jacobson and Hollyday (1982), Gatesy (1999) and Smith et al. (2006) (Table 1). Results All the measurements obtained are listed in Table 2. Figure 2 and Table 3 show the results of the regression analyses for each muscle and for the total muscular mass of the hindlimb. R2-values ranged from 0.89 to 0.99, while b values ranged between 1.04 and 1.43. Except for M. tibialis cranialis and M. puboischiofemoralis, which showed isometric growth relative to body mass, all other muscles exhibited positive allometric growth patterns (Table 3). The M. iliotibialis lateralis, M. flexor cruris, M. fibularis longus and M. obturatorius medialis showed strong positive allometry with relatively high coefficients (range 1.30–1.43) (see also
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Scaling of the hindlimb muscle mass as a whole As a whole, the total hindlimb muscular mass of the greater rhea showed a positive allometric growth pattern (b = 1.18). In contrast, for the closely related ostrich, Smith et al. (2006) found an isometric relationship (b = 1.06) between the total hindlimb muscle mass and body mass. This disparity could be due to the use of different age ranges between the two studies. Smith et al. (2006) analyzed ostriches that ranged between 24 and 43 weeks of age, but birds younger than 6 months were not included. By contrast, this study utilized a broader range of ages because birds younger than 6 months were included. Regarding other not closely related birds, the hindlimb muscle mass of the non-cursorial ducks (Anatidae, Anseriformes) selected primarily for market weight, scaled with negative allometry (b = 0.70–0.87) (Maruyama et al., 1999). However, positive allometry (b = 1.18) between total hindlimb muscle mass and body mass has been found for neonates of non-cursorial geese and ducks (Anseriformes), shore birds (Charadriformes, Scolopacidae), gulls and terns (Laridae and Sternidae) and some non-anseriform aquatic birds (Rallidae, Podicipedidae) (Visser and Rikclefs, 1995). This pattern of growth in neonate precocial and semiprecocial birds is associated © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
15 500
10 500
19 000
18 000
20 000
22 000
5000
5000
4000
5000
3000
3000
4000
3000
484.72
618.85
544.98
466.90
2424.27
1154.52
2742.37
2707.74
3467.42
3825.12
1632.17
600.96
667.68
743.63
502.92
700.41
264.40
336.83
384.63
293.02
41.50
54.39
46.24
38.27
39.97
tmm.
4.47
1.85
6.63
5.54
8.05
8.34
5.25
1.67
2.47
2.29
1.46
2.00
0.76
0.72
0.84
0.97
0.13
0.13
0.10
0.07
0.10
am.
2.11
2.77
2.63
2.26
2.02
110.82
32.63
104.48
103.48
152.30
162.80
84.90
25.11
26.07
27.05
15.66
29.53
14.42
16.80
18.03
12.99
cf.
238.1
56.62
210.71
228.64
304.58
329.97
144.6
45.44
52.57
51.80
36.37
56.91
2.19
27.75
30.47
19.56
3.05
4.06
3.65
2.74
3.03
fcr.
4.27
5.62
5.11
0.56
4.17
344.82
118.89
417.71
409.74
488.06
588.56
246.18
104.70
92.8
99.17
69.76
99.57
34.36
41.81
45.49
32.91
ill.
133.74
50.43
118.03
141.9
174.91
217.23
85.20
28.96
34.06
35.48
20.67
33.46
14.16
22.69
21.94
15.04
2.60
3.63
3.03
3.20
2.43
ilc.
1.69
2.27
1.98
1.83
1.85
105.26
48.08
115.85
109.2
141.4
163.92
59.19
26.03
21.77
25.09
15.82
23.18
12.39
15.03
17.53
13.14
ic.
5.01
5.05
7.50
7.13
10.64
10.64
3.03
2.46
1.42
1.29
1.41
1.52
1.01
1.13
1.25
0.92
0.16
0.24
0.15
0.14
0.18
im.
8.24
5.15
9.42
11.7
15.25
13.95
5.050
2.70
2.96
3.62
1.61
3.16
1.61
1.84
2.61
1.63
0.24
0.33
0.23
0.20
0.26
icr.
18.36
9.12
18.66
14.11
20.87
19.06
9.16
5.76
3.17
4.54
3.31
4.41
2.12
2.97
2.81
2.48
0.42
0.51
0.43
0.28
0.32
isc.
10.28
7.60
9.96
8.88
15.42
11.55
5.87
2.46
2.79
2.53
1.96
2.10
1.20
0.94
1.29
1.23
0.25
0.22
0.19
0.19
0.16
iex.
32.93
27.56
24.73
30.22
39.66
48.09
15.69
12.76
9.94
8.40
8.26
9.13
5.39
5.63
6.35
5.68
1.06
1.42
1.10
1.01
1.02
pic.
109.68
30.62
122.03
103.80
190.84
164.53
58.76
25.84
25.79
24.23
16.69
27.11
9.18
12.86
15.11
10.11
0.97
1.32
0.99
0.91
0.90
om.
5.25
7.12
6.00
5.29
4.93
254.32
151.93
276.38
319.07
418.09
393.62
182.40
96.42
82.59
98.98
69.01
90.10
38.63
44.62
48.29
43.21
ft.
3.403
4.91
3.86
3.96
3.05
195.54
164.49
235.30
242.03
311.03
374.00
134.70
37.07
64.73
71.65
47.25
63.85
23.18
32.25
34.78
25.30
if.
417.05
205.25
580.84
476.01
583.02
636.32
313.44
88.13
115.15
145.03
94.10
120.83
51.04
55.17
67.29
53.71
7.73
9.51
7.83
7.59
7.54
gs.
2.13
3.09
2.35
1.98
1.97
178.81
86.89
247.40
251.33
273.45
299.1
126.11
26.51
53.20
59.53
38.47
54.26
16.93
18.29
23.72
16.75
fl.
1.91
2.41
2.09
1.94
1.85
66.38
41.54
96.79
70.52
91.63
102.38
41.89
20.71
20.73
28.95
19.46
23.6
10.97
10.79
15.1
10.87
tc.
25.4
13.69
27.63
22.47
29.07
32.72
14.77
5.73
6.99
7.08
4.6
7.76
2.74
3.18
3.97
3.01
0.45
0.61
0.54
0.42
0.41
edl.
158.88
91.15
219.97
146.23
189.80
240.20
92.36
40.53
46.44
44.92
35.51
46.34
21.24
21.65
26.60
22.51
3.49
4.02
3.84
3.45
3.59
df.
Muscle abbreviations bm.: body mass, tmm: total muscle mass. MLP: osteological appended collection of the Division Paleontologıa Vertebrados, Museo de La Plata, Argentina. am. (M. ambiens), cf. (M. caudofemoralis), fcr. (M. flexor cruris group), ill. (M. iliotibialis lateralis), ilc. (M. iliotibialis cranialis), ic. (M. iliotrocantericus caudalis), im. (M. iliotrocantericus medialis), icr. (M. iliotrocantericus cranialis), isc. (M. ischiofemoralis), iex. (M. iliofemoralis externus), pic.(M. puboischiofemoralis), om.(M. obturatorius medialis), ft. (M. femorotibialis group), if. (M. iliofibularis), gs. (M. gastrocnemius), fl. (M. fibularis longus), tc. (M. tibialis cranialis), edl. (M. extensor digitorum longus), df. (M. digital flexor group). a Approximate age.
Adult
MLP 880
8 month
MLP 882
Adult
5 months
MLP 887
Adult
5 months
MLP 886
MLP 879
5 months
MLP 885
MLP 878
5 months
MLP 884
Adult
3 months
MLP 891
Adult
3 months
MLP 890
MLP 897
3 months
MLP 889
MLP 877
9600
3 months
MLP 888
8 montha
1 month
MLP 896
Adult
1 month
MLP 895
MLP 883
1 month
MLP 894
MLP 876
4900
1 month
MLP 893
491.1
1 month
MLP 892
bm.
Age
Specimen
Table 2. Raw measurements (g) for each specimen studied
M. B. J. Picasso Leg muscles scaling of Greater Rhea
455
Leg muscles scaling of Greater Rhea
M. B. J. Picasso
(a) 3.0
flexor cruris
Table 3. Results of allometric analyses for each muscle and total muscle mass
iliotibialislateralis
2.5
iliotibialiscranialis iliotrochanterichuscaudalis
2.0
Muscles and Total muscle mass
R2
b
b lower CI
b upper CI
0.97 0.98 0.89 0.95 0.98 1.00
1.18 1.12 1.30 1.43 1.12 1.17
1.09 1.05 1.12 1.28 1.05 1.13
1.29 1.20 1.51 1.58 1.19 1.21
4.19 2.70 3.16 3.39 2.61 2.91
0.98
1.08
1.02
1.15
3.74
0.99
1.08
1.03
1.13
3.53
0.99 0.98 0.99 0.99
1.09 1.14 0.97 1.37
1.03 1.07 0.92 1.30
1.15 1.21 1.02 1.45
3.39 3.82 2.61 3.73
0.99 0.99 0.99 0.99 0.99 0.99
1.14 1.21 1.18 1.31 1.04 1.14
1.10 1.15 1.13 1.24 1.00 1.10
1.19 1.27 1.23 1.38 1.08 1.18
2.33 2.71 2.32 3.22 2.52 3.42
1.00 0.99
1.10 1.18
1.06 1.14
1.13 1.22
2.43 1.59
a
puboischiofemoralis
1.5
obturatoriusmedialis
1.0 0.5 0.0 –0.5 2.6
2.8
3.0
3.2
3.4
3.6
3.8
4.0
4.2
4.4
4.6
(b) 3.0
femorotibialis iliofibularis
2.5
gastrocnemius
2.0
tibialiscranialis
1.5
flexoresdigitii extensordigitorumlongus
1.0 0.5 0.0 –0.5 –1.0 2.6
2.8
3.0
3.2
3.4
3.6
3.8
4.0
4.2
4.4
4.6
Fig. 2. Linear regressions of log-transformed data describing the relationships between body mass and muscle mass; (a) pelvic muscles, (b) femoral and tibiotarsal muscles. For a better understanding of the figure, only pertinent muscles have been included.
with the generation of heat by shivering of the leg muscles (Choi et al., 1993). Unfortunately, no data have been published so far documenting whether this positive allometric relationship between leg muscles and body mass in these birds is maintained throughout postnatal life. In this regard, the deviation from isometry that characterizes the entire postnatal life of the greater rhea might be related to the functional demands of a larger body size and a specialized locomotion. Similar results have been found in other vertebrates such as mammalian bipedal hoppers (Alexander et al., 1981; Bennett and Taylor, 1995; McGowan et al., 2008). These studies of static allometry show a positive allometric scaling of hindlimb muscle mass with respect to body mass, whereas in quadrupeds, this relationship is isometric. Also, bipedal mammals tend to have larger leg muscles than quadrupeds (Alexander et al., 1981; Pollock and Shadwick, 1994). The same can be seen in the greater rhea, in which the hindlimb muscles tend to represent a large portion of body mass which may be as a consequence of the positive allometric growth of both extensor and flexors muscles. Leg muscles of the greater rhea represent between 8.5% and 15.8% of the body mass according to age (Picasso et al., 2012), and similar value were reported also for adults of the ostrich (Smith et al., 2006) and the emu (Patak and Baldwin, 1998). In this sense, positive allometric scaling of leg muscle mass in the
456
Hip muscles M. ambiens M. caudofemoralis M. flexor cruris M. iliotibialis lateralis M. iliotibialis cranialis M. iliotrocantericus caudalis M. iliotrocantericus medialis M. iliotrocantericus cranialis M. ischiofemoralis M. iliofemoralis externus M. puboischiofemoralisa M. obturatorius medialis Knee and ankle muscles M. femorotibialis M. iliofibularis M. gastrocnemius M. fibularis longus M. tibialis cranialisa M. extensor digitorum longus M. digital flexor group Total muscle mass CI, 95% confidence interval. Indicates isometry.
a
greater rhea could be one of the factors that contribute to maintain running performance with increasing body mass. However, further studies on muscular architecture and its scaling with body mass will be useful to complement and extend these inferences. Studies on these aspects in adult ostrich or in bipedal hoppers, like kangaroos, show that the hindlimb muscle architecture is optimized for maximizing force production and to support the body mass (Smith et al., 2006; McGowan et al., 2008). Allometric growth could also be related to locomotor parameters. Smith et al. (2010) found that in ostriches, as body mass increases with age, differences arise in kinematic parameters during locomotion, such as an increase in stride length. As ratite birds usually present similar kinematic parameters during locomotion (Gatesy and Biewener, 1991; Abourachid and Renous, 2000), it is plausible that the positive allometry of muscle masses in the greater rhea might be related to a shift in kinematic parameters as the animal grows and perfects its motion. Unfortunately, no kinetic or kinematics studies have been performed to date on R. americana. © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
Leg muscles scaling of Greater Rhea
M. B. J. Picasso
Scaling of individual muscles: a comparison with other birds Interesting questions arise when the allometric exponents for specific muscles of this species are compared with the same muscles in other birds. For example, the M. gastrocnemius (an antigravity muscle) of non-running birds such as the californian gull (Larus californicus) and the black noddy (Anous minutus) show an isometric growth pattern with respect to body mass during postnatal growth (Carrier and Leon, 1990; Bennett, 2008), whereas in the greater rhea, this muscle scaled positively with body mass. This pattern could be reflecting differences in locomotor style: in running birds such as the greater rhea, increasing speed is achieved by increase of their stride length (Gatesy and Biewener, 1991; Abourachid and Renous, 2000), and for this, extension of the ankle joint is key, because it lengthens the limb and propels the body forward (Smith et al., 2006). Thus, the extensor muscles of this joint have a particularly important role in providing the power required for effective high speed locomotion (Smith et al., 2006). This is reflected by the positive allometry observed. The M. iliofibularis, which flexes the knee joint and is a hip extensor, scaled positively with body mass both in the greater rhea and the chicken (Gallus gallus) (Helmi and Cracraft, 1977). This might be associated with the evolution of bird bipedalism, in which the movement of the hindlimb became knee-dominated in contrast with the femoral retraction pattern observed in crocodilians and limbed lepidosaurs (Gatesy, 1990; Hutchinson, 2002). The M. puboischiofemioralis and M. tibialis cranialis grew isometrically. Helmi and Cracraft (1977) found a similar pattern of growth in the M. puboischiofemoralis of the chicken, the mass of this muscle remained isometric with increasing body mass, but the length of this muscle presented positive allometry. Unfortunately, there is no information about postnatal scaling of M. tibialis cranialis. The isometric growth pattern of muscle mass might possibly reflect their more general function in avian hindlimb, not related to a specific adaptation. Nevertheless, further studies on muscle architecture of these muscles will contribute to explore the scaling patterns of other features such as fascicle length and physiological cross sectional area, and to understand their relationship with functional aspects. As a large running bird, the greater rhea presents allometric growth of the hindlimb musculoskeletal system. This positive allometry found for almost all muscles, together with that of the bones, such as tarsometatarsus length (Picasso, 2012), results in a long limb with massive and powerful muscles, specialized to support a large body mass and to attain relatively high running speeds.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 452–459
Final conclusions and future directions Muscle mass data are simple to obtain and can be used to explore the relative functional importance of individual muscles or muscle groups in the maintenance of posture, joint movements and locomotor performance. In addition, the information derived from modern species can be usefully applied to paleontological studies in which muscle mass cannot be measured, but can be reconstructed (e.g. Hutchinson, 2004a,b; Hutchinson et al., 2011). Birds are an extant clade of theropod dinosaurs (Gauthier, 1986; Farlow et al., 2000), a group characterized by bipedal locomotion and digitigrady. Thus, studies of morpho-functional aspects of bipedalism in extant birds become essential to understand non-avian theropod locomotion (Farlow et al., 2000; Hutchinson, 2004a,b). Further research that focuses on growth patterns of hindlimb muscle masses of birds with different terrestrial locomotor styles is needed to shed light on the variation of muscular growth patterns. In addition, studies on muscle architecture and kinetics, and on the kinematics of the greater rhea, will also contribute to the knowledge of myological specializations for cursorial locomotion and will expand and enhance the present findings. Acknowledgements The author thanks F.J. Degrange for his friendship, help and support during the dissections and C.C. Morgan for her useful comments. C.C. Morgan and C. Mosto improved the English version of this paper.
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