Ontogenetic scaling patterns and functional anatomy of the pelvic limb musculature in emus (Dromaius novaehollandiae)

Abstract

Emus (Dromaius novaehollandiae) are exclusively terrestrial, bipedal and cursorial ratites with some similar biomechanical characteristics to humans. Their growth rates are impressive, as their body mass increases eighty-fold from hatching to adulthood whilst maintaining the same mode of locomotion throughout life. These ontogenetic characteristics stimulate biomechanical questions about the strategies that allow emus to cope with their rapid growth and locomotion, which can be partly addressed via scaling (allometric) analysis of morphology. In this study we have collected pelvic limb anatomical data (muscle architecture, tendon length, tendon mass and bone lengths) and calculated muscle physiological cross sectional area (PCSA) and average tendon cross sectional area from emus across three ontogenetic stages (n = 17, body masses from 3.6 to 42 kg). The data were analysed by reduced major axis regression to determine how these biomechanically relevant aspects of morphology scaled with body mass. Muscle mass and PCSA showed a marked trend towards positive allometry (26 and 27 out of 34 muscles respectively) and fascicle length showed a more mixed scaling pattern. The long tendons of the main digital flexors scaled with positive allometry for all characteristics whilst other tendons demonstrated a less clear scaling pattern. Finally, the two longer bones of the limb (tibiotarsus and tarsometatarsus) also exhibited positive allometry for length, and two others (femur and first phalanx of digit III) had trends towards isometry. These results indicate that emus experience a relative increase in their muscle force-generating capacities, as well as potentially increasing the force-sustaining capacities of their tendons, as they grow. Furthermore, we have clarified anatomical descriptions and provided illustrations of the pelvic limb muscle-tendon units in emus.

Keywords: Biomechanics; Bone; Emu; Locomotion; Muscle; Palaeognathae; Ratite; Scaling; Tendon.

Figure 1. Schematic anatomical representation of Emu pelvic limb anatomy.

Schematic anatomical representation of the most superficial layer of muscles, in lateral view, of the pelvic limb of an adult emu.

Figure 2. Schematic anatomical representation of Emu pelvic limb anatomy.

Schematic anatomical representation of the intermediate layer of muscles, from a lateral view, of the pelvic limb of an adult emu.

Figure 3. Schematic anatomical representation of Emu pelvic limb anatomy.

Schematic anatomical representation of the deeper layer of muscles, from a lateral view, of the pelvic limb of an adult emu.

Figure 4. Normalized data: 16 month old group only.

Normalized relative muscle parameters for individual muscles in emu pelvic limbs of the 16 month old birds only (Group 3; mean body mass 38.5 kg); mean values (error bars showing ±1 S.D.) are shown. Abbreviations for muscles are in Table 1. The key on the right side of the figure shows how muscle mass (M_m), physiological cross-sectional area (PCSA), and fascicle length (L_f) were normalized. L_f values were adjusted to be 1/10 of the actual results in order to be of similar magnitude to the others. Muscles are organised from top to bottom in decreasing order of muscle mass.

Figure 5. Ontogenetic scaling exponents of muscle properties.

Ontogenetic scaling exponents and 95% confidence intervals (shown as error bars around mean exponent) for muscle mass (red), PCSA (blue) and fascicle length (green) for individual muscles in emu pelvic limbs. Abbreviations for muscles are in Table 1. Dashed lines indicate the expected isometric scaling exponent for each parameter. Data are for (A) proximal limb muscles and (B) distal limb muscles.

Figure 6. Ontogenetic scaling exponents and 95% confidence intervals for masses of individual muscles in emu pelvic limbs, from the USA group.

Abbreviations for muscles are in Table 1. Dashed line indicates the expected isometric scaling exponent (1.0), and the number above each parameter indicates the number of muscles included in each regression analysis.

Figure 7. Ontogenetic scaling exponents of tendon properties.

Ontogenetic scaling exponents and 95% confidence intervals for tendon mass (red), average cross-sectional area (blue) and length (green) for 20 individual muscles in emu pelvic limbs. Abbreviations for muscles are in Table 1. Dashed lines indicate the expected isometric scaling exponent for each parameter.