Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms

Abstract

Quantitative functional anatomy of amniote thoracic and abdominal regions is crucial to understanding constraints on and adaptations for facilitating simultaneous breathing and locomotion. Crocodilians have diverse locomotor modes and variable breathing mechanics facilitated by basal and derived (accessory) muscles. However, the inherent flexibility of these systems is not well studied, and the functional specialisation of the crocodilian trunk is yet to be investigated. Increases in body size and trunk stiffness would be expected to cause a disproportionate increase in muscle force demands and therefore constrain the basal costal aspiration mechanism, necessitating changes in respiratory mechanics. Here, we describe the anatomy of the trunk muscles, their properties that determine muscle performance (mass, length and physiological cross-sectional area [PCSA]) and investigate their scaling in juvenile Alligator mississippiensis spanning an order of magnitude in body mass (359 g-5.5 kg). Comparatively, the expiratory muscles (transversus abdominis, rectus abdominis, iliocostalis), which compress the trunk, have greater relative PCSA being specialised for greater force-generating capacity, while the inspiratory muscles (diaphragmaticus, truncocaudalis ischiotruncus, ischiopubis), which create negative internal pressure, have greater relative fascicle lengths, being adapted for greater working range and contraction velocity. Fascicle lengths of the accessory diaphragmaticus scaled with positive allometry in the alligators examined, enhancing contractile capacity, in line with this muscle's ability to modulate both tidal volume and breathing frequency in response to energetic demand during terrestrial locomotion. The iliocostalis, an accessory expiratory muscle, also demonstrated positive allometry in fascicle lengths and mass. All accessory muscles of the infrapubic abdominal wall demonstrated positive allometry in PCSA, which would enhance their force-generating capacity. Conversely, the basal tetrapod expiratory pump (transversus abdominis) scaled isometrically, which may indicate a decreased reliance on this muscle with ontogeny. Collectively, these findings would support existing anecdotal evidence that crocodilians shift their breathing mechanics as they increase in size. Furthermore, the functional specialisation of the diaphragmaticus and compliance of the body wall in the lumbar region against which it works may contribute to low-cost breathing in crocodilians.

Keywords: allometry; archosaur; axial anatomy; breathing; crocodilian; flexibility; locomotion; muscle architecture; ventilatory mechanics.

FIGURE 1

Scaling of snout‐vent length with body mass in specimens ranging 0.359–5.497 kg

FIGURE 2

Lateral view of the anatomy of the trunk in Alligator mississippiensis. Anterior is to the left. a) The tripartite ribs 1–8 including the sternal (ventral), intermediate (lateral) and vertebral (dorsal) rib elements and their uncinate processes. Subsequent panels illustrate muscle layers from superficial to deep. b) The iliocostalis (IC) is covered by a thick fascia (the dorsal fascia) in the thoracic region which was only visible in specimens with SVL >0.40 m and body mass >1.77 kg. The obliquus externus superficialis (OES) attaches the ventrolateral IC, medial to the dorsal fascia; the rectus abdominis (RA) and the truncocaudalis (TC) attach to the ventrolateral rim of the OES and make up the ventral body wall. c) Following the removal of the dorsal fascia and OES, the IC lies with a myotomal arrangement across and between the verterbral ribs, while the obliquus externus profundus (OEP) is connected strongly to the ventral rim of the IC, dorsal lateral rims of the RA and TC. d) The intercostales externi dorsales and ventrales (IED and IEV) occupy the vertebral and intermediate intercostal spaces, respectively. The obliquus internus (OI) attaches to the ventral rim of the IC in the lumbar region (dotted line). e) The intercostales interni (II) occupy the spaces between both the sternal and the intermediate rib elements. The OI is continuous from the II. f) The intercostales internalis dorsalis longus (ICID) and transversus abdominis (TA). Notice how the TA extends dorsally only as far as the intermediate rib elements and the ICID occupy only the distal ends of the vertebral rib elements. The transversus abdominis (TA) is medial to the OI and also attached to the ventral rim of the IC as well as the mediolateral edge of the RA together with the eighth and floating sternal rib

FIGURE 3

Ventral view of the muscles of the infrapubic abdominal wall in Alligator mississippiensis. a) The truncocaudalis (TC), ischiotruncus (ISCHU) and ischiopubis (ISP). The ISP was always darker in colouration and a thick fat pad always lay beneath it. b) Following removal of the TC and ISCHU. The ISP and fat pad have also been removed from the specimen's left side, revealing the pubio‐ischio femoralis (PIF). c) Origin of the diaphragmaticus on the last gastralial set

FIGURE 4

Size‐normalised trunk muscle architectural properties. a) Mean ± SD relative muscle masses. Masses of the pectoralis (PEC) and serratus (SER) are also included for comparison. b) Function space plot of axial muscles. Normalised PCSA (PCSA/body mass^(0.67)) is plotted against normalised fascicle length (Fascicle length/body mass^(0.33)) with one data point per muscle per individual. c) Rectus abdominis (RA) and iliocostalis (IC). d) Transversus abdominis (TA), obliquus externus superficialis (OES), obliquus externus profundus (OEP), ischiopubis (ISP), ischiotruncus (ISCHU), truncocaudalis (TC) and diaphragmaticus (DI). Data points for expiratory and inspiratory muscles are denoted by a ‘+’ and ‘−’, respectively. Circles represent muscles whose potential roles in breathing have not yet been investigated

FIGURE 5

Scaling exponents for muscle architectural properties versus body mass. Boxes indicate the exponent and 95% CIs. Horizonal lines indicate exponent value for isometry in length (yellow, 0.33) PCSA (blue, 0.67) and mass (red, 1)