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

Rose, Kayleigh; Tickle, Peter G.; Elsey, Ruth M.; Sellers, William I.; Crossley, Dane A.; Codd, Jonathan R.

doi:10.1111/joa.13523

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

Kayleigh Rose

, Peter G. Tickle, Ruth M. Elsey, William I. Sellers, Dane A. Crossley, Jonathan R. Codd

Journal of Anatomy, Volume: 239, Issue: 6

Swansea University Author: Kayleigh Rose

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DOI (Published version): 10.1111/joa.13523

Abstract

Quantitative functional anatomy of amniote thoracic and abdominal regions is cru-cial 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 (a...

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Published in:	Journal of Anatomy
ISSN:	0021-8782 1469-7580
Published:	Wiley 2021
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URI:	https://cronfa.swan.ac.uk/Record/cronfa57450
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However, the inherent flexibility of these systems is not well studied, and the functional spe-cialisation 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 mus-cle 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, ili-ocostalis), 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 contrac-tion 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 expira-tory 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 in-dicate a decreased reliance on this muscle with ontogeny. Collectively, these find-ings would support existing anecdotal evidence that crocodilians shift their breathing mechanics as they increase in size. 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spelling	2021-12-06T15:38:34.3697470 v2 57450 2021-07-25 Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms 83a47731b96af0d69fcbdb6c4c5a20aa 0000-0001-7023-2809 Kayleigh Rose Kayleigh Rose true false 2021-07-25 SBI Quantitative functional anatomy of amniote thoracic and abdominal regions is cru-cial 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 spe-cialisation 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 mus-cle 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, ili-ocostalis), 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 contrac-tion 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 expira-tory 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 in-dicate a decreased reliance on this muscle with ontogeny. Collectively, these find-ings 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 Journal Article Journal of Anatomy 239 6 Wiley 0021-8782 1469-7580 allometry, archosaur, axial anatomy, breathing, crocodilian, flexibility, locomotion, muscle architecture, ventilatory mechanics 23 7 2021 2021-07-23 10.1111/joa.13523 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University Another institution paid the OA fee This research was supported by fund-ing from the National Science Foundation (NSF- 17565187) to DAC and the Biotechnology and Biological Sciences Research Councils (BBSRC– BB/I021116/1) to JRC. NSF- 17565187, BBSRC– BB/I021116/1 2021-12-06T15:38:34.3697470 2021-07-25T12:44:00.5440877 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Kayleigh Rose 0000-0001-7023-2809 1 Peter G. Tickle 2 Ruth M. Elsey 3 William I. Sellers 4 Dane A. Crossley 5 Jonathan R. Codd 6 57450__20678__adec15fb855d42fea66ae045ff2e8ce1.pdf 57450.pdf 2021-08-19T14:58:02.1382351 Output 2168995 application/pdf Version of Record true © 2021 The Authors. This is an open access article under the terms of the Creative Commons Attribution License true eng http://creativecommons.org/licenses/by/4.0/
title	Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms
spellingShingle	Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms Kayleigh Rose
title_short	Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms
title_full	Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms
title_fullStr	Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms
title_full_unstemmed	Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms
title_sort	Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms
author_id_str_mv	83a47731b96af0d69fcbdb6c4c5a20aa
author_id_fullname_str_mv	83a47731b96af0d69fcbdb6c4c5a20aa_***_Kayleigh Rose
author	Kayleigh Rose
author2	Kayleigh Rose Peter G. Tickle Ruth M. Elsey William I. Sellers Dane A. Crossley Jonathan R. Codd
format	Journal article
container_title	Journal of Anatomy
container_volume	239
container_issue	6
publishDate	2021
institution	Swansea University
issn	0021-8782 1469-7580
doi_str_mv	10.1111/joa.13523
publisher	Wiley
college_str	Faculty of Science and Engineering
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hierarchy_top_title	Faculty of Science and Engineering
hierarchy_parent_id	facultyofscienceandengineering
hierarchy_parent_title	Faculty of Science and Engineering
department_str	School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
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description	Quantitative functional anatomy of amniote thoracic and abdominal regions is cru-cial 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 spe-cialisation 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 mus-cle 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, ili-ocostalis), 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 contrac-tion 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 expira-tory 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 in-dicate a decreased reliance on this muscle with ontogeny. Collectively, these find-ings 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
published_date	2021-07-23T04:13:12Z
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score	11.012678

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

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