Scaling of buccal mass growth and muscle activation determine the duration of feeding behaviors in the marine mollusc Aplysia californica.

Allometry Biting Buccal Mass Elastic forces Micro-CT Muscle Forces Slow Movement Swallowing

Journal

The Journal of experimental biology
ISSN: 1477-9145
Titre abrégé: J Exp Biol
Pays: England
ID NLM: 0243705

Informations de publication

Date de publication:
08 Apr 2024
Historique:
received: 18 08 2023
accepted: 12 03 2024
medline: 8 4 2024
pubmed: 8 4 2024
entrez: 8 4 2024
Statut: aheadofprint

Résumé

The mechanical forces experienced during movement and the time constants of muscle activation are important determinants of the durations of behaviors, which may both be affected by size-dependent scaling. The mechanics of slow movements in small animals are dominated by elastic forces and are thus quasistatic (i.e., always near mechanical equilibrium). Muscular forces producing movement and elastic forces resisting movement should both scale identically (proportional to mass⅔), leaving the scaling of the time constant of muscle activation to play a critical role in determining behavioral duration. We tested this hypothesis by measuring the duration of feeding behaviors in the marine mollusc Aplysia californica whose body sizes spanned three orders of magnitude. The duration of muscle activation was determined by measuring the time it took for muscles to produce maximum force as Aplysia attempted to feed on tethered inedible seaweed, which provided an in vivo approximation of an isometric contraction. The timing of muscle activation scaled with mass0.3. The total duration of biting behaviors scaled identically, with mass0.3, indicating a lack of additional mechanical effects. The duration of swallowing behavior, however, exhibited a shallower scaling of mass0.17. We suggest that this was due to the allometric growth of the anterior retractor muscle during development, as measured by micro computed tomography scans (microCT) of buccal masses. Consequently, larger Aplysia did not need to activate their muscles as fully to produce equivalent forces. These results indicate that muscle activation may be an important determinant of the scaling of behavioral durations in quasistatic systems.

Identifiants

pubmed: 38584490
pii: 346508
doi: 10.1242/jeb.246551
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : UK Research and Innovation
ID : MR/T046619/1
Organisme : National Science Foundation
ID : DBI 2015317
Organisme : Royal Society
ID : UF130507

Informations de copyright

© 2024. Published by The Company of Biologists Ltd.

Auteurs

Stephen M Rogers (SM)

Department of Life Sciences, University of Lincoln, Brayford Pool Campus, Lincoln LN6 7TS, UK.

Jeffery P Gill (JP)

Department of Biology, Case Western Reserve University, Cleveland, Ohio 44106-7080, USA.

Ana Skalski De Campos (AS)

Department of Biology, Case Western Reserve University, Cleveland, Ohio 44106-7080, USA.

Katherine Wang (K)

Department of Biology, Case Western Reserve University, Cleveland, Ohio 44106-7080, USA.

Gregory P Sutton (GP)

Department of Life Sciences, University of Lincoln, Brayford Pool Campus, Lincoln LN6 7TS, UK.

Hillel J Chiel (HJ)

Departments of Biology, Neurosciences, and Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106-7080, USA.

Classifications MeSH