Mechanical specialization of the obliquely striated circular mantle muscle fibres of the long-finned squidDoryteuthis pealeii

Abstract

SUMMARYThe centrally located, mitochondria-poor (CMP) and superficially located,mitochondria-rich (SMR) circular muscle fibres in the mantles of some squids provide one of the few known examples of specialization in an obliquely striated muscle. Little is known of the mechanical properties or of the mechanisms and performance consequences of specialization in these fibres. We combined morphological and physiological approaches to study specialization in the SMR and CMP fibres of the long-finned squid Doryteuthis pealeii. The mean thick filament length was 3.12±0.56 μm and 1.78±0.27μm for the SMR and CMP fibres, respectively. The cross-sectional areas of the whole fibre and the core of mitochondria were significantly higher in the SMR fibres, but the area occupied by the myofilaments did not differ between the two fibre types. The area of sarcoplasmic reticulum visible in cross sections was significantly higher in CMP fibres than in SMR fibres. In live bundles of muscle fibres partially isolated from the mantle, mean peak isometric stress during tetanus was significantly greater in SMR [335 mN mm–2 physiological cross section (pcs)] than in CMP (216 mN mm–2 pcs) fibres. SMR fibres had a lower average twitch:tetanus ratio (SMR=0.073; CMP=0.18) and a twofold lower unloaded maximum shortening velocity at 20°C (SMR=2.4 L0s–1; CMP=5.1 L0 s–1),where L0 was the preparation length that yielded the highest tetanic force. The structural differences in the two muscle fibre types play a primary role in determining their mechanical properties, and the significant differences in mechanical properties indicate that squid have two muscle gears. A simple model of the mantle shows that a gradient of strain and strain rate exists across the mantle wall, with fibres adjacent to the outer edge of the mantle experiencing 1.3- to 1.4-fold lower strain and strain rate than fibres adjacent to the inner edge of the mantle. The model also predicts that the CMP fibres generate virtually no power for slow jetting while the SMR fibres are too slow to generate power for the escape jets. The transmural differences in strain and strain rate predicted by the model apply to any cylindrical animal that has circumferentially oriented muscle fibres and an internal body cavity.