Analogues of red and white muscle in squid mantle

Abstract

In five species of squid, varying in life-style from fast-swimming pelagic predators to sluggish benthic forms, the circular muscle of the mantle was found to be metabolically and structurally differentiated into inner, middle, and outer zones. In the middle zone, mitochondrial abundance and the ratios of oxidative to glycolytic enzyme activities were low. This zone was sandwiched between thinner bands of muscle lining both the inner and outer edges of the mantle. In these bands, mitochondrial abundance and the ratios of oxidative to glycolytic enzyme activities were high. It is proposed that this metabolic differentiation is analogous to the development of red and white muscles in vertebrates and that it serves a similar function, white muscle mainly supporting burst-type swimming and red muscle sustaining steadystate oxidative work.Ofall the Mollusca, squid are by far the most capable swimmers, some being able to attain speeds of 10-15 knots (1, 2). These speeds are attained by cyclic inhalant and exhalant movements of the mantle muscle to produce a characteristic jet propulsion movement. From visual observations of pelagic squid, at least two kinds of swimming (steady-state and burst) can be clearly deciphered. In vertebrates (3), and fish in particular, red, intermediate, and white muscle types are specialized for these two kinds of locomotion, although there may be some overlapping functions in active species like the tuna (4). However, except for a few casual observations (5), such an organization has never been described in cephalopods (6).In reexamining this problem in a number of squid species, we have found clear evidence of metabolic differentiation ofthe mantle musculature. In one common pattern, found in Loligo opalescens, two distinct bands on the inner and outer edge of the mantle are specialized toward a highly oxidative metabolism, whereas the middle mantle displays a higher dependence on anaerobic glycolysis. Evidence from enzyme measurements, histochemistry, and polarized light plus interference contrast microscopy indicates that, compared to the middle mantle, the two oxidative bands ofmuscle display relatively higher activities of oxidative enzymes, higher mitochondrial abundance, and lower myofibrillar density. Variations on this theme were observed in the five squid species examined. While this work was in progress, parallel and independent studies on Alloteuthis (7) showed greater mitochondrial abundance and capillarity in outer and inner bands of the mantle, thus confirming and extending our observations.

Critical temperatures in the cephalopodSepia officinalisinvestigated usingin vivo31P NMR spectroscopy

“…We thus conclude that an energetic limitation of radial muscle fibres is responsible for the observed increases in [P i ] and the correlated decreases in ventilation pressures once phosphagen usage starts. Radial fibres have a mitochondrial content as low as that of central 'anaerobic' circular fibres (Bone et al, 1981;Mommsen et al, 1981) and thus may be especially sensitive to enduring ventilation exercise at high intensities. Considering that radial fibres constitute about 30% of total mantle volume in the cuttlefish (Milligan et al, 1997), and assuming that solely radial fibres deplete their phosphagen stores as ventilation pressures increase while, on the other hand, circular fibre energy status remains constant, it is possible to estimate metabolite changes for the radial fibre compartment.…”

“…The inner and outer layers of circular fibres possess high densities of mitochondria (Bone et al, 1981;Mommsen et al, 1981), leading to enhanced baseline oxygen demand. Approximately 30% of the mantle volume consists of radial muscle fibres that have a key role in ventilation (Milligan et al, 1997).…”

Ontogeny of mantle musculature and implications for jet locomotion in oval squidSepioteuthis lessoniana

“…The radial muscle fibres are also uninucleate and may be up to 5·m in diameter (Bone et al, 1981;Mommsen et al, 1981). In both radial and circular muscles, the myofilament array surrounds a core of mitochondria and the single nucleus (Marceau, 1905;Hanson and Lowy, 1957).…”

Muscle specialization in the squid motor system

“…Although aspects of the biochemistry and ultrastructure of squid mantle and fin muscle fibres relevant to their aerobic capacity have been studied previously (Bone et al, 1981;Kier, 1989;Mommsen et al, 1981), the biochemistry of the myofilaments of the mantle and fin muscle fibres, and indeed other cephalopod muscle fibres, has not yet been analysed. A comparative analysis is needed of myofilament biochemistry from a diverse sample of fibres that differ in contractile properties.…”