Comparative studies of high performance swimming in sharks I. Red muscle morphometrics, vascularization and ultrastructure

Abstract

SUMMARYTunas (family Scombridae) and sharks in the family Lamnidae are highly convergent for features commonly related to efficient and high-performance(i.e. sustained, aerobic) swimming. High-performance swimming by fishes requires adaptations augmenting the delivery, transfer and utilization of O2 by the red myotomal muscle (RM), which powers continuous swimming. Tuna swimming performance is enhanced by a unique anterior and centrally positioned RM (i.e. closer to the vertebral column) and by structural features (relatively small fiber diameter, high capillary density and greater myoglobin concentration) increasing O2 flux from RM capillaries to the mitochondria. A study of the structural and biochemical features of the mako shark (Isurus oxyrinchus) RM was undertaken to enable performance-capacity comparisons of tuna and lamnid RM. Similar to tunas, mako RM is positioned centrally and more anterior in the body. Another lamnid, the salmon shark (Lamna ditropis), also has this RM distribution, as does the closely related common thresher shark (Alopias vulpinus; family Alopiidae). However, in both the leopard shark(Triakis semifasciata) and the blue shark (Prionace glauca),RM occupies the position where it is typically found in most fishes; more posterior and along the lateral edge of the body. Comparisons among sharks in this study revealed no differences in the total RM quantity (approximately 2–3% of body mass) and, irrespective of position within the body, RM scaling is isometric in all species. Sharks thus have less RM than do tunas(4–13% of body mass). Relative to published data on other shark species,mako RM appears to have a higher capillary density, a greater capillary-to-fiber ratio and a higher myoglobin concentration. However, mako RM fiber size does not differ from that reported for other shark species and the total volume of mitochondria in mako RM is similar to that reported for other sharks and for tunas. Lamnid RM properties thus suggest a higher O2 flux capacity than in other sharks; however, lamnid RM aerobic capacity appears to be less than that of tuna RM.

Does the physiology of chondrichthyan fishes constrain their distribution in the deep sea?

“…By contrast, the aerobic enzyme activities in both types of muscles decline with depth in teleosts but not in chondrichthyans (Condon et al, 2012;Dickson et al, 1993;Drazen et al, 2013;Drazen and Seibel, 2007;SpeersRoesch et al, 2006;Treberg et al, 2003). Other red muscle aerobic/oxidative properties are comparable between deep-sea and shallow demersal chondrichthyans (Bernal et al, 2003 The deep sea can be broadly defined as depths >200 m, incorporating the midwater (200-1000 m), bathyal (1000-4000 m), abyssal (>4000 m) and hadal (trenches >6000 m) zones. The deep sea is characterized by five major environmental characteristics that pose challenges to the persistence of animal life (Herring, 2002).…”

Red muscle function in stiff-bodied swimmers: there and almost back again

“…Bernal & Sepulveda [24] recently confirmed speculations of red muscle endothermy in the common thresher shark, as suggested by the presence of a vascular counter-current heat exchanger [22]. A detailed account of red muscle distribution in the three thresher species reveals patterns consistent with those noted in other fishes with either superficial or internalized red muscle [18,23]. Specifically, all three species possess about the same relative amount of red muscles, similar to other sharks studied (2.3 -3.0% of body mass), being distributed along the length of the body, including in the tail.…”

Oxygen utilization and the branchial pressure gradient during ram ventilation of the shortfin mako,Isurus oxyrinchus: is lamnid shark–tuna convergence constrained by elasmobranch gill morphology?

“…Specifically, the interlamellar channel width in the mako is approximately twice that of tunas, N. C. Wegner and others resulting in one-half the lamellar frequency and one-half the gill surface area (Wegner et al, 2010b). This smaller respiratory area results in a lower volume of water that can be processed by the gills per unit time and this likely contributes to a reduced aerobic capacity in lamnids when compared with tunas, as manifested by lower aerobic enzyme activities, smaller amounts of red muscle and reduced sustainable swimming speeds (Bernal et al, 2003a;Bernal et al, 2003b;Sepulveda et al, 2007).…”

“…However, it is now well established that lamnid aerobic capacity is less than that of tunas. Lamnids have lower mitochondrial densities and aerobic enzyme activities (Bernal et al, 2003b), smaller gill surface areas (Muir, 1969;Emery and Szczepanski, 1986;Wegner et al, 2010a;Wegner et al, 2010b) and lower amounts of red muscle (Graham et al, 1983;Bernal et al, 2003a). Water-tunnel studies also indicate that the maximum sustainable swimming speed of the shortfin mako is much lower than that of tunas (Dewar and Graham, 1994;Blank et al, 2007;Sepulveda et al, 2007).…”