Muscle enzyme activities in a deep‐sea squaloid shark, Centroscyllium fabricii, compared with its shallow‐living relative, Squalus acanthias

Abstract

The activities of several enzymes of energy metabolism were measured in the heart, red muscle, and white muscle of a deep and a shallow living squaloid shark, Centroscyllium fabricii and Squalus acanthias, respectively. The phylogenetic closeness of these species, combined with their active predatory nature, similar body form, and size makes them well matched for comparison. This is the first time such a comparison has been made involving a deep-sea elasmobranch. Enzyme activities were similar in the heart, but generally lower in the red muscle of C. fabricii. Paralleling the trend seen in deep-sea teleosts, the white muscle of C. fabricii had substantially lower activities of key glycolytic enzymes, pyruvate kinase and lactate dehydrogenase, relative to S. acanthias or other shallow living elasmobranchs. Unexpectedly, between the squaloid sharks examined, creatine phosphokinase activity was higher in all tissues of the deep living C. fabricii. Low white muscle glycolytic enzyme activities in the deep-sea species coupled with high creatine phosphokinase activity suggests that the capacity for short burst swimming is likely limited once creatine phosphate supplies have been exhausted.

Aerobic and anaerobic enzyme activity in the hake Merluccius gayi gayi related to the Oxygen Minimum Zone off central-southern Chile

“…This support the predominance of aerobic metabolism in all the tissues except muscle, agreeing with other studies carried out on fish (Childress & Somero 1979, Yang et al 1992, Panepucci et al 2000, Panepucci et al 2001, Treberg et al 2003 and most vertebrates (Hochachka & Somero 1973).…”

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

“…In white muscle of teleosts, the activities of enzymes related to glycolytic capacity decrease in correlation with the depth-related decline in whole-animal oxygen consumption rate . Glycolytic enzyme activities also decrease with depth in white muscle of chondrichthyans, implying similarly low metabolic rates as deep-sea teleosts (Condon et al, 2012;Drazen and Seibel, 2007;Treberg et al, 2003). 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).…”

“…Glycolytic enzyme activities also decrease with depth in white muscle of chondrichthyans, implying similarly low metabolic rates as deep-sea teleosts (Condon et al, 2012;Drazen and Seibel, 2007;Treberg et al, 2003). 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.…”

“…et al, 2012; Dickson et al, 1993;Kryvi et al, 1981;Treberg et al, 2003). Deep-sea chondrichthyans and teleosts swim at similar, slow speeds (∼0.1-0.3 m s −1 ) (Bagley et al, 1994;Carey and Clark, 1995;Watanabe et al, 2012), so the retention in deep-sea chondrichthyans of greater metabolic capacity in red muscle and aerobic capacity in white muscle suggests a greater reliance upon sustained swimming compared with deep-sea teleosts.…”

The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities

“…Oxygen consumption rates have now been measured for deep-and shallow-living representatives of many major phyla, both benthic and pelagic, and in several regions. Biochemical proxies of metabolism have provided estimates of metabolic capacity in many additional species (Torres & Somero 1988;Childress & Somero 1990;Seibel et al 1998Drazen 2002a;Seibel & Walsh 2003;Treberg et al 2003;Dalhoff 2004;Thuesen et al 2005b), while submersibles, landers and new tagging techniques have provided detailed studies of locomotion and behaviour in the deep sea (Priede et al 1990;Marshall & Diebel 1995;Villanueva et al 1997;Hunt & Seibel 2000;Bailey et al 2003Bailey et al , 2005Drazen & Robison 2004;Robison 2004;Seibel et al 2005). More than 10 years have passed since the last specific reviews of deep-sea metabolic rates (Childress 1995;Mahaut et al 1995).…”