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Muscle Enzyme Activities in a Deep-Sea Squaloid Shark, Centroscyllium Fabricii, Compared with Its Shallow-Living Relative, Squalus Acanthias JASON R

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Muscle Enzyme Activities in a Deep-Sea Squaloid Shark, Centroscyllium Fabricii, Compared with Its Shallow-Living Relative, Squalus Acanthias JASON R JOURNAL OF EXPERIMENTAL ZOOLOGY 300A:133–139 (2003) Muscle Enzyme Activities in a Deep-Sea Squaloid Shark, Centroscyllium fabricii, Compared With Its Shallow-Living Relative, Squalus acanthias JASON R. TREBERG1n, R. AIDAN MARTIN2, and WILLIAM R. DRIEDZIC1 1Ocean Sciences Centre, Memorial University of Newfoundland, St. John’s, Newfoundland, A1C 5S7, Canada 2ReefQuest Centre for Shark Research, Vancouver, BC V7X 1A3, Canada 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. J. Exp. Zool. 300A:133–139, 2003. r 2003 Wiley-Liss, Inc. INTRODUCTION to the deep-sea and not some other factor. For example, Sullivan and Somero (’80), as well as Aspects of the metabolic and biochemical adap- Siebenaller et al. (’82), have suggested interspe- tations found in deep-sea fish have received cific differences in white muscle enzyme activities significant study (see Somero, ’92; Childress, ’95; from shallow and deep living fish may be explained Gibbs, ’97 for recent reviews). While numerous in part by the feeding and locomotory habits of data on differences between deep and shallow each species. As explained by Gibbs (’97), these living teleosts are available, to our knowledge data are further confounded by the potential similar data on elasmobranchs are entirely lack- influence of phylogenetic differences. ing. Deep-sea teleosts generally have reduced To eliminate as many confounding factors as metabolic rates and low levels of key enzymes of possible, some investigators have made efforts to energy metabolism in white muscle compared to utilise species of close phylogeny, with similar life- shallow living species. No trend between enzyme styles, but inhabiting different depths. This is activity and depth has been observed in the heart exemplified by the work on Sebastolobus alasca- or brain of teleosts. nus and S. altivelis, the latter of which inhabits With no data available on deep-sea elasmo- deeper water (for example, Siebenaller and branchs, we test the hypothesis that the activities Somero, ’78, ’79, ’82). of several enzymes of energy metabolism in the Although C. fabricii and S. acanthias belong to heart, red muscle, and white muscle of the deep different families (Etmopteridae and Squalidae, living Centroscyllium fabricii differ from that of respectively) they are both basal squaloids in the the shallow living Squalus acanthias as well as n literature values for other elasmobranch species. Correspondence to: Jason Treberg, Ocean Sciences Centre, Memorial University of Newfoundland, St. John’s, NL, A1C 5S7, Interpretation of data on the adaptations of Canada. E-mail: [email protected] deep-sea fish is often difficult due to the inability Received 24 March 2003; Accepted 15 July 2003 Published online in Wiley InterScience (www.interscience.wiley. to conclude that differences are due to adaptation com). DOI: 10.1002/jez.a.10318. r 2003 WILEY-LISS, INC. 134 J.R. TREBERG ET AL. order Squaliformes (de Carvalho, ’96; Compagno, nitrogen. Red muscle was taken from the lateral ’99). Furthermore, sharks feature low genetic region between the second dorsal fin and the diversity (Smith, ’86) and slow rates of genetic caudal peduncal, and white muscle was sampled change across familial and ordinal taxa (Martin from the deep dorsal region below the first dorsal et al., ’92). Morphologically, squaloids are ‘extre- fin. In the case of C. fabricii, only animals that mely homogeneous’ (Bigelow and Schroeder, ’57). were still responsive to handling were sampled. The chosen species share the same basic body form Tissues were stored at or below À601C until and swimming style (Thompson and Simanek, ’77) analysis (between 20 and 30 months). Although and are of similar size, having many body and morphological characteristics in common (Bigelow À1 À1 and Schroeder, ’48; Bass et al., ’76; Compagno, TA BL E 1. Ac t iv i t i e s ( mmol min g wet tissue ) of heart enzymes in Squalus acanthias and Centroscyllium fabricii ’84). The general prey categories, and trophic level, Squalus Centroscyllium are very similar between these species (Cortez, Enzyme acanthias fabricii ’99) with S. acanthias known to be an active Oxidative predator of fast-swimming prey (Bigelow and CS 5.1270.81 3.7271.27 Schroeder, ’48, ’53; Compagno, ’84). The non- MDH 54.976.00 59.3713.2 overlapping tricuspidate teeth of C. fabricii sug- gest grasping fast-moving prey, an interpretation Amino acid AlaAT 0.5670.17 0.3970.28 supported by stomach contents (Bigelow and n Schroeder, ’53; Compagno et al., ’89; Ebert et al., AspAT 24.975.41 12.074.58 7 7 ’92). Both species appear to be active predators, GDH 0.60 0.23 0.64 0.23 and they are among the few shark species known Ketone body to school (Bigelow and Schroeder, ’53; Temple- bHBDH 0.3170.29 0.2070.10 man, ’63; Compagno, ’84). While there are many similarities between these Glycolytic/anaerobic n species, C. fabricii is abundant at 550–1010m PK 34.375.39 23.976.01 (Bigelow and Schroeder, ’57) or 400–1340m LDH 48.975.44 40.078.19 7 7 n (Templeman, ’63), depending on region, whereas CPK 2.14 0.89 7.23 2.43 S. acanthias is uncommon below 180m Values are means7SD with n¼5forall.n - sig. di¡erence between spe- (Templeman, ’63). cies (po0.05, Student’s t-test). Abbreviations: MDH, malate dehydrogen- ase; AlaAT, alanine aminotransferase; GDH, glutamate dehydrogenase In addition to being the first data of this kind on otherwise see text for full enzyme names. a deep-sea elasmobranch, we measured a greater variety of enzymes than in previous studies on À1 À1 teleosts and for the first time include red muscle in TA BL E 2. Ac t iv i t i e s ( mmol min g wet tissue )ofredmuscle enzymes in Squalus acanthias and Centroscyllium fabricii the tissues surveyed for enzyme activities involved with energy metabolism in a deep-sea fish. Enzyme S. acanthias C. fabricii MATERIALS AND METHODS Oxidative CS 9.9271.48 5.8470.78n Animals MDH 51.075.95 75.179.70n Specimens of C. fabricii were captured by otter Amino acid trawl on the CCGS Teleost in November, 1999 off AlaAT 2.1070.19 0.5970.25n AspAT 29.475.86 18.373.84n the coast of Newfoundland where bottom tem- n perature was between 3.5 and 51C. C. fabricii were GDH 5.9770.85 1.4170.23 caught in water with a bottom depth below 1000 m Ketone body and ranged from approximately 300 to 900 grams. bHBDH 2.4970.61 1.1170.63n S. acanthias were caught by otter trawl in Passamaquoddy Bay, New Brunswick, in less than Glycolytic/anaerobic 100 m of water at approximately 10 to 121Cin PK 29.675.26 26.479.04 n August, 2000, and weighed between approxi- LDH 20.174.98 33.577.79 7 7 n mately 400 and 1150 grams. All animals were CPK 32.8 6.15 56.7 17.1 killed by a blow to the head and tissues were Values are means7SD with n¼5 for all. n - sig. di¡erence between dissected out, blotted dry, and frozen with liquid species (po0.05, Student’s t-test). See Table 1 for abbreviations. DEEP-SEA SHARK MUSCLE ENZYMES 135 TA BL E 3. Ac t iv i t i e s ( mmol minÀ1 g wet tissueÀ1) of white muscle enzymes in Squalus acanthias and Centroscyllium fabricii S. acanthias Enzyme S. acanthias C. fabricii C. fabricii Shallow elasmobranchs Oxidative 7 7 n CS 0.54 0.18 0.24 0.04 024681012 7 7 n MDH 2.39 0.27 4.05 1.03 (a) Citrate synthase (µmol min-1 g-1) Amino acid n AspAT 2.0970.24 0.8270.39 S. acanthias C. fabricii Glycolytic/anaerobic n PK 101717.3 18.475.25 Shallow elasmobranchs LDH 160725.0 35.979.75n 7 7 n CPK 94.0 4.43 107 8.95 0 1020304050 (b) Pyruvate kinase (µmol min-1 g-1) Values are means7SD with n¼5forall.n - sig. di¡erence between species (po0.05, Student’s t-test). See Table 1 for abbreviations. S. acanthias C. fabricii Shallow elasmobranchs S. acanthias 020406080 C. fabricii (c) Lactate dehydrogenase (µmol min-1 g-1) Shallow elasmobranchs Fig. 2. Red muscle enzyme activities for (a) citrate synthase, (b) pyruvate kinase and (c) lactate dehydrogenase 02468 10 12 in S. acanthias and C. fabricii compared to shallow living (a) Citrate synthase (µmol min-1 g-1) elasmobranchs. Shallow living elasmobranchs, values are means7SD, n¼5 for all enzymes. Data for shallow living elasmobranchs: Crabtree and Newsholme, 1972; Alp et al., S. acanthias 1976; Zammit et al., 1978; Moon and Mommsen, 1987; C.
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