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Key metabolic enzymes and muscle structure in triplefin fishes (Tripterygiidae): a phylogenetic comparison

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Abstract

Metabolic potential and muscle development were investigated relative to habitat and phylogeny in seven species of New Zealand triplefin fishes. Activity was measured in three principal glycolytic enzymes (lactate dehydrogenase, pyruvate kinase and phosphofructokinase) and two oxidative enzymes (citrate synthase and L3-hydroxyacyl CoA:NAD+ oxidoreductase). The non-bicarbonate buffering capacity of caudal muscle was also estimated. Phylogenetic independent contrast analyses were used to reduce the effects of phylogenetic history in analyses. A positive relationship between metabolic potential and the effective water velocity at respective habitat depths was found only after the exclusion from analyses of the semi-pelagic species Obliquichthys maryannae. O. maryannae showed high glycolytic enzyme activities, and displayed double the activity of both oxidative enzymes relative to the six benthic species. Histochemically stained sections taken immediately posterior to the vent showed that adult O. maryannae and larval Forsterygion lapillum had significantly more red muscle, and smaller cross-sectional areas of white and red muscle fibres, than adults of benthic species. The distribution of red muscle in adult O. maryannae resembled that of larval F. lapillum, and differed from the typical teleost pattern seen in adults of the six benthic species. Both adult O. maryannae and larval F. lapillum have an expansive lateralis superficialis muscle, typical of larval fish, which encompasses much of the caudal trunk. Results suggest that anaerobic potential in New Zealand triplefins: (a) increases with the locomotory requirements of different habitats, and (b) displays a negative relationship with depth-dependent water velocities in benthic species. O. maryannae appears to have increased aerobic potential for sustained swimming by paedomorphic retention of larval muscle architecture.

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Abbreviations

β :

buffering capacity

C :

wave velocity

CS :

citrate synthase

DNBT :

5-5′-dithio-bis(2 nitrobenzoic acid)

g :

gravity

H :

average wave height

HOAD :

β-hydroxyacyl co-enzyme A dehydrogenase

ICA :

independent contrast analysis

L :

wave length

LDH :

lactate dehydrogenase

ML :

maximum likelihood

MP :

maximum parsimony

NJ :

neighbour joining

O dia :

orbital diameter

PFK :

phosphofructokinase

PK :

pyruvate kinase

SDH :

succinate dehydrogenase

SSLR :

sum of squares linear regression

T :

period

v :

effective linear velocity

V :

orbital particle velocity

References

  • Abe H (2000) Role of histidine-related compounds as intracellular proton buffering constituents in vertebrate muscle. Biochemistry 65:757–765

    CAS  PubMed  Google Scholar 

  • Abe H, Dodson GP, Höeger U, Parkhouse WS (1985) Role of histidine-related compounds to intracellular buffering in fish skeletal muscle. Am J Physiol 249:449–454

    Google Scholar 

  • Ayling A, Cox GJ (1982) Collins guide to the sea fishes of New Zealand. Collins, Auckland

  • Barrow KD, Jamieson DD, Norton RS (1980) Phosphorus-31 NMR studies of energy metabolism in tissue from the marine invertebrate, Tapes watlingi. Euro J Biochem 3:289–298

    Google Scholar 

  • Batty RS (1984) Development of swimming movements and musculature of larval herring (Clupea harengus). J Exp Biol 110:217–229

    CAS  PubMed  Google Scholar 

  • Bell D (1988) Fundamentals of electric circuits, 4th edn. Prentice Hall, p 452

  • Bone Q (1978) Locomotor muscle. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 7. Academic Press, New York, pp 361–424

  • Brix O, Clements KD, Wells RMG (1999) Haemoglobin components and oxygen transport in relation to habitat distribution in triplefin fishes (Tripterygiidae) Comp Physiol B 169:329–334

    Google Scholar 

  • Castellini MA, Somero GN (1981) Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J Comp Physiol B 143:191–198

    CAS  Google Scholar 

  • Chih CP, Ellington WR (1985) Metabolic correlates of intracellular pH change during rapid concentration of intracellular pH change during rapid contractile activity in a molluscan muscle. J Exp Zool 236:27–34

    CAS  Google Scholar 

  • Crockett EL, Sidell BD (1990) Some pathways of energy metabolism are cold adapted in Antarctic fishes. Physiol Zool 63:472–488

    Google Scholar 

  • Davis LG, Dibner D, Battey J F (1986) Basic methods in molecular biology. Elsevier, New York

  • Denny MW (1985) Wave forces on intertidal organisms: a case study. Limnol Oceanogr 30:1171–1187

    Google Scholar 

  • Devoto SH, Melanćon E, Eisen JS, Westerfield M (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122:3371–3380

    CAS  PubMed  Google Scholar 

  • Diaz-Uriarte R, Garland T Jr (1996) Testing hypotheses of correlated evolution using phylogenetically independent contrasts: sensitivity to deviations from Brownian motion. Syst Biol 45:27–47

    Google Scholar 

  • Dickson KA, Gregorio MO, Gruber SJ, Loefler KL, Tran M, Terrell C (1993) Biochemical indices of aerobic and anaerobic capacity in muscle tissues of California elasmobranch fishes differing in typical activity level. Mar Biol 117:185–193

    CAS  Google Scholar 

  • Eastman JT (1993) Antarctic fish biology. Evolution in a unique environment. Academic Press, San Diego

  • Eastman JT (1997) Phyletic Divergence and specialization for pelagic life in the Antarctic notothenioid fish Pleurogramma antarcticum. Comp Biochem Physiol A 118:1095–1101

    Article  Google Scholar 

  • Felsenstein J (1985a) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1985b) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Francis M (2001) Coastal fishes of New Zealand, 3rd edn. Reed, Auckland

  • Fricke R (1994) Tripterygiid fishes of Australia, New Zealand and the South West Pacific Ocean (Teleostei). Koeltz Scientific, Konigstein

  • Garland T Jr, Ives AR (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155:346–364

    PubMed  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Garland T Jr, Midford PE, Ives AR (1999) An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am Zool 39:374–388

    Google Scholar 

  • Goldspink G (1998) Selective gene expression during adaptation of muscle in response to different physiological demands (review). Comp Biochem Physiol B Biochem Mol Biol 120:5–15

    Article  CAS  PubMed  Google Scholar 

  • Goolish EM (1991) Aerobic and anaerobic scaling in fish. Biol Rev 66:33–56

    Google Scholar 

  • Graves JE, Somero GN (1992) Electrophoretic and functional enzymic evolution in four species of eastern Pacific barracudas from different thermal environments. Evolution 36:97–106

    Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

  • Hochachka PW (1994) Muscles as molecular and metabolic machines. CRC, Boca Raton

  • Hochachka PW, Somero GN (1973) Strategies of biochemical adaptation. Saunders, Philadelphia

  • Huang BQ, Lin YCW, Chung H (2000) Muscle development in larvae of the red sea bream Pagrus major. J Fish Soc Taiwan 27:263–271

    Google Scholar 

  • Humason GL (1972) Animal tissue techniques, 2nd edn. Freeman, San Francisco

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Nat Acad Sci USA 86:6196–6200

    CAS  PubMed  Google Scholar 

  • Koumans JTM, Akster HA (1995) Myogenic cells in development and growth in fish. Comp Biochem Physiol A 110:3–20

    Article  Google Scholar 

  • Lapointe F-J, Garland T Jr (2001) A generalised permutation model for the analysis of cross-species data. J Class 18:109–127

    Google Scholar 

  • Mathieu-Costello O, Agey PJ, Logemann RB, Brill RW, Hochachka PW (1992) Capillary-fiber geometrical relationships in Tuna red muscle. Can J Zool 70:1218–1229

    Google Scholar 

  • Miller RG, Boska MD, Moussavi RS, Carson PJ, Weiner MW (1988) Phosphorus-31 NMR studies of high-energy phosphates and pH in human muscle fatigue, comparison of aerobic and anaerobic exercise. J Clin Invest 81:1190–1196

    CAS  PubMed  Google Scholar 

  • Montgomery J, Clements K (2000) Disaptation and recovery in the evolution of Antarctic fishes. TREE 15:267–271

    Article  PubMed  Google Scholar 

  • Müller UK, Stamhuis EJ, Videler JJ (2000) Hydrodynamics of unsteady fish swimming and the effects of body size: comparing the flow fields of fish larvae and adults. J Exp Biol 203:193–206

    PubMed  Google Scholar 

  • Newsholme EA, Crabtree B (1986) Maximum catalytic activity of some key enzymes in provision of physiologically useful information about metabolic fluxes. J Exp Biol 239:59–167

    Google Scholar 

  • Palumbi SR, Martin AP, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fools guide to PCR. Special Publication, Department of Zoology, University of Hawaii

  • Paulin C, Roberts C (1992) The rockpool fishes of New Zealand. Museum of New Zealand, Te Papa Tongarewa, Wellington

  • Patruno M, Radaelli G, Mascarello F, Carnevali M, Candia D (1998) Muscle growth in response to changing demands of functions in the teleost Sparus aurata (L.) during development from hatching to juvenile. Anat Embryol 198:487–504

    Article  CAS  PubMed  Google Scholar 

  • Pierce VA, Crawford DL (1997) Phylogenetic analysis of thermal acclimation of the glycolytic enzymes in the genus Fundulus. Physiol Zool 70:597–609

    CAS  PubMed  Google Scholar 

  • Proctor C, Mosse PRL, Hudson RCL (1980) A histochemical and ultrastructural study of the development of the propulsive musculature of the brown trout, Salmo trutta L., in relation to its swimming behaviour. J Fish Biol 16:309–329

    Google Scholar 

  • Powers DA, Schulte PM (1998) Evolutionary adaptations of gene structure and expression in natural populations in relation to a changing environment; a multidisciplinary approach to address the million-year saga of a small fish. J Exp Zool 282:71–94

    CAS  PubMed  Google Scholar 

  • Rahman MS, Storey KB (1988) Role of covalent modification in the control of glycolytic enzymes in response to environmental anoxia in goldfish. J Comp Physiol B 157:813–820

    CAS  Google Scholar 

  • Rome LC (1995) Some advances in integrative muscle physiology. Comp Biochem Physiol B 120:51–72

    Article  Google Scholar 

  • Rome LC, Funke RP, Alexander RM, Lutz G, Aldridge H, Scott F, Freadman M (1988) Why animals have different muscle fibre types. Nature 335:824–827

    CAS  PubMed  Google Scholar 

  • Russell RCH, Macmillan DH (1953) Waves and tides. Greenwood, Westport Connecticut

  • Sänger AM (1997) The so-called tonic muscle fibre type in cyprinid axial muscle: their morphology and response to endurance exercise training. J Fish Biol 50:487–497

    Article  Google Scholar 

  • Schmidt-Nielsen K (1984) Scaling, why is animal size so important? Cambridge University Press, New York

  • Siebenaller JF, Somero GN (1982) The maintenance of different enzyme activities levels in congeneric fishes living at different depths. Physiol Zool 55:171–179

    CAS  Google Scholar 

  • Siebenaller JF, Somero GN, Haedrich RL (1982) Biochemical characteristics of macrourid fishes differing in their depths of distribution. Biol Bull 163:240–249

    CAS  Google Scholar 

  • Su JY, Storey KB (1995) Fish muscle phosphofructokinase: influences of protein concentration on enzyme kinetic behaviour. Int J Biochem Cell Biol 27:1277–1283

    Article  CAS  Google Scholar 

  • Suarez RK, Staples JF, Lighton JRB, West TG (1997) Relationships between enzymatic flux capacities and metabolic flux rates: non-equilibrium reactions in muscle glycolysis. Proc Natl Acad Sci USA 94:7065–7069

    Article  CAS  PubMed  Google Scholar 

  • Sullivan KM, Somero GN (1980) Enzyme activities of fish skeletal muscle and brain as influenced by depth of occurrence and habits of feeding and locomotion. Mar Biol 60:91–98

    CAS  Google Scholar 

  • Syms C (1995) Multi-scale analysis of habitat association in a guild of blennioid fishes. Mar Ecol Prog Ser 125:31–43

    Google Scholar 

  • Vetter RD, Lynn EA (1997) Bathymetric demography, enzyme activity patterns and bioenergetics of deep-living scorpaenid fishes (genera Sebastes and Sebastolobus): paradigms revisited. Mar Ecol Prog Ser 155:173–188

    Google Scholar 

  • Vetter RD, Lynn EA, Garza M, Costa AS (1994) Depth zonation and metabolic adaptation in Dover sole, Microstomus pacificus, and other deep living flatfishes; factors that affect the sole. Mar Biol 120:145–159

    Google Scholar 

  • Webber J-M, Haman F (1996) Pathways for metabolic fuels and oxygen in high performance fish. Comp Biochem Physiol A 113:33–38

    Article  Google Scholar 

  • Wells RMG, Summers G, Beard LA, Grigg GC (1988) Ecological correlates of intracellular buffering capacity in the muscles of Antarctic fishes. Polar Biol 8:321–326

    Google Scholar 

  • Wieser W (1995) Energetics of fish larvae, the smallest vertebrates. Acta Physiol Scand 154:279–290

    CAS  PubMed  Google Scholar 

  • Willis TJ, Roberts CD (1996) Re-colonisation and recruitment of fishes to intertidal rockpools at Wellington, New Zealand. Environ Biol Fish 47:329–343

    Google Scholar 

  • Yang T, Somero GN (1993) Effects of feeding and food deprivation on oxygen consumption, muscle protein concentration and activities of energy metabolism enzymes in muscle and brain of shallow-living (Scorpaena guttata) and deep-living (Sebastolobus alascanus) scorpaenid fishes. J Exp Biol 181:213–232

    CAS  Google Scholar 

  • Zänder CD, Nieder J, Martin K (1999) Vertical distribution patterns. In: Horn MH, Martin KLM, Chotkowski MA (eds) Intertidal fishes: life in two worlds. Academic Press, San Diego, pp 26–53

    Google Scholar 

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Acknowledgements

We would like to thank Brady Doak, Murray Birch (skippers of the R.V. Proteus), Nick Tolimieri and Lisa Clements for the collection of animals; Beryl Davies for assistance with histological preparations; Theodore Garland Jr. and Shane Lavery for help with comparative methods and analysis; and Rufus Wells for helpful comments on methodology and the manuscript. This paper was substantially improved by the constructive comments of two anonymous referees. This study met ethical requirements of the University of Auckland and was supported by the Marsden Fund of the New Zealand Royal Society. Experiments complied with current New Zealand laws.

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Correspondence to A. J. R. Hickey.

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Communicated by I.D. Hume

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Hickey, A.J.R., Clements, K.D. Key metabolic enzymes and muscle structure in triplefin fishes (Tripterygiidae): a phylogenetic comparison. J Comp Physiol B 173, 113–123 (2003). https://doi.org/10.1007/s00360-002-0313-9

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