Abstract
The swimming performance of two fish species, the brown trout and whitefish, having initially different swimming strategies, was measured after nine different training programs in order to relate the effects of exercise on Ca2+ handling and oxidative capacity of swimming muscles. The time to 50% fatigue was measured during the training period, and compared with the density of dihydropyridine (DHP) and ryanodine (Ry) receptors and succinate dehydrogenase (SDH) and phosphorylase activity determined by histochemical analysis of the swimming muscles. Overall, both trained brown trout and whitefish had superior swimming performance as compared to control ones. Interestingly, the training programs had different effect on the two species studied since brown trout achieved the highest swimming performance, swimming against the water flow velocity of 2 BL s−1 while among whitefish the best efficiency was seen after training with lower swimming velocities. Training also induced a significant increase in DHP and Ry receptor density in both species. Generally, in brown trout the most notable increase in the receptor densities was observed in red muscle sections from the fish swimming for 6 weeks against water currents of 1 BL s−1 (DHPR 176.5 ± 7.7% and RyR 231.4 ± 11.8%) and white muscle sections against 2 BL s−1 (DHPR 129.6 ± 12.4% and RyR 161.9 ± 15.5%). In whitefish the most prominent alterations were noted in samples from both muscle types after 6 weeks of training against water current of 1.5 BL s−1 (DHPR 167.1 ± 16.9% and RyR 190.4 ± 19.4%). Finally, after all the training regimens the activity of SDH increased but the phosphorylase activity decreased significantly in both the species. To conclude, our findings demonstrate an improved swimming performance and enhanced Ca2+ regulation and oxidative capacity after training. Moreover, there seems to be a connection between the swimming performance and receptor levels, especially in white swimming muscles of different fish species, regardless of their initially deviant swimming behaviours. However, depending on the training regimen the divergent swimming behaviours do cause a different response, resulting in the most prominent adaptational changes in the receptor levels of red muscle samples with lower swimming velocities in brown trout and with higher ones in whitefish.
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Abbreviations
- BL:
-
Body length
- CF:
-
Fulton’s condition factor
- CICR:
-
Calcium induced calcium release
- CL:
-
Control level
- DHP:
-
Dihydropyridine
- DHPR:
-
Dihydropyridine receptor
- EC:
-
Excitation–contraction
- Ry:
-
Ryanodine
- RyR:
-
Ryanodine receptor
- SDH:
-
Succinate dehydrogenase
- SR:
-
Sarcoplasmic reticulum
- U crit :
-
Critical swimming speed
References
Altringham JD, Ellerby DJ (1999) Fish swimming: patterns in muscle function. J Exp Biol 202:3397–3403
Anttila K, Mänttäri S, Järvilehto M (2006) Effects of different training protocols on Ca2+ handling and oxidative capacity in skeletal muscle of Atlantic salmon (Salmo salar L.). J Exp Biol 209:2971–2978. doi:10.1242/jeb.02341
Anttila K, Mänttäri S, Järvilehto M (2007) Expression of dihydropyride and ryanodine receptors in type IIA fibres of rat skeletal muscle. Acta Histochem Cytochem 40:35–41. doi:10.1267/ahc.06028
Berchtold MW, Brinkmeier H, Müntener M (2000) Calcium ion in skeletal muscle: Its crucial role for muscle function, plasticity, and disease. Physiol Rev 80:1215–1265
Cole NJ, Johnston IA (2001) Plasticity of myosin heavy chain expression with temperature acclimitation is gradually acquired during ontogeny in common carp (Cyprinus carpio L.). J Comp Physiol 171B:321–326. doi:10.1007/s003600100179
Davie PS, Wells RM, Tetens V (1986) Effects of sustained swimming on rainbow trout muscle structure, blood oxygen transport, and lactate dehydrogenase isozymes: evidence for increased aerobic capacity of white muscle. J Exp Zool 237:159–171
Davison W (1997) The effects of exercise training on teleost fish, a review of recent literature. Comp Biochem Physiol 117A:67–75
Day N, Butler PJ (1996) Environmental acidity and white muscle recruitment during swimming in the brown trout (Salmo trutta). J Exp Biol 199:1947–1959
Dubowitz W, Pearse AG (1960) A comparative histochemical study of oxidative enzyme and phosphorylase activity in skeletal muscle. Z Zellforch Microsk Anat Histochem 2:105–117
Farrell AP, Johansen JA, Suarez RK (1991) Effects of exercise-training on cardiac performance and muscle enzymes in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 9:303–312
Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82:893–922. doi:10.1152/physrev.00013.2002
Franck JPC, Morrissette J, Keen JE, Londraville RL, Beamsley M, Block BA (1998) Cloning and characterization of fiber type-specific ryanodine receptor isoforms in skeletal muscles of fish. Am J Physiol 275:C401–C415
Franzini-Armstrong C, Ferguson DC, Champ C (1988) Discrimination between fast- and slow-twitch fibers of guinea pig skeletal muscle using the relative surface density of junctional transverse tubule membrane. J Muscle Res Cell Motil 9:403–414
Froemming GR, Murray BE, Harmon S, Pette D, Ohlendieck K (2000) Comparative analysis of the isoform expression pattern of Ca2+-regulatory membrane proteins in fast-twitch, slow-twitch, cardiac, neonatal and chronic low-frequency stimulated muscle fibers. Biochim Biophys Acta 1466:151–168
Golden KL, Marsh JD, Jiang Y, Brown T, Moulden J (2003) Gonadectomy of adult male rats reduces contractility of isolated cardiac myocytes. Am J Physiol 285:E449–E453
Heggenes J (1998) Habitat selection by brown trout (Salmo trutta) and young Atlantic salmon (S. salar) in streams: static and dynamic hydraulic modelling. Reg Riv Res Man 12:155–169
Holk K, Lykkeboe G (1998) The impact of endurance training on arterial plasma K+ levels and swimming performance of rainbow trout. J Exp Biol 201:1373–1380
Houlihan DF, Laurent P (1987) Effects of exercise training on the performance, growth, and protein turnover of rainbow trout (Salmo gairdneri). Can J Fish Aquat Sci 44:1614–1621
Johnston IA, Moon TW (1980) Endurance exercise training in the fast and slow muscles of a teleost fish (Pollachius virens). J Comp Physiol 135B:147–156
Kandarian S, O’Brien S, Thomas K, Schulte L, Navarro J (1992) Regulation of skeletal muscle dihydropyridine receptor gene expression by biomechanical unloading. J Appl Physiol 72:2510–2514
Koulen P, Janowitz T, Johenning FW, Ehrlich BE (2001) Characterization of the calcium-release channel/ryanodine receptor from zebrafish skeletal muscle. J Membr Biol 183:155–163
Kraemer WJ, Patton JF, Gordon SE, Harman EA, Deschenes MR, Reynolds K, Newton RU, Triplett NT, Dziados JE (1995) Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations. J Appl Physiol 78:976–989
Lamb GD (2000) Excitation–contraction coupling in skeletal muscle: comparison with cardiac muscle. Clin Exp Pharmacol Physiol 27:216–224
McCall GE, Byrnes WC, Dickson A, Pattany PM, Fleck SJ (1996) Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training. J Appl Physiol 81:2004–2012
McDonald DG, McFarlane WJ, Milligan CL (1998a) Anaerobic capacity and swim performance of juvenile salmonids. Can J Aquat Sci 55:1198–1207
McDonald DG, Milligan CL, McFarlane WJ, Croke S, Currie S, Hooke B, Angus RB, Tufts BL, Davidson K (1998b) Condition and performance of juvenile Atlantic salmon (Salmo salar): effects of rearing practices on hatchery fish and comparison with wild fish. Can J Fish Aquat Sci 55:1208–1219
McFarlane WJ, McDonald DG (2002) Relating intramuscular fuel use to endurance in juvenile rainbow trout. Physiol Biochem Zool 75:250–259
Morrissette J, Xu L, Nelson A, Meissner G, Bolck BA (2000) Characterization of RyR1-slow, a ryanodine receptor specific to slow-twitch skeletal muscle. Am J Physiol 279:R1889–R1898
Mänttäri S, Järvilehto M (2005) Comparative analysis of mouse skeletal muscle fibre type composition and contractile responses to calcium channel blocker. BMC Physiol 5:4. doi:10.1186/1472-6793-5-4
Mänttäri S, Pyörnilä A, Harjula R, Järvilehto M (2001) Expression of L-type calcium channels associated with postnatal development of skeletal muscle function in mouse. J Muscle Res Cell Mot 22:61–67
Mänttäri S, Anttila K, Järvilehto M (2005) Effects of downstream migration on myosin heavy chain expression and dihydropyridine receptor density in farmed smolt of Atlantic salmon. J Fish Biol 66:1437–1446
Nachlas MM, Tsou K, De Saiza E, Cheng C, Seligman A (1957) Cytochemical demonstration of succinic dehydrogenase by the use of new p-nitrophynyl substituted ditetrazole. J Histochem Cytochem 3:170–195
Nelson JA, Tang Y, Boutilier RG (1994) Differences in exercise physiology between two Atlantic cod (Gadus morhua) populations from different environment. Physiol Zool 67:330–354
Ørtenblad N, Lunde PK, Levin K, Andersen JL, Pedersen PK (2000) Enhanced sarcoplasmic reticulum Ca2+ release following intermittent sprint training. Am J Physiol 279:R152–R160
Pearson MP, Spriet LL, Stevens ED (1990) Effects of sprint training on swim performance and white muscle metabolism during exercise and recovery in rainbow trout (Salmo gairdneri). J Exp Biol 149:45–60
Saborido A, Molano F, Moro G, Megías M (1995) Regulation of dihydropyridine receptor levels in skeletal and cardiac muscle by exercise training. Pflügers Arch 429:364–369
Salama A, Nikinmaa M (1989) Species differences in the adrenergic responses of fish red cells: studies on whitefish, pikeperch, trout and carp. Fish Physiol Biochem 6:167–173
Staron RS, Karapondo DL, Kraemer WJ, Fry AC, Gordon SE, Falkel JE, Hagerman FC, Hikida RS (1994) Skeletal muscle adaptations during early phase of heavy-resistance training in men and woman. J Appl Physiol 76:1247–1255
Svetovidov AN (1984) Salmonidae. In: Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean. Unesco, Paris, pp 373–383
Sänger AM, Pötscher U (2000) Endurance exercise training affects fast white axial muscle in the cyprinid species Chalcalburnus chalcoides mento (Agassiz, 1832), cyprinidae, teostei. Basic Appl Myol 10:297–300
Watabe S (2002) Temperature plasticity of contractile proteins in fish muscle. J Exp Biol 205:2231–2236
Wilson RW, Egginton S (1994) Assessment of maximal sustainable swimming performance in rainbow trout (Oncorhynchus mykiss). J Exp Biol 192:299–305
Young PS, Cech JJ (1993) Improved growth, swimming performance, and muscular development in exercise-conditioned young-of-the-year striped bass (Morone saxatilis). Can J Fish Aquat Sci 50:703–707
Acknowledgments
The authors wish to thank Minna Orreveteläinen, Marja-Liisa Martimo-Halmetoja, Sinikka Koskela, Mervi Päätalo and Katarina Stebelova for technical support. This research was performed in collaboration with the Finnish Game and Fisheries Research Institute, Taivalkoski and funded by the Oulu University Scholarship Foundation.
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Communicated by I.D. Hume.
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Anttila, K., Järvilehto, M. & Mänttäri, S. The swimming performance of brown trout and whitefish: the effects of exercise on Ca2 + handling and oxidative capacity of swimming muscles. J Comp Physiol B 178, 465–475 (2008). https://doi.org/10.1007/s00360-007-0239-3
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DOI: https://doi.org/10.1007/s00360-007-0239-3