Marine Biology

, Volume 156, Issue 1, pp 25–38 | Cite as

Effect of reproduction on escape responses, metabolic rates and muscle mitochondrial properties in the scallop Placopecten magellanicus

  • Edouard KraffeEmail author
  • Réjean Tremblay
  • Sonia Belvin
  • Jeqn-René LeCoz
  • Yanic Marty
  • Helga Guderley
Original Paper


In scallops, gametogenesis and spawning can diminish the metabolic capacities of the adductor muscle and reduce escape response performance. To evaluate potential mechanisms underlying this compromise between reproductive investment and escape response, we examined the impact of reproductive stage (pre-spawned, spawned and reproductive quiescent) of the giant scallop, Placopecten magellanicus, on behavioural (i.e., escape responses), physiological (i.e., standard metabolic rates and metabolic rates after complete fatigue) and mitochondrial capacities (i.e., oxidative rates) and composition. Escape responses changed markedly with reproductive investment, with spawned scallops making fewer claps and having shorter responses than pre-spawned or reproductive-quiescent animals. After recuperation, spawned scallops also recovered a lower proportion of their initial escape response. Scallop metabolic rate after complete fatigue (VO2max) did not vary significantly with reproductive stage whereas standard metabolic rate (VO2min) was higher in spawned scallops. Thus spawned scallops had the highest maintenance requirements (VO2min/VO2max). Maximal capacities for glutamate oxidation by muscle mitochondria did not change with reproductive stage although levels of ANT and cytochromes as well as cytochrome C oxidase (CCO) activity did. Total mitochondrial phospholipids, sterols and the proportion of phospholipid classes differed only slightly between reproductive stages. Few modifications were detected in the fatty acid (FA) composition of the phospholipid classes except in cardiolipin (CL). In this class, pre-spawned and spawned scallops had fairly high proportions of 20:5n-3 whereas this FA in reproductive-quiescent scallops was threefold lower and 22:6n-3 was significantly higher. These changes paralleled the increases in CCO activity and suggest an important role of CL on the modifications of CCO activity in scallops. However, mitochondrial properties could not explain the decreased recuperation ability from exhausting exercise in spawned scallops. Shifts in maintenance requirements (VO2min/VO2max) and aerobic scope (VO2max − VO2min) provided the best explanation for the impact of reproduction on escape response performance.


Reproductive Stage Escape Response Phospholipid Class Reproductive Investment Standard Metabolic Rate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Adenine nucleotide translocase


Atresic volume fraction


Bovine serum albumin






Cytochrome C oxidase






Gamete volume fraction


Gonadosomatic index


Monounsaturated fatty acids






Plasmalogen ethanolamine


Polyunsaturated fatty acids


Saturated fatty acids


Standard metabolic rates



This research was supported by a grant from NSERC to HG. EK received post-doctoral support from the Reseau Aquacole du Québec and from the Université de Bretagne Occidentale. The direction of innovation and technology of the Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec (MAPAQ) allowed accessibility and metabolic measurements at CAMGR.


  1. Bailey DM, Peck LS, Bock C, Pörtner HO (2003) High-energy phosphate metabolism during exercise and recovery in temperate and Antarctic scallops: an in vivo 31P-NMR study. Physiol Biochem Zool 76:622–633. doi: CrossRefGoogle Scholar
  2. Barber BJ, Blake NJ (1981) Energy storage and utilization in relation to gametogenesis in Argopecten irradians concentricus (Say). J Exp Mar Biol Ecol 52:121–134. doi: CrossRefGoogle Scholar
  3. Barber BJ, Blake NJ (1985) Substrate catabolism related to reproduction in the bay scallop Argopecten irradians concentricus, as determined by O/N and RQ physiological indexes. Mar Biol (Berl) 87:13–18. doi: CrossRefGoogle Scholar
  4. Barber BJ, Blake NJ (1991) Reproductive physiology. In: Shumway SE (ed) Scallops: biology. ecology and aquaculture. Elsevier, Amsterdam, pp 377–428Google Scholar
  5. Berger A, German JB, Gershwin ME (1993) Biochemistry of CL: sensitivity to dietary fatty acids. In: Kissela JE (ed) Advances in food and nutrition research, vol 37. Academic Press, San Diego, pp 259–338Google Scholar
  6. Blier PU, Lemieux H (2001) The impact of the thermal sensitivity of cytochrome c oxidase on the respiration rate of Arctic charr red muscle mitochondria. J Comp Physiol B 171:246–253. doi: CrossRefGoogle Scholar
  7. Boadas MA, Nusetti OA, Mundarain F, Lodeiros C, Guderley H (1997) Seasonal variation in the properties of muscle mitochondria from the tropical scallop Euvola (Pecten) ziczac. Mar Biol (Berl) 128:247–255. doi: CrossRefGoogle Scholar
  8. Bonardelli JC, Himmelman JH, Drinkwater K (1996) Relation of spawning of the giant scallop, Placopecten magellanicus, to temperature fluctuations during downwelling events. Mar Biol (Berl) 124:637–649. doi: CrossRefGoogle Scholar
  9. Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC, Brookes PS et al (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392:353–362. doi: CrossRefPubMedCentralGoogle Scholar
  10. Brokordt KB, Himmelman JH, Guderley HE (2000a) Effect of reproduction on escape responses and muscle metabolic capacities in the scallop Chlamys islandica Müller 1776. J Exp Mar Biol Ecol 251:205–225. doi: CrossRefGoogle Scholar
  11. Brokordt KB, Himmelman JH, Nusetti OA, Guderley HE (2000b) Reproductive investment reduces recuperation from exhaustive escape activity in the tropical scallop Euvola zizac. Mar Biol (Berl) 137:857–865. doi: CrossRefGoogle Scholar
  12. Brokordt KB, Guderley H (2004) Energetic requirements during gonad maturation and spawning in scallops: sex differences in Chlamys islandica (Müller 1776). J Shell Res 23:25–32Google Scholar
  13. Brokordt KB, Fernandez M, Gaymer C (2006) Domestication reduces the capacity to escape from predators. J Exp Mar Biol Ecol 329:11–19. doi: CrossRefGoogle Scholar
  14. Chance B, Williams GR (1956) The respiratory chain and oxidative phosphorylation. Adv Enzymol 17:65–134Google Scholar
  15. Chih PC, Ellington WS (1986) Control of glycolysis during contractile activity in the phasic adductor muscle of the bay scallop, Argopecten irradians concentricus: identification of potential sites of regulation and a consideration of the control of octopine dehydrogenase activity. Physiol Zool 59:563–573CrossRefGoogle Scholar
  16. Clandinin MT, Field CJ, Hargraves K, Morson L, Zsigmond E (1985) Role of diet fat in subcellular structure and function. Can J Physiol Pharmacol 63:546–556CrossRefGoogle Scholar
  17. Davies R, Moyes CD (2007) Allometric scaling in centrarchid fish: origins of intra- and inter-specific variation in oxidative and glycolytic enzyme levels in muscle. J Exp Biol 210:3798–3804. doi: CrossRefGoogle Scholar
  18. de Zwaan A, Thompson RJ, Livingstone DR (1980) Physiological and biochemical aspects of valve snap and valve closure responses in the giant scallop Placopecten magellanicus.II. Biochemistry. J Comp Physiol 137:105–114CrossRefGoogle Scholar
  19. Delgado M, Pérez Camachao A (2007) Influence of temperature on gonadal development of Ruditapes philippinarum (Adams and Reeve, 1850) with special reference to ingested food and energy balance. Aquaculture 264:398–407. doi: CrossRefGoogle Scholar
  20. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509Google Scholar
  21. Groen AK, Wanders RJA, Westerhoff HV, Van der Meer R, Tager JM (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257:2754–2757PubMedGoogle Scholar
  22. Guderley HE, Rojas FM, Nusetti OA (1995) Metabolic specialization of mitochondria from scallop phasic muscles. Mar Biol (Berl) 122:409–416. doi: CrossRefGoogle Scholar
  23. Guderley H, Turner ND, Else PL, Hulbert AJ (2005) Why are some mitochondria more powerful than others: Insights from comparisons of muscle mitochondria from three terrestrial vertebrates. Comp Biochem Physiol B 142:172–180. doi: CrossRefGoogle Scholar
  24. Hazel JR (1972a) The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L.) - I. Properties of the enzyme and the effect of lipid extraction. Comp Biochem Physiol 43B:837–861Google Scholar
  25. Hazel JR (1972b) The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L.)-II. Lipid reactivation of the soluble enzyme. Comp Biochem Physiol 43B:863–882Google Scholar
  26. Hulbert AJ, Else PL (2005) Membranes and the setting of energy demand. J Exp Biol 208:1593–1599. doi: CrossRefGoogle Scholar
  27. Kraffe E, Soudant P, Marty Y, Kervarec N, Jehan P (2002) Evidence of a tetradocosahexaenoic cardiolipin in some marine bivalves. Lipids 37:507–514. doi: CrossRefGoogle Scholar
  28. Kraffe E, Soudant P, Marty Y (2004) Fatty acids of serine, ethanolamine and choline plasmalogens in some marine bivalves. Lipids 39:59–66. doi: CrossRefGoogle Scholar
  29. Kraffe E, Marty Y, Guderley H (2007) Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J Exp Biol 210:149–165. doi: CrossRefGoogle Scholar
  30. Lafrance M, Cliche G, Haugum G, Guderley H (2003) Comparison of cultured and wild sea scallops, Placopecten magellanicus (Gmelin, 1791), using behavioral responses, morphometric and biochemical indices. Mar Ecol Prog Ser 250:183–195. doi: CrossRefGoogle Scholar
  31. Livingstone DR, de Zwaan A, Thompson RJ (1981) Aerobic metabolism, octopine production and phosphoarginine as sources of energy in the phasic and catch adductor muscles of the giant scallop Placopecten magellanicus during swimming and the subsequent recovery period. Comp Biochem Physiol 70B:35–44Google Scholar
  32. Lowe DM, Moore MN, Bayne BL (1982) Aspects of gametogenesis in the marine mussel Mytilus edulis L. Mar Biol Ass U.K. 62:133–145CrossRefGoogle Scholar
  33. Lubet P (1959) Recherches sur le cycle sexuel et l’émission des gamètes chez les mytilidés et les pectinidés. Rev Trav Inst Peches Marit 23:389–548Google Scholar
  34. MacDonald BA, Thompson RJ (1986) Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus. Mar Biol (Berl) 93:37–48. doi: CrossRefGoogle Scholar
  35. Marty Y, Delaunay F, Moal J, Samain JF (1992) Changes in the fatty acid composition of the scallop Pecten maximus (L.) during larval development. J Exp Mar Biol Ecol 163:221–234. doi: CrossRefGoogle Scholar
  36. Napolitano GE, Ackman RG (1992) Anatomical distributions and temporal variations of lipid classes in sea scallops Placopecten magellanicus (Gmelin) from Georges Bank (Nova Scotia). Comp Biochem Physiol 103:645–650. doi: Google Scholar
  37. Palacios E, Racotta IS, Arjona O, Marty Y, Le Coz JR, Moal J et al (2007) Lipid composition of the pacific lion-paw scallop, Nodipecten subnodosus, in relation to gametogenesis 2. Lipid classes and sterols. Aquaculture 266:266–273. doi: CrossRefGoogle Scholar
  38. Paradies G, Petrosillo G, Pistolese M, Ruggiero FM (2002) Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 286:135–141. doi: CrossRefGoogle Scholar
  39. Pernet F, Tremblay R, Bourget E (2003) Biochemical indicator of sea scallop (Placopecten magellanicus) quality based on lipid class composition. Part I: Broodstock conditionning and young larvae performance. J Shell Res 22:365–376Google Scholar
  40. Pernet F, Bricelj VM, Parrish CC (2005) Effect of varying dietary levels of w6 polyunsaturated fatty acids during the early ontogeny of the sea scallop, Placopecten magellanicus. J Exp Mar Biol Ecol 327:115–133. doi: CrossRefGoogle Scholar
  41. Robinson NC, Zborowski J, Talbert LH (1990) Cardiolipin-depleted bovine heart cytochrome c oxidase: Binding stoichiometry and affinity for cardiolipin derivatives. Biochemistry 29:8962–8969. doi: CrossRefGoogle Scholar
  42. Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758CrossRefGoogle Scholar
  43. Rolfe DFS, Newman JM, Buckingam JA, Clark MG, Brand MD (1999) Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol 276:C692–C699CrossRefGoogle Scholar
  44. Schlame M, Rua D, Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39:257–288. doi: CrossRefGoogle Scholar
  45. Schlame M, Ren M (2006) Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett 580:5450–5455. doi: CrossRefGoogle Scholar
  46. Shaw BL, Battle HI (1957) The gross microscopic anatomy of the digestive tract of the oyster Crassostrea virginica (Gmelin). Can J Zool 35:325–346. doi: CrossRefGoogle Scholar
  47. Shumway SE, Barter J, Stahlnecker J (1988) Seasonal changes in oxygen consumption of the giant scallop, Placopecten magellanicus (Gmelin). J Shell Res 7:77–82Google Scholar
  48. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD et al (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:176–185. doi: CrossRefGoogle Scholar
  49. Soletchnik P, Razet D, Geairon P, Faury N, Goulletquer P (1997) Ecophysiology of maturation and spawning in oyster (Crassostrea gigas): metabolic (respiration) and feeding (filtration and absorption rates) responses at different maturation stages. Aquat Living Resour 10:177–185. doi: CrossRefGoogle Scholar
  50. Soudant P, Marty Y, Moal J, Robert R, Quéré C, Le Coz JR et al (1996) Effect of food fatty acids and sterol quality on Pecten maximus gonad composition and reproduction process. Aquaculture 143:361–378. doi: CrossRefGoogle Scholar
  51. Thompson RJ, Livingstone DR, de Zwaan A (1980) Physiological and biochemical aspects of valve snap and valve closure responses in the giant scallop Placopecten magellanicus. I. Physiology. J Comp Physiol 137:97–104CrossRefGoogle Scholar
  52. Tran D, Massabuau JC, Vercelli C (2008) Influence of sex and spawning status on oxygen consumption and blood oxygenation status in oysters Crassostrea gigas in a Mediterranean lagoon (Thau, France). Aquaculture 277:58–65. doi: CrossRefGoogle Scholar
  53. Tremblay I, Guderley H, Fréchette M (2006) Swimming performance, metabolic rates, and their correlates in the iceland scallop Chlamys islandica. Physiol Biochem Zool 79:1046–1057. doi: CrossRefGoogle Scholar
  54. Watkins SM, Carter LC, German JB (1998) Docosahexaenoic acid accumulates in cardiolipin and enhances HT-29 cell oxidant production. J Lipid Res 39:1583–1588PubMedGoogle Scholar
  55. Williams JN (1964) A method for the simultaneous quantitative estimation of cytochromes A, B, C1 and C in mitochondria. Arch Biochem Biophys 107:537–543. doi: CrossRefGoogle Scholar
  56. Wodtke E (1981) Temperature adaptation of biological membranes. The effects of acclimatation temperature on the unsaturation of the main neutral and charged phospholipids in mitochondrial membranes of the carp (Cyprinus carpio L.). Biochim Biophys Acta 640:698–709. doi: CrossRefGoogle Scholar
  57. Yamaoka S, Urade R, Kito M (1988) Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. J Nutr 118:290–296CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Edouard Kraffe
    • 1
    • 2
    Email author
  • Réjean Tremblay
    • 3
  • Sonia Belvin
    • 3
  • Jeqn-René LeCoz
    • 4
  • Yanic Marty
    • 1
  • Helga Guderley
    • 2
  1. 1.Unité mixte CNRS 6521Université de Bretagne OccidentaleBrest Cedex 3France
  2. 2.Département de BiologieUniversité LavalQuebecCanada
  3. 3.Institut des Sciences de la MerRimouskiCanada
  4. 4.UMR 100 Physiologie et Ecophysiologie des Mollusques Marins, IfremerCentre de BrestPlouzanéFrance

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