Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

ANT:

Adenine nucleotide translocase

AVF:

Atresic volume fraction

BSA:

Bovine serum albumin

CAT:

Carboxyatractyloside

CL:

Cardiolipin

CCO:

Cytochrome C oxidase

diacylPC:

Diacylphosphatidylcholine

diacylPE:

Diacylphosphatidylethanolamine

GVF:

Gamete volume fraction

GSI:

Gonadosomatic index

MUFA:

Monounsaturated fatty acids

PI:

Phosphatidylinositol

PS:

Phosphatidylserine

PlsmPE:

Plasmalogen ethanolamine

PUFA:

Polyunsaturated fatty acids

SFA:

Saturated fatty acids

SMR:

Standard metabolic rates

References

  • 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:https://doi.org/10.1086/376920

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1016/0022-0981(81)90031-9

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1007/BF00397001

    Article  CAS  Google Scholar 

  • Barber BJ, Blake NJ (1991) Reproductive physiology. In: Shumway SE (ed) Scallops: biology. ecology and aquaculture. Elsevier, Amsterdam, pp 377–428

    Google Scholar 

  • 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 259–338

    Google Scholar 

  • 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:https://doi.org/10.1007/s003600000169

    Article  Google Scholar 

  • 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:https://doi.org/10.1007/s002270050089

    Article  Google Scholar 

  • 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:https://doi.org/10.1007/BF00351045

    Article  Google Scholar 

  • 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:https://doi.org/10.1042/BJ20050890

    Article  CAS  PubMed Central  Google Scholar 

  • 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:https://doi.org/10.1016/S0022-0981(00)00215-X

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1007/s002270000415

    Article  CAS  Google Scholar 

  • Brokordt KB, Guderley H (2004) Energetic requirements during gonad maturation and spawning in scallops: sex differences in Chlamys islandica (Müller 1776). J Shell Res 23:25–32

    Google Scholar 

  • Brokordt KB, Fernandez M, Gaymer C (2006) Domestication reduces the capacity to escape from predators. J Exp Mar Biol Ecol 329:11–19. doi:https://doi.org/10.1016/j.jembe.2005.08.007

    Article  Google Scholar 

  • Chance B, Williams GR (1956) The respiratory chain and oxidative phosphorylation. Adv Enzymol 17:65–134

    CAS  Google Scholar 

  • 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 59:563–573

    Article  CAS  Google Scholar 

  • Clandinin MT, Field CJ, Hargraves K, Morson L, Zsigmond E (1985) Role of diet fat in subcellular structure and function. Can J Physiol Pharmacol 63:546–556

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1242/jeb.003897

    Article  CAS  Google Scholar 

  • 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 137:105–114

    Article  Google Scholar 

  • 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:https://doi.org/10.1016/j.aquaculture.2006.11.009

    Article  Google Scholar 

  • 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 226:497–509

    CAS  Google Scholar 

  • 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 257:2754–2757

    CAS  PubMed  Google Scholar 

  • Guderley HE, Rojas FM, Nusetti OA (1995) Metabolic specialization of mitochondria from scallop phasic muscles. Mar Biol (Berl) 122:409–416. doi:https://doi.org/10.1007/BF00350873

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1016/j.cbpc.2005.07.006

    Article  Google Scholar 

  • 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:837–861

    Google Scholar 

  • 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:863–882

    Google Scholar 

  • Hulbert AJ, Else PL (2005) Membranes and the setting of energy demand. J Exp Biol 208:1593–1599. doi:https://doi.org/10.1242/jeb.01482

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1007/s11745-002-0925-z

    Article  CAS  Google Scholar 

  • Kraffe E, Soudant P, Marty Y (2004) Fatty acids of serine, ethanolamine and choline plasmalogens in some marine bivalves. Lipids 39:59–66. doi:https://doi.org/10.1007/s11745-004-1202-x

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1242/jeb.02628

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.3354/meps250183

    Article  CAS  Google Scholar 

  • 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:35–44

    CAS  Google Scholar 

  • Lowe DM, Moore MN, Bayne BL (1982) Aspects of gametogenesis in the marine mussel Mytilus edulis L. Mar Biol Ass U.K. 62:133–145

    Article  Google Scholar 

  • Lubet P (1959) Recherches sur le cycle sexuel et l’émission des gamètes chez les mytilidés et les pectinidés. Rev Trav Inst Peches Marit 23:389–548

    Google Scholar 

  • 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:https://doi.org/10.1007/BF00428653

    Article  Google Scholar 

  • 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:https://doi.org/10.1016/0022-0981(92)90051-B

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1016/0305-0491(92)90384-4

    Google Scholar 

  • 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:https://doi.org/10.1016/j.aquaculture.2007.02.030

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1016/S0378-1119(01)00814-9

    Article  CAS  Google Scholar 

  • 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 22:365–376

    Google Scholar 

  • 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:https://doi.org/10.1016/j.jembe.2005.06.008

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1021/bi00490a012

    Article  CAS  Google Scholar 

  • Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    Article  CAS  Google Scholar 

  • 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–C699

    Article  CAS  Google Scholar 

  • Schlame M, Rua D, Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39:257–288. doi:https://doi.org/10.1016/S0163-7827(00)00005-9

    Article  CAS  Google Scholar 

  • Schlame M, Ren M (2006) Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett 580:5450–5455. doi:https://doi.org/10.1016/j.febslet.2006.07.022

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1139/z57-026

    Article  Google Scholar 

  • Shumway SE, Barter J, Stahlnecker J (1988) Seasonal changes in oxygen consumption of the giant scallop, Placopecten magellanicus (Gmelin). J Shell Res 7:77–82

    Google Scholar 

  • 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:https://doi.org/10.1016/0003-2697(85)90442-7

    Article  Google Scholar 

  • 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:https://doi.org/10.1051/alr:1997019

    Article  Google Scholar 

  • 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:https://doi.org/10.1016/0044-8486(96)01276-8

    Article  CAS  Google Scholar 

  • 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 137:97–104

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1016/j.aquaculture.2008.02.002

    Article  Google Scholar 

  • 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:https://doi.org/10.1086/507780

    Article  CAS  Google Scholar 

  • Watkins SM, Carter LC, German JB (1998) Docosahexaenoic acid accumulates in cardiolipin and enhances HT-29 cell oxidant production. J Lipid Res 39:1583–1588

    CAS  PubMed  Google Scholar 

  • 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:https://doi.org/10.1016/0003-9861(64)90313-3

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1016/0005-2736(81)90100-0

    Article  CAS  Google Scholar 

  • Yamaoka S, Urade R, Kito M (1988) Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. J Nutr 118:290–296

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Unité mixte CNRS 6521, Université de Bretagne Occidentale, C.S. 93837, 29238, Brest Cedex 3, France

    Edouard Kraffe & Yanic Marty

  2. Département de Biologie, Université Laval, Quebec, QC, G1K 7P4, Canada

    Edouard Kraffe & Helga Guderley

  3. Institut des Sciences de la Mer, 310 allée des Ursulines, Rimouski, QC, G5L 3A1, Canada

    Réjean Tremblay & Sonia Belvin

  4. UMR 100 Physiologie et Ecophysiologie des Mollusques Marins, Ifremer, Centre de Brest, B.P. 70, 29280, Plouzané, France

    Jeqn-René LeCoz

Authors
  1. Edouard Kraffe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Réjean Tremblay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sonia Belvin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeqn-René LeCoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanic Marty
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Helga Guderley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edouard Kraffe.

Additional information

Communicated by H.O. Pörtner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kraffe, E., Tremblay, R., Belvin, S. et al. Effect of reproduction on escape responses, metabolic rates and muscle mitochondrial properties in the scallop Placopecten magellanicus . Mar Biol 156, 25–38 (2008). https://doi.org/10.1007/s00227-008-1062-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-008-1062-4

Keywords

Search

Navigation