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Swimming and Muscle Structure in Fish

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Swimming and Muscle Structure in Fish 3ß MAG CA NN08201 40951 1996-05-12 7^' k3 TT^^MI ,G AND MUSCLE STRUCTURE INFIS H Igor L. Y. *ts Swimming and muscle structure in fish Igor L.Y. Spierts Proefschrift terverkrijgin g van degraa d van doctor opgeza g van derecto r magnificus van deLandbouwuniversitei t te Wageningen, dr. C.M. Karssen, in hetopenbaa rt e verdedigen opvrijda g 28me i 1999 desnamiddag s tehal f tweei n deaul a Abstract Spierts,I.L.Y . 1999.Swimmin g and muscle structure in fish. Doctoral thesis, Experimental Zoology Group,Wageninge n Agricultural University, P.O.Bo x 338,670 0 AH Wageningen, The Netherlands ISBN: 90-9012702-X Subject headings: Carp axial muscle, fish swimming, myotendinous junctions, force transmission, titin isoforms, muscle activity,car plarvae ,ontogeny , elastic energy, Cyprinuscarpio L. Thescop eo fthi s serieso f studies wast odetermin e (from micro-t o macro-level) how the structure of axialmuscle soffis h isadapte dt oth e functional, sometimes contrasting, demands of different modes of swimming (e.g. continuous swimming and fast-starts) in relation to fish size and age. Posterior fibres of adultcar phav ea longe rphas eo feccentri c activity (active whilebein g stretched) than anterior fibres and will therefore develop greater forces. Posterior and red fibres are subjected to larger sarcomere strains during continuous swimming and have special adaptations to these functional demands: (1) stronger MTJs, and (2) larger isoforms of the giant elastic muscle protein titin. A quantitative electron-microscopical study showed that a linear correlation exists between the surface areao fMTJ s (measure for strength) and the size and duration of the load on ajunction . Fibres with larger surface areas consequently can bear larger loads during swimming. Gel-electrophoresis and micro-mechanical experiments revealed that fibres with larger titin isoforms require less passive tension for thesam e sarcomere strain.A slarva l musclefibres possesse d smaller titins than that of any adult muscle fibre the titin isoform changes during ontogeny. The shorter titin isoform is thought to helprestrictin g form changes of fast swimming carp larvae and to increase the elastic contribution to thetai lbea tb yelasti cenerg ystorag ei nthi stitin isofor m during theinitia l bending that is subsequently released inth efollowin g bending. This study corroborates the idea that (small) differences in muscle function during swimming,turnin g andescapin g canb euse d topredic t and possibly explain structural differences between various typeso f muscles infish o f different age and size. This research were supported by the Life Sciences Foundation (project 805-28.266, NWO-SLW), whichi ssubsidise d byth eNetherland s Organisation for Scientific Research. Coverdesign :Wi mValen . STELLINGEN 1 Spieren die aan verschillende mechanische eisen moeten voldoen blijken bij die eisen passende (ultra) structuren te bezitten. Dit proefschrift. 2 De elastische eigenschappen van een spier worden in belangrijke mate bepaald door het elastische spiereiwit titine. Aangezien zeer kort na de dood van een vis het titine door proteolytische enzymen afgebroken wordt zijn de resultaten van vele micro-mechanische experimenten, waarbij aan spiervezels getrokken werd, onbetrouwbaar. De belangrijke elastische bijdrage van titine aan dergelijke kracht-lengte metingen is dan namelijk niet met zekerheid bekend. Dit proefschrift. 3 Het is tegenwoordig niet alleen mogelijk maar het wordt ook noodzakelijk om structuur­ functierelaties i nd emorfologi e toto pmoleculai r niveau te onderzoeken. Dit proefschrift. 4 Tijdens snelle starten vankarper s (C- en S- ontsnappingsreacties) zijn niet alleen witte maar ook rodespiere n langsd elichaamsa s van devi sactief .I knee m daarom aan dat rode spieren tijdensdez e krachtige en snelle bewegingen een (geringe) bijdrage leveren aan de productie van kracht. Ditproefschrift (hoofdstuk6, 7). 5 Het is als wetenschapper belangrijk om niet met alle winden mee te waaien, doch het luisteren naard ewin d ind ebome n vanhe teige nonderzoeksvel d blijft essentieel. 6 Wetenschap bedrijven zonder regelmatig een second opinion te krijgen is als roeien zonder peddels. 7 'De onnodige oorlog'. Nooit is er een oorlog geweest, die gemakkelijker vermeden had kunnen worden dandie ,welk e zojuist heeft verwoest wat doord e vorige worsteling nog van dewerel d was overgelaten. Sir Winston Leonard Spencer-Churchill. De Tweede Wereldoorlog. 1. Van oorlog tot oorlog, 1919-1938(1989). Tirion-Baarn, 374 pp. 8 Deuiteenlopend ebelange n vand ehuidig eEuropes e partnersé n hetontbreke n van een goede democratische structuur in Europa verhinderen een éénduidig Europees optreden dal noodzakelijk is om een crisis als in de Balkan snel aan te kunnen pakken, c.q. te kunnen vermijden. 9 Eenomscholin g naard eInformatisering s Technologie is tegenwoordig de meest succesvolle carrièrewijziging voorlangduri gwerkeloz eacademici . 10 Degeschiedeni s leerton s dat ervaringen slechts deels overdraagbaar zijn. Elke generatie zal zelfervaringe n moeten opdoen en een weg uit problemen moeten bepalen, want de tevoren doorandere naangedrage noplossinge n worden nauwelijks opgevolgd. Dit kan ook niet want kennise nervarin gzij n tweeverschillend e vormen vanweten . G.H.M.A. Spierts. 11 Dedikt eva nee nproefschrif t ispositie f gecorreleerd met de gehanteerde ondermarge van de pagina. Stellingenbi jhe t proefschrift: 'Swimmingan d musclestructur e in fish' vanIgo rL.Y . Spierts,Wageningen , 28me i 1999. 'Carpe Diem' 1 maart 1998 Pijn in mijn hart... Mijn eersteleermeeste r inhe t spiergebeuren, zalmij n verdereleve n zeker inkleuren. Al diediscussie s en hete vuren, ikzo u nuwille n dat zevoo reeuwi gkonde n duren. Riej e hebt altijd veel voormi j betekend, enwa te r gebeurt, daar had iknooi t op gerekend. Ik wou dati k deklo k terugko n draaien, en nogeen s ouderwets metjo u kon kraaien, omhe t hoogste woord in dieen eruimte , enn u wou ikda ti k geen enkel gesprek verzuimde. Wate roo kza l gebeuren, ik hoopda t ikj e afe nto eno go pka nfleuren. Met mijn eigenwijsheid dieji j tochóó k hebt, hoopi kda t mijn band metjo u nooit meer verlept. Riebedank t voor alleswatj e meto tno gto eheb t gegeven, kennis,aandacht , ruziese n deervaringe n uitjo u leven. Ik hebdie prespec t voorjou w enorme kracht, endatj e ondanks 't gebeuren vanhe t afgelopenjaa r toch altijd weerlacht . Riei khe bj e erglere n waarderen, endi talle sza li kmaa rhee l moeilijk kunnen verteren. Maaréé n ding staati nel k geval voorop, jouw aanwezigheid verlicht vââk mijn (soms) duisterekop . Voor detoekoms t ben iknie tbang , ali s de weg vóór ons toch noger g lang. Igor voor Rie CONTENTS/INHOUD Chapter 1 General introduction 7 Chapter2 Swimming.T ob epublishe d in aGerma n textbook on fish for students (as one chapter): J.W.M. Osse and I.L.Y. Spierts (1999) 25 Chapter3 Musclegrowt han dswimmin gi nlarva eo f Clarias gariepinus (Burchell). Published: H.A.Akster , J.A.J.Verreth , I.L.Y. Spierts,T . Berbner, M. Schmidbauer and J.W.M. Osse (1995) ICES Marine Science Symposia 201: 45-50 79 Chapter4 Localdifference s inmyotendinou sjunction s in axialmuscl efibres o f carp (Cyprinuscarpio L.) .Published : I.L.Y. Spierts,H.A .Akster , I.H.C.Vo san d J.W.M. Osse (1996). Journal of Experimental Biology 199: 825-833 89 Chapter5 Expression oftiti nisoform s inre d and whitemuscl e fibres of carp (Cyprinuscarpio L. )expose d to different sarcomere strains during swimming. Published: I.L.Y. Spierts, H.A.Akste r and H.L. Granzier (1997). Journalof Comparative PhysiologyB 167: 543-551 107 Chapter6 Kinematicsan dmuscl edynamic s of C-an dS-start so f carp (Cyprinuscarpio L.) . Published: I.L.Y.Spiert san dJ.L . vanLeeuwe n (1999). Journalof Experimental Biology20 2 (4): 393-406 125 Chapter7 Howcar p(Cyprinus carpio L.) activateth etrun k muscles during C- and S-starts. Inpreparation : I.L.Y. Spierts,J.L . vanLeeuwen , A. Terlouw and J.W.M. Osse 153 Chapter8 Expression of titin isoforms during theontogen y of carp (Cyprinus carpioL. ) in relation to fast swimming. In preparation: I.L.Y. Spierts 175 Summary/ Samenvatting Swimming and muscle structure infish. Submitted :I.L.Y .Spiert s (1999). Netherlands Journalof Zoology 193 References 203 Dankwoord 217 Curriculum vitae... 219 List of publications... 220 1 General introduction Igor L.Y. Spierts ExperimentalZoolog y Group,Wageninge n Instituteo fAnima l Sciences (WIAS),Wageninge n Agricultural University, P.O.Bo x 338,670 0A H Wageningen; The Netherlands Chapter 1 CONTENTS 1.1. Outline of this thesis 1.2. Chapter 2: Swimming 1.3. Chapter 3: Muscle growth and swimming of larval Clarias gariepinus (Burchel!) 1.4. Chapter 4: Differences in force transmission and in myotendinous junctions in axial muscle of carp (Cyprinus carpio L.) 1.5. Chapter 5: The relation between differences in sarcomere strain in swimming carp and the expression of titin isoforms 1.6. Chapter 6: Kinematics and muscle dynamics of C- and S-starts of adult carp 1.7. Chapter 7: Muscle performance during C- and S-starts of adult carp 1.8. Chapter 8: Expression of titin isoforms during the ontogeny of carp in relation to fast swimming 1.9. Scientific significance 1.10. Relevance for society General introduction 1.1. OUTLINE OF THIS THESIS Thescop eo fth epresen t thesisi st odetermin eho wth e structure of axialmuscle so f fish is adapted toth efunctional , sometimes contrasting, demands of different modes of swimming. Changes of the muscularsyste m withfish siz ean dag ebelon gt othi squestion . Studieso f larval muscle development, of myotendinousjunction s (MTJs, the connections between muscle fibres and tendons), of the giant elasticmuscl eprotei n titin ando fstrain si n sarcomeresdurin gcontinuou s andfas t swimming in larval andadul tcar pwer eperformed . Only afe w highlights of theobtaine d resultsca n be mentioned. During swimming posterior muscle fibres of adult carp have a longer phase of eccentric activity (activewhil ebein g stretched) than anterior fibres and will therefore develop greater forces.
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