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The metabolic cost of turning right side up in the Mediterranean spur-thighed tortoise (Testudo graeca)

  • 1.

    Lyson, T. R. et al. Origin of the unique ventilatory apparatus of turtles. Nat. Commun. 5(5211), 1–11. https://doi.org/10.1038/ncomms6211 (2014).

    CAS 
    Article 

    Google Scholar 

  • 2.

    Gans, C. & Hughes, G. The mechanism of lung ventilation in the tortoise Testudo graeca Linné. J. Exp. Biol. 47(1), 1–20 (1967).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 3.

    Jackson, D. C., Singer, J. H. & Downey, P. T. Oxidative cost of breathing in the turtle Chrysemys picta bellii. Am. J. Physiol. 261, R1325–R1328 (1991).

    CAS 
    PubMed 

    Google Scholar 

  • 4.

    Landberg, T., Mailhot, J. D. & Brainerd, E. L. Lung ventilation during treadmill locomotion in a semi-aquatic turtle, Trachemys scripta. J. Exp. Zool. 311A, 551–562. https://doi.org/10.1002/jez.478 (2009).

    Article 

    Google Scholar 

  • 5.

    Ruhr, I., Rose, K., Sellers, W., Crossley, D. II. & Codd, J. Turning turtle: Scaling relationships and self-righting ability in Chelydra serpentina. Proc. R. Soc. B. 288, 20210213. https://doi.org/10.1098/rspb.2021.0213 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 6.

    Pritchard, P. C. H. Encyclopaedia of Turtles (TFH, 1979).

    Google Scholar 

  • 7.

    Carr, A. Handbook of Turtles: The Turtles of the United States, Canada, and Baja California (Cornell University Press, 1952).

    Google Scholar 

  • 8.

    Rivera, G. Ecomorphological variation in shell shape of the freshwater turtle Pseudemys concinna inhabiting different aquatic flow regimes. Int. Comp. Biol. 48(6), 769–787. https://doi.org/10.1093/icb/icn088 (2008).

    Article 

    Google Scholar 

  • 9.

    McNeill Alexander, R. Gaits of mammals and turtles. J. R. Soc. Jpn. 11(3), 314–319 (1993).

    Article 

    Google Scholar 

  • 10.

    Zani, P. A. & Kram, R. Low metabolic cost of locomotion in ornate box turtles, Terrapene ornate. J. Exp. Biol. 211, 3671–3676. https://doi.org/10.1242/jeb.019869 (2008).

    Article 
    PubMed 

    Google Scholar 

  • 11.

    Sellers, W. I., Rose, K. A. R., Crossley, D. A. II. & Codd, J. R. Inferring cost of transport from whole-body kinematics in three sympatric turtle species with different locomotor habits. Comp. Biochem. Physiol. A. 247, 110739. https://doi.org/10.1016/j.cbpa.2020.110739 (2020).

    CAS 
    Article 

    Google Scholar 

  • 12.

    Chiari, Y., van der Meijden, A., Caccone, A., Claude, J. & Gilles, B. Self-righting potential and the evolution of shell shape in Galápagos tortoises. Sci. Rep. 7(1), 1–8. https://doi.org/10.1038/s41598-017-15787-7 (2017).

    CAS 
    Article 

    Google Scholar 

  • 13.

    Woledge, R. C. The energetics of tortoise muscle. J. Physiol. 197(3), 685–707 (1968).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 14.

    Steyermark, A. C. & Spotila, J. R. Body temperature and maternal identity affect snapping turtle (Chelydra serpentina) righting response. Copeia 4, 1050–1057. https://doi.org/10.1643/0045-8511(2001)001[1050:BTAMIA]2.0.CO;2 (2001).

    Article 

    Google Scholar 

  • 15.

    Rubin, A. M., Blob, R. W. & Mayerl, C. J. Biomechanical factors influencing successful self-righting in the Pleurodire turtle, Emydura subglobosa. J. Exp. Biol. 221, jeb182642. https://doi.org/10.1242/jeb.182642 (2018).

    Article 
    PubMed 

    Google Scholar 

  • 16.

    Penn, D. & Brockmann, H. J. Age-biased stranding and righting in male horseshoe crabs, Limulus polyphemus. Anim. Behav. 49, 1531–1539. https://doi.org/10.1016/003-3472(95)90074-8 (1995).

    Article 

    Google Scholar 

  • 17.

    Bonnet, X. et al. Sexual dimorphism in steppe tortoises (Testudo horsfieldii): Influence of the environment and sexual selection on body shape and mobility. Biol. J. Linn. Soc. 72, 357–372. https://doi.org/10.1006/bjls.2000.0504 (2001).

    Article 

    Google Scholar 

  • 18.

    Zuffi, M. A. L. & Corti, C. Aspects of population ecology of Testudo hermanni hermanni from Asinara Island, NW Sardinia (Italy, Western Mediterranean Sea): Preliminary data. Amphib-Reptil. 24, 441–447 (2003).

    Article 

    Google Scholar 

  • 19.

    Domokos, G. & Várkonyi, P. L. Geometry and self-righting of turtles. Proc. R. Soc. B. 275(1630), 11–17. https://doi.org/10.1098/rspb.2007.1188 (2008).

    Article 
    PubMed 

    Google Scholar 

  • 20.

    Mann, G. K. H., O’Riain, M. J. & Hofmeyr, M. D. Shaping up to fight: Sexual selection influences body shape and size in the fighting tortoise (Chersina angulata). J. Zool. 269, 373–379. https://doi.org/10.1111/j.1469-7998.2006.00079x (2006).

    Article 

    Google Scholar 

  • 21.

    Golubović, A., Bonnet, X., Djordjević, S., Djurakic, M. & Tomović, L. Variations in righting behavior across Hermann’s tortoise populations. J. Zool. 291, 69–75. https://doi.org/10.1111/jzo.12047 (2013).

    Article 

    Google Scholar 

  • 22.

    Golubović, A., Andelkovic, M., Arsovski, D., Bonnet, X. & Tomović, L. Locomotor performances reflect habitat constraints in an armoured species. Behav. Ecol. Sociobiol. 71, 93. https://doi.org/10.1007/s00265-017-2318-0 (2017).

    Article 

    Google Scholar 

  • 23.

    Ashe, V. M. The righting reflex in turtles: A description and comparison. Psychol. Sci. 20, 150–152. https://doi.org/10.3758/BF03335647 (1970).

    Article 

    Google Scholar 

  • 24.

    Golubović, A., Tomović, L. & Ivanović, A. Geometry of self-righting: The case of Hermann’s tortoises. Zool. Anz. 254, 99–105. https://doi.org/10.1016/j.jcz.2014.12.003 (2015).

    Article 

    Google Scholar 

  • 25.

    Finkler, M. S. Influence of water availability during hatching on hatchling size, body composition, desiccation tolerance, and terrestrial locomotor performance in the snapping turtle, Chelydra serpentina. Physiol. Biochem. Zool. 72, 714–722. https://doi.org/10.1086/316711 (1999).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 26.

    Stojadinović, D., Milošević, D. & Crnobrnja-Isailović, J. Righting time versus shell size and shape dimorphism in adult Hermann’s tortoises: Field observations meet theoretical predictions. Anim. Biol. 63(4), 381–396. https://doi.org/10.1163/15707563-00002420 (2013).

    Article 

    Google Scholar 

  • 27.

    Delmas, V., Baudry, E., Girondot, M. & Prevot-Julliard, A.-C. The righting reflex as a fitness indicator in freshwater turtles. Biol. J. Linn. Soc. 91, 99–109. https://doi.org/10.1111/j.1095-8312/2007.00780.x (2007).

    Article 

    Google Scholar 

  • 28.

    Burger, J. Behavior of hatchling diamondback terrapins (Malaclemys terrapin) in the field. Copeia 1976, 742. https://doi.org/10.2307/1443457 (1976).

    Article 

    Google Scholar 

  • 29.

    Landberg, T., Mailhot, J. D. & Brainerd, E. L. Lung ventilation during treadmill locomotion in a terrestrial turtle, Terrapene carolina. J. Exp. Biol. 206, 3391–3404. https://doi.org/10.1242/jeb.00553 (2003).

    Article 
    PubMed 

    Google Scholar 

  • 30.

    Gaunt, A. S. & Gans, C. Mechanics of respiration in the snapping turtle, Chelydra serpentina (Linné). J. Morph. 128, 195–227. https://doi.org/10.1002/jmor.1051280205 (1969).

    Article 

    Google Scholar 

  • 31.

    Lambertz, M., Böhme, W. & Perry, S. F. The anatomy of the respiratory system in Platysternon megacephalum Gray, 1831 (Testudines: Crytodira) and related species, and its phylogenetic implications. Comp. Biochem. Physiol. 156, 330–336. https://doi.org/10.1016/j.cbpa.2009.12.016 (2010).

    CAS 
    Article 

    Google Scholar 

  • 32.

    de Souza, R. B. B. & Klein, W. The influence of the post-pulmonary septum and submersion on the pulmonary mechanics of Trachemys scripta (Cryptodira: Emydidae). J. Exp. Biol. 224(12), 242386. https://doi.org/10.1242/jeb.242386 (2021).

    Article 

    Google Scholar 

  • 33.

    Jodice, P. G. R., Epperson, D. M. & Visser, G. H. Daily energy expenditure in free-ranging gopher tortoises (Gopherus polyphemus). Copeia 2006(1), 129–136. https://doi.org/10.1643/0045-8511(2006)006[0129:DEEIFG]2.0.CO;2 (2006).

    Article 

    Google Scholar 

  • 34.

    Zera, A. J. & Harshman, L. G. The physiology of life history trade-offs in animals. Ann. Rev. Ecol. Syst. 32, 95–126. https://doi.org/10.1146/annurev.ecolsys.32.081501.114006 (2001).

    Article 

    Google Scholar 

  • 35.

    Shadmehr, R., Huang, H. J. & Ahmed, A. A. A representation of effort in decision-making and motor control. Curr. Biol. 26, 1929–1934. https://doi.org/10.1016/j.cub.2016.05.065 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 36.

    Shepard, E. L. C. et al. Energy landscapes shapes animal movement ecology. Am. Nat. 182(3), 298–312. https://doi.org/10.1086/671257 (2013).

    Article 
    PubMed 

    Google Scholar 

  • 37.

    Baudinette, R. V., Miller, A. M. & Sarre, M. P. Aquatic and terrestrial locomotory energetics in a toad and a turtle: A search for generalisations among ectotherms. Physiol. Biochem. Zool. 73(6), 672–682. https://doi.org/10.1086/318101 (2000).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 38.

    Hailey, A. & Coulson, I. M. Measurement of time budgets from continuous observation of thread-trailed tortoises (Kinixys spekii). Herp. J. 9, 15–20 (1999).

    Google Scholar 

  • 39.

    Kram, R. & Taylor, C. R. Energetics of running: A new perspective. Nature 346, 265–267. https://doi.org/10.1038/346265a0 (1990).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar 

  • 40.

    Taylor, C. R. Relating mechanics and energetics during exercise. Adv. Vet. Sci. Comp. Med. 38A, 181–215 (1994).

    CAS 
    PubMed 

    Google Scholar 

  • 41.

    Cavagna, G. A. & Kaneko, M. Mechanical work and efficiency in level walking and running. J. Physiol. 268(2), 467–481. https://doi.org/10.1113/jphysiol.1977.sp011866 (1977).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 42.

    Carrier, D. R., Deban, S. M. & Fischbein, T. Locomotor function of the pectoral girdle “muscular sling” in trotting dogs. J. Exp. Biol. 209, 2224–2237. https://doi.org/10.1242/jeb.02236 (2006).

    Article 
    PubMed 

    Google Scholar 

  • 43.

    Heglund, N. C. & Cavagna, G. A. Efficiency of vertebrate locomotory muscles. J. Exp. Biol. 115, 283–292. https://doi.org/10.1242/jeb.115.1.283 (1985).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 44.

    Barclay, C. J. The basis of difference in thermodynamic efficiency among skeletal muscles. Clin. Exp. Pharm. Physiol. 44(12), 1279–1286. https://doi.org/10.1111/1440-1681.12850 (2017).

    MathSciNet 
    CAS 
    Article 

    Google Scholar 

  • 45.

    Nwoye, L. O. & Goldspink, G. Biochemical efficiency and intrinsic shortening speed in selected fast and slow muscles. Experientia 37, 856–857. https://doi.org/10.1007/BF1985678 (1981).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 46.

    Lambert, M. Temperature, activity and field sighting in the Mediterranean spur-thighed or common garden tortoise Testudo graeca. Biol. Conserv. 21, 39–54. https://doi.org/10.1016/0006-3207(81)90067-7 (1981).

    Article 

    Google Scholar 

  • 47.

    Tracy, R., Zimmerman, L., Tracy, C., Bradley, K. & Castle, K. Rates of food passage in the digestive tract of young desert tortoises: Effects of body size and diet quality. Chelonian Conserv. Biol. 5(2), 269–273. https://doi.org/10.2744/1071-8443(2006)5[269:ROFPIT]2.0.co;2 (2006).

    Article 

    Google Scholar 

  • 48.

    Huey, R. & Kingsolver, J. Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4(5), 131–135. https://doi.org/10.1016/0169-5347(89)90211-5 (1989).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 49.

    Lailvaux, S. & Irschick, D. Effects of temperature and sex on jump performance and biomechanics in the lizard Anolis carolinensis. Funct. Ecol. 21(3), 534–543. https://doi.org/10.1111/j.1365-2435.2007.01263.x (2007).

    Article 

    Google Scholar 

  • 50.

    Lighton, J. Measuring Metabolic Rates: A Manual for Scientists (Oxford University Press, 2008).

    Book 

    Google Scholar 

  • 51.

    Brody, S. Bioenergetics and Growth (Reinhold, 1945).

    Google Scholar 

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