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Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour

Ian A. Johnston* and Genevieve K. Temple

Gatty Marine Laboratory, School of Biology, University of St Andrews, St Andrews, Fife KY16 8LB, Scotland, UK



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Fig. 1. Influence of acclimation temperature on relative feed intake (solid line) and spontaneous swimming activity (open circles) for largemouth mass (Micropterus salmoides). The test temperature was the same as acclimation temperature. Values are means ± S.E.M. (N=6-9 fish). Adapted from Lemons and Crawshaw (1985Go) with permission.

 


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Fig. 2. The forced exercise model used to examine the thermal plasticity of swimming in the goldfish (Carassius auratus L.) The maximum speed that could be sustained for 2min in a rotating chamber is shown as a function of test temperature for fish acclimated to 5°C ([UNK]), 15°C ({circ}), 25°C ({blacktriangledown}) and 35°C ({nabla}). Adapted from Fry and Hart (1948Go) with permission.

 


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Fig. 3. Thermal plasticity of fast-start behaviour in various fish species. The figure illustrates maximum length-specific speed during escape responses in fish acclimated to different temperatures in (A) goldfish Carassius auratus, N=10, (B) killifish Fundulus heteroclitus, N=5, (C) long-spined sea scorpion Taurulus bubalis, N=7, and (D) short-horn sculpin Myoxocephalus scorpius, N=9. Arrows indicate the direction of the acclimation response at a specified test temperature; the horizontal line (in D) indicates no change. Values are means ± S.E.M. See original publications for experimental details. The data are adapted from Johnson and Bennett (1995Go) and Temple and Johnston (1998Go). L, total body length.

 


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Fig. 4. (A) Thermal plasticity of Mg2+-Ca2+ myofibrillar ATPase activity acquired during ontogeny in the common carp. The time course of changes in enzymic activity was longer for juveniles at 14 weeks (purple) than at 20 weeks (green) post-hatch. The blue and red shaded areas represent the myofibrillar ATPase activity of 120 mm total length (TL) 10°C- and 21°C-acclimated carp respectively. The lengths of the fish during the experiment are indicated with colour-coded arrows. (B,C) Changes in myosin heavy chain (MyHC) peptide maps (top) and their densitometric scans (bottom) with age and acclimation temperature. Bands characteristic of 21°C-acclimated and 10°C-acclimated fish are indicated by left- and right-facing arrowheads, respectively. The MyHC composition characteristic of cold acclimation was not observed in any fish greater than 37 mm total length. Adapted from Cole and Johnston (2001Go).

 


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Fig. 5. Thermal plasticity of fast-start behaviour in the long-spined sea scorpion (Taurulus bubalis Euphr.). (A,B) Representative contour plots showing how the non-dimensional body curvature, C, changes with time and body position (0=snout, 1.0=tail) during fast-starts. L, body length. (A) Results for a 15°C-acclimated fish tested at 20°C; (B) results for a 5°C-acclimated fish tested at 20°C. The slope of the solid line is inversely proportional to the rate at which the wave of curvature (Û, s-1) travels down the fish. The grey area indicates the period over which the mean inertial power requirements were calculated. (C) The velocity of the wave of curvature (Û) travelling down the body of the fish for 5°C-acclimated (circles) and 15°C-acclimated (triangles) individuals. (D) The power requirements of the contralateral contraction of escape responses. An asterisk indicates significant differences between acclimated groups at 0.8 and 20°C. Values are means ± S.E.M. (N=7). From Temple (1998Go).

 


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Fig. 6. Influence of seasonal acclimatisation (A) and laboratory acclimation (B,C,D) and on the power output of fast muscle fibres from the short-horn sculpin (Myoxocephalus scorpius). (A) The relationship between cycle frequency and power output (W kg-1 wet muscle mass) of fast fibre bundles undergoing sinusoidal length changes. From Johnson and Johnston (1991Go). (B) Strain. (C) Maximum instantaneous and (D) mean power (W Kg-1 wet muscle mass) output of fast fibres undergoing length change patterns recorded during the contralateral contraction of a fast-start escape response. Asterisks indicate significant differences between acclimation groups: *P<0.05, **P<0.001. Values are means ± S.E.M. (N=6 for 5°C-acclimated fish and N=7 for 15°C-acclimated fish). From Temple et al. (2000Go).

 


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Fig. 7. (A—D) Influence of temperature acclimation on maximum speed during locomotion, Umax, in (A) tadpoles and (B) adults of the striped marsh frog (Limnodynastes peronii) and (C) tadpoles and (D) adults of the African clawed frog (Xenopus laevis). (E) Influence of temperature acclimation on the time from last stimulus to 50 % tetanic relaxation, RT1/2, of isolated gastrocnemius muscle from adult X. laevis. From Wilson and Franklin (1999Go, 2000Go) and Wilson et al. (2000Go) with permission. Values are means ± S.E.M. (A, N=15; B—E, N=10-12). Asterisks denote significant differences between groups (P<0.05).

 


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Fig. 8. Developmental plasticity of myofibrillar protein composition and slow muscle innervation patterns in the myotomal muscles of Atlantic herring (Clupea harengus) reared at 12 or 5 °C. After hatching, temperature was allowed to rise, mimicking a seasonal warming. MyHC, myosin heavy chains; LC2, myosin light chain 2; TNI, troponin I; TNT, troponin T; LC3f, myosin light chain 3. Blue, embryonic pattern; yellow, adult pattern. Data from Johnston et al. (1997Go, 1998Go).

 


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Fig. 9. Influence of rearing temperature on dorsal and anal fin ray muscle development in Atlantic herring (Clupea harengus). (A) Embryos were incubated at 5 °C (open circles) or 12 °C (filled circles) until first feeding and then reared at ambient temperature. (B,C) Whole-mount larvae of 16.2 mm total length stained for acetylcholinesterase activity following the 5 °C (B) and 12 °C (C) rearing regimes. From Johnston et al. (2001Go). a, anus; frm, fin ray muscles; ms, myosepta. (D) Number of dorsal fin ray muscles (second-order polynomials were fitted to the data) and (E) number of anal fin ray muscles innervated in relation to total body length (TL) in larvae reared under the two thermal regimes shown in A. First-order linear regressions were fitted to the data.

 


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Fig. 10. (A) Escape response of Clyde herring larva (Clupea harengus) 18 mm total length, filmed at 200 frames s-1. (B) Maximum velocity attained during escape responses in Clyde herring larvae reared at 5 °C (open circles, dashed line) and 12 °C (filled circles, solid line) until first feeding, when they were transferred to ambient seawater temperatures. Each point represents an escape response from one larva. First-order linear regressions were fitted to the data. 5 °C, Umax=-3.12TL1.92, r2=0.42, P=0.002; 12 °C, Umax=2.20TL1.21, r2=0.48, P=0.001), where Umax is maximum swimming velocity (m s-1) and TL is total length (mm). From Johnston et al. (2001Go).

 

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