Reduced swimming abilities in fast-growing transgenic common carp Cyprinus carpio associated with their morphological variations

Journal of Fish Biology

Volumn 74, Issue 1, 2009, Pages 186-197

  Li, D ^a,b   Hu, W ^a   Wang, Y ^a   Zhu, Z ^a   Fu, C ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Cyprinidae; Growth; Morphology; Swimming performance; Trade off; Transgene

Indexed keywords

GROWTH HORMONE;

ANIMAL; ARTICLE; CARP; COMPARATIVE STUDY; GENETICS; HISTOLOGY; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; SWIMMING; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARPS; GROWTH HORMONE; PRINCIPAL COMPONENT ANALYSIS; SWIMMING;

CYPRINIDAE; CYPRINIFORMES; CYPRINUS CARPIO;

EID: 58549101949     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2008.02128.x     Document Type: Article

References (74)

1. Álvarez, D. Metcalfe, N. B 2005). Catch-up growth and swimming performance in threespine sticklebacks (Gasterosteus aculeatus): seasonal changes in the cost of compensation. Canadian Journal of Fish Aquatic Sciences 62, 2169 2176.
2. Arendt, J. D 1997). Adaptive intrinsic growth rates: an integration across taxa. The Quarterly Review of Biology 72, 149 177.
3. Arendt, J. D 2003). Reduced burst speed is a cost of rapid growth in anuran tadpoles: problems of autocorrelation and inferences about growth rates. Functional Ecology 17, 328 334.
4. Arendt, J. Hoang, L 2005). Effect of food level and rearing temperature on burst speed and muscle composition of western spadefoot toad (Spea hammondii). Functional Ecology 19, 982 987.
5. Arnott, S. A., Chiba, S. Conover, D. O 2006). Evolution of intrinsic growth rate: metabolic costs drive trade-offs between growth and swimming performance in Menidia menidia. Evolution 60, 1269 1278.
6. Beamish, F. W. H 1978). Swimming capacity. In Fish Physiology, Vol. 7 (Hoar, W. H. Randall, D. J., eds pp. 101 187. New York, NY : Academic Press.
7. Bell, W. H. Terhune, L. D. B 1970). Water tunnel design for fisheries research. Fisheries Research Board of Canada Technical Reports 195, 1 69.
8. Billerbeck, J. M., Lankford, T. E. Conover, D. O 2001). Evolution of intrinsic growth and energy acquisition rates. I. Tradeoffs with swimming performance in Menidia menidia. Evolution 55, 1863 1872.
9. Biro, P. A., Abrahams, M. V., Post, J. R. Parkinson, E. A 2004). Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proceedings of the Royal Society B 271, 2233 2237.
10. Biro, P. A., Abrahams, M. V., Post, J. R. Parkinson, E. A 2006). Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. Journal of Animal Ecology 75, 1165 1171.
11. Blake, R. W 2004). Fish functional design and swimming performance. Journal of Fish Biology 65, 1193 1222.
12. Blake, R. W., Law, T. C., Chan, K. H. S. Li, J. F. Z 2005). Comparison of the prolonged swimming performances of closely related, morphologically distinct three-spined sticklebacks Gasterosteus spp. Journal of Fish Biology 67, 834 848.
13. Boily, P. Magnan, P 2002). Relationship between individual variation in morphological characters and swimming costs in brook charr (Salvelinus fontinalis) and yellow perch (Perca flavescens). Journal of Experimental Biology 205, 1031 1036.
14. Bourke, P., Magnan, P. Rodrigues, M. A 1997). Individual variations in habitat use and morphology in brook charr. Journal of Fish Biology 51, 783 794.
15. Brauner, C. J., Iwama, G. K. Randalld, J 1994). The effect of short-duration seawater exposure on the swimming performance of wild and hatchery-reared juvenile coho salmon (Oncorhynchus kisutch) during smoltification. Canadian Journal of Fisheries and Aquatic Sciences 51, 2188 2194.
16. Brett, J. R 1964). The respiratory metabolism and swimming performance of young sockeye salmon. Canadian Journal of Fisheries and Aquatic Sciences 21, 1183 1226.
17. Burnaby, T. P 1966). Growth-invariant discriminant functions and generalized distances. Biometrics 22, 96 110.
18. Dayton, G. H., Saenz, D., Baum, K. A., Langerhans, R. B. Dewitt, T. J 2005). Body shape, burst speed and escape behavior of larval anurans. Oikos 111, 582 591.
19. Deitch, E. J., Fletcher, G. L., Petersen, L. H., Costa, I. A. S. F., Shears, M. A., Driedzic, W. R. Gamperl, A. K 2006). Cardiorespiratory modifications, and limitations, in post-smolt growth hormone transgenic Atlantic salmon Salmo salar. Journal of Experimental Biology 209, 1310 1325.
20. Devlin, R. H., Yesaki, T., Biagy, C. A., Donaldson, E. M., Swanson, P. Chan, W. K 1994). Extraordinary salmon growth. Nature 371, 209 210.
21. Devlin, R. H., Yesaki, T. Y., Donaldson, E. M., Du, S. J. Hew, C. L 1995). Production of germline transgenic Pacific salmonids with dramatically increased growth performance. Canadian Journal of Fisheries and Aquatic Sciences 52, 1376 1384.
22. Devlin, R. H., Sundstrom, L. F. Muir, W. M 2006). Interface of biotechnology and ecology for environmental risk assessments of transgenic fish. Trends in Biotechnology 24, 89 97.
23. Du, S. J., Gong, Z. Y., Fletcher, G. L., Shears, M. A., King, M. J., Idler, D. R. Hew, C. L 1992). Growth enhancement in transgenic Atlantic salmon by the use of an 'all-fish' chimeric growth hormone gene construct. Biotechnology 10, 176 181.
24. 2 transgenic common carp (Cyprinus carpio). Marine Biotechnology 4, 604 611.
25. Dynes, J., Magnan, P., Bernatchez, L. Rodriguez, M. A 1999). Genetic and morphological variations between two forms of lacustrine brook charr. Journal of Fish Biology 47, 775 787.
26. Farrell, A. P. Steffensen, J. F 1987). An analysis of the energetic cost of the branchial and cardiac pumps during sustained swimming in trout. Fish Physiology and Biochemistry 4, 73 79.
27. Farrell, A. P., Bennett, W. Devlin, R. H 1997). Growth-enhanced transgenic salmon can be inferior swimmers. Canadian Journal of Zoology 75, 335 337.
28. Fisher, R. Hogan, J. D 2007). Morphological predictors of swimming speed: a case study of pre-settlement juvenile coral reef fishes. Journal of Experimental Biology 210, 2436 2443.
29. Fu, C., Hu, W., Wang, Y. Zhu, Z 2005). Developments in transgenic fish in the people's Republic of China. Revue Scientifique et Technique-office International des Epizooties 24, 299 307.
30. Fu, C., Li, D., Hu, W., Wang, Y. Zhu, Z 2007a). Fast-growing transgenic common carp mounting compensatory responses. Journal of Fish Biology 71 (Suppl. B 174 185.
31. 2 'all-fish' growth hormone gene transgenic common carp. Journal of Fish Biology 70, 347 361.
32. Gregory, T. R. Wood, C. M 1998). Individual variation and interrelationships between swimming performance, growth rate, and feeding in juvenile rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 55, 1583 1590.
33. Gregory, T. R. Wood, C. M 1999). Interactions between individual feeding behaviour, growth, and swimming performance in juvenile rainbow trout (Oncorhynchus mykiss) fed different rations. Canadian Journal of Fisheries and Aquatic Sciences 56, 479 486.
34. Hawkins, D. K. Quinn, T. P 1996). Critical swimming velocity and associated morphology of juvenile coastal cutthroat trout (Oncorhynchus clarki clarki), steelhead trout (Oncorhynchus mykiss), and their hybrids. Canadian Journal of Fisheries and Aquatic Sciences 53, 1487 1496.
35. Hill, J. A., Kiessling, A. Devlin, R. H 2000). Coho salmon (Oncorhynchus kisutch) transgenic for a growth hormone gene construct exhibit increased rates of muscle hyperplasia and detectable levels of differential gene expression. Canadian Journal of Fisheries and Aquatic Sciences 57, 939 950.
36. Hu, W., Wang, Y. Zhu, Z 2007). Progress in the evaluation of transgenic fish for possible ecological risk and its containment strategies. Science in China Series C: Life Sciences 50, 573 579.
37. Kolok, A. S. Oris, J. T 1995). The relationship between specific growth rate and swimming performance in male fathead minnows (Pimephales promelas). Canadian Journal of Zoology 73, 2165 2167.
38. Law, T. C. Blake, R. W 1996). Comparison of the fast-start performance of closely related, morphologically distinct threespine sticklebacks (Gasterosteus spp.). The Journal of Experimental Biology 199, 2595 2604.
39. Lee, C. G., Devlin, R. H. Farrell, A. P 2003). Swimming performance, oxygen consumption and excess post-exercise oxygen consumption in adult transgenic and ocean-ranched coho salmon. Journal of Fish Biology 62, 753 766.
40. Li, D., Fu, C., Hu, W., Wang, Y. Zhu, Z 2007). Rapid growth cost in 'all-fish' growth hormone gene transgenic carp: reduced critical swimming speed. Chinese Science Bulletin 52, 923 926.
41. Mangel, M. Munch, S. B 2005). A life-history perspective on short- and long-term consequences of compensatory growth. American Naturalist 166, E155 E176.
42. Martinez, R., Estrada, M. P., Berlanga, J., Guillen, I., Hernandez, O., Cabrera, E., Pimentel, R., Morales, R., Herrera, F., Morales, A., Pina, J. C., Abad, Z., Sanchez, V., Melamed, P., Lleonart, R. de la Fuente, J 1996). Growth enhancement in transgenic tilapia by ectopic expression of tilapia growth hormone. Marine Molecular Biology and Biotechnology 5, 62 70.
43. McGarigal, K., Cushman, S. Stafford, S 2000). Multivariate Statistics for Wildlife and Ecology Research. New York, NY : Springer-Verlag.
44. McKenzie, D. J., Martinez, R., Morales, A., Acosta, K., Taylor, E. W., Steffensen, J. F. Estrada, M. P 2003). Effects of growth hormone transgenesis on metabolic rate, exercise performance and hypoxia tolerance in tilapia hybrids. Journal of Fish Biology 63, 398 409.
45. McLaughlin, R. L. Grant, J. W. A 1994). Morphological and behavioural differences among recently-emerged brook charr, Salvelinus fontinalis, foraging in slow vs. fast-running water. Environmental Biology of Fishes 39, 289 300.
46. Morgan, I. J. Metcalfe, N. B 2001). Deferred costs of compensatory growth after autumnal food shortage in juvenile salmon. Proceedings of the Royal Society B 268, 295 301.
47. Munch, S. B. Conover, D. O 2004). Nonlinear growth cost in Menidia menidia: theory and empirical evidence. Evolution 58, 661 664.
48. Nam, Y. K., Noh, J. K., Cho, Y. S., Cho, H. J., Cho, K. N., Kim, C. G. Kim, D. S 2001). Dramatically accelerated growth and extraordinary gigantism of transgenic mud loach Misgurnus mizolepis. Transgenic Research 10, 353 362.
49. Nanami, A 2007). Juvenile swimming performance of three fish species on an exposed sandy beach in Japan. Journal of Experimental Marine Biology and Ecology 348, 1 10.
50. Ostenfeld, T. H., McLean, E. Devlin, R. H 1998). Transgenesis changes body and head shape in Pacific salmon. Journal of Fish Biology 52, 850 854.
51. Plaut, I. (2001). Critical swimming speed: its ecological relevance. Comparative Biochemistry and Physiology A 131, 41 50.
52. Rahman, M. A., Mak, R., Ayad, H., Smith, A. Maclean, N 1998). Expression of a novel piscine growth hormone gene results in growth enhancement in transgenic tilapia (Oreochromis niloticus). Transgenic Research 7, 357 369.
53. Robinson, B. W. Wilson, D. S 1994). Character release and displacement in fishes: a neglected literature. American Naturalist 144, 596 627.
54. Rolf, F. J. Bookstein, F. L 1987). A comment on shearing as a method for 'size correlation'. Systematic Zoology 36, 356 367.
55. Sagnes, P., Gaudin, P. Statzner, B 1997). Shifts in morphometrics and their relation to hydrodynamic potential and habitat use during grayling ontogenesis. Journal of Fish Biology 50, 846 858.
56. Seiler, S. M. Keeley, E. R 2007). Morphological and swimming stamina differences between Yellow cutthroat trout (Oncorhynchus clarkia bouvieri), rainbow trout (Oncorhynchus mykiss) and their hybrids. Canadian Journal of Fisheries and Aquatic Sciences 64, 127 135.
57. Sheehan, T. F., Kocik, J. F., Cadrin, S. X. Legault, C. M 2005). Marine growth and morphometrics for three populations of Atlantic salmon from eastern Maine, USA. Transactions of the American Fisheries Society 134, 775 788.
58. Snorrason, S. S., Skulason, S., Jonsson, B., Malmquist, H. J., Sandlund, O. T. Lindem, T 1994). Trophic specialization in Arctic charr Salvelinus alpinus (Pisces: Salmonidae): morphological divergence and ontogenic niche shifts. Biological Journal of the Linnean Society 52, 1 18.
59. Stamps, J. A 2007). Growth-mortality tradeoffs and 'personality traits' in animals. Ecology Letters 10, 355 363.
60. Stevens, E. D. Devlin, R. H 1999). Intestinal morphology in growth hormone transgenic coho salmon. Journal of Fish Biology 56, 191 195.
61. Stevens, E. D. Devlin, R. H 2005). Gut size in GH-transgenic coho salmon is enhanced by both the GH transgene and increased food intake. Journal of Fish Biology 66, 1633 1648.
62. Stevens, E. D., Sutterlin, A. Cook, T 1998). Respiratory metabolism and swimming performance in growth hormone transgenic Atlantic salmon. Canadian Journal of Fisheries and Aquatic Sciences 55, 2028 2035.
63. Stevens, E. D., Wagner, G. N. Sutterlin, A 1999). Gut morphology in growth hormone transgenic Atlantic salmon. Journal of Fish Biology 55, 517 526.
64. Strauss, R. E. Bookstein, F. L 1982). The truss: body form reconstructions in morphometrics. Systematic Zoology 31, 113 135.
65. Sundström, L. F., Lõhmus, F., Tymchuk, W. E. Devlin, R. H 2007). Gene-environment interactions influence ecological consequences of transgenic animals. Proceedings of the Royal Society B 104, 3889 3894.
66. Taylor, E. B. Foote, C. J 1991). Critical swimming velocities of juvenile sockeye salmon and kokanee, the anadromous and non-anadromous forms of Oncorhynchus nerka (Walbaum). Journal of Fish Biology 38, 407 419.
67. Tudorache, C., Viaenen, P., Blust, R. Boech, G. D. E 2007). Longer flumes increase critical swimming speeds by increasing burst-glide swimming duration in carp Cyprinus carpio, L. Journal of Fish Biology 71, 1630 1638.
68. 1 generation. Chinese Science Bulletin 46, 1174 1177.
69. Webb, P. W 1975). Hydromechanics and energetics of fish propulsion. Bulletin of the Fisheries Research Board of Canada 190, 109 119.
70. Webb, P. W 1982). Locomotor patterns in the evolution of Actinopterygians fishes. American Zoologist 22, 329 342.
71. Webb, P. W 1984). Body form, locomotion and foraging in aquatic vertebrates. American Zoologist 24, 107 120.
72. Zbikowska, H. M 2003). Fish can be first-advances in fish transgenesis for commercial applications. Transgenic Research 12, 379 389.
73. Zhu, Z. Y 1992). Growth hormone gene and the transgenic fish. In Agricultural Biotechnology (You, C. B. Chen, Z. Z., eds pp. 106 116. Beijing : China Science and Technology Press.
74. Zhu, Z., Li, G., He, L. Chen, S 1985). Novel gene transfer into the fertilized eggs of goldfish (Carassius auratus L. 1758). Journal of Applied Ichthyology 1, 31 34.