Effects of growth hormone transgenes on the behavior and welfare of aquacultured fishes: A review identifying research needs

Applied Animal Behaviour Science

Volumn 104, Issue 3-4, 2007, Pages 265-294

  Hallerman, Eric M ^a   McLean, Ewen ^a   Fleming, Ian A ^b  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Aquaculture; Behavior; Fish; Growth hormone; Transgenic; Welfare

Indexed keywords

ANIMAL WELFARE; AQUACULTURE PRODUCTION; BEHAVIORAL RESPONSE; FISH CULTURE; GENE EXPRESSION; GENETICALLY MODIFIED ORGANISM; GROWTH RESPONSE; HORMONE; STOCK ENHANCEMENT;

ANIMALIA; CYPRINIDAE; CYPRINUS CARPIO; ONCORHYNCHUS KISUTCH; PISCES; SALMO SALAR; TILAPIA;

EID: 34047176303     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2006.09.008     Document Type: Review

References (181)

1. Abrahams M.V., and Sutterlin A. The foraging and antipredator behavior of growth-enhanced transgenic Atlantic salmon. Anim. Behav. 58 (1999) 933-942
2. Amanuma K., Takeda H., Amanuma H., and Aoki Y. Transgenic zebrafish for detecting mutations caused by compounds in aquatic environments. Nat. Biotechnol. 18 (2000) 62-65
3. AquaNet. Production of Transgenic Tilapia for the Treatment of Diabetes: ES-cell Approach (2005). http://www.aquanet.ca/ http://www.aquanet.ca (accessed September 27, 2005)
4. Avashti A. GM Fish Produce Cheap Blood-clotting Agent (2004). http://www.newscientist.com/ http://www.newscientist.com (accessed September 27, 2005)
5. Bartke A. Can growth hormone (GH) accelerate aging? Evidence from GH-transgenic mice. Neuroendocrinolgy 78 (2003) 210-216
6. Bartke A., Chandrashekar V., Bailey B., Zaczek D., and Turyn D. Consequence of growth hormone (GH) overexpression and GH resistance. Neuropeptides 36 (2002) 201-208
7. Bessey C., Devlin R.H., Liley N.R., and Biagi C.A. Reproductive performance of growth-enhanced transgenic coho salmon. Trans. Am. Fish. Soc. 133 (2004) 1205-1220
8. Biagi C.A., Byatt J.C., Devlin R.H., Smailus D.E., and Yesaki T.Y. Growth of domesticated transgenic fish. Nature 409 (2001) 781-782
9. Biro P.A., Abrahams M.V., Post J.R., and Parkinson E.A. Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 271 (2004) 2233-2237
10. Bjornsson B.T., Taranger G.L., Hansen T., Steffansson S.O., and Haux C. The interrelation between photoperiod, growth hormone, and sexual maturation of adult Atlantic salmon (Salmo salar). Gen. Comp. Endocrinol. 93 (1994) 70-81
11. Blier P.U., Lemieux H., and Devlin R.H. Is the growth rate of fish set by digestive enzymes or metabolic capacity of the tissues? Insight from transgenic coho salmon. Aquaculture 209 (2002) 379-384
12. Brem G., Brenig B., Horstgen-Schwark G., and Winnacker E.-L. Gene transfer in tilapia (Oreochromis niloticus). Aquaculture 68 (1988) 209-219
13. Cabezas L., Herrera F., Martinez R., Arenal A., Estrada M.P., and de la Fuente J. Growth performance of transgenic hybrid tilapia (Oreochromis sp.) under intensive culture conditions. In: Fitzsimmons K. (Ed). Tilapia Aquaculture: Proceedings of the Fourth International Symposium on Tilapia in Aquaculture. Orlando, Florida, November 9-12, 1997 (1997) 109-115 NRAES-106
14. Carvan III M.J., Dalton T.P., Stuart G.W., and Nebert D.W. Transgenic zebrafish as sentinels for aquatic pollution. Ann. N. Y. Acad. Sci. 919 (2000) 133-147
15. Chandroo K.P., Duncan I.J.H., and Moccia R.D. Can fish suffer? Perspectives on sentience, pain, fear, and stress. Appl. Anim. Behav. Sci. 86 (2004) 225-250
16. Chatakondi N., Lovell R.T., Duncan P.L., Hayat M., Chen T.T., Powers D.A., Weete J.D., Cummins K., and Dunham R.A. Body composition of transgenic common carp, Cyprinus carpio, containing rainbow trout growth hormone gene. Aquaculture 138 (1995) 99-109
17. 14C in the skeletal muscle of rainbow trout, Salmo gairdneri, after administration of growth hormone. Pakistani J. Zool. 10 (1978) 119-123
18. Chourrout D.R., Guyomard, and Houdebine L.-M. High efficiency gene transfer in rainbow trout (Salmo gairdneri Rich.) by microinjection into egg cytoplasm. Aquaculture 51 (1986) 143-150
19. Clarke W.C., Farmer S.W., and Hartwell K.M. Effect of teleost pituitary growth hormone on growth of Tilapia mossambica and on growth and seawater adaptation of sockeye salmon Oncorhynchus nerka. Gen. Comp. Endocrinol. 33 (1977) 174-178
20. Cook J.T., McNiven M.A., Richardson G.F., and Sutterlin A.M. Growth rate, body composition, and feed digestibility/conversion of growth-enhanced transgenic Atlantic salmon. Aquaculture 188 (2000) 15-32
21. Cook J.T., McNiven M.A., and Sutterlin A.M. Metabolic rate of pre-smolt growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188 (2000) 33-45
22. Cook J.T., Sutterlin A.M., and McNiven M.A. Effect of food deprivation on oxygen consumption and body composition of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188 (2000) 47-63
23. Cui, Z., 1998. Biosafety assessment of GH-transgenic common carp (Cyprinus carpio L.). Ph.D. Dissertation. Institute of Hydrobiology, Chinese Academy of Science, Wuhan, China.
24. 2 red carp (Cyprinus carpio L. red var.). Chin. Sci. Bull. 41 (1996) 591-596
25. de la Fuente J., Guillen I., Martinez R., and Estrada M.P. Growth regulation and enhancement in tilapia: basic research findings and their applications. Genet. Anal.: Biomol. Eng. 15 (1999) 85-90
26. de la Fuente J., Hernandez O., Martinez R., Guillen I., Estrada M.P., and Lleonart R. Generation, characterization and risk assessment of transgenic tilapia with accelerated growth. Biotechnologia Aplicada 12 (1996) 221-230
27. Devlin R.H., Biagi C.A., and Yesaki T.Y. Growth viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236 (2004) 607-632
28. Devlin R.H., Biagi C.A., Yesaki T.Y., Smailus D.E., and Byatt J.C. A growth-hormone transgene boosts the size of wild but not domesticated trout. Nature 409 (2001) 781-782
29. Devlin R.H., Byatt J.C., McLean E., Yesaki T.Y., Krivi G.G., Jaworski E.G., and Donaldson E.M. Bovine placental lactogen is a potent stimulator of growth and displays strong binding to hepatic receptor sites of coho salmon. Gen. Comp. Endocrinol. 95 (1994) 31-41
30. Devlin R.H., D'Andrade M., Uh M., and Biagi C.A. Population effects of growth hormone transgenic coho salmon depend on food availability and genotype by environment interactions. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 9303-9308
31. Devlin R.H., Johnsson J.I., Smailus D.E., Biagi C.A., Johnsson E., and Bjornsson B.T. Increased ability to compete for food by growth hormone transgenic coho salmon (Oncorhynchus kisutch Walbaum). Aquac. Res. 30 (1999) 1-4
32. Devlin R.H., Swanson P., Clarke W.C., Plisetskaya E., Dickhoff W., Moriyama S., Yesaki T.Y., and Hew C.L. Seawater adaptability and hormone levels in growth-enhanced transgenic coho salmon, Oncorhynchus kisutch. Aquaculture 191 (2000) 367-385
33. Devlin R.H., Yesaki T.Y., Biagi C.A., Donaldson E.M., Swanson E.M.P., and Chan W.-K. Extraordinary salmon growth. Nature 371 (1994) 209-210
34. Devlin R.H., Yesaki T.Y., Donaldson E.M., Du S.J., and Hew C.L. Production of germline transgenic Pacific salmonids with dramatically increased growth performance. Can. J. Fish. Aquat. Sci. 52 (1995) 1376-1384
35. Devlin R.H., Yesaki T.Y., Donaldson E.M., and Hew C.L. Transmission and phenotypic effects of an antifreeze/GH gene construct in coho salmon (Oncorhynchus kisutch). Aquaculture 137 (1995) 161-169
36. Dodd A., Curtis P.M., Williams L.C., and Love D.R. Zebrafish: bridging the gaps between development and disease. Hum. Mol. Genet. 9 (2000) 2443-2449
37. Dooley K., and Zon L.I. Zebrafish: a model system for the study of human disease. Curr. Opin. Genet. Dev. 10 (2000) 252-256
38. Du S.J., Gong Z.Y., Fletcher G.L., Shears M.A., King M.J., Idler D.R., and Hew C.L. Growth enhancement in transgenic Atlantic salmon by the use of an all-fish chimeric growth hormone gene construct. BioTechnology 10 (1992) 176-181
39. Dunham, R.A., 1994. Predator Avoidance, Spawning and Foraging Ability of Transgenic Catfish, http://www.nbiap.vt.edu/brarg/brasym94/dunham.htm.
40. 1 complementary DNA when subjected to low dissolved oxygen. Mar. Biotechnol. 4 (2002) 323-327
41. Dunham R.A., Chitmanat C., Nichols A., Argue B., Powers D.A., and Chen T.T. Predator avoidance of transgenic channel catfish containing salmonids growth hormone genes. Mar. Biotechnol. 1 (1999) 545-551
42. Dunham R.A., and Devlin R.H. Comparison of traditional breeding and transgenesis in farmed fish with implications for growth enhancement and fitness. In: Murray J.D., Anderson G.B., Oberbauer A.M., and McGloughlin M.N. (Eds). Transgenic Animals in Agriculture (1998), CABI, Wallingford, UK 209-229
43. Dunham R.A., Eash J., Askins J., and Townes T.M. Transfer of the metallothionein-human growth hormone fusion gene into channel catfish. Trans. Am. Fish. Soc. 116 (1987) 87-91
44. Dunham R.A., Ramboux A.C., Duncan P.L., Hayat M., Chen T.T., Lin C.M., Kight K., Gonzalez-Villasenor I., and Powers D.A. Transfer, expression and inheritance of salmonid growth hormone genes in channel catfish, Ictalurus punctatus, and effects on performance traits. Mar. Mol. Biol. Biotechnol. 1 (1992) 380-389
45. Dunham R.A., Warr G.W., Nichols A., Duncan P.L., Argue B., Middleton D., and Kucuktas H. Enhanced bacterial disease resistance of transgenic channel catfish Ictalurus punctatus possessing cecropin genes. Mar. Biotechnol. 4 (2002) 338-344
46. Eales J.G., Devlin R., Higgs D.A., McLeese J.M., Oakes J.D., and Plohman J. Thyroid function in growth-hormone-transgenic coho salmon (Oncorhynchus kisutch). Can. J. Zool. 82 (2004) 1225-1229
47. Einum S., and Fleming I.A. Highly fecund mothers sacrifice offspring survival to maximise fitness. Nature 405 (2000) 565-567
48. Einum S., and Fleming I.A. Selection against late emergence and small offspring in Atlantic salmon. Evolution 54 (2000) 628-639
49. Einum S., and Fleming I.A. Implications of stocking: ecological interactions between wild and released salmonids. Nordic J. Freshwater Res. 75 (2001) 56-70
50. Entis E. Aquabiotech: a blue revolution?. World Aquaculture 28 1 (1997) 12-15
51. Food and Agriculture Organization of the United Nations (FAO). Fisheries Global Information System (2005). http://www.fao.org/figis http://www.fao.org/figis (accessed September 27, 2005)
52. Farrell A.P., Bennett W., and Devlin R.H. Growth-enhanced transgenic salmon can be inferior swimmers. Can. J. Zool. 75 (1997) 335-337
53. Fauconneau B., Mady M.P., and LeBail P.-Y. Effect of growth hormone on muscle protein synthesis in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Fish Physiol. Biochem. 15 (1996) 49-56
54. Fleming I.A., Hindar K., Mjølnerød I.B., Jonsson B., Balstad T., and Lamberg A. Lifetime success and interactions of farm salmon invading a native population. Proc. R. Soc. Lond. Ser. B 267 (2000) 1517-1523
55. Fleming I.A., Agustsson T., Finstad B., Johnsson J.I., and Björnsson B.Th. Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 59 (2002) 1323-1330
56. Fletcher G.L., Shears M.A., King M.J., Goddard S.V., Kao M.H., Du S.J., Davies P.L., and Hew C.L. Biotechnology for aquaculture: transgenic salmon with enhanced growth and freeze-resistance. Bull. Aquacult. Assoc. Can. 92 3 (1992) 31-33
57. Fletcher G.L., Davies P.L., and Hew C.L. Genetic engineering of freeze resistant Atlantic salmon. In: Hew C.L., and Fletcher G.L. (Eds). Transgenic Fish (1992), World Scientific Publishing, River Edge, NJ 190-208
58. Fletcher G.L., Shears M.A., Yaskowiak E.S., King M.J., and Goddard S.V. Gene transfer: potential to enhance the genome of Atlantic salmon for aquaculture. Aust. J. Exp. Agric. 44 (2004) 1095-1100
59. Foster A.R., Houlihan D.F., Gray C., Medale F., Fauconneau B., Kaushik S.J., and LeBail P.-Y. The effects of ovine growth hormone on protein turnover in rainbow trout. Gen. Comp. Endocrinol. 82 (1991) 111-120
60. 4 human growth hormone transgenic carp fed diets with different protein levels. J. Fish Biol. 53 (1998) 115-129
61. 4 human growth hormone transgenic red carp (Cyprinus carpio) fed with different protein levels. Aquaculture 189 (2000) 287-292
62. Gill J.A., Sumpter J.P., Donaldson E.M., Dye H.M., Souza L.M., Berg T., Wypych J., and Langley K. Recombinant chicken and bovine growth hormones accelerate growth in aquacultured juvenile Pacific salmon Oncorhynchus kisutch. BioTechnology 3 (1985) 643-646
63. Golovan S.P., Hayes M.A., Phillips J.P., and Forsberg C.W. Transgenic mice expressing bacterial phytase as a model for phosphorus pollution control. Nat. Biotechnol. 19 (2001) 429-433
64. Gross M.L., Schneder J.F., Moav N., Alvarez C., Myster S.H., Liu Z., Hew C., Hallerman E.M., Hackett P.B., Guise K.S., Faras A.J., and Kapuscinski A.R. Molecular analysis and growth evaluation of northern pike (Esox lucius) microinjected with growth hormone genes. Aquaculture 103 (1992) 253-273
65. Guillen I., Berlanga J., Valenzuela C.M., Morales A., Toledo J., Estrada M.P., Puentes P., Hayes O., and LaFuente J. Safety evaluation of transgenic tilapia with accelerated growth. Mar. Biotechnol. 1 (1999) 2-14
66. Guillen I., Estrada M.P., Morales R., Melamed P., and de la Fuente J. The interrelation of body growth with growth hormone, insulin-like growth factor and prolactin levels in juvenile tilapia (Oreochromis aureus). Miner. Biotechnol. 10 (1998) 1-10
67. Guillen I., Martinez O., Hernandez O., Estrada M.P., Pimentel R., Herrera F., Morales A., Rodriguez A., Sanchez V., Abad Z., Hidalgo Y., Lleonart R., Cruz A., Vasquez J., Sanchez T., Figueroa J., Krauskopf M., and de la Fuente J. In: Donaldson E.M., and Mackinlay D.D. (Eds). Aquaculture Biotechnology Symposium Proceedings on International Congress on The Biology of Fishes. San Francisco, CA, July 14-18, 1996 (1996) 63-72
68. Hallerman E.M., and Kapuscinski A.R. Ecological implications of using transgenic fishes in aquaculture. ICES Mar. Sci. Symp. 194 (1992) 56-66
69. Hernandez O., Guillen I., Estrada M.P., Cabrera E., Pimentel R., Pina J.C., Abad Z., Sanchez V., Hidalgo Y., Martinez R., Lleonart R., and de la Fuente J. Characterization of transgenic tilapia lines with different ectopic expression of tilapia growth hormone. Mar. Mol. Biol. Biotechnol. 6 (1997) 367-377
70. Hew C.L., Fletcher G.L., and Davies P.L. Transgenic salmon: tailoring the genome for food production. J. Fish Biol. 47 Suppl. A (1995) 1-19
71. Hew C.L., Poon R., Xiong F., Gauthier S., Shears M., King M., Davies P., and Fletcher G. Liver-specific and seasonal expression of transgenic Atlantic salmon harboring the winter flounder antifreeze protein gene. Transgenic Res. 8 (1999) 405-414
72. Hill J.A., Kiessling A., and Devlin R.H. Coho salmon (Oncorhynchus kisutch) transgenic for a growth hormone gene construct exhibit increased rates of muscle hyperplasia and detectable levels of differential gene expression. Can. J. Fish. Aquat. Sci. 57 (2000) 939-950
73. Hinits Y., and Moav B. Growth performance studies in transgenic Cyprinus carpio. Aquaculture 173 (1999) 285-296
74. Hoar W.S. The physiology of developing fish. In: Hoar W.S., and Randall D.J. (Eds). Fish Physiology vol. XIB (1988), Academic Press, London 275-343
75. Huang C.-H., Higgs D.A., Balfry S.K., and Devlin R.H. Effect of dietary Vitamin E level on growth, tissue lipid proliferation, and erythrocyte fragility of transgenic coho salmon, Oncorhynchus kisutch. Comp. Biochem. Physiol. A 139 (2004) 199-204
76. Jhingan E., Devlin R.H., and Iwama G.K. Disease resistance, stress response, and effects of triploidy in growth hormone transgenic coho salmon. J. Fish Biol. 63 (2003) 806-823
77. Johnsson J.I., and Bjornsson B.T. Growth hormone increases growth rate, appetite and dominance in juvenile rainbow trout, Oncorhynchus mykiss. Anim. Behav. 48 (1994) 177-186
78. Johnsson J.I., and Bjornsson B.T. Growth-enhanced fish can be competitive in the wild. Funct. Ecol. 15 (2001) 654-659
79. Johnsson J.I., Jonnson E., Petersson E., Jarvi T., and Bjornsson B.T. Fitness-related effects of growth investment in brown trout under field and hatchery conditions. J. Fish Biol. 57 (2000) 326-336
80. Johnsson J.I., Petersson E., Jonsson E., Bjornsson B.T., and Jarvi T. Domestication and growth hormone alter antipredator behavior and growth patterns in juvenile brown trout, Salmo trutta. Can. J. Fish. Aquat. Sci. 53 (1996) 1546-1554
81. Johnsson J.I., Petersson E., Jonsson E., and Bjornsson B.T. Growth hormone-induced effects on mortality, energy status, and growth: a field study on brown trout (Salmo trutta). Funct. Ecol. 13 (1999) 514-522
82. Jonsson E., Johnsson J.I., and Bjornsson B.T. Growth hormone increases predation exposure of rainbow trout. Proc. R. Soc. Lond. Ser. B 263 (1996) 647-651
83. Jonsson E., Johnsson J.I., and Bjornsson B.T. Growth hormone increases aggressive behavior in juvenile rainbow trout. Horm. Behav. 33 (1998) 9-15
84. Jonsson E., Johnsson J.I., and Bjornsson B.T. Growth hormone increases risk-taking in foraging rainbow trout. Trends Comp. Endocrinol. Neurobiol. 839 (1998) 636-638
85. Jonsson N., Jonsson B., and Fleming I.A. Does early growth cause a phenotypically plastic response in egg production of Atlantic salmon?. Funct. Ecol. 10 (1996) 89-96
86. Kajiura L.J., and Rollo C.D. A mass budget for transgenic "supermice" engineered with extra rat growth hormone genes: evidence for energetic limitation. Can. J. Zool. 72 (1994) 1010-1017
87. Kang D.Y., and Devlin R.H. Effects of 3,5,3′-triiodo-l-thryonine (T-3) and 6-n-propyl-2-thiouracil (PTU) on growth of GH-transgenic coho salmon, Oncorhynchus kisutch. Fish Physiol. Biochem. 29 (2003) 77-85
88. Kieffer T.J., Scieldrop P.J., McLean E., Donaldson E.M., and Brown J.C. A radioimmunoassay for onchorynchid growth hormone targeted at the physiological range. Can. J. Physiol. Pharmacol. 72 (1994) 1155-1161
89. Kiron V., Puangkaew J., Ishizaka K., Satoh S., and Watanabe T. Antioxidant status and nonspecific immune responses in rainbow trout (Oncorhynchus mykiss) fed two levels of Vitamin E along with three lipid sources. Aquaculture 234 (2004) 361-379
90. Kiron V., Watanabe T., Kukuda H., Okamoto N., and Takeuchi T. Protein nutrition and defence mechanisms in rainbow trout Oncorhynchus mykiss. Comp. Biochem. Physiol. 111A (1995) 351-359
91. Komourdijian M.P., Saunders R.L., and Fenwick J.C. The effect of porcine somatotropin on growth and survival in seawater of Atlantic salmon (Salmo salar) parr. Can. J. Zool. 54 (1976) 531-535
92. Kotrschal K., van Staaden M.J., and Huber R. Fish brains: evolution and environmental relationships. Rev. Fish Biol. Fish. 8 (1998) 373-408
93. Krasnov A., Pitkanen T.I., and Molsa H. Gene transfer for targeted modification of salmonid fish metabolism. Genet. Anal. 15 (1999) 115-119
94. Leatherland J.F., and Nuti R.A. Effect of bovine growth hormone on plasma free fatty acid concentration and liver, muscle and carcass lipid content in rainbow trout (Salmo gairdneri Richardson). J. Fish Biol. 19 (1981) 487-498
95. Lee C.G., Devlin R.H., and Farrell A.P. Swimming performance, oxygen consumption, and excess post-exercise oxygen consumption in adult transgenic and ocean-ranched coho salmon. J. Fish Biol. 62 (2003) 753-766
96. Le Gac F., Blaise O., Fostier A., and Le Bail P.-Y. Growth hormone (GH) and reproduction: a review. Fish Physiol. Biochem. 11 (1993) 219-232
97. Le Gac F., Ollitrault M., Loir M., and LeBail P.-Y. Evidence for binding and action of growth hormone in trout testis. Biol. Reprod. 46 (1992) 949-957
98. Leggatt R.A., Devlin R.H., Farrell A.P., and Randall D.J. Oxygen uptake of growth hormone transgenic coho salmon during starvation and feeding. J. Fish Biol. (2003) 1053-1066
99. Lemieux H., Blier P., and Dutil J.-D. Do digestive enzymes set a physiological limit upon growth rate and conversion efficiency in Atlantic cod (Gadus morhua)?. Bull. Aquac. Soc. Can. 97 (1997) 54-56
100. MacLatchy D.L., Kawauchi H., and Eales J.G. Stimulation of hepatic thyroxine 5′-deiodinase activity in rainbow trout (Oncorhynchus mykiss) by Pacific salmon growth hormone. Comp. Biochem. Physiol. 101A (1992) 689-691
101. Maclean, Penman D., and Talwar S. Introduction of novel genes into the rainbow trout. Proceedings of the World Symposium on Selection, Hybridization Genetic Engineering in Aquaculture. Bordeaux, France, May 27-30, 1986 (1987) 325-333
102. Maclean N., Rahman M.A., Sohm F., Hwang G., Iyengar A., Ayad H., Smith A., and Farahmand H. Transgenic tilapia and the tilapia genome. Gene 295 (2002) 265-277
103. Madsden S.S. Enhanced hypoosmoregulatory response to growth hormone after cortisol treatment in immature rainbow trout. Fish Physiol. Biochem. 8 (1990) 271-281
104. Mao W., Wang Y., Wang W., Wu B., Feng J., and Zhu Z. Enhanced resistance to Aeromonas hydrophila infection and enhanced phagocytic activities in human lactoferrin-transgenic grass carp (Ctenopharyngodon idellus). Aquaculture 242 (2004) 93-103
105. 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., and de la Fuente J. Growth enhancement in transgenic tilapia by ectopic expression of tilapia growth hormone. Mol. Mar. Biol. Biotechnol. 5 (1996) 62-70
106. Martinez R., Arenal A., Estrada M.P., Herrera F., Huerta V., Vasquez J., Sanchez T., and de la Fuente J. Mendelian transmission, transgene dosage, and growth phenotype in transgenic tilapia (Oreochromis hornorum) showing ectopic expression of homologous growth hormone. Aquaculture 173 (1999) 271-283
107. Martinez R., Juncal J., Zaldivar C., Arenal A., Guillen I., Morera V., Carillo O., Estrada M., Morales A., and Estrada M.P. Growth efficiency in transgenic tilapia (Oreochromis sp.) carrying a single copy of a homologous cDNA growth hormone. Biochem. Biophys. Res. Commun. 267 (2000) 466-472
108. McCormick S.D., Sakamoto T., Hasegawa S., and Hirano T. Osmoregulatory actions of insulin-like growth factor-I in rainbow trout (Oncorhynchus mykiss). J. Endocrinol. 130 (1991) 87-92
109. McKenzie D.J., Martinez R., Morales A., Acosta J., Morales R., Taylor E.W., Steffensen J.F., and Estrada M.P. Effects of growth hormone transgenesis on metabolic rates, exercise performance, and hypoxia tolerance in tilapia hybrids. J. Fish Biol. 63 (2003) 398-409
110. McLean E., and Devlin R.H. Application of biotechnology to enhance growth of salmonids and other fish. In: Fingerman M., and Nagabhushanam R. (Eds). Recent Advances in Marine Biotechnology, vol. 4: Aquaculture. Part B. Fishes (2000), Science Publishers, Enfield, NH 17-55
111. McLean E., Donaldson E.M., Mayer I., Teskeredzic E., Teskeredzic Z., Pitt C.G., and Souza L.M. Evaluation of a sustained-release polymer encapsulated form of recombinant porcine somatotropin upon long-term growth performance of coho salmon Oncorhynchus kisutch. Aquaculture 122 (1994) 359-368
112. McLean E., Devlin R.H., Byatt J.C., Clarke W.C., and Donaldson E.M. Impact of a controlled release formulation of recombinant growth hormone upon growth and seawater adaptation in coho (Oncorhynchus kisutch) and chinook (Oncorhynchus tshawytscha) salmon. Aquaculture 156 (1997) 113-128
113. McLean E., and Donaldson E.M. The role of growth hormone in the growth of poikilotherms. In: Schreibman M.P., Scanes C.G., and Pang P.K.T. (Eds). The Endocrinology of Growth, Development, and Metabolism in Vertebrates (1993), Academic Press, New York 43-71
114. Mench J.A. Ethics, animal welfare and transgenic farm animals. In: Murray J.D., Anderson G.B., Oberbauer A.M., and McGloghlin M.M. (Eds). Transgenic Animals in Agriculture (1999), CABI International, Wallingford, UK 25-268
115. Moav B., Liu Z., Moav N.L., Gross M.L., Kapuscinski A.R., Faras A.J., Guise K., and Hackett P.B. Expression of heterologous genes in transgenic fish. In: Hew C.L., and Fletcher G.L. (Eds). Transgenic Fish (1992), World Scientific, Singapore 120-141
116. Montero D., Socorro J., Tort L., Caballero M.J., Robaina L., Vergara J.M., and Izquierdo M.S. Glomerulonephritis and immunosuppression associated with dietary essential fatty acid deficiency in gilthead sea bream, Sparus aurata L., juveniles. J. Fish Dis. 27 (2004) 297-306
117. Moore C.J., and Mepham T.B. Transgenesis and animal welfare. Altern. Lab. Anim. 23 (1995) 380-397
118. Mori T., and Devlin R.H. Transgene and host growth hormone gene expression in pituitary and nonpituitary tissues of normal and growth hormone transgenic salmon. Mol. Cell. Endocrinol. 149 (1999) 129-139
119. Moyle P.B., and Cech J.J. Fishes: An Introduction to Ichthyology. 5th ed. (2004), Prentice-Hall, Saddle River, NJ
120. Mozdziak P.E., Pophal S., Borwornpinyo S., and Pettite J.N. Transgenic chickens expressing β-galactocidase hydrolyze lactose in the intestine. J. Nutr. 133 (2003) 3076-3079
121. Munro A.D., and Dodd J.M. Forebrain of fishes: neuroendocrine control mechanisms. In: Nistico G., and Bolis L. (Eds). Progress in Nonmammalian Brain Research vol. III (1983), CRC Press, Boca Raton, FL 2-78
122. Nam Y.K., Cho Y.S., Cho H., and Kim D.S. Accelerated growth performance and stable germ-line transmission in androgenetically derived homozygous transgenic mud loach, Misgurnus mizolepis. Aquaculture 209 (2002) 257-270
123. Nam Y.K., Noh J.K., Cho Y.S., Cho H.J., Cho K.-N., Kim C.G., and Kim D.S. Dramatically accelerated growth and extraordinary gigantism of transgenic mud loach Misgurnus mizolepis. Transgenic Res. 10 (2001) 353-362
124. National Research Council (NRC). Animal Biotechnology: Scientific Concerns (2002), National Academy Press, Washington, DC
125. O'Connor P.K., Reich B., and Sheridan M.A. Growth hormone stimulates hepatic lipid mobilization in rainbow trout, Oncorhynchus mykiss. J. Comp. Physiol. 163B (1993) 427-431
126. Ortuno J., Esteban M.A., and Meseguer J. The effect of dietary intake of Vitamins C and E on the stress response of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol. 14 (2003) 145-156
127. Ostenfeld T., McLean E., and Devlin R.H. Transgenesis changes body and head shape of Pacific salmon. J. Fish Biol. 52 (1998) 850-854
128. Palmiter R.D., Brinster R.L., Hammer R.E., Trumbauer M.E., Rosenfeld M.G., Birnberg N.C., and Evans R.M. Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion gene. Nature 300 (1982) 611-615
129. Pew Initiative on Food and Biotechnology, 2003. Future fish: issues in science and regulation of transgenic fish. Pew initiative on food and biotechnology, Washington, DC, http://www.pewagbiotech.org.
130. Pitkanen T.I., Krasnov A., Teerijoki H., and Molsa H. Transfer of growth hormone (GH) genes into Arctic charr (Salvelinus alpinus L.). I. Growth response to various GH constructs. Genet. Anal.: Biomol. Eng. 15 (1999) 91-98
131. Prunet P., Pisam M., Claireaux J.P., Boeuf G., and Rambourg A. Effects of growth hormone on gill chloride cells in juvenile Atlantic salmon (Salmo salar). Am. J. Physiol. 266 (1994) R850-R857
132. Purcell V.G., Rexroad C.E., Bolt J., Miller K.F., Wall R.J., Hammer R.E., Pinkert K.A., Palmiter R.D., and Brinster R.L. Progress on gene transfer in farm animals. Vet. Immunol. Immunopathol. 17 (1987) 303-312
133. Rahman M.A., and Maclean N. Growth performance of transgenic tilapia containing an exogenous piscine growth hormone gene. Aqaculture 173 (1999) 333-346
134. Rahman M.A., Mak R., Ayad H., Smith A., and Maclean N. Expression of a novel piscine growth hormone gene results in growth enhancement in transgenic tilapia (Oreochromis niloticus). Transgenic Res. 7 (1998) 357-369
135. Rahman M.A., Ronyai A., Engidaw B.Z., Jauncey K., Hwang G.-L., Smith A., Roderick E., Penman D., Varadi L., and Maclean N. Growth and nutritional trials on transgenic Nile tilapia containing an exogenous fish growth hormone gene. J. Fish Biol. 59 (2001) 62-78
136. Ramirez-Yanez G.O., Smid J.R., Young W.G., and Waters M.J. Influence of growth hormone on the craniofacial complex of transgenic mice. Eur. J. Orthod. 27 (2005) 494-500
137. Roberts S.B., McCauley L.A.R., Devlin R.H., and Goetz F.W. Transgenic salmon overexpressing growth hormone exhibit decreased myostatin transcript and protein expression. J. Exp. Biol. 207 (2004) 3741-3748
138. Rokkones E., Alestrom P., Skjervold H., and Gautvik K.M. Microinjection and expression of a mouse metallothionein human growth hormone fusion gene in fertilized salmonid eggs. J. Comp. Physiol. B 158 (1989) 751-758
139. Rollin B.E. The Frankenstein Syndrome: Ethical and Social Issues in the Genetic Engineering of Animals (1995), Cambridge University Press, Cambridge, UK
140. Rollo C.D., Foss J., Lachmansingh E., and Singh R. Behavioral rhythmicity in transgenic growth hormone mice: trade-offs, energetics, and sleep-wake cycles. Can. J. Zool. 75 (1997) 1020-1034
141. Sarangi N., Mandall A.B., Bandyopadhyay A.K., Venugopal T., Mathavan S., and Pandian T.J. Electroporated sperm-mediated gene transfer in Indian major carps. Asia-Pacific J. Mol. Biol. Biotechnol. 7 (1999) 151-158
142. Saunders R.L., Fletcher G.L., and Hew C.L. Smolt development in growth hormone transgenic Atlantic salmon. Aquaculture 168 (1998) 177-193
143. Sedikki H., Boeuf G., Maxime V., and Peyraud C. Effects of growth hormone treatment on oxygen composition and seawater adaptability in Atlantic salmon parr and pre-smolts. Aquaculture 148 (1996) 49-62
144. Sheela S.G., Pandian T.J., and Mathavan S. Electroporatic transfer, stable integration, and transmission of pZp beta ypGH and pZp beta rtGH in Indian catfish, Heteropneustes fossilis (Bloch). Aquac. Res. 30 (1999) 233-248
145. Shamblott M.J., Cheng C.M., Bolt D., and Chen T.T. Appearance of insulin-like growth factor mRNA in liver and pyloric ceca of a teleost in response to exogenous growth hormone. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 6943-6946
146. Shrimpton J.M., Devlin R.H., McLean E., Byatt J.C., Donaldson E.M., and Randall D.J. Increased gill corticosteroid receptor concentration and seawater tolerance in juvenile coho salmon (Oncorhynchus kisutch) treated with growth hormone and placental lactogen. Gen. Comp. Endocrinol. 98 (1995) 1-15
147. Smith D.C.W. The role of the endocrine organs in the salinity tolerance of trout. Mem. Soc. Endocrinol. 5 (1956) 83-101
148. Sneddon L.U. The evidence for pain in fish: the use of morphine as an analgesic. Appl. Anim. Behav. Sci. 83 (2003) 153-162
149. Stevens E.D., and Devlin R.H. Intestinal morphology in growth hormone transgenic coho salmon. J. Fish Biol. 56 (2000) 191-195
150. Stevens E.D., and Devlin R.H. Gill morphometry in growth hormone transgenic coho salmon, Oncorhychus kisutch, differs markedly for that in GH transgenic Atlantic salmon. J. Fish Biol. 58 (2000) 113-117
151. Stevens E.D., and Devlin R.H. Gut size in GH-transgenic coho salmon is enhanced by both the GH transgene and increased food intake. J. Fish Biol. 66 (2005) 1633-1648
152. Stevens E.D., and Sutterlin A. Gill morphology in growth hormone transgenic salmon. Environ. Biol. Fish. 54 (1999) 411-415
153. Stevens E.D., Sutterlin A., and Cook T. Respiratory metabolism and swimming performance in growth hormone transgenic Atlantic salmon. Can. J. Fish. Aquat. Sci. 55 (1998) 2028-2035
154. Stevens E.D., Wagner G.N., and Sutterlin A. Gut morphology of GH transgenic salmon. J. Fish Biol. 55 (1999) 517-526
155. Sun, L., 1990. Effect of bovine growth hormone on fish growth and intestinal amino acid transport. Ph.D. Dissertation. Rutgers, the State University of New Jersey, New Brunswick, NJ.
156. Sundstrom L.F., Devlin R.H., Johnsson J.I., and Biagi C.A. Vertical position reflects increased feeding motivation in growth hormone transgenic coho salmon (Oncorhynchus kisutch). Ethology 109 (2003) 701-712
157. Sundstrom L.F., Lohmus M., Devlin R.H., Johnsson J.I., Biagi C.A., and Bohlin T. Feeding on profitable and unprofitable prey: comparing behavior of growth enhanced transgenic and normal coho salmon (Oncorhynchus kisutch). Ethology 110 (2004) 381-396
158. Sundstrom L.F., Lohmus M., Johnsson J.I., and Devlin R.H. Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 271 (2004) S350-S352
159. Takagi Y., Moriyama S., Hirano T., and Yamada J. Effects of growth hormones on bone formation and resorption in rainbow trout (Oncorhynchus mykiss), as examined by histomorphometry or the pharyngeal bone. Gen. Comp. Endocrinol. 86 (1992) 90-95
160. Tymchuk W.E.V., Abrahams M.V., and Devlin R.H. Competitive ability and mortality of growth-enhanced transgenic coho salmon fry and parr when foraging for food. Trans. Am. Fish. Soc. 134 (2005) 381-389
161. Uzbekova S., Chyb J., Ferrierre F., Bailhache T., Prunet P., Alestrom P., and Breton B. Transgenic rainbow trout expressed sGnRH-antisense RNA under the control of sGnRH promoter of Atlantic salmon. J. Mol. Endocrinol. 25 (2000) 337-350
162. Van Reenen C.G., Meuwissen T.H.E., Hopster H., Oldenbroek K., Kruip T.A.M., and Blokhuis H.J. Transgenesis may affect farm animal welfare: a case for systematic risk assessment. J. Anim. Sci. 79 (2001) 1763-1779
163. Venugopal T., Anathy V., Kirankumar S., and Pandian T.J. Growth enhancement and food conversion efficiency of transgenic fish, Labeo rohita. J. Exp. Biol. 301A (2004) 477-490
164. Wang R., Zhang P., Gong Z., and Hew C.L. Expression of the antifreeze protein gene in transgenic goldfish (Carassius auratus) and its implication in cold adaptation. Mol. Mar. Biol. Biotechnol. 4 (1995) 20-26
165. 1 generation. Chin. Sci. Bull. 46 (2001) 1174-1177
166. Ward A.C., and Lieschke G.J. The zebrafish as a model system for human disease. Front. Biosci. 7 (2002) 827-833
167. Wei Y., Xie Y., Xu K., Li G., Liu D., Zhou J., Li J., and Zhu Z. Heredity of human growth hormone gene in transgenic carp (Cyprinus carpio L.). Chin. J. Biotechnol. 8 (1992) 140-144
168. Winn R.N., Norris M.B., Brayer K.J., Torres C., and Muller S.L. Detections of mutations in transgenic fish carrying a bacteriophage λ cII transgene target. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 12655-12660
169. Wolf E., Kahnt E., Ehrlein J., Hermanns W., Brem G., and Wanke R. Effects of long-term elevated serum levels of growth-hormone on life expectancy of mice-lessons from transgenic animal-models. Mech. Ageing Dev. 68 (1993) 71-87
170. Wu G., Sun Y., and Zhu Z. Growth hormone gene transfer in common carp. Aquat. Living Resour. 16 (2003) 416-420
171. Zbikowska H.M. Fish can be first-advances in fish transgenesis for commercial applications. Transgenic Res. 12 (2003) 379-389
172. Zeng Z., Hu W., Wang Y., Zhu Z., Zhou G., Liu S., Zhang X., Luo C., and Liu Y. The genetic improvement of tetraploid fish by pCAgcGHc-transgenics. High Technol. Lett. 7 (2001) 6-12
173. Zhang F., Wang Y., Hu W., Cui Z., and Zhu Z. Physiological and pathological analysis of the mice fed with "all-fish" gene transferred Yellow River carp. High Technol. Lett. 7 (2000) 17-19
174. Zhang J.X., Meidinger R., Forsberg C.W., Krell P.J., and Phillips J.P. Expression and processing of a bacterial endonuclease in transgenic mice. Arch. Biochem. Biophys. 367 (1999) 317-321
175. Zhang P.J., Hayat M., Joyce C., Gonzalez-Villasenor L.I., Lin C.M., et al. Gene transfer, expression and inheritance of pRSV-rainbow trout-GH cDNA in the common carp Cyprinus carpio (Linnaeus). Mol. Reprod. Dev. 25 (1990) 3-13
176. Zhong J., Wang Y., and Zhu Z. Introduction of the human lactoferrin gene into grass carp (Ctenopharyngodon idellus) to increase resistance against GCH virus. Aquaculture 214 (2002) 93-101
177. Zhu Z. Generation of fast-growing transgenic fish: methods and mechanisms. In: Hew C.L., and Fletcher G.L. (Eds). Transgenic Fish (1992), World Publishing, Singapore 92-119
178. Zhu Z. Collection of the Technical Materials of the National 863 High-tech Project of China, "Middle-scale Trial of Fast-growing Transgenic Common Carp" (2000), Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China
179. Zhu Z., Li G., He L., and Chen S. Novel gene transfer into the fertilized eggs of goldfish (Carassius auratus L. 1758). Z. Angew. Ichthyol. 1 (1985) 31-34
180. Zhu Z., Xu K., Xie Y., Li G., and He L. A model of transgenic fish. Sci. Sin. B 2 (1989) 147-155
181. Zou J.J., Trudeau V.L., Cui Z., Brechin J., McKenzie K., Zhu Z., Houlihan D.F., and Peter R.E. Estradiol stimulates growth hormone production in female goldfish. Gen. Comp. Endocrinol. 106 (1997) 102-112