Assessment of paternal effect and physiological cost of metamorphosis on growth of young winter flounder Pseudopleuronectes americanus juveniles in a cold environment

Journal of Fish Biology

Volumn 76, Issue 4, 2010, Pages 930-948

  Fraboulet, E ^a   Lambert, Y ^b   Tremblay, R ^a   Audet, C ^a  

^a INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

^b MAURICE LAMONTAGNE INSTITUTE   (Canada)

Author keywords

Energy allocation; Ontogeny; Settlement; Triacylglycerol

Indexed keywords

PLEURONECTOIDEI; PSEUDOPLEURONECTES AMERICANUS;

EID: 77951654975     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2010.02538.x     Document Type: Article

References (95)

1. Amara R, Galois R. Nutritional condition of metamorphosing sole: spatial and temporal analyses. Journal of Fish Biology 2004, 64:72-88. 10.1111/j.1095-8649.2004.00284.x
2. Amara R, Meziane T, Gilliers C, Hermel G, Laffargue P. Growth and condition indices in juvenile sole Solea solea measured to assess the quality of essential fish habitat. Marine Ecology Progress Series 2007, 351:201-208.
3. Bang A, Grønkjær P, Clemmesen C, Høie H. Parental effects on early life history traits of Atlantic herring (Clupea harengus L.) larvae. Journal of Experimental Marine Biology and Ecology 2006, 334:51-63.
4. Bell J G, Tocher D R, MacDonald F M, Sargent J R. Effect of diet rich in linoleic (18:2n-6) and α-linolenic (18:3n-3) acids on the growth, lipid class and fatty acid composition and eicosanoid production in juvenile turbot (Scophthalmus maximus L.). Fish Physiology and Biochemistry 1994, 13:105-118.
5. Ben Khemis I, de la Noüe J, Audet C. Feeding larvae of winter flounder Pseudopleuronectes americanus (Walbaum) with live prey or microencapsulated diet: linear growth and protein, RNA and DNA content. Aquaculture Research 2000, 31:377-386.
6. Benoît H P, Pepin P, Brown J A. Patterns of metamorphic age and length in marine fishes, from individual to taxa. Canadian Journal of Fisheries and Aquatic Sciences 2000, 57:856-869.
7. Bertram D F, Chambers R C, Leggett W C. Negative correlations between larval and juvenile growth rates in winter flounder: implications of compensatory growth for variation in size-at-age. Marine Ecology Progress Series 1993, 96:209-215.
8. Bertram D F, Miller J M, Leggett W C. Individual variation in growth and development during the early life of winter flounder, Pleuronectes americanus. Fisheries Bulletin 1997, 95:1-10.
9. Blanc J M. Comparison of experimental designs for estimating quantitative genetic parameters in fish. Aquaculture Research 2003a, 34:1099-1105.
10. Blanc J M. Paternal variation in juvenile survival and growth of the triploid hybrid between female rainbow trout (Oncorhynchus mykiss Walbaum) and the male brown trout (Salmo trutta L.). Aquaculture Research 2003b, 34:205-210.
11. Bolker J A, Hill C R. Pigmentation development in hatchery-reared flatfishes. Journal of Fish Biology 2000, 56:1029-1052. 1010.1006/jfbi.2000.1260
12. Buckley L J. Relationship between RNA-DNA ratio, prey density and growth rate in Atlantic cod (Gadus morhua) larvae. Journal of the Fisheries Research Board of Canada 1979, 36:1497-1502.
13. Buckley L J. RNA-DNA ratio: an index of larval fish growth in the sea. Marine Biology 1984, 80:291-298.
14. Buckley L J. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (North Atlantic). 1989, Winter flounder., ,
15. Buckley L J, Caldarone E M, Ong T L. RNA-DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia 1999, 401:265-277.
16. Butts I A E, Litvak M K. Parental and stock effects on larval growth and survival to metamorphosis in winter flounder (Pseudopleuronectes americanus). Aquaculture 2007a, 269:339-348.
17. Butts I A E, Litvak M K. Stock and parental effects on embryonic and early larval development of winter flounder Pseudopleuronectes americanus (Walbaum). Journal of Fish Biology 2007b, 70:1070-1087. 1010.1111/j.1095-8649.2007.01369.x
18. Chambers R C, Leggett W C. Size and age at metamorphosis in marine fishes: an analysis of laboratory-reared winter flounder (Pseudopleuronectes americanus) with a review of variation in other species. Canadian Journal of Fisheries and Aquatic Sciences 1987, 44:1936-1947.
19. Chambers R C, Leggett W C. Possible causes and consequences of variation in age and size at metamorphosis in flatfishes (pleuronectiformes): an analysis at the individual, population, and species levels. Netherlands Journal of Sea Research 1992, 29:7-24.
20. Chambers R C, Leggett W C, Brown J A. Variation in and among early life history traits of laboratory-reared winter flounder Pseudopleuronectes americanus. Marine Ecology Progress Series 1988, 47:1-15.
21. Clemmesen C. The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration. Marine Biology 1994, 118:377-382.
22. Clynick B G, McKindsey C W, Archambault P. Distribution and productivity of fish and macroinvertebrates in mussel aquaculture sites in the Magdalen islands (Québec, Canada). Aquaculture 2008, 283:203-210.
23. Conover D O. Local adaptation in marine fishes: evidence and implication for stock enhancement. Bulletin of Marine Science 1998, 62:477-493.
24. Duman J G, Devries A L. Freezing resistance in winter flounder Pseudopleuronectes americanus. Nature 1974, 247:237-238.
25. Dwyer K S, Parrish C C, Brown J A. Lipid composition of yellowtail flounder (Limanda ferruginea) in relation to dietary lipid intake. Marine Biology 2003, 143:659-667.
26. Evans J P, Geffen A J. Male characteristics, sperm traits, and reproductive success in winter-spawning Celtic Sea Atlantic herring, Clupea harengus. Marine Biology 1998, 132:179-186.
27. Falconer D S, Mackay T F C. Introduction to Quantitative Genetics 1996, Harlow, Pearson Education Limited
28. Ferron A, Leggett W C. An appraisal of condition measures for marine fish larvae. Advances in Marine Biology 1994, 30:217-303.
29. Folch J, Lees M, Sloane Stanley G H. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 1957, 226:497-509.
30. Fraboulet E, Lambert Y, Litvak M K, Audet C. The effects of latitudinal origin and paternal contribution on larval growth of winter flounder in a northern environment. Transactions of the American Fisheries Society 2009, 138:407-415.
31. Fraser A J. Triacylglycerol content as a condition index for fish, bivalve, and crustacean larvae. Canadian Journal of Fisheries and Aquatic Sciences 1989, 46:1868.
32. Fukuda M, Sako H, Shigeta T, Shibata R. Relationship between growth and biochemical indices in laboratory-reared juvenile Japanese flounder (Paralichthys olivaceus), and its application to wild fish. Marine Biology 2001, 138:47-55.
33. Galois R, Lagardere F, Richard P. Changes in biochemical composition and otolith microstructure of larval common sole, Solea solea (L.) under experimental starvation. La Mer 1990, 28:273-285.
34. Garant D, Dodson J J, Bernatchez L. Differential reproductive sucess and heritability of alternative reproductive tactics in wild Atlantic salmon (Salmo salar L.). Evolution 2003, 57:1133-1141.
35. Geffen A J, Van der veer H W, Nash R D M. The cost of metamorphosis in flatfishes. Journal of Sea Research 2007, 58:35-45.
36. Gilliers C, Amara R, Bergeron J P, Le Pape O. Comparison of growth and condition indices of juvenile flatfish in different coastal nursery grounds. Environmental Biology of Fishes 2004, 71:189-198.
37. Gorshkov I, Meiri H, Rosenfeld S, Ben-Atia S, Lutzki A, Peduel B, Ron G, Gorshkova A, Skvortzov A, Tandler A. Parental effects on sex ratios in progeny of the European sea bass (Dicentrarchus labrax). Israeli Journal of Aquaculture-Bamidgeh 2003, 55:265-273.
38. Green B S, McCormick M I. Maternal and paternal effects determine size, growth and performance in larvae of a tropical reef fish. Marine Ecology Progress Series 2005, 289:263-272.
39. Gwak W S, Tanaka M. Developmental change in RNA:DNA ratios of fed and starved laboratory-reared Japanese flounder larvae and juveniles, and its application to assessment of nutritional condition for wild fish. Journal of Fish Biology 2001, 59:902-915. 910.1006/jfbi.2001.1703
40. Gwak W S, Tsusaki T, Tanaka M. Nutritional condition, as evaluated by RNA/ DNA ratios, of hatchery-reared Japanese flounder from hatch to release. Aquaculture 2003, 219:503-514.
41. Håkanson J L. Analysis of lipid components for determining the condition of anchovy larvae, Engraulis mordax. Marine Biology 1989, 102:143-151.
42. Hartree E F. Determination of protein: a modification of the Lowry method that gives a linear photometric response. Analytical Biochemistry 1972, 48:422-427.
43. Hebert K P, Goddard P L, Smoker W W, Gharrett A J. Quantitative genetic variation and genotype by environment interaction of embryo development rate in pink salmon (Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Sciences 1998, 55:2048-2057.
44. Herbinger C M, Doyle R W, Pitman E R, Paquet D, Mesa K A, Morris D B, Wright J M, Cook D. DNA fingerprint based analysis of paternal and maternal effects on offspring growth and survival in communally reared rainbow trout. Aquaculture 1995, 137:245-256.
45. Hoie H, Folkvord A, Johannessen A. The influence of different parental combinations and incubation temperature on the RNA and DNA content of herring larvae at hatching: a pilot study. Journal of Fish Biology 1999, 55:110-118. 110.1006/jfbi.1999.1055
46. Kamler E. Parent-egg-progeny relationship in teleost fishes: an energetics perspective. Reviews in Fish Biology and Fisheries 2005, 15:399-421.
47. Lister J S, Neff B D. Paternal genetic effects on foraging decision-making under the risk of predation. Ethology 2006, 112:963-970.
48. Malloy K D, Targett T E. Effects of ration limitation and low temperature on growth, biochemical condition, and survival of juvenile summer flounder from two Atlantic coast nurseries. Transactions of the American Fisheries Society 1994, 123:182-193.
49. McCraken F D. Seasonal movements of the winter flounder, Pseudopleuronectes americanus (Walbaum), on the Atlantic coast. Journal of the Fisheries Research Board of Canada 1963, 20:551-586.
50. Mercier L, Audet C, de la Noüe J, Parent B, Parrish C C, Ross N W. First feeding of winter flounder (Pseudopleuronectes americanus) larvae: use of Brachionus plicatilis acclimated at low temperature as live prey. Aquaculture 2004, 229:361-376.
51. Mommsen T P. Paradigm of growth in fish. Comparative Biochemistry and Physiology 2001, 129:207-219.
52. de Montgolfier B, Audet C, Lambert Y. Growth of early juvenile winter flounder (Pseudopleuronectes americanus Walbaum). Aquaculture Research 2005, 36:1595-1601.
53. Munro H N, Fleck A. The determination of nucleic acids. Methods of Biochemical Analysis 1966, 113-116. Glick D, In, ed.), pp., New York, NY, Interscience
54. Neff B D. Increased performance of offspring sired by parasitic males in bluegill sunfish. Behavioral Ecology 2004, 15:327-331.
55. Neff B D, Lister J S. Genetic life history effects on juvenile survival in bluegill. Journal of Evolutionary Biology 2007, 20:517-525.
56. Ojaveer E. On the external and parental effects in early development of herring (Clupea pallasi) at the NE Kamchatka. Fisheries Research 2006, 81:1-8.
57. Osse J W M, Van den Boogaart J G M. Size of flatfish larvae at transformation, functional demands and historical constraints. Journal of Sea Research 1997, 37:229-239.
58. Panagiotaki P, Geffen A J. Parental effects on size variation in fish larvae. Journal of Fish Biology 1992, 41:37-42. 10.1111/j.1095-8649.1992.tb03866.x
59. Parrish C C. Separation of aquatic lipid classes by chromarod thin-layer chromatography with measurement by iatroscan flame ionization detection. Canadian Journal of Fisheries and Aquatic Sciences 1987, 44:722-731.
60. Parrish C C. Determination of total lipid, lipid classes, and fatty acids in aquatic samples. Lipids in Freshwater Ecosystems 1999, 4-20. Arts M TWainman B C. In, eds), pp., New York, NY, Springer-Verlag
61. Parrish C C, Wells J S, Yang Z, Dabinett P. Growth and lipid composition of scallop juveniles, Placopecten magellanicus, fed the flagellate Isochrysis galbana with varying lipid composition and the diatom Chaetoceros muelleri. Marine Biology 1998, 133:461-471.
62. Pearcy W G. Seasonal changes in osmotic pressure of flounder sera. Science 1961, 134:193-194.
63. Pereira J J, Goldberg R, Ziskowski J J, Berrien P L, Morse W W, Johnson D L. Essential fish habitat source document: winter flounder, Pseudopleuronectes americanus, life history and habitat characteristics. 1999
64. Perry G M L, Audet C, Laplatte B, Bernatchez L. Shifting pattern in genetic control at the embryo-alevin boundary in brook charr. Evolution 2004, 58:2002-2012.
65. Petersson E, Jarvi T. Characteristics of brown trout males influence growth and survival of their offspring. Journal of Fish Biology 2007, 71:493-509. 410.1111/j.1095-8649.2007.01501.x
66. Plante S, Audet C, Lambert Y, de la Noüe J. Comparison of stress responses in wild and captive winter flounder (Pseudopleuronectes americanus Walbaum) broodstock. Aquaculture Research 2003, 34:803-812.
67. Probst W N, Kraus G, Rideout R M, Trippel E A. Parental effects on early life history traits of haddock Melanogrammus aeglefinus. ICES Journal of Marine Science 2006, 63:224-234.
68. Quinn G P, Keough M J. Experimental Design and Data Analysis for Biologists 2002, Cambridge, Cambridge University Press
69. Reynolds J D, Gross M R. Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata. Philosophical Transactions of the Royal Society B 1992, 250:57-62.
70. Richard P, Bergeron J P, Boulhic M, Galois R, Person-Le Ruyet J. Effect of starvation on RNA, DNA and protein content of laboratory-reared larvae and juveniles of Solea solea. Marine Ecology Progress Series 1991, 72:69-77.
71. Rideout R M, Trippel E A, Litvak M K. Paternal effect on haddock early life history traits. Journal of Fish Biology 2004, 64:695-701. 610.1046/j.1095-8649.2003. 00335.x
72. Rinchard J, Lee K J, Czesny S, Ciereszko A, Dabrowski K. Effect of feeding cottonseed meal-containing diets to broodstock rainbow trout and their impact on the growth of their progenies. Aquaculture 2003, 227:77-87.
73. Rose K A, Jeffrey A T, Chambers R C, Klein-MacPhee G, Danila D J. Simulating winter flounder population dynamics using coupled individual-based young-of-the-year and age-structured adult models. Canadian Journal of Fisheries and Aquatic Sciences 1996, 53:1071-1091.
74. Sabatés A, Rossi S, Reyes E. Lipid content in the early life stages of three mesopelagic fishes. Journal of Fish Biology 2003, 63:881-891. 810.1046/j.1095-8649.2003.00196.x
75. Saillant E, Chatain B, Fostier A, Przybyla C, Fauvel C. Parental influence on early development in the European sea bass. Journal of Fish Biology 2001, 58:1585-1600. 1510.1006/jfbi.2001.1564
76. Saillant E, Ma L, Wang X, Gatlin D M, Gold J R. Heritability of juvenile growth traits in red drum (Sciaenops ocellatus L.). Aquaculture Research 2007, 38:781-788.
77. Sargent J R, McEvoy L, Estevez A, Bell G, Bell M, Henderson J, Tocher D. Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 1999, 179:217-229.
78. Schreiber A M. Metamorphosis and early larval development of the flatfishes (Pleuronectiformes): an osmoregulatory perspective. Comparative Biochemistry and Physiology B 2001, 129:587-595.
79. Seikai T, Tanangowan J B, Tanaka M. Temperature influence on larval growth and metamorphosis of the Japanese flounder Paralichthys olivaceus in the laboratory. Bulletin of the Japanese Society of Scientific Fisheries 1986, 52:977-982.
80. Sogard S M. Size-selective mortality in the juvenile stage of teleost fishes: a review. Bulletin of Marine Science 1997, 60:1129-1157.
81. Sogard S M, Olla B L. Endurance of simulated winter conditions by age-0 walleye pollock: effects of body size, water temperature and energy stores. Journal of Fish Biology 2000, 56:1-21. 10.1111/j.1095-8649.2000.tb02083.x
82. Sokal R R, Rohlf J F. Biometry: The Principles and Practice of Statistics in Biological Research 1995, New York, NY, W.H. Freeman and Company
83. Thorpe J P, Morgan R I J. Parental influence on growth rate, smolting rate and survival in hatchery reared juvenile Atlantic salmon, Salmo salar. Journal of Fish Biology 1978, 13:549-556. 510.1111/j.1095-8649.1978.tb03467.x
84. Trippel E A. Estimation of male reproductive success of marine fishes. Journal of Northwest Atlantic Fisheries Sciences 2003, 33:81-113.
85. Trippel E A, Kraus G, Köster F W. Maternal and paternal influence on early life history traits and processes of Baltic cod Gadus morhua. Marine Ecology Progress Series 2005, 303:259-267.
86. Unwin M J, Kinnison M T, Boustead N C, Quinn T P. Genetic control over survival in Pacific salmon (Oncorhynchus spp.): experimental evidence between and within populations of New Zealand Chinook salmon (O. tshawytscha). Canadian Journal of Fisheries and Aquatic Sciences 2003, 60:1-11.
87. Van Guelpen L, Davis C C. Seasonal movements of the winter flounder, Pseudopleuronectes americanus, in two contrasting inshore locations in Newfoundland. Transactions of the American Fisheries Society 1979, 108:26-37.
88. van der Veer H W, Berghahn R, Rijnsdop A D. Impact of juvenile growth on recruitment in flatfish. Netherlands Journal of Sea Research 1994, 32:153-173.
89. Vøllestad L A, Lillehammer T. Individual variation in early life-history traits in brown trout. Ecology of Freshwater Fish 2000, 9:242-247.
90. Wang X, Ross K E, Saillant E, Gatlin D M, Gold J R. Quantitative genetics and heritability of growth-related traits in hybrid striped bass (Morone chrysops♀×Morone saxatilis♂). Aquaculture 2006, 261:535-545.
91. Wedekind C, Muller R, Spicher H. Potential genetic benefits of mate selection in whitefish. Journal of Evolutionary Biology 2001, 14:980-986.
92. Yamamoto T, Reinhardt U G. Paternal effect on otolith size at emergence in masu salmon. Journal of Fish Biology 2003, 62:1226-1231. 1210.1046/j.1095-8649.2003.00103.x
93. Yamashita Y, Tanaka M, Miller J M. Ecophysiology of juvenile flatfish in nursery grounds. Journal of Sea Research 2001, 45:205-218.
94. Ziskowski J, Murchelano R. Fin erosion in winter flounder. Marine Pollution Bulletin 1975, 6:26.
95. DeCelles G R, Cadrin S X. An interdisciplinary assessment of winter flounder stock structure. 2007, 1-20. http://www.ices.dk/products/cmdocsindex.asp, Available at