Linking size and age at sexual maturation to body growth, productivity and recruitment of Atlantic cod stocks spanning the North Atlantic

Fisheries Research

Volumn 138, Issue , 2013, Pages 52-61

  Köster, Friedrich W ^a   Trippel, Edward A ^b   Tomkiewicz, Jonna ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b ST ANDREWS BIOLOGICAL STATION   (Canada)

Author keywords

Atlantic cod; Growth; Recruitment; Sexual maturation; Surplus production

Indexed keywords

GADUS MORHUA;

EID: 84871749569     PISSN: 01657836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fishres.2012.07.002     Document Type: Article

References (83)

1. Ajiad A., Jakobsen T., Nakken O. Sexual difference in maturation of northeast Arctic cod. J. Northw. Atl. Fish. Sci. 1999, 25:1-15.
2. Alm G. Connection between maturity, size, and age in fishes. Rep. Inst. Fresh. Res. Drott. 1959, 40:5-145.
3. Armstrong M.J., Gerritsen H.D., Allen M., McCurdy W.J., Peel J.A.D. Variability in maturity and growth in a heavily exploited stock: cod (Gadus morhua L.) in the Irish Sea. ICES J. Mar. Sci. 2004, 61:98-112.
4. Beyer J.E.B., Lassen H. The effect of size-selective mortality on the size-at-age of Baltic herring. Dana 1994, 10:203-234.
5. Blanchard J.L., Heffernan O.A., Fox C.J. North Sea. Spawning and Life History Information for North Atlantic Cod Stocks 2005, vol. 274:76-88. ICES Coop. Res. Rep.
6. Spawning and Life History Information for North Atlantic Cod Stocks 1994, vol. 205. ICES Coop. Res. Rep., 103 pp.
7. Brander K.M. The effect of temperature on growth of Atlantic cod (Gadus morhua L.). ICES J. Mar. Sci. 1995, 52:1-10.
8. Brander K.M. Effects of environmental variability on growth and recruitment in cod (Gadus morhua) using a comparative approach. Oceanol. Acta 2000, 23:485-495.
9. Brander K.M. Checklist for the synthesis of information on spawning and life history of North Atlantic cod stocks and summary tables. Spawning and Life History Information for North Atlantic Cod Stocks 2005, vol. 274:1-10. ICES Coop. Res. Rep.
10. Brander K.M., Mohn R. Effect of the North Atlantic Oscillation on recruitment of Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 2004, 61:1558-1564.
11. Burton M.P.M., Penny R.M., Biddiscombe S. Time course of gametogenesis in Northwest Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 1997, 54(Suppl. 1):122-131.
12. Campana S.E., Mohn R.K., Smith S.J., Chouinard G.A. Spatial implications of a temperature based growth model for Atlantic cod (Gadus morhua) off the eastern coast of Canada. Can. J. Fish. Aquat. Sci. 1995, 52:2445-2456.
13. Cardinale M., Modin J. Changes in size-at-maturity of Baltic cod (Gadus morhua) during a period of large variations in stock size and environmental conditions. Fish. Res. 1999, 41:285-295.
14. Chabot D., Dutil J.D. Reduced growth of Atlantic cod in non-lethal hypoxic conditions. J. Fish Biol. 1999, 55:472-491.
15. Chouinard, G.A., Currie, L.G., Poirier, G.A., Swain, D.P., Benoît, H.P., Hurlbut, T., Daigle, D., Savoie, L., 2005. Assessment of the southern Gulf of St. Lawrence cod stock. Can. Sci. Adv. Secr. Res. Doc. 2005/007, 95 pp.
16. Clark, D.S., Hinze, J.M., 2004. Assessment of cod in Division 4x in 2004. Can. Sci. Adv. Secr. Res. Doc. 2004/100, 35 pp.
17. Cook R.M., Kunzlik P.A., Hislop J.R.G., Poulding D. Models of growth and maturity for North Sea cod. J. Northw. Atl. Fish. Sci. 1999, 25:91-99.
18. D'Amours D. The distribution of cod (Gadus morhua) in relation to temperature and oxygen level in the Gulf of St. Lawrence. Fish. Oceanogr. 1993, 2:24-29.
19. Dickson R.R., Meincke J. The North Atlantic Oscillation and the ocean's response in the 1990. ICES Mar. Sci. Symp. 2003, 219:15-24.
20. Drinkwater K.F. A review of the role of climate variability in the decline of northern cod. Fisheries in a Changing Climate. American Fisheries Society Symposium 32 2002, 113-130. N.A. McGinn (Ed.).
21. Drinkwater K.F. The response of Atlantic cod (Gadus morhua) to future climate change. ICES J. Mar. Sci. 2005, 62:1327-1337.
22. Drinkwater K.F., Mountain D.B. Climate and oceanography. Northwest Atlantic Groundfish: Perspectives on a Fishery Collapse 1997, 3-25. American Fisheries Society, Bethesda, MD. J.G. Boreman, B.S. Nakashima, J.A. Wilson, R.L. Kendell (Eds.).
23. Drinkwater, K., Loeng, H., 2005. Physical oceanography of Atlantic cod habitats. ICES CM 2005/AA:12.
24. Dutil J.-D., Castonguay M., Gilbert D., Gascon D. Growth, condition, and environmental relationship in Atlantic cod (Gadus morhua) in the northern Gulf of St. Lawrence and implications for management strategies in the Northwest Atlantic. Can. J. Fish. Aquat. Sci. 1999, 56:1818-1831.
25. Dutil J.-D., Brander K.M. Comparing productivity of North Atlantic cod (Gadus morhua) stocks and limits to growth production. Fish. Oceanogr. 2003, 12:502-512.
26. Dutil, J.-D., Gauthier, J., Lambert, Y., Fréchet, A., Chabot, D., 2003. Cod stocks rebuilding and fish bioenergetics: low productivity hypothesis. Can. Sci. Adv. Secr. Res. Doc. 2003/060, 39 pp.
27. Dutil J-D., Lambert Y. Natural mortality from poor condition in Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 2000, 57:826-836.
28. Eliassen J.E., Vahl O. Seasonal variations in biochemical composition and energy content of liver, gonad and muscle of mature and immature cod, Gadus morhua (L.) from Balsfjorden, northern Norway. J. Fish Biol. 1982, 20:707-716.
29. Fréchet, A., Gauthier, J., Schwab, P., Pageau, L., Savenkoff, C., Castonguay, M., Chabot, D., Tournois, C., Lussier, J.-F., Spingle, J., Collier, F., 2005. The status of cod in the Northern Gulf of St. Lawrence (3Pn, 4RS) in 2004. Can. Sci. Adv. Secr. Res. Doc. 2005/060, 71 pp.
30. González-Troncoso, D., Vázquez, A., 2010. Assessment of the Cod Stock in NAFO Division 3M. NAFO SCR Doc. 10/41, 44 pp.
31. Grift R.E., Heino M., Rijnsdorp A.D., Kraak S.B.M., Dieckmann U. Three-dimensional maturation norms for North Sea plaice. Mar. Ecol. Prog. Ser. 2007, 334:213-224.
32. Hanson J.M., Chouinard G.A. Evidence that size-selective mortality affects growth of Atlantic cod (Gadus morhua L.) in the southern Gulf of St. Lawrence. J. Fish Biol. 1992, 41:31-41.
33. Healey, B.P., Murphy, E.F., Stansbury, D.E., Brattey, J., 2003. An Assessment of the Cod Stock in NAFO Divisions 3NO. NAFO SCR Doc. No. 03/59, 60 pp.
34. Hutchings J.A. Life history consequences of overexploitation to population recovery in Northwest Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 2005, 62:824-832.
35. ICES, 1990. Report of the Working Group on cod stocks off East Greenland. ICES CM 1990/Assess: 12.
36. ICES, 2004. Report of the North-Western Working Group. ICES CM 2004/ACFM: 25.
37. ICES, 2005. Report of the Arctic Fisheries Working Group. ICES CM 2005/ACFM: 20.
38. ICES, 2005. Report of the Baltic Fisheries Assessment Working Group. ICES CM 2005/ACFM: 19.
39. ICES, 2011. Report of the Workshop on Implementing the ICES Fmsy Framework (WKFRAME-2). ICES CM 2011/ACOM: 33.
40. Jobling M. Food and growth relationships of the cod, Gadus morhua L., with special reference to Balsfjorden, northern Norway. J. Fish Biol. 1982, 21:357-371.
41. Jørgensen C., Ernande B., Fiksen Ø., Dieckmann U. The logic of skipped spawning in fish. Can. J. Fish. Aquat. Sci. 2006, 63:200-211.
42. Kinnison M.T., Quinn T.P., Unwin M.J. Correlated contemporary evolution of life history traits in New Zealand Chinook salmon, Oncorhynchus tshawytscha. Heredity 2011, 106:448-459.
43. Köster F.W., Möllmann C., Neuenfeldt S., Vinther M., St John M.A., Tomkiewicz J., Voss R., Hinrichsen H.H., Kraus G., Schnack D. Fish stock development in the Central Baltic Sea (1976-2000) in relation to variability in the physical environment. ICES Mar. Sci. Symp. 2003, 219:294-306.
44. Kuparinen A., O'Hara R.B., Merila J. The role of growth history in determining age and size at maturation in exploited fish populations. Fish Fish. 2008, 9:201-207.
45. Lambert Y., Dutil J.-D. Condition and energy reserves of Atlantic cod (Gadus morhua) during the collapse of the northern Gulf of St. Lawrence stock. Can. J. Fish. Aquat. Sci. 1997, 54:2388-2400.
46. Lambert Y., Yaragina N.A., Kraus G., Marteinsdottir G., Wright P.J. Using environmental and biological indices as proxies for egg and larval production of marine fish. J. Northw. Atl. Fish. Sci. 2003, 33:115-159.
47. Lambert, Y., Kjesbu, O.S., Kraus, G., Marteinsdottir, G., Thorsen, A., 2005. How variable is the fecundity within and between cod stocks? ICES C.M. 2005/Q: 13.
48. Lilly G.R. Southern Labrador and eastern Newfoundland (NAFO Divisions 2J+3KL). Spawning and Life History Information for North Atlantic Cod Stocks 2005, vol. 274:146-157. ICES Coop. Res. Rep.
49. Lilly, G.R., Murphy, E.F., 2004. Biology, fishery and status of the 2GH and 2J3KL (northern) cod stocks: information supporting an assessment of allowable harm under the Species at Risk Act for the COSEWIC-defined Newfoundland and Labrador population of Atlantic cod (Gadus morhua). Can. Sci. Adv. Secr. Res. Doc. 2004/102, 107 pp.
50. Marshall C.T., Needle C.L., Thorsen A., Kjesbu O.S., Yaragina N.A. Systematic bias in estimates of reproductive potential of an Atlantic cod (Gadus morhua) stock: implications for stock-recruit theory and management. Can. J. Fish. Aquat. 2006, 63:980-994.
51. Marshall C.T., McAdam B.J. Integrated perspectives on genetic and environmental effects on maturation can reduce potential for errors of inference. Mar. Ecol. Prog. Ser. 2007, 335:301-310.
52. Marteinsdóttir G., Begg G.A. Essential relationships incorporating the influence of age, size and condition on variables required for estimation of reproductive potential in Atlantic cod Gadus morhua. Mar. Ecol. Prog. Ser. 2002, 235:235-256.
53. Mayo R.K., Col L.A., 2006. The 2005 assessment of the Gulf of Maine Atlantic cod stock. US Dep. Commer., Northeast Fish Sci. Cent. Ref. Doc. 06-02, 109 pp.
54. Meyer, A., 1973. German research report, subarea I and East Greenland. ICNAF Redbook, III, pp. 41-43.
55. Morgan M.J., Colbourne E.B. Variation in maturity-at-age and size in three populations of American plaice. ICES J. Mar. Sci. 1999, 56:673-688.
56. Morgan M.J., Murua H., Kraus G., Lambert Y., Marteinsdottir G., Marshall C.T., O'Brien L., Tomkiewicz J. The evaluation of reference points and stock productivity in the context of alternative indices of stock reproductive potential. Can. Fish. Aquat. Sci. 2009, 66:404-414.
57. Morgan M.J., Rideout R.M., Colbourne E.B. Impact of environmental temperature on Atlantic cod Gadus morhua energy allocation to growth, condition and reproduction. Mar. Ecol. Prog. Ser. 2010, 404:185-195.
58. Neuheimer A.N., Grønkjær P. Climate effects on size-at-age: growth in warming waters compensates for earlier maturity in an exploited marine fish. Glob. Change Biol. 2012, 10.1111/j.1365-2486.2012.02673.x.
59. O'Brien, L., Munroe, N.J., Col, L., 2005. Georges Bank Cod in: Assessment of 19 Northeast groundfish stocks through 2004. 2005 Groundfish Assessment Review Meeting (GARM). Report of the SAW Northern and Southern Demersal Working Groups, Northeast Fisheries Science Center, Woods Hole, Massachusetts.
60. Olsen E.M., Heino M., Lilly G.R., Morgan M.J., Brattey J., Ernande B., Dieckmann U. Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 2004, 428:932-935.
61. Olsen E.M., Lilly G.R., Heino M., Morgan M.J., Brattey J., Dieckmann U. Assessing changes in age and size at maturation in collapsing populations of Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 2005, 62:811-823.
62. Rätz H.-J., Lloret J. Variation in fish condition between Atlantic cod (Gadus morhua) stocks, the effect on their productivity and management implications. Fish. Res. 2003, 6:369-380.
63. Rideout R.M., Tomkiewicz J. Skipped spawning in fishes: more common than you might think. Mar. Coast. Fish. 2011, 3:176-189.
64. Rideout R.M., Morgan M.J., Lilly G.R. Variation in the frequency of skipped spawning in Atlantic cod (Gadus morhua) off Newfoundland and Labrador. ICES J. Mar. Sci. 2006, 63:1101-1110.
65. Rijnsdorp A.D. Relationship between juvenile growth and the onset of sexual maturity of female North Sea plaice, Pleuronectes platessa. Can. J. Fish. Aquat. Sci. 1993, 50:1617-1631.
66. Rochet, M.J., 2000. Spatial and temporal patterns in age and size at maturity and spawning stock biomass of North Sea Gadoids. ICES C.M. 2000/N: 26.
67. Salvanes A.G.V., Skjaeraasen J.E., Nilsen T. Sub-populations of coastal cod with different behaviour and life-history strategies. Mar. Ecol. Prog. Ser. 2004, 267:241-251.
68. Shelton P.A., Sinclair A.F., Chouinard G.A., Mohn R., Duplisea D.E. Fishing under low productivity conditions is further delaying recovery of Northwest Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 2006, 63:235-238.
69. Stearns S.C., Crandall R.E. Plasticity for age and size at sexual maturity: a life-history response to unavoidable stress. Fish Reproduction: Strategies and Tactics 1984, 13-33. Academic Press, London, UK. G.W. Potts, R.J. Wooton (Eds.).
70. Steingrund P., Hansen B., Gaard E. Cod in Faroese waters. Spawning and life history information for North Atlantic cod stocks 2005, vol. 274:50-55. ICES Coop. Res. Rep.
71. Swain, D.P., Chouinard, G.A., 2000. Spawning stock characteristics and cod recruitment success in the southern Gulf of St. Lawrence. Can. Sci. Adv. Secr. Res. Doc. 2000/148, 14 pp.
72. Tobin D., Wright P.J. Temperature effects on female maturation in a temperate marine fish. J. Exp. Mar. Biol. Ecol. 2011, 403:9-13.
73. Thorpe J.E. Maturation responses of salmonids to changing developmental opportunities. Mar. Ecol. Prog. Ser. 2007, 335:285-288.
74. Tomkiewicz J., Lehmann K.M., St John M.A. Oceanographic influences on the distribution of Baltic cod, Gadus morhua, during spawning in the Bornholm Basin of the Baltic Sea. Fish. Oceanogr. 1998, 7:48-62.
75. Tomkiewicz, J., Eriksson, M., Baranova, T., Feldman, V., 1997. Maturity ogives and sex ratios for Baltic cod: establishment of a database and time series. ICES CM 1997/CC: 20.
76. Tomkiewicz J., Morgan M.J., Burnett J., Saborido-Rey F. Available information for estimating reproductive potential of Northwest Atlantic groundfish stocks. J. Northw. Atl. Fish. Sci. 2003, 33:1-21.
77. Trippel E.A. Age at maturity as a stress indicator in fisheries. Bioscience 1995, 45:759-771.
78. Trippel E.A., Harvey H.H. Comparison of methods used to estimate age and length of fishes at sexual maturity using populations of white sucker (Catostomus commersoni). Can. J. Fish. Aquat. Sci. 1991, 48:1446-1459.
79. Trippel E.A., Kjesbu O.S., Solemndal P. Effects of adult age and size structure on reproductive output in marine fishes. Early Life History and Recruitment in Fish Populations 1997, 31-62. Chapman & Hall, London, UK. R.C. Chambers, E.A. Trippel (Eds.).
80. Trippel E.A., Morgan M.J., Fréchet A., Rollet C., Sinclair A., Annand C., Beanlands D., Brown L. Changes in age and length at sexual maturity of northwest Atlantic cod, haddock and Pollock stocks 1972-1995. Can. Tech. Rep. Fish. Aquat. Sci. 1997, 2157:120.
81. Wieland K., Storr-Paulsen M. East and west greenland. Spawning and life history information for North Atlantic cod stocks 2005, vol. 274:39-47. ICES Coop. Res. Rep.
82. Wright P.J., Milar C.P., Gibb F.M. Intrastock differences in maturation schedules of Atlantic cod, Gadus morhua. ICES J. Mar. Sci. 2011, 68:1918-1927.
83. Yoneda M., Wright P.J. Effect of temperature and food availability on reproductive investment of first-time spawning male Atlantic cod, Gadus morhua. ICES J. Mar. Sci. 2005, 62:1383-1387.