ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on November 13, 2006
ICES Journal of Marine Science: Journal du Conseil 2007 64(2):211-217; doi:10.1093/icesjms/fsl021
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The role of growth changes in the decline and recovery of North Atlantic cod stocks since 1970
International Council for the Exploration of the Sea, H. C. Andersens Boulevard, DK–1553 Copenhagen V, Denmark
Correspondence to K. M. Brander: tel: +45 33386728; fax: +45 33934215; e-mail: keith{at}ices.dk
Brander, K. M. 2007. The role of growth changes in the decline and recovery of North Atlantic cod stocks since 1970. – ICES Journal of Marine Science, 64: 211–217.
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Introduction |
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 Top Introduction Trends in cod biomass...Patterns of declineCauses and consequences of...Weight-at-age does not increase...References |
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The three principal aims of this essay are: (i) to describe the changes in biomass that have taken place in North Atlantic cod (Gadus morhua) stocks since 1970; (ii) to investigate potential causes of prolonged periods of decline in biomass; and (iii) to encourage the development and testing of more detailed and rigorous models of the processes causing decline in biomass, in particular by including the role of changes in weight-at-age. The working definition of a "prolonged period of decline" adopted here is a period during which total biomass or weight-at-age declines in five of seven consecutive years.
North Atlantic cod have been subjected to excessive fishing pressure for many years, and 14 of the 15 stocks analysed here have declined since 1970. In ten of these stocks the periods of decline in total biomass were preceded by or coincided with declines in mean weight-at-age. Ten stocks also experienced periods of increasing cod biomass, which were accompanied by increasing weight-at-age. The changes in weight-at-age are probably due to environmental factors. The interpretation of these trends does not challenge the conclusion that fishing is a major cause of observed stock declines, but it does raise questions concerning both the prevalence and magnitude of environmental effects and the processes through which they act. Although recruitment is the major cause of variability in biomass, my thesis is that more attention should be paid to variability in weight-at-age and its causes. Weight-at-age changes provide evidence of changes in growth which may in turn be due to changes in environmental conditions, influencing production.
Total landings of North Atlantic cod declined from >3 million tonnes in 1970 to less than 1 million tonnes in 2000, accompanied by a lowering of total stock biomass, for which the term "collapse" has frequently been used (Harris, 1998). The downward trend has been particularly marked in the Northwest Atlantic, fisheries for cod along most of the Canadian shelf having been stopped or severely restricted since the early 1990s, with the aim of allowing the stocks to recover; regrettably there are as yet few signs of recovery there. The declines in Northeast Atlantic stocks, while serious, have not been as extreme as those in the Northwest Atlantic, and cod fisheries have continued, with restrictions on total catch and some seasonal and area closures.
There is considerable interest in establishing the causes of the declines, in order to learn how to avoid such changes in the future, to provide appropriate advice for ongoing management of stocks on which fishing continues, and to make forecasts of the likelihood and time scale of stock recovery (Rice et al., 2003). These concerns are addressed here by bringing together information about the trends in total biomass and weight-at-age for 15 cod stocks, divided between the Northeast and the Northwest Atlantic, and describing the patterns of change that have taken place.
Superimposed on the trends caused by fishing mortality, fish populations undergo large fluctuations in biomass, which are generally ascribed to variability in recruitment (Cushing, 1996). Cod are no exception to this, but the variability in recruitment is actually remarkably small (Brander, 2003). The emphasis on recruitment as the cause of biomass fluctuation has drawn attention away from variability in weight-at-age, and here I try to redress the balance a little: most declines and recoveries of cod stocks since 1970 have been accompanied or preceded by changes in weight-at-age. The causes of these changes in weight-at-age may be an important component of understanding why total biomass fluctuates. Growth and survival to recruitment are intimately related processes in the life history (Pepin, 1999). Variability in weight-at-age and recruitment (numbers-at-age) are not alternative, independent explanations of biomass fluctuations; both must be considered.
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Trends in cod biomass and weight-at-age |
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TopIntroductionTrends in cod biomass...Patterns of declineCauses and consequences of...Weight-at-age does not increase...References |
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Information on many characteristics of North Atlantic cod life histories and population processes has recently been assembled and published in a standard format for 17 stocks, together with extensive reference lists (ICES, 2005). Data on 15 of these stocks are presented here (Table 1), with some additional information from primary sources, which are either cited in ICES (2005) or here.
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Trends in population biomass for each cod stock are represented by total biomass. This is the product of population number- and weight-at-age, the former being derived from catch-at-age using virtual population analysis (VPA), the latter from sampling of commercial and research survey catches.
Trends in weight of individual cod are represented by stock weight-at-age averaged over five age groups, beginning in each case with the age at which the fish attain 1 kg. This range was chosen to represent the most abundant and best sampled ages in the catch, i.e. those large enough to exceed the size over which gear selection occurs, but excluding older age classes, which are influenced by small number effects. Weight-at-age (state) is not intended to represent growth (rate) in this analysis, but changes in weight-at-age provide evidence of changes in growth. The time-series of biomass and weight-at-age are shown in Figure 1. A seven-year moving window analysis of the time-series of total biomass and mean weight is used to identify "prolonged periods of decline" (Table 2).
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The quality and the completeness of the time-series were erratic prior to 1970, so almost all the data used are for subsequent years. Although the time-series are referred to as "data", they are in fact model output. Changes to VPAs, which are in many cases updated annually, alter the estimates of numbers and stock biomass, but for earlier years such retrospective changes are small and do not affect the main trends.
Mean annual bottom temperature for each stock is taken from Brander (1995) and Myers et al. (2001). The depth-averaged 5-year running mean of water-column temperature for the Newfoundland Shelf (Stn 27) is from Colbourne and Anderson (2003).
Mean weight-at-age is plotted as a function of biomass per unit area in Figure 2 for 14 stocks, and the regression equations and coefficients of determination (r2) are shown. Biomass is presented per unit of area occupied by the stock (in kg ha–1) in this figure, in order to allow comparisons of the range of densities between stocks. Total biomass of cod per unit area was calculated using estimates of habitat area from Myers et al. (2001). The habitat area for each stock is defined as the area of shelf of depth <300 m. The distribution in the Barents Sea is truncated by a thermal limit and in the Baltic by a salinity limit. The habitat area for the Icelandic stock includes the shelf area of East Greenland (ICES area XIVb), because cod from the Icelandic stock sometimes occupy this area before they mature.
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Patterns of decline |
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TopIntroductionTrends in cod biomass...Patterns of declineCauses and consequences of...Weight-at-age does not increase...References |
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The six cod stocks in Canadian waters all experienced a prolonged period of decline which began in the mid-1980s and ended in the mid-1990s (Figure 1; Table 2). The decline in biomass in these six stocks was in every case preceded by a decline in mean weight-at-age. The lag between the decline in biomass and the decline in weight-at-age was 5 y for four of the six stocks, 2 y for the southern Grand Bank stock and 8 y for the southern Gulf of St Lawrence. The biggest decline in biomass was in the southern Grand Bank stock, for which the total biomass in 1995 was just 3% of its 1984 level. The smallest decline was in the southern Newfoundland stock, which fell to 26% of its 1985 level by 1993. The decline in weight-at-age was in every case much smaller than the decline in biomass (34–80% of the original level).
The Canadian cod stocks share other common patterns of change in total biomass and weight-at-age. Both declined until about 1975, followed by a substantial increase to the early or mid-1980s. Weight-at-age increased in all Canadian stocks after 1995, but total biomass only increased in some. The depth-averaged 5-y mean of temperature at Stn 27 on the Newfoundland shelf shown in Figure 1 shares some of the trends described for weight-at-age and total biomass. The southernmost stock in the Northwest Atlantic is the shared stock on Georges Bank. It underwent a prolonged period of decline in total biomass from 1988 to 1995, but not in weight-at-age.
The offshore cod stock at Greenland is included in Tables 1 and 2, but it lacks a complete, consistent time-series since 1992 because the biomass is too small to assess. It had a prolonged period of decline from 1966 to 1975 (to 5% of its start level), which was preceded by a decline in weight-at-age (lagged by 3 y).
With the exception of the Celtic Sea, Northeast Atlantic cod stocks also declined after 1970, but the declines do not share a common pattern and are much smaller than those among the Canadian stocks. In the Northeast Atlantic there have also been a number of periods of rapid increase in total biomass. For example, the stock at Faroe declined to 19% of its 1984 level by 1991, but increased quickly to its original level by 1996. On both sides of the North Atlantic, changes in mean weight-at-age are smaller in the warmer water stocks (Georges Bank, North Sea, Irish Sea, Celtic Sea), and there are no prolonged periods of decline in weight-at-age in any of these areas, or in the Baltic.
As total population biomass is the product of number-at-age and individual weight-at-age, a change in weight-at-age will (other things being equal) result in an immediate and proportional change in biomass. However, a density-dependent relationship would cause weight-at-age to decline as biomass increased, so a negative relationship between weight-at-age and biomass may be regarded as evidence of density-dependent effects (Lorenzen and Engberg, 2002). Plotting weight-at-age as a function of biomass (per unit area), eight regressions are nominally statistically significant (two at p < 0.05, six at p < 0.01; Figure 2). Seven of the significant relationships are positive. The only negative relationship is for the Eastern Baltic stock. The models do not take temporal autocorrelation into account.
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Causes and consequences of changes in weight-at-age |
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TopIntroductionTrends in cod biomass...Patterns of declineCauses and consequences of...Weight-at-age does not increase...References |
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All North Atlantic cod stocks have declined in total biomass since 1970, with the exception of the stock in the Celtic Sea. Overfishing is a major cause of decline in every case, but there may be other contributing factors.
A period of prolonged decline in weight-at-age began between 1978 and 1982 in all Canadian cod stocks (Table 2), probably the consequence of an adverse change in the productivity of the stocks (Dutil et al., 1999; Drinkwater, 2002; Dutil and Brander, 2003). This must have had an immediate, proportional effect on biomass, but the effect is not detectable either because it was too small and/or because it was obscured by other changes (e.g. in stock numbers). The decline in biomass in the six Canadian stocks began 2–8 y later, and was much greater than the change in weight-at-age.
Could a change in weight-at-age cause a lagged decline in stock biomass? I suggest two explanations and proposals for further modelling. First, the allocation of energy to routine metabolism, somatic growth, and reproduction may change (Nisbet et al., 2000), resulting in non-linear changes in reproductive output, by altering age and size at maturity, specific fecundity, and egg viability. Dynamic energy budget models would be suitable for exploring this process (Nisbet et al., 2000). Second, when weight-at-age changes, the effect of fishing on the stock is altered in several ways. For example, a total allowable catch (TAC) intended to harvest a defined proportion of the stock will only do so if the weight-at-age has been correctly predicted. An unanticipated decline in weight-at-age would cause fishing mortality to be greater than intended (more small fish being caught). Moreover, fishers dump fish of poor condition (highgrading), resulting in additional mortality (Kulka, 1997). Even before the underlying processes are revealed, it would seem worthwhile to monitor persistent changes in mean weight-at-age, because a decline may provide early information of increased risk of stock decline.
All stocks have experienced periods of increasing total biomass, which are generally attributed to one or more years of good recruitment. In many cases (Figure 1), however, the stock increases coincided with increasing weight-at-age, suggesting that here too changes in individual growth and productivity played a role.
Changes in mean weight-at-age are generally attributed to changes in growth rate attributable to (i) "environmental" factors, the principal one being ambient temperature; (ii) food availability (including density-dependent effects); and (iii) selective effects of fishing (Krohn et al., 1997; Swain et al., 2003), but it can be difficult to disentangle these, because their effects can be direct or indirect and they interact with each other. For example, temperature has a direct effect on growth rate, but also an indirect effect by altering the production of food organisms (ICES, 2002). Another reason why it is difficult to assign causes with confidence is the poor quality of field information on the contributing factors; for want of more precise, directly observed information, various proxies are used. Interannual changes in temperature may be represented by mean bottom temperature at a fixed station or by a value for the area occupied by cod during an annual fishing survey (i.e. ambient temperature is unknown); population biomass is used to represent density-dependent effects (i.e. intensity of competition for food is unknown), and selective effects of fishing are inferred from sizes backcalculated from otolith increments (i.e. actual selection by fishing activity is unknown) (Sinclair et al., 2002).
Observed changes in weight-at-age have been attributed to all of these causes and to their combinations in different stocks. The depth-averaged temperature at Stn 27 on the Newfoundland shelf (Figure 1) is an indicator of major changes in the thermal environment of the Canadian shelf, with widespread consequences for the ecosystems (Frank et al., 2005). The prima facie evidence of patterns of change in weight-at-age and total biomass, which are similar to this temperature pattern, point to a causal connection. Temperature influences growth of cod, and evidence from experiments and in the field shows that the effect of temperature change is progressively greater at low temperatures (Bjornsson and Steinarsson, 2002; Brander, 2003; Folkvord, 2005). This may explain why the warm-water stocks (Georges Bank, North Sea, Irish Sea, Celtic Sea) show less variability in weight-at-age than the cold-water stocks. More detailed studies of the growth changes in individual Canadian cod stocks support the existence of a temperature effect, but also the effects of prey availability (Krohn et al., 1997), density-dependence, and a common pattern of residuals, which may be attributable to size-selective mortality (Swain et al., 2003). Other published work (Dutil et al., 1999; Rätz and Lloret, 2003) has shown that declines in biomass were also accompanied by declines in fish condition; those authors also considered the implications for productivity and management.
Unlike in the Northwest Atlantic, where the oceanographic and biological environment of the Canadian shelf is dominated by changes in the Labrador Slope Current, Northeast Atlantic stocks do not show common patterns of change in weight-at-age. A second major difference between Northeast and Northwest Atlantic cod stocks is that the former occupy areas with mean temperatures >4°C, whereas the latter occupy areas with mean temperatures <4°C, with the exception of Georges Bank. For some Northeast Atlantic stocks, there is evidence that temperature causes changes in weight-at-age (Brander, 2000; Ottersen and Loeng, 2000), but it is difficult to distinguish direct temperature effects from the associated effects on production or dynamics of forage species, such as capelin (Michalsen et al., 1998). Interannual variability in capelin (Mallotus villosus) abundance seems to play a major role in changes in weight-at-age in the Arcto-Norwegian and Icelandic cod stocks and is important in the Northwest Atlantic too (Rose and O'Driscoll, 2002). Weight-at-age changes at Faroe, which are particularly closely coupled with changes in total biomass (Figure 2) have been linked to changes in plankton production (Steingrund and Gaard, 2005). The Eastern Baltic is the only stock with a significant negative relationship between weight-at-age and stock abundance, but this has been ascribed to the closely coupled predator–prey relationships between cod and its principal prey species there, sprat (Sprattus sprattus) and herring (Clupea harengus), rather than to density-dependence (Gislason, 1999).
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Weight-at-age does not increase as biomass declines |
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TopIntroductionTrends in cod biomass...Patterns of declineCauses and consequences of...Weight-at-age does not increase...References |
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The hypothesis that growth is density-dependent is not refuted by the overwhelmingly positive relationships between total biomass and weight-at-age (Figure 2), but it does suggest that density-dependent effects are neither widespread nor influential. Growth may be density-dependent in situations where there is competition for a limited supply of food or some other essential item, but direct evidence of such competition is difficult to obtain. By definition, density-dependence is more likely where density is high (relative to food availability and requirement), and the absolute scaling used in Figure 2 may, therefore, provide some insight into the stocks and times when it is more or less likely to occur. In the areas at the warm end of the species range (Georges Bank, Irish Sea, Celtic Sea), the density of cod has always been low (<10 kg ha–1), and the species is a minor component of the total demersal fish community. In many other stocks, which were at much higher densities prior to stock decline, the levels have also fallen below 10 kg ha–1. A convincing, process-based case for density-dependent growth in those stocks probably requires detailed information on aggregation, food availability, and spatial dynamics.
A recent meta-analysis found evidence that density-dependent growth was a key mechanism in the regulation of fish populations (Lorenzen and Engberg, 2002). However, among the nine marine stocks which they analysed, five did not show evidence of density-dependent growth, including the only cod stock (North Sea). As their meta-analysis only included biomass, it did not consider alternative explanations for the changes observed in growth, such as prey abundance (Krohn et al., 1997; Gislason, 1999), size-selective fishing, and temperature (Ottersen and Loeng, 2000; Swain et al., 2003).
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Acknowledgements |
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This work is a contribution to the ICES/GLOBEC Cod and Climate Change programme, funded by the UK Department of Environment, Food and Rural Affairs (Defra), the Norwegian Research Council, the Danish Institute for Fisheries Research (DIFRES), and the French Research Institute for Exploitation of the Sea (Ifremer). Thanks are due to Henrik Sparholt for useful discussions and to anonymous referees for suggesting improvements.
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References |
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TopIntroductionTrends in cod biomass...Patterns of declineCauses and consequences of...Weight-at-age does not increase...References |
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Bishop C. A., Murphy E. F., Davis M. B., Baird J. W., Rose G. A. (1993) An assessment of the cod stock in NAFO Divisions 2J+ 3KL. NAFO Scientific Council Research Documents 93/86 51.
Bjornsson B. and Steinarsson A. (2002) The food-unlimited growth rate of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 59:494–502.[CrossRef]
Brander K. M. (1995) The effect of temperature on growth of Atlantic cod (Gadus morhua L.). ICES Journal of Marine Science 52:1–10.
Brander K. M. (2000) Effects of environmental variability on growth and recruitment in cod (Gadus morhua) using a comparative approach. Oceanologica Acta 23:485–496.[Medline]
Brander K. M. (2003) What kinds of fish stock predictions do we need and what kinds of information will help us to make better predictions? Scientia Marina 67:21–33.[Web of Science]
Brattey J., Cadigan N. G., Healey B. P., Lilly G. R., Murphy E. F., Stansbury D.E., Mahé J-C. (2003) An assessment of the cod (Gadus morhua) stock in NAFO Subdiv. 3Ps in October 2003. Canadian Science Advisory Secretariat Research Document 2003/092 98.
Chouinard G. A., Swain D. P., Currie L. G., Poirier G. A., Rondeau A., Benoit H., Hurlbut T., et al. (2003) Assessment of the southern Gulf of St Lawrence cod stock, February 2003. Canadian Science Advisory Secretariat Research Document 2003/015 118.
Colbourne E. B. and Anderson J. T. (2003) Biological response in a changing ocean environment in Newfoundland waters during the latter decades of the 1900s. ICES Marine Science Symposia 219:169–181.
Cushing D. H. (1996) Towards a science of recruitment in fish populations(Ecology Institute, Oldendorf).
Drinkwater K. F. (2002) A review of the role of climate variability in the decline of northern cod. American Fisheries Society Symposium 32:113–130.
Dutil J. D. and Brander K. M. (2003) Comparing productivity of North Atlantic cod (Gadus morhua) stocks and limits to growth production. Fisheries Oceanography 12:502–512.[CrossRef][Web of Science]
Dutil J. D., Castonguay M., Gilbert D., Gascon D. (1999) Growth, condition, and environmental relationships in Atlantic cod (Gadus morhua) in the northern Gulf of St Lawrence and implications for management strategies in the Northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 56:1818–1831.[CrossRef]
Folkvord A. (2005) Comparison of size-at-age of larval Atlantic cod (Gadus morhua) from different populations based on size- and temperature-dependent growth models. Canadian Journal of Fisheries and Aquatic Sciences 62:1037–1052.[CrossRef]
Frank K. T., Petrie B. D., Choi J. S., Leggett W. C. (2005) Trophic cascades in a formerly cod-dominated ecosystem. Science 308:1621–1623.
Fréchet A., Gauthier J., Schwab P., Bourdages H., Chabot D., Collier F., Grégoire F., et al. (2003) The status of cod in the Northern Gulf of St Lawrence (3Pn, 4RS) in 2002. Canadian Science Advisory Secretariat Research Document 2003/065 90.
Gislason H. (1999) Single and multispecies reference points for Baltic fish stocks. ICES Journal of Marine Science 56:571–583.
Harris M. (1998) Lament for an Ocean: the Collapse of the Atlantic Cod Fishery: a True Crime Story(McClelland & Stewart, Toronto).
Healey B. P., Stansbury D. E., Brattey J. (2003) An assessment of the cod stock in NAFO Divisions 3NO. NAFO Scientific Council Research Documents 03/59 62.
Hunt J. J. and Hatt B. (2002) Population status of eastern Georges Bank cod (Unit areas 5Zj,m) for 1978–2002. Canadian Science Advisory Secretariat Research Document 2002/72 48.
ICES. (1996) Report of the North Western Working Group. ICES Document CM 1996/15.
ICES. (2002) Report of the ICES/GLOBEC workshop on the dynamics of growth in cod. ICES Cooperative Research Report 252:97.
ICES. (2005) Spawning and life history information for North Atlantic cod stocks. ICES Cooperative Research Report 274: pp. 152.
Krohn M., Reidy S., Kerr S. (1997) Bioenergetic analysis of the effects of temperature and prey availability on growth and condition of northern cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 54:Suppl. 1113–121.[CrossRef]
Kulka D. W. (1997) Discarding of cod (Gadus morhua) in the northern cod and northern shrimp directed trawl fisheries, 1980–94. NAFO Scientific Council Studies 29:67–79.
Lilly G. R. and 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 of the COSEWIC-defined Newfoundland and Labrador population of Atlantic cod (Gadus morhua). Canadian Science Advisory Secretariat Research Document 2004/102 107.
Lilly G. R., Shelton P. A., Brattey J., Cadigan N. G., Healey B. P., Murphy E. F., Stansbury D. E., et al. (2003) An assessment of the cod stock in NAFO Divisions 2 J + 3 KL in February 2003. Canadian Science Advisory Secretariat Research Document 2003/023 160.
Lorenzen K. and Engberg K. (2002) Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons. Proceedings of the Royal Society of London 269: pp. 49–54 Series B.[Medline]
Michalsen K., Ottersen G., Nakken O. (1998) Growth of North-east Arctic cod (Gadus morhua L.) in relation to ambient temperature. ICES Journal of Marine Science 55:863–877.
Mohn R. K., Fanning L. P., MacEachern W. J. (1998) Assessment. of 4VsW cod in 1997 incorporating additional sources of mortality. Canadian Stock Assessment Secretariat Research Document 1998/78 32.
Myers R. A., MacKenzie B. R., Bowen K. G., Barrowman N. J. (2001) What is the carrying capacity for fish in the ocean? A meta-analysis of populations dynamics of North Atlantic cod. Canadian Journal of Fisheries and Aquatic Sciences 58:1464–1476.[CrossRef]
Nisbet R. M., Muller E. B., Lika K., Kooijman S. A. L. M. (2000) From molecules to ecosystems through dynamic energy budget models. Journal of Animal Ecology 69:913–926.[CrossRef]
O'Brien L., Munroe N. J., Col L. (2002. A) Georges Bank Atlantic cod. Northeast Fisheries Science Center Reference Document NEFSC 02-16 522.
Ottersen G. and Loeng H. (2000) Covariability in early growth and year-class strength of Barents Sea cod, haddock and herring: the environmental link. ICES Journal of Marine Science 57:339–348.
Pepin P. (1999) An appraisal of the size-dependent mortality hypothesis for larval fish: comparison of a mulitspecies study with an empirical review. Canadian Journal of Fisheries and Aquatic Sciences 50:2166–2174.
Rice J. A., Shelton P. A., Rivard D., Chouinard G. A., Fréchet A. (2003) Recovering Canadian Atlantic cod stocks: the shape of things to come. ICES Document CM 2003/U: 06.
Rose G. A. and O'Driscoll R. L. (2002) Capelin are good for cod: can the northern stock rebuild without them? ICES Journal of Marine Science 59:1018–1026.
Rätz H. J. and Lloret J. (2003) Variation in fish condition between Atlantic cod (Gadus morhua) stocks, the effect on their productivity and management implications. Fisheries Research 60:369–380.[CrossRef][Web of Science]
Sinclair A. F., Swain D. P., Hanson J. M. (2002) Disentangling the effects of size-selective mortality, density, and temperature on length-at-age. Canadian Journal of Fisheries and Aquatic Sciences 59:372–382.[CrossRef]
Steingrund P. and Gaard E. (2005) Relationship between phytoplankton and cod production on the Faroe Shelf. ICES Journal of Marine Science 62:163–176.
Swain D. P., Sinclair A. F., Castonguay M., Chouinard G. A., Drinkwater K. F., Fanning L. P., Clark D. S. (2003) Density- versus temperature-dependent growth of Atlantic cod (Gadus morhua) in the Gulf of St Lawrence and on the Scotian Shelf. Fisheries Research 59:327–341.[CrossRef]
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