ICES Journal of Marine Science, 62: 1322e1326 (2005) doi:10.1016/j.icesjms.2005.04.023 The implications of warming climate for the management of North Sea demersal fisheries R. M. Cook and M. R. Heath Cook, R. M., and Heath, M. R. 2005. The implications of warming climate for the management of North Sea demersal fisheries. e ICES Journal of Marine Science, 62: 1322e1326. Since the 1950s, records from the North Sea show a gradual increase in temperature. Using temperature as a proxy indexing the state of the environment, relationships between recruitment, spawning-stock biomass, and temperature are investigated for major North Sea stocks. Cod, plaice, and sole exhibit significant negative relationships between temperature and recruitment, while there is evidence of a positive effect for saithe and whiting. Stockrecruitment models that incorporate temperature are developed and used to examine implications for the management of these stocks with small increases in mean winter sea surface temperature. These suggest that for cod, minimum safe biomass reference points are unlikely to be achieved even at fishing mortality rates that are considered safe. The same analysis suggests that sustainable fishing for cod is still possible with higher yields than have been experienced in recent years. Crown Copyright Ó 2005 Published by Elsevier Ltd on behalf of International Council for the Exploration of the Sea. All rights reserved. Keywords: climate change, cod, demersal fish, fishery management, haddock, North Sea, plaice, saithe, sole, whiting. Received 23 June 2004; accepted 27 April 2005. R. M. Cook and M. R. Heath: FRS Marine Laboratory, PO Box 101, 375 Victoria Road, Aberdeen AB11 9DB, Scotland, UK. Correspondence to R. M. Cook: tel: C44 1224 295393; fax: C44 1224 295511; e-mail: cookrm@marlab.ac.uk. Introduction Recent crises in the European fishing industry have attracted considerable public interest and prompted a number of independent enquiries into the causes of the problems (Anon., 2004a; RSE, 2004). While these enquiries have concluded that fishing is the main factor causing the decline of whitefish stocks such as cod and plaice, there remains a popular perception that environmental factors, such as climate change, are the main cause (Anon., 2004b; Schiermeier, 2004). Establishing a convincing link between the environment and population change is often difficult. Myers (1998), for example, found that most published relationships between recruitment and environmental parameters were not robust and tended to break down when data from additional years in the time-series were added. Where correlations between recruitment and the environment are discovered, the mechanism driving the relationship is usually a matter of speculation. Temperature is known to affect the biology of fish (Brander, 1995). Some important stocks, including North Sea cod (Gadus morhua) andplaice(pleuronectes platessa), produce fewer recruits in years when winter sea surface temperature is warm (Planque and Frédou, 1999; van der Veer and Witte, 1999; O Brien et al., 2000; Clark et al., 2003; Wegner et al., 2003), and this may be related to changes in plankton populations on which larval fish feed (Beaugrand et al., 2003). Hence, declining stock size might be expected if there is a warming trend in ocean climate. While there is a growing body of observations that links temperature to recruitment, it does not follow that long-term stock trends are driven by developments in temperature alone. Such trends need to be distinguished from the effects of spawning-stock biomass (SSB), since the size of the spawning stock will also affect the number of eggs produced. Trends in SSB depend on recruitment over time and the survival rate of juvenile and adult fish. In order to investigate the relative contribution of environment and fishing on stock trends, we examined the relationship between temperature and the production of recruits for a number of major demersal fish stocks in the North Sea, 1054-3139/$30.00 Crown Copyright Ó 2005 Published by Elsevier Ltd on behalf of International Council for the Exploration of the Sea. All rights reserved.
Implications of warming climate for the management of North Sea demersal fisheries 1323 then examined the productivity of the stocks at different fishing mortality rates. It appears that the implications of rising sea temperature are mixed. Some species show a positive temperature relationship and would be expected to benefit from a warming trend, while for others, a warmer regime means that the stocks will be less productive. However, despite showing lower productivity at higher temperatures, cod still appear capable of producing higher yields than have been achieved in recent years, even if the warmer climate experienced since the 1990s continues. Source data Temperature data were taken from the International Bottom Trawl Survey (IBTS) (ICES, 2002a) for the period from 1970. The data are sea surface temperatures from 10 stations distributed throughout the North Sea obtained during February and March each year (Figure 1). For earlier years (1957e1969), mean February sea surface temperatures were taken from the ICES hydrographic database for the same rectangles as the IBTS. Spring coincides with the onset of spawning for the demersal stocks, and temperature may 60 N 55 N 0 5 E 10 E therefore measure an environmental state that influences the survival rate of the earliest life stages of these fish. The relationship between temperature and recruitment was examined for six North Sea fish stocks, cod, haddock (Melanogrammus aeglifinus), whiting (Merlangius merlangus), saithe (Pollachius virens), plaice, and sole (Solea solea). Catch, recruitment, and spawning-stock biomass data were taken from the reports of the Advisory Committee on Fishery Management (see Table 1). Estimates of population-related quantities are based on the analysis of the age compositions of catch and survey data (Darby and Flatman, 1994; Shepherd, 1999). Data for maturity, mean weight-at-age, natural mortality-at-age, and the fishing selection pattern used to estimate equilibrium yields and SSB were taken from the relevant ICES Working Groups (Table 1). Methods The temperature data for the 10 stations are highly correlated. To reduce redundancy, a unified temperature index was derived for the North Sea by performing a factor analysis on the individual station data using methods that allow for missing data (Little and Rubin, 1987). A single factor analysis was performed and the factor scores estimated using Bartlett s method (Bartlett, 1938). The factor scores were then used as the temperature index. This procedure is very similar to performing a principal component analysis and taking the first component scores as the index. Most of the variation in the data (about 80%) is accounted for by the first principal component, so the factor scores are likely to be an index that reflects the common signal in the individual station data. The relationship between recruitment, R, and SSB was modelled using a standard Ricker function (Ricker, 1954). Although there are many other standard models, the Ricker formulation (Needle, 2002) has the advantage of having few parameters while still encompassing a range of shapes. It is therefore a useful general purpose model for applying a consistent approach to a range of stocks. The parameters of the stock-recruit model were estimated by fitting a modified model, which incorporates Table 1. Data sources used in the analysis. Recruitment is in millions of fish and SSB is in thousands of tonnes. Stock Stock summary data source Stock biological data source 50 N Figure 1. Temperature sampling stations for the IBTS in the North Sea used in the calculation of the temperature index. Cod ICES, 2003a ICES, 2003b Haddock ICES, 2003a Not used Whiting ICES, 2002b Not used Saithe ICES, 2003a ICES, 2003b Plaice ICES, 2003a ICES, 2003b Sole ICES, 2003a ICES, 2003b
1324 R. M. Cook and M. R. Heath a temperature component, T (Stocker et al., 1985; Planque and Frédou, 1999; Clark et al., 2003). 0.8 Haddock RZaSSBe ðctÿssb=bþ ð1þ where R is recruitment, and a, b, and c are model parameters. The model was fitted assuming gammadistributed errors using GenStat, which also provided an estimate of the precision of these parameters. In order to investigate the importance of temperature at different rates of fishing, we calculated an equilibrium SSB and an equilibrium yield for a range of fishing mortality rates, F, for two temperature regimes using a standard agestructured production model, as described by Shepherd (1982) and Cook (2000). This assumes fixed rates of natural mortality, growth, age-at-maturity, and fishing selection pattern. Temperature may affect all of these quantities either directly or indirectly. However, the effect is likely to be complex, and it cannot be assumed, for example, that rising temperature will inevitably result in faster growth since food availability may also be affected. The default assumption of fixed biological characteristics, therefore, may have to be modified in the light of subsequent new evidence and may alter the overall conclusions. Results Table 2 shows the fitted parameter values from the stockrecruitment model and an estimate of their variance. The temperature coefficient, c, is significantly different from zero and positive for saithe but negative for cod, plaice, and sole (Figure 2). There is some indication of a positive statistically significant effect for whiting. No temperature effect is discernible for haddock. Figure 3 shows the temperature index, T, plotted by year since 1957. From 1988 onwards, the index is predominantly positive, while in earlier years it is typically negative. If the recent warming period continues as suggested by climate models (Gordon et al., 2000; Pope et al., 2000), stocks with a negative relationship with temperature might be expected to support smaller fisheries. In order to investigate the potential effects of temperature on these stocks, we used the fitted stock-recruit model to calculate expected Maximum Table 2. Fitted parameter values (a, b, and c) and their standard errors (s.e.). Parameter value 0.4 0-0.4-0.8 Cod Saithe Plaice Sole Whiting Figure 2. The confidence interval for the temperature coefficient, c, for each of the six stocks. Stocks for which the value of c is significantly different from zero show evidence of a temperature related effect. Sustainable Yield, MSY, SSB, and the fishing mortality rate at MSY, F msy. We considered two temperature regimes, one with a mean temperature index over the period 1957e1987 of ÿ0.37 and the other with a mean index from 1988 to 2001 of 0.7. The scaling of the index means that the temperature difference between the two regimes is about 1(C. In view of the depleted state of some stocks, we also calculated the equilibrium SSB for the stock if fished at the maximum safe fishing mortality rate, F pa,as defined by the International Council for the Exploration of the Sea (ICES, 2003a). Figure 4 shows the ratio of MSY in the cold regime to MSY in the warm regime and similarly for F msy. The warmer regime leads to much lower values at MSY for cod, plaice, and sole, but an increase for saithe. For the warmer regime, the figure also shows the ratio of the equilibrium biomass at F pa to the minimum safe biomass, B pa, defined by ICES. This ratio is less than one for cod, plaice, and sole, which indicates that, in the prevailing temperature regime, these stocks cannot reach their minimum safe level unless they are fished well below F pa. It means that the pa values, calculated by ICES on the full historical time-series may be too demanding, especially where these values form rebuilding targets within stock recovery plans. Year range a a(s.e.) b b(s.e.) c c(s.e.) R 2 Cod 1963e2001 4.52 0.85 246.30 71.20 ÿ0.24 0.08 47 Saithe 1967e1999 2.65 0.42 339.90 68.90 0.16 0.08 16 Plaice 1957e2002 4.32 1.06 273.80 60.50 ÿ0.19 0.05 26 Sole 1957e2001 6.80 1.87 54 842.00 14 328.00 ÿ0.26 0.11 11 Haddock 1963e2001 372.50 180.70 445.34 296.90 0.06 0.28 0 Whiting 1960e1998 7.33 1.76 1994.00 1351.00 0.12 0.08 29
Implications of warming climate for the management of North Sea demersal fisheries 1325 Temperature Index 3.00 2.00 1.00 0.00-1.00-2.00-3.00 Discussion 1957 1960 1963 1966 1969 1972 1975 1978 1981 1984 1987 1990 1993 1996 1999 Figure 3. The temperature index, T, plotted against time. The lower productivity of some stocks in a warmer regime does not necessarily mean that their dependent fisheries are jeopardized. In the case of cod, for example, the yield at MSY is potentially larger during a warm period than the mean catch realized in recent years (Figure 5). This is because for many years the stock has been fished well beyond F msy, and this has contributed to the depletion of the stock. Provided the stock can recover from its present low biomass, there is potential for a much larger fishery. Recovery will require a substantial reduction in fishing mortality rate from the typical historical values, which were close to 0.9. More recent values have been in the region of 0.75 (ICES, 2004), but this is unlikely to be low enough to ensure recovery. There has been some rebuilding of the spawning biomass in the most recent years, and this will assist in increasing the probability of better recruitment, which is also required to support improvements in stock biomass. The situation is not optimistic for the flatfish. For these two stocks, fishing mortality in the past has been only slightly above F msy, which means that the downward revision of F msy for a warmer regime implies yields below those observed in recent years. Ratio 2.00 1.50 1.00 0.50 Fmsy MSY B(Fpa)(h)/Bpa 0.00 Cod Saithe Plaice Sole Figure 4. The ratio of F msy (solid) and Maximum Sustainable Yield, MSY (hatched), at the higher temperature regime (h) to the same quantity at the lower temperature regime. The open bars show the ratio of the equilibrium biomass at F pa calculated for the higher temperature regime (h) to the value of B pa used by ICES. [000t] 350 300 250 200 150 100 50 0 Cod Saithe Plaice Sole MSY(h) mean catch Bmsy(h) Figure 5. The values of MSY and B msy for the warmer temperature regime (h); shown for comparison is the mean catch (1988e2001), the period of the warmer regime. While these results have important implications for stock recovery and future productivity, it is important to put them in context. It should be noted that the modelled recruitment response is mainly related to annual temperature anomalies. These probably act as a proxy for different aspects of ecosystem variability compared with underlying decadalscale variability. The latter reflects the global warming signal identified by the IPCC climate change models and latitudinal shifts in plankton species diversity identified by Beaugrand et al. (2002). Fundamental changes to the North Sea ecosystem would be expected with largely unknown consequences for most commercial fish stocks. In contrast, interannual variability can be regarded as essentially stochastic and driven by year-to-year differences in, for example, storm events. One might expect fish stocks to react differently to these two aspects of ecosystem variability. For example, decadal changes would be expected to cause chronic effects such as faster growth and earlier maturation, both of which would offset lower productivity produced by the effect of annual temperature anomalies on recruitment. These uncertainties make it difficult to make stock projections with any confidence. Nevertheless, there are reasons to believe that a sustainable fishery is possible even with the relatively warm temperature regimes observed in the last decade. However, current precautionary biomass reference points may not be achievable at the fishing mortality rate threshold (F pa ) established during earlier decades when the climate conditions were more favourable. ICES precautionary values may have been calculated during a period of favourable recruitment and therefore may not reflect the true productivity of the stock (Daan et al., 1994). The Report of the UK government Strategy Unit (Anon., 2004a) concluded that one requirement for a sustainable future for the whitefish industry is reduced fleet capacity. The analysis supporting this finding did not consider saithe and, contrary to our findings, assumed that the effect of temperature on sole was positive. Our results do not necessarily alter the Strategy Unit conclusions, but they do serve as a reminder that major restructuring needs to be pursued with care in the light of substantial uncertainties.
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