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Temperature and the recruitment of Atlantic cod
(Gadus morhua)1
B. Planque and T. Frédou

Abstract: Variability in the recruitment of fish has been attributed to either changes in the environment or variations in
the size of reproductive stocks. Disentangling the effects of environment and stock has proven to be problematic and
has resulted in recurrent controversy between studies supporting either hypothesis. In the present study, we examine the
relationship between interannual changes in temperature and variation in recruitment for nine Atlantic cod (Gadus
morhua) stocks in the North Atlantic. We show that for individual stocks, the relationship often appears weak and
statistically not significant. On the other hand, by combining in a single metaanalysis the results from individual
stocks, we demonstrate that recruitment of Atlantic cod is linked to interannual fluctuations in temperature in such a
way that for stocks located in warm water the relationship is negative, for stocks located in cold water the relationship
is positive, and there is no relationship for stocks located in the middle of the temperature range.

Résumé : La variabilité du recrutement des populations nectoniques a été attribuée, tantôt aux changements de
l’environnement, tantôt aux variations de la taille du stock reproducteur. La séparation des effets environnementaux de
ceux liés aux stocks demeure problématique et a provoqué une contreverse entre les études appuyant l’une ou l’autre
des deux hypothèses. Nous présentons ici, une étude des effets de la température sur le recrutement de neuf stocks de
morue franche (Gadus morhua). Nous montrons que pour chaque stock pris séparément, la relation du recrutement avec
la température apparait généralement faible et souvent non significative du point de vue statistique. En revanche,
l’analyse combinée des neuf stocks permet de démontrer qu’une telle relation existe à l’échelle du bassin nord-
Atlantique. Les variations du recrutement sont positivement liées aux changement de température dans les eaux froides,
négativement dans les eaux chaudes et aucun lien entre le recruitment et la température n’est observé dans les eaux
Planque and Frédou 2077

Introduction For example, experimental work has demonstrated that tem-
perature affects reproductive potential (Van Der Kraak and
Variability in fish recruitment has been attributed to either Pankhurst 1996), timing of spawning (Kjesbu 1994), embry-
changes in the environment or variations in the size of repro- onic and larval development (Rombough 1996), and growth
ductive stocks. Disentangling the effects of environment and (Solberg and Tilseth 1987). In addition, field observations
spawning stock has proven to be problematic because of the have confirmed the effects of temperature on adult growth
small amount of data generally available, combined with a (Brander 1995), timing of spawning (Hutchings and Myers
high degree of variability of this data. This has resulted in 1994a), and migration patterns (Rose et al. 1994). However,
persistent controversy between studies supporting either hy- strong evidence of environmental control on recruitment op-
pothesis, particularly because of their implications for fisher- erating in the wild is still sparse. Many of the environment–
ies management strategies.
recruitment relationships proposed have been criticised for
Biological research suggests that a number of environ-
several reasons: first, because by scrutinising many environ-
mental factors influence life history processes (e.g., see re-
mental factors (exploratory analysis), one would ultimately
view by Brander 1997) and recruitment-related processes.
find a relationship that is statistically significant but proba-
bly spurious and, second, because many of the relationships
Received March 3, 1999. Accepted June 18, 1999. that were significant in first analysis have been rejected
J15044 when retested with additional data (e.g., see Frank 1997 and
Myers 1998). Yet, from these many attempts to relate re-
B. Planque.2 Centre for Environment, Fisheries & cruitment variations to environment, one generalisation ap-
Aquaculture Science, Lowestoft Laboratory, Pakefield Road,
pears to stand out: in most cases, correlations for stocks
Lowestoft, Suffolk NR33 0HT, U.K.
T. Frédou. Centre for Environment, Fisheries & Aquaculture located at the limit of the species’ geographical distribution
Science, Lowestoft Laboratory, Pakefield Road, Lowestoft, remain significant after retesting.
Suffolk NR33 0HT, U.K., and School of Biological Sciences, Atlantic cod (Gadus morhua) has provided one of the ma-
University of East Anglia, Norwich, Norfolk NR4 7TJ, U.K. jor North Atlantic fish resources, and its fisheries can be
©British Crown Copyright 1999. Reproduced with the traced back to the very early days (see Kurlansky 1997). The
permission of the Controller of Her Majesty’s Stationery species has been more intensively studied than any other
Office. marine fish species (Brander 1997). Cod stocks are found
Author to whom all correspondence should be addressed. around the North Atlantic margin from Georges Bank to
e-mail: west of Greenland in the western North Atlantic and from

Can. J. Fish. Aquat. Sci. 56: 2069–2077 (1999) © 1999 NRC Canada

Monday, November 01, 1999 10:47:04 AM

prior to study- gests that these effects of temperature can be detected for ing the possible connection between environment and recruitment. and these fluctuations will con- updated for the Irish Sea by Planque and Fox (1998).8 Faeroes (ICES Vb) 1961–1994 2 7. For each model that can be fitted to a specific stock. differences between these series are study. tion on stock and recruitment at low values is rare. Myers 1997). However. In consequence. 1992) and established in practice (Myers and Barrowman 1996).vp Monday. The SSB fluctuates between years. The distribution of the species encompasses a wide 1995 and internet site http://www. 56. By this ap. November 01. Second. the nature of the temperature–recruitment relationship from although in theory the level of recruitment is dependent on stock cold to warm waters. the data are generally highly scattered level of recruitment is related to the size of the reproductive around the theoretical stock–recruitment curve. ways considered data on recruits for the youngest age available. production. Instead. be- © 1999 NRC Canada J:\cjfas\cjfas56\CJFAS-11\F99-114. but this assumption can be violated (see the case of bines the results from all individual stocks. there has not yet been a study cruitment is evident from the theory (e. (NAFO) analyses and provided by R. This can be done by calculating the recruitment residuals from a tionships between recruitment and temperature varied be- fitted stock–recruitment model. Third. In geographical distribution of stocks before performing the analysis. for stocks located in cold It is commonly accepted that recruitment is linked to the level of water the relationship is positive.4 Georges Bank (NAFO 5Z) 1977–1995 3 8 North Sea (ICES IV) 1960–1992 1 8. and there is no relationship eggs spawned. generally referred to as the spawning stock biomass (SSB).ca/~myers/welcome. SSB–recruitment models such as Beverton–Holt or Ricker contain we reexamine the temperature–recruitment relationship of the implicit assumption of proportionality between SSB and egg nine Atlantic cod stocks and develop a method that com.dal. tribute to changes in recruitment levels. The selection of stocks. raw re- Data on the number of recruits for nine stocks around the North cruitment estimates were used for each stock studied. Here. so that the adequacy proach. the num- stock. so that the rowman 1996. Fish. determining the precise form of the stock–recruitment relationship Recently. Northeast Arctic cod in Marshall et al. literature review on Atlantic cod stocks by Ottersen (1996). 1998). By doing Atlantic were taken from International Council for the Exploration this. bottom temperature ranging from an average of 2 to 11°C In the virtual population analysis procedure. the recruitment Recruitment series were not corrected for stock fluctuations. the methods used to establish rela. tween temperature and recruitment across the North Atlantic. these different series may produce different results. We have al- In the present study. Mean bottom temperatures are from Brander (1995). ment of Atlantic cod is affected by interannual changes in The length of recruitment series and age of recruits varied among temperature in such a way that for stocks located in warm the nine stocks studied and are summarised in Table 1.6 Irish Sea (ICES VIIa) 1968–1995 0 10 Celtic Sea (ICES VIIf–VIIk) 1970–1995 1 11 Note: Standard ICES and NAFO geographical areas for fisheries statistics are given in parentheses. see Hilborn and Walters that has analysed in a comparable way the relationship be. the application of metaanalysis to the study of in the case of individual stocks remains a difficult task.html). First. multiple series of recruitment resid- It should be noted that the present work is not an exploratory ual can be derived. Sci. we test the hypothesis that recruit. the Celtic Sea to the Barents Sea in the eastern North Atlan. with stocks distributed in waters with Recruitment data were derived from virtual population analysis. tween studies. and because a large range of models can be fitted. using a similar strategy. levels. This is for stock–recruitment relationships has demonstrated that the several reasons. which in turn is related to the size of the mature for stocks located in the middle of the temperature range. sug. Of course. consequence. it was assumed that the stocks have not reached such a low of the Sea (ICES) or Northwest Atlantic Fisheries Organisation level that they cannot produce a strong year-class. A stock. we can test for the existence of a gradual change in of the SSB–recruitment model can be questioned.A. changes in recruitment itself. the choice of a particular fit of SSB–recruitment may corrupt the results of the analysis. and for some stocks. a time se- Materials and methods ries of recruitment residuals can be calculated. Vol. distinct studies produced Although the existence of a relationship between stock and re- contradictory results.mscs. However. Summary of the data on Atlantic cod recruitment used in the present study. tic.. shape of the curve close to the origin is not known precisely.g. Aquat. despite the apparent lack of statistical significance ber of years of data is limited (rarely above 40) and the informa- when stocks are considered independently (Myers and Bar. 1999 Table 1. 1999 10:47:05 AM . the number of recruits (Brander 1995). Age of Mean bottom Stock Years recruits (years) temperature (°C) Newfoundland (NAFO 2J–3KL) 1959–1989 3 2 West Greenland (NAFO 1) 1952–1989 3 3 Northeast Arctic (ICES II) 1951–1990 3 4 Iceland (ICES Va) 1951–1993 3 5. there is in practice a large degree of uncertainty when esti- mating a particular model of the stock–recruitment relationship. J. but when compared with environ- and years of data was done on the basis of availability and known mental data. For this reason. Temperature was the only environmental parameter tested only due to the choice of the SSB–recruitment model and not to for correlation with recruitment. it seems appropriate to correct recruitment data for SSB changes. water the relationship is negative.Color profile: Disabled Composite Default screen 2070 Can. regions. is back-calculated using data on the structure of the population measured by fisheries statistics and research surveys. range of temperature. Myers (see Myers et al. some stocks. Also. Therefore.

increasing number of months. (1998) and by a comparison ral heterogeneity. COADS contains sea surface temperature (SST) month is analogous to a correlation coefficient and varies from –1 in the form of monthly summaries in boxes of 2 × 2° and covers (negative autocorrelation) to +1 (positive autocorrelation).g. the analysis. tions for temperature in each region. First. the above assumption can be violated in some cases. November 01. Areas are indicated by thick boxes and are named. degree of persistence of temperature anomalies. for which temperature series were extracted.vp Monday. who showed that where am. sure the interannual variability in temperature is to compare tem- cades. Third. these anomalies may show spatial heterogeneity with temperature profiles from ICES (Frédou 1998). Second. 1. cause Atlantic cod has been heavily exploited during the past de. Location of the areas and subareas for which SST series were selected. The values of the correlation co- Before comparing changes in recruitment with changes in tem. as shown by Ottersen et al. one year may have had a Temperature warmer summer that was compensated by a cooler winter).” One of the most common ways to mea. the following ones. 1999 10:47:10 AM . as in ied. Figure 1 indicates the areas and subareas variability in temperature. These functions indicate the the time series have to be consistent and sufficiently long to per. the series will First. two years with similar annual temperature may display important seasonal differences (e. The adequately the area of distribution of eight of the nine stocks stud. the data available from COADS were too Wei (1990). (1998). environmental temperature does not strictly correspond to “ambi. Subareas are delimited by thin lines and are numbered. higher temperature in warm years and vice versa.y – t m• tion.y is the anomaly for a given month m and a given year y. (1) am. will be discussed further. efficients are given as an indication of heterogeneity but were not perature.Color profile: Disabled Composite Default screen Planque and Frédou 2071 Fig. This last point has been largely discussed in the case of the Northeast Arctic cod by Ottersen et al. tm. To as- The temperature data suitable for comparison with Atlantic cod sess how temperature anomalies are transferred from one month to recruitment series have to fulfill several requirements.. In the Barents Sea.y = tm. sparse and we used instead the temperature series of the Kola sec- tion (Tereshchenko 1996). 1987). we have constructed the autocorrelation func- perature time series have to be available for every stock. In the same way that temperature anomalies can display tempo- chronous. so that they at the subregional scale. the autocorrelation function (ACF) was calculated by com- A temperature data set that fulfills most of these requirements is paring the original anomalies series with the same series lagged by the Comprehensive Ocean–Atmosphere Data Set (COADS) (Wood. When comparing the © 1999 NRC Canada J:\cjfas\cjfas56\CJFAS-11\F99-114. Second. the monthly temperature anomalies were derived from the preferably correspond to large oceanic areas rather than to single original series as follows: sampling points so that they can be representative of the change in temperature experienced by the stocks over their area of distribu. This perature values averaged over the months January–December. However. The fluctuations in temperature of the Spatial heterogeneity Kola section and of other areas in the Barents Sea are almost syn. ent” temperature. although the population generally experiences and tm • is the temperature for month m averaged over all years. it is necessary to define what is meant by “interannual tested for significance. The ACF value calculated for each ruff et al. tem. When areas were large enough to perform are comparable with COADS data in other regions. ACF was calculated for each region from lag 1 to 24 months. form the analysis over a number of years. we assessed the degree of spatial heterogeneity by measuring the Pearson correlation coefficient between temperature Temporal heterogeneity anomalies time series in subareas.y is the original temperature record for the same month and year.

The in some of the recruitment and temperature time series. 1999 Table 2.. we ranked the 250 values of each distribution and correlation over the standard parametric one is that the resulting subsampled 10% of the values at regular intervals. West Greenland.) ature was permuted (i.21 0. the p values used are also one-sided. we have used the slope of the regression line β as a mea- sure of the temperature–recruitment relationship and have tested The recruitment estimates were log2 transformed prior to the whether this slope varies from being positive in cold waters to be- correlation and regression analyses. 1999 10:47:10 AM . while the regression analysis was used to esti. The regression analysis was performed using the method of Spatial and temporal heterogeneity in regional Kendall and Gibbons (1990) given in Sokal and Rohlf (1995). The N2 can sometimes be greater than N (when autocorrelation is negative) and Results in such a case. pothesis. there was no permutation of individual slope values between distributions). Table 2 gives the Pearson correlation coefficients be- increase of 1°C in temperature is associated with a twofold in.e.83 0. The permutation was performed on posed by Quenouille (1952): the mean bottom temperature in such a way that each empirical distribution was kept unchanged but the associated bottom temper- (2) N2 = N/(1 + r1 + r1′ + r2 + r2′ +. The connection between temperature and recruitment was Atlantic cod to the other. conversely a value of –1 shows that a similarity in temperature time series within regions. ships but rather whether the relationship between recruitment and riod encompasses the spawning season for all the stocks consid. Because autocorrelation exists this had no detectable effect on the final correlation value). As temperatures for the nonparametric correlation.26 6 –0. and so on. and Newfoundland areas.. the signifi- Spearman rank correlation was calculated on the resulting 225 val- cance of the correlation can be biased due to overestimation of the ues (25 times nine stocks).55 0.Color profile: Disabled Composite Default screen 2072 Can. It should be noted that because where N2 is the adjusted sample size. we have studied the temperature–recruitment single stocks relationship across all Atlantic cod stocks in a single analysis. One of the advantages of the nonparametric lated.45 3 0.06 5 0. The connection between tem- perature changes and recruitment levels can be interpreted directly Sea. since this pe.16 4 0. we have always selected temperature Connection between temperature and recruitment for averaged over the entire region (i.20 0. r2 esis (β should decrease with increasing temperature). correlations were calculated as in Wei (1990) and only the autocorrelation at 1-year lag was taken into account. To test this hy- temperature increase or decrease. 56. for regions covering sufficiently large oceanic areas: North sion curve is not affected by outliers. Therefore.19 –0. a factor of 2. indicating that interannual temperature changes in the differ- © 1999 NRC Canada J:\cjfas\cjfas56\CJFAS-11\F99-114. the original sample size (N) was kept. Sci. It is also expected that for stocks not lo- ship for each stock. Icelandic Sea. Therefore. all the correlation values are positive and high.82 0.62 0. Fish. normality in temperature or recruitment data is from 250 to 25 for computational purposes (we later tested that not required to perform the analysis.02 0.03 0.27 0. Also. the statistical and r2′ are the 2-year-lag autocorrelations. 1 1 2 3 4 5 2 0.28 0. we have selected this approach. To do so. ative at the warm limit. The correla- resampling the residuals from the regression 250 times for each tion between interannual temperature changes and recruitment was stock. we have reestimated the empirical distribution estimated by a Monte-Carlo permutation number of degrees of freedom using the general correction pro- procedure (5000 permutations). Here. one does not test the significance of single relation- anomalies averaged over the months February–June.39 0.82 0. not the subareas). Then the Spearman rank correlation coefficient between em- determined for all stocks using the nonparametric Spearman rank pirical distributions of β and mean bottom temperatures was calcu- correlation coefficient..e.92 0. These coefficients indicate the degree of crease in recruitment. 1. November 01.69 0.65 0. The coefficient was tested against its number of degrees of freedom. In the similar temperature change is linked to a decline in recruitment by North Sea. tween subareas. N is the original sample size. In When comparing recruitment and temperature. This was performed by despite large differences in mean recruitment levels. The uncertainty in the regression slope used to stabilise the variance and to transform absolute changes in β was assessed by estimating the empirical distribution of β using a recruitment into relative changes so that all stocks are comparable bootstrapping procedure (Efron 1979). The log transformation was ing negative in warm ones.72 –0.20 Note: The subareas are defined in Fig. and. recruitment with temperature.03 –0.. The aim of that coefficient is not influenced by outliers that are often present in bi- procedure was to reduce the number of data in each distribution ological data. 1 West Greenland. West Greenland. Aquat. the nonparametric regression Spatial heterogeneity in temperature series was assessed does not require normality of the data and the slope of the regres.vp Monday.77 0. The correlation is positive at the cold limit of the temperature distribution and neg- analysis was used to test the statistical significance of the relation. combined stocks In addition to analyses of temperature–recruitment relationship for Connection between temperature and recruitment for each individual stock. Iceland. we hypothesise that the relationship measured by correlation and regression analyses. we have a prior expectation on the nature of the alternative hypoth- r1 and r1′ are the 1-year-lag autocorrelations of the two series.89 0. cated at the edge of the temperature distribution. The temperature anomalies for each year are calculated over the months of February–June. and Newfoundland wa- from the slope of the regression (β): a slope of +1 indicates that an ters. The auto. Vol. test is one-sided.71 0. there will be no mate the degree to which recruitment changes in relation to a 1°C relationship between temperature and recruitment. J. Correlation between temperature time series from distinct subareas in the North Sea. temperature varies from one end of the temperature distribution of ered.82 0. North Sea Newfoundland 1 2 3 4 Iceland.

For Iceland and values for the first four lags are generally higher in the east- West Greenland. In the case of the Newfoundland region. Relationships between SST and Atlantic cod recruitment perature vary considerably within the Newfoundland area. November 01. Note the persistence of temperature anomalies over 5-month periods that recruitment anomalies for West Greenland are plotted on a (such as the February–June period selected for comparison with distinct scale due to the higher variability in recruitment in this recruitment data).58 25 21 plays a sharp decrease and is already close to zero at lag Note: ns.38* 0.98 33 32 similar. son between temperature and recruitment (see next section). late interannual changes in temperature is critical. 2.43 38 31 4 months. In New- are highlighted in the figure. the correlation at lag 1 month is the Iceland 0. recruitment varied by up to a factor of positive value and decreases towards zero. 3. Northeast Arctic 0.13 ns –0. lies in each region.05 ns –0. Regional connections between temperature and lected are much lower. as they correspond to the per. not significant. 1999 10:47:13 AM . Table 3 shows the correlation coefficient. even if based on a different set of months (warm Irish Sea –0. in the New- for each stock and N2 is the adjusted sample size estimated from the method of Quenouille (1952) (see Materials and methods section for foundland region the choice of the months retained to calcu- details).98 27 (29) winters generally coincide with warm springs. **p < 0.08 ns –0. which the temperature is averaged is critical to the resulting original and corrected sample size. The ACFs for the other regions display various patterns between the two extremes.05. region.54** –0. This indicates that interannual fluctuations in tem.92 40 31 In the Barents Sea.93) and it remains the highest when inte- Faeroes –0. For Newfoundland –0. ACF for the time series of monthly temperature Fig. but the level of correlation varies between stocks. The average correlation over the four lags is also indicated Stock r β N N2 as an index of persistence of the temperature anomaly. both cases the correlations are positive and high. The first four lags 1000 with temperature fluctuations of about 2°C. In New- foundland. Spearman correlation coefficient (r) and regression slope equivalent to the February–June period chosen for compari- (β) between temperature and log2 recruitment of Atlantic cod. It can be noted that the mean autocorrelation ent subareas have followed parallel patterns. For each area.). *p < 0.Color profile: Disabled Composite Default screen Planque and Frédou 2073 Fig. the autocorrelation dis- Celtic Sea –0. the amplitude of changes in temper- sistence of a temperature anomaly for a period of 5 months. often close to zero and sometimes recruitment negative.43 31 (33) all regions.41 43 35 highest (ACF1 = 0. etc.81). The lines correspond to the fit of a nonparametric 4 months (indicated by the solid circles) and is an indicator of regression (see Materials and methods section for details). In contrast with the Barents Sea. for each stock together with the linear regression fit.23 ns 1. the choice of area over rank correlation. ature is lower (<1°C) and recruitment varied by up to a © 1999 NRC Canada J:\cjfas\cjfas56\CJFAS-11\F99-114. Scatterplots of log2 recruitment of Atlantic cod against anomalies for the nine areas in the North Atlantic.vp Monday.42* 0. parametric regression for each stock.01 18 18 the interannual variability in temperature is likely to remain North Sea –0. N is the sample size 3 months. the ACF starts with a In West Greenland. the ACFs show a marked decline during the first West Greenland 0. Fig. only two subareas were compared and in ern than in the western part of the North Atlantic. and slope of the non- temperature time series.42* –0. cruitment anomalies plotted against temperature anomalies ure 2 shows the ACFs based on monthly temperature anoma.01.18 ns –0.02 34 26 grated over 4 months (ACF1–4 = 0. Parentheses in the N2 column indicate when N2 is greater than N. The value in temperature (February–June) for the nine stocks in the North parentheses is the mean autocorrelation value from lag 1 to Atlantic. foundland and Faeroes. This indicates that Georges Bank –0. It for the nine stocks have been assessed using Spearman’s also suggests that in this region. Figure 3 shows log2 re- Temporal heterogeneity was assessed for all regions. Table 3. correlation values between the five subareas se.

it is tions in recruitment despite a larger range in temperature reasonable to assume that the effect of temperature on the variation (about 4°C). we are left Discussion with the observation that for the Celtic Sea and Georges Bank stocks (stocks located at the warm limit) and for the In their demonstration of the relationship between stock West Greenland and Newfoundland stocks (cold limit) the and recruitment levels. Georges Bank. In this study. J. The data are stock (Hutchings and Myers 1994b. change: a positive relationship in cold waters. Faeroes. 4 that the northern cod stock (Newfoundland) stands out of this general pattern. as shown by the correlations in Table 2. however.vp Monday. In the case of the northern cod stock. several populations. First. 1999 Fig. BA. 2. several assump- tions were made: (i) the area over which temperature is aver- aged is representative of the area of distribution of the Atlantic cod stock. r = –0. CE.83 and the statistical significance is greatly improved Positive relationships (increase in Atlantic cod recruitment with p = 0. Sci. recommended that general hypotheses on recruitment should sults alone that a gradual change in the temperature–recruitment be tested with a similar approach. determined by a bootstraping procedure. it is often not possible to conclude that a Atlantic. West Greenland. using data sets from relationship does exist. Second. GB. tween β distributions and mean bottom temperature reaches and Iceland at p < 0.Color profile: Disabled Composite Default screen 2074 Can. It is clear. and (iii) recruitment has not been affected by exceptional forcing that would have masked the effects of temperature. Iceland. NS. This indicates that the null hypothesis (effect of temperature on recruitment is independent of mean temperature) can be rejected. FA. recruitment relationship was assessed by testing the exis- tence of a link between the regression line slope β and the mean bottom temperature of each stock. the estimate of β for the northern cod stock is tistical significance of the relationships is generally low (Ta- highly uncertain and it would be appropriate to treat this ble 3). The apparent trend is for β to be positive for stocks located in cold waters and gradually decrease to negative values for stocks in warm waters. there is a high degree of factor of 30. Vol. For each stock. the link is estimated by the slope of the relationship between temperature and recruitment exists. In the Celtic Sea. and the sta- consequence. These results show that interannual recruitment of Northern cod have been masked by the dra- changes in recruitment are generally large and that the am- matic reduction in SSB that preceded the collapse of the plitude of these changes varies among stocks. Figure 4 shows the distributions of β against the mean bottom temperatures. Aquat. Celtic Sea. and Newfoundland. correlations are not significant. it is difficult to conclude from the correlation re. Irish and the gradual change in the nature of the temperature– Sea. In also highly scattered around the regression lines.0016. The rank correlation between β distributions and mean bottom temperature is r = –0. (ii) the temperature anomaly signal does not vary substantially within the 5-month period over which it is averaged. as demonstrated in Fig. stock is removed from the analysis. ses fail to give significant answers. November 01. When performing the calculation of β . as expected. Boxes and lines indicate the 50 analysis is to combine the data from all stocks in a single and 95% limits of the empirical distribution of the slopes. Link between SST and recruitment plotted against mean tionships and (ii) for stocks located at the cold and warm bottom temperature for nine Atlantic cod stocks in the North temperature limits. For temperate waters the value of β is close to zero. North Sea.01. Barents Sea. IR. Newfoundland (northern cod). The stock of Georges Bank shows similar varia- intermonth variability. Fish. the rank correlation be- Correlations are significant in the North Sea. Stocks: NE. However. WG. West Greenland. Later. Myers and Barrowman (1996) illus- correlation analysis cannot reject the null hypothesis that no trated how powerful metaanalysis can be when single analy- relationship between temperature and recruitment exists. Third. IC.59 and the associated probability is p = 0. the spatial homogene- ity in temperature in this area is extremely low. from Fig. 4.027. Transatlantic connection Barents Sea (Northeast Arctic cod). whereas negative relationships are signifi- cant in the Irish Sea and North Sea.05 and in the Irish Sea at p < 0. we present a metaanalysis The conclusions of the stock-by-stock correlation analysis of data on nine cod stocks and show that the relationship are that (i) there is a high degree of scatter in the data that between temperature and recruitment follows a gradual results in difficulty in obtaining statistically significant rela. Faeroe Results from all stocks were combined in a single analysis Islands (Faeroes). 1997). When the northern cod Bank. 56. Myers et al. these three assumptions are violated. Georges stock separately from the others. transatlantic analysis. 1999 10:47:15 AM . no relation- © 1999 NRC Canada J:\cjfas\cjfas56\CJFAS-11\F99-114. at high temperature anomalies) are significant in the Barents Sea and Iceland. Myers (1998) Therefore. nonparametric regression (β from Table 3) represented by the One way to overcome the limitation of the above correlation horizontal line within the box.

For example. (1985): warm waters. Such short-term forecast. casts and actual surveys should raise questions about It has recently been observed that the changes in popula- possible changes in the population dynamics. Kjesbu temperature and recruitment could explain the unexpected et al. β. First. and T are recruitment. (1996) have showed that the intensity of spawning and strong year-class of North Sea cod in 1996. This mass. 4) was fitted using least squares nonlinear regression. The resulting model is a three-di- effects of the environment on recruitment should be stronger mensional surface (where SSB. lying mechanisms. monitoring SST is a rela. the extent of the spawning period vary with the size of indi- ciated with the rapid and extreme cooling of the North Sea vidual Atlantic cod. recruitment links described here and to understand the under- ment could exist independently of food-related control. In addition. It can be seen sions). if one can understand such ing is probably of limited value because assessment surveys mechanisms and identify which key processes are affected already produce recruitment estimates within a few months. spawning stock bio- significance of correlation analyses on single stocks. The stock–recruitment relationship is the core of current management procedures and is used to determine the level of fishing mortality that a stock can support and ultimately to advise on total allowable catch. The present study demonstrates the existence (4) R = SSB·e(α–β ·SSB)·e(Ψ·T). which was asso. it is unlikely that temperature–recruitment such knowledge. Although such time period and might therefore become more sensitive to © 1999 NRC Canada J:\cjfas\cjfas56\CJFAS-11\F99-114. Ottersen et al. agement strategies that will tend to maximise the recruit- ship. of a significant temperature–recruitment relationship despite the general pattern of apparent low (or lack of) statistical where R. In the Such information could be used to assess the impact of man- present study. within the range of observed values in the Irish Sea. respectively. see Hilborn and Walters 1992): (3) R = a·SSB·e–β ·SSB (or its equivalent form R = SSB·e(α–β ·SSB)) and include temperature in a form similar to that proposed ship in temperate waters. taking into account the link between (Marteinsdottir and Thorarinson 1998). The lines show the fit of a combined stock/temperature– agement. and a negative relationship in by Stocker et al. Figure 5 shows an example of such a fit for the Irish as a unifying factor for previous results from a number of Sea cod stock. recruitment forecasts would depend. Also. or the accuracy of recruitment esti. T. is only evident at the limit of Atlantic cod distribution.. Second.g.Color profile: Disabled Composite Default screen Planque and Frédou 2075 Fig. discrepancies between temperature-based fore. productivity in lower trophic levels (Rothschild 1994). It is It has been argued that temperature may not be directly clear that the fitted curves and particularly the slopes at the linked to recruitment but only acts as a proxy for marine origin vary greatly under the distinct temperature regimes. But forecasting recruitment is not the only way by which temperature information can be used for fisheries management.and long-term forecasts. tribution are associated with the fluctuations in recruitment mates. it has to be remembered that the fluctuations in temperature only account for a lim- ited fraction of the recruitment variability in an individual stock. so that the uncertainty associated with any prediction will be high. and α.to long-term forecasting spawn over a smaller geographical area and for a shorter of recruitment based on climate forecasts. cannot be demonstrated. For example. 1999 10:47:17 AM . it might be possible to design man- but it could be used as a test for the accuracy of the relation. and temperature. November 01. relationships will ever be used in fisheries management if tively easy task that could help in forecasting recruitment the mechanism by which temperature modulate recruitment levels several months in advance. In short. and R are the three dimen- at the limit of a species’ spatial distribution. one can build a stock–recruitment model from the Ricker model (e. From this observation. the link between temperature and recruitment agement strategies under various climatic scenarios. the nature of tion structure and particularly the reduction in age-class dis- environmental forcing. most of the stock– recruitment models do not currently include environmental factors when this could be easily achieved. Recruitment of Irish Sea cod plotted against SSB prediction would certainly be of great value to fisheries man- (points).vp Monday. position (and consequently reduced size composition) would One can also envisage medium. ment chances of a given population on a biological basis. 5. The model medium-range (10 years) climate predictions upon which the (eq. The modelled “surface” is plotted in the form studies that showed apparently contradictory results on the of three curves corresponding to three temperatures “slices” effects of temperature on Atlantic cod recruitment. and Ψ are the transatlantic relationship is consistent with the view that the associated coefficients. this idea finds its limits in the low accuracy of recruitment model for three distinct temperatures. This is particularly important for two rea- There are immediate applications that could be made of sons. Yet. SSB. by temperature changes. For example. (Loewe 1996) and the following poor year-class of 1997 (1994) have argued that populations with reduced age com- when warmer conditions prevailed. Biological research is needed to confirm the temperature– which suggests that direct effects of temperature on recruit.

Chambers and don. Associated measurements. C. Can. Bergen. Loeng. challenges of recruitment prediction. Hilborn. R. Sci. V. N. 55: 1372–1377. Chapman and Hall. Z. Norwich. Sci. 198: 471–481. M. 7: 1–26.A. Mar. ploited fish populations will display amplified responses to Marshall. probable that in the near future. Sci. and Thorarinson. Prog. 177–223. B. F. Ser. K.T. 451–467. 1994. ological Controls on Fish Stocks. thesis. Symp. Quantitative fisheries stock as. O. tion: interannual variability and the influence of temperature.D. Kjesbu.. pp.. E. This work was Myers. The authors wish to thank Dr.J. London. R..K.. J. 1987.J. J..W. Edited by R. Can. Sci. U. Cambridge University Press.S. 1985.K. Aquat. Ser. 495–512. Changes in distribution of Atlantic cod and thermal New York.W. B. Bishop. Varia. Acknowledgements Myers. U.. it is Loewe.J. Sci. Myers at Dal. London.J. J.. Sci. D. J. Cambridge. and Nakken.. 1998. Long-term changes in temperature and cod larval development. M. M. 1979. 7: 91–106. Frank. 55: 1766–1783. and Kulka.vp Monday. Hutchings. K. K. Butterworth. Sci.A. Environmental impact on variability in recruit- ment. and Myers.A. We are also greatly indebted to all the worldwide spawner and recruitment data. 1996. and the possible ways by which this could be done Marteinsdottir.. Kjesbu. among yolk-sac larvae of cod (Gadus morhua L. 2024. J. East Anglia. Timing of cod reproduc. 108: 21–31. Michalsen. 53: 610–620. Ø. Chapman and Hall. 94: 707–724. Edited by C. References Ph.S. and Gibbons. ences in rearing temperature and light regime. 1997. 72: 347–349..K. Chapman and Hall. ation and recruitment of Pacific herring (Clupea harengus pallasi) eter. Edited by R. Choice. J. Bootstrap methods.A. and Rohlf. Time of start of spawning in Atlantic cod Stocker. 174–180. Chambers and E. Mar. R. J. If such is the case. N. 198: 542–552. 1998. Cambridge. J.. ICES J. scientists at CEFAS who supported our efforts and com. 1996.M. 1998. pp. Seasonal and year-to-year variations of tion in annual egg production in individual captive Atlantic cod temperature and salinity along the Kola meridian transect. on the reproductive performance of fish. Lon- cruitment in fish populations. M. 1996..J. U. Can.C. The effects of temperature on embryonic and Frédou. 1999 10:47:18 AM . P. 52: 1–10. When do environment-recruitment correlations work? Rev. T. Ecol. Haist. London. In Early life history and recruitment ual stocks only.K. R.A. Physical and Bi.H.. Aquat. In Global warming: im- © 1999 NRC Canada J:\cjfas\cjfas56\CJFAS-11\F99-114.S. H. and Fox. Symp. 1997. A. 1994a.. M. Rep. 1996. Rothschild. Jonathan Cape. Effects of climate change on cod (Gadus Mar. and Myers. Tereshchenko.R. S. J..K. U. Hutchings. In Global warming: implications for freshwater Ottersen.S. Is fish recruitment related housie University for providing recruitment data and Steve to spawners abundance? Fish.A.G. Kjesbu. Fish Biol. Solemdal. Cambridge University Press. Edward Arnold.A. Baird. U.. In Global warming: implications for fresh- recruitment — a transatlantic study. N. Interannual variability in tempera- Ann. Ottersen. dynamics and uncertainty. G. T. O. Atkinson. 1980–1992.G. Sci. University of water and marine fish. Fish. Summary of providing SST data. J. Fish. J. 8: 285–305. J. 1994.M. Sarsia. P. larval growth and distribution of Arcto-Norwegian cod. What can be learned from Atlantic. another look at the jackknife. Fish. 1990. Ulltang.J. P. Quenouille. Ecol. and Fonn. Improving the stock– have not yet been fully explored. U. 1994. U. Influence of temper- tic cod (Gadus morhua L. Cod. Environmental vari- (Gadus morhua) females in relation to vitellogenic oocyte diam.A.G. N. Gadus morhua. B. R.A. in fish populations. Bratland. Sci. C. ICES (Gadus morhua). Vol. 1998. and Barrowman. 45: in the Strait of Georgia. 198: 333–345.. Bridson.. and environmental changes.M.A. 51: of statistics in biological research. Rombough. Appl. Decadal transients in biological productiv- Mar. The main difficulty will recruitment relationships in Icelandic cod (Gadus morhua) by likely be in reconciling results on temperature–recruitment including age diversity of spawners. 2126–2146.. 1996. 1995. G. V. 56.Color profile: Disabled Composite Default screen 2076 Can.. G. and Barrowman. and Raknes. A biography of the fish that changed the Van Der Kraak. O. Aquat.A. Sci. C. temperature. the collapse of a renewable resource? Atlantic cod. Aquat. and Fournier. Fish.. Recruitment variations in fish populations as- management strategies that take place at the level of individ- sessed using meta-analysis. Rank correlation methods. The utility of early life history studies and the 172: 101–105. Fish.A. Yaragina. Aquat. sessment. ICES Mar. Freeman and Co. 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