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Temperature and the recruitment of Atlantic cod

(Gadus morhua)1
B. Planque and T. Frdou

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.

Rsum : La variabilit du recrutement des populations nectoniques a t attribue, tantt aux changements de
lenvironnement, tantt aux variations de la taille du stock reproducteur. La sparation des effets environnementaux de
ceux lis aux stocks demeure problmatique et a provoqu une contreverse entre les tudes appuyant lune ou lautre
des deux hypothses. Nous prsentons ici, une tude des effets de la temprature sur le recrutement de neuf stocks de
morue franche (Gadus morhua). Nous montrons que pour chaque stock pris sparment, la relation du recrutement avec
la temprature apparait gnralement faible et souvent non significative du point de vue statistique. En revanche,
lanalyse combine des neuf stocks permet de dmontrer quune telle relation existe lchelle du bassin nord-
Atlantique. Les variations du recrutement sont positivement lies aux changement de temprature dans les eaux froides,
ngativement dans les eaux chaudes et aucun lien entre le recruitment et la temprature nest observ dans les eaux
tempres.
Planque and Frdou 2077

Introduction For example, experimental work has demonstrated that tem-

Variability in fish recruitment has been attributed to either
changes in the environment or variations in the size of repro-
ductive stocks. Disentangling the effects of environment and
spawning stock has proven to be problematic because of the
small amount of data generally available, combined with a
high degree of variability of this data. This has resulted in
persistent controversy between studies supporting either hy-
pothesis, particularly because of their implications for fisher-
ies management strategies.
Biological research suggests that a number of environ-
mental factors influence life history processes (e.g., see re-
view by Brander 1997) and recruitment-related processes.
Received March 3, 1999. Accepted June 18, 1999.
J15044
B. Planque.2 Centre for Environment, Fisheries &
Aquaculture Science, Lowestoft Laboratory, Pakefield Road,
Lowestoft, Suffolk NR33 0HT, U.K.
T. Frdou. Centre for Environment, Fisheries & Aquaculture
Science, Lowestoft Laboratory, Pakefield Road, Lowestoft,
Suffolk NR33 0HT, U.K., and School of Biological Sciences,
University of East Anglia, Norwich, Norfolk NR4 7TJ, U.K.
1
British Crown Copyright 1999. Reproduced with the
permission of the Controller of Her Majestys Stationery
Office.
2
Author to whom all correspondence should be addressed.
e-mail: b.planque@cefas.co.uk
perature affects reproductive potential (Van Der Kraak and
Pankhurst 1996), timing of spawning (Kjesbu 1994), embry-
onic and larval development (Rombough 1996), and growth
(Solberg and Tilseth 1987). In addition, field observations
have confirmed the effects of temperature on adult growth
(Brander 1995), timing of spawning (Hutchings and Myers
1994a), and migration patterns (Rose et al. 1994). However,
strong evidence of environmental control on recruitment op-
erating in the wild is still sparse. Many of the environment
recruitment relationships proposed have been criticised for
several reasons: first, because by scrutinising many environ-
mental factors (exploratory analysis), one would ultimately
find a relationship that is statistically significant but proba-
bly spurious and, second, because many of the relationships
that were significant in first analysis have been rejected
when retested with additional data (e.g., see Frank 1997 and
Myers 1998). Yet, from these many attempts to relate re-
cruitment variations to environment, one generalisation ap-
pears to stand out: in most cases, correlations for stocks
located at the limit of the species geographical distribution
remain significant after retesting.
Atlantic cod (Gadus morhua) has provided one of the ma-
jor North Atlantic fish resources, and its fisheries can be
traced back to the very early days (see Kurlansky 1997). The
species has been more intensively studied than any other
marine fish species (Brander 1997). Cod stocks are found
around the North Atlantic margin from Georges Bank to
west of Greenland in the western North Atlantic and from

Can. J. Fish. Aquat. Sci. 56: 20692077 (1999) 1999 NRC Canada

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Table 1. Summary of the data on Atlantic cod recruitment used in the present study.
Stock Years
Newfoundland (NAFO 2J3KL) 19591989
West Greenland (NAFO 1) 19521989
Northeast Arctic (ICES II) 19511990
Iceland (ICES Va) 19511993
Faeroes (ICES Vb) 19611994
Georges Bank (NAFO 5Z) 19771995
North Sea (ICES IV) 19601992
Irish Sea (ICES VIIa) 19681995
Celtic Sea (ICES VIIfVIIk) 19701995
Note: Standard ICES and NAFO geographical areas for fisheries statistics are given in parentheses. Mean
bottom temperatures are from Brander (1995).
the Celtic Sea to the Barents Sea in the eastern North Atlan-
tic. The distribution of the species encompasses a wide
range of temperature, with stocks distributed in waters with
bottom temperature ranging from an average of 2 to 11C
(Brander 1995).
In the present study, we test the hypothesis that recruit-
ment of Atlantic cod is affected by interannual changes 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. A
literature review on Atlantic cod stocks by Ottersen (1996),
updated for the Irish Sea by Planque and Fox (1998), sug-
gests that these effects of temperature can be detected for
some stocks. However, the methods used to establish rela-
tionships between recruitment and temperature varied be-
tween studies, and for some stocks, distinct studies produced
contradictory results. Also, there has not yet been a study
that has analysed in a comparable way the relationship be-
tween temperature and recruitment across the North Atlantic.
Recently, the application of metaanalysis to the study of
stockrecruitment relationships has demonstrated that the
level of recruitment is related to the size of the reproductive
stock, despite the apparent lack of statistical significance
when stocks are considered independently (Myers and Bar-
rowman 1996; Myers 1997). Here, using a similar strategy,
we reexamine the temperaturerecruitment relationship of
nine Atlantic cod stocks and develop a method that com-
bines the results from all individual stocks. By this ap-
proach, we can test for the existence of a gradual change in
the nature of the temperaturerecruitment relationship from
cold to warm waters.
Materials and methods
It should be noted that the present work is not an exploratory
study. Temperature was the only environmental parameter tested
for correlation with recruitment. The selection of stocks, regions,
and years of data was done on the basis of availability and known
geographical distribution of stocks before performing the analysis.
Recruitment
Data on the number of recruits for nine stocks around the North
Atlantic were taken from International Council for the Exploration
of the Sea (ICES) or Northwest Atlantic Fisheries Organisation
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Can. J. Fish. Aquat. Sci. Vol. 56, 1999
Age of Mean bottom
recruits (years) temperature (C)
3 2
3 3
3 4
3 5.8
2 7.4
3 8
1 8.6
0 10
1 11
(NAFO) analyses and provided by R.A. Myers (see Myers et al.
1995 and internet site http://www.mscs.dal.ca/~myers/welcome.html).
Recruitment data were derived from virtual population analysis.
In the virtual population analysis procedure, the number of recruits
is back-calculated using data on the structure of the population
measured by fisheries statistics and research surveys. We have al-
ways considered data on recruits for the youngest age available.
The length of recruitment series and age of recruits varied among
the nine stocks studied and are summarised in Table 1.
It is commonly accepted that recruitment is linked to the level of
eggs spawned, which in turn is related to the size of the mature
stock, generally referred to as the spawning stock biomass (SSB).
The SSB fluctuates between years, and these fluctuations will con-
tribute to changes in recruitment levels. Therefore, prior to study-
ing the possible connection between environment and recruitment,
it seems appropriate to correct recruitment data for SSB changes.
This can be done by calculating the recruitment residuals from a
fitted stockrecruitment model.
Although the existence of a relationship between stock and re-
cruitment is evident from the theory (e.g., see Hilborn and Walters
1992) and established in practice (Myers and Barrowman 1996),
determining the precise form of the stockrecruitment relationship
in the case of individual stocks remains a difficult task. This is for
several reasons. First, the data are generally highly scattered
around the theoretical stockrecruitment curve. Second, the num-
ber of years of data is limited (rarely above 40) and the informa-
tion on stock and recruitment at low values is rare, so that the
shape of the curve close to the origin is not known precisely. Third,
SSBrecruitment models such as BevertonHolt or Ricker contain
the implicit assumption of proportionality between SSB and egg
production, but this assumption can be violated (see the case of
Northeast Arctic cod in Marshall et al. 1998), so that the adequacy
of the SSBrecruitment model can be questioned. In consequence,
although in theory the level of recruitment is dependent on stock
levels, there is in practice a large degree of uncertainty when esti-
mating a particular model of the stockrecruitment relationship.
For each model that can be fitted to a specific stock, a time se-
ries of recruitment residuals can be calculated, and because a large
range of models can be fitted, multiple series of recruitment resid-
ual can be derived. Of course, differences between these series are
only due to the choice of the SSBrecruitment model and not to
changes in recruitment itself, but when compared with environ-
mental data, these different series may produce different results. In
consequence, the choice of a particular fit of SSBrecruitment may
corrupt the results of the analysis. For this reason, the recruitment
series were not corrected for stock fluctuations. Instead, raw re-
cruitment estimates were used for each stock studied. By doing
this, it was assumed that the stocks have not reached such a low
level that they cannot produce a strong year-class. However, be-
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Planque and Frdou
Fig. 1. Location of the areas and subareas for which SST series were selected. Areas are indicated by thick boxes and are named.
Subareas are delimited by thin lines and are numbered.
cause Atlantic cod has been heavily exploited during the past de-
cades, the above assumption can be violated in some cases. This
will be discussed further.
Temperature
The temperature data suitable for comparison with Atlantic cod
recruitment series have to fulfill several requirements. First, tem-
perature time series have to be available for every stock. Second,
the time series have to be consistent and sufficiently long to per-
form the analysis over a number of years. Third, the series will
preferably correspond to large oceanic areas rather than to single
sampling points so that they can be representative of the change in
temperature experienced by the stocks over their area of distribu-
tion. This last point has been largely discussed in the case of the
Northeast Arctic cod by Ottersen et al. (1998), who showed that
environmental temperature does not strictly correspond to ambi-
ent temperature, although the population generally experiences
higher temperature in warm years and vice versa.
A temperature data set that fulfills most of these requirements is
the Comprehensive OceanAtmosphere Data Set (COADS) (Wood-
ruff et al. 1987). COADS contains sea surface temperature (SST)
in the form of monthly summaries in boxes of 2 2 and covers
adequately the area of distribution of eight of the nine stocks stud-
ied. In the Barents Sea, the data available from COADS were too
sparse and we used instead the temperature series of the Kola sec-
tion (Tereshchenko 1996). The fluctuations in temperature of the
Kola section and of other areas in the Barents Sea are almost syn-
chronous, as shown by Ottersen et al. (1998) and by a comparison
with temperature profiles from ICES (Frdou 1998), so that they
are comparable with COADS data in other regions.
Temporal heterogeneity
Before comparing changes in recruitment with changes in tem-
perature, it is necessary to define what is meant by interannual
variability in temperature. One of the most common ways to mea-
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2071
sure the interannual variability in temperature is to compare tem-
perature values averaged over the months JanuaryDecember.
However, two years with similar annual temperature may display
important seasonal differences (e.g., one year may have had a
warmer summer that was compensated by a cooler winter). To as-
sess how temperature anomalies are transferred from one month to
the following ones, we have constructed the autocorrelation func-
tions for temperature in each region. These functions indicate the
degree of persistence of temperature anomalies.
First, the monthly temperature anomalies were derived from the
original series as follows:
(1) am,y = tm,y t m
where am,y is the anomaly for a given month m and a given year y,
tm,y is the original temperature record for the same month and year,
and tm is the temperature for month m averaged over all years.
Second, the autocorrelation function (ACF) was calculated by com-
paring the original anomalies series with the same series lagged by
increasing number of months. The ACF value calculated for each
month is analogous to a correlation coefficient and varies from 1
(negative autocorrelation) to +1 (positive autocorrelation). The
ACF was calculated for each region from lag 1 to 24 months, as in
Wei (1990).
Spatial heterogeneity
In the same way that temperature anomalies can display tempo-
ral heterogeneity, these anomalies may show spatial heterogeneity
at the subregional scale. When areas were large enough to perform
the analysis, we assessed the degree of spatial heterogeneity by
measuring the Pearson correlation coefficient between temperature
anomalies time series in subareas. The values of the correlation co-
efficients are given as an indication of heterogeneity but were not
tested for significance. Figure 1 indicates the areas and subareas
for which temperature series were extracted. When comparing the
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Table 2. Correlation between temperature time series from distinct subareas in the North Sea, Iceland, West Greenland,
and Newfoundland areas.
North Sea
1 2 3 4 Iceland, 1
2 0.83 0.69
3 0.89 0.92
4 0.55 0.82 0.72
5 0.62 0.77 0.82 0.82
6 0.19
Note: The subareas are defined in Fig. 1. The temperature anomalies for each year are calculated over the months of FebruaryJune.
recruitment with temperature, we have always selected temperature
averaged over the entire region (i.e., not the subareas).
Connection between temperature and recruitment for
single stocks
When comparing recruitment and temperature, we have selected
anomalies averaged over the months FebruaryJune, since this pe-
riod encompasses the spawning season for all the stocks consid-
ered. The connection between temperature and recruitment was
measured by correlation and regression analyses. The correlation
analysis was used to test the statistical significance of the relation-
ship for each stock, while the regression analysis was used to esti-
mate the degree to which recruitment changes in relation to a 1C
temperature increase or decrease.
The recruitment estimates were log2 transformed prior to the
correlation and regression analyses. The log transformation was
used to stabilise the variance and to transform absolute changes in
recruitment into relative changes so that all stocks are comparable
despite large differences in mean recruitment levels. The correla-
tion between interannual temperature changes and recruitment was
determined for all stocks using the nonparametric Spearman rank
correlation coefficient. One of the advantages of the nonparametric
correlation over the standard parametric one is that the resulting
coefficient is not influenced by outliers that are often present in bi-
ological data. Also, normality in temperature or recruitment data is
not required to perform the analysis. Because autocorrelation exists
in some of the recruitment and temperature time series, the signifi-
cance of the correlation can be biased due to overestimation of the
number of degrees of freedom. Therefore, we have reestimated the
number of degrees of freedom using the general correction pro-
posed by Quenouille (1952):
(2) N2 = N/(1 + r1 + r1 + r2 + r2 +...)
where N2 is the adjusted sample size, N is the original sample size,
r1 and r1 are the 1-year-lag autocorrelations of the two series, r2
and r2 are the 2-year-lag autocorrelations, and so on. The auto-
correlations were calculated as in Wei (1990) and only the
autocorrelation at 1-year lag was taken into account. The N2 can
sometimes be greater than N (when autocorrelation is negative) and
in such a case, the original sample size (N) was kept.
The regression analysis was performed using the method of
Kendall and Gibbons (1990) given in Sokal and Rohlf (1995). As
for the nonparametric correlation, the nonparametric regression
does not require normality of the data and the slope of the regres-
sion curve is not affected by outliers. The connection between tem-
perature changes and recruitment levels can be interpreted directly
from the slope of the regression (): a slope of +1 indicates that an
increase of 1C in temperature is associated with a twofold in-
crease in recruitment, and, conversely a value of 1 shows that a
similar temperature change is linked to a decline in recruitment by
a factor of 2.
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Newfoundland
West Greenland, 1 1 2 3 4 5
0.71 0.45
0.65 0.16
0.02 0.20 0.06
0.28 0.27 0.21 0.26
0.03 0.03 0.39 0.20
Connection between temperature and recruitment for
combined stocks
In addition to analyses of temperaturerecruitment relationship for
each individual stock, we have studied the temperaturerecruitment
relationship across all Atlantic cod stocks in a single analysis. In
this approach, one does not test the significance of single relation-
ships but rather whether the relationship between recruitment and
temperature varies from one end of the temperature distribution of
Atlantic cod to the other. Here, we hypothesise that the relationship
is positive at the cold limit of the temperature distribution and neg-
ative at the warm limit. It is also expected that for stocks not lo-
cated at the edge of the temperature distribution, there will be no
relationship between temperature and recruitment. To test this hy-
pothesis, we have used the slope of the regression line as a mea-
sure of the temperaturerecruitment relationship and have tested
whether this slope varies from being positive in cold waters to be-
ing negative in warm ones. The uncertainty in the regression slope
was assessed by estimating the empirical distribution of using a
bootstrapping procedure (Efron 1979). This was performed by
resampling the residuals from the regression 250 times for each
stock. Then the Spearman rank correlation coefficient between em-
pirical distributions of and mean bottom temperatures was calcu-
lated. To do so, we ranked the 250 values of each distribution and
subsampled 10% of the values at regular intervals. The aim of that
procedure was to reduce the number of data in each distribution
from 250 to 25 for computational purposes (we later tested that
this had no detectable effect on the final correlation value). The
Spearman rank correlation was calculated on the resulting 225 val-
ues (25 times nine stocks). The coefficient was tested against its
empirical distribution estimated by a Monte-Carlo permutation
procedure (5000 permutations). The permutation was performed on
the mean bottom temperature in such a way that each empirical
distribution was kept unchanged but the associated bottom temper-
ature was permuted (i.e., there was no permutation of individual
slope values between distributions). It should be noted that because
we have a prior expectation on the nature of the alternative hypoth-
esis ( should decrease with increasing temperature), the statistical
test is one-sided. Therefore, the p values used are also one-sided.
Results
Spatial and temporal heterogeneity in regional
temperatures
Spatial heterogeneity in temperature series was assessed
for regions covering sufficiently large oceanic areas: North
Sea, Icelandic Sea, West Greenland, and Newfoundland wa-
ters. Table 2 gives the Pearson correlation coefficients be-
tween subareas. These coefficients indicate the degree of
similarity in temperature time series within regions. In the
North Sea, all the correlation values are positive and high,
indicating that interannual temperature changes in the differ-
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Planque and Frdou 2073

Fig. 2. ACF for the time series of monthly temperature
anomalies for the nine areas in the North Atlantic. The value in
parentheses is the mean autocorrelation value from lag 1 to
4 months (indicated by the solid circles) and is an indicator of
the persistence of temperature anomalies over 5-month periods
(such as the FebruaryJune period selected for comparison with
recruitment data).
Fig. 3. Scatterplots of log2 recruitment of Atlantic cod against
temperature (FebruaryJune) for the nine stocks in the North
Atlantic. The lines correspond to the fit of a nonparametric
regression (see Materials and methods section for details). Note
that recruitment anomalies for West Greenland are plotted on a
distinct scale due to the higher variability in recruitment in this
region.

Table 3. Spearman correlation coefficient (r) and regression slope

equivalent to the FebruaryJune period chosen for compari-
() between temperature and log2 recruitment of Atlantic cod.
son between temperature and recruitment (see next section).
The average correlation over the four lags is also indicated
Stock r N N2 as an index of persistence of the temperature anomaly. For
Newfoundland 0.13 ns 0.43 31 (33) all regions, the ACFs show a marked decline during the first
West Greenland 0.23 ns 1.43 38 31 4 months, but the level of correlation varies between stocks.
Northeast Arctic 0.42* 0.92 40 31 In the Barents Sea, the correlation at lag 1 month is the
Iceland 0.38* 0.41 43 35 highest (ACF1 = 0.93) and it remains the highest when inte-
Faeroes 0.05 ns 0.02 34 26
grated over 4 months (ACF14 = 0.81). This indicates that
Georges Bank 0.08 ns 0.01 18 18
the interannual variability in temperature is likely to remain
North Sea 0.42* 0.98 33 32
similar, even if based on a different set of months (warm
Irish Sea 0.54** 0.98 27 (29)
winters generally coincide with warm springs, etc.). In the
case of the Newfoundland region, the autocorrelation dis-
Celtic Sea 0.18 ns 0.58 25 21
plays a sharp decrease and is already close to zero at lag
Note: ns, not significant; *p < 0.05; **p < 0.01. N is the sample size 3 months. In contrast with the Barents Sea, 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). Parentheses in the N2 column indicate when N2 is greater than N. late interannual changes in temperature is critical. The ACFs
for the other regions display various patterns between the
two extremes. It can be noted that the mean autocorrelation
ent subareas have followed parallel patterns. For Iceland and values for the first four lags are generally higher in the east-
West Greenland, only two subareas were compared and in ern than in the western part of the North Atlantic.
both cases the correlations are positive and high. In New-
foundland, correlation values between the five subareas se- Regional connections between temperature and
lected are much lower, often close to zero and sometimes recruitment
negative. This indicates that interannual fluctuations in tem- Relationships between SST and Atlantic cod recruitment
perature vary considerably within the Newfoundland area. It for the nine stocks have been assessed using Spearmans
also suggests that in this region, the choice of area over rank correlation. Table 3 shows the correlation coefficient,
which the temperature is averaged is critical to the resulting original and corrected sample size, and slope of the non-
temperature time series. parametric regression for each stock. Figure 3 shows log2 re-
Temporal heterogeneity was assessed for all regions. Fig- cruitment anomalies plotted against temperature anomalies
ure 2 shows the ACFs based on monthly temperature anoma- for each stock together with the linear regression fit.
lies in each region. For each area, the ACF starts with a In West Greenland, recruitment varied by up to a factor of
positive value and decreases towards zero. The first four lags 1000 with temperature fluctuations of about 2C. In New-
are highlighted in the figure, as they correspond to the per- foundland and Faeroes, the amplitude of changes in temper-
sistence of a temperature anomaly for a period of 5 months, ature is lower (<1C) and recruitment varied by up to a

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Fig. 4. Link between SST and recruitment plotted against mean
bottom temperature for nine Atlantic cod stocks in the North
Atlantic. For each stock, the link is estimated by the slope of the
nonparametric regression ( from Table 3) represented by the
horizontal line within the box. Boxes and lines indicate the 50
and 95% limits of the empirical distribution of the slopes,
determined by a bootstraping procedure. Stocks: NE,
Newfoundland (northern cod); WG, West Greenland; BA,
Barents Sea (Northeast Arctic cod); IC, Iceland; FA, Faeroe
Islands (Faeroes); GB, Georges Bank; NS, North Sea; IR, Irish
Sea; CE, Celtic Sea.
factor of 30. The stock of Georges Bank shows similar varia-
tions in recruitment despite a larger range in temperature
variation (about 4C). These results show that interannual
changes in recruitment are generally large and that the am-
plitude of these changes varies among stocks. The data are
also highly scattered around the regression lines, and the sta-
tistical significance of the relationships is generally low (Ta-
ble 3). In the Celtic Sea, Faeroes, West Greenland, Georges
Bank, and Newfoundland, correlations are not significant.
Correlations are significant in the North Sea, Barents Sea,
and Iceland at p < 0.05 and in the Irish Sea at p < 0.01.
Positive relationships (increase in Atlantic cod recruitment
at high temperature anomalies) are significant in the Barents
Sea and Iceland, whereas negative relationships are signifi-
cant in the Irish Sea and North Sea. However, we are left
with the observation that for the Celtic Sea and Georges
Bank stocks (stocks located at the warm limit) and for the
West Greenland and Newfoundland stocks (cold limit) the
correlation analysis cannot reject the null hypothesis that no
relationship between temperature and recruitment exists.
Therefore, it is difficult to conclude from the correlation re-
sults alone that a gradual change in the temperaturerecruitment
relationship does exist.
The conclusions of the stock-by-stock correlation analysis
are that (i) there is a high degree of scatter in the data that
results in difficulty in obtaining statistically significant rela-
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Can. J. Fish. Aquat. Sci. Vol. 56, 1999
tionships and (ii) for stocks located at the cold and warm
temperature limits, it is often not possible to conclude that a
relationship between temperature and recruitment exists.
One way to overcome the limitation of the above correlation
analysis is to combine the data from all stocks in a single
transatlantic analysis.
Transatlantic connection
Results from all stocks were combined in a single analysis
and the gradual change in the nature of the temperature
recruitment relationship was assessed by testing the exis-
tence of a link between the regression line slope and the
mean bottom temperature of each stock. Figure 4 shows the
distributions of against the mean bottom temperatures. The
apparent trend is for to be positive for stocks located in
cold waters and gradually decrease to negative values for
stocks in warm waters. For temperate waters the value of
is close to zero, as expected. The rank correlation between
distributions and mean bottom temperature is r = 0.59 and
the associated probability is p = 0.027. This indicates that
the null hypothesis (effect of temperature on recruitment is
independent of mean temperature) can be rejected. It is
clear, however, from Fig. 4 that the northern cod stock
(Newfoundland) stands out of this general pattern.
When performing the calculation of , 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, (ii) the temperature anomaly signal does
not vary substantially within the 5-month period over which
it is averaged, and (iii) recruitment has not been affected by
exceptional forcing that would have masked the effects of
temperature. In the case of the northern cod stock, these
three assumptions are violated. First, the spatial homogene-
ity in temperature in this area is extremely low, as shown by
the correlations in Table 2. Second, there is a high degree of
intermonth variability, as demonstrated in Fig. 2. Third, it is
reasonable to assume that the effect of temperature on the
recruitment of Northern cod have been masked by the dra-
matic reduction in SSB that preceded the collapse of the
stock (Hutchings and Myers 1994b; Myers et al. 1997). In
consequence, the estimate of for the northern cod stock is
highly uncertain and it would be appropriate to treat this
stock separately from the others. When the northern cod
stock is removed from the analysis, the rank correlation be-
tween distributions and mean bottom temperature reaches
r = 0.83 and the statistical significance is greatly improved
with p = 0.0016.
Discussion
In their demonstration of the relationship between stock
and recruitment levels, Myers and Barrowman (1996) illus-
trated how powerful metaanalysis can be when single analy-
ses fail to give significant answers. Later, Myers (1998)
recommended that general hypotheses on recruitment should
be tested with a similar approach, using data sets from
several populations. In this study, we present a metaanalysis
of data on nine cod stocks and show that the relationship
between temperature and recruitment follows a gradual
change: a positive relationship in cold waters, no relation-
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Planque and Frdou
Fig. 5. Recruitment of Irish Sea cod plotted against SSB
(points). The lines show the fit of a combined stock/temperature
recruitment model for three distinct temperatures. The model
(eq. 4) was fitted using least squares nonlinear regression.
ship in temperate waters, and a negative relationship in
warm waters. The present study demonstrates the existence
of a significant temperaturerecruitment relationship despite
the general pattern of apparent low (or lack of) statistical
significance of correlation analyses on single stocks. This
transatlantic relationship is consistent with the view that the
effects of the environment on recruitment should be stronger
at the limit of a species spatial distribution. It can be seen
as a unifying factor for previous results from a number of
studies that showed apparently contradictory results on the
effects of temperature on Atlantic cod recruitment.
It has been argued that temperature may not be directly
linked to recruitment but only acts as a proxy for marine
productivity in lower trophic levels (Rothschild 1994). In the
present study, the link between temperature and recruitment
is only evident at the limit of Atlantic cod distribution,
which suggests that direct effects of temperature on recruit-
ment could exist independently of food-related control.
There are immediate applications that could be made of
such knowledge. For example, monitoring SST is a rela-
tively easy task that could help in forecasting recruitment
levels several months in advance. Such short-term forecast-
ing is probably of limited value because assessment surveys
already produce recruitment estimates within a few months,
but it could be used as a test for the accuracy of the relation-
ship. Also, discrepancies between temperature-based fore-
casts and actual surveys should raise questions about
possible changes in the population dynamics, the nature of
environmental forcing, or the accuracy of recruitment esti-
mates. For example, taking into account the link between
temperature and recruitment could explain the unexpected
strong year-class of North Sea cod in 1996, which was asso-
ciated with the rapid and extreme cooling of the North Sea
(Loewe 1996) and the following poor year-class of 1997
when warmer conditions prevailed.
One can also envisage medium- to long-term forecasting
of recruitment based on climate forecasts. Although such
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2075
prediction would certainly be of great value to fisheries man-
agement, this idea finds its limits in the low accuracy of
medium-range (10 years) climate predictions upon which the
recruitment forecasts would depend.
In short- and long-term forecasts, 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. But forecasting recruitment is not the only way
by which temperature information can be used for fisheries
management.
The stockrecruitment 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. Yet, most of the stock
recruitment models do not currently include environmental
factors when this could be easily achieved. For example, one
can build a stockrecruitment model from the Ricker model
(e.g., see Hilborn and Walters 1992):
(3) R = aSSBe SSB
(or its equivalent form R = SSBe( SSB))
and include temperature in a form similar to that proposed
by Stocker et al. (1985):
(4) R = SSBe( SSB)e(T).
where R, SSB, and T are recruitment, spawning stock bio-
mass, and temperature, respectively, and , , and are the
associated coefficients. The resulting model is a three-di-
mensional surface (where SSB, T, and R are the three dimen-
sions). Figure 5 shows an example of such a fit for the Irish
Sea cod stock. The modelled surface is plotted in the form
of three curves corresponding to three temperatures slices
within the range of observed values in the Irish Sea. It is
clear that the fitted curves and particularly the slopes at the
origin vary greatly under the distinct temperature regimes.
Such information could be used to assess the impact of man-
agement strategies under various climatic scenarios.
Biological research is needed to confirm the temperature
recruitment links described here and to understand the under-
lying mechanisms. This is particularly important for two rea-
sons. First, it is unlikely that temperaturerecruitment
relationships will ever be used in fisheries management if
the mechanism by which temperature modulate recruitment
cannot be demonstrated. Second, if one can understand such
mechanisms and identify which key processes are affected
by temperature changes, it might be possible to design man-
agement strategies that will tend to maximise the recruit-
ment chances of a given population on a biological basis.
It has recently been observed that the changes in popula-
tion structure and particularly the reduction in age-class dis-
tribution are associated with the fluctuations in recruitment
(Marteinsdottir and Thorarinson 1998). In addition, Kjesbu
et al. (1996) have showed that the intensity of spawning and
the extent of the spawning period vary with the size of indi-
vidual Atlantic cod. From this observation, Ottersen et al.
(1994) have argued that populations with reduced age com-
position (and consequently reduced size composition) would
spawn over a smaller geographical area and for a shorter
time period and might therefore become more sensitive to
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2076
changing environmental conditions. If such is the case, it is
probable that in the near future, most of the heavily ex-
ploited fish populations will display amplified responses to
environmental changes.
Understanding the effects of environment on recruitment
could be of great value if integrated into management proce-
dures, and the possible ways by which this could be done
have not yet been fully explored. The main difficulty will
likely be in reconciling results on temperaturerecruitment
relationships that are evident at the transatlantic scale and
management strategies that take place at the level of individ-
ual stocks only.
Acknowledgements
The authors wish to thank Dr. Ransom A. Myers at Dal-
housie University for providing recruitment data and Steve
Worley at the National Center for Atmospheric Research for
providing SST data. We are also greatly indebted to all the
scientists at CEFAS who supported our efforts and com-
mented on earlier versions of this manuscript. This work was
funded by MAFF under program MF0420, Physical and Bi-
ological Controls on Fish Stocks.
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