833

Historical spatiotemporal dynamics of eastern

North Sea cod
Valerio Bartolino, Massimiliano Cardinale, Henrik Svedäng, Hans W. Linderholm,
Michele Casini, and Anders Grimwall
Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by SLU-Biblioteket on 04/30/12

Abstract: Recent analyses of historical data of fish abundance and distribution have shown the importance of a long tempo-
ral perspective in the evaluation of the current status of fish populations, but pose numerous difficulties such as fragmenta-
tion and inhomogeneities in the amount of available information in space and time. Using mixed-effects models in a
multiscale analysis, we identified an appropriate spatiotemporal scale of investigation of a high-quality, spatially explicit his-
torical data set, and we reconstructed the long-term spatial dynamics of Atlantic cod (Gadus morhua) in the Kattegat–
Skagerrak along the 20th century. We identified a northern and southern main aggregation of adult cod in the study area,
corresponding to the Skagerrak portion of the North Sea and the Kattegat cod stocks, respectively. The stocks showed spe-
cificities in their spatial dynamics, but common extensive loss of coastal aggregations during the last decades when only
13% (Kattegat) and 35% (Skagerrak) of the estimated early century cod biomass was left. Our reconstruction showed that
the collapse of the cod stocks in the area followed the peak in landings in the 1960s–1970s, suggesting that the postwar de-
velopment of the industrial fisheries played a major role in the decrease of local abundances and disappearance of local
adult cod aggregations.
Résumé : Des analyses récentes de données historiques sur l’abondance et la distribution de poissons ont démontré l’impor-
tance d’une perspective temporelle à long terme dans l’évaluation de l’état actuel des populations de poissons. Ces analyses
For personal use only.

présentent toutefois de nombreuses difficultés, telles qu’une fragmentation et une hétérogénéité spatiales et temporelles de la
quantité d’information disponible. En utilisant des modèles à effets mixtes dans une analyse multi-échelle, nous avons cerné
une échelle spatiotemporelle convenant à l’étude d’un ensemble de données historiques spatialement explicites de haute qua-
lité et reconstitué la dynamique spatiale à long terme de la morue franche (Gadus morhua) dans la région du Cattégat et du
Skagerrak au cours du 20e siècle. Nous avons cerné deux grandes agrégations, septentrionale et méridionale, de morues
adultes dans la région à l’étude, correspondant aux stocks de la région du Skagerrak de la mer du Nord et du Cattégat, res-
pectivement. Si les deux stocks présentaient des spécificités en ce qui concerne leur dynamique spatiale, ils étaient tous
deux caractérisés par la disparition généralisée d’agrégations côtières durant les dernières décennies, alors qu’il ne restait
que 13 % (Cattégat) et 35 % (Skagerrak) de la biomasse de morue estimée du début du siècle. La reconstitution a démontré
que l’effondrement des stocks de morue dans la région s’est produit dans la foulée de la pointe des débarquements des an-
nées 1960–1970, portant à croire que le développement des pêches industrielles dans l’après-guerre a joué un rôle majeur
dans la diminution de l’abondance locale et la disparition d’agrégations locales de morues adultes.
[Traduit par la Rédaction]

Introduction historical abundance and distribution of the exploited popula-

tions (Roberts 2007; Cardinale et al. 2009). Availability and
There is an increasing demand for historical baselines of access to historical time series have been generally scarce
marine ecosystems (Pauly 1995). This is particularly relevant and mostly postdate the start of intensive exploitation. Hence,
for the evaluation of harvested populations and to set goals the baselines used to evaluate harvested populations have
for their sustainable management and conservation (Pitcher typically referred to situations of high and prolonged exploi-
2001; Pinnegar and Engelhard 2008). This requires a long- tation (Pitcher 2001).
term perspective, at least before the onset of industrial or In recent years, the use of historical data has received more
large-scale intensive fishing practices, and estimation of the attention (Christensen et al. 2003; Rosenberg et al. 2005;
Received 13 August 2011. Accepted 1 March 2012. Published at www.nrcresearchpress.com/cjfas on 12 April 2012.
J2011-0343
Paper handled by Associate Editor C. Tara Marshall.
V. Bartolino. Swedish University of Agricultural Sciences, Department of Aquatic Resources, Marine Research Institute, 45330 Lysekil,
Sweden; University of Gothenburg, Department of Earth Sciences, Regional Climate Group, 40530 Gothenburg, Sweden.
M. Cardinale, H. Svedäng, and M. Casini. Swedish University of Agricultural Sciences, Department of Aquatic Resources, Marine
Research Institute, 45330 Lysekil, Sweden.
H.W. Linderholm. University of Gothenburg, Department of Earth Sciences, Regional Climate Group, 40530 Gothenburg, Sweden.
A. Grimwall. Swedish Institute for the Marine Environment, 40530 Gothenburg, Sweden.
Corresponding author: V. Bartolino (e-mail: valerio.bartolino@slu.se).

Can. J. Fish. Aquat. Sci. 69: 833–841 (2012) doi:10.1139/F2012-028 Published by NRC Research Press
 834
Thurstan et al. 2010). Several research institutes and govern-
mental agencies around the world have realized the impor-
tance of historical data to assess the present and are
currently investing time and resources to recover and analyse
information stored in their archives (ICES 2010). With few
exceptions (Cardinale et al. 2011; Rogers et al. 2011),
fisheries-dependent historical data have been employed to in-
fer the status of exploited fish populations in the early phase
of industrialized fisheries (i.e., Thurstan et al. 2010).
Although very informative, this kind of data suffers from the
limitations set by the fishermen behaviour and market re-
Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by SLU-Biblioteket on 04/30/12
quests, rather than the dynamics of the exploited populations
and ecosystems.
Long time series offer the necessary variability and con-
trasting situations to investigate the response of harvested
populations to both environmental changes and exploitation.
However, the analysis of historical data poses challenging is-
sues related to undesirable features, such as fragmentation of
the available information, lack of homogeneous sampling de-
sign, and unbalanced sampling efforts in both time and
space.
Usually, appropriate scales of investigation are defined by
sampling protocols within each discipline of the experimental
sciences. For instance, only over certain areal extents and
lengths of time, measurements of primary productivity can
reveal large-scale climatic shifts and not just fluctuations re-
For personal use only.
lated to smaller scale interactions between species (Melillo et
al. 1993; Nemani et al. 2003). Although it has become in-
creasingly clear that the problem of scale is a necessary pre-
requisite for developing a more complete understanding of
ecosystem dynamics (Wiens 1989; Levin 1992; McGill
2010) and responses to anthropogenic impacts (Bartolino et
al. 2012), the issue how scale can affect and limit the study
of historical data has never been addressed. The scale issue
is particularly relevant in the analysis of historical field data,
where sampling intensity is often heterogeneous in space and
time, despite the fact that temporal and spatial scales are
often correlated (Wiens 1989). How can we cope with the
lack of a uniform scale of investigation? Using historical
data requires an a posteriori approach for detecting a suitable
scale of analysis (i.e., long time after the sampling occurred)
to mediate information collected at different intensity and
coverage over time and to match, at the best, the processes
of interest.
Here, we reconstructed the spatial dynamics of the com-
mercially important Atlantic cod (Gadus morhua) in the Ska-
gerrak and Kattegat, eastern North Sea (ENS). The Skagerrak
and Kattegat have been important fishing areas since the
Middle Ages, along the coasts for Atlantic herring (Clupea
harengus), and offshore for demersal fishes such as cod, had-
dock (Melanogrammus aeglefinus), European ling (Molva
molva), Atlantic halibut (Hippoglossus hippoglossus), rays,
and skates (Haneson and Rencke 1923). Offshore, long lines
were the most important fishing gears until the 20th century.
In the beginning of the 1900s, trawl fishery was introduced,
which increased the fishing pressure considerably (Andersson
1954). However, fishing mortality can be assumed to have
been still at moderate levels in the beginning of the 20th cen-
tury in the Skagerrak and Kattegat for most of the demersal
1Supplementary data are available with the article through the journal Web site at http://nrcresearchpress.com/doi/suppl/10.1139/f2012-028.
Can. J. Fish. Aquat. Sci. Vol. 69, 2012
species, including cod, similar to what has been inferred for
the central North Sea before the onset of steam trawling fish-
ery in the 1880s (Mackinson 2002). Here, we show how a
convenient scale of analysis can be detected from a high-
quality historical data set of the distribution of Atlantic cod
and how it can be applied to improve the reconstruction of
the abundance of this fish population. Finally, the estimates
are discussed in light of a century of exploitation in the area.
Material and methods
Data
A database was established by compiling all known ar-
chived data from experimental otter trawl surveys carried out
in the Skagerrak and Kattegat from 1906 to 2007 by the
Swedish Institute of Marine Research and its predecessors
(Fig. 1). Four different types of bottom trawls and eight re-
search vessels were used during the study period, as a result
of different sampling programs amd consequence of advance-
ments in fishing technology. On average 59 hauls were con-
ducted every year when the sampling occurred during
daytime, comprising a total of 4378 observations for the
whole time series. Characteristics of the included trawl types
and the statistics of validated and approved hauls are sum-
marized in Supplemental Table S11 (for more details see Car-
dinale et al. 2009, 2010). Since 1974, most surveys have
been conducted by the Swedish research vessel Argos within
IBTS (International Bottom Trawl Survey; ICES 1992), how-
ever, national trawl surveys were also carried out. An exten-
sive coastal trawl survey was launched in 2001, including the
Kattegat and the eastern coastal part of the Skagerrak. Trawl
station information include date, haul duration, towing speed,
setting and hauling position (latitude and longitude; positions
were reconstructed from detailed fishing area information for
those hauls carried out prior to the use of more advanced
navigation equipments, i.e., GPS), and depth (metres). Only
hauls conducted exclusively during daylight hours were used
in the analysis. For each haul, the number and the total
length (cm) of cod specimens were recorded. For some hauls
(less than 3% of the total), length–frequency data were not
available, although the total number of fish caught by species
was reported. In these cases, the length–frequency distribu-
tion, as estimated in the same year, semester, and area, was
used to calculate the number of fish per length class (1 cm).
We calculated local abundance of adult cod as the biomass
per swept area (kg·km–2) of those individuals equal to or
larger than 39 cm in total length (the size at which 50% of
fish are usually mature). Fish biomass was calculated using
an annual length–mass relationship based on data collected
at the time of the survey since 1981. The masses previous to
1981 were estimated using average parameter values for
1981–2007.
Results were discussed in the light of additional informa-
tion on environmental temperature and fisheries exploitation.
We used the Met Office Hadley Centre’s sea ice and sea sur-
face temperature (SST) data set, HadISST1. This data set is a
combination of monthly globally complete fields of SST and
sea ice concentration on a 1° latitude–longitude grid from
1870 (obtained from http://badc.nerc.ac.uk/view/badc.nerc.ac.
Published by NRC Research Press
 Bartolino et al. 835

Fig. 1. Map of the eastern North Sea, with shaded region indicating the study area and the points the observations (see Fig. 3 for details on
temporal variability of the sampling spatial coverage).

62 N

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56 North
Sea

54
Germany

6 8 10 12 14 16

Longitude (°E)

uk__ATOM__dataent_hadisst; see Rayner et al. (2006) for use of the available information to reconstruct the spatial dis-
more details). We selected SSTs from the grid cells that cov- tribution of this population during the 20th century. We con-
ered the Skagerrak–Kattegat area for the analyses. structed space–time grids at different resolution to analyze
Landings data (1903–2007) from the Skagerrak and Katte- the data and investigate this issue. The grids spanned from 2
gat were collated from official ICES sources (http://ices.dk/ to 15 years time intervals (larger time intervals were not in-
fish/catchstatistics.asp). vestigated because they are outside the life span of cod) and
from 0.01° to 0.12° (longitude–latitude) spatial resolutions.
Analysis Fine grids were represented by a high number of spatiotem-
We performed a multiscale analysis to understand if a tem- poral cells (3164 cells for the highest resolution of 2 years
poral and spatial scale that optimize the fit between the and 0.01°), while coarse grids had a low number of spatio-
model and the data can be identified, according to the main temporal cells (737 cells for the lowest resolution of 15 years
objective of describing long-term spatiotemporal dynamics and 0.12°). Then, each cell was considered as a spatiotempo-
of the cod adult population in the Kattegat and Skagerrak. ral unit of investigation where multiple observations could
Although our data set on local abundance of cod have in- occur. We explored the performances in terms of Akaike in-
formation on the year when the sampling occurred, it is not formation criterion (AIC; Akaike 1974) of a population of
obvious if an annual time step would represent an optimal generalized additive mixed models (GAMMs; Pinheiro and

Published by NRC Research Press

 836
Bates 2000; Wood 2006) fitted with restricted maximum like-
lihood (REML). These are regression techniques where the
relationships between dependent and independent covariates
are modeled with a smoothing term and therefore are desir-
able in our application for their ability to model nonlinear-
ities that often characterize biological systems. We used a
mixed model approach to account for changes in the spatio-
temporal dependency of the data across different resolutions
with no prior averaging of the response variable. This al-
lowed direct comparison of the effect of different spatiotem-
poral scales on model goodness of fit with a selection
Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by SLU-Biblioteket on 04/30/12
criterion such as AIC. The response variable xm,y,t,k,(f,l) was
the natural logarithm of local abundance of adult cod ob-
served during the month m of the year y at a particular loca-
tion f,l (identified by longitude and latitude degrees), and
within the time–space interval t,k. The spatial distribution of
Atlantic cod in the ENS was reconstructed in relation to sea-
sonality (m, month), bathymetric preference (D, depth), and
according to the best combination of temporal and spatial
scales identified via AIC. Observations laying within the
same spatiotemporal cell were not averaged but rather consid-
ered as repeated measurements, and such dependency was
treated as a random effect. The model was specified as fol-
lows:
xm;y;t;k;ðf;lÞ ¼ a þ g½Df;l  þ st0 ½f; l þ s00 ½m; t þ dy
For personal use only.
þ dt;k þ em;y;t;k;ðf;lÞ
where a is an overall intercept; g and s are one-dimensional
(Wood 2004) and two-dimensional (Wood 2003) smoothing
functions, respectively; dt,k is a random effect independent
and identically distributed Nð0; s 2t;k Þ that accounts for the
nonindependence of those observations laying in the same
spatiotemporal unit (replicated measurements); dy is a random
effect independent and identically distributed Nð0; s 2y Þ that
accounts for interannual variability in the abundance of cod;
and em,y,t,k,(f,l) is the error term independent and identically
distributed N(0, s2). In the specific, s′ is an isotropic smooth-
ing function (Wood 2006) on the geographical coordinates f
and l specific for each time period t, while s″ is a tensor pro-
duct smoothing function to account for large scale temporal
variations in the month effect.
An estimate of the overall adult cod biomass in the study
area was obtained by integrating the model predictions (back-
transformed to the original scale) for each time interval t over
the same estimation grid (Maunder and Punt 2004). A total
of 1000 replicates were sampled from the probability distri-
bution of the model estimates in each point of the grid and
integrated for each replicate to provide a measure of the un-
certainty in the estimated adult cod biomass. The regression
models were fitted using R and the library gamm4 (Wood
2011).
Results
The multiscale analysis of cod data showed high variability
around the relationship between predictability and scale. A
positive relationship between the model performances (de-
crease in the AIC scores) and the temporal and spatial scales
was found up to an optimum for a temporal and spatial reso-
lution of 12 years and 0.06°, respectively. A second peak is
observed for a time–space scale of 11–12 years and 0.09°,
Can. J. Fish. Aquat. Sci. Vol. 69, 2012
suggesting that the temporal scale may be better defined
than the spatial scale within the space–time window investi-
gated (Fig. 2).
The model on cod distribution (Table 1) showed a positive
relationship with bottom depth up to a depth of 120 m (see
online Supplemental Fig. S11). Inspection of model residuals
revealed neither major departure from normality nor temporal
and spatial autocorrelation.
Prediction maps of the historical distribution of cod in the
ENS (Fig. 3) combined information on the associated uncer-
tainty (Hengl 2007). Estimated uncertainty is lower since
mid-1970s when the IBTS started to systematically sample
the study area. Confident estimates characterize also most of
the study area until the mid-1930s, while large uncertainty is
associated with the estimates during the decades before and
after the Second World War, particularly in the southern part
of the study area, and in the 1960s and early 1970s, before
the onset of IBTS.
A bimodal distribution, with a northern and a southern
main aggregation of adult fish, characterizes the spatial distri-
bution of cod in the ENS (Fig. 3). They are characteristic fea-
tures of the distribution of cod in the study area, but follow
different temporal dynamics along the century investigated.
The sounthern aggregation of adult cod went through wide
fluctuations in size and abundance. The main events of con-
traction in the abundance and distribution of the southern ag-
gregation occurred in the time intervals 1914–1925 and
progressively from the 1960s. Focusing on the last three dec-
ades showed an unprecedented contraction during the last
time period (1998–2007).
The northern aggregation displayed substantially different
dynamics. At the very beginning of the 20th century, large
aggregations of adult cod were found off the northern coast
of Denmark. The westernmost part of these aggregations dis-
appeared around 1920, and the reduced peak of aggregation
in the Skagerrak shifted eastward toward the Swedish coast.
In the 1930s, the northern aggregation was highly contracted.
A possible coastal aggregation at the northern limit of the
study area was estimated from the 1940s to the early 1970s,
but these estimations were driven by a reduced number of
observations and were associated with large uncertainty. The
establishment of systematic international surveys in the mid-
1970s gives a clear picture of further reduction of the already
low cod abundances during the 1980s and mid-1990s. Such
contraction is particularly evident along the Swedish coast,
where adult cod biomass in the last period was extremely
low. Only recently (1998–2007), local abundances of cod
have slightly increased in the western part of the northern ag-
gregation, but not in the southern aggregation.
Cod biomass in the study area showed an initial profound
decline around the 1920s, followed by a rapid recovery of the
southern aggregation in the 1930s and of the northern aggre-
gation in the 1940s (Fig. 4).
Biomass levels remained high during the 1950s and
through the 1960s in the Skagerrak. Because of the elevated
uncertainty, no reliable estimate of the aggregated cod bio-
mass was possible for the Kattegat during the 1950s, while
in the 1960s the adult fish biomass in the Kattegat was as-
sessed to approximately 50% of its initial value. This was fol-
lowed by a progressive decline of the stock up to the
historical minimum observed during the last decade (1998–
Published by NRC Research Press
 Bartolino et al. 837

Fig. 2. (a) AIC surface as function of temporal and spatial scales from all the generalized additive mixed models tested and their rank and
(b) AIC profiles from the same surface. The circle, gross line, and arrow identify the model that ranked first, with a time–space resolution of
12 years and 0.06°, respectively.
(a) (b)
167 154 100 110 121 108 149 134 124 153 140 161

14 109 88 59 10 36 4 32 73 37 61 27 56

157 150 91 60 75 22 80 116 83 115 97 143

17450
12 84 62 19 6 21 1 7 38 3 33 9 31

105 95 47 8 40 5 20 43 2 28 18 24
Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by SLU-Biblioteket on 04/30/12

10
Time scale

148 139 96 52 78 39 82 69 58 76 111 92

122 103 41 16 44 11 35 49 23 57 42 45 17400

AIC
8 132 119 48 26 63 25 72 77 14 66 74 67

165 163 147 104 135 87 131 151 106 146 128 138

6 168 160 125 93 126 81 98 113 55 107 142 144

129 118 85 34 46 13 54 65 17 53 90 50 17350

4 156 141 127 71 89 29 86 117 30 70 94 102

158 137 114 51 79 15 68 101 12 64 123 99 0.01°-0.12°

2 166 162 159 145 136 112 133 152 120 130 164 155
0.06°
17300

0.02 0.04 0.06 0.08 0.10 0.12 2 4 6 8 10 12 14

For personal use only.

Space scale Time scale

Table 1. Parameters estimated for the generalized additive mixed model

effects on the local abundance of adult cod (ln(kg·km–2)).

Model component Estimate SE EDF P value

Fixed effects
Intercept 2.648 0.110 <0.001
g(Df,l) 4.194 <0.001
st0 ðf; lÞ 4.950–20.534 <0.001
s″(m,t) 12.782 <0.001

Random effects
dy 0.532
dt,k 0.609
de 2.380
Note: Estimated equivalent degrees of freedom (EDF) (or parametric coeffi-
cients for the intercept and the random effect) are shown together with the statisti-
cal significance. Model R2 = 0.31; sample size is 4378 observations.

2007) when only 13% of the initial adult cod biomass was
left. In the Skagerrak, the stock declined largely in the end
of the 1970s and early 1980s and experienced its historical
minimum (i.e., approx. 20% of the estimated initial biomass)
in the following time period (1986–1997). During the last
decade, adult cod biomass in the northern area moderately in-
creased to 35% of the early century estimates.
Discussion
In this study, we reconstructed the wide variations in spa-
tial distribution and abundance of cod in the ENS during the
last 100 years. The historical perspective given by our analy-
sis offers a unique opportunity of investigating the spatial and
temporal dynamics of a fish species from the onset of indus-
trial fisheries in the area, up to the last decades of extremely
intense exploitation. These results may contribute to define
historical baselines for a more objective evaluation of the sta-
tus of cod populations in the ENS.
Our analysis provided spatially explicit estimates of adult
cod biomass together with associated uncertainties and gave a
clear picture of the impact of poorly sampled areas and periods
on model predictions and on our ability to reconstruct the past.
We showed, through visualization and mapping, that recon-
struction of past fish distribution can be highly uncertain, but
also that historical sources bring valuable information for a
more correct interpretation of the present. This is of particular
relevance in the case of harvested populations, such as Atlantic
cod, which have experienced long histories of exploitation that
have affected their geographical distribution and abundance.

Published by NRC Research Press

 Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by SLU-Biblioteket on 04/30/12
For personal use only.

838

Fig. 3. Maps of the estimated distribution of adult cod biomass (logarithm of kg·km–2) in the eastern North Sea, with the associated standard error visualized through whitening. Bubbles
are the observed mean log-abundance in each cell and time interval.

59.0 1906 - 1913 1914 - 1925 1928 - 1937 1938 - 1947 1951 - 1961
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Longitude (°E)

Published by NRC Research Press

Can. J. Fish. Aquat. Sci. Vol. 69, 2012
 Bartolino et al. 839

Fig. 4. (a) Average sea surface temperature (SST, 1902–2007) in the
study area; vertical dashed lines identify the 12-year time resolution
of the analysis. Estimated adult cod biomass in the Skagerrak (b)
and Kattegat (c) parts of the study area along the 20th century and
commercial landing time series disaggregated for Sweden (continu-
ous lines) and Denmark (dashed line). Shaded vertical bands indi-
cate the two world wars.
11.0
(a)
SST (°C)
was studied at a resolution of 12 years and 0.06°, an increase
in predictability of the spatial dynamics was observed, as de-
tected by a minimum in the AIC. At the current stage of
understanding and with the available data, we cannot inter-
pret the spatiotemporal scale identified as the result of under-
lying ecological processes (i.e., numerical dominance of
particularly strong year classes, spatial resolution of aggrega-
tive phases such as spawning aggregations). Thus, the resolu-

10.5 tion identified is likely to be a compromise between the level

10.0 of spatial structuring of the adult cod population and the
9.5
9.0 fragmentation and coverage of the available information.
Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by SLU-Biblioteket on 04/30/12

8.5 This deviation from the general positive relationship between

data predictability and scale of investigation (Levin 1987;
(b) WW1 WW2
Wiens 1989) may be expected when the scale of analysis
1.2 20000 matches the resolution of sampling (Goodwin and Fahrig
1998) or its best approximation (as in this study). Moreover,
1.0 the result is consistent with the long-living performance of a
15000
species such as the Atlantic cod, and it responds to the objec-
0.8
tive of improving the fit of the model to the data.
We found that cod dynamics were not homogeneous in
space in the study area. Variations in local abundances are
0.6 10000 likely to reflect heterogeneities in the processes regulating
the distribution and abundance of cod, such as the patterns
0.4 of exploitation and the environmental variability, but could
5000 also result from underlying spatial structuring of the cod pop-
0.2 ulation in the ENS (i.e., Svedäng et al. 2007, 2010b). Fluctu-
Biomass index
For personal use only.

Landings (103 t)

ations in the northern aggregation appeared highly influenced

0.0 by the dynamics of the westernmost part of the distribution.
0 The recent increase of the adult cod abundances was limited
3.0
to the western part of the northern area and contrasted with
(c) the extremely low abundances of the coastal areas as pre-
WW1 WW2 20000
2.5 dicted by our model. This suggested a major contribution of
the neighbouring North Sea cod population to the abundan-
ces in the Skagerrak rather than recovery of the local aggre-
2.0 15000
gations along the Swedish Skagerrak coast. Major changes of
the inshore demersal fish community have been reported
1.5 along the Swedish Skagerrak coast during the last 20 years
10000 (Svedäng 2003). Coastal cod populations experienced a dra-
matic contraction. Variability of juvenile cod abundance in
1.0
the coastal areas, under very low densities of the local adult
cod populations, has been recently explained through connec-
5000
0.5 tivity between the offshore and inshore systems (Svedäng and
Svenson 2006). In line with this interpretation, the marginal
habitats of the North Sea cod distribution in the Skagerrak,
0.0
0 as mapped by our model, may play a role not only for the
1907 1931 1955 1979 2003
expansion and dynamics of the North Sea stock, but also for
the supply of recruits and probability of recolonization of the
Year coastal areas.
Although there are a number of issues affecting the analy- The complete loss of adult cod aggregations was even more
sis of fragmented historical data, we think that the use of his- evident for the southern aggregations in recent years. The
torical data to assess the distribution and abundance of high abundances along the coastal areas were the most af-
natural populations has been far too limited. Moreover, in fected, suggesting targeting of the former coastal aggregations
those few cases where historical information were analysed, and limited exchange of fish with the neighbouring areas (i.e.,
the importance of scale has been neglected. We showed how the Skagerrak and Öresund; Svedäng et al. 2010a).
modeling can provide the necessary linkages between differ- The time period around the 1920s was characterized by
ent scales of resolution at which historical data have been particularly low abundances of adult cod in the ENS, in con-
collected, improving the use of the information available and trast with the elevated estimates at the beginning and middle
returning more robust estimates. of the century, which we are not able to explain at the current
Our results show that a decrease of model performances stage of understading and with the available data. Interest-
may occur when sparse and fragmented data are analysed at ingly, a similar decrease in fish stock size during the 1920s
too small temporal and spatial scales. When cod distribution was reported in the same area for other species such as Euro-

Published by NRC Research Press

 840
pean plaice (Pleuronectes platessa) (Cardinale et al. 2011). At
that time the landings were rapidly increasing as a conse-
quence of the developing trawl fishery in the area (http://ices.
dk/fish/catchstatistics.asp), but the biomass harvested was still
moderate compared with the rest of the time series. Other rea-
sons likely influenced the low values of cod abundance ob-
served during the 1920s in the ENS and protracted to the
1930s in the Skagerrak, such as a low contribution from the
North Sea stock, as suggested by our reconstruction of the
spatial distribution. It is also important to note that the period
around the 1920s recorded the lowest average temperatures of
Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by SLU-Biblioteket on 04/30/12
the whole century, and ultimately, we may not exclude unac-
counted variations in the catchability for this period. Interest-
ingly, plankton samples collected by Danish scientists during
the first half of the century in the Kattegat showed a similar
latitudinal temporal pattern in the abundance of cod eggs and
larvae (Knudsen 1953). They found that during the 1930s, the
central and southern Kattegat had higher relative densities of
early life stages of cod than the northern Kattegat (Knudsen
1953), a possible result of a lower contribution from the adja-
cent Skagerrak during that period. Moreover, consistent with
our estimates of a high adult cod biomass during the war and
postwar period, exceptionally high abundance of cod eggs and
larvae were observed in the Kattegat during the early 1950s
(Knudsen 1953).
A rapid decrease of cod biomass was estimated for the last
For personal use only.
part of the time series, in agreement with the high fishing
mortality (i.e., threefold higher than the fishing mortality es-
timated at the maximum sustainable yield) estimated by the
assessment in the Kattegat and North Sea during the last
40 years (ICES 2009). We found that the Skagerrak aggrega-
tion peaked between the 1960s and the early 1970s, support-
ing the hypothesis of a “gadoid outburst” in the North Sea
during that time (Cushing 1984), and dropped immediately
after. For the Kattegat aggregation, it is more difficult to
identify when the stock started to contract because of the
high uncertainty associated to the 1950s estimates. If the Kat-
tegat cod was at high levels during the 1950s, we may infer a
major collapse of the stock in the 1960s and a progressive
contraction during the last decades of the century.
Unfortunately, information on fishing mortality or fishing
effort were not available before 1960s, and it was not possi-
ble to formally test and disentangle the effect of harvesting
and environmental variability within our model. However,
contraction of adult cod abundance in the ENS was
synchronized with a peak in commercial landings between
the 1960s and the 1970s, while a clear warming trend started
in the second half of the 1980s in this area. Rather than ex-
cluding or supporting the contribution of the environment to
determine the current low levels of cod in the ENS, our re-
construction suggests that the postwar development of the in-
dustrial fisheries played a major role in the decrease of cod
local abundances. Further investigations at a finer scale
should be carried on shorter and data-richer time periods
(i.e., the last 30 years of IBTS groundfish survey) to evaluate
the relative contribution of harvesting and environment on
the spatiotemporal dynamics of this species.
It is important to recognize that our measures of local
abundance of adult cod rely on the assumption that catchabil-
ity is constant over time. Changes in catchability have sel-
dom been estimated for survey data (Marchal et al. 2003);
Can. J. Fish. Aquat. Sci. Vol. 69, 2012
however, technological advancement may become relevant
when analysing long time series of data collected under the
potential effect of increasing catching efficiency (Cardinale
et al. 2010). Under the reasonable assumption of constant
catching efficiency within the 12-year time resolution of our
analysis, the estimated spatial structure of cod would not be
affected by unaccounted technological creep. On the contrary,
the temporal decrease in the estimated adult cod biomass can
be assumed to be an underestimation of the real decline of
these cod stocks.
The progressive decrease in the availability of marine nat-
ural resources has spurred the need of increasing efficiency
and effort of harvesting to maintain elevated catches and
profits (Hilborn and Walters 1992). This has contributed to
the unnoticed dramatic decline of huge populations, which
were believed to be inexhaustible (Roberts 2007). Under-
standing local decline of natural populations is of outmost
importance when discussing conservation and management
of oceanic resources, because it is at local scale that mecha-
nisms of population regulation and, ultimately, extinction op-
erate (Cowlishaw et al. 2009). Our reconstruction showed
that the decrease of cod abundance in the ENS occurred
with a loss of spatial structure, which taken together with a
philopatric behaviour of the coastal cod populations (Sve-
däng et al. 2007) may represent an important limit for the re-
covery of cod in this area.
Acknowledgements
This work is funded by the Swedish Environmental Protec-
tion Agency as part of the project “Waking the Deads”. We
also thank David Rayner, Patrik Jonsson, Johan Lövgren,
and three reviewers for comments on the manuscript, and the
scientists of the former Swedish Board of Fisheries who col-
lected data along a century of bottom trawl surveys.
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