Cod Behaves in Mysterious Ways:Shifting Distribution in the North Sea During the Last Century. ICES CM 2011/D:06

International Council for the Exploration of the Sea ICES CM 2011/D:06

Theme Session D Linking the History to the Present: Understanding the History of Fish, Fisheries and Management

Cod behaves in mysterious ways: shifting distribution in the North Sea during the last century

Georg H. Engelhard*, David A. Righton, Tina K. Kerby, and John K. Pinnegar

Centre for Environment, Fisheries and Aquaculture Science, Pakefield Road, Lowestoft NR33 0HT, UK

* Author for correspondence ([email protected])

Summary

The distribution of cod within the North Sea has shown major shifts over the course of the last century. This has become evident from an analysis of almost one-hundred years of British commercial fisheries data, digitised from Cefas archives. Combined with contemporary fisheries data, these span the period 1913–2010 (excepting both World Wars), at the spatially detailed level of ICES rectangle (0.5° Latitude, 1° Longitude). New analysis of old data reveals that during most of the Twentieth Century, North Sea cod distribution was very different from that in the most recent period (2000– 2010). Whereas historically, densities of cod catches were especially concentrated in the central and north-western North Sea, they are presently concentrated in the northern- and north-easternmost part of the North Sea. We attempt to reveal the extent to which climate, fishing, or both have contributed to the recent shift in distribution.

Keywords: cod, distribution shift, climate, North Sea

INTRODUCTION

Historically, cod Gadus morhua has arguably been the most important of commercial fish species, and its fishery has played a prominent role in the economical and political development of Europe as well as North America over the past centuries (e.g. Kurlansky 1997). More recently, disputes over cod fishing grounds have led to such well-known conflicts as the British-Icelandic ‘Cod Wars’ of 1950s– 1970s (Gilchrist 1978; Jónsson 1982), which ultimately contributed to the international establishment of 200-miles Exclusive Economic Zones. Currently, cod remains one of the world’s most important fish stocks, and in 2004 ranked 12th among all fish species in terms of global landings (and even higher in terms of value of landings; FAO 2007). This is in spite of significant declines in landings of most cod stocks during recent decades (review: Engelhard et al. 2010a) and a collapse of populations off eastern Canada and the U.S. (Kurlansky 1997). The North Sea cod stock has shown a particularly marked decline since the 1980s, even more noteworthy since it followed a period of very high productivity known as the ‘gadoid outburst’ (late 1960s to mid-1980s: Daan 1978; Hislop 1996). During the gadoid outburst, not only cod but also haddock Melanogrammus aeglefinus, whiting Merlangius merlangus, saithe Pollachius virens and Norway pout Trisopterus esmarki produced some of the largest year-classes on record (Holden 1978; Jones & Hislop 1978). Whilst landings of cod had remained fairly stable throughout the period 1900– 1950, they rose enormously during the 1960s and remained very high until the mid-1980s, when the recent marked decline began. Survey indices and stock assessment have indicated that the high landings were not only due to substantially increased fishing effort but also to a considerable extent, to very high recruitment and biomass levels (Pope & Macer 1996). Unfortunately, the recruitment of North Sea cod has remained low since the late 1990s, and the spawning stock biomass has been at historically low levels for almost two decades now (ICES 2010). The past three decades have also seen a shift in the mean distribution of cod within the North Sea, to more northerly and on average deeper waters; this was reported by studies based on research survey data (International Bottom Trawl Surveys, IBTS; see Hedger et al. 2004; Perry et al. 2005; Rindorf & Lewy 2006; Dulvy et al. 2008). As this shift coincided with the population decline it is important to understand its causes, not only because of predicted links between distribution and abundance (e.g., Blanchard et al. 2005) but also because changes in fish distributions may have knock-on effects upon fisheries (Pinnegar et al. 2010). Two main hypotheses have been put forward (Engelhard et al. 2010b). Firstly, climate change is expected to result in contractions, expansions, or shifts in fish distribution (review: Rijnsdorp et al. 2009). In the North Sea, a warming trend has happened over the past 30 years; this has coincided with a northward shift in many, but not all, North Sea fish species (Beare et al. 2004; Perry et al. 2005), and an average, deepening shift of around –3.6 m per decade since the 1980s (Dulvy et al. 2008). Secondly, fishing pressure has over the same period been consistently higher in the southern compared to northern North Sea (Jennings et al. 1999); with a greater rate of fishery-induced depletion in the south, a northward shift in mean population distribution is to be expected. However, the rather short time-span of fishery-independent survey data (past three decades) makes it very hard to disentangle these two hypotheses (which are not mutually exclusive). This has motivated the current study based on a unique dataset of British commercial catch per unit effort

(cpue) records spanning a far longer timespan—approaching one century—covering both warming and cooling periods, and including periods of contrasting levels of fishing effort. The aims of the present paper are to:

1. Describe long-term distribution shifts of cod within the North Sea over the period 1913–2010; 2. Compare the current (2000–2010) distribution with that throughout the Twentieth Century; 3. Examine to what extent distribution shifts can be explained by variables related to climate change, fishing pressure, and/or stock abundance.

METHODS

Data and modelling of cod distributions

In broad lines the methodology follows that of our companion paper describing the long-term distribution shifts of sole Solea solea and plaice Pleuronectes platessa in the North Sea (Engelhard et al. 2011). For the period 1913–1980, cod data were obtained from historical fisheries ‘statistical charts’ (catalogued in Engelhard 2005) that were produced by the UK Ministry of Agriculture, Fisheries and Food (MAFF; now the UK Department for Environment, Food and Rural Affairs [Defra]). These show fishing effort (hours fished) and fish landings by British otter trawlers (either steam- or motor-driven) for each ICES rectangle (0.5° Latitude, by 1° Longitude) in the North Sea. These data record all fish that were landed by the otter trawl fleet into England and Wales (1913, 1968–1980) or into England, Scotland and Wales (1920–1967). For the period 1968–2010, data on otter trawler landings into Scotland were obtained from the Fisheries Management Database (FMD) of Marine Scotland (cf. Greenstreet et al. 1999). For 1982–2010, data on otter trawl landings into England and Wales were obtained from the Fisheries Activity Database (FAD) of Defra/Cefas. Over the time-span examined, important improvements have occurred in the cod fishing power, or technical efficiency, of otter trawlers (Robinson 2000; Engelhard 2008). Our aim is not to analyse temporal changes in absolute cpue values as proxies for the abundance of cod, but rather to look at trends in spatial distribution of catches. We therefore normalised the cpue values in any given year (divided by the annual mean cpue for the entire area), to overcome the confusing effect of an increase in fishing power of trawlers. We are assuming that relative cpue by the commercial fleet gives an appropriate indication of the spatial distribution of the species. We acknowledge that potential bias might arise from uneven spatial distribution of effort by more or less powerful vessels within the North Sea. By decade, we calculated cpue values by rectangle for a large area encompassing the majority of the North Sea (shaded in Figure 2). As an approach to quantify shifts in population distribution, we calculated the ‘centres of gravity’ of the latitudinal, longitudinal, and depth distributions of North Sea cod, using methods akin to those developed and applied by Heino et al. (2008). This analysis was based on a slightly less extensive area within the North Sea that included only those rectangles with cpue data for the majority of years in our time-series (see polygon line in Figure 2). Within this polygon, the latitudinal (or longitudinal) centre of gravity of distribution in a given year was calculated as the average of the

latitudes (or longitudes) of all rectangle centres, weighted by the cpue value in each rectangle. Weighted standard deviations and standard errors of the weighted mean longitudes were calculated (Bevington 1969). The centres of gravity of depth distributions were calculated analogously and, given that cod generally live close to the seafloor, based on the mean sea depth in any given rectangle.

Modelling distribution shifts in relation to climate, abundance and fishing pressure

We examined cod distribution in relation to: (1) climatic variables and (2) cod fishing pressure and abundance. As a broad-scale climate indicator, the North Atlantic Oscillation (NAO) winter index (December of the previous year to March of the focal year) for 1913–2007 was taken from Jones et al. (1997), with updated values provided online by the Climatic Research Unit, University of East Anglia, Norwich, UK (www.cru.uea.ac.uk/~timo/projpages/nao_update.htm; see Figure 1a). The NAO is associated with speed and direction of westerly winds across the North Atlantic, and is particularly important in winter when it exerts a strong influence on European weather patterns, and on Atlantic water inflow into the North Sea; a positive NAO is generally linked with strong wind circulation and higher atmospheric and sea temperatures in western Europe (Hurrell 1995; Jones et al. 1997; Ottersen et al. 2001). We also considered the Atlantic Multidecadal Oscillation (AMO), a climatic mode that manifests itself as a 20–30 year cycle in de-trended sea surface temperature series for the North Atlantic (Figure 1b). These data (back to 1871) were obtained from NOAA (Global Change Master Directory). As an indicator of sea temperature variations within the North Sea, the Hadley interpolated sea surface temperature (HadISST) time-series was used (Figure 2c). Annual and winter (January–March) means of sea surface temperatures, interpolated to 1° latitude by 1° longitude, were used as described by Rayner et al. (2003), with updated values provided online by the UK Meteorological Office. In order to describe the effects of fishing pressure, estimates of fishing mortality (F) on 2–4 year old cod for the years 1921–1938 and 1946–1962 were taken from Pope & Macer’s (1996) long- term study on North Sea cod population dynamics. For the period from 1963 up to the present, the F time-series was extended with data from the most recent ICES Working Group reports (ICES, 2010). As descriptors for the population abundance of North Sea cod, we used estimates of recruitment at age 1 and of spawning stock biomass (SSB); these were taken from the same sources (years 1921–1938 and 1946–1962 from Pope & Macer 1996; years 1963–present from ICES 2010). The fishing mortality, recruitment, and SSB time series are shown in Figures 1d–f. We used correlations as a first approach to explore which environmental, abundance, and/or fishing pressure variables might be associated with descriptors of cod distribution (latitudinal, longitudinal and depth). Pearson cross-moment correlations (rp) were used, as most variables did not show distributions significantly different from normality (one-sample Kolmogorov-Smirnov tests, P > 0.05). The exception was cod recruitment, which was log-normally distributed and hence log- transformed before parametric statistical analyses.

3 (a) (b) 0.4 2 0.2 1 NAO winter index AMO index 0.0 0 -0.2 -1 -0.4 -2

1920 1930 1940 1950 1960 1970 1980 1990 2000 1920 1930 1940 1950 1960 1970 1980 1990 2000 Year Year 1.2 11.5 (c) (d) 1.0 11.0 0.8 10.5 0.6 Hadley SST (°C) FCod (ages 2-4) 0.4 10.0 0.2 9.5 0.0

1920 1930 1940 1950 1960 1970 1980 1990 2000 1920 1930 1940 1950 1960 1970 1980 1990 2000 Year Year 300 (e) (f) 250 2000 200 150 Cod recruitsCod (age SSBCod ('000 t) 1000 100 500 50 0 0

1920 1930 1940 1950 1960 1970 1980 1990 2000 1920 1930 1940 1950 1960 1970 1980 1990 2000 Year Year

Figure 1. Time-series of variables examined here for possible relationships with North Sea cod distribution shifts. (a) NAO winter index; (b) Atlantic Multidecadal Oscillation (AMO) index; (c) Hadley interpolated sea surface temperature for the North Sea; (d) North Sea cod fishing mortality, averaged over ages 2–4 years; (e) cod recruitment at age 1; (f) North Sea cod spawning stock biomass. Long-term variability is illustrated by heavy solid lines, representing values smoothed with a low-pass filter with five weights (1, 3, 4, 3, and 1) to remove fluctuations with periods <3 years (following Hurrell 1995).

RESULTS

Shifts in North Sea cod distribution

Long-term cpue data suggest that the spatial distribution of cod within the North Sea did shift during the Twentieth Century but especially markedly during its last decade, and moreover that the distribution during the first decade of the Twenty-first Century has been almost opposite to that during most of the Twentieth Century (Figure 2). For approximately 70 years the distribution of North Sea cod remained remarkably similar: from the 1920s to 1980s, cod abundances were generally high throughout the (especially western) central and northern North Sea. Shifts within this period were comparatively minor; cod cpue tended to be highest around the Orkneys and Shetlands in the 1920s, to the north-east of England from the 1930s to 1950s, in both these areas during the 1970s–1980s. The situation changed considerably during the last two decades, during which a ‘hollowing out’ of the cod population was observed, off the coasts of England and eastern Scotland as revealed by spatial distribution maps of cod cpue (Figure 2). This was also evidenced in a marked eastward shift of cod distribution in the 1990s, with a relative increase in the central-eastern North Sea. In the 2000s, cod abundance in the southern-central North Sea appears to have very much decreased, and high cod cpue values are now mainly concentrated near the edge of the Norwegian Trench and off the Shetlands and Orkneys (Figure 2). These distribution shifts are reflected in changes in the latitudinal, longitudinal, and depth centres of gravity of distribution, which were more marked during recent than during earlier decades (Figure 3). This was most striking for the longitudinal centre of gravity of distribution (Figure 3b): this remained almost constant at 1°E throughout the period 1913–1985, then shifted markedly eastward thereafter, to around 3°E in the late 1990s, but again considerably westward in the early 2000s. The latitudinal centre of gravity showed a southward shift from the 1920s to 1940s, followed by a generally more northward shift from the 1950s onwards, but with fairly irregular changes in the 1980s and 1990s (e.g. relatively south in the 1990s; Figure 3a). The trend in depth distribution of cod closely mimics that of the latitudinal distribution, reflecting the general north–south depth gradient in the North Sea: there was a shallowing shift from the 1920s–1940s, followed by a generally deepening shift from the 1950s to the present (Figure 3c). This deepening shift, however, was only temporarily interrupted in the mid- to late 1990s, when cod distribution was particularly shallow (coinciding with the temporary more southerly and easterly distribution). During the 2000s the centre of gravity of cod distribution has been particularly deep, and particularly far northward, compared to all earlier decades in the time-series.

Figure 2 (next page). Long-term changes in relative cod cpue within the North Sea. For each decade, spatial distribution of cod cpue by British trawlers within the grey-shaded area is indicated by the size of the black circles (proportional to cpue). In rectangles where no cpue data were available in a given decade (no effort or effort <50 hours), white circles represent the long-term average cpue. For each decade, the white cross indicates the centre of gravity of cod distribution, with its standard error (shorter, thick white lines) and standard deviation (longer, thin white lines) in the latitudinal and longitudinal directions.

61° 61° 61° 59° 59° 59° 57° 57° 57° 55° 55° 55° 53° 53° 53°

1920s 1930s Late 1940s 51° 51° 51° 4° 2° 0° 3° 4° 6° 8° 4° 2° 0° 3° 4° 6° 8° 4° 2° 0° 3° 4° 6° 8° 61° 61° 61° 59° 59° 59° 57° 57° 57° 55° 55° 55° 53° 53° 53°

1950s 1960s 1970s 51° 51° 51° 4° 2° 0° 3° 4° 6° 8° 4° 2° 0° 3° 4° 6° 8° 4° 2° 0° 3° 4° 6° 8° 61° 61° 61° 59° 59° 59° 57° 57° 57° 55° 55° 55° 53° 53° 53°

1980s 1990s 2000s 51° 51° 51° 4° 2° 0° 3° 4° 6° 8° 4° 2° 0° 3° 4° 6° 8° 4° 2° 0° 3° 4° 6° 8°

58.5 (a) 58.0 Latitude (°N) 57.5 57.0 56.5

1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2010 3 (b) 2 Longitude (°E) 1 0

1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2010 70 (c) 80 90 Depth (m) 100 110 120

1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 Year

Figure 3. Long-term changes in (a) latitudinal and (b) longitudinal centre of gravity of North Sea cod distribution; and (c) long-term changes in mean depth distribution of North Sea cod. Bars indicate the standard errors around the estimates.

Distribution shifts: correlations with climate and fisheries variables

Correlation analyses suggested that North Sea cod distribution shifts were not straightforwardly related to any of the climatic and fisheries-related variables examined here. There were no significant correlations between any of the four climatic variables (NAO winter index, AMO, Hadley annual mean SST and Hadley winter SST) and the latitudinal, longitudinal, and depth distributions of cod; the only exception was a significant positive correlation between cod longitude and Hadley SST (Table 1).

58.0 58.0 58.0 Latitude (°N) 57.5 57.5 57.5 57.0 57.0 57.0

4 5 6 7 -2 -1 0 1 2 3 -0.4 -0.2 0.0 0.2 0.4 2.5 2.5 2.5 2.0 2.0 2.0 Longitude (°E) 1.5 1.5 1.5 1.0 1.0 1.0

4 5 6 7 -2 -1 0 1 2 3 -0.4 -0.2 0.0 0.2 0.4 105 105 105 95 95 95 Depth (m) 90 90 90 85 85 85 80 80 80 75 75 75

4 5 6 7 -2 -1 0 1 2 3 -0.4 -0.2 0.0 0.2 0.4 Hadley winter NAO winter inde AMO index

Figure 4. Relationships of Hadley winter SST (left), NAO (centre), and AMO (right) with metrics of North Sea cod latitudinal (top), longitudinal (middle) and depth distribution. White symbols refer to the years 2000–2010 (particularly northerly and deep distribution), and black symbols to all earlier years (1913–1999).

Table 1. Correlations (rp) between cod distribution in the North Sea (latitude, longitude, and depth) and variables related to climate and cod fishing pressure and abundance. Correlations significantly different from zero (P < 0.05) are shown in bold.

Latitudinal shift Longitudinal shift Depth shift

Variable rp P rp P rp P Climate NAO winter index –0.042 0.720 0.155 0.182 –0.069 0.556 AMO index –0.074 0.524 0.169 0.145 –0.203 0.078 Hadley SST 0.148 0.208 0.454 <0.0001 0.100 0.397 Hadley winter SST 0.184 0.116 0.194 0.098 0.115 0.328 Fisheries Cod F (ages 2–4) 0.109 0.347 0.568 <0.0001 0.266 0.019 Cod log recruitment –0.075 0.513 –0.038 0.742 0.075 0.516 Cod SSB 0.105 0.364 –0.523 <0.0001 –0.089 0.442

The lack of clear correlations between most climatic variables and cod distribution is illustrated in Figure 4, where the latitudinal, longitudinal, and depth centres of gravity for all years are plotted as a function of Hadley winter SST, NAO winter index, and AMO and no obvious patterns are revealed. However, the northerly and deep distribution during the years 2000–2010 (shown as white symbols in Figure 4) does stand out in the relationship between the AMO index and cod latitudinal and depth distribution; if the analysis would have been restricted to the period 1913–1999, highly significant (P < 0.0001), negative correlations between the AMO and cod latitude and depth distribution would have been found (Figure 4, right-hand panels). The variables examined describing cod fishing pressure and abundance, i.e., fishing mortality (F), recruitment and SSB, were not significantly correlated with cod latitudinal or depth centres of gravity (Table 1, Figure 5), with the exception of a correlation between F and depth distribution (P = 0.019, Table 1) which was however, poorly fitting with the data (Figure 5, lower left panel). There were, however, highly significant correlations between the longitudinal distribution of cod and both fishing mortality and SSB (Table 1). The directions of these correlations were such that the higher cod F and low SSB (characterising recent decades) were associated with more easterly distributions (Figure 5, middle panels), although these relationships appeared non-linear. 58.0 58.0 58.0 Latitude (°N) 57.5 57.5 57.5 57.0 57.0 57.0

0.4 0.6 0.8 1.0 1.2 8.0 8.5 9.0 9.5 50 100 150 200 250 2.5 2.5 2.5 2.0 2.0 2.0 Longitude (°E) 1.5 1.5 1.5 1.0 1.0 1.0

0.4 0.6 0.8 1.0 1.2 8.0 8.5 9.0 9.5 50 100 150 200 250 105 105 105 95 95 95 Depth (m) 90 90 90 85 85 85 80 80 80 75 75 75

0.4 0.6 0.8 1.0 1.2 8.0 8.5 9.0 9.5 50 100 150 200 250 Cod F Log recruitment SSB ('000 t) Figure 5. Relationships of cod fishing mortality (left), log recruitment (centre), cod SSB (right) with metrics of North Sea cod latitudinal (top), longitudinal (middle) and depth distribution. White symbols refer to the years 2000–2010 (particularly northerly and deep distribution), and black symbols to all earlier years (1913–1999).

DISCUSSION

This study shows that distribution shifts of North Sea cod have not been limited to the most recent three decades (as reported by survey-based studies: Hedger et al. 2004; Perry et al. 2005; Rindorf & Lewy 2006; Dulvy et al. 2008), but have taken place throughout the past 100 years. However, the distribution has shifted more markedly and irregularly in the past 2–3 decades than in the entire 70- years period previously. As a result, the current North Sea cod distribution is almost opposite to that during most of the Twentieth Century. Cod are now mainly distributed in the northern- and north- easternmost parts, whereas historically, high abundances were to be found in the western-central North Sea—but the cod stock in this region has been ‘hollowed out’ considerably since the 1980s. The appropriateness of commercial cpue to describe cod distribution could be challenged, given the well-known problems with commercial landings data such as discarding and misreporting (e.g., Enever et al. 2009). However, for the period where both International Bottom Trawl Survey (IBTS) and commercial cpue data are available (late 1970s–2000s), the key findings reported here agreed with survey-based studies (northward shift: Hedger et al. 2004; Perry et al. 2005; deepening shift: Dulvy et al. 2008; but no detailed distribution maps provided in these studies). Further, our distribution maps for the most recent decades (Figure 2) matched IBTS-based maps on cod distribution (ICES Fishmap; ICES 2010). Still, it would be desirable to test statistically how similar survey- and commercial cpue-based maps of cod distribution are in the period of overlapping time- series; this is a step that could not yet be achieved in the present study. This will be particularly relevant, as we anticipate that data issues with commercial cpue related with discarding and under- reporting practices will have been particularly prominent for recent decades, owing to strict quota management regulations since the 1980s (Bannister 2004). Earlier on the British otter trawl fleet fishing fishing for roundfish within the North Sea was fairly uniform and there is evidence that its cod fishing power remained relatively stable for many decades, especially during the period when it was dominated by steam trawlers (i.e. 1900s–early 1960s: Gulland 1964; Engelhard 2008). This suggests that normalised cpue data are appropriate to describe cod spatial distributions (and note that commercial cpue are not used here to derive long-term trends in abundance). Our study revealed that in the most recent, warm, decade, cod showed a particularly northerly and deep distribution compared to almost the entire earlier period (in line with Perry et al. 2005; Dulvy et al. 2008). This is in agreement with expectations from climate change, where a shift to deeper and more northerly waters is to be expected (Rijnsdorp et al. 2009). However, correlation analysis revealed that the shift could not be straightforwardly attributed to temperature change or other climate variables: neither the Hadley annual mean or winter SST, nor the AMO, nor the NAO were significantly correlated with cod’s latitudinal or depth shift (Table 1, Figure 4). Thus it may not be justified to conclude that climate change is the main cause behind the shift (contra Perry et al. 2005), and an explanation of “cod swimming north” to seek out a specific temperature niche is also most likely too simplified (see already discussion in Hedger et al. 2004). The unexpected distribution during the warm mid- to late 1990s stands out, when it was temporarily rather southerly and shallow, and exceptionally easterly. It is noteworthy that this easterly distribution followed the period of most marked decline in cod SSB, which has been generally attributed to both reduced recruitment and consistent high fishing pressure (Figure 1; Bannister 2004;

Horwood et al. 2006), as well as the particularly marked reduction in cod abundance in its previous stronghold, the western-central North Sea off England and Scotland (Figure 2). Moreover, fishing effort is not uniformly distributed, and international otter trawling effort during 1990–1995 was higher close to England and Scotland than in the eastern North Sea (Jennings et al. 1999). Indeed the longitudinal shift of cod was found to be significantly correlated with fishing pressure and SSB, where high F and low SSB were associated with the more easterly distribution (Table 1). This tentatively suggests that heavier depletion in the western than eastern North Sea (earlier reported by Houghton & Flatman 1981; see also Hutchinson et al. 2003) could be related to the eastward shift of the 1990s, although further analysis is required to substantiate this. The apparent lack of significant correlations between cod distribution shifts and climatic variables is in contrast with recent findings on long-term distribution shifts of two flatfish species in the North Sea (Engelhard et al. 2011), where plaice showed a significant northwestward and deepening shift in relation to warming sea temperatures, and where sole showed a shallowing, southwestward shift which could be attributed to both warming temperatures and fishing pressure. Why are links between climatic variables and metrics of cod distribution considerably less clear than those exhibited by the two flatfish species? Perhaps our metrics to describe distributional responses (latitudinal, longitudinal, and depth centre of gravity) are less appropriate for cod than for plaice and sole, given that cod have tended to show a more widespread and irregular distribution pattern within the North Sea (Daan et al. 1990; Andrews et al. 2005) than plaice and sole, with high abundances in a more distinct region (mainly the shallower southern and east-central regions; Engelhard et al. 2011). There is evidence of sub-structuring of North Sea cod into distinct subpopulations (Hutchinson et al. 2001), which appear to have differed in rates of depletion and local recruitment (Hutchinson et al. 2003; Holmes et al. 2008). Thus the use of a single metric such as latitudinal centre of gravity might not fully capture the distribution dynamics of North Sea cod. Similarly, whereas beam trawl fishing effort targeting flatfish has been consistently distributed in the shallower southern-central North Sea, otter trawling effort targeting roundfish has shown a more patchy and disjunct distribution (Jennings et al. 1999; Callaway et al. 2002). Cod fishing mortality might not fully capture local differences in depletion rates, which could have resulted in the hollowing out of the west-central North Sea cod stock. Cod are moreover capable of very extensive seasonal migrations (e.g. Righton et al. 2007; but see Hunter et al. 2004 on long-distance movements by plaice). There is evidence based on information from data storage tags, that in spite of climate change, individual adult North Sea cod actively sought out warmer-than-average water temperatures to reside in (Neat & Righton 2007); this was especially the case in the relatively warm, southern North Sea. A few cod were exceptions actively seeking out colder temperatures, confirming that cooler waters were within reach of the fish (Neat & Righton 2007), and possibly coinciding with physiological and genetic differences between sub-stocks (Petersen & Steffensen 2002). Most did not, however, leading the authors to conclude that the changing thermal regime of the North Sea is not yet causing adult cod to move to cooler waters (but warming temperatures might still impact recruitment and prey availability). In summary, although we have documented important distribution shifts of cod throughout the course of the past century, it has proven difficult to partition especially the latitudinal and depth shifts to climatic or fisheries variables; the significant correlations between the longitudinal shift and

both F and SSB warrant further study. We conclude that it would be too simplistic to solely attribute the recent, northward shift of cod to climate change (in line with Neat & Righton 2007, but less so with Perry et al. 2005). The next challenge is a more comprehensive analysis to what extent the current distribution, different as it is from historic patterns, may have resulted from an interplay between climate, local differences in depletion, productivity and possibly predation—so far, the relative importance of these factors remains elusive.

ACKNOWLEDGEMENTS

This study was supported by the Department for Food, Environment and Rural Affairs of the UK (Defra project M1108 ‘100 Years of Change in Fish and Fisheries’) and by the European Union (FP6 project RECLAIM ‘Resolving Climatic Impacts on Fish Stocks’). Joyce Petrie, Bill Turrell, and Phil Kunzlik (Marine Scotland) provided Scottish fisheries data from 1968 onwards. Suzy Baldry and Phil Davison contributed to the digitising of Cefas historical fisheries data, and Peter Robinson extracted the data from the Fisheries Activity Database of Defra/Cefas. The study benefited from earlier discussions with Ken Drinkwater, Mikko Heino, Laurie Kell, Adriaan Rijnsdorp, and Andy South.

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