ICES Journal o f M arin e Science (2011), 68(6), 1 0 9 0 -1 1 0 4 . doi:10.1093/icesjm s/fsr031
Nine decades of North Sea sole and plaice distribution
G eorg H. E n gelh ard 1* John K. P in n eg a r1, Laurence T. K eli1'2, an d Adriaan D. R ijnsdorp3'4
l Centre fo r Environment, Fisheries and Aquaculture Science (Cefas), Pakefield Road, Lowestoft NR33 OHT, UK
2International Commission fo r the Conservation o f Atlantic Tunas (ICCAT), C/Corazón de Maria, 8, 28002 Madrid, Spain
^Wageningen Institute fo r Marine Resources and Ecosystem Studies (IMARES), IJmuiden, The Netherlands
4Aquaculture and Fisheries Croup, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
*Corresponding Author: tel: + 44 IS02 527747; fax: + 44 IS02 513865; e-mail: georg.engelhard@cefas.co.uk.
Engelhard, C. H., Pinnegar, J. K., Keli, L. T., and Rijnsdorp, A. D. 2011. Nine decades of N orth Sea sole and plaice distribution. - ICES Journal of
Marine Science, 68: 1090-1104.
R eceived 1 July 2010; a c c e p te d 13 Feb ru ary 2011; a d v a n c e a ccess p u b lic a tio n 11 A pril 2011.
R ecent stu d ies based m ainly o n research survey d a ta suggest th a t w ithin th e N orth Sea, sole Solea solea a n d plaice Pleuronectes platessa
have e xhibited d istrib u tio n shifts in re c e n t d e c a d e s— on average so u th w a rd for sole a n d n o rth w a rd to d e e p e r w aters for plaice. V arious
h y p o th eses m ay a c c o u n t for such shifts, including clim ate ch an g e effects a n d m o re intensive fishing in so u th e rn a n d shallow er w aters;
have m ad e use o f a un iq u e d a ta se t o f c atch a n d effort d a ta for British N o rth Sea traw lers; th ese cover nine d e ca d es (sp an n in g th e
p eriod 1 9 1 3 -2 0 0 7 ) a n d are spatially d etailed by ICES rectangle (0.5° latitu d e by 1° longitude). W e quantify, for th e first tim e,
long-term d istrib u tio n changes o f N o rth Sea sole a n d plaice over a p eriod ap p ro ac h in g a century, a n d d e m o n s tra te th a t th e distri­
b u tio n shift in plaice w as a ttrib u ta b le to clim ate ch an g e ra th e r th a n to fishing, b u t th a t b o th clim ate a n d fishing played a role in
th e d istrib u tio n shift o f sole. T he discussion also highlights th e p o ten tial im p a c t o f additio n al factors, including e u tro p h ica tio n ,
prey availability, a n d h a b ita t m odification.
Keywords; climate, depth, fishing, latitude, longitude, plaice, sole.
Introduction
T em perature is o n e o f th e p rim a ry factors, along w ith food avail­
ability a n d th e pro v isio n o f suitable spaw ning a n d n u rsery
grounds, th a t d e te rm in e fish d istrib u tio n p atterns, a n d m o st fish
species te n d to prefer a specific te m p e ra tu re range (C o û tan t,
1977; R ijnsdorp et al., 2009). C onsequently, shifts in lo n g -term
tem p e ra tu re resulting fro m clim ate change are expected to result
in contractio n s, expansions, o r shifts in fish d istrib u tio n , especially
near the p e rip h e ry o f a species’ range (review: P innegar et al.,
2010). In the N o rth Sea, a w a rm ing tre n d has h a p p en e d over the
past th ree decades, w ith a p articu larly steep tem p e ra tu re rise in
1 9 8 8 -1 9 8 9 , a lth o u g h th ere w ere also som e relatively cold years;
this has coincided w ith a n o rth w a rd shift in th e d istrib u tio n o f
m any, b u t n o t all, fish species in the N o rth Sea (Beare et al.,
2004; H edger et al., 2004; P erry et al., 2005), som etim es b y as
m u c h as 400 k m . D ulvy et al. (2008) d em o n strated , however,
th a t there has b e en n o n e t shift in the m ea n latitu d e o f th e fish
assem blage as a w hole (because som e w ere m oving n o rth a n d
som e w ere m o ving so u th ), b u t th ere has been a d eepening a n d
this has h a p p en e d at a rate o f a ro u n d —3.6 m per decade
(D ulvy et al., 2008).
In th e N o rth Sea, plaice Pleuronectes platessa a n d sole Solea
solea are principally cau g h t in a m ixed flatfish beam -traw l
fishery. L andings o f plaice b y w eight are appro x im ately five
tim es greater th a n those o f sole; how ever, because sole are c o n ­
siderably m o re valuable, landings o f the tw o species are roughly
o f equal value overall (Pilling et al., 2008). Plaice a n d sole have
© C row n c opyright [2011]
b een targeted b y fishing fleets since th e early n in ete en th c en tu ry
a n d conseq u en tly good fishery statistics exist for these species,
unlike for m an y others. B oth species have displayed d istin ct d istri­
b u tio n shifts since th e 1980s. F or plaice, a shift to m o re offshore
w aters has b e en re p o rte d (van Keeken et al., 2007), at a “deep en ­
in g ” rate o f - 3 .9 6 m p e r decade (D ulvy et al., 2008). For sole,
P erry et al. (2005) re p o rte d a generally so u th w ard d istrib u tio n
shift, i.e. o p p o site to the an tic ip a te d response to clim ate change
in th e n o rth e rn hem isphere, assum ing a latitu d in a l g radient o f sea­
w ater tem p eratu res, a n d th e a u th o rs suggested th a t this m ig h t
relate to im p ro v ed e n v iro n m en ta l co n d itio n s in th e so u th e rn
N o rth Sea, because o f ru n -o ff fro m rivers (i.e. h igher p ro d u c tiv ity
in recent years). T here has also b een a c o n c o m ita n t shift to shal­
low er w aters, a t a rate o f + 7 .6 4 m per decade (D ulvy et al.,
2008). H ow ever, in te rn atio n al fisheries landings d a ta for the
m o st recent years tentatively suggest a n o rth w a rd range expansion
for sole (R ijnsdorp, 2010), so th e re lationship betw een d istrib u tio n
a n d clim ate in this w arm -w ater species rem ains p o o rly u n d e rsto o d
a n d u n c ertain (D ulvy et al., 2008).
M ost studies o n N o rth Sea fish d istrib u tio n have so far been
based o n fishery -in d ep en d en t survey d a ta from go v ern m en t in sti­
tutes a n d have been lim ited to the m o st recent th ree to four
decades (H edger et al., 2004; P erry et al., 2005; H id d in k a n d ter
H ofstede, 2008), because o f scarcity o r absence o f older, consist­
ently collected survey d a ta w ith reasonable spatial coverage. O ver
this p e rio d (1 9 7 0 -2 0 1 0 ), how ever, sea tem p eratu res in the
N o rth Sea generally have increased in th e so u th a n d at th e sam e
tim e fishing pressure has been consistently h igher in th e so u th e rn
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b u t th e relatively sh o rt tim e-sp an o f d a ta se ts analysed so far ( ~ 3 decades) has c o m p lica te d th e sep aratio n o f th ese tw o effects. W e
N in e decades o f N orth Sea sole a n d plaice distribution
p a rt th a n farth er n o rth (Jennings et al., 1999). T his m akes it p a r­
ticularly h a rd to disentangle the p o ten tial effects o f clim ate change
a n d fishing pressure o n d istrib u tio n shifts (and these hypotheses
are n o t m u tu a lly exclusive), because a greater rate o f
fishery-induced d e p le tio n in the so u th e rn N o rth Sea th a n the
n o rth w o u ld look like a n a p p are n t “n o rth w a rd ” shift, as m ight
be an ticip ated to have h a p p en e d u n d e r clim ate change. T his diffi­
culty in in te rp re ta tio n has m o tiv ated th e c u rre n t stu d y b ased o n a
u n iq u e d ataset o f B ritish co m m ercial catch per u n it effort (cpue)
records sp a n n in g a far longer tim e -sp a n — th e past n in e decades—
covering b o th w arm in g a n d cooling periods a n d inclu d in g periods
o f c o n trastin g levels o f fishing effort.
H ere we quantify, for th e first tim e, lo n g -term d istrib u tio n
changes o f N o rth Sea sole a n d plaice over a p e rio d ap p ro ach in g
a century. W e in te rp re t the findings in th e light o f clim ate
change a n d lo n g -te rm changes in fishing pressure. W e test the
hypotheses that:
2. L onger tim e-series o f fish d istrib u tio n d a ta offer greater insight
in to likely m ec h an ism s/in flu e n c es th a n sh o rte r tim e-series
derived from fish ery -in d ep en d en t surveys.
were calculated b y rectangle for a large area encom passing m o st o f
th e N o rth Sea (shaded in Figure 1).
As a n ap p ro ac h to quan tify lo n g -te rm changes in p o p u latio n
d istrib u tio n , we calculated the “centres o f gravity” o f the la titu d i­
nal, lo n gitudinal, a n d d e p th d istrib u tio n s o f the tw o species (as in
H ein o et al., 2003; see also R in d o rf a n d Lewy, 2006). T his analysis
was b ased o n a n area w ith in th e N o rth Sea th a t inclu d ed o nly those
rectangles w ith cpue d a ta for th e m o st years in the tim e-series (see
th e polygon line in Figure 1). W ith in this polygon, th e latitu d in al
(o r lo n g itu d in al) centre o f gravity o f d istrib u tio n in a given year
was calculated as the average o f the latitudes (o r longitudes) o f
all rectangle centres, w eighted b y the cpue value in each rectangle.
W eighted sta n d ard deviations a n d sta n d ard erro rs o f th e w eighted
m ea n latitudes w ere calculated (Bevington, 1969). T he centres o f
gravity o f d e p th d istrib u tio n s w ere calculated analogously and,
given th a t b o th flatfish species are bottom -dw ellers, based o n the
m ea n sea d e p th in a n y given rectangle.
W e exam ined sole a n d plaice d istrib u tio n in relatio n to
(i) clim ate variables a n d (ii) fishing pressure. As a broad-scale
clim ate in dicator, the N o rth A tlantic O scillation (N A O ) w inter
in d ex (D ecem ber o f th e previous year to M arch o f th e focal
year) for 1 9 1 3 -2 0 0 7 was tak en from Jones et al. (1997), w ith
3. D ata fro m co m m ercial fisheries can yield useful insight in to the
lo n g -te rm im plications o f clim ate change.
Methods
For the p e rio d 1 9 1 3 -1 9 8 0 , d a ta w ere o b tain e d fro m “statistical
ch arts” (catalogued in E ngelhard, 2005) th a t w ere p ro d u c ed by
th e UK M in istry o f A griculture, Fisheries a n d Food [MAFF; no w
th e UK D e p a rtm e n t for E n vironm ent, F ood a n d R ural Affairs
(D efra)]. T hese display fishing effort (h o u rs fished) a n d fish la n d ­
ings b y B ritish o tte r traw lers (either steam - o r m o to r-d riv en ) for
each ICES rectangle (0.5° latitu d e b y I o lo ngitude) in the N o rth
Sea. These d a ta reco rd all fish th a t w ere lan d ed b y the o tte r
traw l fleet in to E ngland a n d W ales (1913, 1 9 6 8 -1 9 8 0 ) o r in to
E ngland, Scotland, a n d W ales (1 9 2 0 -1 9 6 7 ). For the p erio d
1 9 6 8 -2 0 0 7 , d a ta o n o tte r traw ler landings in to S cotland were
o b tain e d fro m th e Fisheries M an ag em en t D atabase o f M arine
S cotland (cf. G reenstreet et a í, 1999). F or 1 9 8 2 -2 0 0 7 , data o n
o tte r traw l landings in to E ngland a n d W ales w ere o b tain ed from
th e Fisheries A ctivity D atabase o f D efra/C efas.
O ver th e tim e -sp a n exam ined, im p o rta n t im p ro v em en ts have
h a p p en e d in th e flatfish catching pow er, o r technical efficiency,
o f o tte r traw lers (W im penny, 1953; R obinson, 2000), a lth o u g h a
recent lo n g -te rm analysis suggested th a t plaice fishing pow er o f
m o to r o tte r traw lers a ro u n d the M ille n n iu m was n o t m arkedly
h igher th a n th a t o f steam o tte r traw lers o f the 1920s (b u t an
o rd e r o f m ag n itu d e low er th a n in b eam traw lers; Engelhard,
2008). O u r a im was n o t to analyse tem p o ral changes in absolute
cpue values, b u t ra th e r to look at tren d s in spatial d istrib u tio n
o f catches. W e therefore no rm alized th e cpue values in any given
year (divided b y th e a n n u al m ean ), to overcom e th e confusing
effect o f a n increase in fishing pow er. W e assum ed th a t relative
cpue b y the co m m ercial fleet gives an a p p ro p ria te in d ic a tio n o f
the spatial d istribution o f the species, b u t acknowledge th at p otential
bias m ight arise from uneven spatial d istribution o f effort b y m ore
o r less pow erful vessels w ithin the N o rth Sea. By decade, cpue values
Figure 1. M ap of th e N orth Sea displaying, for each rectangle, the
num ber of years in th e 77-year time-series w here British o tte r trawler
cpue data were available (based on th e rule th a t a t least 10 h of
fishing effort had occurred in the rectangle in the given year). The
grey-shaded area encom passes those rectangles where we calculated
cpue by year or decade for spatial distribution maps. The thick-lined
polygon encom passes those rectangles included in analyses on
centres of gravity of cpue distributions.
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1. L ong-term shifts in sole a n d plaice d istrib u tio n are b e tte r
explained b y clim ate variables th a n b y indices o f fishing
pressure.
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u p d a te d values p ro v id ed o n lin e b y th e C lim atic Research U nit,
U niversity o f East A nglia, N orw ich, U K (w w w .cru.uea.ac.uk/
~ tim o /p ro jp a g e s/n a o _ u p d a te .h tm ; Figure 2a). T he NA O is
associated w ith speed a n d d irec tio n o f w esterly w inds across the
N o rth A tlantic a n d is particu larly im p o rta n t in w in ter w h en it
exerts a stro n g influence o n E u ro p ean w eather p a tte rn s a n d o n
A tlantic w ater inflow in to th e N o rth Sea; a positive NA O is gen er­
ally linked w ith stro n g w in d c irculation a n d h igher atm ospheric
a n d sea tem p eratu res in w estern E urope (H urrell, 1995; Jones
et al., 1997; O ttersen et al., 2001). W e also considered the
A tlantic M ultidecadal O scillation (A M O ), a clim ate m o d e th at
m anifests itself as a 2 0 -3 0 -y e a r cycle in d e -tre n d ed sea surface
tem p e ra tu re series for th e N o rth A tlantic. These d a ta (back to
1871) w ere o b tain e d fro m NOAA (G lobal C hange M aster
D irectory). A n u m b e r o f lo n g -te rm coastal tem p e ra tu re tim eseries w ere exam ined fro m sites a ro u n d th e N o rth Sea, including
those fro m M arsdiep (D u tc h coast; o b tain e d fro m M ackenzie
a n d Schiedek, 2007), H elgoland R oads (G erm an coast; o b tain e d
fro m W iltshire a n d M anly, 2004), a n d D over (U K coast; o b tain e d
fro m w w w .cefas.co.uk/data.aspx). As a m o re generic in d ic a to r o f
sea te m p e ra tu re v ariations w ith in th e N o rth Sea, the H adley
in te rp o lated sea surface tem p e ra tu re (H adlSST ) tim e-series was
used (Figure 2b). A n n u a l m ea n o f sea surface tem peratures,
in te rp o lated to I o latitu d e b y I o longitude, was used as described
b y R ayner et al. (2003), w ith u p d a te d values p rovided online by
th e UK M eteorological Office. For seabed te m p e ra tu re (SBT), n o
com prehensive tim e-series covering th e en tire span o f this stu d y
was available, b u t fo r a sh o rte r p e rio d (1980 o n ), w in ter SBT
d a ta w ere calculated as average SBT in 80 ICES rectangles
sam pled d u rin g the a n n u a l w in ter In tern a tio n a l B o tto m Trawl
Surveys (IBTS) o f ICES (o b tain ed from D ulvy et a í , 2008).
To describe the effects o f fishing pressure, estim ates o f fishing
m o rta lity (F ) o n 4 -8 -y e a r-o ld plaice for the years 1 9 2 9 -1 9 3 7
a n d 1 9 4 7 -1 9 9 2 w ere tak en from R ijnsdorp a n d M illn er’s (1996)
lo n g -te rm stu d y o n N o rth Sea plaice stock dynam ics. Estim ates
o f F for 4 -8 -y e a r-o ld sole for the years 1 9 5 7 -1 9 9 3 w ere taken
05
1920
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1960
Y ear
1980
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Figure 2. Time-series of environm ental variables and fishing pressure exam ined here for possible relationships with N orth Sea sole and plaice
distributions, (a) NAO w inter index; (b) Hadley interpolated annual average sea surface tem perature for the N orth Sea; (c) N orth Sea sole
fishing mortality, averaged over ages 4 - 8 years (from Millner and Whiting, 1996); and (d) N orth Sea plaice fishing mortality, averaged over
ages 4 - 8 years (from Rijnsdorp and Millner, 1996). Long-term variability is illustrated by heavy solid lines, representing values sm oothed with a
low-pass filter with five weights (1, 3, 4, 3, and 1) to remove fluctuations with periods < 3 years (following Hurrell, 1995).
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(b)
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N in e decades o f N orth Sea sole a n d plaice distribution
7
-
1920s
1930s
L a te 1
1950S
1960s
1970S
1990s
2000s
7
1980s
Figure 3. Long-term changes in relative sole cpue within th e N orth Sea. For each decade, spatial distribution of sole cpue by British trawlers
within th e grey-shaded area is indicated by th e area sizes of the black circles (proportional to cpue). In rectangles where no cpue data were
available in a given decade (no effort), white circles represent th e long-term average cpue. For each decade, the w hite cross indicates the
centre of gravity of sole distribution, with its standard error (shorter, thick w hite lines) and standard deviation (longer, thin white lines) in the
longitudinal and latitudinal directions.
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• • •
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G. H . Engelhard et al.
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Figure 4. Long-term changes in (a) latitudinal and (b) longitudinal centre of gravity of N orth Sea sole distribution (calculated as th e m ean
latitude and longitude weighted with sole cpue; bars indicate s.e. of weighted means); and (c) long-term changes in m ean depth distribution of
N orth Sea sole (with s.e.).
from M illner a n d W h itin g (1996). B oth F tim e-series were
extended w ith recent d a ta from ICES W o rking G roup rep o rts
(ICES, 2009). These fishing m o rta lity tim e-series are illustrated
in Figure 2c a n d d.
W e used c o rre latio n s as a first a p p ro a c h to explore w hich
e n v iro n m e n ta l a n d / o r fishing pre ssu re variables m ig h t be
associated w ith d e sc rip to rs o f sole a n d plaice d is trib u tio n
(latitu d in a l, lo n g itu d in al, a n d d e p th ). P e a rso n ’s c ro ss-m o m e n t
co rre latio n s (>p) w ere used, because n o n e o f th e variables
displayed d istrib u tio n s significantly differen t fro m n o rm a lity
(o n e -sam p le K o lm o g o ro v -S m irn o v tests, p > 0.05). T here
was, how ever, a m o d e ra te o r w eak a u to c o rre la tio n b etw een
several tim e-series variables. To a cc o u n t fo r this, th e test p r o ­
c ed u re for significance o f c o rre latio n s was a d ju ste d follow ing
P yper a n d P e te rm a n [1998, E q u a tio n (1 )], b y re d u cin g the
“effective” degrees o f free d o m (a n d th erefo re p -v alu es) a cc o rd ­
ing to th e degree o f a u to c o rre la tio n (a d ju ste d p-v alu es are
referred to here as p a¿ß .
M ultiple linear regressions w ere th e n used as a n ap p ro ach to
exam ine th e relative im p o rta n ce o f e n v iro n m en ta l a n d fishing
pressure variables as d e te rm in a n ts o f sole a n d plaice d istrib u tio n .
As explan ato ry variables, these m odels inclu d ed fishing pressure
(sole F o r plaice F ), th e NAO w in ter index, A M O , a n d H adley
SST (o th er sea tem p e ra tu re tim e-series w ere closely correlated
w ith H ad ley SST, a n d w ere n o t inclu d ed to avoid th e p ro b lem o f
m u lticollinearity). Initially, we started w ith a m o d el w ith all c o n ­
sidered e x planatory variables, b u t n o interactions. F or exam ple, for
sole latitu d in a l d istrib u tio n , th e startin g m o d el was
S o le la titu d e ~ S o le i7 + N A O + A M O + H adley SST.
(1)
H ow ever, o nly param eters th a t significantly c o n trib u te d to the fit
(p < 0.05) w ere retain ed in th e m o d el fo rm u latio n s. Finally, we
checked w h eth er any se c o n d -o rd e r interactio n s betw een clim ate
a n d fishing pressure w o u ld significantly im p ro v e th e fit (p <
0.05). F or the final m odel, we give th e stan d ard ized ß coefficients,
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CT>
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N in e decades o f N orth Sea sole a n d plaice distribution
1930s
1950s
1960s
1980s
1990s
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1920s
2000s
Figure 5. Long-term changes in relative plaice cpue within the N orth Sea. For each decade, spatial distribution of plaice cpue by British
trawlers within the grey-shaded area is indicated by th e area sizes of th e black circles (proportional to cpue). In rectangles where no cpue data
were available in a given decade (no effort), w hite circles represent the long-term average cpue. For each decade, the white cross indicates the
centre of gravity of plaice distribution, with its standard error (shorter, thick w hite lines) and standard deviation (longer, thin w hite lines) in
th e longitudinal and latitudinal directions.
G. H . Engelhard et al.
1096
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o b tain e d after sta n d ard iza tio n (su b tractin g th e m ea n a n d dividing
b y th e sta n d ard deviation) o f th e e x planatory variables. T he sta n ­
dard ized ß coefficients are indicative o f th e relative stren g th o f the
relationships betw een e n v iro n m en t a n d fishing pressure w ith each
fish d istrib u tio n m etric; it sh o u ld be n o ted , how ever, th a t they
can n o t be directly in te rp rete d as su b stan tiatin g causative effects.
Results
Shifts in fish distributions
O ver the past n in e decades, b o th sole a n d plaice displayed long­
term , m ultid ecad al changes in spatial d istrib u tio n . M agnitudes
o f each shift regarding “centres o f gravity” o f latitu d e a n d longi­
tu d e w ere ~ l ° - 2 ° fo r b o th species (co rresp o n d in g to 142 km
for plaice a n d 93 k m fo r sole); those o f d e p th d istrib u tio n s were
~ 2 0 m for plaice, < 1 0 m for sole. T he d irec tio n a n d tim in g o f
shifts were, however, very different for the tw o species.
Sole distribution shifts
Sole have always b e en d istrib u te d in th e shallow so u th e rn a n d
so u th eastern N o rth Sea, w ith o nly very sm all n u m b ers in the
n o rth e rn N o rth Sea, w here they are absent fro m m o st rectangles.
F igure 3 show s the d istrib u tio n o f sole cpue over the N o rth Sea
b y decade, fro m the 1920s to th e 2000s. In the 1920s a n d 1930s,
high sole cpue values w ere d istrib u te d evenly betw een the
S o u th e rn B ight a n d G erm an Bight, b u t th e relative im p o rta n ce
o f th e G erm an B ight increased d u rin g th e 1950s a n d 1960s.
Since th e 1970s, th e im p o rta n ce o f th e G erm an B ight has
decreased, a n d fro m th e 1980s on, sole cpue has been considerably
h igher in th e S o u th e rn Bight, especially close to th e T ham es
E stuary a n d so u th e aste rn E ngland. U nfortunately, w e lack
B ritish o tte r traw ler cpue d a ta for th e so u th e aste rn m o st p a rt o f
th e G erm an B ight for m u c h o f the 1990-2000s.
N o rth Sea sole have exhibited m ark ed m ultid ecad al flu ctu ­
atio n s in th e ir latitu d in a l centre o f gravity (Figure 4a), w hich
shifted fro m ~ 5 3 ° N in th e 1920s, n o rth w a rd s to ~ 5 4 ° N in the
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Figure 6. Long-term changes in (a) latitudinal and (b) longitudinal centre of gravity of N orth Sea plaice distribution (calculated as the m ean
latitude and longitude weighted with plaice cpue; bars indicate s.e. of weighted means); and (c) long-term changes in m ean dep th distribution
of N orth Sea plaice (with s.e.).
1097
N in e decades o f N orth Sea sole a n d plaice distribution
1960s, th e n southw ards again to ~ 5 3 ° N in the 1990s (and to a
so u th e rn m o st latitu d e o f 52.5°N in 2002). T here have b e en less
sm o o th a n d m o re irregular shifts in lo n g itu d in al centre o f
gravity (Figure 4b), n o tab ly a w estw ard shift fro m ca. 1960 to
2000 (reflecting increased relative im p o rta n ce o f th e T ham es
E stuary region). T here has b e en a m o re lim ited shift in d e p th d is­
trib u tio n (Figure 4c), b u t this b ro ad ly parallels the latitu d in al
p attern .
N o rth Sea. F ro m th e 1950s to the 1980s, th ere was a n eastw ard
lo n g itu d in al shift (Figure 6b) related to th e te m p o ra ry m u ch
greater im p o rta n ce o f the e a s t-c e n tra l N o rth Sea in this period.
T he centre o f gravity “ju m p e d ” w estw ards b y 3° lo n g itu d e from
1988 to 1995 (a n d b y > 1 ° in 1 9 9 3 -1 9 9 4 alone), the latter reflected
a n a p p are n t p o p u la tio n collapse in th e e a s t-c e n tra l N o rth Sea, b u t
also th e recently increased a b u n d an c e o ff Scotland.
Correlations betw een environm ental and fisheries
variables
Plaice distribution shifts
Plaice are generally m o re a b u n d a n t in th e so u th e rn a n d central
pa rts o f the N o rth Sea th a n in the n o rth . T heir d istrib u tio n
differs fro m sole in being o n average m u ch m o re n o rth e rn a n d
encom passing m o st o f th e n o rth e rn N o rth Sea, w here, a lthough
at low er cpue values, th ey are typically caught b y o tte r traw lers
in m o st rectangles, except for th o se th a t com prise the deepest
w aters in th e no rth w est a n d the N orw egian T rench (Figure 5).
Plaice have over th e past n in e decades also exhibited m ajo r d is­
trib u tio n shifts, b u t q u ite different from th o se observed for sole
(Figure 5). D u rin g th e 1920-1940s (a n d in 1913), the highest
plaice cpue values w ere observed in the S o u th e rn B ight a n d the
G erm an Bight, in rectangles closest to th e coast o f so u th eastern
E ngland, th e N etherlands a n d G erm any, a n d w ith cpue values
rap id ly decreasing n o rth w a rd s a n d northw estw ards. D u rin g the
1960-1980s, the e a s t-c e n tra l N o rth Sea becam e far m o re im p o r­
tan t, in clu d in g a n offshore area stretching fro m th e D ogger B ank
n o rth to th e G reat a n d T ittle Fisher Bank, b u t w ith relatively low
c pue along m o st o f th e E nglish a n d Scottish coasts. D u rin g the
1990-2000S, plaice cpue d ro p p e d m arkedly in the previously
im p o rta n t e a s t-c e n tra l N o rth Sea, especially in m an y rectangles
close to D e n m ark a n d G erm any, b u t rem ain ed high in the
c entral N o rth Sea. In the (late) 1990-2000s, th ere was a sudden,
m ark ed increase in relative plaice cpue o ff Scotland, O rkney, a n d
Shetland.
F ro m the sta rt o f o u r tim e-series in 1913 to W orld W ar II, the
centre o f gravity o f N o rth Sea plaice d istrib u tio n rem ain ed c o n ­
sta n t regarding latitude, longitude, a n d d ep th . Since then,
how ever, th e centre o f gravity has alm ost c o n tin u o u sly shifted
n o rth w a rd s b y m o re th a n 2° latitu d e fro m th e late 1940s to the
2000s (Figure 6a). A ccordingly, plaice have m oved offshore to
greater d ep th s b y ~ 2 0 m since 1947 (Figure 6c), tracking th e lati­
tu d in a l shift a n d reflecting th e n o r t h - s o u t h d e p th grad ien t in the
Before p roceeding to exam ine co rrelations betw een clim ate v a ri­
ables a n d /o r fishing pressure vs. sole a n d plaice d istrib u tio n , it
is necessary to de te rm in e w h eth er such variables are them selves
correlated. A n analysis revealed th a t all sea surface a n d b o tto m
tem p e ra tu re datasets (H adley, M arsdiep, H elgoland, a n d D over
SST; IBTS w in ter SBT) w ere highly correlated (all rp> 0.75, all
p a d j IO- 5 , adjusted fo r a u to c o rrela tio n ). Similarly, th e NAO
w in ter in d ex exhibited a stro n g positive co rrelatio n w ith H adley
SST (rp = 0.462, p¡¡¿j < IO- 7 ), b u t b y c ontrast, the A M O index
was o nly weakly co rrelated w ith H ad ley SST (rp = 0.227, p adj =
0.04), despite itself being derived from the c o m b in ed H adley
SST a n d N O AA O I SST datasets.
Sole a n d plaice fishing m o rta lity w ere strongly correlated w ith
each o th er (rp = 0. 678, p¡¡¿j< 0.0002), b u t n e ith e r was signifi­
cantly co rrelated w ith a n y o f the clim ate variables (all rp< 0.24,
a ll P a d j> 0 .1 ) .
Because all sea surface tem p e ra tu re datasets w ere highly c o rre ­
lated, fu rth e r analysis o n relationships betw een clim ate a n d sole o r
plaice d istrib u tio n s was o nly carried o u t using the H ad ley SST
d ataset (along w ith NA O a n d A M O ), because this was ju d g ed to
provide a representative in d ex o f regional hydroclim ate.
Distribution shifts in relation to clim ate and fishing
All th ree m easures o f N o rth Sea sole a n d plaice d istrib u tio n —
m ea n latitude, longitude, a n d d e p th — w ere strongly correlated
w ith the H adley a n n u al in d ex o f sea surface tem p e ra tu re in the
N o rth Sea (Table 1). T he d irec tio n o f co rrelations was such th a t
for sole, w arm er tem p eratu res were associated w ith m o re
so u th e rn , w estern, a n d shallow er d istrib u tio n p a tte rn s (Figure 7,
left panels). Conversely, for plaice, h igher tem p eratu res were
associated w ith a m o re n o rth w e stern a n d a deeper d istrib u tio n
Table 1. Correlations (rp) betw een sole and plaice distribution in the N orth Sea (latitude, longitude, and d epth) and variables related to
clim ate and fishing pressure.
Latitudinal shift
Variable
Sole
NAO w inter index
AM O index
Hadley SST
Sole F (ages 4 - 8 )
Plaice
NAO w inter index
AM O index
Hadley SST
Plaice F (ages 4 - 8 )
rP
-
0.246
-0 .0 5 2
0.355
0.781
Longitudinal shift
Depth shift
P adj
rP
P adj
rP
P adj
0.035
- 0 .1 7 4
0.017
0.138
0.887
-0 .2 2 5
-0 .1 0 7
0.054
0.374
0.393
0.631
<0.005
<0.001
-0.022
-0.0 5 4
0.850
0.652
0.666
<0.005
<0.0001
-0.015
-0.085
0.900
0.478
0.431
-0.098
0.348
0.826
<0.005
<0.0001
-0.085
0.467
<0.001
-0.530
-0.443
<0.0002
<0.0005
0.449
-0.115
0.375
0.455
-0.046
<0.0005
0.718
There was weak or moderate autocorrelation within these variables. To account for this, the test procedure for significance of correlations was adjusted according
to autocorrelation following Pyper and Peterman [1998; Equation (1)]. Correlations different from zero at adjusted p < 0.005 are shown emboldened.
G. H . Engelhard et al.
1098
(b).
0) m
'S s
CO -
(d)
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.2
0.3
0.4
0.5
0.6
0.7
0.8
o
if
o
cô
CM "
7» •
y ••
o
O.
.
9.5
10.0
10.5
11.0
11.5
Hadley SST (°C)
Sole F (ages 4 -8 )
Figure 7. Relationships of Hadley SST (left) and sole fishing pressure (right) with m etrics of N orth Sea sole distribution: (a and b) latitudinal
centre of gravity; (c and d) longitudinal centre of gravity; and (e and f) m ean d ep th distribution. Regression lines indicate significant
relationships.
p a tte rn (Figure 8, left panels). Each o f th e co rrelations w ith H adley
SST was significant beyond th e p a¿, < 0.005 level.
T he NAO w in ter in d ex was significantly correlated o nly w ith the
latitu d in a l d istrib u tio n o f sole a n d n o t very strongly (p a¿j = 0.035);
the co rrelatio n w ith the d e p th d istrib u tio n o f sole a p p ro ach ed sig­
nificance (pa¿j = 0.054), such th a t a m o re negative phase o f the
NAO w o u ld be associated w ith m o re so u th e rn a n d p erhaps
deeper d istrib u tio n o f sole (Table 1). T he NAO w in ter in d ex was
n o t co rrelated w ith sole lo n g itu d in al d istrib u tio n a n d w ith n o n e
o f th e m easures o f plaice d istrib u tio n . How ever, plaice lo n g itu d in al
d istrib u tio n was strongly co rrelated w ith th e A M O in d ex (p¡¡dj<
0.0002), such th a t a m o re positive phase o f A M O was associated
w ith a m o re w estern d istrib u tio n o f this species.
Fishing m o rta lity o n sole (averaged over ages 4 - 8 years) was
correlated highly significantly w ith th e latitudinal, lo n gitudinal,
as well as d e p th d istrib u tio n (Table 2 a n d Figure 7, right
panels). H ig h er fishing m o rta lity o n sole was associated w ith a n
o n average m o re so u th e rn , w estern, a n d shallow er d istrib u tio n
o f th e species. In c ontrast, fishing m o rta lity o n N o rth Sea plaice
(Figure 7, rig h t panels) was n o t co rrelated significantly w ith
either th e latitudinal, longitu d in al, o r d e p th d istrib u tio n o f the
species.
M ultiple regression analyses w ere co n d u cted to explore th e rela­
tive stren g th o f relationships o f clim ate a n d fishing pressure v ari­
ables w ith d istrib u tio n al responses o f sole a n d plaice (Table 2).
R egression m odels co n firm ed th a t H adley SST was a h ighly signifi­
can t p re d ic to r o f th e latitudinal, longitu d in al, a n d d e p th responses
o f b o th fish species (all p < 0.0005); also th a t fishing m o rta lity was
a significant p re d ic to r for sole (p < IO- 5 ), b u t n o t plaice d istri­
b u tio n . T he NAO w in ter index, however, was rejected as a p re d ic ­
to r for sole o r plaice d istrib u tio n (p > 0.05) b y any regression
m o d el th a t also inclu d ed H adley SST, the latter displaying far
greater e x planatory pow er. In contrast, the A M O was retained as
a significant p re d ic to r o f plaice lo n g itu d in al d istrib u tio n (p <
IO- 5 ), also w ith th e in clu sio n o f H adley SST (a h igh A M O being
associated w ith a w estw ard d isplacem ent). T he A M O was also a sig­
nificant p re d ic to r o f plaice latitu d in a l a n d d e p th d istrib u tio n , b u t
o nly in m odels th a t inclu d ed H ad ley SST as covariate.
T here was n o evidence th a t interactio n s betw een clim ate a n d
fishing m o rta lity p ro v id ed a d d itio n al e x planatory pow er. For
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(f)
1099
N in e decades o f N orth Sea sole a n d plaice distribution
(a)
(b)
9.5
10.0
10.5
11.0
0.6
0.4
0.2
11.5
0.8
1.0
(d)
Tj. -
LU
• •
CM -
10.0
10.5
11.0
0.2
11.5
0.6
0.4
0.8
1.0
(f)
o
o
♦♦
• i
o
in
.
♦♦
o .
co
9.5
10.0
10.5
11.0
11.5
Hadley SST (°C)
0.2
0.3
0.4
0.5
0.6
0.7
0.8
Plaice F (ages 4-8)
Figure 8. Relationships of Hadley SST (left) and plaice fishing pressure (right) with metrics of North Sea plaice distribution: (a and b)
latitudinal centre of gravity; (c and d) longitudinal centre of gravity; and (e and f) m ean dep th distribution. Regression lines are included only
w here correlations are significant (p < 0.05, adjusted for autocorrelation).
sole, th e in te ra c tio n H adley SST x sole F d id n o t explain la titu d i­
nal, lo ngitudinal, o r d e p th responses significantly (a llp > 0.2). For
plaice, the interactio n s H ad ley SST x plaice F (all p > 0.6) a n d
A M O x plaice F ( all p > 0.4) d id n o t explain any o f the responses
in d istrib u tio n m etrics.
A c o m p a riso n o f th e stan d ard ized ß coefficients in final m odels
(Table 2) lent su p p o rt to the n o tio n th a t betw een fishing m o rta lity
a n d H adley SST, th e fo rm er was th e stronger p re d ic to r o f sole
latitudinal, lo n gitudinal, a n d d e p th d istrib u tio n responses,
a lth o u g h b o th variables w ere highly significant predictors. For
plaice, w here th e effect o f fishing m o rta lity o n d istrib u tio n was
insignificant, the H ad ley SST a n d A M O c o n trib u te d ap p ro x i­
m ately equally to th e d istrib u tio n responses.
Discussion
O ver th e past n in e decades, b o th sole a n d plaice exhibited long­
term , m ultid ecad al changes in spatial d istrib u tio n w ith in the
N o rth Sea. M agnitudes o f each shift regarding “centres o f
gravity” o f latitu d e a n d lo n g itu d e w ere ~ l ° - 2 ° for b o th species;
th o se o f d e p th d istrib u tio n s w ere ~ 2 0 m for plaice, < 1 0 m for
sole. T he d irec tio n a n d tim in g o f shifts w ere, however, very differ­
e n t in th e tw o species: since the 1950s m ain ly northeastw ards and
to d eeper w aters in N o rth Sea plaice, b u t m ain ly southw estw ards
a n d to shallow er w aters in N o rth Sea sole (by 142 a n d 93 km ,
respectively). B oth species displayed co rrelations w ith th e H adley
SST, b u t in o p p o site directions; for sole, b u t n o t plaice, a close c o r­
relatio n w ith fishing m o rta lity was also observed.
U nlike in recent studies based o n IBTS (P erry et al., 2005;
D ulvy et al., 2008), w e used d a ta derived from co m m ercial catch
records, so it is necessary to co n sid er w h eth er o r n o t these
provide a representative a n d n o n -b iased p ictu re o f fish d istri­
b u tio n in th e past o r sim ply a reflection o f favoured fishing
localities. Im p ro v em en ts in fishing pow er o f U K o tte r traw lers
have clearly h a p p en e d (E ngelhard, 2008), b u t this p ro b lem was
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o>
G. H . Engelhard et al.
1100
Table 2. Regression models on distribution responses of N orth Sea sole and plaice (latitudinal, longitudinal, and d epth) to variables
related to clim ate and fishing pressure.
Response variable
Predictor
Sole latitudinal shift
Hadley SST
Sole F (ages 4 - 8 )
Hadley SST
Sole F (ages 4 - 8 )
Hadley SST
Sole F (ages 4 - 8 )
A M O Index
Hadley SST
A M O Index
Hadley SST
A M O Index
Hadley SST
Sole longitudinal shift
Sole d ep th shift
Plaice latitudinal shift
Plaice longitudinal shift
Plaice d ep th shift
//standardized
s.e.
-0 .1 6 1
- 0.350
- 0 .1 4 8
- 0.473
- 1 .3 4 8
- 1 .9 9 3
- 0.209
0.322
- 0.423
- 0.298
- 1 .7 7 8
3.502
0.036
0.039
0.045
0.047
0.353
0.376
0.074
0.071
0.082
0.079
0.788
0.759
t
p-value
4.426
9.045
3.330
9.974
3.821
5.303
2.828
4.529
-5 .1 8 1
- 3.786
- 2.256
4.614
0.00006
<0.00001
0.002
<0.00001
0.0004
<0.00001
0.006
0.00003
<0.00001
0.0003
0.028
0.00002
-
Final models are presented following a backward selection procedure, from a full model th at included the NAO winter index, AMO, Hadley SST, and fishing
mortality as main effects. Only the terms th at significantly explained the distribution metric (p < 0.05) were retained. None of the interactions between
environmental variables and fishing pressure was significant (p > 0.05). Standardized ß coefficients are displayed here, obtained after standardization of the
explanatory variables and indicative of the relative strength of these in explaining the response variable.
responses. A lthough n o su p p o rt for a n interactive effect was
fo u n d in this study, the im p o rta n ce o f n o t o nly exam ining
clim ate a n d fishing effects separately, b u t also th eir p o ten tial in te r­
action, has b een em phasized recently (P erry et al., 2010). A lthough
clear relationships w ere fo u n d betw een SST a n d flatfish d istri­
b u tio n s, the effects o f SBT co u ld n o t be fully explored, because
o f th e lack o f data for m o st o f th e earlier decades; w here tim e-series
overlapped, SST a n d SBT w ere closely correlated. N ote th at
a lth o u g h sole a n d plaice are b e n th ic as a d u lts/la te juveniles,
th eir eggs a n d early juveniles are fo u n d in the pelagic zone, close
to th e sea surface. It is c u rre n tly unclear w h eth er the d o m in a n t
clim ate-related im p a c t o n fish d istrib u tio n p a tte rn s h appens
th ro u g h processes th a t occu r d u rin g th e early life-history stages
(as suggested b y R in d o rf a n d Lewy, 2006), o r th ro u g h tem p e ra tu re
toleran ces/p referen ces d u rin g th e a d u lt phase, a n d consequently
w h eth er SST o r SBT is the m o st a p p ro p ria te e n v iro n m en ta l v ari­
able to consider.
Plaice seem to have resp o n d ed largely to clim ate changes w ith a
shift to the n o rth , the west, a n d to deeper w aters, fully in line w ith
expectations assum ing a n o r t h - s o u t h SST g radient in the n o r th ­
e rn h em isphere (P erry et al., 2005; D ulvy et al., 2008; R ijnsdorp
et al., 2009). T he lack o f a relationship w ith fishing m o rta lity
suggests th a t clim ate is th e d o m in a tin g driver o n plaice d istri­
b u tio n , a n d n o t fishing. In the N o rth Sea, juvenile plaice are ty p i­
cally co n ce n tra ted in shallow inshore w aters a n d m ove gradually
offshore as th ey b ecom e larger. Surveys in the W ad d e n Sea have
d e m o n stra ted th a t 1-group plaice are n o w alm ost absent from
th e area w here th ey w ere o nce very a b u n d a n t. T he “plaice b o x ”
(an area o f the D u tc h a n d G erm an coast closed to m o st plaice
fishing u n d e r th e EU C o m m o n Fisheries Policy since 1989:
P astoors et al., 2000) is n o w considered m u ch less effective as a
m an ag em en t m easure th a n 10 o r 15 years ago, a n d this has been
a ttrib u te d to th e d istrib u tio n shift resulting fro m lo n g -term
clim ate change (van Keeken et al., 2007). M arin e p ro tec te d area
b o u n d aries, such as those associated w ith th e “plaice b o x ”, m ay
have to b e “adaptive” in fu tu re a n d m ove w ith th e fish th ey are
try in g to p ro tect. It is interesting to n o te th a t th e a p p are n t
b im o d a l d istrib u tio n p a tte rn o f plaice d istrib u tio n in recent
years (1990s a n d 2000s in Figure 5), such th a t high cpue values
were reco rd ed in the central N o rth Sea, b u t also o ff n o rth ea st
Scotland. T his su d d e n o ccurrence o f large n u m b ers o f plaice off
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overcom e, because n o a tte m p t was m ad e to estim ate the absolute
biom ass in any p a rticu la r area. Instead, relative spatial d istri­
b u tio n s o f cpue were used. Spatial d istrib u tio n s o f cpue co u ld be
influenced b y the level o f targeting o f a species b y th e fleet
(Gillis et al., 2008; Q uirijns et al., 2008). H ow ever, alth o u g h
N o rth Sea plaice a n d particu larly sole are targeted extensively by
b eam traw lers, th ey are m erely im p o rta n t bycatch species for the
UK o tte r traw l fleet used here to provide cpue indices; this fleet
p rim a rily catches ro u n d fish (e.g. cod a n d h ad d o ck ) in a m ixed
fishery (B annister, 2004).
F u rth e r evidence o f representativeness o f o u r cpue m ap s for
“tru e ” sole a n d plaice a b u n d an c e d istrib u tio n s is p rovided by
great sim ilarity w ith spatial d istrib u tio n s based o n IBTS available
for recent decades (P erry et al., 2005; D ulvy et al., 2008). This
being said, th e p a tte rn s in recent decades m ay be affected b y the
c o m p e titio n betw een o tte r traw lers a n d b e am traw lers
(R ijnsdorp et al., 2008), because a n analysis o f th e D u tc h dem ersal
fleet since th e 1950s has revealed th a t th e o tte r traw l fleet has been
o u tco m p e te d a n d largely displaced to d eeper w aters b y th e highly
efficient b eam traw l fleet th a t o perates in this region. A lthough this
w ould b e expected to affect the to ta l effort expended b y th e o tte r
traw l fleet in a n area, w e w o u ld n o t generally an ticip ate a n im pact
o n catch rates (i.e. cpue). H ow ever, co m m ercial fishers m ay in te r­
act o n local g ro u n d s a n d “interference c o m p e titio n ” betw een
vessels has b e en observed. In such cases, this is k n o w n to affect
the re lationship betw een cpue a n d fish stock biom ass (Gillis a n d
P eterm an, 1998; Poos a n d R ijnsdorp, 2007).
It has also b een im p o rta n t to establish th a t clim ate variables
a n d fishing pressure are n o t significantly correlated, i.e. th a t the
tw o factors are n o t c o n fo u n d ed , because this has b e en o n e o f
the m ajo r concerns voiced a b o u t earlier studies (P erry et al.,
2005; D ulvy et al., 2008). It was n o t surp risin g th a t th e various
N o rth Sea te m p e ra tu re tim e-series were highly correlated,
because this was also observed b y M ackenzie a n d Schiedek
(2007). H ow ever, it is im p o rta n t a n d useful to n o te th a t in the
long term , there w ere n o significant co rrelations betw een fishing
m o rta lity (in eith er species) a n d a n y clim ate variable. T his offers
the h o p e th a t a lo n g er-term analysis o f fish d istrib u tio n s could
start to p in d o w n th e p rim a ry influences th a t are c o n fo u n d ed in
the sh o rte r te rm a n d also the possibility o f a n y effects o f the in te r­
actio n betw een clim ate a n d fishing pressure o n d istrib u tio n
N in e decades o f N orth Sea sole a n d plaice distribution
affected plaice d istrib u tio n (Nye et al., 2009). Elsew here in the
N o rth Sea, A ttrill a n d Pow er (2002) d e m o n stra ted th a t p attern s
in the NAO coincided w ith v a ria tio n in th e stru c tu re o f th e fish
assem blage, explaining 54% o f v ariation, a n d th a t th e grow th o f
m an y juvenile fish, in clu d in g sole, w ere also influenced b y the
NAO. A stu d y o f th e changing fish c o m m u n ity in th e B ristol
C hannel (H enderson, 2007) identified tw o p e riods o f discrete
change in the fish c o m m u n ity over th e past 25 years. T he first
change h a p p en e d in the late 1980s a n d involved a n a b ru p t shift
in th e relative a b u n d an c e o f the “p e rm a n e n t” m em b ers o f the
co m m u n ity , coinciding w ith observed changes in the p lan k to n
o f the n o rth east, a n d was co rrelated w ith the w in ter NAO. A
second discrete change, affecting the to ta l species assem blage, h a p ­
p en ed in th e early 1990s. T his was m ark ed b y a su d d e n a lteratio n
in th e set o f “occasionally o c cu rrin g ” species. T his change was c o r­
related w ith average seaw ater te m p e ra tu re (and possibly th e A M O )
ra th e r th a n NAO.
A p a rt fro m clim ate a n d fishing, o th er factors m ay also have h ad
a n im p o rta n t influence o n plaice a n d sole d istrib u tio n s th ro u g h ­
o u t the tw en tieth century. These m ay have in clu d e d h a b ita t m o d i­
fication, changes in prey resources a n d /o r overall system
productivity, a n d changes in p re cip ita tio n a n d ru n -o ff patterns.
P erhaps fish p o p u latio n s have been affected b y successive loss o f
im p o rta n t so u th e rn plaice (a n d sole) n u rse ry g rounds. T he
D u tc h a n d Belgian coasts w ere previously very good n u rse ry
g ro u n d s for plaice (W im penny, 1953), b u t several an th ro p o g e n ic
changes have strongly altered this. In p articular, th e closure o f
th e Z uiderzee in th e early 1930s a n d th e closure o f estuaries o f
th e R hine, M euse, a n d Scheldt in the 1960s a n d 1970s (H eip,
1989) will have likely reduced the re cru itm e n t fro m these
n u rse ry g ro u n d s a n d hence m ay have affected th e a b u n d an c e
a n d d istrib u tio n o f o lder age groups in the N o rth Sea
(R ijnsdorp et al., 1992; R ochette et al., 2010).
In the coastal w aters o f the w estern M e d ite rran e a n a n d the Bay
o f Biscay, w hich are affected b y th e ru n -o ff o f the R hone a n d the
Loire, respectively, sole re cru itm e n t a n d grow th has b een positively
affected b y th e river ru n -o ff subsidising th e b e n th ic foodw eb w ith
a d d itio n o f n u trie n ts a n d terrestrial organic m a tte r (Salen-P icard
et al., 2002; Le Pape et al., 2003). Plaice exp an sio n n o rth w a rd s
in the N o rth Sea d u rin g th e 1 9 5 0 - 1980s m ig h t have hap p en ed
because o f n u trie n t e n ric h m e n t a n d e u tro p h ic a tio n o f the
coastal zone, because th e plaice grow th rate is k n o w n to correlate
strongly w ith various e u tro p h ic a tio n param eters (e.g. p h o sp h o ru s
in p u ts), a n d th ere is evidence o f increased b e n th ic p ro d u c tiv ity in
large areas o f the N o rth Sea d u rin g this period. Sole a n d plaice in
th e G erm an B ight have b e en particu larly heavily influenced b y
river ru n -o ff a n d n u trie n t in p u ts th a t increased in the 1960s and
1970s, b u t w hich have subsequently declined (C olijn et al., 2002;
P h ilip p a rt et al., 2007).
T he decrease in relative a b u n d an c e in th e G erm an B ight in
recent decades m ay b e d u e to th e increase in sm all-bodied, sm all­
m o u th e d flatfish, such as solenette Buglossidium luteum a n d scaldfish Arnoglossus laterna, w hich m ay co m p ete w ith plaice a n d sole
in this region (Jennings et al., 2008; v a n H al et al., 2010), in c o n ­
ju n c tio n w ith changes in th e p ro d u c tiv ity o f th e b e n th ic ecosys­
tem . A n analysis o f plaice a n d sole diets in 1996 c o m p a red w ith
th e begin n in g o f th e tw en tieth c en tu ry has revealed th a t p oly­
chaetes have increased a n d bivalves decreased (R ijnsdorp and
V ingerhoed, 2001). These results m ig h t reflect a change in
system productivity, b u t equally they are consistent w ith the
hypothesis th a t b eam traw ling has im p ro v ed the feeding
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S cotland co u ld result from a n invasion fro m th e west (this m ight
be a n explan atio n for th e su d d e n “ju m p ” in longitude; Figure 6),
as well as a g radual shift in th e centre o f gravity fro m the southeast.
ICES stock assessm ents a n d fish ery -in d ep en d en t surveys provide
little evidence o f a shift in plaice p o p u latio n s fro m the west to
th e east side o f Scotland, because plaice p o p u latio n s have only
ever been relatively sm all o ff th e Scottish H ighlands a n d islands.
F ro m o u r analyses, sole seem to have re sp o n d ed to clim ate
change a n d fishing, a n d the relationship w ith fishing seem s p a r­
ticularly strong. T his is in line w ith extensive targ etin g o f this
highly priced species b y th e large N o rth Sea b eam traw l fleet,
o ften in preference to plaice (Pilling et al., 2008). C o n trary to
sim ple expectations regarding th e m an ifestatio n o f clim ate
change, sole have exhibited a southw estw ard shift to shallow er
w aters w ith w arm ing, in line w ith P erry et al. (2005). In the
N o rth Sea, th e n o rth tends to be colder th a n th e so u th in
su m m er, b u t th e so u th tends to be colder th a n th e n o rth in
w inter. Som e so u th e rn N o rth Sea species, such as sole, have
been previously excluded fro m large areas o f shallow inshore
ha b ita t along th e c o n tin e n ta l coast in w inter, because these
w aters cool d o w n to well below 3°C, a critical tem p e ra tu re
below w hich sole suffer im p aired physiological fu n c tio n a n d
increased m o rta lity (W oodhead, 1964a, b ). C onsequently, in the
past, sole ten d e d to overw inter in d eeper w aters before re tu rn in g
to th e shallow s in spring, to avoid th e lethally cold w in ter tem p e ra ­
tures (H e n d erso n a n d Seaby, 2005). H ow ever, th ere is evidence
th a t sole have sta rte d spaw ning in coastal w aters earlier, because
o f the ra p id ly w arm in g seas in w in ter since the 1980s (Teal et al.,
2008). D u rin g severe w in ter cond itio n s, such as those experienced
in the 1960s a n d in 1996, sole w ere excluded fro m the shallow s to
th e extent th a t m ass m o rta lity events w ere re p o rte d (W oodhead,
1964a; H o rw o o d a n d M illner, 1998). A sim ilar m ass m o rta lity
event for sole was re p o rte d in early 1929 (L um by a n d A tkinson,
1929), n o tab ly o n th e T erschelling g ro u n d o ff th e D u tc h coast.
T his coincided w ith seaw ater tem p eratu res th a t were 5°C colder
th a n w ere considered “n o rm a l” for th a t tim e o f year. B etter acces­
sibility to shallow, inshore w aters in w in ter m ig h t also explain w hy
several o th e r sm all, w a rm -to lera n t so u th e rn species have recently
displayed southw ard, “shallow ing” d istrib u tio n shifts (D ulvy
et al., 2008). T his is equally a m an ifestatio n o f changing clim ate
c o n d itio n s in th e N o rth Sea as the m o re w idely k n o w n (and
re p o rte d ) “n o rth w a rd ” shift o f m arin e organism s in recent years.
T here are m an y exam ples in th e literature w here fish d istri­
b u tio n a n d /o r a b u n d an c e has been related to the NAO
(O ttersen et al., 2001; A ttrill a n d Power, 2002; H e nderson,
2007). H ere, a c o rre latio n o f th e NAO w ith sole latitu d in a l (and
p erhaps d e p th ) d istrib u tio n was fo u n d , b u t n o significant relatio n ­
ships in a regression m o d el th a t also inclu d ed th e H adley SST. It is
p erhaps n o t surp risin g th a t stronger correlations w ere identified
w ith sea tem p eratu res w ith in the N o rth Sea, because tem p e ra tu re
is the physical variable experienced directly b y the fish a n d kn o w n
to affect th e ir g row th a n d behaviour. T he NAO w ould have a m u ch
m o re indirect influence (see also E ngelhard a n d H eino, 2006). In
ad d itio n , this stu d y p ro v id ed evidence indicatin g the im p o rta n ce
o f the A M O , a n in d ex th a t is b e co m in g increasingly p o p u la r in
studies o f fish a n d clim ate in th e N o rth A tlantic (Nye et al.,
2009). T he A M O was significantly related to plaice (b u t n o t
sole) d istrib u tio n , especially if th e effect o f sea te m p e ra tu re was
acco u n ted fo r in regression m odels; this suggested th a t a p art
fro m im m ed iate tem p e ra tu re effects, lo n g -te rm fluctu atio n s in
th erm o h alin e circu latio n a n d hence shifts in tem p e ra tu re regim e
1101
1102
co n d itio n s for the tw o flatfish species, b y enhan cin g th e a b u n ­
dance o f sm all o p p o rtu n istic b e n th ic species, such as polychaetes,
in th e heavily traw led areas. H ow ever, th e changes in d iet m ay also
be related to e u tro p h ic a tio n a n d p o llu tio n . A recent co m p a riso n o f
plaice diet in the central N o rth Sea (JKP, u n p u b lish ed d a ta ) d u rin g
the early 1900s (1 9 0 2 -1 9 0 9 ), 1950s (1 9 5 0 -1 9 5 9 ), a n d early
tw enty-first c e n tu ry (2 0 0 4 -2 0 0 9 ) has revealed sim ilar changes in
diet, w ith a sw itch away fro m bivalves such as Spisida a n d Ensis
tow ards polychaetes, crabs, a n d sandeels. This suggests th a t it is
n o t e u tro p h ic a tio n o r p o llu tio n th a t has affected diets (a n d th ere ­
fore grow th a n d possibly d istrib u tio n ) in th e central N o rth sea,
a n d th a t th e cause is m o re likely to be increased traw ling pressure,
allied w ith lo n g -te rm clim ate change.
Conclusions
Acknowledgements
GH E, JKP, a n d A D R w ere su p p o rte d th ro u g h th e EU FP6 project
RECLAIM; GH E, JKP, a n d LTK w ere also su p p o rte d th ro u g h the
U K ’s D e p artm en t for F ood, E n v iro n m e n t a n d R ural Affairs (c o n ­
tracts M F1201, M A010, a n d M F1108), a n d LTK was also su p ­
p o rte d b y th e EU U N C O V E R p roject (co n tract 022717). JKP
thanks th e conveners o f the In tern a tio n a l S ym posium o n
C lim ate C hange Effects o n Fish a n d Fisheries for inviting h im to
p resen t this m aterial a n d CLISAP (an excellence cluster at the
U niversity o f H a m b u rg ) in su p p o rtin g his a tte n d an c e at th e sym ­
p o siu m . W illiam C heung, N ick D ulvy, C h risto p h er Lynam , D avid
M axwell, a n d o n e a n o n y m o u s referee gave valuable feedback a n d
advice o n th e statistical analysis.
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