www.elsevier.com/locate/seares
Journal of Sea Research 51 (2004) 313–328
Growth changes in plaice, cod, haddock and saithe in the North
Sea: a comparison of (post-)medieval and present-day growth rates
based on otolith measurements
Loes J. Bollea,*, Adriaan D. Rijnsdorpa, Wim van Neerb, Richard S. Millnerc,Piet I. van Leeuwena, Anton Ervynckd, Richard Ayersc, Ellen Ongenaee
aNetherlands Institute for Fisheries Research, P.O. Box 68, 1970 AB IJmuiden, The Netherlandsb IPA V-09, Royal Museum of Central Africa, 3080 Tervuren, Belgium
cCentre for Environment, Fisheries and Aquaculture Science, Pakefield Road, Lowestoft, NR33 0HT, UKd Institute for the Archaeological Heritage of the Flemish Community, Phoenix-building, Kon. Albert II-laan 19, Box 5, 1210 Brussels, Belgium
eFisheries Research Station, Ankerstraat 1, 8400 Ostend, Belgium
Received 15 November 2003; accepted 20 January 2004
Abstract
Fishing effort has strongly increased in the North Sea since the mid-19th century, causing a substantial reduction in the
population size of exploited fish stocks. As fisheries research has developed simultaneously with the industrialisation of the
fisheries, our knowledge of population dynamics at low levels of exploitations is limited. Otoliths retrieved from archaeological
excavations offer a unique opportunity to study growth rates in the past. This study compares historical and present-day growth
rates for four commercially important demersal fish species. A total of 2532 modern otoliths (AD 1984–1999) and 1286
historical otoliths (AD 1200–1925) obtained from archaeological excavations in Belgium and Scotland were analysed.
Comparison of the growth patterns between eras revealed a major increase in growth rate of haddock, whereas growth changes
were not observed in saithe and only in the smaller size classes of plaice and cod. Comparison of our results with literature data
indicates that the observed growth rate changes in plaice and cod occurred within the 20th century. Apparently the onset of
industrialised fisheries has not greatly affected the growth of plaice, cod and saithe populations in the North Sea. This result
contradicts the expectation of density-dependent limitation of growth during the era of pre-industrialised fishing, but is in
agreement with the concentration hypothesis of Beverton (Neth. J. Sea Res. 34 (1995) 1) stating that species which concentrate
spatially into nursery grounds during their early life-history may ‘saturate’ the carrying capacity of the juvenile habitat even
though the adult part of the population is not limited by the adult habitat.
D 2004 Elsevier B.V. All rights reserved.
Keywords: Pleuronectes platessa; Gadus morhua; Melanogrammus aeglefinus; Pollachius virens; Otoliths; Back-calculation; Archaeological
excavations; Density-dependent growth; Concentration hypothesis
1385-1101/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.seares.2004.01.001
* Corresponding author.
E-mail address: [email protected] (L.J. Bolle).
1. Introduction
Knowledge of population dynamic processes is
important in creating a scientific basis for sustainable
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328314
exploitation of fisheries resources. Growth is one of
these processes and changes in growth have a pro-
found impact on the productivity of a fish stock. For
instance, the increase in haddock landings in the
1960s has been partly ascribed to increased growth
rates (Jones and Hislop, 1978). Similarly, changes in
plaice landings coincided with changes in growth
rates (Bannister, 1978; Rijnsdorp and Van Beek,
1991). Besides a direct effect on the biomass of fish
stocks, changes in growth affect the reproductive
output, because both maturation and egg production
are affected by growth (Rothschild, 1986; Rijnsdorp,
1993a; Grift et al., 2003).
Examining the response of marine fish populations
to heavy exploitation has been severely hampered by
the lack of data from the pre-industrialised fishing era
(Pope and Macer, 1996; Rijnsdorp and Millner, 1996).
Among archaeozoologists there is a growing interest
to analyse fish remains from excavations. Thanks to
the systematic use of sieves during the last two
decades, the number of fish remains available for
study has increased dramatically (Van Neer and
Ervynck, 1993). Many archaeological sites have
yielded thousands of fish remains, but otoliths are
often underrepresented due to the unstable nature of
otoliths in comparison to fish bones. Favourable
conditions for the preservation of otoliths are found
in waterlogged contexts such as cesspits and deep
refuse pits. Archaeozoologists have mainly focused
on using otoliths to establish seasonal patterns in
fishing (Monks and Johnston, 1993; Van Neer et al.,
in press). However, the growth patterns laid down in
these archaeological otoliths offer fisheries biologists
a unique opportunity to study growth rates in the past.
Although growth rates as such are not directly rele-
vant to the archaeological interpretation of the sites,
the reconstruction of age and fish length distributions
of landings based on growth patterns in otoliths
allows inferences about fish trade and marketing
strategies (Van Neer et al., 2002).
From studies of heavily exploited fish populations
the general pattern emerges that growth during the
adult phase is not related to population size, whereas
growth in the juvenile phase may be density depen-
dent (Cushing, 1981; Valiela, 1984; Daan et al.,
1990; Van der Veer et al., 1994; Rijnsdorp, 1994).
The question arises whether or not these patterns also
apply to less heavily exploited populations, as den-
sity-dependent processes may become more pro-
nounced at reduced levels of exploitation. The
increase in growth observed in several flatfish species
since the beginning of the 20th century is potentially
related to increased exploitation (Rijnsdorp, 1994).
Furthermore, growth rates of adult plaice were re-
duced after World War II, coinciding with the build-
up of biomass as a consequence of reduced fishing
during the war (Beverton and Holt, 1957; Rijnsdorp
and Van Leeuwen, 1992). The response to changes in
exploitation may differ between species in relation to
their life history and their position within the food
web. Increased exploitation results in a decrease of
larger fish, but the number of small fish may increase
in response to the reduction of predation pressure
(Rice and Gislason, 1996; Daan et al., 2003). How-
ever, the abundance of adults is less likely to affect
the juveniles of species that utilise sheltered nursery
areas such as plaice and saithe.
Sufficient numbers of archaeological otoliths to
examine growth rates are available for four commer-
cially important demersal fish species: plaice (Pleuro-
nectes platessa), cod (Gadus morhua), haddock
(Melanogrammus aeglefinus) and saithe (Pollachius
virens). These species differ in their current distribu-
tion within the North Sea. Haddock and saithe inhabit
the deeper waters to the north, plaice is mainly caught
in the southern and central areas and cod occurs
throughout the North Sea (Knijn et al., 1993). Because
these species occupy different niches within the eco-
system, they may differ in their response to increased
exploitation. Inter- and intra-specific interactions
through competition for food or predation may only
occur in size-classes that overlap in distribution
(Rijnsdorp and Van Beek, 1991). The species studied
comprise the whole spectrum of spatial overlap.
Juveniles of plaice and saithe are concentrated in
coastal nursery grounds that are spatially segregated
from the adult distribution area (Wimpenny, 1953;
Daan et al., 1990). On the other side of the spectrum,
we find haddock where juveniles and adults co-occur
in the same areas. Cod occupies an intermediate
position (Hislop, 1984; Daan et al., 1990; Munk et
al., 1999).
Our objective is to compare growth rates in recent
years with those prior to the onset of industrialised
fishing. It is hypothesised that the substantial increase
in exploitation since the mid-19th century has brought
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328 315
the population size of exploited fish stocks below a
level where density-dependent regulation occurs.
Therefore, present-day growth rates of the adults are
expected to be higher in all four species. Changes in
the juvenile phase are expected to differ among
species. For species of which the juveniles are subject
to high predation mortality (cod and haddock), in-
creased exploitation of the larger fish may result in
increased density of the juveniles and hence lower
growth rates. Such an inverse relationship between the
population size of adults and juveniles is not expected
to exist in plaice and saithe.
2. Materials and methods
2.1. Archaeological excavations
Otoliths (sagittae) were obtained from several
excavation sites (Fig. 1 and Table 1) in Belgium
Fig. 1. Map showing the regions within the North Sea and
(Raversijde, Mechelen, Ostend and Bruges) and one
site in Scotland (Robert’s Haven). Species identifica-
tions were based on descriptions and images of
otoliths (Chain, 1936; Härkönen, 1986; Nolf and
Steurbaut, 1989) and on comparisons with a reference
collection. Among at least 18 marine fish species
encountered on these sites, otoliths of four commer-
cially important demersal fish species (plaice, cod,
haddock and saithe) were selected for growth analysis.
Approximately 5% of the otoliths were a priori
excluded because identification was uncertain or be-
cause the surface was severely eroded.
The archaeological material refers to three main
periods (Table 1). Late-medieval otoliths were avail-
able from Raversijde (1425–1475), Bruges (1350–
1450) and Robert’s Haven (1200–1400), post-medie-
val material (Mechelen 1700–1800; Bruges 1650–
1750 and Ostend 1650–1700) originated from the
period prior to the era of industrialised fisheries, and
two samples (Mechelen and Bruges 1875–1925) refer
the locations of the archaeological excavation sites.
Table 1
Overview of the otolith samples included in the growth analyses
Archaeological Period Number of otoliths
site/RegionPlaice Cod Haddock Saithe
Raversijde 1425–1475 474 32 215
Mechelen 1700–1800 62 42 189
1875–1925 21
Ostend 1650–1700 2 30
Bruges 1350–1450 1
1650–1750 30 2
1875–1925 14
Robert’s Haven 1200–1400 70 1 101
Total 601 146 438 101
English Channel
(VIId)
1995–1999 177 86
Southern North Sea
(IVc)
1995–1999 210 108
Central North Sea
(IVb)
1995–1999 394 137 226
Northern North Sea
(IVa)
1984–1995 108 112 202 114
Irish Sea (VIIa) 1995–1999 163 93
West of Scotland
(VIa)
1995–1999 40 76 168
Skagarrak (IIIa) 1995–1999 118
Total 1210 612 596 114
The samples were obtained from archaeological excavation sites
(1200–1925) or from surveys and market sampling programmes
(1984–1999).
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328316
to the period roughly corresponding with the onset of
industrialised fisheries. The samples were dated by
cultural artefacts (mainly ceramics types) found in the
same contexts and by the stratigraphic position of these
contexts. At the Raversijde excavation site, a single
depositional event was discovered, where all otoliths
(129 plaice otoliths) probably originate from a single
fishing trip. In all other cases, the samples were derived
from contexts accumulated over several decades (Van
Neer and Pieters, 1997; Van Neer et al., 2002).
Robert’s Haven and Raversijde were coastal vil-
lages. The fish remains from Robert’s Haven repre-
sent fish that was landed by the inhabitants
themselves and probably caught in local coastal
waters. In the case of Raversijde, historical sources
indicate that plaice and haddock were probably
caught in local coastal waters, whereas the cod
remains may partially represent fish that was caught
in more northern waters. Without doubt, the majority
of the marine fish consumed at Ostend came from its
own harbour or from smaller fishing villages nearby.
The towns Bruges and Mechelen are located inland
and the remains of marine fish represent imported
specimens. During the early post-medieval period,
the Flemish (Belgian) fishery suffered from political
troubles and marine fish marketed in inland towns
probably originated from the southern part of the
Netherlands. After the revival of the Flemish fishery
around 1900, fish sold on inland markets may have
come from either Flemish or Dutch fishing villages
along the Southern Bight and English Channel (Van
Neer et al., 2002).
2.2. Present-day otolith samples
Present-day otoliths (sagittae) were selected from
material collected during ongoing research vessel sur-
veys andmarket sampling programmes. Cod and plaice
samples covered a wide range of fishing grounds, while
haddock samples were more restricted in area coverage
due to the current distribution pattern of haddock. As
the historical saithe material was limited in number and
quality, a correspondingly smaller sample of present-
day saithe otoliths was included, from the northern
North Sea only (Fig. 1 and Table 1).
With the exception of haddock from region VIa
(1984–1995), all otolith samples were collected be-
tween 1995 and 1999. Samples were restricted to the
spawning season (approximately January – March)
and the summer (July – September). The target was to
sample the full size range evenly for each region and
season (10 plaice, 3 cod, 8 haddock and 8 saithe per 5-
cm size class), but fish smaller than the minimum
landing size were not always available. The plaice
samples were also stratified by sex. Only one of the
pair of sagittal otoliths of each fish was included in the
growth analysis.
2.3. Otolith preparations and measurements
All otoliths were embedded in black polyester resin
and transverse sections were cut through the nucleus,
exposing the annual ring structure (Bedford, 1983;
Bolle et al., 2003; Millner et al., ms. in prep.). For the
accuracy of the analysis it is essential that the plane of
section is as close to the primordial core as possible
since deviations will affect the measurements. Images
of the sectioned otoliths were digitised with a camera
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328 317
attached to a binocular microscope. The width of the
otolith and the annuli were measured using image
analysing software. An experienced age reader
marked the translucent-opaque transition at the outer-
most tips of each annulus. The X–Y coordinates of
these annotations and the greatest width of the whole
otolith were recorded. The X–Y measurements were
then converted to annulus diameter. The direction of
otolith growth changes with age from posterior-ante-
rior (increase in otolith width) to dorso-ventral (in-
crease in otolith thickness). This is illustrated for a
plaice otolith in Fig. 2. The annulus diameter was
calculated for the main axis of growth, which was
defined as the greatest width axis. Therefore, the X–Y
coordinates of the tips of each annulus were projected
on the main axis of growth (A–A in Fig. 2). The
distance between the projected tips of annulus i is the
otolith diameter at age i.
2.4. Measurement errors
Interpreting otolith structures is a difficult and
complex task involving knowledge of the life history
of a species and experience in age reading. Because
different age readers were involved, training and
calibration exercises were carried out at the start of
the project. Furthermore, duplicate measurements
were carried out subsequently to estimate measure-
ment errors induced by different interpretations. A
total of 211 plaice, 213 cod, 199 haddock and 20
saithe otoliths were re-aged and re-measured by an
independent second reader without prior knowledge
of the first results.
The readers agreed on the age and the position of
the annuli in the majority of otoliths. In some cases, a
different interpretation of the structure caused sub-
stantial differences in increment measurements, while
in others disagreement on age (for example, whether
Fig. 2. Transversal section of a plaice otolith. Incremental
measurements are projected on the main axis of growth A-A.
or not an annulus had been laid down on the edge)
barely affected increment measurements. Despite dif-
ferences at the level of the individual fish, on average
the differences were insignificant (P < 0.05 in paired t-
test for each species and annulus). Consequently, the
conclusion was drawn that there is no reader-induced
bias in the growth analyses.
2.5. Growth analyses
Growth patterns were examined in almost all oto-
liths listed in Table 1. A small number of otoliths (12
historical and 8 modern) were rejected because the
growth checks were poorly visible. Another 41 mod-
ern otoliths (33 plaice and 8 haddock) were excluded
because these fish were in their first year of life,
providing no information on annual growth.
The basic comparisons of growth patterns were
carried out using the direct otolith measurements
instead of back-calculated fish length, because these
are less prone to error. First, we calculated the mean
diameter for each annulus giving a reconstruction of
the otolith width at age. The increase in diameter
between two consecutive annuli is referred to as the
annual increment. Because these increments decrease
with otolith size, just as the body size increments
decrease with body size, they are plotted as a function
of the otolith width at the beginning of the growing
season. The mean increment per otolith size class was
calculated for plotting purposes, while the individual
estimates were used in the statistical analyses. Annual
increments smaller than the range of a size class may
lead to multiple entries for a single fish in a size class.
To avoid this, the annual increment per size class was
first averaged for individuals before the sample aver-
age was calculated.
If the estimation of growth rate is affected by age at
capture then any differences between modern and
historical growth rates may be merely due to differ-
ences in the age compositions of the samples com-
pared. To correct for this potential sampling bias,
measurements were weighted so that the effective
age composition of the modern otoliths equalled that
of the historical otoliths. For each age at capture, all
measurements of modern otoliths were weighted by
the sample size of historical otoliths divided by the
sample size of modern otoliths. The measurements of
historical otoliths were not weighted, but if an age at
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328318
capture was not represented in the modern samples
then these measurements were excluded.
Conversion of otolith sizes into fish lengths was
required to be able to reconstruct the length of the
fish at capture in the case of the archaeological
samples and to compare our results to fish length
at age observations reported in previous studies. For
all four species the relationship between otolith
width and fish length was best described by a power
function (Rijnsdorp et al., 1990; Bolle and Rijns-
dorp, 2000):
elogðFLÞ ¼ a þ b*elogðOW Þ ð1Þ
where FL is fish length (cm) and OW is otolith
width (mm) at the time of capture. The parameter
estimates are presented in Table 2 and can be used to
reconstruct the fish length according to following
derivatives of formula (1):
Li ¼ Ea*ðOiÞb ð2Þ
Li ¼ FL*ðOi=OW Þb ð3Þ
where Li is fish length and Oi is otolith width at the
time of annulus formation of the ith annulus.
If fish length at time of capture is known then the
proportionality method (3) can be used. Fish length
at capture is registered for all modern otoliths, but is
unknown for otoliths retrieved from archaeological
excavation sites. For historical otoliths the recon-
struction of fish length can only be done using (2).
In some cases otolith type (left or right), sex, season
and/or region may have a minute, though statistical-
ly significant effect on the relationship between
otolith width and fish length (Bolle and Rijnsdorp,
2000). As so many factors have no or only marginal
Table 2
Parameter estimates and correlation coefficients of the regression
model elog(FL) =a+h*elog(OW), where FL is fish length in cm
and OW is otolith width in mm (source: Bolle and Rijnsdorp,
2000)
Species N R2 a h
Plaice 1207 0.95 1.473 1.399
Cod 1232 0.97 1.279 1.456
Haddock 592 0.95 1.107 1.521
Saithe 109 0.93 0.806 1.969
effects on the fish - otolith size relationship, it seems
unlikely that it has changed much over time.
3. Results
3.1. Age and size distributions
Fig. 3 presents the age and fish length distributions
for each species and era. The observed fish length is
plotted for the modern specimens, whereas the recon-
structed fish length is presented for the historical
otoliths. The age and length distributions of the
historical otolith samples presumably reflect those of
historical catches. This is not the case for the modern
otolith samples, as these were stratified by fish length.
Therefore the age distributions of present-day land-
ings were included in Fig. 3 (ICES, 2003). The
present-day catches showed a clear shift towards
younger fish in the case of haddock and cod, a small
shift towards younger fish for plaice and a shift
towards older fish for saithe.
The age and size distributions of the modern and
historical otolith samples were different. The youngest
age groups and smallest size classes of all species
except saithe were over-represented in the modern
samples compared to the historical samples (Fig. 3).
Furthermore, the larger size classes of plaice and
haddock, and the older age groups of plaice were
relatively over-sampled in the modern samples.
The age and size distributions also differed be-
tween excavation sites, especially in cod. Most of the
cod landed in Raversijde and Robert’s Haven were
40–70 cm and 2–4 years old, whereas most of the
cod marketed in Mechelen corresponded to larger
(>80 cm) and older (6+) fish. Such differences be-
tween sites were probably related to trade: fishermen
consumed the smaller fishes themselves and exported
the larger ones to the inland markets (Van Neer et al.,
2002). Differences between regions also occurred in
the modern otoliths samples, but these were less
pronounced than in the historical samples (Bolle and
Rijnsdorp, 2000).
3.2. Geographic variations in growth rates
The modern otolith samples of cod and especially
plaice covered a large part of the North Sea and
Fig. 3. The age and size distributions of the modern and historical otolith samples and the age distributions of present-day landings for (a) plaice,
(b) cod, (c) haddock,and (d) saithe.
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328 319
Fig. 4. Geographic variations in mean annual increment per otolith
size class for (a) plaice, (b) cod, and (c) haddock.
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328320
adjacent waters (Table 1 and Fig. 1), allowing an
analysis of the geographic variation in growth (Fig. 4).
The annual growth increments were largest in cod
from the English Channel (region VIId) and smallest
in the northern North Sea (region IVa). Small plaice
also showed the highest growth rates in region VIId
and the lowest rates in region IVa, while larger plaice
grew fastest in the southern North Sea (region IVc)
and slowest in region VIa. The annual growth incre-
ments of haddock did not differ between the three
regions sampled.
3.3. Comparison of growth rates between eras
Growth rates in the era of pre-industrialised fish-
eries were compared with present-day growth rates by
plotting the mean annual increments for each species
and era (Fig. 5). The means were weighted by the age
distributions of the samples (Section 2.5). As latitu-
dinal trends in growth were observed (Fig. 4), a
distinction was made between southern and northern
samples.
The growth patterns recorded in plaice otoliths
from Belgian excavation sites were compared with
modern growth patterns in the southern North Sea and
the English Channel (Fig. 5a). Because the increase in
fishing effort already started in the second half of the
19th century, the otoliths dated 1875–1925 were
excluded. Modern growth rates were significantly
higher in the smaller size classes. No growth changes
were observed in the larger size classes.
Fig. 5b compares the growth patterns of cod
otoliths found at Belgian excavation sites with modern
growth patterns in the southern North Sea and the
English Channel. This comparison showed a signifi-
cant difference in the smaller size classes. However, it
was uncertain whether all of the archaeological oto-
liths from Belgium represent fish caught in local
coastal waters. The difference in growth rate was
smaller but still significant if the Belgian otoliths
were compared with modern samples from the north-
ern North Sea. Cod otoliths from Robert’s Haven were
compared with present-day otoliths from regions VIa
and IVa (Fig. 5c). Although the growth rates appeared
to be similar in all size classes, the differences in the
smallest size classes were significant.
The majority of gadoid otoliths found at the Belgian
excavation sites were haddock otoliths. Haddock is
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328 321
scarce in the southern North Sea and English Channel
at present, so the archaeological samples were com-
pared with modern otoliths from regions IVa and IVb
(Fig. 5d). The growth rates of all size classes are
currently much higher than in the past.
All historical saithe otoliths were from Robert’s
Haven, and all modern saithe otoliths were caught in
region IVa. Current growth rate appeared to be slight-
ly lower than in the 13th–14th century samples but
the difference was insignificant (Fig. 5e).
A general linear model was used to examine the
significance of the observed differences between
modern and historical growth rates. A linear decline
in growth rate (annual increment) with size was
assumed, and age at capture was included in the
model. The analyses were carried out using otolith
measurements rather than back-calculated fish length.
In all species except saithe, the difference between
modern and historical growth rates was significant
(Table 3). To examine the significance of era in the
larger size classes, the model was re-run several times,
stepwise dropping the smaller size class (ANOVA
tables not presented). Modern and historical growth
rates did not significantly differ in the larger size
classes of plaice (otolith >3.5 mmc fish length >25cm), northern cod (otolith >3 mmc fish length >18cm) and southern cod (otolith >6 mmc fish length>50 cm). The difference was significant in all size
classes of haddock.
The age at capture significantly affected the
growth rate estimation in all species (Table 3),
which means that the size of an otolith increment
was partly dependent on the age at capture and
comparisons between samples could be biased by
different age compositions. This potential bias was
minimised because the measurements were weighted
by the age distribution. Furthermore, modern and
historical growth rates were compared within age
groups (age at capture). This was only possible for a
small number of age groups because of the limited
number of otoliths. The observed patterns within age
Fig. 5. Comparison of modern and historical growth patterns for (a)
plaice, (b) southern cod, (c) northern cod, (d) haddock, and (e)
saithe. The weighted mean annual increment is plotted as a function
of otolith size class. The weighting procedure is described in the
text. The number of observations for each era and size class, and the
standard deviation of the mean are presented in the plots.
Table 3
ANOVA table from the regression analysis of annual increment
(Oi + 1–Oi) as a function Oi (otolith width of the ith annulus), era
(pre-industrial or present-day) and age (age at capture)
Source df partial SS MS F P
Plaice
Model (R2 = 0.60) 5 366.2 73.2 924.7 < .0001
Error 3140 248.7 0.1
Corrected Total 3145 614.9
Oi 1 28.2 28.2 355.5 < .0001
Era 1 23.5 23.5 296.8 < .0001
Oi*Era 1 13.2 13.2 166.4 < .0001
Log(Age) 1 10.9 10.9 137.2 < .0001
Oi*Log(Age) 1 3.2 3.2 40.6 < .0001
Southern Cod
Model (R2 = 0.81) 5 362.6 72.5 555.5 < .0001
Error 668 87.2 0.1
Corrected Total 673 449.8
Oi 1 31.7 31.7 242.5 < .0001
Era 1 7.9 7.9 60.4 < .0001
Oi*Era 1 2.9 2.9 21.9 < .0001
Log(Age) 1 9.6 9.6 73.6 < .0001
Oi*Log(Age) 1 6.4 6.4 49.4 < .0001
Northern Cod
Model (R2 = 0.60) 5 137.2 27.4 186.6 < .0001
Error 622 91.5 0.1
Corrected Total 627 228.7
Oi 1 7.4 7.4 50.1 < .0001
Era 1 1.6 1.6 11.1 0.001
Oi*Era 1 1.5 1.5 10.4 0.001
Log(Age) 1 2.7 2.7 18.4 < .0001
Oi*Log(Age) 1 0.4 0.4 2.5 0.116
Haddock
Model (R2 = 0.64) 5 266.6 53.3 827.1 < .0001
Error 2366 152.6 0.1
Corrected Total 2371 419.2
Oi 1 12.1 12.1 186.9 < .0001
Era 1 1.5 1.5 24.0 < .0001
Oi*Era 1 1.2 1.2 18.8 < .0001
Log(Age) 1 0.2 0.2 3.2 0.074
Oi*Log(Age) 1 0.7 0.7 11.3 0.001
Saithe
Model (R2 = 0.67) 5 29.5 5.9 204.3 < .0001
Error 496 14.3 0.0
Corrected Total 501 43.9
Oi 1 5.8 5.8 201.1 < .0001
Era 1 0.0 0.0 0.0 0.848
Oi*Era 1 0.0 0.0 1.5 0.219
Log(Age) 1 1.3 1.3 44.8 < .0001
Oi*Log(Age) 1 1.6 1.6 56.8 < .0001
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328322
groups were similar to the overall patterns (not
presented).
4. Discussion
4.1. Fishing patterns
Although present-day fisheries exploit the whole
North Sea, historical fisheries were probably concen-
trated in coastal waters (Van Neer et al., 2002) where
younger age groups are generally more abundant.
Despite these differences, comparison of the catch
compositions showed a clear shift towards younger
fish in the present-day catches of cod and haddock
and to lesser extent in the plaice catches, which
corroborates the presumed lower level of exploitation
in the pre-industrial era. The relatively low number of
10 year and older plaice in the historical catches is
probably related to seasonal migration and fishing
patterns. Older plaice are only abundant in the south-
ern North Sea during the spawning period between
December and February, while plaice fisheries in the
16th century along the Dutch coast started in February
– March and lasted for about two to three months
(Egmond, 1997). The historical saithe sample showed
a bimodal age distribution with a peak on age groups
3 to 5 and 9 to 10+, but it is doubtful whether this
pattern reflects the historical catch composition be-
cause of the small sample size.
4.2. Methodology growth analyses
The reconstruction of growth patterns in fish pop-
ulations based on the analysis of increments in otoliths
may be subject to bias. Firstly, sampling bias can occur
if growth rates are estimated using only market samples
(Rijnsdorp and Van Leeuwen, 1992). Growth rates of
the youngest age groups (age at capture), which are
only partially recruited to the exploited population, will
be overestimated because only the fastest growing fish
will have reached marketable sizes. This bias cannot
have occurred in the modern growth rate estimates
(with the exception of saithe), because survey and
market samples were used. The historical otoliths,
however, can be considered to represent a historical
market sample. This source of bias probably affects
plaice more than the gadoid species, because the latter
L.J. Bolle et al. / Journal of Sea R
grow faster and fewer age groups are only partially
recruited to the fisheries. However, comparisons of
growth rates estimated for fully recruited age groups,
which are insensitive to this bias, confirm the overall
differences in growth rate observed.
A second source of bias may be introduced through
mortality. In every population a certain variation in
growth rate will occur. Each size class consists of
relatively young, fast-growing fish as well as older,
slower-growing fish, but the proportion of the initial
growth rate types changes with increasing size. If
mortality is independent of size, the probability that
fish survive to a certain size class will be higher for
fast-growing fish than for slow-growing fish. If size-
selective mortality occurs certain growth types may be
selectively removed from the population. In exploited
fish populations the fast-growing fish of a year class
will be caught first, and it may take several years
before the slowest-growing fish are subject to fishing
mortality (Ricker, 1969). Fishing mortality usually
causes selective removal of fast-growing fish, but
the direction of selectivity may vary if a dome-shaped
selection pattern occurs in which intermediate-sized
fish are more vulnerable to fishing mortality than large
fish (Sinclair et al., 2002a). Sinclair et al. (2002b)
examined the relative importance of size-selective
mortality, density and temperature using an integrated
statistical model and concluded that size-selective
mortality was the dominant effect in the growth
analyses of cod in the Gulf of St. Lawrence, Canada.
A simulation study (Rijnsdorp, 1999) showed that
size-selective mortality bias in back-calculation stud-
ies is strongest when growth rates are estimated using
otoliths of large fish that are close to their maximum
size, whereas the bias is insignificant when otoliths of
smaller fish are analysed. In the present study only
very few fish close to their maximum size were
analysed. Assuming an unchanged selection pattern,
the comparison of growth rates within an age group
(age at capture) will be unbiased. To minimise age
effects due to sampling bias or size-selective mortal-
ity, the growth rates were weighted for the age
distribution of the samples. Furthermore, the growth
rates were also compared within age groups and these
results confirmed the overall patterns. Age was in-
cluded in the statistical analyses and the differences in
growth rates corrected for age effects is significant in
plaice, cod and haddock.
4.3. Changes in growth
Given the above considerations, we may conclude
that an increase in growth rate has occurred in cod,
haddock and plaice since the pre-industrialised era. In
cod and plaice, the increase was restricted to the
smaller size classes, whereas in haddock an increase
in growth occurred over the full size range. The
question now arises of whether the increase in growth
took place in the period of the expansion of the
fisheries in the second half of the 19th century, when
stock biomass probably showed its sharpest decline as
can be inferred from the decline in catch rates (Sah-
rhage and Wagner, 1978; Rijnsdorp and Millner,
1996), or in the course of the 20th century. The results
of our study are compared with growth curves for
different time periods during the 20th century taken
from the literature (Fig. 6). These comparisons show
that the sizes at age estimated for the pre-industrial-
ised era are strikingly close to those recorded for the
first half of the 20th century.
Growth in haddock in the 1926–1939 period was
slightly lower than in the pre-industrialised era (Fig.
6d). The archaeological otoliths (1425–1800) were
obtained from Belgian excavations sites and historical
evidence suggests that these fish were caught in a
local fishery (Van Neer et al., 2002). As latitudinal
differences in growth rates have been reported (Par-
rish and Jones, 1952; Jones, 1962), it is probable that
these specimens will have exhibited higher growth
rates than contemporaneous specimens from the cen-
tral and northern North Sea. The rather high numbers
of haddock otoliths found at Belgian excavation sites
indicate that this species must have been quite nu-
merous in the southern North Sea in the (post-)medi-
eval period, whereas nowadays haddock only occurs
in the central and northern North Sea. This interpre-
tation is supported by an analysis of trade and tax
archives (Holm and Bager, 2001). Between the 1920s
and the 1950s the growth increased coinciding with an
overall decrease in abundance (Jones and Hislop,
1978). In the 1960s, the growth rates of the two
extremely abundant year classes of 1962 and 1967
as well as those of the following two weak year
classes born in 1963 and 1968 were retarded, indicat-
ing a density-dependent response (Jones, 1983). In the
long term, there has been an increase in mean lengths
at age, and the lengths at age of the 1961 and 1966
esearch 51 (2004) 313–328 323
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328324
year classes which preceded the strong 1962 and 1967
year classes were the highest recorded since the 1920s
(Jones, 1983). Growth rates have continued to in-
crease in the 1980s (Wagner and Dethloff, 1985), and
current growth rates as revealed by back-calculations
appear to be the highest ever reported for the North
Sea. Since the gadoid outbursts in the 1960s popula-
tion size has decreased, and during the last two
decades population size is more or less stable with
occasional peaks corresponding to the maturation of
above-average year classes (Hislop, 1996; ICES,
2003). The changes in haddock growth rates appear
to be closely related to changes in population size.
Density-dependent growth was also reported for other
haddock stocks (Marshall and Frank, 1999).
In cod, the mean size at age estimated for the
whole North Sea in the early 20th century (Graham,
1934) did not differ from the medieval growth curve
for the northern North Sea, and was slightly higher
than the growth curve based on otoliths from Belgian
excavation sites (Fig. 6b–c). Between 1930 and the
1970s, mean size-at-age has slightly increased due to
growth rate changes in the smaller size classes. In the
northern North Sea this difference is very small and
almost non-existent if fitted Von Bertalanffy growth
curves are compared (Daan, 1974, 1978). Houghton
and Flatman (1981) examined annual weight gain in
relation to VPA stock size estimates for the period
1963–1977 and concluded that growth in the western
North Sea was density dependent. However, a critical
re-examination by Daan et al. (1990) showed that
alternative interpretations were possible. They con-
cluded that a significant downward trend in annual
weight gain existed only for 1-group cod, but that this
trend was not significantly related to population
density. Bromley (1989) investigated the evidence
for density-dependent growth in gadoids using survey
data for the period 1977–1987. He focussed on 1 and
2 group cod, haddock and whiting and found that in
Fig. 6. Comparison of fish length at age curves estimated for
different time periods for (a) plaice, (b) southern cod, (c) northern
cod, (d) haddock, and (e) saithe. The numbers between brackets in
the legends refer to the following sources: (1) Fig. 3 in Rijnsdorp
and Van Leeuwen (1992); (2) page 67 in Graham (1934); (3a) Table
3 in Daan (1974); (3b) Table 6 in Daan (1974); (4) Table 25 in Jones
and Hislop (1978); (5) Fig. 39 in Wagner and Dethloff (1985); (6)
Table 5 in Cieglewicz and Draganik (1969); (7) Tables 1–2 in
Moguedet et al. (1987).
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328 325
all but 1-group cod a negative correlation existed
between size-at-age and density. However, most of
the variation was caused by an area effect and
evidence for density-dependent growth within areas
was minimal. Brander (1999) ascribed most of the
variability in cod growth rates to temperature effects.
Overall, there appears to be little support for density-
dependent growth in North Sea cod. For Barents Sea
cod, an inverse relationship is observed between the
abundance and the mean size-at-age of juveniles.
Ottersen et al. (2002) argue that both abundance and
mean size-at-age are mainly determined by abiotic
density-independent mechanisms during the first half
year of the fishes’ life.
The available data on saithe did not provide
evidence for a change in growth since the pre-indus-
trial era, since the back-calculated growth for the
present and the pre-industrial era fall within the range
of observations reported in the literature (Fig. 6e).
In plaice, the pre-industrial growth curve (1425–
1800) was very similar to the 1930s growth curve, but
well below the present-day growth curves (1970–
1979 and 1995–1999, Fig. 6a). Rijnsdorp and Van
Leeuwen (1996) showed that the growth rates of the
smaller size classes increased in the 1960s and 1970s.
These changes in growth were not related to temper-
ature but coincided with an increase in nutrients in the
coastal waters, which resulted in an increase in
benthic productivity in the plaice nursery areas (Beu-
kema, 1989; Beukema and Cadée, 1988). It also
coincided with an increase in trawling impact on the
benthos, which may have enhanced the productivity
of opportunistic benthic species (Rijnsdorp and Van
Beek, 1991; Rijnsdorp and Van Leeuwen, 1996).
Therefore, the lower growth rate of juveniles before
the 1960s is likely to have been caused by competition
for food. Borley (1916) transplanted juvenile plaice
from the crowded inshore nursery grounds to a
shallow offshore bank where no small plaice occurred.
Growth of the transplanted plaice increased to a level
comparable to the rate observed in the 1970s and
1980s (Rijnsdorp and Van Leeuwen, 1992). A densi-
ty-dependent reduction in growth has been reported
for the juveniles of abundant year classes in the early
20th century, a phenomenon that still occurs today
despite the improved feeding conditions (Rijnsdorp
and Van Leeuwen, 1996; ICES, 2003). Evidence for
changes in growth of adult plaice is not equivocal. A
suggestion for density-dependent growth in the adult
phase stems from the decrease in mean weight-at-age
of adults during World War II, when fishing was
substantially reduced and the biomass of plaice in-
creased threefold (Beverton and Holt, 1957). Further-
more, the back-calculated length increment of adults
was reduced at the end of the war and the years
immediately following the war (Rijnsdorp and Van
Leeuwen, 1992). However, this reduction may also
have been due to the survival of slower growing fish
that would have been selectively removed by the
fishery if the fishery had continued during the war
(Rijnsdorp, 1999). Given the similarity in growth rates
of plaice larger than 30 cm between the pre-industrial
era and the current time, it is concluded that density-
dependent growth in adult plaice does not play a
major role in the North Sea.
Other factors such as the temperature regime
(Brander, 1999), the overall productivity of the eco-
system (Cushing, 1982) or selective fishing (Stokes et
al. 1993; Law, 2000; Heino and Godo, 2002) may also
have influenced the changes in growth rates. Growth
rate is positively correlated with temperature (Fonds et
al., 1992) and the observed geographical variation in
growth rates is likely to reflect the latitudinal trend in
temperature. For haddock, no clear latitudinal pattern
was detected in the present study because of the
restricted sampling range, but geographic and latitu-
dinal differences in growth rates were reported by
Parrish and Jones (1952) and Jones (1962). On
average temperatures have increased by about 1.5
jC since the Middle Ages (KNMI, 1999). The periodbetween 1400–1700 AD was the coldest period since
the last glacial and is referred to as the ‘Little Ice Age’
(Lamb, 1995). However, these temperature recon-
structions refer to air temperatures in winter, whereas
water temperatures in summer mainly determine
growth rates of fish. Furthermore, within time frames
corresponding to the precision of the dating of ar-
chaeological otoliths (50–200 years), variations in
temperature regimes are indicated that often greatly
exceed the long-term increase (KNMI, 1999). Decad-
al-scale changes in marine ecosystems have been
reported in relation to climate forcing (Cushing,
1982), but the effect of changes in the overall pro-
ductivity of the North Sea ecosystem on growth is
difficult to evaluate. These uncertainties make it
difficult to assess the effect of climate changes on
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328326
growth rate comparisons between eras. Nevertheless,
it is unlikely that temperature rise alone can explain
the growth rate changes in haddock, taking into
account the relatively small growth rate changes
observed in the other species.
Demersal fisheries in the North Sea only harvest
fish above a certain minimum size and therefore may
cause an evolutionary change in life-history traits,
such as growth, maturation and reproduction (Stokes
et al., 1993; Law, 2000; Heino and Godo, 2002). The
reduction in the reproductive size and age observed in
North Sea plaice and northeast Arctic cod has been
shown to be partly due to such an evolutionary change
(Rijnsdorp, 1993b; Heino et al., 2002; Grift et al.,
2003). As maturation will channel energy resources
from somatic growth to reproduction, a reduction of
the size at first maturation is expected to result in a
decrease in somatic growth. Also direct selection for
certain growth types may occur, as shown experimen-
tally by Conover and Munch (2002). If a fisheries-
induced decrease in growth rate occurred, it may have
confounded an increase in growth rate due to the
release of the density-dependent competition.
In conclusion, an unequivocal interpretation of the
observed changes in growth cannot be given. Never-
theless, our study lends support for the hypothesis of
density-dependent growth in the adult phase in the
case of haddock, and it indicates that growth in
juvenile plaice may be related to density-dependent
processes. Our results do not provide evidence for
density-dependent growth in adult plaice, cod and
saithe, nor do they support the hypothesis that growth
of juvenile gadoids has decreased because of in-
creased juvenile abundance related to reduced preda-
tion pressure.
The lack of density-dependent growth in the adult
stages of plaice, cod and saithe may be related to the
difference in habitat availability for the successive life
history stages. Beverton (1995) hypothesised that
marine species, which concentrate spatially into nurs-
ery grounds, may saturate the carrying capacity of the
juvenile habitat, whereas the adult stage may not be
limited by adult habitat (Beverton, 1995; Iles and
Beverton, 2000). This hypothesis is related to the
nursery size hypothesis put forward by Rijnsdorp et
al. (1992) and the member/vagrant hypothesis pre-
sented by Sinclair and Iles (1989). As plaice, saithe
and to a lesser extent cod concentrate during the
juvenile phase (Daan et al., 1990), the ‘concentration
hypothesis’ may explain why we did not find a change
in growth during the adult life phase, whereas in
haddock, a species that does not concentrate during
the juvenile phase, an increase in growth rate was
observed. Whether density-dependent processes occur
in the adult phase depends on the relative size of the
habitats available for the successive life history stages.
In the Baltic, an enclosed sea basin with a relatively
large zone of shallow nursery grounds compared to
the size of the adult habitat, a large increase in adult
growth was observed during the increase in fishing
effort in the 20th century (Rijnsdorp, 1994).
Our study has shown that fish remains available
from archaeological sources may play an important
role in biological research of population dynamic
processes. Further work may extend the analysis to
other species and other areas to test whether our
conclusion of the lack of density-dependent growth
in the adult stages in species with limited nursery
grounds holds true.
Acknowledgements
We wish to thank Dr. James Barrett (University of
York), Bieke Hillewaert (Stedelijke Archeologische
Dienst Bruges), the ‘Mechelse Vereniging voor
Stadsarcheologie’, and Dr. Marnix Pieters (Institute
for the Archaeological Heritage of the Flemish
Community) for providing historical otoliths, and
Stina Bilstrup (Danish Institute for Fisheries Re-
search) and Andrew Newton (Marine Laboratory
Aberdeen) for providing additional present-day oto-
liths. Furthermore, thanks are due to Daphne Stal-
paert, Peter De Smedt, Gerrit Rink, Michael Easey,
Phillip Watts and Myrtle Boon for their help with
ageing and increment measurements and to Dr. Dirk
Nolf (Royal Belgian Institute of Natural Sciences) for
his help with the identification of the historical
otoliths. Finally we thank Niels Daan, Henk Heessen
and two anonymous referees for critical reading of the
manuscript. Funding for this study was provided by a
research grant (FAIR CT97-3462) from the Commis-
sion of the European Community. Wim Van Neer’s
contribution to this paper also represents research
results of the Interuniversity Poles of Attraction
Programme - Belgian Federal Science Policy Office.
L.J. Bolle et al. / Journal of Sea Research 51 (2004) 313–328 327
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Growth changes in plaice, cod, haddock and saithe in the North Sea: a comparison of (post-)medieval and present-day growth rates based on otolith measurementsIntroductionMaterials and methodsArchaeological excavationsPresent-day otolith samplesOtolith preparations and measurementsMeasurement errorsGrowth analyses
ResultsAge and size distributionsGeographic variations in growth ratesComparison of growth rates between eras
DiscussionFishing patternsMethodology growth analysesChanges in growth
AcknowledgementsReferences