Growth changes in plaice, cod, haddock and saithe in the North … · Growth changes in plaice, cod, haddock and saithe in the North Sea: a comparison of (post-)medieval and present-day

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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).


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


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


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.


Fig. 4. Geographic variations in mean annual increment per otolith

size class for (a) plaice, (b) cod, and (c) haddock.


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


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


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


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


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


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


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


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).


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


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.


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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

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Growth changes in plaice, cod, haddock and saithe in the North … · Growth changes in plaice, cod, haddock and saithe in the North Sea: a comparison of (post-)medieval and present-day