vitale_phd_thesis.pdf (1.8 MB) - Göteborgs universitet

Faculty of Science 

2008 

Reproductive aspects of Kattegat cod (Gadus morhua): 

implications for stock assessment and management 

Francesca Vitale 

Doctoral thesis 

Department of Marine Ecology 

Swedish Board of Fisheries 

University of Gothenburg 

Institute of Marine Research 

Sven Lovén Centre for Marine Science Turistgatan 5 

Kristineberg Marine Research Station 

SE-453 21 Lysekil, Sweden 

SE-450 34 Fiskebäckskil, Sweden 

Akademisk avhandling för filosofie doktorsexamen i Marin Zoologi vid Göteborgs 

Universitet. Avhandlingen försvaras den 5 juni 2008, kl 10.00 på Sven Lovén Centrum 

för Marina Vetenskaper - Kristinebergs Marina Forskningsstation, Fiskebäckskil. 

Examinator: Prof. Mike Thorndyke 

Fakultetsopponent: Dr. Jonna Tomkiewicz, National Institute of Aquatic Resources, 

Technical University of Denmark, Kavalergården, 6, DK-2920, Charlottenlund, 

Denmark. 

1

CONTENTS 

ABSTRACT 3 

LIST OF PUBLICATIONS 4 

INTRODUCTION 5 

REPRODUCTIVE CYCLE 8 

Ovarian gross morphology 9 

Ovarian cellular development 10 

Comparisons between the staging systems 13 

Potential energetic proxies of maturity status 15 

FECUNDITY 17 

SPAWNING AGGREGATIONS 21 

CONCLUSIONS AND IMPLICATION FOR MANAGEMENT 24 

REFERENCES 26 

ACKNOWLEDGEMENTS 39 

2

Abstract 

The Kattegat cod (Gadus morhua) stock has been estimated to be currently at its lowest level since 1971 

and the biomass of reproducing fish (spawning stock biomass, SSB) has been reduced by 95%. The whole 

stock is compressed to a few age classes and the reproduction is mainly dependent on first spawners. 

Despite rigorous catch limitations, there are no signs of recovery and since the year 2000 this stock has 

been considered outside safe biological limits. Assessment and management of fish populations currently 

rely on estimations of SSB, which in turn are based on the proportion of mature fish within age classes in 

the population (i.e. maturity ogives). A proper identification of mature individuals in the population is thus 

a crucial step for a precise estimation of SSB, and ultimately for evaluating the status of the stock and 

establishing harvest levels. In this study the gonadal development of cod in the Kattegat and Sound was 

studied by investigating ovarian histological structure on a temporal scale. Starting from existing maturity 

criteria, a modified system based on histological features was developed in order to emphasize crucial 

steps in the developmental process. Furthermore alternative indicators of maturity status were identified in 

the gonadosomatic index (GSI) and hepatosomatic index (HSI), representing the ratio of gonad and liver 

weight to the body weight, respectively. Comparisons between histological and routinely used 

macroscopical (visual) maturity judgement evidenced consistent discrepancies. The visual analysis 

consistently overestimates the proportion of mature females in all age classes. The overestimation is more 

severe for first-time spawners, due to a decreasing error with increasing age. According to present results 

the female spawning biomass (FSB) of Kattegat cod may have been overestimated by up to 35% for more 

than 20 years. 

Fecundity in cod has been shown to be tightly coupled with maternal size, condition and spawning 

experience, with first-time spawners having a lower reproductive success. In Kattegat cod, just prior to the 

spawning season fish length explains the largest part of fecundity variability. On the other hand, the 

maternal condition (HSI and body condition), did not consistently increase the explanatory power 

provided by fish size alone. However, in order to determine the maternal influence on egg production, the 

condition of the individual fish should be quantified at an earlier stage of the maturation process, when 

energy is initially allocated to egg production. SSB, currently used as reproductive potential predictor in 

stock assessment models, fails to accurately account for the effect that variation in length composition and 

fish condition has on the stock reproductive output. This leads to an overestimation of the reproductive 

potential when the stock is dominated by small individuals as is the case of the Kattegat cod stock. Taken 

together, the overestimation of the stock reproductive success may have led to the implementation of 

regulating measures far above the stock capacity, masking the need of a more drastic catch control. 

The use of fishery dependent and independent data shows that cod have been aggregating and spawning in 

specific areas in the southern Kattegat for more than 25 years, although in considerably reduced numbers 

over time. It was thus indicated that spawning activity may have also ceased in some areas previously 

depicted as spawning grounds. These findings were supported by independent samplings of individual 

physiological and histologically determined maturity status. 

On the whole, a revision of Kattegat cod stock assessment models and a re-evaluation of the reference 

points, based on increased stock-specific biological knowledge, is strongly suggested. The use of more 

accurate methods for estimating individual maturity may integrate and reinforce the routinely used 

methodology during research surveys. However, a monitoring program based on direct measurements of 

stock fecundity, and factors influencing it, ought to be considered. The acquired knowledge on the 

persistence of the spawning aggregations may facilitate the implementation of a more temporally and 

spatially controlled fishing activity. This thesis represents an insight into the reproductive biology of 

Kattegat cod, aiming to enhance the accuracy and precision in biological data used for stock assessment 

and thus assist fishery management decisions. 

Keywords: Gadus morhua, fecundity, histology, Kattegat cod, maturity ogives, physiological indices, 

spawning grounds, SSB, stock assessment, stock management. 

Department of Marine Ecology, University of Gothenburg 

Sven Lovén Centre for Marine Science - Kristineberg Marine Research Station 

S-450 34 Fiskebäckskil, Sweden 

3

LIST OF PUBLICATIONS 

I. Vitale, F., Cardinale M. and Svedäng, H., 2005. Evaluation of the temporal 

development of the ovaries in Gadus morhua from the Sound and Kattegat, North 

Sea. Journal of Fish Biology, 67: 669-683. doi:10.1111/j.0022-1112.2005.00767.x 

II. 

III. 

IV. 

Vitale, F., Svedäng, H and Cardinale, M., 2006. Histological analysis invalidates 

macroscopically determined maturity ogives of the Kattegat cod (Gadus morhua) 

and suggests new proxies for estimating maturity status of individual fish. ICES 

Journal of Marine Science, 63: 485-492. doi:10.1016/j.icesjms.2005.09.001 

Vitale, F., Thorsen, A. and Kjesbu, O.S. Potential fecundity of Kattegat cod 

(Gadus morhua) in relation to pre-spawning body size and condition. Manuscript 

Vitale, F., Börjesson P., Svedäng H. and Casini M., 2008. The spatial distribution 

of cod (Gadus morhua L.) spawning grounds in the Kattegat, eastern North Sea. 

Fisheries Research 90: 36-44. doi: 10.1016/j.fishres.2007.09.023 

Publications I, II and IV are reproduced with the permission from the publishers. 

4

INTRODUCTION 

Cod (Gadus morhua) has since the Middle Ages been one of the most 

socioeconomically important fish species, triggering the development of more and more 

sophisticated fishing tools for increasing the catches (Kurlansky, 1998). The 

consequence has been a decline in cod stocks all over the North Atlantic (Myers et al., 

1996; Cook et al., 1997; Hutchings, 2000) and not least the stock inhabiting the 

Kattegat area (Svedäng and Bardon, 2003; Cardinale and Svedäng, 2004). 

The International Council for the Exploration of the Sea (ICES) including 20 members 

countries was founded in 1902. The main aim was to promote marine research in North 

Atlantic (including the adjacent Baltic and North Sea) for evaluating the effects of 

fishery activity in comparison to natural fluctuations and carry out an international 

coordination research of the sea. ICES is aimed at estimating and determining safe 

harvesting limits to prevent the collapse of commercial fish stocks. Scientists must 

therefore determine the quantity of fish that can be caught without reducing the 

spawning stock to a level where recruitment to the stock is seriously threatened. In other 

words, the main goal is to develop harvest control rules for preserving sufficient stock 

reproductive potential to allow a sustainable exploitation. 

Fish stocks’ abundance and fishing mortality are presently assessed using age-structured 

models, such as virtual population analysis (VPA), based on catch, effort and survey 

data (Pelletier and Laurec, 1992). The harvest is generally regulated through the 

establishment of annual total allowable catches (TAC). The cod stock in the Kattegat 

(ICES Subdivision 21) is currently assessed as a separate stock. The assessment relies 

on survey data from the International Bottom Trawl Survey (IBTS) carried out in the 1 st 

and 3 rd quarters of the year on board of the Swedish R/V Argos, and from the Danish 

Kattegat Bottom trawl carried out in the 1 st and 4 th quarters of the year on board of the 

Danish R/V Havfisken. 

The demersal fishery in the Kattegat, most exclusively Danish (~70%) and Swedish 

(~30%), is based on trawling activity and it targets crayfish (Nephrops norvegicus), cod 

and flatfishes (in particular plaice-Pleuronectes platessa and sole- Solea solea). Back in 

the 1950s and 1960s there was also a developed fishery on other species such as 

haddock (Melanogrammus aeglefinus) and pollack (Pollachius pollachius). Due to the 

decline of these two stocks, cod and, to a small extent whiting (Merlangius merlangus) 

are presently the only gadoid species fished in the area. Cod is mostly fished during the 

spawning period in the 1 st quarter of the year by a trawl fishery directed on the 

spawning grounds, historically recognized in the central and southern part of the 

Kattegat (Pihl and Ulmestrand, 1988; Hagström et al., 1990; Svedäng and Bardon, 

2003). In addition, cod are incidentally exploited in the Nephrops fishery, taking place 

the whole year around in the deeper parts of the Kattegat. In this fishery cod are 

captured as by-catch species and successively discarded if the allowed quota is 

surpassed or if the fish is under the allowed catchable size. 

The assessment of Kattegat cod has shown a drastic reduction in total biomass and 

biomass of reproducing fish (spawning stock biomass, SSB) since 1970s (Figure 1), 

mainly attributable to overfishing. This decline occurred in concomitance with the 

disappearance of separate spawning aggregations (Svedäng and Bardon, 2003). 

5

Consequently the number of recruits (1 year-old individuals), despite the significant 

inflow of eggs and larvae from the Skagerrak-North Sea cod stocks (Cardinale and 

Svedäng, 2004; Svedäng and Svenson, 2006) is also severely reduced (Figure 1). In 

accordance, catches have been limited and commercial landings have steadily declined 

from around 15.000 in 1970 to 876 in 2006, which is the lowest value in the time series. 

Despite the rigorous catch limitations, the stock has not shown any sign of recovery and 

at present is considered as severely depleted. Currently, the spawning stock biomass 

remains at historically low levels, and at the present state the fishery is largely 

dependent on the strength of incoming year classes (ICES, 2007). The stock has been 

considered outside safe biological limits since year 2000, and from 2002 and onwards, 

the ICES Advisory Board has recommended zero catches from the area. 

a 

80000 

70000 

60000 

Recruits 

Total Biomass 

SSB 

50000 

40000 

30000 

20000 

10000 

0 

b 

25000 

1970 

20000 

1975 

1980 

1985 

1990 

1995 

2000 

2005 

Landings 

15000 

10000 

5000 

0 

1970 

1975 

1980 

1985 

1990 

1995 

2000 

2005 

Year 

Figure 1: Time series of (a) Number of recruits (1 year-old individuals), Total biomass and 

SSB (in tonnes) and (b) commercial landings in Kattegat cod ( in tonnes)(ICES, 2007). 

6

Stock-recruitment models are important tools for the management of exploited 

populations (Ricker, 1975). These models represent a fundamental link between the 

parental population and the number of offspring produced, i.e. recruitment. The 

relationship between the SSB and the number of recruits is used to determine to what 

extent a stock may be harvested. Furthermore, annual TACs are determined by using 

SSB as one of the reference points. Accurate estimates of the SSB thus represent a key 

factor for evaluating the status of the stock and establishing harvest levels. 

SSB is calculated as the aggregated weight of mature individuals in each age class. The 

correct identification of mature individuals in the population is thus the crucial step for a 

precise estimation of SSB. Histological analyses of reproductive organs are considered 

the most accurate means for evaluating the degree of individual maturation (Murua et 

al., 2003; Kjesbu et al., 2003; Tomkiewicz et al., 2003a). However, the assignment of 

individual maturity status is conventionally based on macroscopical (visual) inspection 

of the reproductive organs. Therefore the accuracy of SSB estimations is mainly 

dependent on the ability of the observer to discriminate reproductively active 

individuals. The subjectivity of this method entails the risk to introduce an error in the 

estimations of the SSB, distorting the relationship between stock and recruitment 

(Murawsky et al., 2001). 

An additional issue concerns the use, in most stock-recruitment models, of the SSB as a 

proxy of stock reproductive potential, assuming that SSB is proportional to the stock 

total annual egg production (Marshall et al., 2006 and references therein). This 

assumption implies that equal biomass weights generate the same reproductive output. 

An increasing number of studies have challenged this assumption, arguing that 

demography (Solemdal et al., 1995; Trippel, 1998; Trippel, 1999; Tomkiewicz et al., 

2003b), spawner quality (Jørgensen, 1990; Kjesbu et al., 1991; Solemdal et al., 1995; 

Marshall et al., 1998; Trippel, 1998) and environmental variability (Pörtner et al., 2001; 

Koops et al., 2003; Lambert et al., 2003) have a strong influence on reproductive 

success. Furthermore, the SSB estimates are often derived from combined male and 

female maturity data. Growth, maturation and mortality are known to be sexually 

dimorphic in many marine fish species, i.e. earlier maturity and shorter lifespan in males 

(Tomkiewicz et al., 2003b and references therein). Therefore skewed sex-ratio affects 

the composition of the spawning stocks and compromises the reliability of SSB as a 

measure of stock reproductive potential. Consequently, concerns about the use of SSB as 

a suitable proxy for stock reproductive potential have been increasingly raised 

(Jørgensen, 1990; Kjesbu et al., 1991; MacKenzie et al., 1998; Trippel, 1999; Kraus et 

al., 2002; Marshall et al., 2003: Köster et al., 2003;). In light of these issues, information 

about stock structure, spawners’ size at age, sex ratio, proportion of mature at age, 

fecundity, which all in turn influence offspring number, size and viability are 

fundamental for accurate estimations of stock reproductive potential. 

Stock-specific knowledge about fish reproductive biology is therefore an essential tool 

when managing a stock and represents the basis for the establishment of a sustainable 

yield. From a management point of view, accurate knowledge about maturity status is 

important for determining the size at which maturity is first reached, i.e. when the fish 

can be considered as adult. This information can be used for establishing the minimum 

size at capture to allow fish to reproduce at least once before being captured. 

Furthermore, temporal and spatial information on the maturation pattern are essential for 

identifying spawning grounds and determining the timing of area closure to protect the 

7

spawning activity. Moreover, understanding the relationships between age/size at 

maturity or fecundity, food availability and population size is fundamental for predicting 

the vulnerability of the stock to increasing exploitation pattern and/or changing 

environmental condition. Therefore investigations of reproductive biology are not only 

important for understanding stock dynamics, but represent the basis for a correct stock 

assessment upon which effective management strategies have to rely. 

In this thesis, I investigated the temporal development of the ovaries in cod from 

Kattegat and the Sound and explored possible differences in maturity schedule between 

the two subpopulations. This led to the development of a histologically based maturity 

scale where key events for discriminating maturing individuals are emphasized (I). In 

paper II, the new built histological scale is used in an attempt to validate the 

conventionally used visual evaluation of ovaries. The detected differences are 

successively used to reconstruct the historical (1971-2004) female spawning stock 

biomass (FSB) of Kattegat cod. Furthermore, potential proxies of maturity status are 

sought among physiological parameters. Paper III examines the potential fecundity in 

pre-spawning individuals and explores its relationship with the maternal size and 

condition. In addition, the length-specific potential and relative fecundity and oocyte 

size are investigated in Kattegat cod and compared to the more healthy Northeast Arctic 

cod stock (NEAC). In paper IV combined survey and commercial data, together with 

individual histological maturity and physiological status, are used for detecting putative 

spawning areas and testing the stability of spawning aggregations. The scope of this 

thesis was therefore the acquisition of accurate stock-specific information about timing, 

location and quality of reproductive performances in Kattegat cod in order to improve 

the assessment and assist the implementation of a more realistic management plan 

aiming at the recovery of this stock. 

REPRODUCTIVE CYCLE 

Natural selection favours individuals who efficiently gather energy and matter from the 

environment and effectively allocate it in order to maximize its fitness. Ideally, a fish 

would mature early at a large size and produce numerous and large offspring over a long 

reproductive life span. However, in the real world resources are limited and allocated 

according to the physiological trade-offs between metabolic needs, survival and 

reproduction. The energy demand related to reproduction also includes the behavioural 

aspects linked to it (courtship and migration) beyond the main energy consumption 

involved in gonadal development. 

Hence each fish species displays a reproductive strategy (Murua and Saborido-Rey, 

2003), which is the overall pattern of reproduction typically shown by individuals in a 

species, and a reproductive tactic which includes variations in the typical pattern, in 

response to the environmental fluctuations (Wootton, 1984; Murua et al., 2003). 

Most of the studies on fish reproduction have focused on females, partly because of the 

maternal origin of the nourishment in the early life stage and partly because eggs more 

than sperms represent a limiting factor for the offspring production (Helfman et al., 

1997). 

8

Cod, as all gadoids, is an iteroparous species, which means that spawning occurs more 

than once during lifetime, in contrast with semelparous species, such as eel (Anguilla 

anguilla) which have only one breading season and successively die. Fecundity is 

determinate in cod which implies that the number of eggs that will develop is fixed 

before the onset of the maturation process (Kjesbu and Kryvi, 1989; Morrison, 1990). 

Species with indeterminate fecundity show continuous oocytes recruitment during the 

entire spawning period. 

Ovaries are paired elongate hollow organs situated ventrally to the swim bladder and 

consist of several transverse ovigerous folds projecting into the lumen where growing 

germ cells, i.e. oocytes, originated by meiosis from primordial cells (oogonia), become 

eggs (oogenesis). The ovarian development in cod is group synchronous showing 

discrete cohorts of developing oocytes co-existing in the gonad, successively recruited 

and spawned as discrete groups (i.e. batches) (Kjesbu and Kryvi, 1989). The described 

pattern can be observed throughout the whole organ due to the homogeneity 

characteristic of cod ovaries (Kjesbu et al., 1990). 

The different phases the ovary goes through during the developmental process have been 

classified and used for building a large number of maturity scales. Individuals are 

assigned to different stages, according to their maturity status. Maturity scales are an 

important tool for determining stock specific spawning pattern and for recognising 

reproductively active individuals. Their accuracy is a crucial prerequisite for a correct 

estimation of the maturity ogives, (i.e. the proportion of mature individuals at age in the 

population) and consequently of the SSB. 

Ovarian gross morphology 

During the maturation process, ovaries undergo different modifications in the gross 

morphology showing changes in size, vascularisation, consistency and colour. At the 

beginning, ovaries are small, translucent yellow-reddish structures situated in the 

posterior part of the abdominal cavity. Following the maturation process, ovaries 

become larger, firmer, more opaque dark-red/orange and fill most of the cavity. As 

ripening begins oocytes become increasingly evident through the ovarian surface, at first 

as opaque granules and successively as transparent eggs as spawning approaches. After 

the eggs are released the now reddish-grey ovary appears shrunk and contracted, i.e. 

spent stage, and successively enters the recovering stage (Table 1). 

The macroscopical (visual) examination of reproductive organs is a low cost and quick 

method for assessing maturity, allowing the analysis of a large amount of samples. The 

judgement of the reproductive status based on the gross anatomy of the ovary is 

therefore ideal for routine monitoring of fish stocks in order to estimate the maturity 

ogives. Specimens are assigned to one of the different stages included in the used 

maturity scale according to their external appearance. The maturity scales may vary on a 

national level as different countries utilize different criteria. The national scale is 

successively converted into the international conventionally approved staging system 

before reporting to ICES. 

The 4-stages maturity scale (ICES, 1999) presented in Table 1, is used during the IBTS 

performed annually in Kattegat, Skagerrak and North Sea. 

9

VIRGIN 

MATURING 

SPAWNING 

SPENT 

Ovaries small, elongated, whitish, translucent. No signs 

of development. 

Development has obviously started, eggs are becoming 

larger and the ovaries are filling more and more of the 

body cavity but eggs cannot be extruded with only 

moderate pressure. 

Will extrude eggs under moderate pressure to advanced 

stage of extruding eggs freely with some eggs still in 

the gonad. 

Ovaries shrunken with few residual eggs and much 

slime. Resting condition, firm, not translucent, showing 

no development. 

Table 1: Macroscopical maturity scale from the manual for the International Bottom Trawl 

Surveys (IBTS) 

According to the 4-stages scale, only individuals assigned to the first stage are 

considered immature (juveniles) and therefore have to be excluded form the spawning 

biomass. The second stage should include all the maturing individuals that are going to 

finalize their maturation by the forthcoming spawning season. The third stage, i.e. 

spawning, includes only individuals which are expelling eggs when captured. The last 

stage, i.e. spent, comprises the individuals that have recently released all the eggs, but 

also specimens that have already entered a post-spawning condition (resting stage). All 

the stages from the second and upwards are therefore considered to contribute to the 

annual reproductive potential of the stock and consequently included as mature in the 

estimations of the maturity ogives. 

Ovarian cellular development 

The described modifications of the gross morphology mirror a series of developmental 

changes on a cellular level identifiable by the means of histological analyses. The 

general cellular cycle, common to all teleosts (Wallace and Selman, 1981; Tyler and 

Sumpter, 1996), includes a phase of primary oocyte growth, during which the oocytes 

increase slightly in size and cytoplasmatic structures, such as the circumnuclear ring 

(CNR), begin to appear. The following phases include a first proliferation of spherical 

vesicles (cortical alveoli) followed by a period of yolk accumulation (vitellogenesis). 

Finally, after the final maturation, hydrated oocytes (now eggs) are ovulated into the 

ovarian lumen. The ruptured follicles (post-ovulatory follicles, POF) remain in the 

ovary and persist for a limited time degenerating after spawning. The duration of these 

structures is however still under discussion and might be species specific. In flounder 

(Platichthys flesus), POFs have been seen up to 1 month after spawning (Janssen et al., 

1995) while in cod, POFs have been recognized up to 9 months after spawning 

10

(Saborido-Rey and Junquera, 1998; Rideout, 1999). Vitellogenic oocytes that do not 

complete the maturation undergo a degenerative process called atresia and are 

successively reabsorbed, while the ovary regenerates. 

As mentioned above, oocyte cohorts at different developmental stages co-exist in cod 

ovaries although the first appearance of oocytes showing advanced specific features 

marks the maturity stage and it is used as stage indicator. 

Histological techniques have been increasingly used for investigating the oogenesis of 

cod from different areas (Kjesbu and Kryvi 1989; Saborido-Rey and Junquera, 1998; 

Tomkiewicz et al., 2003a, I) and a number of histological maturity scales have been 

produced. Tomkiewicz and co-workers (2003a) proposed a 10-stages maturity scale for 

the Baltic cod, subdividing the general classification scheme and adding also some 

important stages, which show potential disease that may reduce fecundity. The 

histological analyses of gonadal development in cod from the Kattegat and the Sound 

brought to the development of a 7-stages maturity scale (I, Table 2). 

IMMATURE 

PREVITELLOGENIC 

GROWTH 

ENDOGENOUS 

VITELLOGENESIS 

EXOGENOUS 

VITELLOGENESIS 

FINAL 

MATURATION 

SPENT 

RESTING 

Small oocytes with a dense basophilic cytoplasm, a central nucleus 

and few large nucleoli around its edge (perinucleolar stage) 

Oogonia are always present but they might not be visible 

The nucleus increases in size and multiple nucleoli are formed. A weakly 

stained area called “circumnuclear ring” (CNR) is also present 

The circumnuclear ring moves towards the outer part of the cell and 

gradually disintegrates, while the spherical cortical alveoli appear 

in the superficial half of the cytoplasm. No yolks granules present yet. 

Presence of yolk granules. The nucleus, still centrally located, becomes 

irregular. The occurrence of this stage means that the maturation 

process is in progress, and under normal conditions, the individual will 

develop within the current spawning season 

The chorion becomes thicker, the nucleus migrates towards the animal 

pole and the hydration process occurs 

Post-ovulatory follicles (POFs), after oocytes release into the lumen, 

are distinguishable. 

Oocytes in stage 1 and 2. Some Post-ovulatory structures 

(POF), still present, show signs of previous spawning 

Table 2: Maturity scale based on histological inspection of ovaries (I) 

The critical point in maturity studies is to detect the threshold beyond which an 

individual can be considered as maturing within the present season and unquestionably 

going to spawn within the next spawning season. In other words, it is particularly 

important to specify the minimum level of oocyte development necessary for a female 

11

to be considered mature. According to some studies (Woodhead and Woodhead, 1965; 

Shirokova, 1977; Holdway and Beamish, 1985), individuals presenting oocytes in the 

CNR stage (Table 2 stage 2) are likely to mature within the following spawning season. 

However, ovaries at this stage are always present and the probability of carrying on the 

maturation process depends on the degree of development in relation to the time of the 

year in which they are observed (Woodhead and Woodhead, 1965; Holdway and 

Beamish, 1985; Tomkiewicz et al., 2003a). 

Further studies (Saborido-Rey and Junquera, 1998; Tomkiewicz et al., 2003a) have 

identified the threshold between mature and immature fish in the cortical alveoli stage 

(Table 2, stage 3 and Figure 2a). The content of these alveoli and their role in the 

fertilization have been investigated in a number of teleosts and it has been shown that 

they mainly contain endogenously (in situ, within the oocyte) synthesized glycoproteins 

(Tyler and Sumpter, 1996). This stage is therefore called endogenous vitellogenesis 

(Burton et al., 1997, I) in contrast with the true (exogenous) vitellogenesis occurring 

when yolk granules are formed using vitellogenin sequestered from the maternal liver 

(Tyler and Sumpter, 1996). 

yg 

a 

ca 

Figure 2: Histological sections of oocytes at the a) endogenous vitellogenesis stage with 

cortical alveoli (ca) and b) exogenous vitellogenesis with cortical alveoli and yolk granules 

(yg). Scale bar 100 m. 

b 

The content of cortical alveoli will serve to harden the membrane (vitelline envelope) 

after ovulation and prevent polyspermy (Kitajima et al., 1994). Thus these structures, 

often called yolk vesicles, are not to be considered yolk in a strict sense as their contents 

do not contribute to the embryonic development (Wallace and Selman, 1981). The 

hepatically derived vitellogenin packed in granules during the true vitellogenesis (Table 

2, stage 4 and Figure 2b) is the only precursor of yolk proteins (Tyler, 1991). 

Furthermore, a number of studies (Burton, 1994; Rideout et al., 2000; Campbell et al., 

2006) have provided evidences that fish in cortical alveoli stage can arrest the 

development and remain reproductively inactive. Therefore the maturity scale presented 

in paper I aimed to emphasize the passage from the endogenous to the exogenous 

vitellogenesis as the threshold between immature and mature individuals. An individual 

showing oocytes with cortical alveoli but no yolk granules has to be considered 

maturing, but according to the above cited studies, this does not necessarily mean that it 

12

will be reproductive in the next spawning season. Only fish from the exogenous 

vitellogenic phase, under normal conditions, ought to be considered spawning within 

the current spawning season (Burton et al., 1997, Mackie and Lewis, 2001, I) and 

consequently included in the spawning stock biomass. 

Comparisons between the staging systems 

Some of the ovarian features cannot always be discriminated by the naked eye during 

certain phases of the developmental process. Therefore the consistency of this visual 

method has been increasingly distrusted (Saborido-Rey and Junquera, 1998; Kjesbu et 

al., 2003, II). While advanced stages (late vitellogenesis and spawning) are easily 

recognizable and therefore properly judged, the incongruence is encountered for 

individuals at the beginning of the developmental process. As stated above, the stage 2 

in Table 1 should include all the maturing individuals that will eventually spawn during 

the upcoming spawning season. However, a consistent part of specimens showing initial 

signs of structural modification are erroneously interpreted as maturing and included in 

this stage (I). Such a mistake obviously leads to an overestimation of the part of the 

population contributing to the stock reproductive potential. The comparison between the 

two staging systems (macroscopical and histological) in Kattegat cod shows in fact a 

consistent overestimation of the proportion of mature individuals for all age classes but 

the entity of the estimated bias decreases with increasing age. Consequently larger 

errors are made when judging first spawners (II). It is therefore obvious that the risk is 

amplified in stocks such as Kattegat cod, where the SSB is skewed towards younger and 

smaller individuals. 

A further problem encountered when using the macroscopical scale concerns the resting 

stage, which at the present state is not included in the adopted IBTS macroscopical scale 

(Table 1). It is important to remark that the term resting may represent a source of 

confusion because it is often used to refer both to the individuals immediately after the 

spawning (recovering) as well as to individuals that are omitting spawning (skippers). If 

the maturity status is observed before the spawning season, these confusions are 

avoided due to the unlikelihood to find fish in post-spawning condition. 

The spawning omission appears to be fairly common in cod and it has been estimated 

that around 30% of cod females tend to skip spawning (Walsh et al., 1986: Rideout et 

al., 2000; Jørgensen et al., 2006). This phenomenon may occur either by failing to start 

vitellogenesis (resting) or interrupting it (reabsorbing) or by concluding the process 

without egg release (retaining). The latter type may occur depending on the conditions 

encountered during the spawning season (overcrowding, mate availability, pollution) 

while the first two types (resting and readsorbing) have been often ascribed to low 

temperature (Woodhead and Woodhead 1965; Federov, 1971) or low condition due to 

scarcity of food (Burton and Idler, 1987; Rideout et al., 2000; Rideout et al., 2005) prior 

to the spawning season. 

The external appearance of the fish may be helpful for identifying females that retain 

eggs since overripe eggs and scarce intra-ovarian fluid shape the abdomen giving to it a 

berry-like aspect (Rideout et al., 2005). More difficult is instead the identification of 

13

females in resting and reabsorbing condition, due to their early stage of development. 

Gonads in these conditions may be easily confused with late immature or spent, and in 

the second case the estimation of the spawning stock would be affected. 

Histology is the most accurate way for identifying non-reproductive individuals, by 

detecting signs of previous spawning activity (POF) among oocytes in early maturation 

stage (Tomkiewicz et al., 2003a, Rideout et al., 2005, I). The wall thickness may also 

be used as criterion for identifying non reproductively active individuals, owing that 

immature individuals have thinner ovarian wall than the non-reproductive ones (Rideout 

et al., 2000). However, the presence of POF is the unquestionable sign of previous 

spawning activity. The occurrence of POFs in non-ripening fish at the time of the year 

when adult individuals should be ripening (e.g. in December-January in Kattegat cod) 

suggests that the fish has previously spawned but will not spawn in the upcoming 

season. The identification of non-reproductive females and their exclusion from the 

SSB is fundamental, especially for highly exploited stocks. Therefore the inclusion of 

the resting stage in maturity scales both macroscopical and histological (Tomkiewicz et 

al., 2003a, I) is crucial and when observed before the onset of spawning, this stage has 

to be considered as synonymous to a non-reproductive stage. 

The occurrence of the different stages and the reliability of the visual inspection are 

dependent on the time of sampling in relation to the spawning season. Therefore 

knowledge of the maturation chronology has to be ascertained accurately and on a stock 

specific level. 

The temporal ovarian development shows no differences in maturity schedules between 

cod from Kattegat and the Sound (I). In cod off Newfoundland, females show 

significant cellular changes more than 7 months before the spawning (Burton et al., 

1997) In the Kattegat and the Sound maturing females were found at the earliest in 

October (i.e. 4 months before the spawning peak), ripening continues until January, 

spawning peaks in February, and March marks the end of the spawning season (I). 

When comparing the microscopical and macroscopical staging systems, all age classes 

showed a convergence towards minimum bias in January, i.e. one month before the 

spawning peak (II) when the misjudgement is minimized due to the unmistakable 

advanced stage of the maturity process and to the unlikelihood to find fish in spent or 

post-spawning condition. Consequently, the reliability of visual judgement is dependent 

on the time of sampling. Accurate estimations of maturing fish some months before or 

just after the spawning season can only be assured by using microscopical 

investigations (Saborido-Rey and Junquera, 1998, Kjesbu et al., 2003, II). 

Data on individual maturity status for the estimations of the SSB in the Kattegat are 

annually collected during the surveys performed in February, which hence coincides 

with the spawning season. A recalculation of the historical female spawning biomass 

(FSB) for the period 1991-2004, applying the bias obtained from the comparison 

between the two staging methods, showed a consistent overestimation of the proportion 

of mature females. The re-estimated FSB was in fact always lower than the historical 

FSB, evidencing an overestimation ranging between 21 and 35% (II). Hence the 

histological evaluation of ovarian development has the clear advantage of allowing 

detailed recording of the maturation development occurring in the ovary. Such 

information gives the opportunity to obtain unambiguous interpretation of individual 

maturity status. Estimating the spawning fraction by the means of histological analyses 

14

is a robust way for obtaining accurate estimates of SSB. Maturity ogives based on 

macroscopical evaluation, determined during the spawning season, may instead lead to 

the inclusion of non-reproductive individuals in the SSB estimation. The resulting 

inflated SSB is prone to mislead the management with serious consequences for the 

stock. 

Potential energetic proxies of maturity status 

The use of histology in maturity studies has gained an increasing and unanimous 

approval as considered more consistent and reliable than macroscopical analysis (Murua 

et al., 2003; Tomkiewicz et al. 2003a, II). However it is an expensive and time 

consuming technique and it restricts the analyses to relative small samples. Furthermore 

the collection of ovaries for histological analyses on board of research vessels implies 

the handling of harmful substances, i.e. formaldehyde, necessary for the storage. 

Despite its attested reliability, histology is thus not routinely used and alternative 

indicators of maturity status, mainly linked to the energy resources, have been often 

sought. Substantial energy reserves are in fact required for the reproductive process of a 

fish and the energy expenditures related to reproduction can represent 10-22% of the 

annual energy budget (Jobling, 1982). 

In cod, the gonadal maturation, together with all the events associated with 

reproduction, is mainly promoted by energy gathered and stored during the feeding 

season rather than ingested during the reproduction. In concomitance with the cessation 

of feeding during pre-spawning and spawning periods (Kjesbu et al., 1991; Fordham 

and Trippel, 1999; Lambert and Dutil, 2000) female cod use the stored resources, in 

form of proteins in the muscle (Eliassen and Vahl, 1982) and fat (lipids) in the liver 

(Kjesbu et al., 1991), and transfer them to the gonads. Thus the seasonal variations in 

physiological condition related to reproduction and, in particular gonadosomatic index 

(GSI, ratio of gonad weight to the body weight), hepatosomatic index (HSI, ratio of 

liver weight to the body weight) and Fulton’s condition factor (ratio between fish 

weight and length cubed), have been monitored in different cod stocks (Schwalme and 

Chouinard, 1999; Lambert and Dutil, 1997a; Lambert and Dutil, 2000, Tomkiewicz et 

al., 2003a; I; IV). Seasonal pattern of nutrients storage and depletion may differ among 

cod living in different geographical areas and experiencing different environmental 

conditions, due to the stock–specific variability in feeding periodicity. Cod in 

Norwegian coastal fjords (Hop et al., 1992; Hop et al., 1993; Michalsen et al., 2008), in 

the North Sea and areas west of Scotland (Rae, 1967; Daan, 1973) continue to feed 

actively during winter (Hislop, 1997). 

For Kattegat cod, those indices show increasing trends until the spawning starts, when 

HSI and Fulton’s K values start to decrease again while GSI clearly declines when the 

spawning is concluded (IV; Figure 3). Similar trends in HSI and K have also been 

observed in Baltic cod (Tomkiewicz et al., 2003a). However, for some stocks the active 

consumption of stored resources may occur at an earlier time (Schwalme and 

Chouinard, 1999; Lambert and Dutil, 2000 and references therein; Mello and Rose, 

2005 a and b) possibly due to food-limitations (Jangaard et al., 1967; Hawkins et al., 

1985). 

15

16 

55 

GSI (%) 

12 

8 

233 

25 

4 

0 

7 

41 115 

6 

Oct 

Nov 

Dec 

Jan 

Feb 

Mar 

5 

HSI (%) 

4 

3 

2 

Fulton's K (100*g/cm 3 ) 

1.15 

1.10 

1.05 

1.00 

0.95 

Oct 

Nov 

Dec 

Jan 

Feb 

Mar 

Oct 

Nov 

Dec 

Jan 

Feb 

Mar 

Figure 3: Monthly trends of bioenergetic indices in Kattegat cod from the period 2002- 

2006 (merged years). The sample size is indicated only in the first diagram. Bars 

represent standard errors. 

In paper II a regression tree-model approach was used for testing different variables, as 

predictors of the maturity status in Kattegat cod. In analogy with stepwise procedure, 

only variables that significantly contribute to explain the variance are kept in the final 

model, and accordingly to the parsimony principle, the model are simplified without 

compromising the goodness of fit. Results showed that the best model with the lowest 

misclassification rate includes only GSI (which represents the main discriminating 

factor) and HSI, making these variables useful for tracking the ongoing maturation 

process. Conversely, total length and Fulton’s condition factor were poor predictors and 

their use increased the misclassification rate of the model. HSI is thus a more accurate 

measure of fish condition in cod than Fulton’s condition factor due to the storage of 

energy in the liver (Lambert and Dutil, 1997b; Marshall, 1999). 

The proved ability of GSI to reflect the reproductive status is also confirmed in other 

16

studies on cod (Burton, 1999; Dahle et al., 2003; Tomkiewicz et al., 2003a) as well as 

on riverine fishes (Brewer et al., 2008). Due to the use of liver reserves for producing 

vitellogenin, it is not surprising that there is a relationship between liver condition and 

maturity (II). Seasonal changes in liver size have been studied in Atlantic cod (Eliassen 

and Vahl, 1982; Lambert and Dutil, 1997b; Schwalme and Chouinard, 1999; Hansen et 

al., 2001) and a positive effect of liver condition on the probability of spawning has 

been demonstrated (Ajiad et al., 1999; Bromley et al., 2000; Morgan, 2004; Morgan 

and Lilly, 2006). Additionally fat content in the liver has been related to the progress of 

spawning in female cod (Kjesbu et al., 1991). These findings support the idea of the 

utility of using HSI in maturity status identification. However, the substantial variation 

in HSI observed in Baltic cod, probably due to a longer spawning season and therefore 

higher variation between individual fish compared to the cod in Kattegat (I), rendered it 

of a little use for maturity status prediction in this stock (Tomkiewicz et al., 2003a). 

The condition of the fish, or the quantity of energy stores, may significantly influence 

the reproductive investment in cod (Kjesbu et al., 1991; Chambers and Waiwood, 1996; 

Marshall et al., 1999; Lambert and Dutil, 2000; Ouellet et al., 2001). Reduced fecundity 

(Kjesbu et al., 1991; Marteinsdottir and Steinarsson, 1998; Marshall et al., 1998) or 

even skipped spawning (Burton and Idler, 1987; Rideout et al., 2000) have been 

increasingly associated to low conditioned fish. However, the use of bioenergetic index 

might not be useful for identifying individuals skipping maturity, or more specifically 

individuals in reabsorbing phase, due to the weight of the atretic oocytes (Rideout et al., 

2005) that would nonetheless lead to an increased gonadal weight although in absence 

of reproduction. 

While histology is a more reliable technique than physiological indices, the amount of 

time and the economical cost required may diminish its practical advantage and limit its 

use. The employ of GSI and HSI, once validated, may be incorporated with other 

information, such as minimum length at maturity or macroscopical judgement for 

improving the discrimination between mature and immature individuals (Burton, 1999; 

Rideout et al., 2005). Hence, considering the modest effort required for the collection of 

liver and gonad weight, the recording of those additional parameters should be easily 

included in the routine research sampling procedures for supporting the macroscopical 

maturity judgement when histological analyses cannot be carried out. 

FECUNDITY 

Stock assessment models have been traditionally based on the assumption that SSB 

adequately represented the stock reproductive potential This assumption underlies 

constancy over time of the SSB and of the stock relative fecundity (number of eggs 

produced per unity mass), intuitively hard to be valid. 

Following the decline in stock size and recruitment level experienced by most of the 

commercially exploited fish stocks, several researches have addressed the question of 

how changes in population size affect stock-specific reproductive traits. During the past 

decades an increasing number of studies have evidenced that SSB is not an accurate 

measure of reproductive potential (Jørgensen, 1990; Kjesbu et al., 1991; MacKenzie et 

17

al., 1998; Trippel, 1999; Kraus et al., 2002; Marshall et al., 2003; Köster et al., 2003; 

Marshall et al., 2006), hence the importance of incorporating reproductive biology in 

stock assessment gained credit. 

The alternative concept of stock reproductive potential (SRP) was therefore introduced. 

SRP represents the annual variation in stock’s ability to produce viable eggs and larvae 

that may eventually recruit to the adult population or fishery (Marshall et al., 1998;; 

Trippel, 1999; Murawski et al., 2001). 

Fundamental parameters affecting SRP such as proportion of mature at age, fecundity 

and offspring size and viability (fertilization and hatching success) have shown to vary 

with parental age, size, condition and spawning experience (Jørgensen 1990; Kjesbu et 

al., 1991; Solemdal et al., 1995; Marshall et al., 1998; Trippel, 1998). 

In North Atlantic cod stocks the severe decline in abundance has been accompanied by 

substantial reductions in age and size at first sexual maturation (Trippel et al., 1997) and 

a disproportionate loss of larger, older repeat-spawner (Trippel, 1995) have occurred. 

Laboratory experiments on cod demonstrated that first-time spawners have a lower 

reproductive success, breeding for a shorter time and producing fewer and smaller eggs 

with lower fertilization and hatchings rates (Solemdal et al., 1995; Trippel, 1998; 

Tomkiewicz et al., 2003b). Furthermore, in multiple spawning fishes, older individuals 

are likely to produce more batches, within the spawning season, over a longer period 

than younger ones (Parrish et al., 1986; Lambert, 1990). In addition, the fertilization 

rate is higher when bigger males are involved in the spawning act (Hutchings et al., 

1999). Therefore alterations in the size composition of the breeding stock may 

conceivably lead to changes in stocks’ reproductive success. 

Fecundity estimates do not give information on offspring viability but provides the 

starting number of potential offspring that can be produced. Fecundity data are therefore 

essential for assessing an individual’s reproductive potential and consequently 

providing more reliable estimate of stock recruitment rather than using spawner 

biomass. 

Cod, as most of the marine teleosts, produce a large number of small eggs. The 

estimation of the realized fecundity, i.e. the total number of egg actually spawned, in 

wild fishes is not an easy task. Some studies have estimated realized fecundity by 

collecting released eggs from captive fishes reared in tanks (Kjesbu et al., 1991; Trippel 

et al., 1998; Fordham and Trippel, 1999; Thorsen et al., 2003), while other studies 

counted the number of developing oocytes, and subsequently subtracting the number of 

atretic oocytes (Green Walker et al., 1994, Ma et al., 1998; Witthames et al., 2003). 

However the latter method needs accurate information on the persistence of the atretic 

stage (Murua et al., 2003) and additionally atresia is not routinely examined. 

Consequently many studies have concentrated on measurements of potential (i.e. the 

number of vitellogenic oocytes in the prespawning ovary) or relative (i.e. the number of 

eggs per unity body mass) fecundity and on the ability of biological and/or 

environmental factors in explaining their fluctuations. 

Relationships between fecundity and female age and/or size have been documented in 

many cod populations (Kjesbu et al., 1998, Marshall et al., 1998; Marteinsdottir et al., 

2000, Kraus et al., 2000; Kraus et al., 2002; Marteinsdottir and Begg, 2002; McIntyre 

and Hutchings, 2003; Yoneda and Wright, 2004; III). Both fish length and weight are 

significantly correlated with fecundity in cod, although fish length has been usually 

18

preferred as predictor given the weight large fluctuation during a year cycle (Blanchard 

et al., 2003; Thorsen et al., 2006). The strength of this relationship varies considerably 

between populations (Marteinsdottir and Begg, 2002; McIntyre and Hutchings, 2003), 

geographical areas and years (Lambert et al., 2005), and it becomes weaker when large 

fish are not included in the sample (Kjesbu et al., 1998). 

Also in the Kattegat cod, potential fecundity is tightly linked to the fish size but length 

showed to have a higher predictive power than weight (III). SSB, currently used as 

reproductive potential predictor in stock assessment models, fails to accurately account 

for the effect that variation in length composition has on the stock reproductive success. 

The risk is the overestimation of the reproductive potential when the stock is dominated 

by small individuals (Marshall et al., 2006) as in the case of the Kattegat cod stock. 

This stresses the importance of a continuous monitoring of fecundity on a stock-specific 

level. Despite this awareness and the implementation of easy manageable instruments 

for direct fecundity measurements (Thorsen and Kjesbu, 2001; Friedland et al., 2005; 

Klibansky and Juanes, 2007), this kind of data is still not collected on a routine basis 

(Tomkiewicz et al., 2003b). 

Environmental conditions and nutritional status are known to potentially have strong 

modifying effects on fecundity. Fish condition (Fulton’s K) and also liver index in fish 

like cod that primarily store energy (lipids) in the liver, are considered reliable proxies 

for the effect of environmental change on individual energy content and reproductive 

potential (Kjesbu et al., 1998; Marshall et al., 1999; Lambert and Dutil, 2000). 

Therefore several studies have been investigating both indices reflecting maternal 

energy supply as help to predict fecundity variation (Kjesbu et al., 1991; Marshall et al., 

1998; Lambert et al., 2003; III). Some studies have shown that yearly averages of lipid 

energy (Marshall et al., 1999) or food availability (Kraus et al., 2002) can significantly 

improve predictions of fecundity and egg production. However when the fish condition 

and egg production were measured on the same fish, i.e. just before the spawning 

season, the correlation between them was weak, although significant (Kjesbu et al., 

1998; Kraus et al., 2000; Marteinsdottir and Begg, 2002; Blanchard et al., 2003; III). In 

other words condition measured just prior to the start of the spawning season does not 

increase consistently the predictive power provided by the size alone. These results 

confirm the existence of a threshold in maturation process where the energy stored can 

be representatively used as a measure of egg production (Koops et al., 2004; Skjæraasen 

et al., 2006). 

In fecundity studies, the timing in relation to the maturation cycle is extremely 

important. A too early sampling may lead to biased estimations with loss of oocytes not 

yet recruited to the final stock. On the other hand, sampling too late may lead to the loss 

of oocytes, as they may have already been released. Late vitellogenesis represents the 

optimal phase for studying fecundity, minimizing both sources of error. To detect a 

biologically meaningful influence of maternal condition on egg production, condition 

should instead be quantified at an earlier stage of the maturation process, when energy 

is initially allocated to egg production (Koops et al., 2004; Skjæraasen et al., 2006; III). 

This threshold may be represented by the passage from endogenous to exogenous 

vitellogenesis during which the lipids stored in the liver are used to build up the yolk 

reserves in the developing oocytes (I). During this critical time, depending on the 

individual energetic status, investment in sexual maturation could still be reduced or 

19

skipped (Skjæraasen et al., 2006). Hence at a later stage, just before the spawning starts, 

fish size explains the largest part of fecundity variability (III), while fish condition may 

have a stronger effect in determining recruitment through other mechanisms, such as 

mate competition, spawning duration, size and number of batches and post-reproductive 

survival. 

Beyond parental influences, variability in egg size and number can also result from 

adaptations to different local environment. According to life history theory, the optimal 

trade-off between egg size and number depends on the condition experienced by the 

offspring (Parker and Begon, 1986) and the quality of the habitat into which offspring 

will emerge may act as a selective force. In cod, comparative studies have in fact 

evidenced a decreased size-specific fecundity (Pörtner et al., 2001) with increasing 

latitude and decreasing temperature (Koops et al., 2003). 

In paper III potential and relative fecundity are compared between Kattegat cod and 

Northeast Arctic cod (NEAC) from the main spawning area in Lofoten, caught during 

the pre-spawning season. Cod in Kattegat show a higher size-specific potential and 

relative fecundity in addition to a better pre-spawning condition. However, the size of 

vitellogenic oocytes, which has been shown to represent about 40% of the final egg size 

in cod (Tyler and Sumpter, 1996), is smaller in specimens belonging to Kattegat stock. 

The large variability in size-specific fecundity observed between cod stocks (Lambert et 

al., 2003; Lambert et al., 2005) can be the result of short-term response related to the 

nutritional status of the fish, food availability, growth and/or environmental temperature 

(Lambert et al., 2003). Differences in fecundity might also be associated with different 

life history responses between populations, resulting in different age/size at maturity, 

reproductive effort, egg size and survival (Roff, 2002). 

However, caution is needed when comparing fecundity data from geographically 

separated stocks due to differences in timing of spawning peaks, which may lead to 

biased results. The stock of vitellogenic oocytes is reduced as the fish approach 

spawning and consequently fish in early maturation may have considerable larger 

standing stock of vitellogenic oocytes than fish just prior to spawning (Thorsen et al., 

2006). In this case the oocyte diameter of the sampled Kattegat cod was smaller than 

found for the NEAC. This difference in oocyte size may reflect that the sampled NEAC 

was closer to spawning than the Kattegat cod. The difference in observed fecundity 

between the two stocks may therefore to some degree have been influenced by this 

difference in timing. 

On the other hand, it cannot be ignored that among the effect of the overexploitation an 

increased fecundity is often acknowledged (Lambert et al., 2005; Kjesbu et al., 2007), 

either as a density dependent effect following a release in resources competition (i.e. 

phenotypic plasticity) or as a selective pressure to maximize reproductive output at an 

earlier age. Northeast Arctic cod can be considered a relatively healthy stock, highly 

productive and exposed to much less fishing mortality (Ottersen et al., 2006), while 

Kattegat cod is suffering a very high fishing pressure and is presently at its lowest 

historical level (ICES, 2007). The observed difference may therefore mirror the 

different exploitation pattern experienced by the two stocks. 

A possible shift towards earlier maturation has previously been evidenced in Kattegat 

female cod when compared to the cod in the Sound (I). Those two subpopulations have 

shown marked differences in size structure and abundance (Svedäng et al., 2003; 

20

Svedäng et al., 2004) likely due to differences in technical regulations, whereas no 

genetic differences have hitherto been substantiated. Nevertheless the proportion of 

mature individuals per age class showed to be significantly higher in Kattegat cod, 

implying an earlier maturation or higher maturation rate. Moreover, in the period 1990- 

2006, L50 (length at which 50% of the population is mature) has decreased in the 

Kattegat but not in the Sound, although growth (length-at-age) seems not to differ 

between the two areas (Svedäng and Vitale, in preparation). These observations seem to 

be in contradiction with the expectation that the low cod density in Kattegat should 

decrease intra-specific feeding competition, improving growth (Rindorf et al., 2008). 

However, these results may suggest that Kattegat cod utilize surplus energy for 

reproduction rather than investing in growth. Hence an increase in fecundity, reflected 

in the production of smaller and lower quality eggs, may have occurred in the Kattegat 

as an effect of the exploitation rate. These outcomes raise therefore concerns about the 

reliability of SSB estimations used for the management of Kattegat cod. 

Hence as a consequence of overestimations in SSB due to erroneous maturity 

judgement (II) and possibly as a consequence of overlooked differences in reproductive 

output caused by a changed population structure, the resiliency of Kattegat cod stock 

might have been highly overrated and the actual situation of this stock may be much 

worse than presently believed. 

SPAWNING AGGREGATIONS 

Many of the world’s economically important fish species have evolved migratory life 

histories, showing ontogenetic (between nursery areas and adult populations) and 

seasonal (between spawning and feeding areas) shifts in distribution (Harden Jones, 

1968; Metcalfe et al., 2002). Similarly, cod undertake long seasonal migrations to 

specific locations forming large short-lived spawning aggregations (Brander, 1975; 

Brander, 1994; Rose, 1993; Robinchaud and Rose, 2001). Annual movements to 

spawning grounds have been largely described in cod (Templeman, 1974; Bergstad et 

al., 1987; Rose, 1993; Bagge et al., 1994; Lawson and Rose, 2000) and a consistent 

number of genetic, acoustic and tagging studies have evidenced that cod may regularly 

home to the same spawning ground over long distances year after year, following 

familiar migratory pathways (Godø, 1984; Green and Wrobleski, 2000; Robinchaud and 

Rose, 2001; Windle and Rose, 2005; Svedäng et al., 2007). 

Cod populations exhibit a variety of migratory behaviours which have been recently 

categorized by Robichaud and Rose (2004) according to degree of migration and 

philopatry in four groups: (1)“sedentary resident” exhibiting strong year-around site 

fidelity, (2) “accurate homers” returning to spawn in a specific area, (3) “inaccurate 

homers” returning to spawn in a much broader area near the original site in subsequent 

years and (4) “disperser” presenting a random spawning migration pattern within a large 

area. Interestingly this study showed that the most common strategy among the North 

Atlantic cod populations is to be sedentary. 

According to a recent tagging study (Svedäng et al., 2007) also the cod stock in the 

Kattegat has to be included in the first category, showing a high degree of resident 

behaviour. Although relying on small scale migratory movements, Kattegat cod seems 

to have a strong tendency to home to the same location for reproductive purposes 

21

annually. In paper IV, the stability of the Kattegat cod spawning aggregations has been 

investigated combining fishery dependent and independent surveys and evidencing that 

cod has been aggregating and spawning in specific areas for more than 25 years, albeit 

in drastically reduced numbers. 

The analyses of data relative to the period 1996-2004 (IV) evidenced two important 

spawning areas in the southern part of Kattegat, one close to the entrance to the Sound 

and one off the coast of Falkenberg, confirming previous studies for the period 1981- 

1990 (Pihl and Ulmestrand, 1988; Hagström et al., 1990) and 1975-1999 (Svedäng and 

Bardon, 2003, Figure 4). 

Neighbouring areas, i.e. the bights of Skälderviken and Laholmsbukten, formerly 

depicted as important spawning areas, did not show any sign of spawning activity 

during the studied period, confirming the findings from Svedäng and Bardon (2003) 

who reported the disappearance of spawning aggregations from those two areas after 

1990. Whether these results reflect a contraction in spatial distribution or a loss in 

spawning areas is hard to verify due to the lack of spatial delineation of previous 

investigations. Additionally a loss of spawning areas seemingly occurred in the northern 

part of the Kattegat, i.e. the bay of Kungsbackafjorden and north of Lasö, where 

Hagberg (2005) had identified large spawning aggregations. Only weak signals of 

spawning activities in these areas were obtained in this study (IV). 

Figure 4: Study area. Dashed lines represent the 20m depth contour 

22

The estimations of spawners’ abundance obtained from the Swedish IBTS surveys in 

combination with log-book data from the Swedish cod fishery have therefore shown to 

be a useful tool for detecting spawning areas, providing persistent and precise 

geographical signals. In order to validate these findings, independent samplings of 

individual physiological status were carried out in the depicted spawning and nonspawning 

areas. 

The liver index (HSI) has been shown to be an unreliable measure of eggs production 

for individuals in pre-spawning condition (III) while it represents, together with the GSI 

(Tomkiewicz et al., 2003a) an accurate tool for tracking the ongoing maturation process 

(Morgan and Lilly, 2006; I). The monthly trends in those indices did not show any 

significant difference between the assumed spawning and non spawning areas in 

November and December, which may highlight that individuals start to aggregate 

approximately one month before the spawning season. From January and onwards 

individual GSI and HSI values were clearly higher in the assumed spawning areas, 

evidencing an ongoing maturation process. The energetic pattern together with the 

significant higher proportion of mature females, recognized by accurate ovarian 

histological inspection, allowed the precise localization of cod spawning segregation. 

Investigations of spawning aggregations and their persistence over time are relevant for 

understanding the stock structure and consequently the dynamic of the studied 

population. In case of commercially exploited fish species, the derived increased 

catchability and vulnerability due to the predictable spatial and temporal associations, 

makes this knowledge a concern of fishery science. The highest catch rates in many 

commercial fisheries are in fact achieved by mobile fleets targeting spawning 

aggregations (Beverton, 1990; Hilborn and Walters, 1992; Hutchings, 1996). The 

achieved detection of spawning aggregations by the use of commercial landings (IV) 

clearly confirms that those spatial and temporal aggregations represent a cost-effective 

way to obtain profits. 

The effects of fishing activity in areas where cod spawning takes place at a known time 

are multifaceted. Beyond the well known consequences of a size selective fishing 

mortality on the stock structure (Jennings et al, 2001), derived from the removal of 

larger and more fecund (Solemdal et al., 1995; Trippel, 1998; Tomkiewicz et al., 

2003b) individuals from the population, the complex repertoire of cod reproductive 

behaviours is also strongly impacted. 

A successful reproduction in cod involves complex mating interactions, including 

behavioural and acoustic displays by males and mate choice by females (Brawn, 1961a 

and b; Engen and Folstad, 1999; Hutchings et al., 1999; Nordeide and Foldstad, 2000; 

Rowe and Hutchings, 2003; Rowe and Hutchings, 2004). The release of gametes is 

preceded by a sort of ritual “dance”. A final close physical contact (i.e. ventral mount) 

between the mating pair ensures a synchronized release of eggs and sperms. 

Reproductive physiology in fish is adversely affected by stress, as for instance the 

passage of the trawl, causing alterations in reproductive hormones levels, fecundity 

(Billard et al., 1981; Campbell et al., 1994), eggs’ quality (Kjesbu et al., 1990) and 

courtship performances, likely disturbing spawning synchronization and eventually 

decreasing the fertilization rate (Morgan et al., 1997). The production of abnormal 

larvae has also been observed as one of the effect following a stress (Morgan et al., 

23

1999). Furthermore some studies (Morgan and Trippel, 1996; Lawson and Rose, 2000) 

suggested that males may arrive at the spawning ground first and that females would 

periodically move onto the grounds to release eggs. The different residence time and 

activity on the spawning grounds by males and females lead to an unequal distribution 

and therefore sex ratio on the spawning areas (Robichaud and Rose, 2003) and 

eventually to a possible differentiated fishing pressure on sexes. Altogether, the stock 

reproductive potential is both directly and indirectly seriously threatened by the 

exploitation of spawning grounds. 

Hence in light of the depleted state of most of the cod populations and the consequent 

decreased spawning biomass, information on the spatial distribution of the spawning 

aggregations are not only crucial for elucidating stocks’ structure but represent an useful 

tool for stock management. A successful management of overexploited stocks, as 

Kattegat cod, requires an accurate knowledge of location and timing of the spawning 

activity in order to minimize disturbances and excessive fishing mortality and ensuring 

successful reproduction, vital for rebuilding stocks to sustainable levels. 

CONCLUSIONS AND IMPLICATIONS FOR MANAGEMENT 

The drastic decline for more than three decades faced by the cod stock in Kattegat is 

now undeniable. Although environmental variability is acknowledged among those 

factors that can play an important role in shaping stocks’ dynamics, in the case of 

Kattegat cod, overfishing still remains the main cause of the present severe depletion 

(Cardinale and Svedäng, 2004; ICES, 2007). 

The objectives of fishery management are many-sided, embracing biological, economic, 

social and political aspects (Jennings et al., 2001). One of the main biological goals of a 

management scheme is to promote the recovery of overexploited stocks. This is 

basically achieved by allowing the stock to produce enough offspring for replacing the 

adult removal due to fishing activity. The implementation of increasingly restrictive 

TACs, accordingly to the declining abundance, has had as a main result a decreasing 

catch data quality (ICES, 2007). Discarding of marketable fish (high-grading) in the cod 

fishery and of undersized fish in the Nephrops fishery, together with misreporting, most 

likely contributed to an increased uncontrolled fishing mortality (ICES, 2007), showing 

that the present management plan is not effective in regulating catches. The last three 

years assessment of this stock has in fact been unable to estimate fishing mortality due 

to the uncertainty in catch data. 

The situation of Kattegat cod could be more alarming, if possible, than what is generally 

believed. The use of erroneous methodologies (I) for calculating the proportion of 

mature individuals in the population has led to a consistent overrating of the abundance 

of females that actually contributed to the reproductive potential for more than 20 years 

(II). Additionally, SSB, which is considered at an historical low level and far below the 

safe limit, is at present compressed to a few age classes (2-5 years) and mainly relying 

on first-spawners (Hutchings and Myers, 1993; Caddy and Agnew, 2003), which in turn 

result in a lower quantitative and qualitative reproductive output (Solemdal et al., 1995; 

Trippel, 1998; Tomkiewicz et al., 2003b). The increasing evidence that SSB is not 

equivalent in terms of egg production (Jørgensen, 1990; Kjesbu et al., 1991; MacKenzie 

24

et al., 1998; Trippel, 1999; Marshall et al., 2003: Kraus et al., 2002; Köster et al., 2003; 

Marshall et al., 2006) due to the influence that spawners’ size and condition have on 

recruitment success, has most likely been overlooked in the assessment analyses. 

Taken together, the overestimation of the stock reproductive potential may have led to 

the implementation of regulating measures far above the stock capacity, neglecting 

potential risks. The false perception of the stock status has probably masked the need of 

a more drastic catch control and this may partly explain the absence of any sign of 

recovery. 

Consequently a revision of Kattegat cod stock assessment models and a re-evaluation of 

the reference points, based on increased stock-specific biological knowledge, is strongly 

suggested. The use of more accurate methods, such as histological or bioenergetics 

analyses, for estimating the individual maturity status might integrate and reinforce the 

routinely used methodology during research surveys, at least in those cases when there 

are uncertainties. The observed stock fecundity-length relationship (III) can be used to 

scale estimates of spawner abundance to population egg production (Murua et al, 2003) 

and greatly assist the attainment of an improved assessment, although a monitoring 

program based on direct measurements of stock fecundity, and factors influencing it, 

ought to be implemented. 

Furthermore, the acquired knowledge on the persistence of the spawning aggregations 

(IV) may facilitate the implementation of a more controlled fishing activity during the 

spawning season. Since the year 2002 scientists have been advocating a total closure of 

the fishery in Kattegat area, yet remained unheard. Stocks that remain resident within a 

limited geographic area may be more prone to local extinction but may also be protected 

in a more efficient way by closing specific area to fishing (Polunin, 2002). The 

introduction of no-takes area has an obvious clear effect on species abundance. 

However the results may be comparable to year-around gear restriction, as shown by the 

remarkable effects that the trawling ban, applied since 1932, has had in the Sound. A 

total fishing ban on a limited temporal and spatial scale, as represented by spawning 

closures is also an effective way for protecting a stock. However such a restriction may 

be less successful and not lead to a decrease in total fishing mortality if it only results in 

an increase of the fishing effort in adjacent areas or shifted in time, as occurred in the 

Baltic Sea (Bergström et al., 2007). In the Kattegat as well, the closure during the first 

quarter of year of the bights of Skälderviken and Laholmsbukten from 2003 did not 

produce encouraging results (Bergström et al., 2007), which could be due to the fact 

that the subpopulations in these two areas have yet to recover (IV). Furthermore the 

closure of such a small portion of the area might not be sufficient for enhancing a 

recovery. On the whole, the present management scheme in the Kattegat is mainly 

aimed to improve juvenile survival through supplementary mesh size increase or 

minimum landing size, resulting in an increased pressure on the few remaining large 

spawners. Restoring age structure and SSB, based on temporal and spatial limitation of 

the fishing effort, should instead be opted for, as an appropriate recovery approach in a 

long-term perspective, auxiliary to conventional controls on exploitation rate and 

technical measures. However the management of exploited fish stock is not only an 

ecological but also an economic and social issue of great magnitude. Therefore the 

implementation of drastic regulative measures has to follow a unanimous consensus 

apparently difficult to achieve. 

25

REFERENCES 

Ajiad, A., Jakobsen, T. and Nakken, O., 1999. Sexual differences in maturation of 

northeast Arctic cod. Journal of Northwest Atlantic Fishery Science, 25: 1-15 

Bagge, O., Thurow, F., Steffensen, E. and Jesper, B., 1994. The Baltic cod. Dana, 10: 1- 

28 

Bergstad, O.A., Jorgensen, T. and Dragesund, O., 1987. Life history and ecology of the 

gadoids resources of the Barents Sea. Fisheries Research, 5: 119-161 

Bergström, U., Ask, L., Degerman, E., Svedäng, H., Svenson, A and Ulmestrand, M. 

2007. Effekter av fredningsområden på fisk och kräftdjur i svenska vatten (Effect 

of fishery closures on fishes and crustaceans in Swedish waters. Swedish Board of 

Fisheries Finfo 2007:2; 36 pp. In Swedish with English summary. Available at 

www.fiskeriverket.se 

Beverton, R.J.H., 1990. Small marine pelagic fish and the threat of fishing: are they 

endangered? Journal of Fish Biology, 37 (Supplement A): 5-16 

Billard, R., Bry, C. and Gillet, C., 1981. Stress, environment and reproduction in teleost 

fish. In Stress and Fish (Pickering, A.D., ed.): 185-208. Academic Press, London, 

UK 

Blanchard, J.L., Frank, K.T. and Simon, J.E., 2003. Effect of condition on fecundity and 

total egg production of eastern Scotian Shelf haddock (Melanogrammus 

aeglefinus). Canadian Journal of Fisheries and Aquatic Science, 60: 321-332 

Brander, K.M., 1975. The population dynamic and biology of cod (Gadus morhua L.) in 

the Irish Sea. Ph.D. Thesis. Fisheries Laboratory, Lowestoft, UK 

Brander, K., 1994. Spawning and life history information for North Atlantic cod stocks. 

ICES Cooperative Research Report No. 205: 150pp 

Brawn, V.M., 1961 a. Reproductive behaviour of the cod (Gadus callarias L.). 

Behaviour, 18: 177-198 

Brawn, V.M., 1961 b. Sound production by the cod (Gadus callarias L.). Behaviour 18: 

239-255 

Brewer, S.K., Rabeni, C.F. and Papoulias, D.M., 2008. Comparing histology and 

gonadosomatic index for determining spawning condition of small-bodied riverine 

fishes. Ecology of Freshwater Fish, 17: 54-58 

Bromley, P.J., Ravier, C. and Witthames, P.R., 2000. The influence of feeding regime 

on sexual maturation, fecundity and atresia in first-time spawning turbot. Journal 

of Fish Biology, 56: 264-278 

26

Burton, M.P.M and Idler, D.R., 1987. An experimental investigation on the nonreproductive, 

post-mature state in winter flounder. Journal of Fish Biology, 30: 

643-650 

Burton, M.P.M., 1994. A critical period for nutritional control of early gametogenesis 

in female winter flounder Pleuronectes americanus (Pisces, Teleostei). Journal of 

Zoology, 33: 405-415 

Burton, M.P.M., Penney, R.M., and Biddiscombe, S., 1997. Time course of 

gametogenesis in Northwest Atlantic cod (Gadus morhua). Canadian Journal of 

Fisheries and Aquatic Science, 54 (Supplement 1): 122-131 

Burton, M.P.M., 1999. Notes on Potential Errors in Estimating Spawning Stock 

Biomass: Determining the Effects of Non-participatory Adults for Some 

Groundfish Species. Journal of Northwest Atlantic Fishery Science, 25: 205-213 

Caddy, J.F. and Agnew, D., 2003. A summary of global stock recovery plans for 

marine organisms including indicative information on the time to recovery, and 

associated regime changes that may effect recruitment and recovery success. 

International Council for the Exploration of the Sea, ICES CM 2003/U:08 

Campbell, P.M., Pottinger, T.G. and Sumpter, J.P., 1994. Preliminary evidence that 

chronic confinement stress reduces the quality of gametes produced by brown and 

rainbow trout. Aquaculture, 120: 151-169 

Campbell, B., Dickey, J., Beckman, B., Young, G., Pierce, A., Fukada, H. and Swanson, 

P., 2006. Previtellogenic oocyte growth in salmon: relationships among body 

growth, plasma insulin-like growth factor-1, estradiol-17beta, follicle-stimulating 

hormone and expression of ovarian genes for insulin-like growth factors, 

steroidogenic-acute regulatory protein and receptors for gonadotropins, growth 

hormone, and somatolactin1. Biology of Reproduction, 75:34-44 

Cardinale, M. and Svedäng, H., 2004. Modelling recruitment and abundance of Atlantic 

cod, Gadus morhua, in the Kattegat-Eastern Skagerrak (North Sea): evidence of 

severe depletion due to a prolonged period of high fishing pressure. Fisheries 

Research, 69 (2): 263-282 

Chambers, R.C. and Waiwood, K.G., 1996. Maternal and seasonal differences in egg 

sizes and spawning characteristics of captive Atlantic cod, Gadus morhua. 

Canadian Journal of Fisheries and Aquatic Science, 53: 1986-2003 

Cook, R.M., Sinclair, A. and Stefánsson, G., 1997. Potential collapse of North Sea cod 

stocks. Nature, 385: 521-522 

Daan, N., 1973. A quantitative analysis of the food intake of North Sea cod, Gadus 

morhua. Netherlands Journal of Sea Research, 6: 479–517 

27

Dahle, R., Taranger, G.L., Karlsen, Ø., Kjesbu, O.S. and Norberg, B., 2003. Gonadal 

development and associated changes in liver size and sexual steroids during the 

reproductive cycle of captive male and female Atlantic cod (Gadus morhua L.). 

Comparative Biochemistry and Physiology Part A, 136: 641-653 

Eliassen, J.E. and Vahl, O., 1982. Seasonal variations in biochemical composition and 

energy content of liver, gonad and muscle of mature and immature cod, Gadus 

morhua (L.) from Balsfjorden, northern Norway. Journal of Fish Biology, 20 (6): 

707-716 

Engen, F. and Folstad, I., 1999. Cod courtship song: a song at the expense of dance? 

Canadian Journal of Zoology, 77: 542-550 

Federov, K.Y., 1971. The state of the gonads of the Barents Sea Greenland halibut 

[Reinhardtius hippoglossoides (Walb.)] in connection with failure to spawn. 

Journal of Ichthyology, 11: 673-682 

Fordham, S.E. and Trippel, E.A., 1999. Feeding behaviour of cod (Gadus morhua) in 

relation to spawning. Journal of applied Ichthyology, 15: 1-9 

Friedland, K.D., Ama-Abasi, D., Manning, M, Clarke, L., Kligys, G. and Chambers, 

R.C., 2005. Automated egg counting and sizing from scanned images: rapid 

sample processing and large data volumes for fecundity estimates. Journal of Sea 

Research, 54: 307-316 

Green, J.M. and Wroblewski, J.S., 2000. Movement patterns of Atlantic cod in Gilbert 

Bay, Labrador: evidence for bay residency and spawning site fidelity. Journal of 

Marine Biological Association of the UK, 80: 1077-1085 

Green Walker, M., Witthames, P.R. and De Los Santos, I.B., 1994. Is the fecundity of 

the Atlantic mackerel (Scomber scombrus: Scombridae) determinate? Sarsia, 79: 

13-26 

Gødo, O.R., 1984. Migration, mingling and homing of north-east Arctic cod from two 

separated spawning grounds. In Reproduction and Recruitment of Arctic cod. 

(O.R. Gødo and S. Tilseth Eds). Institute of Marine Research, Bergen, Norway: 

289-302 

Hagberg, J., 2005. Utökad analys av historiska data för att säkerställa referensvärden för 

fisk (Improved analysis of historical data for ensuring fish reference points). 

Swedish Board of Fisheries, 22 pp. (in Swedish) 

Hagström, O., Larsson, P.O. and Ulmestrand, M., 1990. Swedish cod data from the 

international young fish surveys 1981-1990. International Council for the 

Exploration of the Sea, ICES CM 1990/G: 65 

28

Hansen, T; Karlsen, O; Taranger, G.L., Hemre, G.I., Holm, J.C. and Kjesbu, O.S., 2001. 

Growth, gonadal development and spawning time of Atlantic cod (Gadus morhua) 

reared under different photoperiods. Aquaculture, 203 (1-2): 51-67 

Harden Jones, F.R.,1968. Fish Migration. Edward Arnold, Ltd. London 

Hawkins, A.D., Soofiani, N.M. and Smith, G.W., 1985. Growth and feeding of juvenile 

cod (Gadus morhua L.). Journal du Conseil International pour l’Exploration de la 

Mer, 42: 11-32 

Helfman, G., Collette, B. and Facey, D., 1997. The Diversity of Fishes. Blackwell 

Science Inc., Massachusetts 

Hilborn, R. and Walters, C., 1992. Fisheries stock assessment. Chapman and Hall, New 

York 

Hislop, J., 1997. Database report of the stomach sampling project 1991. International 

Council for Exploration of the Sea, Cooperative Research Report No 419: 422 pp 

Holdway, D. A. and Beamish, F. W. H., 1985. The effect of growth rate, size, and 

season on oocyte development and maturity of Atlantic cod (Gadus morhua L.). 

Journal of Experimental Marine Biology and Ecology, 85: 3-19 

Hop, H., Gjøsaeter, J. and Danielssen, D.S., 1992. Seasonal feeding ecology of cod 

(Gadus morhua) on the Norwegian Skagerrak cost. ICES Journal of Marine 

Science, 49: 453-461 

Hop, H., Danielssen, D.S. and Gjøsaeter, J., 1993. Winter feeding ecology of cod 

(Gadus morhua) in a fjord of southern Norway. Journal of Fish Biology, 43: 1-18 

Hutchings, J. and Myers, R., 1993. Effect of age on the seasonality of maturation and 

spawning of Atlantic cod, Gadus morhua, in the Northwest Atlantic. Canadian 

Journal of Fisheries and Aquatic Science, 50: 2468-2474 

Hutchings, J. A., 1996. Spatial and temporal variation in the density of northern cod and 

a review of hypotheses for the stock’s collapse. Canadian Journal of Fisheries and 

Aquatic Science, 53: 943-962 

Hutchings, J.A., Bishop, T.D. and McGregor-Shaw C.R., 1999. Spawning behaviour of 

Atlantic cod, Gadus morhua: evidence of mate competition and mate choice in a 

broadcast spawner. Canadian Journal of Fisheries and Aquatic Science, 56: 97- 

104 

Hutchings, J.A., 2000. Collapse and recovery of marine fishes. Nature, 406: 882-885 

ICES, 1999. Manual for International Bottom Trawl Surveys. ICES CM1999/D2; 

Addendum 2 

29

ICES, 2007. Report of the Baltic fisheries assessment working group (WGBFAS). 

International Council for the Exploration of the Sea, CM 2007/ACFM: 15 

Jangaard, P.M., Brockerhoff, H., Burgher, R.D. and Hoyle, R.J., 1967. Seasonal 

changes in general condition and lipid content of cod from inshore waters. Journal 

of the Fisheries Research Board of Canada, 24: 607-612 

Janssen, P.A.H., Lambert, J.G.D. and Goos, H.J.T., 1995. The annual ovarian cycle and 

the influence of pollution on vitellogenesis in flounder, Pleuronectes flesus. 

Journal of Fish Biology, 47: 509-523 

Jennings, S, Kaiser, M.J. and Reynolds, J.D., 2001. Fishing effects on populations and 

communities. In Marine Fisheries Ecology. Blackwell Science Ltd, Oxford, UK 

Jobling, M., 1982. Food and growth relationships of the cod, Gadus morhua L., with 

special reference to Balsfjorden, north Norway. Journal of Fish Biology, 21: 357- 

372 

Jørgensen, T., 1990. Long-term changes in age at sexual maturity of northeast Arctic 

cod (Gadus morhua L.). Journal du Conseil International pour l’Exploration de la 

Mer, 46: 235-248 

Jørgensen, C., Ernande, B., Fiksen, Ø. and Dieckmann, U., 2006. The logic of skipped 

spawning in fish. Canadian Journal of Fisheries and Aquatic Science, 63: 200-211 

Kitajima, K., Inoue, S., Seko, A., Yu, S., Sato, C., Taguchi, T. and Inoue, Y., 1994. 

Unique structures and structural changes of the cortical alveolar-derived 

glycoproteins in fish eggs upon fertilization and during early development. Third 

International Advisory Committee of the International Marine Biotechnology 

Conference, Tromsø (Norway): 126 pp 

Kjesbu, O. S. and Kryvi, H., 1989. Ooogenesis in cod, Gadus morhua L., studied by 

light and electron microscopy. Journal of Fish Biology, 34: 735-746 

Kjesbu, O. S., Witthames, P. R., Solemdal, P. and Greer Walker, M., 1990. Ovulatory 

rhythm and a method to determine the stage of spawning in Atlantic Cod (Gadus 

morhua). Canadian Journal of Fisheries and Aquatic Science, 47: 1185-1193 

Kjesbu, O. S., Klungsoyr, J, Kryvi, H, Witthames, P. R. and Green Walker, M., 1991. 

Fecundity, atresia and egg size of captive Atlantic Cod (Gadus morhua) in relation 

to proximate body condition. Canadian Journal of Fisheries and Aquatic Science, 

48: 2333-1343 

Kjesbu, O.S., Witthames, P.J., Solemdal, P. and Green Walker, M., 1998. Temporal 

variation in fecundity of Arcto-Norwegian cod (Gadus morhua) in response to 

natural changes in food and temperature. Journal of Sea Research, 40: 303-321 

30

Kjesbu, O.S., Hunter, J.R., and Witthames, P.R., 2003. Report of the working group on 

modern methods to assess maturity and fecundity in warm-and cold-water fish and 

squids. Bergen, Havforskningsinstittuttet, Institute of Marine Research: 1- 140 

Kjesbu, O.S. and Witthames, P.R., 2007. Evolutionary strategies in flatfish and 

groundfish: Relevant concepts and methodological advancements. Journal of Sea 

Research, 58: 23-34 

Klibansky, N. and Juanes, F., 2008. Procedures for efficiently producing high quality 

fecundity data on a small budget. Fisheries Research, 89: 84-89 

Koops, M.A., Hutchings, J.A. and Adams, B.K., 2003. Environmental predictability and 

the cost of imperfect information: influences on offspring size variability. 

Evolutionary Ecology Research, 5: 29-42 

Koops, M.A., Hutchings, J.A. and McIntyre, T.M., 2004. Testing hypotheses about 

fecundity, body size and maternal condition in fishes. Fish and Fisheries, 5: 120- 

130 

Kraus, G., Müller, A., Trella, K. and Köster. F.W., 2000. Fecundity of Baltic cod: 

temporal and spatial variation. Journal of Fish Biology 56: 1327-1341 

Kraus, G., Tomkiewicz, J. and Köster. F.W., 2002. Egg production of Baltic cod in 

relation to variable sex ratio, maturity and fecundity. Canadian Journal of 

Fisheries and Aquatic Science, 59: 1908-1920 

Kurlansky, M., 1998. Cod: a biography of the fish that changed the world. Jonathan 

Cape, London, UK: 300 pp 

Köster. F.W., Hinrichsen, H.H., Schnack, D., St. John, M.A., MacKenzie, B.R., 

Tomkiewicz, J., Möllmann, C., Kraus, G., Plikshs, M., Makarchouk, A. and Aro, 

E., 2003. Recruitment of Baltic cod and sprat stocks: Identification of critical life 

stages and incorporation of environmental variability into stock recruitment 

relationships. Scientia Marina, 67 (Supplement 1): 129-154 

Lambert, T.C., 1990. The effect of population structure on recruitment in herring. 

Journal du Conseil International pour l’Exploration de la Mer , 47: 249-255 

Lambert, Y. and Dutil, J.D., 1997a. Condition and energy reserves of Atlantic cod 

(Gadus morhua) during the collapse of the Northern Gulf of St. Lawrence stock. 

Canadian Journal of Fisheries and Aquatic Science, 54: 2388-2400. 

Lambert, Y. and Dutil, J.D., 1997b. Can simple condition indices be used to monitor 

and quantify seasonal changes in the energy reserves of Atlantic cod (Gadus 

morhua)? Canadian Journal of Fisheries and Aquatic Science, 54 (Supplement 1): 

104-112 

31

Lambert, Y. and Dutil, J.D., 2000. Energetic consequences of reproduction in Atlantic 

cod (Gadus morhua) in relation to spawning level of somatic energy reserves. 

Canadian Journal of Fisheries and Aquatic Science, 57: 815-825 

Lambert, Y., Yaragina, N.A., Kraus, G., Marteinsdottir, G. and Wright, P., 2003. Using 

environmental and biological indices as proxies for egg and larval production of 

marine fish. Journal of Northwest Atlantic Fishery Science, 33: 115-159 

Lambert, Y., Kjesbu, O.S., Kraus, G., Marteinsdottir, G. and Thorsen, A., 2005. How 

variable is the fecundity within and between cod stocks? International Council for 

the Exploration of the Sea, ICES CM 2005/Q:13 

Lawson, G.L. and Rose, G.A., 2000. Seasonal distribution and movements of coastal 

cod (Gadus morhua L.) in Placentia Bay, Newfoundland. Fisheries Research, 49: 

61-75 

Ma , Y., Kjesbu, O.S. and Jørgensen, T., 1998. Effect of ration on the maturation and 

fecundity in captive Atlantic herring (Clupea harengus). Canadian Journal of 

Fisheries and Aquatic Science, 55: 900-908 

MacKenzie,B.R., Tomkiewicz, J., Köster, F and Nissling, A., 1998. Quantifying and 

disaggregating in spawning effect: incorporating stock structure, spatial 

distribution and female influence into estimates of annual population egg 

production. International Council for the Exploration of the Sea, ICES CM 

1998/BB: 11 

Mackie, M. and Lewis, P, 2001. Assessment of gonad staging systems and other 

methods used in the study of the reproductive biology of narrow-barred Spanish 

mackerel, Scomberomorus commerson, in Western Australia. Fisheries Research 

Report Western Australia, 136:1-32 

Marshall, C. T., Kjesbu, O. S., Yaragina, N. A., Solemdal, P. and Ulltang, O., 1998. Is 

spawner biomass a sensitive measure of the reproductive and recruitment potential 

of northeast Arctic cod? Canadian Journal of Fisheries and Aquatic Sciences, 55: 

1766-1783 

Marshall, C.T., Yaragina, N.A., Lambert, Y. and Kjesbu, O.S., 1999. Total lipid energy 

as a proxy for total egg production by fish stocks. Nature 402: 288-290. 

Marshall, C.T., O’Brien, L., Tomkiewicz, J., Marteinsdottir, G., Morgan, M.J., 

Saborido-Rey, F., Köster, F.W., Blanchard, J.L., Secor, D.H., Kraus, G., Wright, 

P.J., Mukhina, N.V. and Björnsson, H., 2003. Developing alternative indices of 

reproductive potential for use in fisheries management: case studies for stocks 

spanning an information gradient. Journal of Northwest Atlantic Fishery Science, 

33: 161-190 

32

Marshall, C.T., Needle, C.L., Thorsen, A., Kjesbu, O.S. and Yaragina, N.A., 2006. 

Systematic bias in estimates of reproductive potential of an Atlantic cod (Gadus 

morhua) stock: implications for stock recruit theory and management. Canadian 

Journal of Fisheries and Aquatic Sciences, 63: 980-994. 

Marteinsdottir, G. and Steinarsson, A., 1998. Maternal influence on the size and 

viability of Iceland cod Gadus morhua eggs and larvae. Journal of Fish Biology, 

52: 1241-1258 

Marteinsdottir, G., Gudmundsdottir, A, Thorsteinsdottir, V. and Stefánsson, G., 2000. 

Spatial variation in abundance, size composition and viable egg production of 

spawning cod (Gadus morhua L.) in Icelandic waters. ICES Journal of Marine 

Science, 57: 824-830 

Marteinsdottir, G. and Begg, G., 2002. Essential relationships incorporating the 

influence of age, size and condition on variables required for estimation of 

reproductive potential in Atlantic cod (Gadus morhua). Marine Ecology Progress 

Series, 235: 235-256 

McIntyre, T.M. and Hutchings, J.A., 2003. Small-scale temporal and spatial variation in 

Atlantic cod life history. Canadian Journal of Fisheries and Aquatic Sciences, 60: 

1111-1121 

Mello, L.G.S. and Rose, G.A., 2005 a. Seasonal cycles in weight and condition in 

Atlantic cod (Gadus morhua L.) in relation to fisheries. ICES Journal of Marine 

Science, 62: 1006-1015. 

Mello, L.G.S. and Rose, G.A., 2005 b. Seasonal variation in abundance and stock 

composition of Atlantic cod (Gadus morhua L.) in Placenta Bay, Newfoundland, 

in relation to fisheries. Fisheries Research, 74: 142-156 

Metcalfe, J.D., Arnild, G.P., and McDowall, P.W., 2002. Migration. In Handbook of 

Fish and Fisheries, Vol.1 (Hart, P.J.B. and Reynolds, J.D., eds.), pp175-199. 

Blackwell Publisher, Oxford, UK 

Michalsen, K., Johannesen, E. and Bogstad, B., 2008. Feeding of mature cod (Gadus 

morhua) on the spawning grounds in Lofoten. ICES Journal of Marine Science, 

65: 571-580 

Morgan, M.J. and Trippel, E.A., 1996. Skewed sex ratios in spawning shoals of Atlantic 

cod (Gadus morhua). ICES Journal of Marine Science, 53: 820-826 

Morgan, M.J., De Blois, E.M. and Rose, G.A., 1997. An observation on the reaction of 

Atlantic cod (Gadus morhua) in spawning shoal to bottom trawling. Canadian 

Journal of Fisheries and Aquatic Sciences, 54 (Supplement 1): 217-223 

33

Morgan, M.J., Wilson, C.E. and Crim, L.W., 1999. The effect of stress on reproduction 

in Atlantic cod. Journal of Fish Biology, 54: 477-488 

Morgan, M.J., 2004. The relationship between fish condition and the probability of 

being mature in American plaice (Hippoglossoides platessoides). ICES Journal of 

Marine Science, 61: 64-70 

Morgan, M.J. and Lilly, G.R., 2006. The impact of condition on reproduction in 

Flemish Cap cod. Journal of Northwest Atlantic Fishery Science, 37: 81-86 

Morrison, C.M., 1990. Histology of the Atlantic cod, Gadus morhua: an atlas. Part 

three. Reproductive tract. Canadian Special Publications of Fisheries and Aquatic 

Sciences 100 

Murawski, S. A., Rago, P. J., and Trippel, E. A., 2001. Impacts of demographic 

variation in spawning characteristics on reference points for fishery management. 

ICES Journal of Marine Science, 58: 1002-1014 

Murua, H. and Saborido-Rey, F., 2003. Female reproductive strategies of marine fish 

species of North Atlantic. Journal of Northwest Atlantic Fishery Science, 33: 23- 

31 

Murua, H., Kraus, G., Saborido-Rey, F., Witthames, P.R., Thorsen A., and Junquera, S, 

2003. Procedures to estimate fecundity of marine fish species in relation to their 

reproductive strategy. Journal of Northwest Atlantic Fishery Science, 33: 33-54 

Myers, R.A., Hutchings, J.A. and Barrowman, N.J., 1996. Hypotheses for the decline of 

cod in the North Atlantic. Marine Ecology Progress Series, 138:293-308 

Nordeide, J.T., Foldstad, I., 2000. Is cod lekking or a promiscuous group spawner? Fish 

and Fisheries, 1: 90-93 

Ottersen, G., Hjermann, D.Ø. and Stenseth, N.C., 2006. Changes in spawning structure 

strengthen the link between climate and recruitment in a heavily fished cod 

(Gadus morhua) stock. Fisheries Oceanography, 15(3): 230-243 

Ouellet, P., Lambert, Y. and Bérubé, I., 2001. Cod egg characteristics and viability in 

relation to temperature and maternal nutritional condition. ICES Journal of Marine 

Science, 58: 672-686 

Parker, G.A. and Begon, M., 1986. Optimal egg size and clutch size: effect of 

environment and maternal phenotype. American Naturalist, 128: 573-592 

Parrish, R.H., Mallicoate, D.L. and Klingbeil, R.A., 1986. Age dependent fecundity, 

number of spawnings per year, sex ration, and maturation stage in Northern 

anchovy, Engraulis mordax. US Fisheries Bulletin, 84: 503-517 

34

Pelletier, D. and Laurec, A. (1992). Management under uncertainty: Defining strategies 

for reducing overexploitation. ICES Journal of Marine Science, 49: 389-401 

Pihl, L. and Ulmestrand, M., 1988. Investigations on coastal cod on the Swedish west 

coast. Länsstyrelsen i Göteborg och Bohus Län., 61 pp. (in Swedish) 

Polunin, N.V.C., 2002. Marine protected areas, Fish and Fisheries. In: Hart, P.J.B., 

Reynolds, J.D. (Eds.), Handbook of fish biology and Fisheries. Blackwell, Oxford, 

UK, pp293-318 

Pörtner, H.O., Berdal, B., Blust, R., Brix, O., Colosimo, A., De Watcher, B., Giuliani, 

A., Johansen, T., Fischer, T., Knust, R., Lanning, G., Naevdal, G., Nedend, A., 

Nyhammer, G., Sartoris, F.J., Serendero, I., Sirabella, P., Thorkildsen, S. and 

Zakhartsev, M., 2001. Climate induced temperature effects on growth 

performance, fecundity and recruitment in marine fish: developing a hypothesis 

for cause and effect relationships in Atlantic cod (Gadus morhua) and common 

eelpout (Zoarces viviparis). Continental Shelf Research 21: 1975-1997 

Rae, B.B. 1967. The food of cod in the North Sea and on west of Scotland grounds. 

Marine Research, 1: 68pp. 

Ricker, W.E., 1975. Computation and interpretation of biological statistics of fish 

population. Bulletin of the Fisheries Research Board of Canada, 191, Ottawa 

Rideout, R.M., 1999. Aspects of the reproductive cycle of Atlantic cod, Gadus morhua 

L., from inshore Newfoundland. MSc thesis. Memorial University of 

Newfoundland, St. John’s: 131 pp. 

Rideout, R. M. and Burton, M. P. M., 2000. Peculiarities in ovarian structure leading to 

multiple-year delays in oogenesis and possible senescence in Atlantic cod, Gadus 

morhua L. Canadian Journal of Zoology, 78: 1840-1844. 

Rideout, R.M., Burton, MPM and Rose, GA., 2000. Observations on mass atresia and 

skipped spawning in northern Atlantic cod, from Smith Sound, Newfoundland. 

Journal of Fish Biology, 57: 1429-1440 

Rideout, R.M., Rose, GA and Burton, MPM., 2005. Skipped spawning in female 

iteroparous fishes. Fish and Fisheries, 6: 50-72 

Rindorf, A., Jensen, H. and Schrum, C., 2008. Growth, temperature and density 

relationships of North Sea cod (Gadus morhua). Canadian Journal of Fisheries and 

Aquatic Sciences, 65: 456-470 

Robichaud D. and Rose G.A., 2001. Multiyear homing of Atlantic cod to a spawning 

ground. Canadian Journal of Fisheries and Aquatic Sciences, 58: 2325-2329 

35

Robichaud D. and Rose G.A., 2003. Sex differences in cod residency on a spawning 

ground. Fisheries Research, 60: 33-44 

Robichaud D. and Rose G.A., 2004. Migratory behaviour and range in Atlantic cod: 

inference from a century of tagging. Fish and Fisheries, 5:185–214 

Roff, D.A., 2002. Life history evolution. Sinauer Associates, Sunderland, MA 

Rose, G.A., 1993. Cod spawning on a migration highway in the Northwest Atlantic. 

Nature, 366: 458-461 

Rowe, S and Hutchings, J.A., 2003. Mating system and the conservation of 

commercially exploited marine fish. Trends in Ecology and Evolution, 18: 567- 

572 

Rowe, S and Hutchings, J.A., 2004. The function of sound production by Atlantic cod 

as inferred from pattern of variation in drumming muscle mass. Canadian Journal 

of Fisheries and Aquatic Sciences, 82: 1391-1398 

Saborido-Rey, F. and Junquera, S., 1998. Histological assessment of variations in sexual 

maturity of cod (Gadus morhua) at the Flemish Cap (north-west Atlantic). ICES 

Journal of Marine Science, 55: 515-521. 

Schwalme, K and Chouinard, G.A., 1999. Seasonal dynamics in feeding, organ weight 

and reproductive maturation of Atlantic cod (Gadus morhua) in the Southern Gulf 

of St. Lawrence. ICES Journal of Marine Science, 56: 303-319 

Shirokova, M.Y., 1977. Peculiarities of the sexual maturation of females of Baltic cod, 

Gadus morhua callarias. Journal of Ichthyology, 17: 574-581 

Skjæraasen, J.E., Nilsen, T. and Kjesbu, O.S., 2006. Timing and determination of 

potential fecundity in Atlantic cod (Gadus morhua). Canadian Journal of Fisheries 

and Aquatic Sciences, 63: 310-320 

Solemdal, P., Kjesbu, O.S. and Fonn, M., 1995. Egg mortality in recruit- and repeatspawning 

cod – an experimental study. ICES CM1995/G:35 

Svedäng, H. and Bardon, G., 2003. Spatial and temporal aspects of the decline in cod 

(Gadus morhua L.) abundance in the Kattegat and eastern Skagerrak. ICES 

Journal of Marine Science 60, 32-37 

Svedäng, H., Svenson A. and Hagberg, J., 2003. Differences in technical fishing 

regulations between the Sound and Kattegat: marked effects on abundance and 

size distribution of dominant demersal fish species. International Council for the 

Exploration of the Sea CM 2003/Z:01 

36

Svedäng, H., Hagberg, J., Börjesson, P., Svenson, A. och Vitale, F. 2004. Bottenfisk i 

Västerhavet. Fyra studier av beståndens status, utveckling och lekområden vid den 

svenska västkusten. Swedish Board of Fisheries Finfo 2004:6: 42 pp. In Swedish 

with English summary. Available at www.fiskeriverket.se 

Svedäng, H and Svenson, A., 2006. Cod Gadus morhua L. populations as behavioural 

units: inference from time series on juvenile abundance in the eastern Skagerrak. 

Journal of Fish Biology, 69 (Supplement C): 151-164 

Svedäng, H., Rigthon, D. and Jonsson, P., 2007. Migratory behaviour of Atlantic cod 

Gadus morhua: natal homing is the prime stock-separating mechanism. Marine 

Ecology Progress Series, 345: 1-12 

Templeman, W., 1974. Migrations and intermingling of Atlantic cod (Gadus morhua) 

stocks of the Newfoundland area. Journal of the Fisheries Research Board of 

Canada, 31:1073-1092 

Thorsen, A. and Kjesbu, O.S., 2001. A rapid method for estimation of oocyte size and 

potential fecundity in Atlantic cod using a computer-aided particle analysis 

system. Journal of Sea Research, 46: 295-308. 

Thorsen, A., Trippel, E.A. and Lambert, Y., 2003. Experimental methods to monitor the 

production and quality of eggs of captive marine fish. Journal of Northwest 

Atlantic Fishery Science, 33: 55-70 

Thorsen, A., Marshall, C.T. and Kjesbu, O.S., 2006. Comparison of various potential 

fecundity models for north-east cod Gadus morhua, L. using oocyte diameter as 

standardizing factor. Journal of Fish Biology, 69: 1709-1730 

Tomkiewicz, J., Tybjerg, L. and Jespersen, Å., 2003 a. Micro- and macroscopic 

characteristic to stage gonadal maturation of female Baltic cod. Journal of Fish 

Biology, 62: 253-275 

Tomkiewicz, J. Morgan, M.J., Burnett, J. and Saborido-Rey, 2003 b. Available 

information for estimating reproductive potential of Northwest Atlantic groundfish 

stocks. Journal of Northwest Atlantic Fishery Science, 33: 1-21 

Trippel, E.A., 1995. Age at maturity as a stress indicator in fisheries. Bioscience, 45: 

759-771. 

Trippel, E.A., Morgan, M.J., Fréchet, A., Rollet, C., Sinclair, A., Annand, C., 

Beanlands, D. and Brown, L, 1997. Changes in age and length at sexual maturity 

of Northwest Atlantic cod, haddock and pollock stocks, 1972-1995. Canadian 

technical Report of Fisheries and Aquatic Science, 2157: 132 pp 

Trippel, E.A., 1998. Egg size and viability and seasonal offspring production of young 

Atlantic cod. Transactions of the American Fisheries Society, 127: 339-359 

37

Trippel, E.A., 1999. Estimation of stock reproductive potential: history and challenges 

for Canadian Atlantic gadoids stock assessment. Journal of Northwest Atlantic 

Fishery Science, 25: 61-81 

Tyler, C.R., 1991. Vitellogenesis in salmonids. In Scott, A.P., Sumpter, J.P., Kime, D.E. 

and Rolfe, J., eds Proc. Fourth Int. Symp Reproductive Physiology of Fish. 

Sheffield, UK: Sheffield University Press, pp 295 

Tyler, C.R. and Sumpter, J.P., 1996. Oocytes growth and development in teleosts. 

Reviews in Fish Biology and Fisheries, 6: 287-318. 

Wallace, R.A. and Selman, K., 1981. Cellular and dynamic aspects of oocyte growth in 

teleosts. American Zoologist, 21: 325-343 

Walsh, S.J., Wells, R. and Brennan, S., 1986. Histological and visual observation on 

oogenesis and sexual maturity of Flemish Cap female cod. NAFO Scientific 

Council Research Document 86/111: 11pp 

Whitthames, P.R., Andersson, E., Greenwood, EL.,N., Lyons, B, Fonn, M. and Kjesbu, 

O.S., 2003. Apoptosis in regressing follicles from Solea solea and Gadus morhua. 

Fish Physiology and Biochemistry, 28: 91-109 

Windle MJS and Rose GA, 2005 Migration route familiarity and homing of transplanted 

Atlantic cod (Gadus morhua). Fisheries Research, 75:193–199 

Woodhead, A. D. and Woodhead, P. J. M., 1965. Seasonal changes in the physiology of 

the Barents Sea Cod, (Gadus morhua L.) in relation to its environment. Endocrine 

changes particularly affecting migration and maturation. Special Publication of the 

International Commission for the Northwest Atlantic Fisheries, 6: 691-715. 

Wootton, R.J., 1984. Introduction: Strategies and tactics. In Fish reproduction: 

strategies and tactics. Edited by G.W. Potts and R.J. Wootton. Academic Press, 

London, UK, pp 13-33. 

Yoneda, M. and Wright, P.J., 2004. Temporal and spatial variation in reproductive 

investment of Atlantic cod Gadus morhua in the northern North Sea and Scottish 

west coast. Canadian Journal of Fisheries and Aquatic Sciences, 276: 237-248 

38

ACKNOWLEDGEMENTS 

Gratitude is the mother of all the virtues (Cicero, Roman orator and philosopher, 106-43 

BC). I am deeply grateful to Henrik Svedäng because without him I would never have 

started (nor concluded) my PhD. Thanks for the leadership, support and for all the great 

laughs…you definitively made those years much funnier. I would also like to thank 

Håkan Wennhage for his “short but intense” supervising and his precious help with all 

the “bureaucratic” aspects. A special thanks goes to Rutger Rosenberg for his valuable 

assistance during those years. 

Thanks to all the people at the Institute of Marine Research in Lysekil: to those working 

on board of Argos and Ancylus for their help in collecting data, despite their 

unwillingness in using the “lethal” formaldehyde; to Rajlie Sjöberg for all the cod 

otoliths she has been reading for me in those years also on short notice request; to 

Joakim Hjelm for his constant understanding and support; to Anne Johansson for her 

unlimited willingness to help me whenever I needed…thanks to all of you for your love, 

friendship and for letting me feeling at home since the very first day. 

I’m also grateful to Merete Fonn, Anders Thorsen and Olav Kjesbu at the Institute of 

Marine Research in Bergen (Norway) for their priceless teaching and their great 

hospitality. 

I would like to express my gratitude to the other members of the “Italienska komplott”, 

Michele (alias Mikälä) and Max...you have been like brothers to me, supporting and 

helping me in every single way. 

There are not enough words for thanking Björn for the joy he brought in my everyday 

life and for being always so lovely and supporting also during my last (totally 

hysterical) days, when everybody else would have instead run away. 

I’m really thankful to Lars Billton from “Brita och Sven Rahmns Stiftelsen” who 

financed my studies showing a sincere trust in the project and in my work. Further 

funds were supplied by the University of Rome “La Sapienza”, Italienska 

Kulturinstitutet “C.M.Lerici”, Kungliga Vetenskaps- och Vitterhetssamhället i Göteborg 

and Adlerbertska Hospitiestiftelsen. 

I would like to dedicate this thesis to my family and friends in Italy because this thesis 

represents one of the reasons why we had to live apart. I want them to know that leaving 

them was one of the hardest things I ever had to do. 

A last but important clarification for the Scandinavians: my correct name is Francesca 

not Fransesca or Franchesca or Franceska or Fransheska…I could list a bunch! 

39

Journal of Fish Biology (2005) 67, 669–683 

doi:10.1111/j.1095-8649.2005.00767.x,availableonlineathttp://www.blackwell-synergy.com 

Evaluation of the temporal development of the ovaries in 

Gadus morhua from the Sound and Kattegat, North Sea 

F. VITALE*, M. C ARDINALE AND H. SVEDÄNG 

National Board of Fisheries, P. O. Box 4-453 21 Lysekil, Sweden 

(Received 6 July 2004, Accepted 8 March 2005) 

The gonadal development of cod Gadus morhua in the Sound and Kattegat, North Sea, was 

studied by investigating their histological structure on a temporal scale by intense sampling from 

September 2002 to May 2003. Different age classes were followed and the proportion mature in 

each age class within each area was analysed. Based on existing maturity criteria, a modified 

system, based on histological features, was developed in order to emphasize the crucial step in the 

developmental process, i.e. the passage from endogenous to exogenous vitellogenesis. Only fish 

that had attained exogenous vitellogenesis could be considered as being reproductively active in 

the forthcoming breeding season (Kjesbu et al., 2003). The histological based maturity scale will 

greatly improve the capability of separating mature from immature individuals in the studied 

areas, that is fundamental for an accurate and unambiguous estimate of the spawning stock 

biomass. Furthermore, the results showed a larger proportion of mature individuals per age class 

in the Kattegat stock compared to the Sound stock, which implied an earlier maturity for this 

stock. This difference in maturation pattern might have been related to a relaxation of competition, 

i.e. enhanced growth rate, as an effect of different levels of exploitation and technical fishing 

regulations between the two adjacent areas. 

# 2005 The Fisheries Society of the British Isles 

Key words: cod; histology; maturation timing; oocyte; vitellogenesis. 

INTRODUCTION 

Fish stocks are currently assessed using age-structured models such as virtual 

population analysis (VPA), which estimates fishing mortality and stock biomass 

from catch, effort and survey data (Pelletier & Laurec, 1992). For a given 

management option within the International Council for the Exploration of 

the Sea (ICES) corresponding annual total allowable catches (TAC) are established 

by using estimated spawning stock biomass (SSB) as a reference point. 

The SSB is defined as the biomass of both sexes contributing to the reproductive 

potential of the stock. Thus, accurate estimation of the proportions of spawning 

fishes within each age class is of vital importance for stock assessment (Marshall 

et al., 1998; Cardinale & Arrhenius, 2000). These proportions, defined as maturity 

ogives, rely on estimates of sexual maturity (Myers & Barrowman, 1996; 

Rochet, 2000a). 

*Author to whom correspondence should be addressed. Tel.: þ46 0523 18743; fax: þ46 0523 13977; 

email: francesca.vitale@fiskeriverket.se 

# 2005 The Fisheries Society of the British Isles 

669

670 F. VITALE ET AL. 

At present, the Kattegat cod Gadus morhua L. population is considered as 

severely depleted, as an effect of a prolonged period of high fishing pressure 

(Svedäng & Bardon, 2003; Cardinale & Svedäng, 2004; ICES, 2004). The stock 

decline coincided with a disappearance of large spawning aggregations in the 

southern part of the Kattegat and survey data have indicated that abundance of 

spawning females have dropped to very low levels in the area (Cardinale & 

Svedäng, 2004). Most of the SSB (>95%) is compressed to a few age classes 

(2–5 years) (ICES, 2004). In such a critical situation, it is important to follow and 

describe the reproductive cycle, as spawning pattern and precise maturity ogives 

are essential information for accurate fish stock assessments. It is also important 

that maturation patterns are followed and elucidated in commercial fish species 

that have faced extreme fishing mortality rates during a considerable long period 

of time (Olsen et al., 2004). No such studies on the temporal development and 

validation of maturity schedule for the Kattegat cod population, however, have 

ever been performed. 

Estimation of the proportion of mature fishes is highly dependent on the 

actual temporal development of the gonads, which is also known to be stockspecific 

(Rochet, 2000b; ICES, 2004). In order to accurately estimate maturity 

ogives in fish stocks, the maturity staging used must be accurate and unambiguous. 

At present, assessment of cod populations within the ICES framework 

relies on macroscopic scales to estimate the proportion of mature individuals 

within each age class (ICES, 2004). There is a great concern about the consistency 

of macroscopic gonadal evaluation, especially with regard to the prespawning 

phase, which is difficult to discriminate macroscopically. Several 

studies, in effect, have indicated that the proportion of mature individuals may 

be improperly estimated when using macroscopic scales (Dias et al., 1998; ICES, 

2004). Imprecision in judgement of maturity stages leads to a biased evaluation 

of reproductive status, and consequently, estimated maturity ogives might 

become highly inaccurate. Therefore it appears extremely important to determine 

at which time of the maturation cycle the discrimination between maturing 

and non-maturing individuals can be made. Among the alternatives approaches 

to assess maturity, such as oocyte size frequency distributions, the gonadosomatic 

index and fat content, histology is considered to be the most reliable 

(Kjesbu et al., 2003). Histology has shown a greater reliability than traditional 

macroscopic evaluations in separating mature from immature individuals 

(Murua & Motos, 1998; Saborido-Rey & Junquera, 1998; Tomkiewicz et al., 

2003), because through histological studies it is possible to identify at what time 

the oocytes start to build up the yolk reserves. The presence of particular yolk 

proteins (cortical alveoli) within the oocyte has often been considered as the first, 

decisive step that enables the individual fish to complete the gonadal development 

for the following breeding season. Under normal conditions, individuals at 

this stage of gonadal development are therefore considered to be maturing 

(Holdway & Beamish, 1985; Saborido-Rey & Junquera, 1998; Murua et al., 

2003). As previous studies have shown, however, interruptions in the spawning 

cycle of cod may occur, and it is important to consider that premature, as well as 

adult fish, could postpone gonadal development and spawning, (Burton et al., 

1997; Rideout & Burton, 2000). Burton (1994) recorded fish that had been 

arrested at this phase of the development (endogenous vitellogenesis). This 

# 2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67, 669–683

DEVELOPMENT OF COD OVARIES 671 

kind of phenomenon is well known in other fish species such as Atlantic salmon 

Salmo salar L. (Johnston et al., 1987), whose gonadal development has started 

but might be interrupted and postponed during the current spawning season, 

and sexual maturity is attained at the very earliest in the following spawning 

season. Consequently, the presence of reproductively inactive females should be 

considered when estimating maturity ogives for a specific fish stock. In addition, 

Saborido-Rey & Junquera (1998) have recorded an overestimation of the proportion 

of maturing cod individuals in the pre-spawning season in relation to the 

estimated proportion of post-spawning fish by the end of the spawning season. 

This overestimation of mature and maturing fish could the result of a doubtful 

inclusion of individuals at the cortical alveoli stage as being considered maturing 

in the forthcoming spawning season. 

The principal aim of this study was therefore to develop a histologically based 

maturity scale specific for the Kattegat cod. It was recognized that such a 

maturity scale must provide information about key events taking place, i.e. to 

recognize the significant step in the developmental process when the individual 

fish is ‘set in train’ to attain sexual maturity. Therefore only fish that have 

attained such a developmental status can be considered as being reproductively 

active in the forthcoming breeding season. This will improve the capability of 

separating mature from immature individuals and consequently the assessment 

and management of this stock. 

The second aim of the study was to describe the temporal maturation pattern 

for different age classes within two studied cod subpopulations in the Kattegat 

and the Sound by analysing the structural events taking place in the ovaries on a 

temporal scale. This aspect is considered as crucial for a correct planning of the 

timetable of sampling of the maturity ogives to be used for stock assessment 

purposes (ICES, 2004). 

The cod in the Sound and Kattegat show marked differences in size structure 

and abundance, the stock in the Sound being in a less depleted state than the one 

in the Kattegat (Svedäng et al., 2003). This divergence in stock status is probably 

due to differences in technical fishing regulations, as towed fishing gears have 

been forbidden since 1932 in the Sound. Although, there is no evidence of genetic 

segregation between the two stocks (Knutsen et al., 2003; C. André, pers. obs.), 

the marked differences in size structure (Svedäng et al., 2003), together with 

unpublished information from on-going tagging experiments in the area 

(H. Sveda¨ng, pers. obs.), supported the view of two separated possibly subpopulations 

of cod. Thus, the second aim of the study was to elucidate possible 

differences in maturation timing between the two adjacent subpopulations whose 

mortality rates and population structure so clearly depart from each other, 

whereas no genetic differentiation between the stocks has so far been evidenced 

(Knutsen et al., 2003). 

MATERIALS AND METHODS 

In order to study the timing of gonadal development prior to the next spawning 

season, the proportion of mature individuals within each age class was analysed. The 

individuals were grouped into three age classes: 2, 3 and 4þ years. The oldest age group 

included all individuals aged 4 years. 



Fish sampling took place on a monthly basis (Table I), from September 2002 to May 

2003 in the Kattegat and the Sound (Fig. 1), with the exception of April in both areas. 

Cod were collected on both commercial fishing vessels and Swedish research vessels. The 

fish were processed immediately after being taken on board. For each fish, total length 

(L T )at05 cm below, total wet mass (M T ) at the nearest 01 g and gutted mass were 

recorded. The range in L T varied between 25 and 84 cm. Otoliths (sagittae) were removed 

from all individuals sampled and transversely sectioned through the centre of the nucleus. 

Therefore, individual age was estimated by a single age reader, counting hyaline zones on 

sectioned otoliths illuminated from above against a dark background (15). 

In order to avoid the tissues from disintegrating, fresh gonads were usually removed 

from the fish within an hour after being taken on board. The gonads were weighed and 

stored in phosphate buffered formaldehyde 36% for 14 days before histological analysis. 

In case of small gonads, the whole gonad was preserved; otherwise a 5 cm long middle 

cross section of the right lobe was stored. Fixed sections of ovary were dehydrated 

through ascending concentrations of ethanol for a specific duration, embedded through 

ascending concentrations of historesin and eventually, polymerized into historesin blocks 

at 4 C. Transverse sections of 2–5 mm in thickness, obtained using a Leica RM2165 

microtome, were dried at 60 C for a short time before staining with toluidine blue 2% 

and 1% borax. This procedure ensured staining of structures such as the nucleus, yolk 

granules and chorion with different tones of blue. The slides were inspected at different 

magnifications by using a Leica DMR light microscope. Representative stages of oocyte 

development (Fig. 2) were photographed using a Leica DC 300 photomicroscope camera. 

DATA ANALYSIS 

The low sample size per age class did not allow month-by-month comparisons to be 

made, and as a consequence, the collected material was merged into 2 month periods. 

The proportion of maturing individuals, as determined by the histological analysis, was 

estimated within each age class. A generalized linear model (GLM) procedure was used in 

order to estimate the effects of age, month and area (i.e. the Kattegat and Sound) on the 

proportion of mature individuals. In addition, difference in Fulton’s condition factor (K), 

K ¼ M T L 3 T , was tested for the two areas among immature and mature individuals 

using a GLM with age as a factor and month as a covariate. Parsimony and model 

selection was evaluated using Akaike information criteria (AIC; Chambers & Hastie, 

1992). The AIC is computed as: AIC ( p) ¼ nln(S Res p ) þ 2p nln(n), where p is the 

number of parameters, S Res is the residual sum of squares of the model and n is the 

number of observations. The second term in AIC increases with p and it serves as a 

penalty for the increasing number of parameters in the model. The AIC statistic accounts 

simultaneously for the d.f. used and the goodness of the fit. More parsimonious models 

have a lower AIC. The error was modelled assuming the binomial distribution (immature 

TABLE I. Number of analysed samples (females) per age group and area, combined into 2 

month periods 

Age (years) 

September to 

October 

November to 

December 

January to 

February 

March to 

May 

Kattegat 2 33 25 37 42 

3 25 20 31 27 

4þ 17 15 36 12 

Sound 2 7 26 60 25 

3 17 14 14 17 

4þ 6 14 0 8 



10° 40′ 0″ E 

11° 45′ 0″ E 

12° 50′ 0″ E 

57° 20′ 0″ N 

1:860 737 

Sweden 

57° 20′ 0″ N 

Kattegat 

56° 15′ 0″ N 

56° 15′ 0″ N 

Copenhagen 

Sound 

10° 40′ 0″ E 11° 45′ 0″ E 12° 50′ 0″ E 

FIG. 1. Study area (., sampling locations). 

against mature individuals). The level of significance was set at 5% for all the statistical 

tests used in this study. 



n cnr 

(a) 

m 

(b) 

ca 

yg 

ho 

pof 

(c) 

(d) 

FIG. 2. Transverse sections of cod ovaries showing oocytes at different stages: (a) primary growth, (b) 

endogenous vitellogenesis, (c) exogenous vitellogenesis and (d) spent. n, nucleus; m, nucleolus; ca, 

cortical alveolus; cnr, circumnuclear ring; yg, yolk granule; ho, hydrated oocyte; pof, postovulatory 

follicle. Scale bar: (a) 25 mm; (b), (c) and (d) 100 mm. Toluidine blue staining. 

RESULTS 

HISTOLOGICAL STAGING SYSTEM 

The oocytes were present in various states of development throughout the 

folds of both ovaries, moving from the wall towards the centre of the organ 

(luminal epithelium). This pattern could be observed throughout the whole 

organ. This homogeneity of the ovary, documented in previous studies (Kjesbu 

et al., 1990), enabled just one section to be selected from each ovary, namely, in 

this study, a middle cross section of the right lobe. The first developmental step 

occurring in the ovary is the oogonial proliferation. Oogonia are small in size 

and with a single nucleolus. Oogenesis begins with the conversion of oogonia 

into oocytes (Kjesbu & Kryvi, 1989). These cells undergo a series of cellular 

modifications preceding the ovulation. 

According to the histological characteristics observed under light microscopy, 

seven discrete stages of the developmental process (oogenesis) were identified. 

Stage 1: immature 

At this premature stage, the oocytes are small with a dense basophilic (intense 

staining) cytoplasm and a central nucleus (germinal vesicle) with few large 



nucleoli around its edge (perinucleolar stage). Oogonia are always present 

(Selman et al., 1993; Coward et al., 2002) but they might be not visible. 

Stage 2: primary (previtellogenic) growth 

The size of the oocyte increases. This phase is characterized by the nucleus 

undergoing major transformation such as an increase in size and the formation 

of multiple nucleoli, which generate large quantity of ribosomal RNA 

(Takashima & Hibiya, 1995). The presence of a light area around the nucleus 

[Fig. 2(a)] shows that cytoplasmatic changes are occurring. This weakly stained 

area is called the ‘circumnuclear ring’ (CNR) (Woodhead & Woodhead, 1965; 

Morrison, 1990). 

Stage 3: endogenous vitellogenesis (cortical alveoli phase) 

At this stage, oocytes growth occurs when triggered by a gonadotropin surge 

(Wallace & Selman, 1981). Prior to vitellogenesis, the ‘circumnuclear ring’ moves 

towards the outer part of the cell and gradually disintegrates, while the spherical 

and transparent vesicles (cortical alveoli) appear in the superficial half of the 

cytoplasm, which is now more acidophilic (light staining). 

At this stage there are no yolk granules present in the cytoplasm [Fig. 2(b)]. 

Stage 4: exogenous vitellogenesis 

This phase represents the true vitellogenesis, during which the maternal hepatically 

derived plasma precursor, vitellogenin (VTG), is packaged into yolk 

protein in the form of granules (Wallace, 1978), easily identifiable because of 

their strong reaction to the toluidine blue [Fig. 2(c)]. These bodies, intensely 

stained, initially appear peripherally, but as they increase in number and size, 

they tend to spread out together with the cortical alveoli, throughout the 

cytoplasm. The shape of the nucleus becomes irregular. The occurrence of this 

stage means that the maturation process is in progress, and under normal 

conditions, the individual will develop within the current spawning season. The 

nucleus is still centrally located. 

Stage 5: final maturation 

The final step is marked by thickening of the chorion, the migration of the 

nucleus towards the animal pole and by the hydration process. The nucleus, 

during the final maturation, moves from the centre to the periphery (Nagahama, 

1983), and eventually breaks down when reaching it. The following water influx 

(hydrated oocyte) is probably driven by the proteolysis of yolk protein into free 

amino acids and consequent osmosis (Craik & Harvey, 1987; Kjesbu & Kryvi, 

1989). 

Stage 6: spent 

At ovulation, oocytes are released into the lumen (Wallace & Selman, 1981) 

while the ruptured follicles (post-ovulatory follicle) remain within the lamellae. 

Post-ovulatory follicles (POFs) are short-lived but readily distinguishable 

[Fig. 2(d)]. At the end of the spawning season, the ovary enters the spent stage 

and residual vitellogenic oocytes are reabsorbed (Tomkiewicz et al., 2003). 



Stage 7: resting 

Oocytes are in stages 1 and 2. Some post-ovulatory structures, are still present 

and show signs of previous spawning (Tomkiewicz et al., 2003). 

TEMPORAL DEVELOPMENT BETWEEN AREAS AND AGE 

CLASSES 

Reproductively active (i.e. likely to be spawning in the forthcoming season) 

females were considered to be in stages 4, 5 and 6 while inactive females were in 

stages 1, 2 and 3. The four periods studied showed an increasing percentage of 

mature (active) females, with the forthcoming spawning season, in both areas 

(Table II). The general tendency was represented by a progression of mostly 

immature ovaries in September to October to mostly early developing in 

November to December. Ripe females were commonly observed by the end of 

January. 

In the Kattegat, all 2 year-old females were found immature (i.e. at stage 1 or 

2) in September to October, whereas 20% of the females aged 3 years and 29% 

of the fish aged 4þ years were considered mature (Fig. 3), i.e. had started 

exogenous vitellogenesis, the step that almost always leads to full maturation 

in the forthcoming spawning season. In November to December, the percentage 

of females aged 2, 3 and 4þ years found with oocytes at stage 4 were 12, 40 and 

80%, respectively. From the beginning of January and to the beginning of 

February, the proportion of sexual mature fish increased even further: 89% of 

the females aged 4þ years or more were ready to release eggs. From February 

until the end of March the proportion of sexual mature females remained high. 

After having released all the eggs or most of them, the fish progressed into a 

spent stage. 

In the Sound, the percentage of reproductively active females aged 3 years in 

September to October was 6%. In November to December the percentage of 

mature individuals had steadily increased in age groups 3 and 4þ years (29 and 

43%, respectively). In January to February, the proportion of the studied 

females in age groups 2, 3 and 4þ years ready to spawn corresponded to 20, 

43 and 75%, respectively. 

TABLE II. Percentage of mature cod females per age group and area, merged into 2 

month periods 

Age (years) 

September to 

October 

November to 

December 

January to 

February 

March to 

May 

Kattegat 2 0 12 24 5 

3 20 40 65 56 

4þ 29 80 89 67 

Sound 2 0 0 20 20 

3 6 29 43 29 

4þ 0 43 75 50 



1·0 

(a) 

0·8 

0·6 

0·4 

0·2 

0·0 

1·0 

37 

60 25 

25 

7 

33 26 

42 

Sept to Oct Nov to Dec Jan to Feb Mar to May 

(b) 

0·8 

Proportion mature 

0·6 

0·4 

0·2 

25 

20 

14 

31 

14 

27 

17 

0·0 

1·0 

0·8 

0·6 

0·4 

0·2 

0·0 

17 


(c) 

36 

15 3 

12 

8 

14 

7 

6 


Month 

FIG. 3. Proportion of mature individuals per area ( , Kattegat; &, The Sound) at ages: (a) 2, (b) 3 and (c) 

4þ years. Values are means S.E. The numbers indicate the sample size. 



DATA ANALYSIS 

For both studied areas, the percentages of fish at various developmental stages 

were calculated for each age class on a 2 month basis from September 

until May (Table II). The initial model was: immature per mature 

(response) ¼ (intercept) þ age þ month þ area with L T modelled as covariate. 

The interaction factors were not included in the model. The L T (covariate) was 

not significant and therefore it was excluded from the final model. Results from 

the comparisons between models with different combinations of the predictors 

showed that the model including all the predictors was the best to explain the 

maturity status of Kattegat cod (Table III). All the analysed predictors (age, 

month and area) were found significant in the final GLM model (Table III). Age 

was the factor explaining most of the variation in mature status. Noteworthy, in 

every studied period of time, was that the percentage of reproductively active 

individuals within age group was significantly lower in the Sound area than in 

the Kattegat. There was a significant difference in K between the two areas 

among immature fish, with Kattegat cod having higher K than the Sound 

while no significant differences were found for mature fish. In both cases, 

month and age were not significant and therefore excluded from the final model. 

DISCUSSION 

Cod spawn many times during a single spawning season, i.e. cod females 

release eggs in discrete batches (Sorokin, 1957). Consequently, oocytes of varying 

developmental stages are present within the ovary at the same time. This 

TABLE III. Results from the comparisons between models with different combinations of 

the predictors. The information criteria (AIC) were used for generalized linear model 

(GLM) model selection, with the error modelled assuming the binomial distribution 

(immature against mature individuals). The Wald statistic is the homologous of the F 

statistic of GLM based on the binomial distribution 

Variables d.f. AIC P 

Age Month Area 6 4824


asynchronous development of the ovary (Wallace & Selman, 1981), which brings 

to a non-simultaneous ripening of eggs destined for spawning, is common in 

other commercial important marine fishes and the staging system described in 

this paper may also apply to those species. 

Essentially, oocytes in all teleosts undergo the same basic pattern of development: 

primary oocyte growth, cortical alveolus stage, vitellogenesis, maturation 

and ovulation (Tyler & Sumpter, 1996). The cycle of gonadal development 

described in the present study has been reported for cod from many areas, and 

a number of different maturity scales, based on histological analyses, have been 

produced. Kjesbu & Kryvi (1989) described four main stages (primary growth, 

cortical alveoli formation, true vitellogenesis and final maturation). According to 

some classification systems, however, some stage has been further subdivided. 

Recently, a 10 stage microscopical maturity scale has been proposed for the 

Baltic cod (Tomkiewicz et al., 2003), which includes the usual stages as well as 

potential gonadal diseases that can reduce fecundity. In the present work, 

oogenesis was divided into seven distinct developmental stages, according to 

common histological criteria. The classification maturity scale presented in this 

study emphasizes the difference between endogenous and exogenous vitellogenesis, 

as they are considered as different stages. According to Holdway & Beamish 

(1985), all oocytes reaching the second stage (when the CNR appears) are likely 

to mature within the subsequent reproductive cycle. Ovaries at this stage are 

always present, however the probability to carry on the maturation process 

depends on the degree of development in relation to the time of the year in 

which they are observed (Woodhead & Woodhead, 1965; Holdway & Beamish, 

1985; Tomkiewicz et al., 2003). The first structures to emerge within the oocyte 

cytoplasm during the gonadotropin-dependent growth phase are the yolk vesicles; 

also known as ‘intravesicular yolk’ (Marza et al., 1937). These oocytes 

contain endogenously synthesized glycoproteins, and subsequently they give 

rise to cortical alveoli; therefore they are not to be considered as yolk in the 

strict sense of the word (Wallace & Selman, 1981). The common use of the term 

‘yolk vesicle’ to describe the cortical alveoli seems inappropriate, because the 

contents of these structures do not contribute to embryonic development 

(Wallace & Selman, 1981). 

Burton (1994), however, recorded fish that had been arrested at endogenous 

vitellogenesis. This vital observation obviously shows that finding ovaries with 

oocytes at stage 3 does not necessarily imply a fish to be in an active reproductive 

state in the forthcoming spawning season. Therefore, only fish containing 

oocytes which have developed up to the exogenous vitellogenesis phase (stage 

4) should be considered as sexually mature (Burton et al., 1997), i.e. they are 

likely to spawn in the forthcoming season. The unawareness of this concept can 

lead to an overestimation of the SSB with hazardous consequences for overexploited 

species such as cod. 

Studies on northern cod off the Canadian coast suggest that exogenous 

vitellogenesis, leading to ripe gonads and spawning, must have started several 

months (c. 7 months) before the spawning period (Burton et al., 1997). This is 

clearly not the case in the Kattegat and Sound, where the first individuals in 

which exogenous vitellogenesis have begun (stage 4), was at the very earliest 

detectable in October, i.e. 4 months before the beginning of the spawning season. 



A consistent amount of specimens were found to be at stage 4 by November to 

December. Consequently the temporal development of ovaries for cod in the 

Sound and Kattegat seems to be shorter than in cod stocks off the Canadian 

coast. 

The spawning season of most of cod populations takes place from December 

until July. Along the Norwegian coast, cod spawning mostly takes place between 

February and April, while the Baltic Sea cod spawns from April to July (Cohen 

et al., 1990). There are no differences in the spawning timing schedule between 

the Sound and Kattegat, as in both subpopulations the spawning season starts in 

January to February and probably finishes by the end of March. The proportion 

of mature individuals of every studied age group, however, was lower in the 

Sound than in the Kattegat, implying that cod, on average, become mature at an 

older age in the Sound. This difference in the maturation pattern might be 

considered as an effect of different levels of exploitation. The cod stock in the 

Kattegat, has probably experienced a higher exploitation rate (Svedäng et al., 

2003). 

As an effect of fishing pressure, removing older and larger fishes, fishes might 

adjust their life-history traits such as reproduction and growth (Rochet & 

Trenkel, 2003), either by phenotypic response or by genetic adjustment. Olsen 

et al. (2004) and Yoneda & Wright (2004) have given support to the hypothesis 

that early-maturing genotypes were favoured relative to late-maturing genotypes 

during the collapse of northern cod. As no genetic differentiation has been linked 

to the two studied sub populations, the higher maturation rate in the Kattegat 

Atlantic cod could thus be due to other factors such as changes in growth rate. It 

is known that age at sexual maturation is positively correlated to growth rate or 

to the accumulation of surplus energy; fishes normally mature at the earliest 

opportunity (Policansky, 1983; Rowe et al., 1991; Thorpe, 1994; Sandstro¨m 

et al., 1995; Svedäng et al., 1996). The onset, or rather cessation of the inhibition 

of the maturation process (Rowe et al., 1991) can act a various stages of 

gametogenesis. The division between endogenous and exogenous vitellogenesis 

might be such a control at which the energetic status of the fish determines 

whether the maturation will proceed or not. 

The authors thank O.S. Kjesbu and M. Fonn from the Institute of Marine Research in 

Bergen for their precious teaching and advices. The authors are also grateful to the crew 

on R/V Ancylus and R/V Argos for assistance in the field. Financial support for this 

research was partially provided through grants from ‘Brita och Sven Rahmns Stiftelse’. 

References 

Burton, M. P. M. (1994). A critical period for nutritional control of early gametogenesis 

in female winter flounder Pleuronectes americanus (Pisces, Teleostei). Journal of 

Zoology 33, 405–415. 

Burton, M. P. M., Penney, R. M. & Biddiscombe, S. (1997). Time course of gametogenesis 

in Northwest Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and 

Aquatic Sciences 54 (Suppl. 1), 122–131. 

Cardinale, M. & Arrhenius, F. (2000). The relationship between stock and recruitment: 

are the assumptions valid? Marine Ecology Progress Series 196, 305–309. 

Cardinale, M. & Svedäng, H. (2004). Modelling recruitment and abundance of Atlantic 

cod, Gadus morhua, in the Kattegat-Eastern Skagerrak (North Sea): evidence of 



severe depletion due to a prolonged period of high fishing pressure. Fisheries 

Research 69, 263–282. 

Chambers, J. M. & Hastie, T. J. (1992). Statistical Models. Pacific Grove, CA: 

Wadsworth & Brooks/Cole. 

Cohen, D. M., Inada, T., Iwamoto, T. & Scialabba, N. (1990). Gadiform fishes of the 

world (order Gadiformes). FAO Species Catalogues, FAO Fisheries Synopsis 10. 

Coward, K., Bromage, N. R., Hibbit, O. & Parrington, J. (2002). Gamete physiology, 

fertilization and egg activation in teleost fish. Reviews in Fish Biology and Fisheries 

12, 33–58. 

Craik, J. C. A. & Harvey, S. M. (1987). Phosphorus metabolism and water uptake during 

final maturation of ovaries of teleosts with pelagic and demersal eggs. Marine 

Biology 90, 285–289. 

Dias, J. F., Peres-Rios, E., Chaves, P. D. T. C. D. & Rossi-Wongtschowski, C. L. D. B. 

(1998). Macroscopical analysis of ovaries of teleosts: Problems of classification 

and recommended procedures. Revista Brasileira de Biologia 58, 55–69. 

Hall, S. J. (1999). Effects of Fishing on Marine Ecosystems and Communities. Oxford: 

Blackwell Science. 

Holdway, D. A. & Beamish, F. W. H. (1985). The effect of growth rate, size, and season 

on oocyte development and maturity of Atlantic cod (Gadus morhua L.). Journal of 

Experimental Marine Biology and Ecology 85, 3–19. 

Hutchings, J. A. (2004). The cod that got away. Nature 428, 899–900. doi: 10.1038/ 

428899a 

Jennings, S. & Kaiser, M. J. (1998). The effect of fishing on marine ecosystems. Advances 

in Marine Biology 34, 201–352. 

Johnston, C. E., Gray, R. W., McLennan, A. & Paterson, A. (1987). Effects of photoperiod, 

temperature, and diet on the reconditioning response, blood chemistry, 

and gonad maturation of Atlantic salmon kelts (Salmo salar) held in freshwater. 

Canadian Journal of Fisheries and Aquatic Sciences 44, 702–711. 

Kjesbu, O. S. & Kryvi, H. (1989). Ooogenesis in cod, Gadus morhua L., studied by light 

and electron microscopy. Journal of Fish Biology 34, 735–746. 

Kjesbu, O. S., Witthames, P. R., Solemdal, P. & Greer Walker, M. (1990). Ovulatory 

rhythm and a method to determine the stage of spawning in Atlantic Cod (Gadus 

morhua). Canadian Journal of Fisheries and Aquatic Sciences 47, 1185–1193. 

Knutsen, H., Jorde, P. E., André, C. & Stenseth, N. CHR (2003). Fine-scaled geographical 

population structuring in a highly mobile marine species: the Atlantic cod. 

Molecular Ecology 12, 385–394. 

Marshall, C. T., Kjesbu, O. S., Yaragina, N. A., Solemdal, P. & Ulltang, O. (1998). Is 

spawner biomass a sensitive measure of the reproductive and recruitment potential 

of northeast Artic cod? Canadian Journal of Fisheries and Aquatic Sciences 55, 

1766–1783. 

Marza, V. D., Marza, E. V. & Guthrie, M. J. (1937). Histochemistry of the ovary of 

Fundulus heteroclitus with special reference to differentiating oocytes. The 

Biological Bulletin 73, 67–92. 

Morrison, C. M. (1990). Histology of the Atlantic cod, Gadus morhua: an atlas. Part 

three. Reproductive tract. Canadian Special Publications of Fisheries and Aquatic 

Sciences 100. 

Murua, H. & Motos, L. (1998). Reproductive modality and batch fecundity of the 

European hake (Merluccius merluccius) in the Bay of Biscay. Reports of 

California Cooperative Oceanic Fisheries Investigations 39, 196–203. 

Murua, H., Kraus, G., Saborido-Rey, F., Witthames, P. R., Thorsen, A. & Junquera, S. 

(2003). Procedures to estimate fecundity of marine fish species in relation to their 

reproductive strategy. Journal of Northwest Atlantic Fishery Science 33, 33–54. 

Myers, R. A. & Barrowman, N. J. (1996). Is fish recruitment related to spawner abundance? 

Fishery Bullettin 94, 707–724. 

Nagahama, Y. (1983). The functional morphology of teleost gonads. In Fish Physiology, 

Vol. IX (Hoar, W. S., Randall, D. J. & Donaldson, E. M., eds), pp. 223–275. New 

York: Academic Press. 



Olsen, E. M., Heino, M., Lilly, G. R., Morgan, M. J., Brattey, J., Ernande, B. & 

Dieckmann, U. (2004). Maturation trends indicative of rapid evolution preceded 

the collapse of northern cod. Nature 428, 932–935. doi: 10.1038/nature02430 

Pelletier, D. & Laurec, A. (1992). Management under uncertainty: Defining strategies for 

reducing overexploitation. ICES Journal of Marine Science 49, 389–401. 

Policansky, D. (1983). Size, age and demography of metamorphosis and sexual maturation 

in fishes. American Zoologist 23, 57–63. 

Rideout, R. M. & Burton, M. P. M. (2000). Peculiarities in ovarian structure leading to 

multiple-year delays in oogenesis an possible senescence in Atlantic cod, Gadus 

morhua L. Canadian Journal of Zoology 78, 1840–1844. 

Rochet, M. J. (2000b). May life history traits be used as indices of population viability? 

Journal of Sea Research 44, 145–157. 

Rochet, M. J. & Trenkel, V. M. (2003). Which community indicators can measure the 

impact of fishing? A review and proposals. Canadian Journal of Fisheries and 

Aquatic Sciences 60, 86–99. 

Rowe, D. K., Thorpe, J. E. & Shanks, A. M. (1991). Role of fat stores in the maturation 

of male Atlantic salmon (Salmo salar) parr. Canadian Journal of Fisheries and 

Aquatic Sciences 48, 405–413. 

Saborido-Rey, F. & Junquera, S. (1998). Histological assessment of variations in sexual 

maturity of cod (Gadus morhua) at the Flemish Cap (north-west Atlantic). ICES 

Journal of Marine Science 55, 515–521. 

Sandstro¨m, O., Neuman, E. & Thoresson, G. (1995). Effects of temperature on life 

history variables in perch. Journal of Fish Biology 47, 652–670. doi: 10.1006/ 

jfbi.1995.0169 

Selman, K., Wallace, R. A., Sarka, A. & Xiaoping, Q. (1993). Stages of oocyte development 

in the zebrafish, Brachydanio rerio. Journal of Morphology 218, 203–224. 

Sorokin, V. P. (1957). The oogenesis and reproductive cycle of the cod (Gadus morhua 

Linn). Trudy Pinro 10, 125–144. (In Russian; English translation No. 72F49 

Ministry of Agriculture Fisheries and Food, U.K. 1961). 

Svedäng, H. & Bardon, G. (2003). Spatial and temporal aspects of the decline in cod 

(Gadus morhua L.) abundance in the Kattegat and eastern Skagerrak. ICES 

Journal of Marine Science 60, 32–37. doi: 10.1006/jmsc.2002.1130 

Svedäng, H., Neuman, E. & Wickstro¨m, H. (1996). Maturation patterns in female 

European eel: Age and size at the silver eel stage. Journal of Fish Biology 48, 

342–351. 

Takashima, F. & Hibiya, T. (1995). An Atlas of Fish Histology. Normal and Pathological 

Features. Tokyo: Kodansha. 

Thorpe, J. E. (1994). An alternative view in salmonids. Aquaculture 121, 105–113. 

Tomkiewicz, J., Tybjerg, L. & Jespersen, Å. (2003). Micro- and macroscopic characteristic 

to stage gonadal maturation of female Baltic cod. Journal of Fish Biology 62, 

253–275. doi: 10.1046/j.1095-8649.2003.00001.x 

Tyler, C. R. & Sumpter, J. P. (1996). Oocytes growth and development in teleosts. 

Reviews in Fish Biology and Fisheries 6, 287–318. 

Wallace, R. A. (1978). Oocyte growth in nonmammalian vertebrates. In The Vertebrate 

Ovary (Jones, R. E., ed.), pp. 469–502. New York: Plenum Press. 

Wallace, R. A. & Selman, K. (1981). Cellular and dynamic aspects of oocyte growth in 

teleosts. American Zoologist 21, 325–343. 

Woodhead, A. D. & Woodhead, P. J. M. (1965). Seasonal changes in the physiology of 

the Barents Sea Cod, (Gadus morhua L.) in relation to its environment. 1. 

Endocrine changes particularly affecting migration and maturation. Special 

Publication of the International Commission for the Northwest Atlantic Fisheries 

6, 691–715. 

Yoneda, M. & Wright, P. J. (2004). Temporal and spatial variation in reproductive 

investment of Atlantic cod Gadus morhua in the northern North Sea and 

Scottish west coast. Marine Ecology Progress Series 276, 237–248. 



Electronic References 

ICES (2004). Report of the Baltic fisheries assessment working group. International 

Council for the Exploration of the Sea C.M. 2004/ACFM: 22. Available at: 

www.ices.dk 

Kjesbu, O. S., Hunter, J. R. & Witthames, P. R. (Eds) (2003). Report of the working 

group on modern methods to assess maturity and fecundity in warm- and coldwater 

fish and squids. Fisken og Havet (Fisket Havet), 12. Available at: 

www.imr.no 

Rochet, M. J. (2000a). Spatial and temporal patterns in age and size at maturity and 

spawning stock biomass of North Sea gadoids. International Council for the 

Exploration of the Sea C.M. 2000/N: 26. Available at: www.ices.dk 

Svedäng, H., Svensson A. & Hagberg, J. (2003). Differences in technical fishing regulations 

between the Sound and Kattegat: marked effects on abundance and size 

distribution of dominant demersal fish species. International Council for the 

Exploration of the Sea C.M. 2003/Z: 01. Available at: www.ices.dk 


ICES Journal of Marine Science, 63: 485e492 (2006) 

doi:10.1016/j.icesjms.2005.09.001 

Histological analysis invalidates macroscopically determined 

maturity ogives of the Kattegat cod (Gadus morhua) 

and suggests new proxies for estimating maturity 

status of individual fish 

F. Vitale, H. Svedäng, and M. Cardinale 

Vitale, F., Svedäng, H., and Cardinale, M. 2006. Histological analysis invalidates macroscopically 

determined maturity ogives of the Kattegat cod (Gadus morhua) and suggests 

new proxies for estimating maturity status of individual fish. e ICES Journal of Marine 

Science, 63: 485e492. 

Assessment and management of fish populations currently rely on correct estimation of the 

spawning-stock biomass (SSB), which is based on accurate maturity ogives of the population. 

Although maturity ogives are usually calculated through macroscopic evaluation of the 

gonads, histology is generally considered to be more accurate. Here we show that the macroscopic 

analysis consistently overestimates the proportion of mature females for all age 

classes in Kattegat cod. The resulting bias showed minimum values for all age classes about 

a month before the spawning season. Consequently, estimation of the incidence of maturation 

in females several months before or after the spawning season can only be accurate 

using histological techniques. Further, the observed bias was used to reconstruct a historical 

data set of maturity ogives of Kattegat cod. The results showed that female spawning biomass 

(FSB) might have been overestimated by up to 35%. However, as histological analysis 

is considered a laborious procedure, proxies of maturity status were sought. It was indicated 

that the gonadosomatic and hepatosomatic indices may serve as robust proxies for discriminating 

mature females from immature, thus greatly enhancing the accuracy of the macroscopic 

maturity evaluation of cod gonads when histological analysis is lacking. 

Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. 

Keywords: GSI, HSI, Kattegat cod, maturity ogives, SSB, stock assessment, tree model. 

Received 16 March 2005; accepted 14 September 2005. 

F. Vitale, H. Svedäng, and M. Cardinale: Swedish Board of Fisheries, PO Box 4, 453 21 

Lysekil, Sweden. Correspondence to F. Vitale: tel: C46 0523 18743; fax: C46 0523 

13977; e-mail: francesca.vitale@fiskeriverket.se. 

Introduction 

Currently, a total allowable catch (TAC) system is the principal 

instrument to control stock exploitation levels for 

Northeast Atlantic commercial fish stocks (ICES, 2005a). 

In this context, the biomass of reproducing fish (i.e. spawning-stock 

biomass, SSB) is used as one of the reference 

points (in concert with the level of fishing mortality) to 

evaluate the status of an exploited stock and to establish future 

harvest levels. In order to establish TACs, fishery biologists 

usually use age-structured models to estimate SSB. 

These models include landings statistics and catch rates 

by age class, fishing effort, survey data, and species-specific 

biological parameters such as natural mortality, weight, and 

proportion of mature individuals at age (Pelletier and Laurec, 

1992). Therefore, the proportion of mature fish of all 

assessed age classes, usually defined as maturity ogives, 

is a crucial variable in the SSB estimation. Errors in estimating 

maturity ogives will lead to spurious SSB estimates, 

distorting the relationship between stock and recruitment 

(Murawski et al., 2001), and thereby increasing the variability 

of assessment results. This is especially problematic 

at low levels of SSB, because the precision in assessment 

projections is usually reduced at low stock levels. 

Cod in the Kattegat are currently assessed as a separate 

stock. Based on all the available information on SSB and 

fishing mortality, the stock is at present considered severely 

depleted (ICES, 2005b), the effect of a prolonged period of 

high fishing pressure (Svedäng and Bardon, 2003; Cardinale 

and Svedäng, 2004). According to the ICES assessment 

in 2005, the Kattegat cod stock has been estimated 

to be at its lowest levels since 1971 and around 95% of 

1054-3139/$32.00 Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.

486 F. Vitale et al. 

the spawning individuals belong to the first four age classes. 

Therefore, enhanced accuracy and precision in biological 

data used for stock assessment are of crucial 

importance. 

For Kattegat cod, maturity ogives are estimated using individual 

fish data collected during the first quarter International 

Bottom Trawl Surveys (IBTS) on board the Swedish 

research vessel ‘‘Argos’’. In order to determine the individual 

stage of sexual maturation, visual (macroscopic) staging 

of reproductive organs is regularly applied. In particular, 

maturity stage of cod is currently evaluated using a fourstage 

scale (Table 1a), in which each gonad is judged by visual 

analysis of external features. However, the subjectivity 

and ambiguity of the visual inspection method may lead to 

severe misclassifications of fish reproductive status. Several 

studies on other cod stocks have shown that histological 

analysis of gonadal development is the most accurate methodology 

to determine the individual stage of sexual maturation, 

exhibiting more consistent results than visual staging 

of reproductive organs (Murua and Motos, 1998; Saborido-Rey 

and Junquera, 1998; Kjesbu et al., 2003; Tomkiewicz 

et al., 2003). 

In this study, visual staging of sexual maturation of Kattegat 

cod was evaluated in concert with the newly introduced 

and validated histological analysis of reproductive 

organs (Vitale et al., 2005). By assuming that histological 

examinations accurately represent the reproductive status 

of individual fish, estimates of the deviation (or error) in using 

visual determination of maturity stage were obtained. 

Because misclassifications using macroscopic analysis are 

even more serious when gonads are sampled several 

months prior to spawning (Kjesbu, 1991), we also analysed 

the deviation within each age class on a monthly basis. This 

result will assist planning of surveys used to estimate maturity 

ogives of Kattegat cod. 

We also include the results of histological analyses in 

cod assessment, to estimate the possible error in SSB determined 

through visual inspection of gonads. In order to reconstruct 

the time-series of proportion of mature ogives 

in each age class and evaluate the effects of the use of incorrect 

maturity ogives on SSB estimation in the past, estimates 

of deviation in visual staging of reproductive status 

were applied to the historical data set of maturity ogives 

(ICES, 2005a). In addition, studies on Northeast Arctic 

cod showed strong arguments for using female-only spawning 

biomass (FSB), rather than SSB, as the independent 

variable in stock-recruitment models (ICES, 2004), suggesting 

that FSB would give a better index of reproductive 

potential than SSB. For these reasons, we considered only 

the female contribution to the reproductive potential of 

the cod stock. Finally, histological analyses are an expensive, 

laborious, and time-consuming procedure and put 

a limit on the number of samples that can be analysed. 

Therefore, we explored all available variables in searching 

for proxies for estimating maturity status of individual fish. 

These alternative criteria may be a way to distinguish 

mature from immature females when histological analysis 

cannot be performed. 

Material and methods 

Data collection 

Cod in the Kattegat start maturing in November, peaking in 

FebruaryeMarch, then enter the spent stage (Vitale et al., 

2005). In order to obtain a good temporal resolution, fish 

sampling took place on a monthly basis, from September 

2002 to May 2003 (with the exception of April 2003) 

both in the Kattegat and the Sound (ICES Subdivisions 

21 and 23, respectively), and from December 2003 to February 

2004 only in the Kattegat. Female cod were caught by 

commercial fishing vessels and by the Swedish research 

vessel ‘‘Argos’’. Sample locations and sample sizes are 

shown in Figure 1 and Table 2, respectively. The fish 

were processed immediately after capture. For each fish, total 

length (TL) to 0.5 cm below, total wet weight (TW), gonad 

(GoW) and liver weight (LW) were measured to the 

nearest 0.1 g. The length ranged from 25 cm to 85 cm. Gonads 

were weighed and stored in phosphate-buffered formaldehyde 

3.6% for 14 days before further preparation for 

histological analysis. Fixed sections of ovary were dehydrated 

through ascending concentrations of ethanol, embedded 

through ascending concentrations of historesin, and 

eventually polymerized into historesin blocks at 4(C. 

Transverse sections of 2e5 mm thick were dried at 60(C 

and stained with toluidine blue. 

For each fish, we estimated Fulton’s condition factor 

(CF) based on total weight as 

CFZTW!TL ÿ3 !100: 

Gonadosomatic (GSI) and hepatosomatic (HSI) indices 

were calculated according to the following equations: 

GSIZGoW!TW ÿ1 !100 

HSIZLW!TW ÿ1 !100: 

Otoliths (sagittae) were removed from all cod sampled 

and transversely sectioned through the centre of the nucleus 

for age reading. Fish were grouped into four age classes: 2, 

3, 4, and 5C. The oldest age group included all cod aged 5 

or more. 

Sexual maturity of each cod was classified according to 

a four-stage macroscopic scale (Table 1a) used in the 

IBTS (ICES, 1999), as well using a microscopic scale, 

based on histological analysis (Table 1b; Vitale et al., 

2005). The latter classification scheme is a seven-stage 

scale that underlines the importance of the passage from endogenous 

to exogenous vitellogenesis, which coincides 

with the beginning of yolk production in the oocytes. These

Histological analysis invalidates maturity ogive of the Kattegat cod 

487 

Table 1. (a) Macroscopic scale from the manual for the International 

Bottom Surveys (IBTS) and (b) histological scale from 

Vitale et al. (2005). 

(a) 

Virgin 

Maturing 

Spawning 

Spent 

(b) 

Immature 

Previtellogenic 

growth 

Endogenous 

vitellogenesis 

Exogenous 

vitellogenesis 

Ovaries small, elongated, whitish, 

translucent. No sign of development 

Development has obviously started, eggs are 

becoming larger and the ovaries are filling 

more and more of the body cavity, but eggs 

cannot be extruded with only moderate 

pressure 

Will extrude eggs under moderate pressure to 

advanced stage of extruding eggs freely with 

some eggs still in the gonad 

Ovaries shrunken with few residual eggs and 

much slime. Resting condition, firm, not 

translucent, showing no development 

Small oocytes with a dense basophilic 

cytoplasm, a central nucleus, and few large 

nucleoli around their edge (perinucleolar 

stage). Oogonia are always present but they 

might not be visible 

The nucleus increases in size and multiple 

nucleoli are formed. A weakly stained area 

called ‘‘circumnuclear ring’’ (CNR) is also 

present 

The circumnuclear ring moves towards the 

outer part of the cell and gradually 

disintegrates, while the spherical cortical 

alveoli appear in the superficial half of the 

cytoplasm. No yolk granules present yet 

Presence of yolk granules. The nucleus, still 

centrally located, becomes irregular. The 

occurrence of this stage means that the 

maturation process is in progress, and under 

normal conditions, the individual will 

develop within the current spawning season 

Final maturation The chorion becomes thicker, the nucleus 

migrates towards the animal pole and the 

hydration process occurs 

Spent 

Post-ovulatory follicles (POFs), after oocytes 

release into the lumen, are distinguishable 

Resting Oocytes in stages 1 and 2. Some 

post-ovulatory structures, still present, show 

signs of previous spawning 

two stages are hardly discernible by the naked eye and consequently 

the most susceptible to misclassification. Burton 

(1994) recorded fish with arrested maturation at endogenous 

vitellogenesis. Therefore, finding ovaries with oocytes in 

this phase of development (stage 3) does not necessarily imply 

that the fish will be active reproductively during the 

forthcoming season. Consequently, only fish containing 

oocytes which had developed up to the exogenous vitellogenesis 

phase (stage 4 and onwards) were considered sexually 

mature, i.e. they are likely to spawn in the forthcoming 

Latitude ºN 

58 

57 

56 

Argos samples 

Commercial samples 

55 

10 11 12 13 

Longitude ºE 

Figure 1. Sample locations in the Kattegat and Sound. 

season. All cod without yolk granules, i.e. from stage 1 to 3, 

were classified as immature and judged to remain as such in 

the forthcoming spawning season. 

Data analysis 

Comparison between visual inspection and histological 

analysis of female gonads 

Fish were classified as either immature or mature both by 

visual and histological inspection of the gonads. The maturity 

status of each was transformed into a binary form, taking 

the value ‘‘0’’ for immature and ‘‘1’’ for mature or 

maturing individuals both in the histological and the macroscopic 

staging of gonads. Owing to the expected binominal 

distribution of data, we used a GLMz (Generalized Linear 

Model) with binomial distribution and a logit link function 

to test for statistical differences between the proportions of 

mature against immature individuals for each age class estimated 

by the two methods (i.e. visual inspection and histological 

analysis of the gonads). The test was based on the 

Wald statistic, which is founded on the binomial distribution 

and analogous to the F-statistics of GLM (General Linear 

Model). 

The deviations in the proportion of mature individuals 

per age class, resulting from the comparisons between 

visual and histological inspection of the gonads, were


Table 2. (top panel) Number of samples histologically analysed per month in 2003e2004 within each age class and (bottom panel) RV 

‘‘Argos’’ samples from IBTS collected in JanuaryeMarch for each age class and used for macroscopic estimation of the maturity ogives 

within the Baltic Assessment working group. 

Age Sep Oct Nov Dec Jan Feb March May 

2 18 22 22 31 31 85 30 24 

3 11 31 24 49 76 58 13 10 

4 1 11 13 16 23 20 4 6 

5C 1 6 3 8 17 2 2 

Total 30 65 65 99 138 180 49 42 

Age 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 

2 69 55 41 68 45 87 100 42 95 55 77 57 47 70 20 

3 20 17 96 38 32 67 52 88 32 79 60 75 48 12 74 

4 15 10 9 68 11 56 25 18 39 9 34 28 60 7 17 

5C 9 7 6 8 25 14 22 15 19 18 10 11 27 7 19 

Total 113 89 152 182 113 224 199 163 185 161 181 171 182 96 130 

considered as an estimate of the bias or deviation from the 

visual inspection method. The relative bias per age class 

(RB i) was defined by the following equation: 

RB i ZðMVI i ÿ MHA i Þ=MHA i ; 

where MVI and MHA are the percentage of mature fish according 

to visual inspection and histological analysis, 

respectively. 

We also estimated the absolute bias resulting from the 

comparison between histological analysis and visual inspection 

of gonads for each age class on a monthly basis. 

The absolute bias was calculated as 

AB i ZMVI i ÿ MHA i : 

Re-estimation of historical SSB of the Kattegat cod stock 

Maturity ogives represent the proportion of mature or maturing 

females within each age class and were calculated as: 

MO i ZMF i =N i ; 

where MO i is the maturity ogive, MF i is the number of mature 

or maturing females, and N i is the total number of females 

at age i. Because historical maturity ogives (ICES, 

2005b) were estimated from cod sampled between January 

and March, the RB i per age class to be used for reconstructing 

historical maturity ogives was calculated using Januarye 

March data only. Between 1971 and 1990, ICES considered 

the proportion of mature individuals as constant. 

The estimated RB i per age class was applied on the historical 

data set of maturity ogives as follows: 

CMO i ZHMO i =ð1CRB i Þ; 

where CMO i and HMO i are the corrected and the historical 

maturity ogives for age i, respectively. RB i for individuals 

older than 5 years was assumed equal to those estimated for 

5-year-old individuals. The corrected time-series (1971e 

2004) of female maturity ogives has been used for reestimating 

FSB of the Kattegat cod stock, and this timeseries 

on FSB is compared with previous estimation of 

FSB (ICES, 2005b). 

Alternative methods of assessing maturity: a tree-model 

application 

Owing to the non-linear nature of the relation between maturity 

status of an individual fish with many morphological and 

physiological state variables, we used a tree-regression model 

(S-PLUS, 2000) for predicting the best combination of variables 

to determine the maturity stage of an individual fish in 

the absence of histological data. Regression tree models are 

based on a recursive partitioning approach, which uses a set 

of predictor variables (x i ) to generate a single response variable 

( y i ) [see Cardinale and Arrhenius (2004) for an application 

of the model in fisheries and for statistical details]. In this 

study, the predictors were area (Kattegat, Sound), month 

(SeptembereMay), fish length (25e85 cm), fish age 

(2e5C), MVI (mature, immature), GSI, HSI, and CF, while 

MHA (mature, immature) was the response. In the tree-model 

diagram the predicted response (MHA) is at the bottom of the 

tree and the predictors come into the system at each node of 

the tree. The top node contains the entire samples. Each of the 

nodes beneath contains a subset of the sample in the nodes 

directly above it. However, a tree model may be more complex 

than necessary to describe the data. Therefore, after the 

initial tree model has been built, a ‘‘tree-pruning approach’’ 

(for optimizing the number of correct predictions) and 

a ‘‘shrink approach’’ (for optimizing internal deviance) are 

performed. Those two functions assess the degree to which 

a tree can be simplified (i.e. parsimony) without sacrificing 

goodness-of-fit. The pruning function achieves parsimonious


489 

state of the model by reducing the number of nodes and the 

number of variables used in the initial model, whereas the 

shrink function contracts each node towards its parents. 

This is analogous to a stepwise procedure, where only variables 

that are significantly contributing to explain the null variance 

are included in the model (S-PLUS, 2000). Pruning can 

be carried out as guided by the cost-complexity criterion or 

simply by stating the desired number of final classes. For 

each specific set of variables, we first constructed a so-called 

complex model that used all variables and possible nodes. 

This will generate a misclassification diagram where misclassification 

(or deviance) rates are indices of the goodness-of-fit 

of the model and analogous to the r 2 of 

regression models. Misclassification decreases with increasing 

number of nodes and then levels off. The number of nodes 

where misclassification levelled off was used to establish the 

desired number of final classes (i.e. pruning approach) in the 

final model, i.e. the degree a tree can be simplified without 

sacrificing goodness-of-fit. Misclassification rates were 

also used to compare between models. 

Two different models were tested. The first model (FDC, 

fishery-dependent complex model) used fishery-dependent 

individual information (i.e. area and month of catch, fish 

length, and age) while the second model (FIC, fishery-independent 

complex model) considered fishery-independent 

(i.e. survey data) individual information (area and month 

of catch, fish length, and age, MVI, GSI, HSI, and CF) as 

predictors of maturity stage. The fishery-dependent simplified 

model (FDS) and the fishery-independent simplified 

model (FIS) are the two simplified models resulting from 

the initial FDC and FIC models, respectively. Model validation 

was performed using a k-fold cross-validation procedure 

(see Efron and Tibshirani, 1995). This consists of 

randomly dividing the data set into two parts, training 

and test data sets. The proportion of tested individuals vs. 

the total number of samples used here was 1:3 (445 individuals 

for training and 222 for testing). Hence, the tree models 

were fitted to the training data set, and thereafter the 

fitted tree model was used to predict maturity stage (immature, 

mature) of the individuals included in the test data set. 

Results 

Comparison between visual inspection 

and histological analysis 

There were no statistical differences in the specific RB i per 

age class between the two years 2003 and 2004 (Generalized 

Linear Model with binomial distribution; p Z 0.18; 

n Z 668). Therefore, the 2003 and 2004 data were merged 

in the successive analysis. The proportion of mature against 

immature individuals was statistically different for the two 

methods (i.e. visual inspection and histological analysis of 

the gonads) (Wald statistic Z 74.7; p ! 0.001). According 

to visual inspection of the gonads, the proportions of mature 

fish increased from 39% in age class 2 to 100% in 

age class 5C (Figure 2). In contrast, the histological 

analysis indicated that the proportion of mature fish increased 

from 24% to 92% for the same age interval. In 

other words, the visual inspection method consistently 

overestimated the proportion of mature individuals for all 

age classes (Figure 2), with RB i increasing with decreasing 

age of the fish. 

Older cod showed greater monthly variability in bias 

than younger ones (Figure 3). On the other hand, all age 

classes showed a convergence towards minimum bias in 

January (Figure 3). 

Re-estimation of historical FSB of the Kattegat 

cod stock 

As a result of the overestimation of the proportion of mature 

individuals attributable to the inaccuracies of visual 

staging, the re-estimated FSB was by definition always lower 

than the historical FSB of Kattegat cod (Figure 4a). The 

re-estimated FSB showed an overestimation that varied between 

21% and 35% of the historical FSB. The difference 

between the re-estimated FSB and the historical FSB of 

Kattegat cod significantly increases (r 2 Z 0.31; p ! 0.05; 

n Z 34) with increasing proportion of first spawners in 

the maturity fraction of the population (Figure 4b). This 

phenomenon was due to the observed increase in RB i 

with decreasing age of the fish (see Figure 2). 

Alternative methods in assessing maturity: 

a tree-model application 

Table 3 shows the results for different regression tree models 

considered for classification of maturity stage of an individual 

fish. Numbers represent the percentages of 

misclassification, i.e. the error in the models in relation to 

the histological classification considered as the true gonadal 

status. Hereafter, we will only refer to the results relative to 

the testing models, i.e. the predictive power of the tree 

model for estimating maturity stage of an individual fish after 

a k-fold cross-validation procedure. 

1.0 

0.8 

0.6 

0.4 

0.2 

0.0 

Macroscopic 

Histological 

2 3 4 5+ 

Figure 2. Comparison between histological and visual staging of 

the gonads. Bars represent standard errors. RB i is the relative 

bias per age class. 

RB i 

1.0 

0.8 

0.6 

0.4 

0.2 

0.0 

RB i ( )


AB i 

1.00 

0.75 

0.50 

0.25 

2 

3 

4 

5+ 

Median (2-5+) 

Table 3. Results for different tree models considered. All numbers 

are percentages and represent the misclassification rates within 

each age class and the total misclassification rate of the model. 

Misclassification rate is a proxy of the goodness-of-fit and the 

equivalent of r 2 for a regression model. The number of nodes indicate 

the complexity of the model and is associated with the number 

of variables used by the model. (Acronyms for models are FDC: 

fishery-dependent complex; FDS: fishery-dependent simplified; 

FIC: fishery-independent complex, and FIS: fishery-independent 

simplified.) n is the number of individuals. 

In both initial complex models, i.e. FDC and FIC, a reduction 

in the number of nodes could be obtained without 

significantly reducing the predictability of the model (data 

not shown). The total misclassification rate of the model 

was higher in FDC and FIC than for the corresponding simplified 

models (FDS and FIS). Moreover, while FDC, FDS, 

and FIC used all available variables, the only variables included 

in the FIS model were GSI and HSI. FIS has the 

minimum number of nodes and the lowest misclassification 

rate. Hence, the use of GSI and HSI significantly increases 

a 

b 

0.00 

20000 

18000 

16000 

14000 

12000 

10000 

8000 

6000 

4000 

2000 

0 

1.0 

0.8 

0.6 

0.4 

0.2 

Sept Oct Nov Dec Jan Feb Mar Apr 

1971 

1973 

Month 

Figure 3. Monthly trend of the absolute bias (AB i ) within age 

classes. 

Macroscopical FSB 

Histological FSB 

RB i 

1975 

1977 

1979 

1981 

1983 

1985 

1987 

1989 

1991 

1993 

1995 

1997 

1999 

2001 

2003 

0.0 

0 10 20 30 40 

RB i ( ) 

Figure 4. (a) Relative bias (RB i ) between the re-estimated (through 

histological analysis) and the historical values of FSB. (b) Relationship 

between RB i and the proportion of first spawners in the 

stock. 

50 

40 

30 

20 

10 

0 

RB i ( ) 

Age FDC FDS FIC FIS 

2 23.3 18.6 1.2 2.3 

3 31.9 33.3 16.7 12.5 

4 33.3 20.8 12.5 12.5 

5C 16.7 50 16.7 16.7 

Total 27.3 26.3 9.3 8.2 

Nodes 55 11 22 4 

n 222 222 222 222 

the power to predict maturity stage of an individual fish and 

led, by comparison, to the most parsimonious model (i.e. 

reduced number of nodes). 

Discussion 

The purpose of this study was to evaluate both existing maturity 

staging methods and the importance of implementing 

accurate and objective maturity determinations, as these are 

fundamental to estimating spawning-stock biomass (SSB). 

This is especially relevant for assessment and management 

of overexploited populations such as the Kattegat cod 

stock. 

The use of the inaccurate visual inspection method for 

determining the proportion of mature cod leads to an overestimation 

of the size of the reproductive part of the stock, 

and, perhaps more important, to an increased and unaccounted 

uncertainty in stock assessment. The use of histology 

in maturity studies has become more and more 

widespread as it is has become more consistent and reliable 

(Kjesbu et al., 2003; Murua et al., 2003; Tomkiewicz et al., 

2003). Here we have shown that visual staging of maturation 

tends to overestimate the gonad maturity status in Kattegat 

female cod. The decreasing trend in relative bias with 

increasing age highlights the fact that the overestimation is 

more severe for first spawners. 

Moreover, the visual staging method puts some constraints 

on the time when maturity surveys should be performed. 

Some features of the gonads are not easily 

discriminated by the naked eye during certain phases of 

the developmental process. In particular, visual inspection 

of the gonads and interpretation of gonad development 

have been considered as complicated and untrustworthy before 

the spawning season (Kjesbu, 1991; Saborido-Rey and


491 

Junquera, 1998). Furthermore, when spent gonads progress 

to the spent/recovering phase after the spawning season, 

there might be a bias towards classifying them as immature. 

This is confirmed by the monthly bias trend, which illustrates 

how the risk of misjudgement, when a visual inspection 

is used is influenced by the time of year at which 

gonads are collected. Hence, the reliability of visual judgement 

is dependent on the time of sampling, suggesting that 

the best time for performing maturity surveys, in order to 

obtain reliable results and to reduce the risk of misjudgement, 

is about a month before the spawning season. In 

the case of the Kattegat cod, this corresponds to January. 

Consequently, identification of mature/maturing females 

several months before or after the spawning season can 

only be accurately obtained by histological techniques. 

The comparison between the FSB estimated according to 

histologically corrected maturity ogives, and the historical 

FSB derived from macroscopically estimated maturity 

ogives (ICES, 2005b), revealed a consistent overestimation 

of the FSB. Moreover, the degree of the overestimation was 

significantly positively related to the proportion of first 

spawners in the population. Considering that the SSB of exploited 

stocks continues to decrease, and the proportion of 

first spawners usually increases as the fraction of older cod 

becomes smaller, it is valuable to minimize the bias in SSB 

estimates. Estimating the spawning fraction by histological 

analysis is a robust way of obtaining accurate estimates of 

the spawning-stock biomass of exploited stocks. Histology 

has the clear advantage of allowing detailed recording of 

the reproductive development occurring in ovarian cells, 

leading to unambiguous interpretation of maturity status 

of an individual fish. 

Owing to the energetically expensive processes of maturation 

and reproduction, considerable energy must be stored 

in individual fish before reproduction. In gadoids such as 

cod, lipid energy is stored primarily in the liver. Marshall 

et al. (1999) found a highly significant, linear relationship 

between the total number of eggs produced and total lipid 

energy in Barents Sea cod. This makes liver weight, and, 

consequently, the hepatosomatic index (HSI) a rapid and 

inexpensive measure of spawner quality (Lambert and Dutil, 

2000). 

According to our results, estimates of GSI and HSI allow 

the ongoing maturation process in Kattegat cod to be 

tracked. In fact the model considering only GSI and HSI 

had a very high classification success (around 95% of the 

individuals analysed), making them useful in detailed reproductive 

studies. In contrast, models including macroscopic 

evaluation criteria (MVI), TL, and CF had larger 

misclassification rates, so these variables were excluded 

from the final model. These results partially overlap with 

those from previous studies on Baltic cod (Tomkiewicz 

et al., 2003), in which TL and GSI supported stage definitions, 

while CF and HSI were of little use for this purpose. 

The contrasting results on the importance of HSI might be 

due to different feeding conditions experienced by the two 

stocks. Also, the more prolonged spawning season in the 

Baltic, continuing for more than six months, naturally leads 

to a higher temporal variation in gonad development within 

the stock. Maturing Baltic cod that will eventually spawn 

during the current spawning season may differ significantly 

in energetic status at a certain time during the spawning 

season, making indices relating to energetic status inappropriate 

for predicting the outcome of the maturation process. 

In conclusion, this study was the first attempt to apply 

histological analyses to the assessment of a cod stock and 

to estimate the possible error in FSB estimation derived 

from the use of visual inspection of the gonads. The results 

clearly indicate that visual inspection of the gonads consistently 

overestimated the reproductive potential of the stock. 

This emphasizes the need to find proxies for minimizing the 

error in estimating maturity ogives and consequently in assessing 

the population when histological analysis is not feasible. 

Therefore, HSI and GSI represent potentially reliable 

indices of maturity stage useful to increase precision of visual 

maturity evaluation of Kattegat cod females. Improving 

the capability of separating mature from immature 

individuals, in order to obtain a more correct estimate of 

SSB, is fundamental to accurate assessment and management 

of the stock. Recognition of this concept is important 

in the context of attaining a sustainable fishery, and ultimately, 

for the recovery of overexploited fish stocks. 

References 

Burton, M. P. M. 1994. A critical period for nutritional control of 

early gametogenesis in female winter flounder Pleuronectes 

americanus (Pisces, Teleostei). Journal of Zoology, 33: 

405e415. 

Cardinale, M., and Arrhenius, F. 2004. Using otolith weight to estimate 

the age of haddock (Melanogrammus aeglefinus): a tree 

model application. Journal of Applied Ichthyology, 20: 470e475. 

Cardinale, M., and Svedäng, H. 2004. Modelling recruitment and 

abundance of Atlantic cod, Gadus morhua, in the Kattegat-eastern 

Skagerrak (North Sea): evidence of severe depletion due to 

a prolonged period of high fishing pressure. Fisheries Research, 

69: 263e282. 

Efron, B., and Tibshirani, R.J. 1995. Cross-validation and the bootstrap: 

estimating the error rate of the predicting rule. Technical 

Report, University of Toronto. 

ICES. 1999. Manual for International Bottom Trawl Surveys. ICES 

CM:1999/D2; Addendum 2. 

ICES. 2004. Report of the study group on growth, maturity and 

condition in stock projections. ICES CM 2004/D:02. 

ICES. 2005a. Report of the ICES Advisory Committee on fishery 

management. ICES CM 2005/ACFM:12. 

ICES. 2005b. Report of the Baltic fisheries assessment working 

group. ICES CM 2004/ACFM:19. 

Kjesbu, O. S. 1991. A simple method for determining the maturity 

stages of northeast Arctic cod (Gadus morhua L.) by in vitro examinations 

of oocytes. Sarsia, 754: 335e338. 

Kjesbu, O. S., Hunter, J. R., and Witthames, P. R. 2003. Report of 

the working group on modern methods to assess maturity and fecundity 

in warm- and cold-water fish and squids. Fisken og 

Havet [Fisken Havet], 12: 1e140.


Lambert, Y., and Dutil, J-D. 2000. Energetic consequences of reproduction 

in Atlantic cod in relation to spawning level of somatic 

energy reserves. Canadian Journal of Fisheries and 

Aquatic Science, 57: 815e825. 

Marshall, T., Yaragina, N. A., Lambert, Y., and Kjesbu, O. S. 1999. 

Total lipid energy as proxy for total egg production by fish 

stocks. Nature, 402: 288e290. 

Murawski, S. A., Rago, P. J., and Trippel, E. A. 2001. Impacts of 

demographic variation in spawning characteristics on reference 

points for fishery management. ICES Journal of Marine Science, 

58: 1002e1014. 

Murua, H., and Motos, L. 1998. Reproductive modality and batch 

fecundity of the European hake (Merluccius merluccius) in the 

Bay of Biscay. Reports of California Cooperative Oceanic Fisheries 

Investigations, 39: 196e203. 

Murua, H., Kraus, G., Saborido-Rey, F., Witthames, P. R., Thorsen, 

A., and Junquera, S. 2003. Procedures to estimate fecundity of 

marine fish species in relation to their reproductive strategy. 

Journal of Northwest Atlantic Fishery Science, 33: 33e54. 

Pelletier, D., and Laurec, A. 1992. Management under uncertainty: 

defining strategies for reducing overexploitation. ICES Journal 

of Marine Science, 49: 389e401. 

Saborido-Rey, F., and Junquera, S. 1998. Histological assessment 

of variations in sexual maturity of cod (Gadus morhua) at the 

Flemish Cap (north-west Atlantic). ICES Journal of Marine 

Science, 55: 515e521. 

S-PLUS. 2000. Guide to Statistics. Data Analysis Products Division, 

vol. 1. MathSoft, Seattle, WA. 

Svedäng, H., and Bardon, G. 2003. Spatial and temporal aspects of 

the decline in cod (Gadus morhua L.) abundance in the Kattegat 

and eastern Skagerrak. ICES Journal of Marine Science, 60: 

32e37. 

Tomkiewicz, J., Tybjerg, L., and Jespersen, Å. 2003. Micro- and 

macroscopic characteristic to stage gonadal maturation of female 

Baltic cod. Journal of Fish Biology, 62: 253e275. 

Vitale, F., Cardinale, M., and Svedäng, H. 2005. Evaluation of 

temporal development of ovaries in cod (Gadus morhua) from 

the Sound and Kattegat. Journal of Fish Biology, 67: 669e683.

III

Potential fecundity of Kattegat cod (Gadus morhua) in relation to prespawning 

body size and condition 

F.Vitale 1 , A. Thorsen 2 and O. S. Kjesbu 2 

1 Swedish Board of Fisheries, Institute of Marine Research, PO Box 4, 45321 Lysekil, Sweden 

2 Institute of Marine Research, PO Box 1870, Nordnes, 5817 Bergen, Norway 

The usefulness of spawning stock biomass (SSB) as a proxy for stock reproductive potential in stockrecruitment 

models has been increasingly undermined. Many investigations have focused on 

explaining the observed variability in fecundity using fish size and various indices of individual 

condition. In this study, the relationship between fish size, maternal condition and fecundity was 

investigated for Kattegat cod during the pre-spawning phase. Results show that in Kattegat cod, just 

prior the onset of spawning, fish length explains the largest part of fecundity variability. Fulton’s K 

and HSI measured just before spawning, did not substantially increase the explained variation in 

fecundity. These finding may corroborate the hypothesis that the energy reserves have to be measured 

at an earlier stage, i.e. near the start of vitellogenesis, for determining their influence on egg 

production. Comparisons between Kattegat and North East Arctic cod stock (NEAC) evidenced that 

females in the Kattegat produce more oocytes (higher size-specific fecundity), although smaller in 

size, per unit of body mass at a given length than NEAC females. These differences may reflect the 

fact that the sampled NEAC was closer to spawning than the Kattegat cod, but the adaptations to 

different environmental conditions and different exploitation rate experienced by the two stocks may 

also explain the observed divergences. These results emphasize that SSB may fail to accurately 

account for the length and condition effects on reproductive potential of the stock. Consequently there 

is a risk of overestimating the reproductive potential when the stock is dominated by small individuals 

as in the case of Kattegat cod stock. A monitoring program based on direct measurement of Kattegat 

cod stock fecundity is therefore strongly suggested in order to improve the assessment of this stock 

and ensure a more sounded management. 

Introduction 

Estimation of individual reproductive investment is central in many types of fish biology 

studies. Reproductive features, namely spawners’ biomass, sex ratio, proportion of mature 

females at age, fecundity, egg viability and hatching success, have a large influence on the 

reproductive potential of a fish stock and vary among species, stocks, geographical areas and 

years (Kjesbu et al., 2007; Marshall et al. 1998; Lambert et al., 2005). 

Estimates of individual potential fecundity (i.e. the number of vitellogenic oocytes in the prespawning 

ovary) are relatively easily obtained in determinate spawners, such as cod (Gadus 

morhua), for which the standing stock of oocytes that will develop is fixed prior to the onset 

of spawning with no further oocyte recruitment later during the spawning season (Kjesbu et 

1

al, 1991). Despite the implementation of manageable methods for direct measurements of 

individual fecundity (Thorsen and Kjesbu, 2001; Friedland et al., 2005; Klibansky and 

Juanes, 2007) the collection of fecundity data has yet to be formally incorporated into fishery 

management. 

Nonetheless, most of the stock-recruitment models, currently used in stock assessment, 

assume proportionality between the spawning stock biomass (SSB) and the total annual egg 

production. Therefore SSB, estimated as the aggregated weight of mature fish in a stock, is 

conventionally used as proxy for the stock reproductive potential. This relationship has, 

however, been increasingly undermined for many cod stocks (Marshall et al, 1998; Marshall 

et al, 1999; Kraus et al., 2002; Köster et al., 2003a; Marshall et al., 2003), as estimates of 

SSB neglect the fluctuations in several important reproductive parameters, such as parental 

age, condition and spawning experience (MacKenzie et al., 1998; Trippel, 1999; Marshall et 

al., 2003; Köster et al., 2003b; Marshall et al., 2006). 

Many studies have found a significant relationship between individual egg production and 

body size (Kjesbu et al., 1998; Marteinsdottir and Begg, 2002; Lambert et al., 2005). 

However the examination of size-specific fecundity in cod has shown a very large variability 

between and within stocks (Kjesbu et al., 1991; Lambert et al., 2003; Lambert et al., 2005). 

The observed variability can be the result of short-term response related to the nutritional 

status of the fish, food availability, growth and/or environmental temperature (Lambert et al., 

2003). Differences in fecundity might also be associated with different life history responses 

of population resulting in different age/size at maturity, reproductive effort, egg size and 

survival (Roff, 2002). 

Several investigations have focussed on explaining the observed variability in fecundity using 

various indices of individual condition (Kjesbu et al., 1998; Marshall et al., 1999; 

Marteinsdottir and Begg, 2002; Blanchard et al., 2003). Reproduction in fact requires a 

substantial energetic investment, which needs to be traded off against growth and metabolic 

maintenance. Consequently, the individual energetic state influences egg production and 

individuals may skip spawning as a consequence of low condition (Burton and Idler, 1987; 

Rideout et al., 2000; Rideout et al., 2005). 

Furthermore, stock reproductive potential is affected by the size composition of the stock 

owing that large/old spawners produce more and higher quality eggs (Solemdal et al., 1995; 

Trippel, 1999; Tomkiewicz et al., 2003) and also that the number of spawning occasions 

2

within the spawning season is considerably higher for bigger females than for smaller ones 

(Parrish et al., 1986; Lambert, 1990). In addition, the fertilization rate is higher when bigger 

males are involved in the spawning act (Hutchings et al., 1999). The Kattegat cod belong to 

the cod stocks that have experienced a large decrease in abundance (>90% since 1970) due to 

a prolonged exploitation (Cardinale and Svedäng, 2004). As a result the abundance of 

spawning cod females in Kattegat has shifted towards fewer and younger age classes (ICES, 

2007) and large spawning aggregations in the southern part have disappeared (Svedäng and 

Bardon, 2003; Vitale et al., 2008). 

This study represents a first attempt to investigate fecundity patterns in the Kattegat stock, 

based on measurements of individual potential fecundity (i.e. total egg production) during 

three consecutive pre-spawning seasons (2004, 2005 and 2006). The aim is to explore the 

relationship between individual body size and potential fecundity and to investigate the ability 

of age and energy related indices in describing the observed individual potential fecundity in 

Kattegat cod. 

Additionally, the size-specific potential and relative fecundity (i.e. number of eggs/unit body 

weight) observed in Kattegat cod was compared with the North East Arctic cod (NEAC), two 

stocks occurring in different environmental conditions and experiencing two different 

exploitation patterns. Results are discussed in terms of different reproductive strategies under 

separable ecological, environmental as well as anthropogenic influences. 

Material and methods 

A total of 233 specimens were caught in Kattegat (ICES SD 21) during the pre-spawning 

season in December and January 2004, December and January 2005 and January 2006. For all 

collected fish, the total length (L) was recorded to the nearest cm, ranging between 26 and 78 

cm. Total wet weight (W), gutted weight (Wgutt), gonad weight (W G ) and liver weight (W L ) 

were also recorded. Age was determined from otoliths and ranged between 2 and 5 years. 

Subsamples of the gonads were stored in 3.6% buffered formaldehyde for a minimum of 14 

days for histology and fecundity measurements. Histological analyses (see Vitale et al., 2005) 

verified that no hydrated oocytes or ovulated eggs were present in the gonads, confirming the 

pre-spawning stage of the gonads. 

3

Individual Fulton’s somatic condition factor (K), Gonadosomatic and Hepatosomatic (HSI) 

indices were calculated, using the following formula: 

K=Wgutt*L (-3) *100 (1) 

HSI = W L * 100*W (-1) (2) 

GSI = W G * 100*W (-1) (3) 

The reliability of the exponent in the K equation was verified through annual linear 

regressions. 

The fecundity was measured using the auto-diametric fecundity method (Thorsen and Kjesbu, 

2001), which is based on the principle that the oocyte density is directly proportional to the 

oocyte diameter, linked by a power curve relationship. 

Only oocytes that were in cortical alveoli or vitellogenic stage were counted and the oocyte 

diameter (OD, defined as the average of ellipse major and minor axis) was measured for 200 

oocytes per sample. The potential fecundity (Fp) was calculated according to the formula: 

Fp= W G (g) * 2.139*10 11 * OD -2.700 (m) (4) 

within the size interval: 300 OD 735 m 

The individual relative fecundity (i.e. number of eggs/unit body mass) was calculated as: 

Fr= Fp* W (-1) (5) 

A generalized linear model (GLMZ), family gamma and log-link function, was used to test if 

there were differences in Fp between samples collected in different months and years. Fp was 

set as dependent variable, year and month as factors and L as covariate. GLMZs were run 

using SPSS software. 

To investigate the relationship between Fp and possible predictors a series of generalized 

linear models (GLMZs) with gamma response (Fp) distribution and log-link function were 

used. The model was defined accordingly: 

Fp ~ ß 1 *X 1 + ß 2 *X 2 + ß 3 *X 3 + ß 0 

4

where ß 0 is the intercept and ß 1 , ß 2 and ß 3 are the coefficients for each variable included in the 

model. 

Owing the autocorrelation between the fish size variables, L and W were never included in 

the same model. Therefore, for the first two model runs only size variables (either L or W) 

were included as predictors. In the subsequent runs, other predictors (K, HSI and age) were 

added one at a time to determine whether they explained a significant amount of variation in 

fecundity additional to that attributed to body size alone. 

The proportion of explained variation (PEV), equivalent to R 2 , for each fitted model was 

calculated as: 

PEV=(null deviance –residual deviance)/null deviance 

where null deviance is the explained variation in the response variable before adding a 

predictor while residual deviance is the variation in the response variable still not explained 

after the addition of a predictor. The statistical analyses were carried out using the r- software 

(freely downloaded at www.r-project .org/). 

Additional samples of female cod were caught at Andenes (Lofoten) during the pre-spawning 

season in early March 2003 and late February 2004 ( see Thorsen et al., 2006). The specimens 

were characterized as belonging to the North East Arctic (NEAC) cod stock by using otolith 

morphology as stock discriminating factor (Rollefsen, 1934). 

Given the large differences in size range between the Kattegat and NEAC cod samples 

(Fig.1), data were filtered and only individuals between 54 and 78 cm (34 and 41 specimens 

for the Kattegat and the NEAC stocks, respectively) were retained in order to obtain a 

comparable size interval. A GLMZ with Fp (or Fr) as dependent variable, month and year as 

factors and length as covariate was used for testing potential differences in samples from 

different months or years. No significant differences were found so data from different 

months and years in these sub-samples were combined. 

The individual potential and relative fecundity at length in the two stocks were thus explored 

and compared. Furthermore, the average OD, HSI, GSI and Fulton’s K at length was 

examined and comparisons between the stocks were made. The differences were tested using 

5

t-Test for independent samples performed using Statistica software. Levene’s test was used 

for testing the homogeneity of variances. 

Results 

The first GLMZs revealed a significant (p0.05) was detected between months. Specimens collected in different months 

were hence merged and the results from the GLMZs for different years are shown in table 1. 

Overall, fish size was able to explain the major fraction of the observed variance in fecundity 

for all the years analysed. No substantial increase in the explanatory power was observed 

when adding fish condition indices to the model built with length alone. 

Body size, specifically length more than weight (87%, 81% and 78% against 76% 73% and 

73% respectively for 2004, 2005 and 2006), was the best predictor of fecundity in all year 

examined explaining more variation, in terms of PEV. 

Neither somatic Fulton’s K nor HSI increased the explained variation in fecundity 

substantially when added to the fecundity-size (either L or W) models, although significant in 

some years. Age was not indicated to be significant and therefore excluded from the models. 

In 2004, the K was not significant when included in both fecundity-size models while the 

inclusion of HSI to the fecundity-length model corresponded to an increase of 2% in the 

explained variance. The addition of HSI to weight-fecundity model increased the explained 

variation of 6% although the total explained variation was lower than the model with length 

alone. 

When considering samples from 2005 an increase of the explained variation by 1% could be 

observed after the inclusion of both K and HSI (in separate runs) in the length-fecundity 

models. The inclusion of K in the weight-fecundity model resulted in no increase of the PEV, 

while an increase on PEV by 1% was detected when adding HSI, although non significant. In 

the analyses of samples from 2006, neither K nor HSI were significant. 

The results from the comparison between specimens from Kattegat and NEAC cod are shown 

in Figure 2, including potential and relative fecundity, oocyte diameter and somatic Fulton’s 

K values. Size specific Fp (p

lower Fp, Fr and Fulton’s K values and a higher oocyte diameter than Kattegat cod in all 

length classes. 

Discussions 

An increasing number of researches have shown that SSB is a rather biased measure of stock 

reproductive potential, because it does not take into account stock-specific features that can 

produce different number of recruits at the same spawning biomass level (Saborido-Rey et al., 

2004, Marshall et al., 1998; Marshall et al., 2006). 

Many studies have concentrated on correlations between indicators of energy reserves and 

potential fecundity and different contributive predictive powers have been found for different 

species and stocks of the same species, highlighting that the importance of any factor can 

differ between species, stocks and geographical areas (see Lambert et al., 2003 for a review). 

In this study, potential fecundity of Kattegat cod was shown to be more tightly coupled with 

body length (78-87 % of variance explained), than with weight (73-75%). Fish size is without 

doubt the factor which at present time has been distinguished as most closely related to 

potential fecundity in cod stocks (Kjesbu et al. 1998; Kraus et al. 2000; Marshall et al. 1998). 

Although weight is generally more correlated with fecundity, length has often been preferred 

(Blanchard et al., 2003; Thorsen et al., 2006) considered that in cod weight can show large 

seasonal variations (Eliassen and Vahl, 1982; Lambert and Dutil, 1997b; Schwalme and 

Chouinard, 1999). However, the strength of the relationship between potential fecundity and 

length varies significantly between stocks (Marteinsdottir and Begg, 2002, Lambert et al., 

2005) reflecting different environmental conditions and stock characteristics. Furthermore the 

relationship becomes weaker when large fish are not present (Kjesbu et al., 1998). This 

stresses the importance of stock-specific investigations, especially in stocks which are subject 

to heavy size-selective fishery which eventually lead to a change in population’s structure in 

concomitance with the disappearance of larger and more fecund individuals (Solemdal et al., 

1995; Trippel, 1999; Tomkiewicz et al., 2003). 

In cod, Fulton’s K and HSI, mirroring total energy and lipid content respectively (Lambert 

and Dutil, 1997 a and b), are often scrutinized for their explanatory power in the observed 

fecundity variability (Marteinsdottir and Begg, 2002; Marshall et al.; 1998; Kraus et al., 

2000). For Kattegat cod, the inclusion of Fulton’s K and HSI measured just before spawning, 

showed no substantial increase of the explained variation in fecundity, compared to the 

7

variation explained by length alone. This result is in accordance with previous studies (Kjesbu 

et al., 1998; Lambert and Dutil, 2000; Kraus et al. 2000; Marteinsdottir and Begg, 2002; 

Blanchard et al., 2003) in which, despite the fish condition had a significant effect on 

fecundity, the explanatory power was generally low. On the contrary, some studies have 

shown that yearly averages of lipid energy (Marshall et al., 1999) or food availability (Kraus 

et al., 2002) can significantly improve predictions of fecundity and egg production. 

Difference in the relative energy investment per egg between stocks and years can influence 

the fecundity-length relationship (Lambert et al., 2005). It is well known that fish in poor 

condition, because of low food availability or changes of metabolism caused by adverse 

temperature, can have reduced fecundity or they can fail completely the maturation process 

(Kjesbu et al., 1991; Burton et al., 1997; Marshall et al. 1998). Hence the well-being of a fish 

is definitively important but the critical phase for influencing the egg production occurs after 

the feeding period, before the onset of maturation processes and the nutritional status may act 

as a control mechanism early in the oogenesis (Kraus et al., 2002; Lambert et al., 2003). The 

low contribution of K and HSI on fecundity found in our study in and previous investigations 

(Kjesbu et al., 1998; Kraus et al., 2000; Marteinsdottir and Begg, 2002) is therefore likely due 

to the fact that physiological measurements were taken at a too advanced stage of the 

maturation process. In order to detect the influence of maternal condition on fecundity, the 

condition is better quantified several months prior to spawning when the stored energy is 

initially reallocated to oocyte production (Koops et al., 2004; Skjæraasen et al., 2006). In our 

study we were not able to investigate the influence of maternal condition long before the 

onset of spawning but we can certainly conclude that two months before spawning, fish 

length is the only factor that biologically matters in the assessment of egg production in 

Kattegat cod. 

This study showed significant differences in oocyte number and size between the Kattegat 

and the NEAC cod stocks within the same length interval. Females in the Kattegat produce 

more oocytes (higher size-specific fecundity), although smaller in size, per unit of body mass 

at a given length than NEAC females. No differences were detected in the HSI but cod in the 

Kattegat were in a significantly better pre-spawning condition in term of Fulton’s K. 

The different environmental condition experienced by cod in the Barents Sea may partly 

explain the larger oocyte size, lower fecundity and lower condition in comparison with 

Kattegat cod, confirming previous studies showing a decreased fecundity with increasing 

latitude (Pörtner et al., 2001; Lambert et al., 2005) and decreasing temperature (Koops et al., 

2003). The variability in fecundity within the same species can be a result of adaptations to 

8

different environmental conditions (Whittames et al., 1995), and the quality of the habitat into 

which offspring will emerge may act as a selective force on propagule size (Parker and 

Begon, 1986). Any increase in egg size, results in a decrease in egg numbers (Svärdson, 

1949) with the optimal trade-off depending on the conditions experienced by the offspring 

(Parker and Begon, 1986). 

However the timing in fecundity studies is extremely important in relation to the maturation 

cycle. Caution is needed when comparing fecundity data from geographically separated 

stocks due to differences in spawning peak, and consequently, shifted maturity stages 

occurrence will lead to biased results. The stock of vitellogenic oocytes is reduced as the fish 

approach spawning and consequently fish in early maturation may have considerable larger 

standing stock of vitellogenic oocytes than fish just prior to spawning (Thorsen et al., 2006). 

In this case the oocyte diameter of the sampled Kattegat cod was smaller than found for the 

NEAC. This difference in oocyte size may reflect that the sampled NEAC was closer to 

spawning than the Kattegat cod. The difference in observed fecundity between the two stocks 

may therefore to some degree have been influenced by this. 

Moreover increased fecundity is often hypothesized to result from increased exploitation of 

stock to compensate higher adult mortality and shorter life span (Lambert et al., 2005). 

Therefore the differences in reproductive investment between the two stocks observed in the 

present study may also be a result of the different exploitation patterns experienced by those 

two stocks (Rijnsdorp, 1994; Trippel, 1995; Rochet, 1998). The lack of historical fecundity 

data in the Kattegat does, however, preclude a rigorous test of this hypothesis. North East 

Arctic cod can be considered a relatively healthy stock, highly productive and exposed to 

much less fishing mortality (Ottersen et al., 2006), while Kattegat cod is suffering a very high 

fishing pressure and is presently at its lowest historical level (ICES, 2007). As an effect of 

size-selected fishery the age composition in Kattegat, as in most Atlantic cod stocks, is 

strongly biased towards young fish, and as a consequence, reproduction in largely dependent 

on first spawners (Hutchings and Myers, 1993; Caddy and Agnew, 2003). 

It has been shown for many fish stocks that first spawners have a lower reproductive success 

than repeat spawners due to their smaller size. They produce relatively fewer and smaller 

eggs, which are less costly and have a lower quality, viability, fertilization rate and hatching 

success (Tomkiewicz et al., 2003 and references therein). Therefore an excessive removal of 

older and larger individuals from a stock may be more important than changes in absolute 

spawning biomass (Scott et al., 1999). 

9

The SSB, currently used as fecundity predictor in stock assessment models, fails to accurately 

account for the effect that variation in length composition has on reproductive potential of the 

stock, and consequently leads to an overestimation of the reproductive potential when the 

stock is dominated by small individuals (Marshall et al., 2006) as in the case of Kattegat cod 

stock. A previous study has already shown that the biomass of spawner females in Kattegat 

cod might have been consistently overestimated for a period of more than 20 years because of 

erroneous methods in maturity judgement (Vitale et al., 2006). Regarded as a whole the 

resiliency to exploitation of Kattegat cod might have been highly overrated, therefore a reexamination 

of the stock-recruitment relationship in this stock is strongly suggested. The 

fecundity-length relationship found in this study can be used to scale estimates of spawner 

abundance to population eggs production (Murua et al., 2003) and greatly assist the 

attainment of an improved assessment of the Kattegat cod stock and hence support the 

implementation of an improved and more realistic fishery harvesting strategy. 

Considering the reducing effect of a size-selective fishing on the size range of spawning fish 

(Jennings et al., 2001) and consequent implications on recruitment success, a continuous 

monitoring of the specific reproductive potential on a stock-specific base ought to be 

enhanced. 

10

Year n Model ß0 p ß0 ß1 p X1 ß2 p K ß3 p HSI df PEV 

2004 45 Fp~L 8.14

120 

100 

80 

Frequency 

60 

40 

20 

0 

10 20 30 40 50 60 70 80 90 100 110 120 

Length (cm) 

130 140 

Kattegat 

NEAC 

Figure 1: Length distributions of the samples showing the overlapping size range. 

12

1500 

1200 

900 

600 

300 

9 

3 

12 

11 

8 

14 

3 

11 

2 

2 

8 

6 

4 

2 

Kattegat 

NEAC 

0 

800 

600 

400 

200 

Mean OD (m) 

Fr (n eggs/gram) 

0 

1 

0.8 

0.6 

Fulton's K (g/cm 3 ) 

Fp (millions) 

54-58 

59-63 

64-68 

69-73 

74-78 

54-58 

59-63 

64-68 

69-73 

74-78 

Length (cm) 

Length (cm) 

Figure 2: Averaged potential (Fp) and relative (Fr) fecundity, oocyte diameter (OD) and Fulton’s K at given length intervals in Kattegat and 

NEAC stocks. Bars represent standard errors. The sample size is shown only in the first graph. 

13

Reference List 

Blanchard, J. L., Frank, K.T. and Simon, J.E., 2003. Effect of condition on fecundity and total 

egg production of eastern Scotian Shelf haddock (Melanogrammus aeglefinus). 

Canadian Journal of Fisheries and Aquatic Science 60 (3): 321-332 

Burton, M.P.M and Idler, D.R., 1987. An experimental investigation on the non-reproductive, 

post-mature state in winter flounder. Journal of Fish Biology 30: 643-650 

Burton, M. P. M., Penney, R. M., & Biddiscombe, S., 1997. Time course of gametogenesis in 

Northwest Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic 

Science 54 (Suppl.1), 122-131 

Caddy, J.F. and Agnew, D., 2003. A summary of global stock recovery plans for marine 

organisms including indicative information on the time to recovery, and associated 

regime changes that may effect recruitment and recovery success. International Council 

for the Exploration of the Sea ICES CM 2003/U:08 

Cardinale, M. and Svedäng, H., 2004. Modelling recruitment and abundance of Atlantic cod, 

Gadus morhua, in the Kattegat-Eastern Skagerrak (North Sea): evidence of severe 

depletion due to a prolonged period of high fishing pressure, Fisheries Research 69/2: 

263-282 

Eliassen, J.E. and Vahl, O., 1982. Seasonal variations in biochemical composition and energy 

content of liver, gonad and muscle of mature and immature cod, Gadus morhua (L.) 

from Balsfjorden, northern Norway. Journal of Fish Biology 20 (6): 707-716 

Friedland, K.D., Ama-Abasi, D., Manning, M, Clarke, L., Kligys, G. and Chambers, R.C., 

2005. Automated egg counting and sizing from scanned images: rapid sample 

processing and large data volumes for fecundity estimates. Journal of Sea Research 54: 

307-316 

Hutchings, J. and Myers, R., 1993. Effect of age on the seasonality of maturation and 

spawning of Atlantic cod, Gadus morhua, in the Northwest Atlantic. Canadian Journal 

of Fisheries and Aquatic Science 50: 2468-2474. 

Hutchings, J.A., Bishop, T.D. and McGregorshaw, 1999. Spawning behaviour of Atlantic 

cod, Gadus morhua: evidence of mate competition, mate choice, and negative effect of 

fishing. Canadian Journal of Fisheries and Aquatic Science 56: 97-104 

14

ICES. (2007). Report of the Baltic Fisheries Assessment Working Group (WGBFAS). 

International Council for the Exploration of the Sea ICES CM 2007/ACFM: 15, 

www.ices.dk 

Jennings, S, Kaiser, M.J. and Reynolds, J.D., 2001. Fishing effects on populations and 

communities. In Marine Fisheries Ecology by Blackwell Science Ltd, Oxford, UK 

Kjesbu, O.S., Klungsøyr, J., Kryvi, H., Witthames, P.R. and Green Walker, M, 1991. 

Fecundity, atresia and egg size of captive Atlantic cod (Gadus morhua) in relation to 

proximate body composition. Canadian Journal of Fisheries and Aquatic Science 48: 

2333-2343 

Kjesbu, O.S., Witthames, P.J., Solemdal, P. and Green Walker, M., 1998. Temporal variation 

in fecundity of Arcto-Norwegian cod (Gadus morhua) in response to natural changes in 

food and temperature. Journal of Sea Research 40: 303-321 

Kjesbu, O.S. and Witthames, P.R., 2007. Evolutionary strategies in flatfish and groundfish: 

Relevant concepts and methodological advancements. Journal of Sea Research 58: 23- 

34 

Klibansky, N. and Juanes, F., 2008. Procedures for efficiently producing High quality 

fecundity data on a small budget. Fisheries Research 89: 84-89 

Koops, M.A., Hutchings, J.A. and Adams, B.K., 2003. Environmental predictability and the 

cost of imperfect information: influences on offspring size variability. Evolutionary 

Ecology Research 5: 29-42 

Koops, M.A., Hutchings, J.A. and McIntyre, T.M., 2004. Testing hypotheses about fecundity, 

body size and maternal condition in fishes. Fish and Fisheries 5:120-130 

Kraus, G., Müller, A., Trella, K. and Köster. F.W., 2000. Fecundity of Baltic cod: temporal 

and spatial variation. Journal of Fish Biology 56: 1327-1341 

Kraus, G., Tomkiewicz, J. and Köster. F.W., 2002. Egg production of Baltic cod in relation to 

variable sex ratio, maturity and fecundity. Canadian Journal of Fisheries and Aquatic 

Science 59: 1908-1920 

Köster, F., Schnak, D. and Möllman, C., 2003 a. Scientific knowledge of biological processes 

that are potentially useful in fish stock prediction. Scientia marina 67 (Supplement 1): 

101-123 

Köster. F.W., Hinrichsen, H.H., Schnack, D., St. John, M.A., MacKenzie, B.R., Tomkiewicz, 

J., Möllmann, C., Kraus, G., Plikshs, M., Makarchouk, A. and Aro, E. 2003 b. 

Recruitment of Baltic cod and sprat stocks: Identification of critical life stages and 

15

incorporation of environmental variability into stock recruitment relationships. Scientia 

Marina 67 (Suppl 1): 129-154 

Lambert, T.C., 1990. The effect of population structure on recruitment in herring. Journal du 

Conseil International pour l’Exploration de la Mer 47:249-255 

Lambert, Y. and Dutil, J.D., 1997 a. Condition and energy reserves of Atlantic cod (Gadus 

morhua) during the collapse of the Northern Gulf of St. Lawrence stock. Canadian 

Journal of Fisheries and Aquatic Science 54: 2388-2400 

Lambert, Y. and Dutil, J.D., 1997 b. Can simple condition indices be used to monitor and 

quantify seasonal changes in the energy reserves of Atlantic cod (Gadus morhua)? 

Canadian Journal of Fisheries and Aquatic Science 54 (Supplement 1): 104-112 

Lambert, Y., Dutil, J.D., 2000. Energetic consequences of reproduction in Atlantic cod 

(Gadus morhua) in relation to spawning level of somatic energy reserves. Canadian 

Journal of Fisheries and Aquatic Science 57, 815-825 

Lambert, Y., Yaragina, N.A., Kraus, G., Marteinsdottir, G. and Wright, P., 2003. Using 

environmental and biological indices as proxies for egg and larval production of marine 

fish. Journal of Northwest Atlantic Fishery Science 33: 115-159 

Lambert, Y., Kjesbu, O.S., Kraus, G., Marteinsdottir, G. and Thorsen, A., 2005. How variable 

is the fecundity within and between cod stocks? International Council for the 

Exploration of the Sea ICES CM 2005/Q:13 

MacKenzie,B.R., Tomkiewicz, J., Köster, F and Nissling, A., 1998. Quantifying and 

disaggregating in spawning effect: incorporating stock structure, spatial distribution and 

female influence into estimates of annual population egg production. International 

Council for the Exploration of the Sea ICES CM 1998/BB:11 

Marshall, C. T., Kjesbu, O. S., Yaragina, N. A., Solemdal, P., Ulltang, O., 1998. Is spawner 

biomass a sensitive measure of the reproductive and recruitment potential of northeast 

Artic cod? Canadian Journal of Fisheries and Aquatic Sciences 55: 1766-1783 

Marshall, C.T., Yaragina, N.A., Lambert, Y. and Kjesbu, O.S., 1999. Total lipid energy as a 

proxy for total egg production by fish stocks. Nature 402: 288-290 

Marshall, C.T., O’Brien, L., Tomkiewicz, J., Marteinsdottir, G., Morgan, M.J., Saborido-Rey, 

F., Köster, F.W., Blanchard, J.L., Secor, D.H., Kraus, G., Wright, P.J., Mukhina, N.V. 

and Björnsson, H., 2003. Developing alternative indices of reproductive potential for 

use in fisheries management: case studies for stocks spanning an information gradient. 

Journal of Northwest Atlantic Fishery Science 33: 161-190 

16

Marshall, C.T., Needle, C.L., Thorsen, A., Kjesbu, O.S. and Yaragina, N.A., 2006. Systematic 

bias in estimates of reproductive potential of an Atlantic cod (Gadus morhua) stock: 

implications for stock recruit theory and management. Canadian Journal of Fisheries 

and Aquatic Sciences 63: 980-994 

Marteinsdottir, G. and Begg, G., 2002. Essential relationships incorporating the influence of 

age, size and condition on variables required for estimation of reproductive potential in 

Atlantic cod (Gadus morhua). Marine Ecology Progress Series 235: 235-256 

Murua, H., Kraus, G., Saborido-Rey, F., Witthames, P.R., Thorsen A., and Junquera, S., 2003. 

Procedures to estimate fecundity of marine fish species in relation to their reproductive 

strategy. Journal of Northwest Atlantic Fishery Science 33: 33-54 

Ottersen, G., Hjermann, D.Ø. and Stenseth, N.C., 2006. Changes in spawning structure 

strengthen the link between climate and recruitment in a heavily fished cod (Gadus 

morhua) stock. Fisheries Oceanography 15(3): 230-243 

Parker, G.A. and Begon, M., 1986. Optimal egg size and clutch size: effect of environment 

and maternal phenotype. American naturalist 128: 573-592 

Parrish, R.H., Mallicoate, D.L. and Klingbeil, R.A., 1986. Age dependent fecundity, number 

of spawnings per year, sex ration, and maturation stage in Northern anchovy, Engraulis 

mordax. US Fisheries Bulletin 84: 503-517 

Pörtner, H.O., Berdal, B., Blust, R., Brix, O., Colosimo, A., De Watcher, B., Giuliani, A., 

Johansen, T., Fischer, T., Knust, R., Lanning, G., Naevdal, G., Nedend, A., Nyhammer, 

G., Sartoris, F.J., Serendero, I., Sirabella, P., Thorkildsen, S. and Zakhartsev, M., 2001. 

Climate induced temperature effects on growth performance, fecundity and recruitment 

in marine fish: developing a hypothesis for cause and effect relationships in Atlantic cod 

(Gadus morhua) and common eelpout (Zoarces viviparis). Continental Shelf Research 

21: 1975-1997 

Rideout, R. M. & Burton, M. P. M., 2000. Peculiarities in ovarian structure leading to 

multiple-year delays in oogenesis and possible senescence in Atlantic cod, Gadus 

morhua L. Canadian Journal of Zoology 78: 1840-1844 

Rideout, R.M., Rose, GA and Burton, MPM., 2005. Skipped spawning in female iteroparous 

fishes. Fish and Fisheries 6: 50-72 

Rijnsdorp, A.D., 1994. Population-regulating processes during the adult phase in flat fish. 

Netherlands Journal of Sea Research 32: 207-223 

17

Rochet, M.J., 1998. Short term effect of fishing history traits of fishes. ICES, Journal of 

Marine Science 55: 371-391 

Roff, D.A., 2002. Life history evolution. Sinauer Associates, Sunderland, MA 

Rollefsen, G., 1934. The cod otoliths as a guide to race, sexual development and mortality. 

Rapports et Procés-Verbaux des Réunions 88:1-5 

Saborido-Rey, F., Morgan, M.J. and Domínguez, R., 2004. Estimation of Reproductive 

Potential fro Flemish Cap cod. Northwest Atlantic Fisheries Organization. Report of 

Scientific Council Meeting Doc. 04/61 

Schwalme, K and Chouinard, G.A., 1999. Seasonal dynamics in feeding, organ weight and 

reproductive maturation of Atlantic cod (Gadus morhua) in the Southern Gulf of St. 

Lawrence. ICES Journal of Marine Science 56: 303-319 

Scott, B., Marteinsdottir, G. and Wright, P., 1999. Potential effects of maternal factors on 

spawning stock-recruitment relationships under varying fishing pressure. Canadian 

Journal of Fisheries and Aquatic Sciences 56: 1882-1890 

Skjæraasen, J.E., Nilsen, T. and Kjesbu, O.S., 2006. Timing and determination of potential 

fecundity in Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic 

Sciences 63: 310-320 

Solemdal, P., Kjesbu, O.S. and Fonn, M., 1995. Egg mortality in recruit- and repeat-spawning 

cod – an experimental study. International Council for the Exploration of the Sea ICES 

CM1995/G35 

SPSS for Windows, Rel. 14.0.0.2005. Chicago: SPSS Inc. 

Statistica Software, 2004. StatSoft, Inc., Version 6.1 

Svardson, G., 1949. Competition and habitat selection in birds. Oikos, 1:157–74 

Svedäng, H. and Bardon, G., 2003. Spatial and temporal aspects of the decline in cod (Gadus 

morhua L.) abundance in the Kattegat and eastern Skagerrak. ICES Journal of Marine 

Science 60: 32-37 

Thorsen, A. and Kjesbu, O.S., 2001. A rapid method for estimation of oocyte size and 

potential fecundity in Atlantic cod using a computer-aided particle analysis system. 

Journal of Sea Research 46: 295-308 

Thorsen, A., Marshall, C.T. and Kjesbu, O.S., 2006. Comparison of various potential 

fecundity models for north-east cod Gadus morhua, L. using oocyte diameter as 

standardizing factor. Journal of Fish Biology 69: 1709-1730 

18

Tomkiewicz, J. Morgan, M.J., Burnett, J. and Saborido-Rey, 2003. Available information for 

estimating reproductive potential of Northwest Atlantic groundfish stocks. Journal of 

Northwest Atlantic Fishery Science 33: 1-21 

Trippel, E.A., 1995. Age at maturity as a stress indicator in fisheries. Bioscience, 45: 759-771. 

Trippel, E.A., 1999. Estimation of stock reproductive potential: history and challenges for 

Canadian Atlantic gadoids stock assessment. Journal of Northwest Atlantic Fishery 

Science 25: 61-81 

Vitale, F., Svedäng, H and Cardinale, M., 2006. Histological analysis invalidates macroscopic 

maturity ogives of cod (Gadus morhua). Use of alternative criteria in estimating 

maturity. ICES Journal of marine Science 63:485-492 

Vitale, F., Börjesson P., Svedäng H. and Casini M., 2008. The spatial distribution of cod 

(Gadus morhua L.) spawning grounds in the Kattegat, eastern North Sea. Fisheries 

Research 90(1-3): 36-44 

Whittames, P.R., Green Walker, M., Dinis, M.T. and Whiting, C.L., 1995. The geographical 

variation in the potential annual fecundity of Dover sole Solea solea (L.) from European 

shelf waters during 1991. Netherlands Journal of Sea Research 34: 45-58 

19

Available online at www.sciencedirect.com 

Fisheries Research 90 (2008) 36–44 

The spatial distribution of cod (Gadus morhua L.) spawning 

grounds in the Kattegat, eastern North Sea 

F. Vitale ∗ ,P.Börjesson, H. Svedäng, M. Casini 

Swedish Board of Fisheries, Institute of Marine Research, P.O. Box 4, S-453 21 Lysekil, Sweden 

Received 12 April 2007; received in revised form 30 August 2007; accepted 14 September 2007 

Abstract 

Similar to many other commercial marine fish species, Atlantic cod (Gadus morhua L.) migrate towards specific sites at spawning. These 

temporal aggregations are generally the most targeted by the commercial fishery. The Kattegat cod has undergone a substantial reduction over the 

past 25 years and both stock size and spawning stock biomass have remained at very low levels since the end of the 1990s. There is, therefore, an 

urgent need to map and document spawning grounds still in use. In the present study, spawning sites of Atlantic cod were identified in the Kattegat 

using a combination of commercial and fishery independent data from 1996 to 2004. Moreover, putative spawning and non-spawning areas were 

also sampled before and during the reproductive season between 2002 and 2006, and the proportion of mature females together with the individual 

physiological status were used to validate and strengthen the spatial analyses. 

The spatial analyses identified several spawning areas in the region and two areas in the southeastern part of the Kattegat which appeared to 

be the most important. The results showed the presence of cod spawning aggregations, although reduced in size, in areas that have been utilized 

for more than 25 years according to historical information. Some local spawning grounds may have also disappeared. The proportion of mature 

females was higher in putative spawning than in non-spawning areas (p < 0.001) and females from spawning areas had higher gonadosomatic 

(p < 0.05) and hepatosomatic (p < 0.001) indices than those from non-spawning areas. 

Knowledge of stock spatial and temporal distribution is essential in designing recovery strategies for depleted fish populations. The unambiguous 

stability of the locations of spawning aggregations over time, as shown in this study, represents a useful aid in order to efficiently implement a 

recovery plan for the collapsing cod stock in this area. 

© 2007 Elsevier B.V. All rights reserved. 

Keywords: Gadus morhua; Kattegat; Spawning grounds; Physiological indices; Stock management 

1. Introduction 

Many commercially important fish species are highly migratory, 

moving over a life cycle between nursery, feeding and 

spawning areas (Harden Jones, 1968; Secor, 2005). Atlantic 

cod is among those species that may seasonally cover long 

distances. The persistence of spawning activities over time at certain 

locations is well documented for many cod stocks: genetic 

and large-scale tagging studies have shown pre-spawning fish 

to follow established migratory pathways and to return to the 

same locations every year (Brander, 1975; Ruzzante et al., 

1999; Green and Wroblewski, 2000; Robichaud and Rose, 2001; 

Wright et al., 2006). 

Information of the spatial distribution of spawning grounds 

is crucial for studies and inference on stock structures, and 

∗ Corresponding author. Tel.: +46 523 18792; fax: +46 523 13977. 

E-mail address: francesca.vitale@fiskeriverket.se (F. Vitale). 

therefore also for fisheries management (Frank and Brickman, 

2001; Smedbol and Stephenson, 2001). Fishing to a high 

degree has traditionally been directed towards various spawning 

grounds. The temporal and spatial concentration of adult 

fish may thus increase vulnerability of a stock unit to fishing 

activities. Considering the fact that the highest catch rates 

are commonly achieved by mobile fleets targeting spawning 

aggregations (Hutchings et al., 1999), information on spatial 

and temporal distribution of spawning grounds is vital, especially 

for stocks that suffer from prolonged over-exploitation, 

and whose reproductive capacity may have become seriously 

hampered. 

Similar to many other cod stocks, the Kattegat cod is in a 

severely depleted state (Svedäng and Bardon, 2003; Cardinale 

and Svedäng, 2004; ICES, 2006). The stock has been considered 

outside safe biological limits since 2000, and from 2002 

and onwards, the ICES Advisory Committee for Fisheries Management 

(ACFM) has recommended a zero take from the area. 

0165-7836/$ – see front matter © 2007 Elsevier B.V. All rights reserved. 

doi:10.1016/j.fishres.2007.09.023

F. Vitale et al. / Fisheries Research 90 (2008) 36–44 37 

The Kattegat cod is thus covered by the EC recovery plan which 

nonetheless allows a Total Allowable Catch. 

Before the decline, spawning cod could be found throughout 

the Kattegat, but the southern part was generally recognized as 

the main spawning area, especially the bay of Skälderviken and 

Laholmsbukten (Pihl and Ulmestrand, 1988; Hagström et al., 

1990; Svedäng and Bardon, 2003). Historically, large spawning 

aggregations were also observed in the bay of Kungsbackafjorden 

and north of Läsö (Hagberg, 2005). The stock decline 

coincided with the disappearance of large spawning aggregations 

and the abundance of adult fish in the area has dropped to 

very low levels (Cardinale and Svedäng, 2004). It is therefore an 

urgent need to map and document current cod spawning grounds 

in the Kattegat. 

Information on the location of spawning cod has hitherto 

been mainly based on research bottom trawl data (Pihl and 

Ulmestrand, 1988; Hagström et al., 1990; Hagberg, 2005). This 

information, as well as more recent data collected by the International 

Bottom Trawl Survey (IBTS), is limited by low spatial and 

temporal coverage. Commercial data on the other hand, can offer 

high coverage but generally suffer from poor spatial resolution. 

The aim of the present study was to identify putative spawning 

grounds for cod in the Kattegat by using a combination of 

commercial and research bottom trawl data. The distribution of 

reported commercial catches during the spawning season was 

used as proxy for adult cod aggregations. It was hence conjectured 

that spawning and non-spawning areas could be depicted 

by combining the log-book data from the Swedish cod fishery 

with abundance estimates of spawning cod obtained from 

surveys. In order to strengthen and validate our findings, we compared 

maturity status and energetic indices of individual females 

before and during the spawning season from the putative spawning 

and non-spawning areas. Finally, the findings were discussed 

with respect to their relevance for fisheries management. 

2. Materials and methods 

2.1. Spatial analysis 

Data on Swedish commercial landings of cod in Kattegat 

(Fig. 1) from 1996 to 2004 were provided by the Swedish Board 

Fig. 1. Map showing the study area. Dashed lines represent the 20 m depth 

contour. 

of Fisheries. Only data from the first quarter of the year were 

used for mapping, as the spawning of cod in Kattegat mainly 

takes place from January to March (Vitale et al., 2005). Based 

on set position, landings of cod (in kg) from the three major bottom 

trawl fisheries (two cod bottom trawls and one Nephrops 

trawl) were aggregated in a grid of ∼10 by 10 km (5 × 5 nautical 

miles). These fisheries were selected because of their wide 

spatial coverage and large contribution (80–92%) to the total 

landings (Table 1). All squares from which landings had been 

reported at least once were included in the analysis. In years 

when no landings were reported in a specific square, this square 

Table 1 

Data on the Swedish cod fishery in the Kattegat (ICES Subdivision 21) during 1996–2004 

Year All year Landings during the 1st quarter 

Quota (tonnes) Total landings (tonnes) Total landings (tonnes) Three largest fisheries (tonnes) % of total 

1996 2850 2334 1355 1150 85 

1997 3150 3303 1774 1475 83 

1998 2780 2509 1050 843 80 

1999 2590 2540 1326 1150 87 

2000 2567 1568 663 608 92 

2001 2300 1191 603 546 91 

2002 987 744 437 373 85 

2003 852 603 325 297 91 

2004 505 575 389 352 91 

Yearly quota and total reported landings obtained from ICES (2006). For the 1st quarter total landings (in tonnes) and landings for the three dominating bottom trawl 

fisheries are presented (in tonnes and as percentage of total landings).

38 F. Vitale et al. / Fisheries Research 90 (2008) 36–44 

Table 2 

Summary of the International Bottom Trawl Survey (IBTS) data used in the study. Catch and Subsample are expressed in number of fish (N) 

Year No. hauls Time of year Catch (N) Subsample (N) No. spawning cod/hour (mean ± S.D.) 

1996 25 29 January–13 February 4711 565 19.1 ± 27.2 




2000 23 24 January–10 February 3616 508 11.4 ± 15 





was assigned the value of zero, hence the analysis relied only 

on survey data. Within years, data were standardized to generate 

distributions with a mean of zero and a standard deviation of one 

(0,1). 

The spatial distribution of sexual mature or spawning cod 

over the same period of time was based on information gathered 

by the International Bottom Trawl Survey (IBTS; Table 2). 

To estimate the number of spawning cod caught per hour in 

each haul, data on catch per unit effort (CPUE) were combined 

with the proportion of sexually mature, running cod ≥30 cm 

(obtained from a sub-sample of the catch). Within years, data 

were standardized to generate distributions of (0,1). 

Spatial interpolation was done using Thiessen polygons 

based on the position of the trawling stations and data were 

transferred to the same 10 km × 10 km grid used for the commercial 

landings, excluding those grid cells that did not have 

their centre within a polygon. The shape of the Thiessen polygons 

varied somewhat between years because the number and 

positions of trawling stations differed between surveys, however 

this does not affect the analysis. Putative spawning grounds 

were depicted by calculating and mapping the arithmetic mean 

of the two standardized grids based on commercial and fishery 

independent (IBTS) data, respectively. 

For the commercial data set, measures of spatial autocorrelation 

based on Queen’s connections were computed using the 

GeoDA software (Anselin, 2004). We used univariate Moran’s 

I to evaluate if observed data was spatially aggregated within 

years, and pair-wise comparisons (multivariate Moran’s I) to 

examine whether these areas persisted over time. The significance 

of trends found in the data set was evaluated using a 

randomisation test. Owing to the small sample size of the IBTS 

data, used to generate abundance maps on spawning adults (see 

Table 2), no attempt was made to estimate spatial autocorrelation 

for this data set or for the combined maps. 

2.2. Physiological investigations 

Altogether 1089 female cod were collected on board commercial 

trawlers and the Swedish research vessels “Argos” and 

“Ancylus” between November and January 2002–2006. In 2003 

samples were also collected in February and March. Total length 

(L T , cm) to the lowest 0.5 cm, whole body mass (M, g), gutted 

body mass (GM, g), liver (M L , g) and gonad mass (M G ,g)to 

the nearest 0.1 g, were recorded on board. However, gutted body 

mass in November–December 2002 and November–December 

2004 was not recorded, and was therefore calculated by the linear 

regression (GM = 0.8426 × M + 11.676; R 2 = 0.993), obtained 

from the data collected in December 2003 and 2005. Gonads and 

otoliths (sagittae) were stored and analysed as described in Vitale 

et al. (2005). Based on a 7-stage scale for gonadal development 

(Table 3), females were classified as either immature (stage 1–3) 

or mature (stage 4–7). Individual age was estimated by counting 

hyaline zones on sectioned otoliths. All age estimates were 

made by a single reader. 

Based on haul position, each trawl haul was mapped and classified 

as inside (entirely within black areas) or outside (entirely 

within white areas) a spawning ground according to the average 

map of identified spawning grounds (Fig. 3, upper panel on the 

Table 3 

Histological maturity scale 

1. Immature Small oocytes with a dense basophilic cytoplasm, a central nucleus and few large nucleoli around its edge (perinucleolar 

stage). Oogonia are always present but they might be not visible 

2. Previtellogenic growth The nucleus increases in size and multiple nucleoli are formed. A weakly stained area called “circumnuclear ring” (CNR) is 

also present 

3. Endogenous vitellogenesis The circumnuclear ring moves towards the outer part of the cell and gradually disintegrates, while the spherical cortical 

alveoli appear in the superficial half of the cytoplasm. No yolks granules present yet 

4. Exogenous vitellogenesis Presence of yolk granules. The nucleus, still centrally located, becomes irregular. The occurrence of this stage means that 

the maturation process is in progress, and under normal conditions, the individual will develop within the current spawning 

season 

5. Final maturation The chorion becomes thicker, the nucleus migrates towards the animal pole and by the hydration process occurs 

6. Spent Post-ovulatory follicles (POFs), after oocytes release into the lumen, are distinguishable 

7. Resting Oocytes in stage 1 and 2. Some post-ovulatory structures, still present, show signs of previous spawning


right). Trawl hauls including grey areas, were not used in the 

study. 

The proportion mature per age class, the hepatosomatic 

index (HSI = 100 × M L × GM −1 ), the gonadosomatic index 

(GSI = 100 × M G × GM −1 ) and the Fulton’s condition factor 

(K = 100 × GM × L T −3 ) were explored using Generalized Linear 

Models (GLZMs). The GLZM can be used to predict 

responses for dependent variables which are non-normally distributed 

and non-linearly related to the predictors. Such a model 

describes any given model in term of its link function. The test 

is based on the Wald-statistic, which is analogous to the F statistic 

of General Linear Model (GLM). The proportions of mature 

Fig. 2. Spatial distribution of (a) commercial landings of cod (≥30 cm) in kg, in the first quarter of the year (left panel), (b) number of spawning cod (≥30 cm) in the 

IBTS February survey (middle panel), and (c) putative spawning grounds in the Kattegat (right panel; the arithmetic mean of the standardized value for commercial 

catches and IBTS within each square). White grid cells = no reported landings; light grey 1.5 standard deviations above the mean. Grid size is approximately 10 km × 10 km (i.e. 5 × 5 nautical miles).


Fig. 2. ( Continued ).


Fig. 3. Average (upper maps) and standard deviation (lower maps) distribution of (a) commercial landings of cod in the first quarter of the year (left panel) and 

(b) putative spawning grounds in the Kattegat 1996–2004. White grid cells = no reported landings; Light grey: 1.5 standard deviations above the mean. Grid size is approximately 10 km × 10 km (i.e. 5 × 5 nautical 

miles). 

fish were compared between areas (spawning or non-spawning), 

using a binomial model with year, month, age and area as categorical 

predictors and log as link function. Three GLZMs with 

year, month, age and area as categorical predictors were also 

employed to explore GSI-, HSI- and K-values in females belonging 

to the two areas. The GLZMs, with log as link function, were 

gamma distributed for GSI and HSI and normal distributed for 

K. The models were expressed as: 

Response x,yλ,ϕ (Prop. mature, GSI, HSI, K) 

= c + ψ × year + δ × month + σ × age + ∂ × area + ε 

where c was the model constant and ψ, δ, σ, ∂ were the predictors’ 

specific parameters and ε was a random error. The level of 

significance for all tests was set at 5%. All the analyses were 

performed using Statistica Software (2004). 

3. Results 

3.1. Spatial analysis 

Data from 1996–2004 clearly indicated that cod catches during 

the Swedish bottom trawl fishery were made to a large extent 

in spatially rather restricted areas in the south eastern part of the 

Kattegat, i.e. either close to the entrance to the Sound, or off the 

coast at Falkenberg (Figs. 2 and 3, left panel). In some years, 

large landings of cod were also reported from Fladen and from 

the northern part of the Kattegat, i.e. north off Läsö. Spatial analyses 

confirmed that a positive autocorrelation was present both 

within years (univariate Moran’s I ranging from 0.20 to 0.48, 

p < 0.001 for all comparisons) and between years (multivariate 

Moran’s I ranging from 0.17 to 0.43; p < 0.001 for all comparisons) 

(Table 4). The CPUE of spawning cod in the IBTS data


Table 4 

Measure of spatial autocorrelation (Moran’s I) computed within and between 

years 

Year 1996 1997 1998 1999 2000 2001 2002 2003 2004 

1996 0.30 0.35 0.29 0.32 0.31 0.25 0.23 0.29 0.27 

1997 0.48 0.40 0.43 0.33 0.27 0.25 0.33 0.26 

1998 0.31 0.35 0.27 0.22 0.19 0.25 0.20 

1999 0.41 0.30 0.22 0.17 0.26 0.24 

2000 0.28 0.23 0.24 0.27 0.29 

2001 0.20 0.24 0.25 0.24 

2002 0.29 0.30 0.25 

2003 0.35 0.31 

2004 0.32 

All within and between year correlations were significant (p < 0.001, based on 

randomization test). 

1996–2004 varied with a factor of 10 over the study period, ranging 

from an average of 34.2 spawning fish per hour in 1998 and 

1999 to 3.2 spawning fish per hour in 2003. However, the occurrence 

of spawning fish was not evenly distributed throughout 

the area, but coincided to a large extent with the areas identified 

as hot spots for the commercial landings (Figs. 2 and 3, middle 

panel). Put together, these data sources indicate several possible 

spawning grounds for cod in the Kattegat (Figs. 2 and 3, right 

panel). 

3.2. Physiological investigations 

Results from the GLZMs showed higher proportions of 

mature, GSI- and HSI-values inside than outside potential 

spawning areas (Table 5). No significant difference could be 

detected for Fulton’s condition factor. Fig. 4 illustrates the 

monthly trends of all the investigated variables. The proportion 

of mature females and GSI indicated an increasing trend 

from December to February, followed by a decrease in March 

Table 5 

Results from the GMZLs, testing differences in proportion of mature females, 

GSI, HIS and K between putative spawning and non-spawning areas 

Effect Degr freed Wald statistic p 

Proportion of mature Month 4 24.0247


4. Discussion 

This study clearly depicted the location of the major cod 

spawning activities in the Kattegat between 1996 and 2004. The 

efficacy of combining commercial landings and fishery independent 

survey data was demonstrated by the very persistent 

and precise geographical signal elicited in the study. These 

results were further corroborated by independent sampling of 

the physiological status of fish in depicted spawning and nonspawning 

areas. The combined methodology used in this study 

thus represents an alternative way of mapping and describing 

the distribution of spawning localities for commercial fish 

species in relation to more expensive and time-consuming egg 

surveys. By using commercial landing data and surveys, either 

in combination or separately, the former spatial distribution of 

spawning localities can be elucidated. This might represent the 

only opportunity to reconstruct the historical spatial population 

structure. 

For the studied period of time, two areas in the southeastern 

part of the Kattegat appeared to be most important, 

one close to the entrance to the Sound and one off 

the coast at Falkenberg (Fig. 1). This observation is in 

general agreement with previous information on location 

of spawning aggregations in the Kattegat for the periods 

1981–1990 (Pihl and Ulmestrand, 1988; Hagström et al., 

1990), and 1975–1999 (Svedäng and Bardon, 2003) and 

with the ongoing study on egg distribution (Svedäng et al., 

2004). In addition, based on survey data only, spawning 

aggregations were also noted in the deeper parts of the southwestern 

Kattegat (Hagström et al., 1990; Fig. 3d, central 

panel). 

However, the present diversity of spawning localities in the 

Kattegat was indicated to be reduced in comparison to what 

can be elucidated about the past distribution of spawning activities, 

i.e. before 1990. Besides the two areas presently indicated 

as the main spawning grounds, only weak signals of spawning 

activities were obtained in the central and northern parts of Kattegat. 

These areas might no longer be recognized as spawning 

grounds, although large spawning aggregations were frequently 

encountered by research surveys in the early part of 20th century 

(Hagberg, 2005). 

Moreover, it was also noted that possibly separate spawning 

locations may have been abandoned in the bights of 

Skälderviken and Laholmsbukten. Svedäng and Bardon (2003) 

depicted rather big spawning aggregations in these areas, 

which eventually disappeared in the beginning of the 1990s. 

Unfortunately, earlier information on the location of spawning 

aggregations in the bights of Laholmsbukten and Skälderviken 

did not include any spatial delineation. As these two former 

spawning areas were situated rather close to the two major 

spawning areas depicted in the present study, it was therefore 

not possible to evaluate whether our results reflect a decline in 

number of spawning areas or merely a contraction in spatial 

distribution. 

The inclusion of physiological parameters strengthened the 

identification of spawning areas in the study. An unambiguous 

difference was found between individuals at the depicted 

spawning and non-spawning grounds in the first quarter of the 

year. Seasonal patterns of energy accumulation and depletion 

in cod, following the cyclic periods of feeding, maturation, 

migration, reproduction and overwintering, has been described 

in several studies (Lambert and Dutil, 1997 and references 

therein). Female cod accumulate mainly energy in the liver in 

the form of lipids. Once the maturing is set in train, this energy 

reserve is successively transferred to the gonads, i.e. during the 

vitellogenesis. Therefore during the spawning season, cod experience 

an increase of gonad weight together with a decrease 

in liver weight, as stored energy is translocated for reproductive 

purposes (Lambert and Dutil, 1997, 2000; Schwalme and 

Chouinard, 1999). Consequently, the energy requirements and 

utilisation, constitute a good basis for assessing the reproductive 

status of individuals, and, ultimately, for discriminating between 

spawning and non-spawning grounds. Our results show that the 

energetic fluctuation is unequivocally occurring in those individuals 

caught in the assumed spawning grounds from January and 

onwards, indicating that cod in the Kattegat start to aggregate in 

January. 

Put together, these results showed that cod has continued 

to aggregate and spawn in specific areas for 25 years or 

more, albeit in drastically reduced numbers. This is a good 

indication of the persistence of the spatial structure in cod populations 

over time and that spawning site fidelity in one way or 

another must be transferred from generation to generation (cf. 

Robichaud and Rose, 2001; Wright et al., 2006; Svedäng et al., 

2007). 

Spatial and temporal fish concentrations are obviously attractive 

for commercial fishing, as they limit the costs for searching 

and harvesting fish shoals. However, in sea areas like the Kattegat, 

targeting spawning aggregations may jeopardise the efforts 

stipulated in the cod recovery plan as the exploitation of those 

areas during the spawning season may represent a considerable 

part of the annual fishing mortality (cf. ICES, 2006). Moreover, 

in the spawning areas larger individuals, which produce 

higher quality and more viable eggs (Trippel et al., 1997) as 

well as higher sperm volume (Trippel and Morgan, 1994), are 

more common and more easily withdrawn from the population 

with serious consequences for the quality of reproductive output. 

It is noteworthy that simply performing trawl passages through 

the spawning aggregations could put an extra stress on cod mating 

behaviour (Brawn, 1961; Hutchings et al., 1999; Nordeide 

and Foldstad, 2000) and spawning synchronization may be disturbed, 

possibly decreasing the fertilization rates (Morgan et al., 

1997). 

In conclusion, in order to successfully implement a recovery 

plan for an over-exploited fish population, such as the Kattegat 

cod, accurate knowledge on spatial and temporal distribution of 

spawning activity might be crucial. The closure of the identified 

spawning areas could reduce fishing mortality and enhance the 

chances for successful reproduction, if the recovery is intended 

to be favoured by a spatial and temporal management of the 

overall fishing effort. The clear-cut persistence of the spawning 

aggregations over time, as shown in this study, is likely to facilitate 

implementation of recovery plans focused on controlling 

fishing activity during the spawning season.


Acknowledgements 

The authors wish to thank the crews on R/V Ancylus and R/V 

Argos for the assistance in the field, Massimiliano Cardinale 

for his useful advices and three anonymous reviewers whose 

criticisms greatly improved the manuscript. 

References 

Anselin, L., 2004. GeoDa 0.95i. Spatial Analysis Laboratory. Department of 

Geography. University of Illinois, Urbana-Champaign Urbana, IL 61801 

(https://www.geoda.uiuc.edu/geoda/geoda). 

Brander, K.M., 1975. The population dynamic and biology of cod (Gadus 

morhua L.) in the Irish Sea. Ph.D. Thesis. Fisheries Laboratoriy, Lowestoft, 

UK. 

Brawn, V.M., 1961. Reproductive behaviour of the cod (Gadus callarias L.). 

Behaviour 18, 177–198. 

Cardinale, M., Svedäng, H., 2004. Modelling recruitment and abundance of 

Atlantic cod, Gadus morhua, in the eastern Skagerrak-Kattegat (North Sea): 

evidence of severe depletion due to a prolonged period of high fishing 

pressure. Fish. Res. 69, 263–282. 

Frank, K.T., Brickman, D., 2001. Contemporary management issues confronting 

fisheries science. J. Sea Res. 45, 173–187. 

Green, J.M., Wroblewski, J.S., 2000. Movement patterns of Atlantic cod in 

Gilbert Bay, Labrador: evidence for bay residency and spawning site fidelity. 

J. Mar. Biol. Ass. UK 80, 1077–1085. 

Hagberg, J., 2005. Utökad analys av historiska data för att säkerställa referensvärden 

för fisk (Improved analysis of historical data for ensuring fish 

reference points). Swedish Board Fish., 22 (in Swedish). 

Hagström, O., Larsson, P.O., Ulmestrand, M., 1990. Swedish cod data from the 

international young fish surveys 1981–1990. ICES CM 1990/G:65. 

Harden Jones, F.R., 1968. Fish Migration. Edward Arnold, Ltd., London. 

Hutchings, J.A., Bishop, T.D., McGregor-Shaw, C.R., 1999. Spawning 

behaviour of Atlantic cod, Gadus morhua: evidence of mate competition and 

mate choice in a broadcast spawner. Can. J. Fish. Aquat. Sci. 56, 97–104. 

ICES, 2006. Report of the ICES Advisory Committee on Fishery Management, 

Advisory Committee on the Marine Environment and Advisory 

Committee on Ecosystems, 2006. ICES Advice. Books 1–10. 6, 310 

pp. (http://www.ices.dk/products/icesadvice/2006PDF/ICES%20Advice% 

202006%20Book%206.pdf). 

Lambert, Y., Dutil, J.D., 1997. Can simple condition indices be used to monitor 

and quantify seasonal changes in the energy reserves of Atlantic cod (Gadus 

morhua)? Can. J. Fish. Aquat. Sci. 54 (Suppl. 1), 104–112. 

Lambert, Y., Dutil, J.D., 2000. Energetic consequences of reproduction in 

Atlantic cod (Gadus morhua) in relation to spawning level of somatic energy 

reserves. Can. J. Fish. Aquat. Sci. 57, 815–825. 

Morgan, M.J., DeBlois, E.M., Rose, G.A., 1997. An observation of the reaction 

of Atlantic cod (Gadus morhua) in a spawning shoal to bottom trawling. 

Can. J. Fish. Aquat. Sci. 54 (Suppl. 1), 217–223. 

Nordeide, J.T., Foldstad, I., 2000. Is cod lekking or a promiscuous group 

spawner? Fish Fish. 1, 90–93. 

Pihl, L., Ulmestrand, M., 1988. Investigations on coastal cod on the Swedish 

west coast. Länsstyrelsen i Göteborg och Bohus Län., 61 pp. (in Swedish). 

Robichaud, D., Rose, G.A., 2001. Multiyear homing of Atlantic cod to a spawning 

ground. Can. J. Fish. Aquat. Sci. 58, 2325–2329. 

Ruzzante, D.E., Taggart, C.T., Cook, D., 1999. A review of the evidence 

for genetic structure of cod (Gadus morhua) population in the Northwest 

Atlantic and population affinities of larval cod off Newfoundland and the 

Gulf of St. Lawrence. Fish. Res. 43, 79–97. 

Schwalme, K., Chouinard, G.A., 1999. Seasonal dynamics in feeding, organ 

weights, and reproductive maturation of Atlantic cod (Gadus morhua)inthe 

southern Gulf of St. Lawrence. ICES J. Mar. Sci. 56, 303–319. 

Secor, D.H., 2005. Fish migration and the unit stock: three formative debates. A 

review of ecological and historical issues related to stock connectivity and 

metapopulations. In: Cadrin, S.X., Friedland, K.D., Waldman, J.R. (Eds.), 

Stock Identification Methods. Applications in Fishery Science. Elsevier Academic 

Press, MA, pp. 17–44. 

Smedbol, R.K., Stephenson, R., 2001. The importance of managing withinspecies 

diversity in cod and herring fisheries of the north-western Atlantic. 

J. Fish Biol. 59 (Suppl. A), 109–128. 

Statistica Software, 2004. Statsoft, Inc., Version 6.1. 

Svedäng, H., Bardon, G., 2003. Spatial and temporal aspects of the decline in 

cod (Gadus morhua L) abundance in the Kattegat and eastern Skagerrak. 

ICES J. Mar. Sci. 60, 32–37. 

Svedäng, H., Hagberg, J., Börjesson, P., Svensson, A., Vitale, F., 2004. Bottenfisk 

ivästerhavet (Demersal fish in the Swedish west coast). Swedish Board Fish. 

Finfo 6, 44 (in Swedish). 

Svedäng, H., Righton, D., Jonsson, P., 2007. Migratory behaviour of Atlantic 

cod Gadus morhua: natal homing is the prime stock separating mechanism. 

MEPS 345, 1–12. 

Trippel, E.A., Morgan, M.J., 1994. Age-specific paternal influences on reproductive 

success of Atlantic cod (Gadus morhua L.) of the Grand Banks, 

Newfoundland. ICES Mar. Sci. Symp. 198, 412–422. 

Trippel, E.A., Kjesbu, O.S., Solemdal, P., 1997. Effect of adult age and 

size structure on reproductive output in marine fishes. In: Cambers, 

R.C., Trippel, E.A. (Eds.), Early Life History and Recruitment in Fish 

Populations. Chapman & Hall, 2-6 Boundary Row, London SE1 8HN, 

pp. 31–55. 

Vitale, F., Cardinale, M., Svedäng, H., 2005. Evaluation of the temporal development 

of the ovaries in Gadus morhua from the Sound and Kattegat, North 

Sea. J. Fish Biol. 67, 669–683. 

Wright, P.J., Galley, E., Gibb, I.M., Neat, F.C., 2006. Fidelity of adult cod to 

spawning grounds in Scottish waters. Fish. Res. 77, 148–158.

vitale_phd_thesis.pdf (1.8 MB) - Göteborgs universitet

You also want an ePaper? Increase the reach of your titles

Delete template?

Save as template?