Mapping the spawning grounds of North Sea cod (Gadus morhua) by direct and indirect means

Despite recent evidence for sub-stock structuring, North Sea cod are assessed as a single unit. As a consequence, knowledge of sub-stock trends is poor. In particular, there are no recent evaluations of which spawning grounds are active. Here we report results from the first ichthyoplankton survey to cover the whole North Sea. Also, this survey, conducted in 2004, was the first to make extensive use of DNA-based molecular methods to unambiguously identify early developmental stage cod eggs. We compare the findings from the plankton survey with estimated egg production inferred from the distribution of mature cod in contemporaneous trawl surveys. Results from both approaches were in general agreement and showed hot spots of egg production around the southern and eastern edges of the Dogger Bank, in the German Bight, the Moray Firth and to the east of the Shetlands. These areas broadly coincide with known spawning locations from the period 1940 to 1970. We were, however, unable to directly detect significant numbers of cod eggs at the historic spawning ground off Flamborough (northeast coast of England). The results demonstrate that most of the major spawning grounds of cod in the North Sea are still active but that some localized populations may have been reduced to the point where it is now difficult to detect the presence of eggs in the plankton.     

Seasonal prevalence and intensity of follicular atresia in Baltic cod Gadus morhua callarias L.

In the present study, 307 ovaries of eastern Baltic cod Gadus morhua callarias sampled during the prespawning and spawning season 2000 were analysed histologically to estimate the seasonal prevalence and intensity of atresia. The number of atretic oocytes per ovary was estimated using a combination of the physical disector method and volume fraction (Delesse principle). Atretic oocytes were observed in 32% of the ovaries. Prevalence of atresia was independent of female size, but increased significantly with declining female condition from prespawning and through the spawning stages. The relative intensity of atresia, i.e. number of atretic oocytes in relation to normally developed vitellogenic oocytes, was low amounting to 1·4% on average. Similar to prevalence, relative intensity of atresia differed significantly between maturity stages and increased with decreasing female condition. The population egg loss due to atresia amounted to 4·6% indicating that Baltic cod was performing close to maximum productivity, i.e. potential egg production.     

Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis

The study of hybrid zones is central to our understanding of the genetic basis of reproductive isolation and speciation, yet very little is known about the extent and significance of hybrid zones in marine fishes. We examined the population structure of cod in the transition area between the North Sea and the Baltic Sea employing nine microsatellite loci. Genetic differentiation between the North Sea sample and the rest increased along a transect to the Baltic proper, with a large increase in level of differentiation occurring in the Western Baltic area. Our objective was to determine whether this pattern was caused purely by varying degrees of mechanical mixing of North Sea and Baltic Sea cod or by interbreeding and formation of a hybrid swarm. Simulation studies revealed that traditional Hardy-Weinberg analysis did not have sufficient power for detection of a Wahlund effect. However, using a model-based clustering method for individual admixture analysis, we were able to demonstrate the existence of intermediate genotypes in all samples from the transition area. Accordingly, our data were explained best by a model of a hybrid swarm flanked by pure nonadmixed populations in the North Sea and the Baltic Sea proper. Significant correlation of gene identities across loci (gametic phase disequilibrium) was found only in a sample from the Western Baltic, suggesting this area as the centre of the apparent hybrid zone. A hybrid zone for cod in the ecotone between the high-saline North Sea and the low-saline Baltic Sea is discussed in relation to its possible origin and maintenance, and in relation to a classical study of haemoglobin variation in cod from the Baltic Sea/Danish Belt Sea, suggesting mixing of two divergent populations without interbreeding.     

The forgotten feeding ground: patterns in seasonal and depth-specific food intake of adult cod Gadus morhua in the western Baltic Sea

This study presents the diet composition of western Baltic cod Gadus morhua based on 3150 stomachs sampled year-round between 2016 and 2017 using angling, gillnetting and bottom trawling, which enhanced the spatio-temporal coverage of cod habitats. Cod diet composition in shallow areas (<20 m depth) was dominated by benthic invertebrate species, mainly the common shore crab Carcinus maneas. Compared to historic diet data from the 1960s and 1980s (limited to depth >20 m), the contribution of herring Clupea harengus decreased and round goby Neogobius melanostomus occurred as a new prey species. Statistical modelling revealed significant relationships between diet composition, catch depth, fish length and season. Generalized additive modelling identified a negative relationship between catch depth and stomach content weight, suggesting reduced food intake in winter when cod use deeper areas for spawning and during peak summer when cod tend to avoid high water temperatures. The results of this study highlight the importance of shallow coastal areas as major feeding habitats of adult cod in the western Baltic Sea, which were previously unknown because samples were restricted to deeper trawlable areas. The results strongly suggest that historic stomach analyses overestimated the role of forage fish and underestimated the role of invertebrate prey. Eventually, this study shows the importance of a comprehensive habitat coverage for unbiased stomach sampling programmes to provide a more reliable estimation of top predator diet, a key information for food web analyses and multispecies models.     

Effects of freezing on length and mass measurements of Atlantic cod Gadus morhua in the Baltic Sea

An aggregated sample of 925 Atlantic cod Gadus morhua collected by four countries in different regions of the Baltic Sea during different seasons were measured (total length, L_T = 161–890 mm and weighed (mass, M = 45–6900 g) both before freezing and after defrosting. The cod were found to decrease significantly in both L_T and M following death and frozen storage. There was an average (±SD) change in L_T of −2.91% (±0.05%) following freezing, independent of starting L_T. Total M changed by −2.65% (±0.14%), independent of starting mass. Shrinkage of L_T and M did not differ significantly between 1 and 4 months frozen storage, though L_T shrinkage was significantly greater after 1 or 4 months in the freezer compared with after 5 days. There was significant variation in L_T and M shrinkage between regions of capture. A significant negative relationship between condition of cod and L_T or M change was also observed. Equations to back-calculate fresh L_T and M from thawed L_T, M and standard length (L_S), gutted L_T, gutted L_S and gutted M are provided.     

On differentiation of cod (Gadus morhua L.) groups in Baltic Sea

Russian Journal of Genetics - Using the AGP*, PGI-1*, PGI-2*, LDH*, IDH*, and PGM* allozyme markers, the differentiation of cod groups during the spawning period in Baltic Sea was evaluated. It was...     

Long-term variation in dates of mass spawning of cod Gadus morhua callarias (Gadidae) in the southeastern part of the Baltic Sea

Long-term data on the numbers of eggs of cod Gadus morhua callarias in ichthyoplankton and the seasonal variation of their distribution in the Gdansk Deep of the Baltic Sea are considered. The spring peak of spawning was observed for the years 1948–1954 and 1960–1964; the spring-summer peak for 1968–1977; and the summer peak for 1955–1959 and 1995–2001. Maximum egg numbers of cod were recorded from the late 1940s to the early 1950s; minimums were recorded in the late 1980s and the late 1990s. The decrease in the numbers of cod eggs in the ichthyoplankton, in general, coincided with a decrease in the proportion of spawners maturing at the beginning of the season of mass reproduction and a decrease in the oxygen content in the near-bottom layer of the Gdansk Deep. It is suggested that a shift of the spawning peak of cod from spring to summer is related to a decrease in the volume of near-bottom waters providing favorable conditions for the reproduction of this population.     

Stock structure of Icelandic cod Gadus morhua L. based on otolith chemistry

Otolith chemistry was used to study the stock structure of Icelandic cod Gadus morhua . Otoliths were collected from spawning cod at 12 and 17 different spawning locations around Iceland during the spawning season in 2002 and 2003, respectively. The otolith elemental composition of cod spawning north and south of Iceland differed substantially from each other, as did spawning cod below and above 125 m depth at the main spawning ground in the south of Iceland. Otolith chemistry differed more between locations than among years within a location, indicating temporal stability between the 2 years. The Icelandic cod stock is managed as a single stock. These results suggest, however, that optimal fisheries management may require different management units than are currently present.     

Ecological implications of Echinorhynchus gadi parasitism of Baltic cod (Gadus morhua)

Of 533 Baltic cod (body length 21–93 cm) 530 were infected with Echinorhynchus gadi at infection intensities from 1 to 490 per host. The heavy infection of large cod (normally not feeding on amphipods) may be explained by a transfer of parasites from prey fishes to the predating large cod.     

Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.)

Reproductive competition may lead to a large skew in reproductive success among individuals. Very few studies have analysed the paternity contribution of individual males in spawning aggregations of fish species with huge census population sizes. We quantified the variance in male reproductive success in spawning aggregations of cod under experimental conditions over an entire spawning season. Male reproductive success was estimated by microsatellite-based parentage analysis of offspring produced in six separate groups of spawning cod. In total, 1340 offspring and 102 spawnings distributed across a spawning season were analysed. Our results show that multiple males contributed sperm to most spawnings but that paternity frequencies were highly skewed among males, with larger males on average siring higher proportions of offspring. It was further indicated that male reproductive success was dependent on the magnitude of the size difference between a female and a male. We discuss our results in relation to the cod mating system. Finally, we suggest that the highly skewed distribution of paternity success observed in cod may be a factor contributing to the low effective population size/census population size ratios observed in many marine organisms.     

Characterization of 18 new microsatellite loci in Atlantic cod (Gadus morhua L.)

Eighteen new microsatellite loci consisting of 10 di‐, 5 tri‐, 2 tetra‐ and 1 heptanucleotide repeats are introduced for the Atlantic cod (Gadus morhua L.). All loci were co‐amplified in two polymerase chain reactions (plus two previously published microsatellites) and all products were typed clearly. The number of alleles per locus ranged from six (PGmo130) to 45 (PGmo76) and the observed heterozygosity ranged from 0.356 (PGmo130) to 0.957 (PGmo95). All loci except one followed Hardy–Weinberg expectations. Genetic linkage disequilibrium analysis between all pairs of loci did not yield any significant values.     

Characterization of new SSR‐EST markers in cod,Gadus morhua

For years, fishermen have noted that cod (Gadus morhua) within the Georges Bank Atlantic fishery spawn multiple times annually with peaks in the spring and in the fall. To evaluate the hypothesis that these differences in reproductive behaviour reflect genetically different spawning populations, we identified eight polymorphic simple sequence repeats within expressed sequence tags (ESTs). Previously, only a few genetic markers have been informative for distinguishing between cod populations of the Northwest Atlantic. The development of additional markers from ESTs will be a valuable tool to improve our understanding of population structure in this commercially important species.     

Historic changes in length distributions of three Baltic cod (Gadus morhua) stocks: Evidence of growth retardation

Understanding how combinations of fishing effort and selectivity affect productivity is central to fisheries research. We investigate the roles of fishing regulation in comparison with ecosystem status for Baltic Sea cod stock productivity, growth performance, and population stability. This case study is interesting because three cod populations with different exploitation patterns and stock status are located in three adjacent but partially, ecologically different areas. In assessing stock status, growth, and productivity, we use survey information and rather basic stock parameters without relying on age readings. Because there is an urgent interest of better understanding of the current development of the Eastern Baltic cod stock, we argue that our approach represents partly a novel way of interpreting monitoring information together with catch data in a simplified yet more informative way. Our study reports how the Eastern and Western Baltic cod have gone toward more truncated size structures between 1991 and 2016, in particular for the Eastern Baltic cod, whereas the Öresund cod show no trend. We suggest that selective fishing may disrupt fish population dynamic stability and that lower natural productivity might amplify the effects of selective fishing. In support of earlier findings on a density‐dependent growth of Eastern Baltic cod, management is advised to acknowledge that sustainable exploitation levels for Eastern Baltic cod are much more limited than perceived in regular assessments. Of more general importance, our results emphasize the need to embrace a more realistic view on what ecosystems can produce regarding tractable fish biomass to facilitate a more ecosystem‐based fisheries management.     

Development of ten new EST-derived microsatellites in Atlantic cod (Gadus morhua L.)

Ten polymorphic microsatellite markers were developed from approximately 1,300 expressed sequence tags (ESTs) of Atlantic cod (Gadus morhua L.). Thirty two primer pairs were designed for EST sequences containing perfect di- tri- tetra- and pentanucleotide motifs and characterised in 96 unrelated fish. Ten markers were successfully amplified with number of alleles from 2 to 13 per locus and observed and expected heterozygosity ranging from 0.03 to 0.69 and 0.03 to 0.74, respectively. Loci Gmo-C131, C132 and C136 deviated from Hardy-Weinberg equilibrium. Genetic linkage disequilibrium analysis between all pairs of the loci showed significant departure from the null hypothesis between loci Gmo-C131 and Gmo-C132 and C128 and Gmo-C133. The gene identity was determined at five of the loci, confirming the associated microsatellites as Type I markers. The new microsatellites reported in this work can be used for conservation and enhancement of wild stocks for commercial harvesting. Jon-Ivar Westgaard and Tekle Tafese have contributed equally to the work.     

Assessment of production of eggs of Eastern Baltic cod (Gadus morhua callarias L.) on the basis of long-term ichthyoplankton data

Proceeding from long-term data on the numbers of eggs of cod in ichthyoplankton, the total annual production of cod eggs at four main spawning grounds of the Baltic Sea was calculated. It was shown that the long-term fluctuations of cod egg production were positively related to the dynamics of the volume of waters coming to the Baltic Sea in years of the North Sea advections. It is suggested that this dependence was determined by a set of adaptations providing the extension of cod reproduction upon the improvement of the environment.     

Karyotyping and cytogenetic mapping of Atlantic cod (Gadus morhua Linnaeus, 1758)

The Atlantic cod (Gadus morhua) is an important natural resource for northern societies and is now also considered to be a promising candidate for aquaculture. In recent years, much effort has been directed towards the development of genomic tools, and genome initiatives for Atlantic cod have been established. Despite the growing attention devoted to the Atlantic cod genomics, basic aspects of its genome structure and organization remain unknown. Thus, the present work aims to study cytogenetic features of the Atlantic cod as a contribution to the knowledge of this species' genome. The Atlantic cod displays a diploid number of 46 chromosomes, with a karyotypic formula 16 m/sm + 30 st/t. Conventional karyotyping was improved by chromosomal mapping of two classes of repetitive sequences. 18S rDNA clusters were assigned to pairs 2 and 4; small amounts of 18S rDNA clusters were occasionally detected on pair 5. These findings could not be related to the geographical origin of the specimens, but were consistent with the variability of these repeated genes in fish in general. 5S ribosomal gene clusters, apparently corresponding to a single 5S rDNA class, were detected on twelve chromosomes (pairs 11, 12, 14, 17, 20 and 21). The present update of the existing but meagre information on the karyotype of Atlantic cod, plus the first physical mapping of repetitive genes in this species herein, opens the way for an integrated approach that combines genetic and physical mapping with the assembly of the genome of this commercially important species.     

Long-term stability and effective population size in North Sea and Baltic Sea cod (Gadus morhua)

DNA from archived otoliths was used to explore the temporal stability of the genetic composition of two cod populations, the Moray Firth (North Sea) sampled in 1965 and 2002, and the Bornholm Basin (Baltic Sea) sampled in 1928 and 1997. We found no significant changes in the allele frequencies for the Moray Firth population, while subtle but significant genetic changes over time were detected for the Bornholm Basin population. Estimates of the effective population size ( N _e ) generally exceeded 500 for both populations when employing a number of varieties of the temporal genetic method. However, confidence intervals were very wide and N _e 's most likely range in the thousands. There was no apparent loss of genetic variability and no evidence of a genetic bottleneck for either of the populations. Calculations of the expected levels of genetic variability under different scenarios of N _e showed that the number of alleles commonly reported at microsatellite loci in Atlantic cod is best explained by N _e 's exceeding thousand. Recent fishery-induced bottlenecks can, however, not be ruled out as an explanation for the apparent discrepancy between high levels of variability and recently reported estimates of N _e  << 1000. From life history traits and estimates of survival rates in the wild, we evaluate the compatibility of the species' biology and extremely low N _e / N ratios. Our data suggest that very small N _e 's are not likely to be of general concern for cod populations and, accordingly, most populations do not face any severe threat of losing evolutionary potential due to genetic drift.     

Survival, activity and feeding ability of Baltic cod (Gadus morhua) yolk-sac larvae at different salinities

Due to unfavourable conditions (declines in salinity and water oxygen content) in the spawning areas, there has been a considerable decrease in the Baltic cod stock since the beginning of the 1980s, and consequently a decrease in catches. In order to examine the feasibility of introducing yolk-sac larvae in areas of low salinity to improve the stock, laboratory experiments were performed on the effects of salinity on the survival, level of activity and feeding ability of larvae. Yolk-sac larvae from spawning cod caught off northern Gotland, Sweden, were exposed to four different salinities: 10 and 15%○ (salinities of the main spawning areas); and 5 and 7%○ (salinities in the Bothnian Sea and the Baltic proper respectively).
The survival of yolk-sac larvae was high at all salinities, even though there was an indication of higher mortality at low salinities in less viable larval groups. No differences were found in swimming speed or feeding ability at the four salinities, but a significant difference in vertical distribution was recorded. There were significant differences in survival, vertical distribution and feeding ability among larval groups, which indicates that larval quality or viability is of greater importance for larval survival than salinity, in the range of 5–15%○.     

The dispersal patterns and behaviour of North Sea cod (Gadus morhua) studied using electronic data storage tags*

The migratory behaviour of adult cod was studied using electronic data storage tags (DSTs). Fifty-eight cod were externally tagged with LOTEK LTD-100 DSTs and released off Lowestoft in March and April 1999. Twenty-two tags were returned by March 2000. Individuals demonstrated significant shifts in behaviour patterns that were associated with migration and residence on feeding grounds. During migration, individuals were very active and utilised a large vertical range. In contrast, individuals demonstrated low activity and a much reduced vertical range whilst on summer feeding grounds. Use of the Tidal Location Method showed that individuals dispersed to feeding grounds in the central and southern North Sea. Our results demonstrate that individual-based studies of fish behaviour can provide information relevant to fisheries management.