© 2005 International Council for the Exploration of the Sea
Differences in spawning time of captive Atlantic cod from four regions of Norway, kept under identical conditions
Institute of Marine Research PO Box 1870 Nordnes, N-5817 Bergen, Norway
*Correspondence to H. Otterå: tel: +47 55238500; fax: +47 55238531. e-mail: haakon{at}imr.no.
Several hundred Atlantic cod (Gadus morhua L.) were collected from selected spawning grounds along the Norwegian coast in March 2002. Four areas or regions that represent a wide range of environmental conditions were chosen for our breeding experiments: Porsangerfjord, Tysfjord, Helgeland, and Øygarden. Cod were transported to Øygarden near Bergen, individually tagged, and kept in sea cages. In both 2003 and 2004, a total of 40 family groups (adult pairs) representing the four regions were monitored for their spawning performance in separate tanks. During the spawning period, the quantity and diameter of eggs were recorded. During 2003, the time of peak spawning differed among groups. It was evident that the broodstock from the Øygarden region spawned about one month earlier than the broodstock collected from the Helgeland region. This also occurred in 2004, two years after the cod were collected, suggesting that the difference has a genetic component. Differences in life history parameters between cod populations, such as spawning cycles as described here, could be adaptive and under genetic control. This must be taken into consideration when assessing precautionary means of overcoming the problem with escapees from future cod mariculture.
Keywords: cod, Gadus morhua, genetic influence, local populations, mariculture, spawning time
Received 22 September 2004; accepted 7 November 2005.
 |
Introduction |
|---|
 Top Introduction Material and methodsResultsDiscussionReferences |
|---|
Knowledge of the genetic structure of wild cod populations is a prerequisite to understanding a wide range of issues dealing with cod mariculture. From an industrial perspective, it is important to select a wild broodstock that produces offspring with high performance in a farming situation, and that is adapted to the local mariculture conditions. For society in general, knowledge of the genetic structure of the species is essential in enabling us to evaluate potential environmental effects of cod farming. Escapees from net cages as well as natural spawning in pens can both contribute to the undesirable spread of farmed cod to the environment. These issues are highly relevant since cod mariculture is a rapidly growing industry. In Norway, annual juvenile production is about five million (2004) and is expected to increase rapidly. Cod mariculture is also developing in several other European countries and North America (Rosenlund and Skretting, 2006).
It is well established that there is genetic differentiation among Atlantic cod stocks in the northern Atlantic. The early studies of Møller (1966, 1968) demonstrated genetic differences among the migratory stocks of northeast Arctic cod or "skrei" and various groups of non-migratory coastal cod. Later allozyme studies revealed less differentiation, resulting in different interpretations of the geographic variation observed (Jørstad, 1984; Mork et al., 1985; Jørstad and Nævdal, 1989; Mork and Giæver, 1999). Recent studies using various DNA techniques, however, have revealed large genetic differences in the Pan 1 locus among cod populations in northern Norway (Fevolden and Pogson, 1995, 1997; Sarvas, 2005). In general, studies based on microsatellite analyses have documented a detailed and complex population structure of Atlantic cod in both the western (Bentzen et al., 1996; Ruzzante et al., 1998) and eastern Atlantic (Hutchinson et al., 2001; Nielsen et al., 2001; Imsland and Jonsdottir, 2002; Jonsdottir et al., 2002; Knutsen et al., 2003).
The biological consequences of genetic differentiation are understood more poorly. Imsland and Jonsdottir (2002) reviewed the stock-specific effects on growth in cod, but this is only one potential trait. Spawning behaviour in cod may also have a genetic component (Nordeide, 1998) and, thus, may be of importance to the genetic structure of populations (Bekkevold et al., 2002). Time of spawning may also be determined genetically in part, as has been shown in several other species (e.g. Pacific salmon species; Ricker, 1972). For Atlantic herring (Clupea harengus), both location and time of spawning are among the most important factors for maintaining the complex population structure (Iles and Sinclair, 1982; Sinclair, 1988; Stephenson et al., 2001). In a review of population structure of Atlantic cod in the western Atlantic, Ruzzante et al. (1999) summarized the genetic information available as well as biological parameters including spawning information (location and time) and natural hydrographic systems, and thus provided an overall explanation for the existence of genetic differentiation in the area.
In fish species with a pelagic egg stage, time of spawning is probably important for recruitment, as Cushing (1969) suggested in the "match–mismatch" hypothesis. Spawning that takes place too early or too late may mean that the start-feeding larvae will miss the zooplankton bloom, which is very important for successful first-feeding (e.g. Ellertsen et al., 1981; Taggart and Frank, 1990; Pepin and Myers, 1991; Sundby, 2000). Brander (1994) found a clear, but not conclusive, correlation between time of spawning and onset of primary production for cod spawning around the British Isles.
Many experiments have focused on the relationship between maternal characteristics and egg quality and viability. Factors such as female age, spawning experience, size, or condition can often be related to egg viability characteristics such as size, energy content, hatching success, etc., and to fecundity (e.g. Kjesbu, 1994; Trippel, 1998; Ouellet et al., 2001). Clemmesen et al. (2003) were even able to find indications that maternal characteristics influence the size of larvae several weeks after hatching.
The present contribution is part of a larger project, in which the spawning and life history attributes of progeny of coastal cod collected from four regions in Norway are being compared. Herein, we focus on the overall success and time of spawning of cod sampled from different regions, while the performance (growth and survival) of the offspring from the experiments will be reported elsewhere.
|
Material and methods |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
Four groups of wild coastal cod were collected, transferred to sea cages, and the natural spawning success of pairs of cod was monitored during two subsequent spawning seasons.
Collection of broodstock
The broodstocks used in the present experiment were collected from Porsangerfjord, Tysfjord, Helgeland, and Øygarden. The localities are spread along the Norwegian coast and represent a broad range of environmental conditions (Figure 1a, b). Broodstock collection was mainly carried out in cooperation with local fishers. Most of these fish were caught by Danish seine, cod traps, or hand gear (for details see Dahle et al., 2006). Fish were transported in tanks with running seawater to the Institute of Marine Research's Parisvatnet field station in Øygarden, west of Bergen, for spawning experiments. Most of the fish were collected in 2002, during the respective spawning seasons of each location, but an additional 40 fish from Tysfjord were collected in spring 2003. Collection of coastal cod from Porsangerfjord was decided upon biological (Jakobsen, 1987) and genetic (Jørstad, 1984) knowledge of the cod in this fjord.
|
The broodstock from each region was kept separately in net pens. Mortality was high during the first period of adaptation to farming conditions, mainly as a result of high summer temperature in combination with inadequate weaning to commercial feeds. In November 2002, after the period of cage adaptation, all surviving fish were measured (length and weight), individually tagged (PIT tags), and samples of blood, white muscle, and a fin clip were taken for genetic analysis (Dahle et al., 2006). After weaning to commercial dry feed (DanFeed, 1562) and tagging, the potential broodstock from all four groups was kept in a common net pen (100 m3) until individuals of each group were taken for use in the comparative spawning experiments.
Because of the high initial mortality, handling of the fish was minimized during the first period, and the spawning status for 2002 was not recorded. However, based on the broodstock size in November 2002 (Table 1) and otolith readings of similar sized fish from the same areas (Porsanger, Tysfjord, and Helgeland: Knut Jørstad, unpublished data; Øygarden: Otterå et al., 1999), it can be concluded that the fish were aged four to six years (Porsangerfjord four to eight years) and were mainly first- and second-time spawners during the first experiment. The Porsangerfjord group had the greatest proportion of second-time spawners, while few of the Tysfjord group were mature the first year.
|
Spawning experiment
Forty outdoor spawning tanks were used for the experiment. Each tank contained approximately 1.8 m3 water (diameter = 1.5 m, height = 1.2 m) and was made of glass fibre-reinforced polyester. The tanks were green inside and had a conical bottom. The water inlet and outlet were at the top of the tanks. The drained water was filtered through a fine-mesh net (500 µm), and placed in a water bath outside each tank so that spawned eggs could be collected and measured (see below). The water to the spawning tanks was taken from the sea at a depth of 20 m and filtered (300 µm) before it entered the tanks. Flow rate was approximately 20 l min–1 tank–1. The temperature during the spawning season was relatively stable, from 5 to 6°C in both years, and salinity varied from 32 to 34. The spawning tanks were covered by a black fine-mesh net, which reduced the light level by about 70%.
Before each spawning season, all available broodstock was measured and their maturation status evaluated. From each group (locality), we selected fish that were healthy and mature. Male–female pairs were transferred to individual spawning tanks in February, presumably before spawning had started. We tried to select males and females of similar size, but the limited quantity of broodstock made that difficult for some of the pairs. Few of the Tysfjord group were mature in the first spawning season; therefore, we chose not to include this group in the 2003 spawning set-up. Nine of the pairs used in 2003 were also used in the 2004 experiment.
The spawning success of the 40 pairs in the tanks was monitored during the spawning season. Monitoring lasted from 22 February to 9 April in 2003 and from 14 February to 3 May in 2004. Eggs were collected from the water-bath filters placed outside each tank every morning. The quantity of eggs was recorded, and the eggs were examined under a binocular microscope. Egg diameter, fertilization rate, cleavage status, and percentage of dead eggs were recorded (only egg diameter is reported here). Some of the egg batches were incubated and hatched for further evaluation of larval and juvenile quality in relation to egg quality and genetic background (results not reported here).
Several of the pairs did not spawn easily, even though the females were mature and ready for spawning. In such cases, we replaced either the female or the male with another from the holding cage, if available, or switched males between spawning tanks. All changes were made within each group. Where one of the partners died or was exchanged during the spawning period, the pair concerned was omitted from the analysis reported here. Table 1 gives an overview of the broodstock used in the experiment. Thorsen et al. (2003) give a general overview of methods related to experimental spawning of cod.
|
Results |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
From the 40 couples of cod that participated in the experiment each year, we managed to obtain eggs from, and to follow through the spawning period, 34 pairs in 2003 and 32 pairs in 2004. Most of the remaining pairs also produced some eggs, but were omitted from the analysis owing to death and/or replacement.
Spawning was very regular for some of the pairs, with spawning every third day accompanied by a decrease in egg diameter during the season (Figure 2). Many of the pairs, however, displayed less regular spawning, with longer and more variable intervals between each batch. Average batch size was 556 ml in 2003 and 599 ml in 2004, and 65% of the batches were between 200 and 1200 ml. Overall, there was a decrease in egg diameter through the spawning period, from around 1.4 mm in mid-February to around 1.2–1.3 mm towards the end of the spawning period (Figure 3). The Porsangerfjord group had the largest mean egg size in both years (2003: mean = 1.36, s.d. = 0.06; 2004: mean = 1.37, s.d. = 0.08), followed by Øygarden (2003: mean = 1.34, s.d. = 0.07; 2004: mean = 1.35, s.d. = 0.08), Helgeland (2003: mean = 1.30, s.d. = 0.06; 2004: mean = 1.31, s.d. = 0.06), and Tysfjord (2004: mean = 1.31, s.d. = 0.09).
|
|
There were differences in time of peak spawning between groups in both 2003 and 2004. In both years, the Øygarden group, followed by Porsangerfjord, spawned earliest and Helgeland latest. In terms of volume of collected eggs, the Øygarden group had spawned 50% of the eggs by 9 March in 2003 and 4 March in 2004 (Figure 4). The corresponding dates are 17 March and 11 March for Porsangerfjord, 23 March for Tysfjord (2004 only), and 26 March and 30 March for Helgeland. In 2003 and possibly also in 2004, the Øygarden group had started spawning before data collection started, which means that some records are missing on the leftmost bar in Figure 4. Furthermore in 2003, monitoring was stopped before all groups had finished spawning, so that the latest batches from the Helgeland group are missing in Figure 4. As a result, the differences in spawning time among groups are underestimated. Despite the incomplete data presented, it is quite clear that peak spawning in the Øygarden group occurred at least one month before the Helgeland group, and this persisted even in the second year.
|
|
Discussion |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
The most interesting observation from this experiment was that time of peak spawning differed between the broodstocks originating from different regions along the Norwegian coast. These broodstocks were held in the same environment from July of the year before the first spawning experiment. The fact that the differences persisted even during the second spawning season after capture suggests that spawning time in cod is genetically determined to some extent.
Concurrent with the collection of broodstock, genetic screening of the cod populations in the four areas was performed. Both the actual broodstock and additional samples were analysed for a number of gene markers (haemoglobin Hbib1, allozymes, Pan 1, and microsatellites). The results are reported in detail in Dahle et al. (2006). Overall, the results demonstrated significant genetic differences among cod from the four areas (all 17 loci, Fst = 0.015). The Tysfjord and Helgeland groups were estimated to be closest. The largest values of Fst were found for the Pan 1, Hbib1, and Gmo132 loci. As opposed to the migratory northeast Arctic cod, Norwegian coastal cod used in the current experiment are believed to be relatively stationary (Bergstad et al., 1987).
The broodstock used in this experiment originated in regions with different temperature and light regimes. In laboratory experiments, Hansen et al. (2001) observed that manipulating photoperiod changed the incidence of sexual maturation, spawning time, fecundity, and egg size in captive cod. Temperature has a strong effect on growth (e.g. Otterlei et al., 1999), and also, indirectly, on size at maturity. It is likely, therefore, that subpopulations of cod are adapted to local environmental conditions, as is suggested by our results. The differences in spawning time shown in the present experiment, however, are not related directly to a north–south gradient, or temperature or light regime (Figure 1b). In Norwegian coastal cod, spawning time may differ by several weeks in spawning groups only a few kilometres from one another (Knut Jørstad, unpublished data). Therefore, the mechanisms for control of spawning time are probably influenced by a number of genetic, environmental, and maternal factors. Quantitative trait loci (QTL) are likely to be involved in the genetic factors, and this should be studied in greater detail through experimental manipulations. Recently, such studies have been carried out in rainbow trout (Oncorhynchus mykiss) using a large number of DNA markers. In these studies, QTLs associated with spawning time (Sakamoto et al., 1999) as well as upper temperature tolerance (Danzmann et al., 1999) were demonstrated.
The experimental set-up used in the present study, where broodstocks are reared under identical conditions prior to spawning, should eliminate most of the direct environmental influence on spawning time between the groups. Maturation of oocytes starts about six months prior to spawning (Anders Thorsen, Institute of Marine Research, pers. comm.), while the broodstock was transferred to a common environment at least seven months before spawning. Therefore, even for the 2003 experiment, females should have had an identical environment through the maturation cycle. Maternal factors like female size and spawning experience are also believed to be important in determining spawning success in cod (Trippel et al., 1997). However, Kjesbu (1994) found no clear relation between fish length and start of spawning for wild Arcto-Norwegian cod, while fecundity increased with female size (Kjesbu et al., 1996). Our broodstock groups were relatively similar in size and age structure, suggesting that maternal effects were of minor importance to the results.
The expected large increase in cod mariculture in Norway and other countries around the North Atlantic may have ecological and genetic consequences for the wild population of cod. The preliminary results presented in the current paper suggest that the selection of broodstock should be carefully considered. The use of a non-native broodstock followed by escapement from sea cages could have a detrimental influence on local stocks. Probably most important, as has been demonstrated in Atlantic salmon (McGinnity et al., 2004), is the possible interbreeding between farmed and wild populations resulting in a decrease in overall fitness. Therefore, further research on the performance of cod related to their genetic origin and its potential influence on wild populations is highly recommended.
|
Acknowledgements |
|---|
We appreciate the skilled technical assistance of Jan Pedersen, Bjørnar Skjold, Beate Hoddevik, Gunnar Bakke, Ole Ingar Paulsen, and Eva Farestveit during the experiment. The Norwegian Ministry of Fisheries financed the project.
|
References |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
-
Aure J. and Strand Ø. (2001) Hydrographic normals and long-term variations at fixed surface layer stations along the Norwegian coast from 1936 to 2000. Institute of Marine Research, Bergen, Norway, 13. 26 pp. (In Norwegian, abstract in English).
Bekkevold D., Hansen M.M., Loeschcke V. (2002) Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.). Molecular Ecology 11:91–102.[CrossRef][Medline]
Bentzen P., Taggart C.T., Ruzzante D.E., Cook D. (1996) Microsatellite polymorphism and the population structure of Atlantic cod (Gadus morhua) in the northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 53:2706–2721.
Bergstad O.A., Jørgensen T., Dragesund O. (1987) Life history and ecology of the gadoid resources of the Barents Sea. Fisheries Research 5:119–161.[CrossRef][Web of Science]
Brander K.M. (1994) The location and timing of cod spawning around the British Isles. ICES Journal of Marine Science 51:71–89.
Clemmesen C., Buhler V., Carvalho G., Case R., Evans G., Hauser L., Hutchinson W.F., Kjesbu O.S., Mempel H., Moksness E., Otterå H., Paulsen H., Thorsen A., Svaasand T. (2003) Variability in condition and growth of Atlantic cod larvae and juveniles reared in mesocosms: environmental and maternal effects. Journal of Fish Biology 62:706–723.[CrossRef][Web of Science]
Cushing D.H. (1969) The regularity of the spawning season of some fishes. Journal du Conseil International pour l'Exploration de la Mer 33:81–92.
Dahle G., Jørstad K.E., Rusaas H.E., Otterå H. (2006) Genetic characterization of broodstock of Atlantic cod, Gadus morhua, collected from four Norwegian coastal cod populations. ICES Journal of Marine Science 63:209–215.
Danzmann R.G., Jackson T.R., Ferguson M. (1999) Epistasis in allelic expression at upper temperature tolerance QTL in rainbow trout. Aquaculture 173:45–58.[CrossRef][Web of Science]
Ellertsen B., Solemdal P., Sundby S., Tilseth S., Westgård T., Øiestad V. (1981) Feeding and vertical distribution of cod larvae in relation to availability of prey organisms. Rapports et Procès-verbaux des Réunions du Conseil International pour l'Exploration de la Mer 178:317–319.
Fevolden S. and Pogson G. (1997) Genetic divergence at the synaptophysin (Syp I) locus among Norwegian coastal and north-east Arctic populations of Atlantic cod. Journal of Fish Biology 51:895–908.[Web of Science]
Fevolden S.E. and Pogson G.H. (1995) Differences in nuclear DNA RFLPs between the Norwegian coastal and the northeast Arctic population of Atlantic cod. In Skjoldal H.R., Hopkins C., Erikstad K.E., Leinaas H.P. (Eds.). Ecology of Fjords and Coastal Waters(Elsevier Science B.V., Amsterdam) pp. 403–415 623 pp.
Hansen T., Karlsen Ø., Taranger G.L., Hemre G.I., Holm J.C., Kjesbu O.S. (2001) Growth, gonadal development and spawning time of Atlantic cod (Gadus morhua) reared under different photoperiods. Aquaculture 203:51–67.[CrossRef][Web of Science]
Hutchinson W.F., Carvalho G.R., Rogers S.I. (2001) Marked genetic structuring in localised spawning populations of cod Gadus morhua in the North Sea and adjoining waters, as revealed by microsatellites. Marine Ecology Progress Series 223:251–260.[Web of Science]
Iles T.D. and Sinclair M. (1982) Atlantic herring stock discreteness and abundance. Science 215:627–633.
Imsland A.K. and Jonsdottir O.D.B. (2002) Is there a genetic basis to growth in Atlantic cod? Fish and Fisheries 3:36–52.[CrossRef]
Jakobsen T. (1987) Coastal cod in northern Norway. Fisheries Research 5:223–234.[CrossRef][Web of Science]
Jonsdottir O.D.B., Imsland A.K., Danielsdottir A.K., Marteinsdottir G. (2002) Genetic heterogeneity and growth properties of different genotypes of Atlantic cod (Gadus morhua L.) at two spawning sites off south Iceland. Fisheries Research 55:37–47.[CrossRef][Web of Science]
Jørstad K.E. (1984) Genetic analyses of cod in northern Norway. In Danielssen D.S., Moksness E., Solemdal P. (Eds.). The Propagation of Cod, Gadus morhua L. pp. 745–760 Flødevigen Rapportserie, 1.
Jørstad K.E. and Nævdal G. (1989) Genetic variation and population structure of cod, Gadus morhua L, in some fjords in northern Norway. Journal of Fish Biology 35:245–252.[Web of Science]
Kjesbu O.S. (1994) Time of start of spawning in Atlantic cod (Gadus morhua) females in relation to vitellogenic oocyte diameter, temperature, fish length and condition. Journal of Fish Biology 45:719–735.[CrossRef][Web of Science]
Kjesbu O.S., Solemdal P., Bratland P., Fonn M. (1996) Variation in annual egg production in individual captive Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 53:610–620.
Knutsen H., Jorde P.E., Andre C., Stenseth N.C. (2003) Fine-scaled geographical population structuring in a highly mobile marine species: the Atlantic cod. Molecular Ecology 12:385–394.[CrossRef][Medline]
McGinnity P., Prodohl P., O Maoileidigh N., Hynes R., Cotter D., Baker N., O'Hea B., Ferguson A. (2004) Differential lifetime success and performance of native and non-native Atlantic salmon examined under communal natural conditions. Journal of Fish Biology 65:173–187.[CrossRef][Web of Science]
Mork J. and Giæver M. (1999) Genetic structure of cod along the coast of Norway: results from isozyme studies. Sarsia 84:157–168.[Web of Science]
Mork J., Ryman N., Ståhl G., Utter F., Sundnes G. (1985) Genetic variation in Atlantic cod (Gadus morhua L.) throughout its range. Canadian Journal of Fisheries and Aquatic Sciences 42:1580–1587.
Møller D. (1966) Genetic differences between cod groups in the Lofoten area. Nature 212:824.[Medline]
Møller D. (1968) Genetic diversity in spawning cod along the Norwegian coast. Hereditas 60:1–32.[Medline]
Nielsen E.E., Hansen M.M., Schmidt C., Meldrup D., Gronkjaer P. (2001) Fisheries – population of origin of Atlantic cod. Nature 413:272.[CrossRef][Medline]
Nordeide J.T. (1998) Coastal cod and north-east Arctic cod – do they mingle at the spawning grounds in Lofoten? Sarsia 83:373–379.[Web of Science]
Otterå H., Kristiansen T.S., Svåsand T., Nordeide J.T., Nævdal G., Borge A., Pedersen J.P. (1999) Enhancement studies of Atlantic cod (Gadus morhua L.) in an exposed coastal area in western Norway. In Howell B.R., Moksness E., Svåsand T. (Eds.). Stock Enhancement and Sea RanchingFishing News Books, Blackwell Science Ltd, Oxford. pp. 257–276.
Otterlei E., Nyhammer G., Folkvord A., Stefansson S.O. (1999) Temperature- and size-dependent growth of larval and early juvenile Atlantic cod (Gadus morhua): a comparative study of Norwegian coastal cod and northeast Arctic cod. Canadian Journal of Fisheries and Aquatic Sciences 56:2099–2111.
Ouellet P., Lambert Y., Bérubé I. (2001) Cod egg characteristics and viability in relation to low temperature and maternal nutritional condition. ICES Journal of Marine Science 58:672–686.
Pepin P. and Myers R.A. (1991) Significance of egg and larval size to recruitment variability of temperate marine fish. Canadian Journal of Fisheries and Aquatic Sciences 48:1820–1828.
Ricker W.E. (1972) Hereditary and environmental factors affecting certain salmonid populations. In Simon R.C. and Larkin P.A. (Eds.). The Stock Concept of Pacific Salmon(The University of British Columbia, Vancouver) pp. 19–160.
Rosenlund G. and Skretting M. (2006) Worldwide status and perspective on gadoid culture. ICES Journal of Marine Science 63:194–197.
Ruzzante D.E., Taggart C.T., Cook D. (1998) A nuclear DNA basis for shelf- and bank-scale population structure in northwest Atlantic cod (Gadus morhua): Labrador to Georges Bank. Molecular Ecology 7:1663–1680.[CrossRef]
Ruzzante D.E., Taggart C.T., Cook D. (1999) A review of the evidence for genetic structure of cod (Gadus morhua) populations in the Northwest Atlantic and population affinities of larval cod off Newfoundland and the Gulf of St. Lawrence. Fisheries Research 43:79–97.[Medline]
Sakamoto T., Danzmann R.G., Okamoto N., Ferguson M.M., Ihssen P.E. (1999) Linkage analysis of quantitative trait loci associated with spawning time in rainbow trout (Oncorhynchus mykiss). Aquaculture 173:33–43.[CrossRef][Web of Science]
Sarvas T. (2005) The Pan I locus and population structure of cod (Gadus morhua L.) in Norway. PhD thesis, University of Tromsø, Norway. 132 pp.
Sinclair M. (1988) Marine Populations. An Assay on Population Regulation and Speciation(University of Washington Press, Seattle, USA) 252 pp.
Stephenson R.L., Clark K.J., Power M.J., Fife F.J., Melvin G.D. (2001) Herring stock structure, stock discreteness and biodiversity. In Funk F., Blackburn J., Hay D., Paul A.J., Stevenson R., Toresen R., Witherell D. (Eds.). Herring: Expectations for a New Millennium(University of Alaska Sea Grant, Fairbanks) pp. 559–571 AK-SG-01-04.
Sundby S. (2000) Recruitment of Atlantic cod stocks in relation to temperature and advection of copepod populations. Sarsia 85:277–298.[Web of Science]
Taggart C.T. and Frank K.T. (1990) Perspectives on larval fish ecology and recruitment processes. Probing the scales of relationships. In Sherman K., Alexander L.M., Gold B.D. (Eds.). Large Marine Ecosystems(American Association for the Advancement of Science, Washington, USA) pp. 151–164.
Thorsen A., Trippel E.A., 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.
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.[CrossRef]
Trippel E.A., Kjesbu O.S., Solemdal P. (1997) Effects of adult age and size structure on reproductive output in marine fishes. In Chambers R.C. and Trippel E.A. (Eds.). Early Life History and Recruitment in Fish Populations(Chapman & Hall, London) pp. 31–62.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  E. K. Stenevik, S. Sundby, and A. L. Agnalt Buoyancy and vertical distribution of Norwegian coastal cod (Gadus morhua) eggs from different areas along the coast ICES J. Mar. Sci., October 1, 2008; 65(7): 1198 - 1202. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Dahle, K.E. Jorstad, H.E. Rusaas, and H. Ottera Genetic characteristics of broodstock collected from four Norwegian coastal cod (Gadus morhua) populations ICES J. Mar. Sci., January 1, 2006; 63(2): 209 - 215. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Kolstad, I. Thorland, T. Refstie, and B. Gjerde Body weight, sexual maturity, and spinal deformity in strains and families of Atlantic cod (Gadus morhua) at two years of age at different locations along the Norwegian coast ICES J. Mar. Sci., January 1, 2006; 63(2): 246 - 252. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||