© 2006 International Council for the Exploration of the Sea
Variation in the frequency of skipped spawning in Atlantic cod (Gadus morhua) off Newfoundland and Labrador
Department of Fisheries and Oceans PO Box 5667, St John's, NL A1C 5X1, Canada
*Correspondence to R. M. Rideout: tel: +1 709 772 6975; fax: +1 709 772 4105. e-mail: rideoutr{at}dfo-mpo.gc.ca.
Macroscopic maturity data collected between January and March of 1978–2004 during groundfish surveys were analysed to determine the frequency of skipped spawning for Atlantic cod (Gadus morhua) populations in the Northwest Atlantic. Nearly 18% of the 6583 potential female spawners sampled during this period would not have spawned in the subsequent spawning season. The frequency of skipped spawning was much higher on the Flemish Cap (NAFO Division 3M, 
33%) and off the south coast of Newfoundland (Subdivision 3Ps, 21%) than that in three areas off eastern Newfoundland and southern Labrador (Divisions 3L, 8%; 3K, 3%; and 2J, <1%). Annual variation in the frequency of skipped spawning was apparent in all areas. Skipped spawning was most common in fish of medium size (60–79 cm). Non-reproductive cod were characterized by lower liver condition than reproductive cod, but not a lower gutted condition. Generalized linear models suggested that relative liver weight was the best predictor of spawning probability, and that age, length, and relative body condition were not good predictors. Models of spawning probability based on relative liver condition suggest that female fish in poor condition in 3KL are more likely to spawn than fish of equal condition in areas 3M and 3Ps.
Keywords: egg production, Gadus morhua, reproduction, reproductive potential, skipped spawning, spawning
 |
Introduction |
|---|
 Top Introduction MethodsResultsDiscussionReferences |
|---|
A growing body of evidence suggests that adverse environmental conditions can result in fish suppressing gamete development and subsequently failing to spawn. This interruption of the normal ripening cycle can occur in both recruit- and repeat-spawners. In the latter case, failure to spawn results in non-annual or skipped spawning (reviewed by Rideout et al., 2005). Skipped spawning can take place through failure to start vitellogenesis or by starting vitellogenesis and subsequently undergoing mass atresia of all vitellogenic oocytes. It is usually linked to poor nutritional condition attributable to reduced prey availability (Rideout et al., 2005). For example, skipped spawning in northern Canadian lakes has been attributed to the short growing season, which may not allow fish to accumulate sufficient energy to support egg production in consecutive years (Kennedy, 1953; Dutil, 1986). Likewise, for orange roughy (Hoplostethus atlanticus) off Australia, skipped spawning may result from the scarce or patchy prey available in this species' deepwater habitat (Bell et al., 1992). Experimental work on captive fish has demonstrated that skipped spawning can be induced through nutritional deprivation (Hislop et al., 1978; Burton and Idler, 1987; Rijnsdorp, 1990; Maddock and Burton, 1994). Skipped spawning may also be related to low availability of specific types of prey. For example, Rideout and Rose (in press) demonstrated that cod (Gadus morhua) of medium size that failed to ripen successfully had significantly higher
13C values than fish that would have spawned, suggesting that they fed more extensively on benthic organisms (presumably pandalid shrimp) than pelagic organisms (presumably capelin, Mallotus villosus). For Flemish Cap cod, skipping a spawning season was linked to low liver condition (Morgan and Lilly, in press), perhaps as a result of fluctuations in the availability of juvenile redfish as prey (Lilly, 1985; Walsh et al., 1986). From a life-history standpoint, skipped spawning may be an adaptive trait. Jørgensen et al. (2006), based on an energy-allocation life-history model, suggested that spawning should be skipped if the expected future gain in reproductive output, discounted by survival, is greater than the expected reproductive success in the current year. Small, short-lived fish are likely to have fewer opportunities to reproduce than longer-living species, and are therefore more likely to invest maximum energy in each reproductive episode even at the risk of increasing post-spawning mortality (i.e. less likely to skip an opportunity to reproduce; Rideout et al., 2005). In longer-living species, however, suppressing gamete development in a year of poor condition can increase the probability of surviving to spawn in subsequent years. In Atlantic cod, skipping spawning when the probability of post-spawning survival is low, such as when fish are in poor condition (Lambert and Dutil, 2000), may increase an individual's lifetime reproductive output by >40% (Rideout et al., 2005).
For cod, skipped spawning appears to be widespread, with reports of non-reproductive fish from the Northwest Atlantic (Walsh et al., 1986; Burton et al., 1997; Schwalme and Chouinard, 1999; Rideout et al., 2000; Morgan and Lilly, in press; Rideout and Rose, in press), the Baltic Sea (Shirokova, 1969), and the Barents Sea (Woodhead and Woodhead, 1965; Oganesyan, 1993; Marshall et al., 1998). Although such reports suggest that reproductive development may be interrupted over the entire geographic range of cod, data are usually insufficient to determine the frequency of skipped spawning in any given area or year. The frequency of skipped spawning has been reported to be very high (sometimes in excess of 40%) for both Flemish Cap (Walsh et al., 1986) and Smith Sound cod (Rideout and Rose, in press). However, cod aggregations in both these areas are somewhat different from those in other parts of the Northwest Atlantic. Cod on the Flemish Cap, an isolated bank to the east of Grand Bank (Figure 1), do not migrate off the Cap and are genetically distinct from other cod stocks (Beacham et al., 2000). Cod in Smith Sound, a small fjord-like inlet on the east coast of Newfoundland (NAFO Division 3L), may not be genetically distinct from fish in nearby areas (Beacham et al., 2000), but they behave differently from most cod in the 2J + 3KL area in that they reside inshore throughout winter instead of undertaking the offshore migration to warmer water historically characteristic of offshore populations (Goddard and Fletcher, 1994; Rose, 2003). The high frequency of skipped spawning observed in these areas may not be typical of cod throughout the Newfoundland and Labrador area.
|
Determining the frequency of skipped spawning is important in understanding the true reproductive potential of a fish population. For example, Rideout and Rose (in press) reported that failure to account for non-reproductive individuals could result in overestimation of population egg production by 8–41% annually in the Smith Sound cod aggregation. Limit reference points under the precautionary approach are often chosen as the spawning-stock biomass below which recruitment is seriously impaired (Mace and Sissenwine, 1993; Shelton and Rivard, 2003). Additionally, predictions about the potential for depleted stocks to rebuild will depend on the underlying assumptions about the stock-recruit relationship. Therefore, reliable estimates of reproductive potential, including the frequency of spawning omission, will play an important role in effective management.
In the current study, we use research vessel survey data to assess the frequency of skipped spawning in NAFO Divisions 2J, 3K, 3L, and 3M, and in Subdivision 3Ps, in an attempt to gauge the significance of skipped spawning to the overall productivity of cod stocks.
|
Methods |
|---|
|
TopIntroductionMethodsResultsDiscussionReferences |
|---|
Data collected during bottom trawl and acoustic surveys, as well as tagging studies (Table 1), were used to determine the frequency of skipped spawning in NAFO Divisions 2J, 3K, 3L, and 3M, and in Subdivision 3Ps. All fish were collected offshore. Only data for females were considered. Maturity stages were assigned according to the classification of Templeman et al. (1978) following macroscopic inspection of the ovaries. Females with small, pink ovaries were classified as immature, and those with opaque oocytes as ripening. Only data from January to March were included in the analyses. Females with small, firm, red ovaries with no opaque oocytes at that time of year were considered non-reproductive (i.e. skipped spawners; corresponding to the "spent L" maturity stage of Templeman et al., 1978). Previous studies on Northwest Atlantic cod have demonstrated the majority of such ovaries to be undergoing mass atresia of all vitellogenic oocytes (Walsh et al., 1986; Rideout et al., 2000), which would have rendered the fish incapable of spawning in the upcoming spawning season. In this case, the phrase non-reproductive is used to indicate a potential spawner that fails to complete vitellogenesis and is therefore not capable of spawning. The phrase post-mature non-reproductive has been used previously to include only non-spawning fish that have spawned successfully in the past (Burton and Idler, 1984). Without the use of histology, it was not possible to distinguish between fish that had spawned in the past and those that had not (Rideout et al., 2005). The frequency of skipped spawning per area or year was calculated as the number of non-reproductive females divided by the total number of mature females sampled. Fish were grouped into 10-cm size classes in order to compare the frequency of skipped spawning among cod of different size.
|
Condition indices were compared between reproductive and non-reproductive females to test the hypothesis that skipped spawning was caused by insufficient energy reserves to fuel gamete development. For this purpose, only fish that were ripening but showed no signs of having started to spawn were included as reproductive, whereas those that had started or finished spawning were not included in the analyses. None of the non-reproductive females collected from 2J had been sampled for body weight data, so 2J was excluded from the analyses of condition. Only a limited number of non-reproductive cod from 3K and 3L had been sampled for weight, so the areas were pooled as 3KL. Fulton's K was calculated as K = W(100/L3), where W is gutted weight in g and L is fork length in cm. Hepatosomatic index was calculated as HSI = (liver weight/W)100%. To alleviate possible correlations between condition indices and fish length, comparisons between reproductive and non-reproductive individuals were made by grouping fish into 10-cm size classes. Condition indices were then compared for each size class using single-factor analysis of variance. In addition, alternative length-independent indices of condition were calculated. Relative K (Kr) and relative liver condition (LKr) were calculated from:
|
|
|
|
and 
are the predicted body weight and liver weight, respectively, from the following length/weight relationships: |
|
|
|
Using quadratic rather than linear relationships resulted in relative condition indices that were not correlated with length (p = 0.9526 for Kr; p = 0.3536 for LKr) whereas those produced using linear relationships were correlated with length (p = 0.0005 for Kr; p = 0.0003 for LKr). For comparisons among areas, Kr and LKr were based relative to predicted values from the relationships between length and gutted weight and length and liver weight, for all data combined. However, when examining these condition indices within a single area, they were looked at relative to predicted values based on fish only from that area.
Generalized linear models were used to determine if age, length, Kr, or LKr significantly influenced the probability of spawning. Ripening females were considered spawners (1), and non-reproductive females were considered non-spawners (0). Age and length were modelled as class variables, and Kr and LKr were modelled as continuous variables. Because of limited sample size in some size classes, each factor was tested separately instead of trying to build an overall model containing several factors. All models had a logit link function and a binomial error structure. Analyses were restricted to fish between 40 and 90 cm because few fish smaller or larger than this range were available.
Pseudo r2 values (Swartzman et al., 1992) were calculated in order to compare the proportion of the deviation accounted for by age, length, Kr, and LKr. This pseudo coefficient of determination was calculated as the deviance in the model containing only the intercept minus the deviance after adding the main factor (e.g. LKr), divided by the null deviance of the model containing only the intercept.
|
Results |
|---|
|
TopIntroductionMethodsResultsDiscussionReferences |
|---|
A total of 18 437 female fish were sampled between 1978 and 2004 (Table 1). Of these, 6583 were considered potential spawners, and nearly 18% of the potential spawners were non-reproductive. There was a high degree of spatial and temporal variability in the frequency of non-reproductive fish (Table 2), with a very low frequency in NAFO Divisions 2J and 3K (<4%), slightly higher in 3L (
8%), and very high in 3M (33%) and 3Ps (21%). Within 3M the proportion ranged from >15% in 1982 to nearly 51% in 1978, and in 3Ps it ranged from 11% in 1987 to nearly 46% in 1978. In 2J, non-reproductive fish were observed in only 1 of the 9 years sampled, although sample sizes were generally small. In 3K, 5 of the 15 years that fish were sampled revealed no evidence of skipped spawning, and in the remaining years the proportion of non-reproductive fish ranged from <1% to nearly 19%. In 3L, there were 4 years with no non-reproductive fish, whereas the remaining 5 years had between 5% and 21% non-reproductive females. Although the data were temporally variable, there were no temporal trends in the proportion of non-reproductive individuals (Table 2).
|
Overall, the proportion of non-reproductive fish was greatest between 60 and 79 cm (Table 3). In 3L and 3Ps, the greatest proportion of non-reproductive fish was in the 60–89 cm range, whereas in 3M the greatest proportion was in the 50–79 cm size range.
|
Differences in Fulton's condition factor between reproductive and non-reproductive females were generally small, whereas the hepatosomatic index was significantly (p < 0.05) smaller in non-reproductive individuals than in individuals that were ripening, in nearly all size classes (Figure 2). Differences in liver size between reproductive and non-reproductive females were also evident when measured as relative liver condition (Figure 3).
|
|
Results of the generalized linear models confirmed that relative liver condition had the largest influence on the probability of spawning in Newfoundland and Labrador cod (Table 4). Overall, the model containing LKr explained >17% of the variability in the probability of spawning; all other factors explained <2.2% of the variability. When analysed by area, the model containing liver condition explained 14%, 18%, and 12% of the variability in the probability of spawning in areas 3KL, 3M, and 3Ps, respectively. Although some other factors had statistically significant influences on the probability of spawning, the amount of variation explained by those factors was very low. For example, in 3Ps, the effect of Kr was significant (p = 0.0015), but the model explained just 1.2% of the observed variation.
|
The effect of LKr on the probability of spawning is apparent both when calculated relative to all fish sampled and when calculated relative to only the fish sampled in that given area (Figure 4). There was a significant area effect on the relationship between LKr and the predicted probability of spawning (p < 0.0001), all three NAFO Divisions differing from each other (Figure 4a). These differences are particularly evident at very low values of LKr. Fish in 3KL were more likely to spawn at low LKr than fish from other areas.
|
Comparison of LKr values between areas using single-factor analysis of variance suggested a difference in condition (p < 0.0001) between the study areas, and a posteriori analyses revealed cod to be in significantly better condition in 3KL than in 3Ps, but not than in 3M, and no significant difference was found in condition between 3M and 3Ps.
|
Discussion |
|---|
|
TopIntroductionMethodsResultsDiscussionReferences |
|---|
The data support the hypothesis that skipped spawning is relatively common for Newfoundland and Labrador cod, and not just confined to somewhat isolated and perhaps nutritionally deprived populations such as those of Smith Sound (Rideout et al., 2000; Rideout and Rose, in press) and the Flemish Cap (Walsh et al., 1986; Morgan and Lilly, in press). The widespread skipping of spawning by cod is not entirely a surprise, because many such claims have been made previously for the species (Woodhead and Woodhead, 1965; Oganesyan, 1993; Burton et al., 1997; Marshall et al., 1998; Schwalme and Chouinard, 1999). Reports of skipped spawning are not limited to cod, but have been made for a number of freshwater, anadromous, and marine fish (reviewed by Rideout et al., 2005). In the Northwest Atlantic, skipped spawning has been reported for other important commercial groundfish such as winter flounder (Pseudopleuronectes americanus; Burton and Idler, 1984), American plaice (Hippoglossoides platessoides; Pitt, 1966), and Greenland halibut (Reinhardtius hippoglossoides; Walsh and Bowering, 1981).
What may be somewhat surprising is the extent of skipped spawning observed for cod. Energy-allocation life-history models for cod have predicted large proportions of skipped spawning (Jørgensen et al., 2006), but the data presented here are among the first to support this prediction. In all, 18% of the potential female spawners sampled since 1978 (in the winter) would not have spawned. In areas 3M and 3Ps, the extent of skipped spawning in some years was >40%. Such findings can greatly influence perceived stock productivity and management strategies. With so many potential spawners failing to spawn in a given year, erroneous inclusion of these fish as part of the spawner biomass can result in overestimating population reproductive potential. For example, Rideout and Rose (in press) reported that failure to recognize the non-spawning portion of the adult cod biomass in Smith Sound, Newfoundland, resulted in overestimation of total egg production by 8–41% annually between the years 1999 and 2004.
The notable extent of skipped spawning was not characteristic of all areas analysed. Northern areas (2J + 3KL) appeared to contain very few non-reproductive females, in comparison with 3M and 3Ps. It is uncertain why such differences exist, but in cod and other species, skipped spawning has been related to fish nutritional condition and diet (Kennedy, 1953; Hislop et al., 1978; Dutil, 1986; Burton and Idler, 1987; Rijnsdorp, 1990; Maddock and Burton, 1994; Rideout et al., 2000; Rideout and Rose, in press). The prey spectrum of cod on the Flemish Cap (3M) is particularly narrow, consisting largely of shrimp, hyperiids, and redfish (Lilly, 1985; Albikovskaya and Gerasimova, 1993; Casas and Paz, 1996). It has been speculated that high levels of skipped spawning in this area in some years may be related to low abundance of juvenile redfish (Walsh et al., 1986). Capelin has historically been the most important prey item for cod in other areas, and low abundance of capelin has had negative impacts on cod reproductive success. For example, both reduced fecundity and skipped spawning in Barents Sea cod have been attributed to low abundance of capelin (Oganesyan, 1993; Kjesbu et al., 1998; Marshall et al., 1998). The low 13C signatures of non-reproductive cod from inshore Newfoundland suggested that they had been feeding less on capelin and more on shrimp than reproductive cod (Rideout and Rose, in press). Changes in capelin distribution during the timeframe of this study make it difficult, however, to explain differences in the prevalence of skipped spawning between 2J + 3KL and 3Ps on the basis of capelin availability. Distribution and abundance of capelin began shifting south in the late 1980s, and capelin became less available to fish in the north, while remaining prominent in the diet of cod more to the south (Lilly, 1994; Carscadden and Nakashima, 1997; Rose and O'Driscoll, 2002). Capelin have been prominent in the diet of 3Ps cod in recent years (Rose and O'Driscoll, 2002; Rideout and Rose, in press). Soviet research suggested that sandlance (Ammodytes spp.) was a major prey item for cod in this area in 1959 and 1960 (Popova, 1962). No feeding data, however, are available for cod in 3Ps for the years examined in the current study. The high levels of skipped spawning observed for cod in this area might indicate low levels of capelin or sandlance feeding during these years. Alternatively, cod may have skipped spawning despite feeding on capelin or sandlance. The energy-allocation life-history model presented by Jørgensen et al. (2006) predicted the prevalence of skipped spawning to increase not only at low but also at high prey availability. This latter scenario is based on the fact that improved growth through increased food intake should increase future fecundity, making skipping spawning in favour of continued feeding an attractive option for increasing lifetime reproductive output.
If diet is responsible for the differences in the propensity to skip spawning in the different areas, it is only partially reflected in the differences in fish condition between the three areas. For example, fish in 3KL were in better condition than those from 3Ps (data for all years combined), which may partially explain the lesser probability of skipping spawning in 3KL. However, the condition of fish in 3KL did not differ significantly from that of fish in 3M, and 3M actually had the highest proportion of non-reproductive fish. It is important here to remember that fish condition in this region follows a seasonal cycle, increasing over the summer feeding period and decreasing during the reproductive period, when feeding is highly reduced. Therefore, the condition of fish when they are sampled may not reflect their condition when the decision to skip spawning was made. Burton (1994) suggested that a critical period exists for winter flounder, whereby individuals not attaining sufficient food immediately following the completion of spawning would not spawn in the subsequent year. If a similar pattern exists for cod, then the condition indices that most explain the decision to skip spawning may occur before it is even possible to distinguish spawners from those that will skip spawning.
It is important here to distinguish between the probability of being an adult and the probability of an adult fish spawning (or skipping spawning). The probability of a fish being an adult tends to increase with age and size (Korsbrekke, 1999; Morgan and Colbourne, 1999), but it can also be influenced by fish condition (Bromley et al., 2000; Marteinsdottir and Begg, 2002; Morgan, 2004) and growth rate, fish with fast growth rates maturing earlier (Rijnsdorp, 1993; Morgan and Colbourne, 1999). In addition, temperature can influence the timing of maturation through influences on growth rate (Sandstrom et al., 1995). In the case of skipped spawning, a fish has already achieved sexual maturity so the probability of spawning in the upcoming season is less dependent on size and more dependent on the amount of energy stored in the liver and available to be allocated to gonad and gamete development.
Relatively low levels of skipped spawning were observed in 3L between 1980 and 1992. In contrast, high levels of skipped spawning were noted in inshore portions of 3L between 1999 and 2004 (Rideout et al., 2000; Rideout and Rose, in press). It is uncertain if these differences reflect temporal changes in environmental conditions or spatial differences between inshore and offshore areas. It is of note that Rideout and Rose (in press) reported the greatest proportion of non-reproductive fish in the smallest size class of potential spawners (40–49 cm), whereas here we observed most non-reproductive fish in the 60–79 cm size range. Data reported here are from 1978 to 2004, but come mainly from the period before 1992, whereas the findings of Rideout and Rose (in press) are based only on data from 1999 to 2004. There have been large decreases in size at maturity of cod over recent decades (Olsen et al., 2005). The large number of skipped spawners found here at 60–79 cm would encompass the size range where fish were maturing for the first time. In other species, such as Solea solea (Ramsay and Witthames, 1996) and Reinhardtius hippoglossoides (Walsh and Bowering, 1981), interruptions in gamete development are more common in smaller, potentially first-time spawners. Engelhard and Heino (2005), on the other hand, suggested that skipped spawning in Atlantic herring (Clupea harengus) was most common among potential second-time spawners.
In this study, we utilize a long-term cod data set that includes macroscopically determined maturity data, which admittedly could produce less accurate results than analyses based on histology (Tomkiewicz et al., 2003; Vitale et al., 2006). While this could reduce the accuracy of our findings, we believe that the impact is relatively small, because previous histological work confirmed the existence of a large proportion of skipped spawners in the area (Walsh et al., 1986; Rideout et al., 2000). In addition, because the data set encompasses a 27-year period and was compiled by numerous individuals, there is the potential for temporal variability as well as variability between observers in the accuracy of assigning maturity stages macroscopically. The use of macroscopically determined maturity stages is therefore considered a limitation of this study, and we encourage the use of histologically determined maturity for such work whenever possible.
Data presented here clearly suggest that skipped spawning in Newfoundland and Labrador cod is more common and widespread than perhaps previously believed. Although liver condition appears to influence the probability of spawning, there are spatial differences among areas with respect to the effects of liver condition. These results indicate that a global model to predict the probability of spawning by cod is likely not appropriate, and that there is a need to examine potential spatial differences in the bioenergetics of this species.
|
Acknowledgements |
|---|
We thank the numerous technical staff and ships' crew involved in the collection of the data. Fran Saborido Rey, Pierre Pepin, Atef Mansour, and an anonymous reviewer provided helpful comments on an earlier version of the manuscript. Funding was provided by Fishery Products International Ltd, The Canadian Centre for Fisheries Innovation, and Fisheries and Oceans Canada.
|
References |
|---|
|
TopIntroductionMethodsResultsDiscussionReferences |
|---|
-
Albikovskaya L.K. and Gerasimova O.V. (1993) Food and feeding patterns of cod (Gadus morhua L.) and beaked redfish (Sebastes mentella Travin) on Flemish Cap. NAFO Scientific Council Studies 19:31–39.
Beacham T. D., Brattey J., Miller K. M., Le K. D., Schulze A. D., Withler R. E. (2000) Population structure of Atlantic cod (Gadus morhua) in the Newfoundland and Labrador area determined from genetic variation. Canadian Stock Assessment Secretariat Research Document, 2000/099. 27 pp.
Bell J.D., Lyle J.M., Bulman C.M., Graham K.J., Newton G.M., Smith D.C. (1992) Spatial variation in reproduction, and occurrence of non-reproductive adults, in orange roughy, Hoplostethus atlanticus Collett (Trachichthyidae), from south-eastern Australia. Journal of Fish Biology 40:107–122.[CrossRef][Web of Science]
Bromley P.J., Ravier C., 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.[CrossRef][Web of Science]
Burton M.P. and Idler D.R. (1984) The reproductive cycle in winter flounder, Pseudopleuronectes americanus (Walbaum). Canadian Journal of Zoology 62:2563–2567.
Burton M.P. and Idler D.R. (1987) An experimental investigation of the non-reproductive, post-mature state in winter flounder. Journal of Fish Biology 30:643–650.[CrossRef][Web of Science]
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 (London) 233:405–415.
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.
Carscadden J.E. and Nakashima B.S. (1997) Abundance changes in distribution, biology, and behaviour of capelin in response to cooler waters of the 1990s. Forage Fishes in Marine Ecosystems. Proceedings of the International Symposium on the Role of Forage Fishes in Marine Ecosystems, pp. 457–468. Alaska Sea Grant College Program Report, 97-01(University of Alaska, Fairbanks) pp. 457–468.
Casas J.M. and Paz J. (1996) Recent changes in the feeding of cod (Gadus morhua) off the Flemish Cap, Newfoundland 1989–1993. ICES Journal of Marine Science 53:750–756.
Dutil J.D. (1986) Energetic constraints and spawning interval in the anadromous Arctic charr (Salvelinus alpinus). Copeia 1986:945–955.[CrossRef]
Engelhard G.H. and Heino M. (2005) Scale analysis suggests frequent skipping of the second reproductive season in Atlantic herring. Biology Letters 1:172–175.[CrossRef][Web of Science][Medline]
Goddard S.V. and Fletcher G.L. (1994) Antifreeze proteins: their role in cod survival and distribution from egg to adult. ICES Marine Science Symposia 198:676–683.
Hislop J.R.G., Robb A.P., Gauld J.A. (1978) Observations on effects of feeding level on growth and reproduction in haddock, Melanogrammus aeglefinus (L.) in captivity. Journal of Fish Biology 13:85–98.[Medline]
Jørgensen C., Ernande B., Fiksen Ø., Dieckmann U. (2006) The logic of skipped spawning in fish. Canadian Journal of Fisheries and Aquatic Sciences 63:200–211.
Kennedy W.A. (1953) Growth, maturity, fecundity and mortality in the relatively unexploited whitefish, Coregonus clupeaformis, of Great Slave Lake. Journal of the Fisheries Research Board of Canada 10:413–441.
Kjesbu O.S., Witthames P.R., Solemdal P., Greer Walker M. (1998) Temporal variations in the fecundity of Arcto-Norwegian cod (Gadus morhua) in response to natural changes in food and temperature. Journal of Sea Research 40:303–321.[CrossRef]
Korsbrekke K. (1999) Variations in maturity of haddock in the Barents Sea in relation to year-class strength, age, size, sex and area. Journal of Northwest Atlantic Fishery Science 25:37–45.
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 Sciences 57:815–825.
Lilly G. R. (1985) Cod (Gadus morhua) on the Flemish Cap fed primarily on redfish (Sebastes sp.) in winter 1984. NAFO Scientific Council Report Document, 85/72. 7 pp.
Lilly G.R. (1994) Predation by Atlantic cod on capelin on the southern Labrador and Northeast Newfoundland shelves during a period of changing spatial distribution. ICES Marine Science Symposia 198:600–611.
Mace P.M. and Sissenwine M.P. (1993) How much spawning per recruit is enough? Risk Evaluation and Biological Reference Points for Fisheries Management. In Smith S.J., Hunt J.J., Rivard D. (Eds.). Canadian Special Publication of Fisheries and Aquatic Sciences 120: pp. 101–118.
Maddock D.M. and Burton M.P.M. (1994) Some effects of starvation on the lipid and skeletal muscle layers of the winter flounder, Pleuronectes americanus. Canadian Journal of Zoology 72:1672–1679.
Marshall C.T., Kjesbu O.S., Yaragina N.A., Solemdal P., Ulltang Ø. (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.
Marteinsdottir G. and Begg G.A. (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.[Web of Science]
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.[CrossRef][Web of Science]
Morgan M.J. and Colbourne E.B. (1999) Variation in maturity-at-age and size in three populations of American plaice. ICES Journal of Marine Science 56:673–688.
Morgan M. J. and Lilly G. R. The impact of condition on reproduction in Flemish Cap cod. Journal of Northwest Atlantic Fishery Science (in press).
Oganesyan S. A. (1993) Periodicity of the Barents Sea cod reproduction. ICES Committee Meeting Papers 1993/G: 64. 11 pp.
Olsen E.M., Lilly G.R., Heino M., Morgan M.J., Brattey J., Dieckmann U. (2005) Assessing changes in age and size at maturation in collapsing populations of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 62:811–823.
Pitt T.K. (1966) Sexual maturity and spawning of the American plaice, Hippoglossoides platessoides (Fabricius), from Newfoundland and Grand Bank areas. Journal of the Fisheries Research Board of Canada 23:651–672.[Web of Science]
Popova O.A. (1962) Some data on the feeding of cod in the Newfoundland area of the Northwest Atlantic. Soviet Fisheries Investigations in the Northwest Atlantic(VNIRO–PINRO, Moscow) (Translated for the US Department of the Interior and the National Science Foundation, Washington, D.C., by Israel Program for Scientific Translation, 1963, pp. 228–248).
Ramsay K. and Witthames P. (1996) Using oocyte size to assess seasonal ovarian development in Solea solea (L.). Journal of Sea Research 36:275–283.[CrossRef]
Rideout R.M., Burton M.P.M., Rose G.A. (2000) Observations on mass atresia and skipped spawning in northern Atlantic cod, from Smith Sound, Newfoundland. Journal of Fish Biology 57:1429–1440.[CrossRef][Web of Science]
Rideout R. M. and Rose G. A. Suppression of reproduction in Atlantic cod (Gadus morhua L.). Marine Ecology Progress Series (in press).
Rideout R.M., Rose G.A., Burton M.P.M. (2005) Skipped spawning in female iteroparous fishes. Fish and Fisheries 6:50–72.[CrossRef][Web of Science]
Rijnsdorp A.D. (1990) The mechanism of energy allocation over reproduction and somatic growth in female North Sea plaice, Pleuronectes platessa L. Netherlands Journal of Sea Research 25:279–290.
Rijnsdorp A.D. (1993) Fisheries as a large-scale experiment on life-history evolution: disentangling phenotypic and genetic effects in changes in maturation and reproduction of North Sea plaice, Pleuronectes platessa L. Oecologia 96:391–401.[CrossRef][Web of Science]
Rose G.A. (2003) Monitoring coastal northern cod: towards an optimal survey of Smith Sound, Newfoundland. ICES Journal of Marine Science 60:453–462.
Rose G.A. and O'Driscoll R.L. (2002) Capelin are good for cod: can the northern stock rebuild without them? ICES Journal of Marine Science 59:1018–1026.
Sandstrom O., Neuman E., Thoresson G. (1995) Effects of temperature on life history variables in perch. Journal of Fish Biology 47:652–670.[CrossRef][Web of Science]
Schwalme K. and Chouinard G.A. (1999) Seasonal dynamics in feeding, organ weights, and reproductive maturation of Atlantic cod (Gadus morhua) in the southern Gulf of St Lawrence. ICES Journal of Marine Science 56:303–319.
Shelton P. A. and Rivard D. (2003) Developing a precautionary approach to fisheries management in Canada – the decade following the cod collapses. NAFO Scientific Council Research Document, 03/1. 16 pp.
Shirokova M.Y. (1969) The sexual maturation rate of the generations of Baltic cod taken from 1961–63. Atlanticeskii Nauchno-Issledovatel'skii Institut Rybnogo Khoziaistva i Okeanografii Trudy Kaliningrad 21:37–44.
Swartzman G., Huang C., Kaluzny S. (1992) Spatial analysis of Bering Sea groundfish survey data using generalized additive models. Canadian Journal of Fisheries and Aquatic Sciences 49:1366–1378.
Templeman W., Hodder V.M., Wells R. (1978) Sexual maturity and spawning in haddock, Melanogrammus aeglefinus, of the southern Grand Bank. ICNAF Research Bulletin 13:53–65.
Tomkiewicz J., Tybjerg L., Jespersen Å. (2003) Micro- and macroscopic characteristics to stage gonadal maturation of female Baltic cod. Journal of Fish Biology 62:253–275.[CrossRef][Web of Science]
Vitale F., Svedäng H., 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.[CrossRef][Web of Science]
Walsh S.J. and Bowering W.R. (1981) Histological and visual observations on oogenesis and sexual maturity in Greenland halibut off northern Labrador. NAFO Scientific Council Studies 1:71–75.
Walsh S. J., Wells R., Brennan S. (1986) Histological and visual observations on oogenesis and sexual maturity of Flemish Cap female cod. NAFO Scientific Council Research Document, 86/111. 11 pp.
Woodhead A.D. and Woodhead P.M.J. (1965) Seasonal changes in the physiology of Barents Sea cod, Gadus morhua L, in relation to its environment. 1. Endocrine changes particularly affecting migration and maturation. ICNAF Special Publication 6:691–715.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||