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Spatial variation in fecundity of Norwegian coastal cod, Gadus morhua (Linnaeus), along the coast of Norway
Fisheries Research 183 (2016) 401–403
Contents lists available at ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Technical note
Spatial variation in fecundity of Norwegian coastal cod, Gadus morhua (Linnaeus), along the coast of Norway M. Blom a,∗ , J. Kennedy b,c a b c
Institute of Life Sciences, Høgskolen i Ålesund, Fogdegården, 6025 Ålesund, Norway Marine Research Institute, Skúlagata 4, P.O. Box 1390, Reykjavík 121, Iceland Biopol, Einbúastíg 2, Skagaströnd, Iceland
a r t i c l e
i n f o
Article history: Received 19 June 2015 Received in revised form 23 May 2016 Accepted 25 May 2016 Handled by George A. Rose Available online 18 July 2016
a b s t r a c t Fecundity of Norwegian coastal cod (NCC) was estimated at several locations along the coast of Norway. There was no significant difference in carcass weight, liver weight or potential fecundity (Fp ) between Lofoten and Verrabotn (Northern region) or between Bømlo and Langesund (Southern region). Fish caught in the Northern region had a higher liver weight and potential fecundity than fish caught in the Southern region. © 2016 Published by Elsevier B.V.
Keywords: Norwegian coastal cod Potential fecundity Liver weight Carcass weight
1. Introduction Variations in reproductive parameters can impact the reproductive potential of fish populations and affect their resilience to a given level of fishing pressure. Coastal cod (Gadus morhua) in Norway are known to consist of genetically distinguishable populations where reproductive parameters (growth and age at maturity) vary between these different populations (Berg and Albert, 2003; Salvanes et al., 2004; Jorde et al., 2007). To investigate the possibility of whether potential fecundity also varies between coastal cod populations, fecundity was estimated from fish caught in four areas over two years. 2. Methods Cod were sampled from four locations along the Norwegian coast; Lofoten, Verrabotn, Bømlo and Langesund during 2003 and 2004 (Fig. 1; Table 1). Fish were caught by local fishermen using Danish seine (Lofoten) and gillnets (all other areas). Sampling was timed to be as close to the beginning of spawning as possible; knowledge on approximate spawning time was based upon advice from local fishermen. In both Lofoten and Verrabotn there is an
∗ Corresponding author. E-mail addresses: [email protected], [email protected] (M. Blom). http://dx.doi.org/10.1016/j.fishres.2016.05.023 0165-7836/© 2016 Published by Elsevier B.V.
overlap in the distribution of costal cod and North-East Arctic cod during the spawning season. Otoliths were used to distinguish between these two types (Rollefsen, 1933; Stransky et al., 2008) by otolith experts at the Institute of Marine Research (Norway) and only fish confirmed as coastal cod were included in this study. Fish with hydrated eggs in their ovary were also excluded from the study as these fish have begun spawning. For each fish, total length (L) (±1 cm) and ungutted weight (W) (±10 g), gonad weight (WG) ) (±1 g), liver weight WL (±1 g) and intestine weight were measured. The otoliths were removed for aging and type classification, and ovary samples were taken and stored in 10% buffered formalin. Carcass weight (Wc ) was calculated by subtracting the weight of the gonad, liver and intestines from the total weight. Potential fecundity was estimated using the Auto-diametric method (Thorsen and Kjesbu, 2001), which works on the principle that oocytes per gram of an ovary is inversely proportional to the average size of the oocytes. The diameter of 200 vitellogenic follicles were measured using a binocular microscope (Olympus SZX12 with a SZX-ILLB200 light foot) at 7× magnification, a camera displaying a live image and computer-aided automatic particle analysis. Potential fecundity was then estimated using the following equation:
Fp = 2.14 × 1011 × D−2.700 × WG O
402
M. Blom, J. Kennedy / Fisheries Research 183 (2016) 401–403
Table 1 The number of fish sampled (n) in each location and year together with details on the latitude of the location, sampling period and the length range of the fish in each sample. Location
Latitude
Year
Dates
n
Length range (cm)
Age range
Lofoten
68–69◦ N
2003 2004
3 Mar–6 Mar 16 Feb–20 Feb
20 27
56–115 56–112
5–9 5–8
Verrabotn
63–64◦ N
2003 2004
31 Mar–3 Apr 8 Mar–12 Mar
11 14
61–79 62–92
5–7 5–11
Bømlo
59–60◦ N
2003 2004
12 Feb–14 Feb 2 Feb–3 Feb
16 7
54–95 63–91
4–7 3–6
Langesund
59−59◦ N
2003 2004
17 Feb–19 Feb 27 Jan–30 Jan
7 23
54– 83 51–80
3–7 3–6
Table 2 The amount of variance explained and p-value (in brackets) in the linear model of fecundity by the different explanatory variables for the Northern and Southern region. Region
Northern
Variable loge Carcass weight (g) loge Liver weight (g) LC (m)
0.79 0.03 0.02
Total
0.84
Southern (<0.0001) (<0.0001) (<0.001)
0.63 0.05
(<0.0001) (<0.001)
0.68
Fig. 1. Location of the four sampling areas along the Norwegian coast.
where DO = average oocyte diameter (m). Leading cohort oocyte diameter (LC) was defined as mean of the largest 10% of vitellogenic oocytes and was used as an indicator of the stage of ovary development. Length, weight, fecundity and liver weight were loge transformed to meet with normal distribution requirements. There were no significant differences in potential fecundity at weight or length between years in any area (ANCOVA, loge Fp = loge W + year, loge Fp = loge L + year, P > 0.05) so fish from same area but different years were combined. The fish from the four areas were combined into two regions, termed Northern (Lofoten and Verrabotn) and Southern region (Bømlo and Langesund) as there were no difference in weight at length (ANCOVA, loge W = loge L + area, P > 0.05) or fecundity at weight (ANCOVA, loge Fp = loge W + area, P > 0.05) between the areas within these regions. Differences in weight at length and fecundity between years, areas and regions were tested using ANCOVA. Multiple linear regression was used to establish the model which best explained the variation in fecundity within a region. The starting model was
Fig. 2. Fecundity versus carcass weight for fish caught in the Northern (♦) and Southern () region. Non-linear regression lines are shown for Northern (solid) and Southern (dashed) region.
opposed to hepatosomatic index as it would give a better reflection of energy reserves within the statistical tests. Hepatosomatic index is a ratio between carcass weight and liver weight and so will vary, in addition to liver weight, with the weight of the carcass and doubt has been placed over the reliability of such ratios (Packard and Boardman, 1999). 3. Results The regression model with the highest explanatory power for the Northern and Southern regions were
loge Fp = loge W + loge L + loge WL + WC + LC
loge Fp = 0.82 (loge WC ) + −0.00083 LC + 0.21 (loge WL ) + 7.77 and loge Fp = 0.67 (loge WC ) + 0.27 (loge WL ) + 7.84
Insignificant terms were then sequentially removed. Explanatory variables in the final model were tested for collinearity using variance inflation factors (VIFs) (Zuur et al., 2009) in the car package for R (Fox and Weisberg, 2009). Liver weight was included as a continuous variable within regression models and ANCOVA as
respectively (Table 2). The VIFs for all variables were <3 indicating that the collinearity among variables were within reasonable limits. Fish from the Northern region had a significantly higher fecundity (Fig. 2) (ANCOVA, loge Fp = loge Wc + region, p < 0.001) and liver weight (Fig. 3) (ANCOVA, loge Fp = loge WL = logWc + region,
M. Blom, J. Kennedy / Fisheries Research 183 (2016) 401–403
Fig. 3. Liver weight versus carcass weight for cod caught in the Northern (♦) and Southern () region. Non-linear regression lines are shown for Northern (solid) and Southern (dashed) region.
p < 0.001) at a given carcass weight than fish from the Southern region (ANCOVA, p < 0.001). Carcass weight at length did not differ significantly between regions (ANCOVA, loge Wc = loge L + region, p > 0.05). The lack of an effect of LC on fecundity in the Southern region (it was a significant factor for fish in the northern region) is likely due to a greater range in LC values in the Northern region (95% percentile; 440–832 m) in comparison with the Southern region (95% percentiles; 525–839 m). The regional difference in liver weight did not fully explain the difference in fecundity between regions (ANCOVA, p < 0.001). A theoretical cod with a carcass weight of 4000 g, an LC of 800 m and a liver weight of 350 g from the Northern and Southern would have a Fp of 3.75 and 3.20 million eggs respectively, i.e. the fecundity of a cod from the Southern region would have a Fp of about 85% of that of a similar sized fish, with a similar liver and carcass weight, from the Northern region when close to spawning. This difference increased with increasing fish size. 4. Discussion Many of the populations of coastal cod along the Norwegian coast are reproductively isolated from each other and there is distinct genetic variation (Jorde et al., 2007; Knutsen et al., 2007). This leads to the possibility that the division of energy between growth and reproduction will differ between areas representing adaptations to the local environment. However, due to the low number of age classes represented in the samples and also a difference between the distributions of age classes between regions made it difficult to establish growth curves or establish if there was a difference in length at age between areas. Thus it was not possible to establish if there was a difference in the division of energy between growth and reproduction between the regions studied. Therefore, whether genetic variations are a source of differences in fecundity between regions remains an open question. Differences in abiotic factors such as temperature may also play a significant role in the differences in fecundity between the two regions. Temperature is known to have an effect on fecundity in cod with fecundity being positively correlated with temperature (Kjesbu et al., 1998; Kraus et al., 2000). Different day lengths
403
between north and south may also have an effect as day length can affect both forage patterns and spawning time (Gjøsaeter and Danielssen, 2011). Energy reserves influence Fp in many species with a positive relationship between the two (Kennedy et al., 2007; Skjæraasen et al., 2010). However, above a specific threshold of energy, while potential fecundity increases with increasing energy reserves, relative fecundity is not affected and remains constant. Below this specific threshold, there is a positive correlation between energy reserves and relative fecundity (Kjesbu, 2009). Such an effect has the potential to explain the difference in fecundity between the two regions as fish from the Southern region had smaller livers. There was, however, no significant correlation between relative fecundity and liver weight or hepatosomatic index in either region. A potential correlation could be confounded by the effect of maturation stage on liver size. As ovary development proceeds, lipids are mobilised from the liver to the gonad, thus liver size decreases towards spawning as seen for NEA cod (Skjæraasen et al., 2010) which can affect the statistical relationship between liver energy and potential fecundity. To get a clearer picture, of whether this is the reason for the effect, samples with a lower variation in maturation stages are needed. References Berg, E., Albert, O.T., 2003. Cod in fjords and coastal waters of North Norway: distribution and variation in length and maturity at age. ICES J. Mar. Sci. 60, 787–797. Fox, J., Weisberg, S., 2009. Car: Companion to Applied Regression R Package Version 02-14, Available at http://cran.r-project.org/web/packages/car. (accessed 6.01.16). Gjøsæter, J., Danielssen, D.S., 2011. Age, growth and otholith annulus formation of cod (Gadus morhua) in the Risør area on the Norwegian Skagerrak coast during 1986–1996. Mar. Biol. Res. 7 (3), 281–288. Jorde, P.E., Knutsen, H., Espeland, S.H., Stenseth, N.C., 2007. Spatial scale of genetic structuring in coastal cod Gadus morhua and geographic extent of local populations. Mar. Ecol. Prog. Ser. 343, 229–237. Kennedy, J., Witthames, P.R., Nash, R.D.M., 2007. The concept of fecundity regulation in plaice (Pleuronectes platessa) tested on three Irish Sea spawning populations. Can. J. Fish. Aquat.Sci. 64, 587–601. 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. J. Sea Res. 40, 303–321. Kjesbu, O.S., 2009. Applied fish reproductive biology: contribution of individual reproductive potential to recruitment and fisheries management. In: Jakobsen, T., Fogarty, M.J., Megrey, B.A., Moksness, E. (Eds.), In Fish Reproductive Biology and Its Implications for Assessment and Management. Wiley-Blackwell, Oxford, UK, pp. 293–332. Knutsen, H., Olsen, E.M., Ciannelli, L., Espeland, S.H., Knutsen, J.A., Simonsen, J.H., Skreslet, S., Stenseth, N.C., 2007. Egg distribution, bottom topography and small-scale cod population structure in a coastal marine system. Mar. Ecol. Prog. Ser. 333, 249–255. Kraus, G., Muller, A., Trella, K., Koster, F.W., 2000. Fecundity of Baltic cod: temporal and spatial variation. J. Fish Biol. 56, 1327–1341. Packard, G.C., Boardman, T.J., 1999. The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comp. Biochem. Physiol. Part A 122, 37–44. Rollefsen, G., 1933. The otoliths of the cod. Rep. Norw. Fish. Mar. Invest. 4, 4–18. Salvanes, A.G.V., Skjæraasen, J.E., Nilsen, T., 2004. Sub-populations of coastal cod with different behaviour and life-history strategies. Mar. Ecol. Prog. Ser. 267, 241–251. Skjæraasen, J.E., Nash, R.D.M., Kennedy, J., Thorsen, A., Nilsen, T., Kjesbu, O.S., 2010. Liver energy, atresia and oocyte stage influence fecundity regulation in Northeast Arctic cod. Mar. Ecol. Prog. Ser. 404, 173–183. Stransky, C., Baumann, H., Fevolden, S.E., Harbitz, A., Høie, H., Nedreaas, K.H., Salberg, A.B., Skarstein, T.H., 2008. Separation of Norwegian coastal cod and Northeast Arctic cod by outer otolith shape analysis. Fish. Res. 90, 26–35. Thorsen, A., 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. J. Sea Res. 46, 295–308. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., Smith, G.M., 2009. Mixed Effects Models and Extensions in Ecology with R. Springer, New York, NY.
Contents lists available at ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Technical note
Spatial variation in fecundity of Norwegian coastal cod, Gadus morhua (Linnaeus), along the coast of Norway M. Blom a,∗ , J. Kennedy b,c a b c
Institute of Life Sciences, Høgskolen i Ålesund, Fogdegården, 6025 Ålesund, Norway Marine Research Institute, Skúlagata 4, P.O. Box 1390, Reykjavík 121, Iceland Biopol, Einbúastíg 2, Skagaströnd, Iceland
a r t i c l e
i n f o
Article history: Received 19 June 2015 Received in revised form 23 May 2016 Accepted 25 May 2016 Handled by George A. Rose Available online 18 July 2016
a b s t r a c t Fecundity of Norwegian coastal cod (NCC) was estimated at several locations along the coast of Norway. There was no significant difference in carcass weight, liver weight or potential fecundity (Fp ) between Lofoten and Verrabotn (Northern region) or between Bømlo and Langesund (Southern region). Fish caught in the Northern region had a higher liver weight and potential fecundity than fish caught in the Southern region. © 2016 Published by Elsevier B.V.
Keywords: Norwegian coastal cod Potential fecundity Liver weight Carcass weight
1. Introduction Variations in reproductive parameters can impact the reproductive potential of fish populations and affect their resilience to a given level of fishing pressure. Coastal cod (Gadus morhua) in Norway are known to consist of genetically distinguishable populations where reproductive parameters (growth and age at maturity) vary between these different populations (Berg and Albert, 2003; Salvanes et al., 2004; Jorde et al., 2007). To investigate the possibility of whether potential fecundity also varies between coastal cod populations, fecundity was estimated from fish caught in four areas over two years. 2. Methods Cod were sampled from four locations along the Norwegian coast; Lofoten, Verrabotn, Bømlo and Langesund during 2003 and 2004 (Fig. 1; Table 1). Fish were caught by local fishermen using Danish seine (Lofoten) and gillnets (all other areas). Sampling was timed to be as close to the beginning of spawning as possible; knowledge on approximate spawning time was based upon advice from local fishermen. In both Lofoten and Verrabotn there is an
∗ Corresponding author. E-mail addresses: [email protected], [email protected] (M. Blom). http://dx.doi.org/10.1016/j.fishres.2016.05.023 0165-7836/© 2016 Published by Elsevier B.V.
overlap in the distribution of costal cod and North-East Arctic cod during the spawning season. Otoliths were used to distinguish between these two types (Rollefsen, 1933; Stransky et al., 2008) by otolith experts at the Institute of Marine Research (Norway) and only fish confirmed as coastal cod were included in this study. Fish with hydrated eggs in their ovary were also excluded from the study as these fish have begun spawning. For each fish, total length (L) (±1 cm) and ungutted weight (W) (±10 g), gonad weight (WG) ) (±1 g), liver weight WL (±1 g) and intestine weight were measured. The otoliths were removed for aging and type classification, and ovary samples were taken and stored in 10% buffered formalin. Carcass weight (Wc ) was calculated by subtracting the weight of the gonad, liver and intestines from the total weight. Potential fecundity was estimated using the Auto-diametric method (Thorsen and Kjesbu, 2001), which works on the principle that oocytes per gram of an ovary is inversely proportional to the average size of the oocytes. The diameter of 200 vitellogenic follicles were measured using a binocular microscope (Olympus SZX12 with a SZX-ILLB200 light foot) at 7× magnification, a camera displaying a live image and computer-aided automatic particle analysis. Potential fecundity was then estimated using the following equation:
Fp = 2.14 × 1011 × D−2.700 × WG O
402
M. Blom, J. Kennedy / Fisheries Research 183 (2016) 401–403
Table 1 The number of fish sampled (n) in each location and year together with details on the latitude of the location, sampling period and the length range of the fish in each sample. Location
Latitude
Year
Dates
n
Length range (cm)
Age range
Lofoten
68–69◦ N
2003 2004
3 Mar–6 Mar 16 Feb–20 Feb
20 27
56–115 56–112
5–9 5–8
Verrabotn
63–64◦ N
2003 2004
31 Mar–3 Apr 8 Mar–12 Mar
11 14
61–79 62–92
5–7 5–11
Bømlo
59–60◦ N
2003 2004
12 Feb–14 Feb 2 Feb–3 Feb
16 7
54–95 63–91
4–7 3–6
Langesund
59−59◦ N
2003 2004
17 Feb–19 Feb 27 Jan–30 Jan
7 23
54– 83 51–80
3–7 3–6
Table 2 The amount of variance explained and p-value (in brackets) in the linear model of fecundity by the different explanatory variables for the Northern and Southern region. Region
Northern
Variable loge Carcass weight (g) loge Liver weight (g) LC (m)
0.79 0.03 0.02
Total
0.84
Southern (<0.0001) (<0.0001) (<0.001)
0.63 0.05
(<0.0001) (<0.001)
0.68
Fig. 1. Location of the four sampling areas along the Norwegian coast.
where DO = average oocyte diameter (m). Leading cohort oocyte diameter (LC) was defined as mean of the largest 10% of vitellogenic oocytes and was used as an indicator of the stage of ovary development. Length, weight, fecundity and liver weight were loge transformed to meet with normal distribution requirements. There were no significant differences in potential fecundity at weight or length between years in any area (ANCOVA, loge Fp = loge W + year, loge Fp = loge L + year, P > 0.05) so fish from same area but different years were combined. The fish from the four areas were combined into two regions, termed Northern (Lofoten and Verrabotn) and Southern region (Bømlo and Langesund) as there were no difference in weight at length (ANCOVA, loge W = loge L + area, P > 0.05) or fecundity at weight (ANCOVA, loge Fp = loge W + area, P > 0.05) between the areas within these regions. Differences in weight at length and fecundity between years, areas and regions were tested using ANCOVA. Multiple linear regression was used to establish the model which best explained the variation in fecundity within a region. The starting model was
Fig. 2. Fecundity versus carcass weight for fish caught in the Northern (♦) and Southern () region. Non-linear regression lines are shown for Northern (solid) and Southern (dashed) region.
opposed to hepatosomatic index as it would give a better reflection of energy reserves within the statistical tests. Hepatosomatic index is a ratio between carcass weight and liver weight and so will vary, in addition to liver weight, with the weight of the carcass and doubt has been placed over the reliability of such ratios (Packard and Boardman, 1999). 3. Results The regression model with the highest explanatory power for the Northern and Southern regions were
loge Fp = loge W + loge L + loge WL + WC + LC
loge Fp = 0.82 (loge WC ) + −0.00083 LC + 0.21 (loge WL ) + 7.77 and loge Fp = 0.67 (loge WC ) + 0.27 (loge WL ) + 7.84
Insignificant terms were then sequentially removed. Explanatory variables in the final model were tested for collinearity using variance inflation factors (VIFs) (Zuur et al., 2009) in the car package for R (Fox and Weisberg, 2009). Liver weight was included as a continuous variable within regression models and ANCOVA as
respectively (Table 2). The VIFs for all variables were <3 indicating that the collinearity among variables were within reasonable limits. Fish from the Northern region had a significantly higher fecundity (Fig. 2) (ANCOVA, loge Fp = loge Wc + region, p < 0.001) and liver weight (Fig. 3) (ANCOVA, loge Fp = loge WL = logWc + region,
M. Blom, J. Kennedy / Fisheries Research 183 (2016) 401–403
Fig. 3. Liver weight versus carcass weight for cod caught in the Northern (♦) and Southern () region. Non-linear regression lines are shown for Northern (solid) and Southern (dashed) region.
p < 0.001) at a given carcass weight than fish from the Southern region (ANCOVA, p < 0.001). Carcass weight at length did not differ significantly between regions (ANCOVA, loge Wc = loge L + region, p > 0.05). The lack of an effect of LC on fecundity in the Southern region (it was a significant factor for fish in the northern region) is likely due to a greater range in LC values in the Northern region (95% percentile; 440–832 m) in comparison with the Southern region (95% percentiles; 525–839 m). The regional difference in liver weight did not fully explain the difference in fecundity between regions (ANCOVA, p < 0.001). A theoretical cod with a carcass weight of 4000 g, an LC of 800 m and a liver weight of 350 g from the Northern and Southern would have a Fp of 3.75 and 3.20 million eggs respectively, i.e. the fecundity of a cod from the Southern region would have a Fp of about 85% of that of a similar sized fish, with a similar liver and carcass weight, from the Northern region when close to spawning. This difference increased with increasing fish size. 4. Discussion Many of the populations of coastal cod along the Norwegian coast are reproductively isolated from each other and there is distinct genetic variation (Jorde et al., 2007; Knutsen et al., 2007). This leads to the possibility that the division of energy between growth and reproduction will differ between areas representing adaptations to the local environment. However, due to the low number of age classes represented in the samples and also a difference between the distributions of age classes between regions made it difficult to establish growth curves or establish if there was a difference in length at age between areas. Thus it was not possible to establish if there was a difference in the division of energy between growth and reproduction between the regions studied. Therefore, whether genetic variations are a source of differences in fecundity between regions remains an open question. Differences in abiotic factors such as temperature may also play a significant role in the differences in fecundity between the two regions. Temperature is known to have an effect on fecundity in cod with fecundity being positively correlated with temperature (Kjesbu et al., 1998; Kraus et al., 2000). Different day lengths
403
between north and south may also have an effect as day length can affect both forage patterns and spawning time (Gjøsaeter and Danielssen, 2011). Energy reserves influence Fp in many species with a positive relationship between the two (Kennedy et al., 2007; Skjæraasen et al., 2010). However, above a specific threshold of energy, while potential fecundity increases with increasing energy reserves, relative fecundity is not affected and remains constant. Below this specific threshold, there is a positive correlation between energy reserves and relative fecundity (Kjesbu, 2009). Such an effect has the potential to explain the difference in fecundity between the two regions as fish from the Southern region had smaller livers. There was, however, no significant correlation between relative fecundity and liver weight or hepatosomatic index in either region. A potential correlation could be confounded by the effect of maturation stage on liver size. As ovary development proceeds, lipids are mobilised from the liver to the gonad, thus liver size decreases towards spawning as seen for NEA cod (Skjæraasen et al., 2010) which can affect the statistical relationship between liver energy and potential fecundity. To get a clearer picture, of whether this is the reason for the effect, samples with a lower variation in maturation stages are needed. References Berg, E., Albert, O.T., 2003. Cod in fjords and coastal waters of North Norway: distribution and variation in length and maturity at age. ICES J. Mar. Sci. 60, 787–797. Fox, J., Weisberg, S., 2009. Car: Companion to Applied Regression R Package Version 02-14, Available at http://cran.r-project.org/web/packages/car. (accessed 6.01.16). Gjøsæter, J., Danielssen, D.S., 2011. Age, growth and otholith annulus formation of cod (Gadus morhua) in the Risør area on the Norwegian Skagerrak coast during 1986–1996. Mar. Biol. Res. 7 (3), 281–288. Jorde, P.E., Knutsen, H., Espeland, S.H., Stenseth, N.C., 2007. Spatial scale of genetic structuring in coastal cod Gadus morhua and geographic extent of local populations. Mar. Ecol. Prog. Ser. 343, 229–237. Kennedy, J., Witthames, P.R., Nash, R.D.M., 2007. The concept of fecundity regulation in plaice (Pleuronectes platessa) tested on three Irish Sea spawning populations. Can. J. Fish. Aquat.Sci. 64, 587–601. 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. J. Sea Res. 40, 303–321. Kjesbu, O.S., 2009. Applied fish reproductive biology: contribution of individual reproductive potential to recruitment and fisheries management. In: Jakobsen, T., Fogarty, M.J., Megrey, B.A., Moksness, E. (Eds.), In Fish Reproductive Biology and Its Implications for Assessment and Management. Wiley-Blackwell, Oxford, UK, pp. 293–332. Knutsen, H., Olsen, E.M., Ciannelli, L., Espeland, S.H., Knutsen, J.A., Simonsen, J.H., Skreslet, S., Stenseth, N.C., 2007. Egg distribution, bottom topography and small-scale cod population structure in a coastal marine system. Mar. Ecol. Prog. Ser. 333, 249–255. Kraus, G., Muller, A., Trella, K., Koster, F.W., 2000. Fecundity of Baltic cod: temporal and spatial variation. J. Fish Biol. 56, 1327–1341. Packard, G.C., Boardman, T.J., 1999. The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comp. Biochem. Physiol. Part A 122, 37–44. Rollefsen, G., 1933. The otoliths of the cod. Rep. Norw. Fish. Mar. Invest. 4, 4–18. Salvanes, A.G.V., Skjæraasen, J.E., Nilsen, T., 2004. Sub-populations of coastal cod with different behaviour and life-history strategies. Mar. Ecol. Prog. Ser. 267, 241–251. Skjæraasen, J.E., Nash, R.D.M., Kennedy, J., Thorsen, A., Nilsen, T., Kjesbu, O.S., 2010. Liver energy, atresia and oocyte stage influence fecundity regulation in Northeast Arctic cod. Mar. Ecol. Prog. Ser. 404, 173–183. Stransky, C., Baumann, H., Fevolden, S.E., Harbitz, A., Høie, H., Nedreaas, K.H., Salberg, A.B., Skarstein, T.H., 2008. Separation of Norwegian coastal cod and Northeast Arctic cod by outer otolith shape analysis. Fish. Res. 90, 26–35. Thorsen, A., 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. J. Sea Res. 46, 295–308. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., Smith, G.M., 2009. Mixed Effects Models and Extensions in Ecology with R. Springer, New York, NY.