Journal of Fish Biology (2004) 64, 1725–1730
doi:10.1111/j.1095-8649.2004.00402.x, available online at http://www.blackwell-synergy.com
BRIEF COMMUNICATIONS
Life-history variation among local populations of
Atlantic cod from the Norwegian Skagerrak coast
E. M. O L S E N *†‡, H. K N U T S E N *, J. G J Ø S Æ T E R *, P. E. J O R D E *§,
J. A. K N U T S E N * A N D N. C. S T E N S E T H *§
*Institute of Marine Research, Department of Coastal Zone, Flødevigen Marine
Research Station, N-4817 His, Norway, †Division of Marine Biology and Limnology,
Department of Biology, University of Oslo, P. O. Box 1064 Blindern, N-0316 Oslo,
Norway and §Centre for Ecological and Evolutionary Synthesis, Department of
Biology, University of Oslo, P. O. Box 1050, Blindern, N-0316 Oslo
(Received 9 April 2003, Accepted 22 February 2004)
Small-scale spatial variation in life history was found among genetically distinct local populations of Atlantic cod Gadus morhua from the Norwegian Skagerrak coast. Among populations,
age at 50% maturity varied from 26 to 38 years, total (LT) length at 50% maturity from 35 to
60 cm, annual survival from 33 to 64%, mean LT at age 4 years from 43 to 63 cm, and mean
# 2004 The Fisheries Society of the British Isles
backcalculated LT at age 1 year from 8 to 12 cm.
Key words: Gadus morhua; growth; life history; maturation; survival.
Recent population genetic studies have shown that coastal Atlantic cod Gadus
morhua L. may be structured into local populations on a scale that is considerably smaller than the dispersal ability of the species (Ruzzante et al., 2000;
Knutsen et al., 2003; Pogson & Fevolden, 2003). Along the Norwegian Skagerrak coast, there is evidence for local populations extending as little as 30 km
(Knutsen, 2003). This population structuring potentially allows for local differences in ecologically important traits, such as age- and size at maturation,
growth and survival. Atlantic cod from fjords and coastal waters of north
Norway show considerable local variation in total length (LT) and maturity at
age (Berg & Albert, 2003). In comparison, little is known about local variation
in life-history traits of Atlantic cod from the Norwegian Skagerrak coast.
Atlantic cod from this southern coastline are known to reach maturity at a
relatively early age and small size (beginning at age 2 years and c. 35 cm LT;
Gjøsæter et al., 1996), and there is some evidence for local variations in growth
rate (Dannevig, 1933). There is also evidence for spatial variation in the ecological dynamics of the Atlantic cod along the Norwegian Skagerrak coast
‡Author to whom correspondence should be addressed. Tel.: þ47 22 85 45 05; fax: þ47 22 85 44 38;
email: espeom@bio.uio.no
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2004 The Fisheries Society of the British Isles
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E. M. OLSEN ET AL.
(Fromentin et al., 1997; Chan et al., 2003). The present study reports on the
analyses of variation in survival, LT and maturity at age, and maturity at LT of
Atlantic cod from several localities along the Norwegian Skagerrak coast.
Atlantic cod were sampled from eight sites (Table I and Fig. 1), which have
also recently been used for population genetic studies (Knutsen, 2003; Knutsen
et al., 2003). The fish were aged from otoliths (sagittae) by a highly experienced
technician at the Flødevigen Marine Research Station, sexed, weighed, measured (LT), and assigned to a maturity status. Growth trajectories could not be
well described with linear regressions or a non-linear model based on the von
Bertalanffy function, but body length of 4 year old Atlantic cod differed
significantly among localities (F7,260, Plocality < 00001; Table I). Otoliths from
a random sub-set of c. 50% of the individuals from each locality (n ¼ 400) were
used for backcalculating LT at age 1 year (LT1). The diameter of the otoliths
was measured at the outer edge of the first hyaline zone. This edge was assumed
to correspond to the end of the first winter period of slow growth and was
thus defined as the diameter at age 1 year. Also, the total diameter of the
otoliths was measured. Otolith diameter at age 1 year differed significantly
among localities and age-groups (analysis of covariance model, ANCOVA,
ln-transformed response variable, F8,268, Ptotal model < 00001, Plocality < 00001,
Page ¼ 0045; Table I). The interaction effect between locality and age was not
significant (P ¼ 012). The age effect was negative (0042). This analysis was
made on a sub-set of the data containing only fish at age 3 or 4 years. Younger
and older age groups were excluded due to the occurrence of small sample sizes
(n < 5). Backcalculated LT1 (Table I) was estimated by a formula consistent with
the body proportional hypothesis (Francis, 1990): LT1 ¼ LTc (D1Dc1)v; where
LTc is LT at capture, Dc is the otolith diameter at capture, D1 is the diameter of
the otolith at the outer margin of the first hyaline zone, and v is the slope of the
regression of ln (LTc) on ln (Dc). This slope was 132 (r2 ¼ 074, n ¼ 400).
Age-based catch curves were used to estimate the instantaneous rate of total
mortality (Z). An ANCOVA model was fitted to the data, with ln (age-specific
catch) as response variable and age and locality as predictor variables. An age
group t was excluded from the analyses if the number of observations nt were
smaller than nt þ 2. The slope of the descending regression line between agegroups estimates Z. Annual survival rates were estimated as S ¼ eZ. A marginally significant difference in the catch-curve estimated Z was found among the
localities (total model r2 ¼ 089, F15,22, Ptotal model < 0001, Plocality age ¼ 0075).
The Atlantic cod generally experienced low annual survival rates, while the
highest survival estimate was found in the Grenland population (Table I).
Estimates of age and LT at 50% maturity were obtained from logistic regression models, with maturity state (juvenile or mature) as response variable, and
age (or LT) and locality as predictor variables. Model selection was based on the
AICc criteria (Burnham & Anderson, 1998). A model with a locality age
interaction effect was selected for modelling age at maturity, while a model
with a locality LT interaction effect was selected for modelling size at maturity. Likelihood ratio tests support this model selection (Plocality age < 00001,
Plocality LT ¼ 00015). Among the sites, age at 50% maturity varied from 26 to
38 years while LT at 50% maturity varied from 35 to 60 cm (Table I). Males and
females were pooled in all statistical analyses. It was tested for an overall effect
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2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 1725–1730
#
101
92
107
101
101
100
109
110
n
M (g)
1847 416
2062 1196
1534 534
1407 599
2757 1300
1598 1687
1109 632
705 521
LT (cm)
56 4
56 12
53 6
53 7
65 10
51 15
46 7
40 8
38
32
34
36
45
42
44
26
(3–7)
(2–5)
(2–5)
(2–8)
(3–7)
(2–10)
(3–8)
(2–6)
Age (years)
182 004
187 005
190 005
198 005
191 005
186 006
218 006
185 008
O1 (mm)
93 04
103 10
117 13
103 06
101 04
81 04
113 04
97 06
LT1 (cm)
564 05
626 18
567 16
538 10
618 08
466 18
427 04
485 19
LT4 (cm)
111 074
107 008
088 019
081 005
072 014
045 006
102 011
080 010
Z
033
034
041
045
049
064
036
045
S
–
33 (29–37)
–
–
38 (28–48)
31 (26–36)
31 (24–38)
26 (24–27)
–
59 (50–67)
–
–
60 (53–66)
42 (38–46)
35 (28–41)
42 (40–44)
A50 (A25–A75) LT50 (L25–L75)
– Not included in analyses due to low proportion of juveniles (<25%) in samples. Also, seven individuals were removed from all analyses because age could
not be estimated from the otoliths.
Høvåg
Bjelland
Bueøya
Tvedestrand
Risør
Grenland
Oslofjorden
Fredrikstad
Locality
TABLE I. Life history of Atlantic cod from the Norwegian Skagerrak coast, sampled (n individuals) during January to March 2000 with
standard cod gillnets (mesh-size 63–70 mm) with help from local fishermen: mean S.D. total length (LT) and mass (M), age with range of
observation in parentheses, mean S.E. otolith diameter at age 1 year (O1, adjusted for age at capture), backcalculated LT at age 1 year (LT1,
based on fish age 4 years at capture), LT at age 4 years (LT4) and instantaneous mortality (Z), annual survival probability (S), and age
(years) and LT (cm) at 50% maturity (A50 and LT50), with maturity quartiles in parentheses
ATLANTIC COD LIFE-HISTORY VARIATION
2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 1725–1730
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E. M. OLSEN ET AL.
60°
Oslo
Oslofjorden
25
Grenland
Norway
Fredrikstad
30′
54
Fredrikstad
Bueøya
35
Risør
38
Tvedestrand
59°
Grenland
40
Bjelland
Risør
Høvåg
Tvedestrand
Bueøya
Bjelland
30′
Høvåg
Skagerrak
58°
km
0
30′
7°
50
8°
Denmark
9°
10°
11°
FIG. 1. Map of the sampled region along the Norwegian Skagerrak coast. Genetic analysis of Atlantic
cod from sampling sites ( ) has previously uncovered separate local populations along this coast
(Knutsen, 2003; Knutsen et al., 2003). The phylogenetic tree depicting the relationship among the
eight samples was constructed from genetic distances of 10 microsatellite loci (DA; Nei et al., 1983),
using the UPGMA method (presenting data from Knutsen, 2003). The tree was tested for robustness in topology by bootstrapping over loci (10 000 replicates), using the POPTREE software
(N. Takezaki, unpubl. ftp://ftp.nig.ac.jp/pub/Bio/njbafd/dos/). The Bjelland and Risør sites are
exposed to the open ocean, while the rest of the sites are found in more sheltered waters. The
Fredrikstad site is within an estuary.
.
of sex on age and LT at maturity (by pooling all sampling sites). In these models
the sex-effect was not significant (P > 030).
There are potential sources of bias in the data: (a) size selectivity of the
sampling gear could have influenced the estimates of life-history variables. This
selectivity, however, should be similar among localities; (b) maturation could
have influenced the body size at age 4 years differently among sites, e.g. population
differences in observed length at age 4 years and backcalculated LT1 are not
consistent (Table I). (c) backcalculated LT could be underestimated (Campana,
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2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 1725–1730
ATLANTIC COD LIFE-HISTORY VARIATION
1729
1990; Lekve et al., 2002). Alternatively, the backcalculated lengths are not
biased, but the surviving Atlantic cod captured in this study could be a nonrandom sub-set produced by size-selective mortality. The negative age-effect on
otolith diameter at age 1 year supports this view; (d) the probability of being mature
for a given age or LT does not distinguish between first-time and repeat spawners,
and may be influenced not only by maturation probabilities but also growth and
mortality rates (Heino et al., 2002); (e) if adult individuals do not spawn every year
(Rideout et al., 2000), this will lead to bias when estimating maturation through the
probability of being mature; (f) the catch-curve approach for estimating Z assume a
stable age distribution, while the year-class strength of the Skagerrak Atlantic cod is
known to fluctuate considerably (Fromentin et al., 1997; Stenseth et al., 1999). To
some extent recruitment instabilities were corrected for by removing age groups
with few observations from the analyses.
This study provides evidence that Atlantic cod from different localities along
the Norwegian Skagerrak coast differ in size and maturity at age, maturity at
LT, and survival. Atlantic cod from Northeast Skagerrak appear to mature at
smaller sizes, as compared to Atlantic cod from Southwest Skagerrak (Table I
and Fig. 1). Atlantic cod from the Grenland fjords experience higher annual
survival as compared to fish from the other sampling sites. This may be an
effect of variation in local management regimes where Grenland has much
lower fishing pressure. In that fjord system local fishermen have not been
allowed to sell (and hence, probably have not been catching) Atlantic cod for
>10 years due to local industrial pollution. A mark-recapture experiment conducted near the Risør site suggests that fishing mortality in general is high in
these coastal populations of Atlantic cod (Julliard et al., 2001).
It is not known to what extent the geographic differences in maturation
reflect genetic variation or phenotypic plasticity. Fishes generally have highly
plastic life histories (Alm, 1959), but there is evidence for genetically based
variation in Atlantic cod life-history traits (Purchase & Brown, 2000; Jónsdóttir
et al., 2002). Since genetic analyses suggests that Atlantic cod from along the
Norwegian Skagerrak coast is structured into several local populations
[FST ¼ 00022, P < 0001 among adult Atlantic cod samples from Skagerrak
(Knutsen, 2003); FST ¼ 00023 among samples from the Norwegian Skagerrak
coast (Knutsen et al., 2003); cf. UPGMA in Fig. 1], the differences found here in
size at age and maturation patterns might have a genetic component. In conclusion, this study shows that life-history traits may vary on a small geographical scale even within a marine habitat with no obvious barriers to migration.
This study was supported by the Norwegian Institute of Marine Research, Flødevigen
Marine Research Station and the Norwegian Research Council. L. A. Vøllestad provided helpful comments on the manuscript.
References
Alm, G. (1959). Connection between maturity, size, and age in fishes. Report of the
Institute of Freshwater Research Drottningholm 40, 6–145.
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 Journal of Marine
Science 60, 787–797.
#
2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 1725–1730
1730
E. M. OLSEN ET AL.
Burnham, K. P. & Anderson, D. R. (1998). Model Selection and Inference: a Practical
Information-theoretic Approach. New York: Springer Verlag.
Campana, S. E. (1990). How reliable are growth back-calculations based on otoliths?
Canadian Journal of Fisheries and Aquatic Sciences 47, 2218–2227.
Chan, K.-S., Stenseth, N. C., Lekve, K. & Gjøsæter, J. (2003). Modeling the population
dynamical effects of pulse disturbances: the algae bloom along the Norwegian
Skagerrak coast in 1988. Ecological Monographs 73, 151–171.
Dannevig, A. (1933). On the age and growth of cod (Gadus callarias L.) from the
Norwegian Skagerrak coast. Fiskeridirektoratets Skrifter Serie Havundersøkelser
4, 1–145.
Francis, R. I. C. C. (1990). Back-calculation of fish length: a critical review. Journal of
Fish Biology 36, 883–902.
Fromentin, J.-M., Stenseth, N. C., Gjøsæter, J., Bjørnstad, O., Falk, W. & Johannessen, T.
(1997). Spatial patterns of the temporal dynamics of three gadoid species along the
Norwegian Skagerrak coast. Marine Ecology Progress Series 155, 209–222.
Gjøsæter J., Enersen K. & Enersen S. E. (1996). Ressurser av torsk og andre fisk i fjorder
på den norske Skagerrakkysten. Fisken og Havet 23, 1–28.
Heino, M., Dieckmann, U. & Godø, O. R. (2002). Measuring probabilistic reaction
norms for age and size at maturation. Evolution 56, 669–678.
Jónsdóttir, Ó. D. B., Imsland, A. K., Danı́elsdóttir, A. K. & Marteinsdóttir, 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.
Julliard, R., Stenseth, N. C., Gjøsæter, J., Lekve, K., Fromentin, J.-M. & Danielssen, D. S.
(2001). Natural mortality and fishing mortality in a coastal cod population:
a release-recapture experiment. Ecological Applications 11, 540–558.
Knutsen, H. (2003). Population structure in Atlantic cod (Gadus morhua L.) revealed by
microsatellite DNA analysis. PhD thesis, University of Oslo.
Knutsen, H., Jorde, P. E., Andre, C. & Stenseth, N. C. (2003). Fine-scaled geographic
population structuring in a highly mobile marine species: the Atlantic cod. Molecular
Ecology 12, 385–394.
Lekve, K., Ottersen, G., Stenseth, N. C. & Gjøsæter, J. (2002). Length dynamics in
juvenile coastal Skagerrak cod: effects of biotic and abiotic processes. Ecology
86, 1676–1688.
Nei, M., Tajima, F. & Tateno, Y. (1983). Accuracy of estimated phylogenetic trees from
molecular data. Journal of Molecular Ecology 19, 153–170.
Pogson, G. H. & Fevolden, S.-E. (2003). Natural selection and the genetic differentiation
of coastal and Arctic populations of the Atlantic cod in northern Norway: a test
involving nucleotide sequence variation at the pantophysin (PanI) locus. Molecular
Ecology 12, 63–74.
Purchase, C. F. & Brown, J. A. (2000). Interpopulation differences in growth rates and food
conversion efficiencies of young Grand Banks and Gulf of Maine Atlantic cod
(Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 57, 2223–2229.
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. doi: 10.100b/jfbi.2000.1405.
Ruzzante, D. E., Wroblewski, J. S., Taggart, C. T., Smedbol, R. K., Cook, D. &
Goddard, S. V. (2000). Bay-scale population structure in coastal Atlantic cod
in Labrador and Newfoundland, Canada. Journal of Fish Biology 56, 431–447.
doi: 10.1006/jfbi.1999.1168.
Stenseth, N. C., Bjørnstad, O. N., Falck, W., Fromentin, J.-M., Gjøsæter, J. & Gray, J. S.
(1999). Dynamics of coastal cod populations: intra- and intercohort density dependence and stochastic processes. Proceedings of the Royal Society of London Series B
266, 1645–1654.
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2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 1725–1730