ORIGINAL PAPER
The role of fecundity regulation and abortive maturationin the reproductive strategy of Norwegian spring-spawningherring (Clupea harengus)
James Kennedy • Richard D. M. Nash •
Aril Slotte • Olav S. Kjesbu
Received: 27 August 2010 / Accepted: 14 February 2011 / Published online: 1 March 2011
� Springer-Verlag 2011
Abstract This study investigates the reproductive strat-
egy, an important component in the estimation of stock
reproductive potential, in Norwegian spring-spawning
(NSS) herring (Clupea harengus), an iteroparous, extreme
capital spawner, through the estimation of fecundity over a
period of 3 years including two complete maturation cycles
and three spawning seasons. NSS herring have an ‘opti-
mistic’ strategy, with almost all adult herring caught in
August being in the vitellogenic stage of ovary develop-
ment, despite overwintering energy levels not being
determined at this time. Fecundity in the summer, i.e.,
more than half a year before spawning in spring (February–
April), was also much higher than could be supported by an
individual’s concurrent energy levels. Consequently,
fecundity was later reduced through atresia with the
majority of this occurring before overwintering. The total
reduction and the length of the time period in which the
reduction took place appeared to vary between years.
During the spawning season, atresia was mostly prevalent
in small first-time spawners\180 g and several individuals
aborted ovary development at this time. Final fecundity
varied between years with a difference of up to 18% and
was linked to annual variations in condition. In conclusion,
this extensive field study has demonstrated that each indi-
vidual herring can display a suite of size-specific repro-
ductive tactics to fine-tune oocyte production in response to
fluctuating levels of planktonic prey.
Introduction
There is a vast array of reproductive strategies among
fishes, and the particular strategy for a particular species
has important consequences at the population level in terms
of stock reproductive potential and sustainable fishing
mortality (Murua and Saborido-Rey 2003). Species that
partake in many breeding events must balance their energy
investment between the current year’s reproduction and
future reproduction to maximise their lifetime reproductive
output. However, when food is seasonal and unpredictable,
the decision of how much energy to invest in reproduction
can have large consequences, especially when development
of the gonads is a lengthy process. To cope with such
variations, animals must have the ability to alter their
reproductive investment as energy dictates. There are
several different mechanisms that can be employed to do
this including the reduction in fecundity in the current
reproductive cycle (Kurita et al. 2003; Kennedy et al.
2007), adjustment of the length of the spawning migration
(Slotte 1999a) or even the skipping of a reproductive event
entirely, either by not restarting ovary development or
through the complete reabsorption of the developing
oocytes (Rideout et al. 2005). These strategies can improve
lifetime fecundity by allowing for increased growth and
higher fecundity in future reproductive events (Jørgensen
et al. 2006) or simply by avoiding death due to low energy
reserves (Trippel and Harvey 1989). There are, thus,
Communicated by D. Righton.
J. Kennedy
Department of Biology, University of Bergen,
P.O. Box 7800, 5020 Bergen, Norway
R. D. M. Nash � A. Slotte � O. S. Kjesbu
Institute of Marine Research, P.O. Box 1870,
5817 Nordnes, Bergen, Norway
Present Address:J. Kennedy (&)
Møreforsking Marin, P.O. Box 5075, 6021 Alesund, Norway
e-mail: [email protected]
123
Mar Biol (2011) 158:1287–1299
DOI 10.1007/s00227-011-1648-0
several factors that must be weighed against each other to
produce the best strategy.
Atlantic herring (Clupea harengus) are an example of a
teleost fish that must balance resources between current
and future reproduction. Based upon data collected by the
Institute of Marine Research (Norway), Norwegian spring-
spawning (NSS) herring have an estimated maximum age
of about 25 years and may spawn up to 20 times. The
biomass, Fulton’s condition factor (K) (see background
information in Nash et al. 2006) and migration routes have
fluctuated greatly in the past 100 years (Holst et al. 2002;
Ndjaula et al. 2010).
Herring are capital determinate spawners. This means
that gonad development is funded from stored reserves
built up during the feeding season. NSS herring feed in the
Norwegian Sea during the summer months with size-
dependent migration where larger individuals migrate to
more northerly and westerly feeding grounds (Misund et al.
1998). In late autumn, NSS herring currently migrate to
overwintering grounds in Northern Norway where they rely
on their stored reserves for energy and gonad growth
(Slotte 1999b). Selection of new overwintering grounds is
likely to be a stochastic process but may be influenced by
the ratio of recruit and repeat spawners (Huse et al. 2010).
In late winter to early spring, they migrate southwards for a
distance of up to 1,500 km from the wintering grounds to
spawn along the Norwegian coast. Unlike many herring
populations (see McQuinn 1997), NSS herring do not show
a strict spawning ground fidelity, rather larger better con-
dition fish migrate to more southerly spawning grounds
(Slotte 1999a). This state-dependent migration is probably
related to larval survival, as the southerly spawning
grounds may provide the resulting larvae with higher
temperatures; hence, the possibility for higher growth and
survival rates (Slotte and Fiksen 2000). To complete the
life cycle, the larvae drift northward from the spawning
grounds and spend the first 3–5 years as immature fish in
the Barents Sea. Thereafter, they migrate to join the adult
populations on the feeding grounds in the Norwegian Sea
(Dragesund 1970).
NSS herring is a suitable candidate for the study of
fecundity regulation as it is relatively long lived and
individuals [320 mm have a low growth rate, growing
\10 mm per year (Dragesund et al. 1980). Slow growth
excludes any confounding effects that growth in body size
can have on fecundity estimation (Kjesbu and Witthames
2007). In addition, herring have a short feeding season,
thus do not feed for a significant period during vitello-
genesis (Slotte 1999b; Kurita et al. 2003). This means that
the majority of the material used for gonad development
comes from stored reserves, thus eliminating any influence
that unaccounted feeding activity can have on fecundity.
During this study, we sampled extensively over 3 years,
NSS herring on the summer feeding grounds, the over-
wintering grounds and on the spawning grounds. This study
investigates the dynamics in maturity and fecundity at
different periods in the year to provide a comprehensive
understanding of the reproductive strategy in an extreme
capital spawner.
Materials and methods
Collection of samples
Herring samples were collected by pelagic trawl in 2006,
2007 and 2008 during the IMR research cruises and from
commercial fishing vessels in the herring summer feeding
area, overwintering area and spawning grounds (Table 1;
Fig. 1). Females were sampled randomly from the catch
and each individual was measured (total length, nearest
5 mm), weighed (total, gonad and intestine weight, nearest
1 g) and scales taken for age reading. A sub-sample of the
ovary was preserved in 10% buffered formalin and trans-
ported back to the laboratory for analysis. To confirm that
growth in length of NSS herring above 320 mm is low, as
growth rate is known to vary in other herring stocks
(Cardinale and Arrhenius 2000; Oskarsson 2008), the mean
length for year classes 1998–2002 were taken from the
IMR central database (CDB) and tracked for the period of
the study. The herring caught for our study were considered
to be a representative sample of the entire mature popu-
lation of NSS herring. The sampling during the feeding
season covered the major areas that herring migrate to
during the summer. During winter, in the period of our
study, the entire adult herring population was thought to be
concentrated into a relatively small area off Northern
Norway. In all years, samples at the spawning grounds
were taken from an extensive area covering most of the
known spawning grounds.
Some autumn spawners were caught during the sam-
pling; these were identified as herring with a gonadoso-
matic index (GSI) (calculation below) above 10% in the
summer (Husebø et al. 2005). Autumn spawners were
excluded from all analyses; therefore, all results pertain
only to NSS herring.
Estimation of fecundity
Fecundity was estimated using the Auto-diametric method
(Thorsen and Kjesbu 2001), which works on the principle
that the number of oocytes per gram of ovary is inversely
proportional to the average size of the oocytes. This rela-
tionship is based upon physical principles, as opposed to
biological, so is unlikely to be affected fish length, weight
or K. For ovaries containing vitellogenic oocytes, the
1288 Mar Biol (2011) 158:1287–1299
123
diameter of 200 vitellogenic follicles were measured using
a binocular microscope at 79 magnification, a camera
displaying a live image and computer-aided automatic
particle analysis program (Image-J, http://www.rsbweb.
nih.gov/ij/) that analyses images captured from the camera.
For ovaries that did not contain vitellogenic oocytes, i.e.
oocytes with an insufficient level of contrast to the back-
ground, 50 randomly selected pre-vitellogenic oocytes
were measured manually using a dissecting microscope
and the manual measurement tool within the image ana-
lysis software. As pre-vitellogenic oocytes have a smaller
size range than vitellogenic oocytes, 50 oocytes were suf-
ficient to get an accurate average oocyte diameter.
The stages in the maturation of herring oocytes can be
related to their diameter. Oocytes \240 lm are in the pre-
vitellogenic stage, 250–375 lm in the cortical alveoli stage
and[375 lm are vitellogenic (Ma et al. 1998; Kurita et al.
2003). Fish with a leading cohort (LC) oocyte diameter
(average diameter of the largest 10% of oocytes)[250 lm
were considered to have commenced ovary development.
Fecundity (F) was calculated for fish with an average
(formalin fixed) oocyte diameter (OD) [400 lm using the
equation from Oskarsson et al. (2002):
F ¼ 1:708� 1010 � 1:04� OW0:936� �
� OD�2:301
OW ¼ Fresh ovary weight(g)
The original equation was based upon fixed ovary weight,
whereas the current study used fresh ovary weight; there-
fore, a correction factor was added to the equation to
correct for the approximate 4% increase in ovary weight
due to fixation (Oskarsson et al. 2002).
When using the Auto-diametric method, the estimation
of fecundity becomes inaccurate for gonads with high
atretic intensity. This is because the weight of the atretic
oocytes is taken into account, however, due to a greater
transparency, they are less likely to be detected, during the
image analysis, than normal oocytes. Atretic oocytes are
smaller than normal oocytes; thus, the average oocyte
diameter will be over-estimated and so fecundity will be
under-estimated. Therefore, ovaries with an atretic inten-
sity greater than 15% were excluded from fecundity ana-
lysis but were noted. Also, ovaries that contained hydrated
oocytes, which indicate spawning may have begun, were
excluded from the fecundity analysis.
K and GSI were calculated for each fish using the fol-
lowing equations.
K ¼ 100; 000� Total weight (gÞ=Length (mm)3
GSI ¼ 100� Gonad weight (g)=Total weight (g)
Table 1 The location, time of sampling, total number of NSS herring sampled (n), length range (mm) and percentage of herring sampled during
the study in pre-vitellogenic (PV) gonadal stage, cortical alveoli (CA), vitellogenic (V) and hydrating oocyte stage (H)
Location Month and year n Length range PV CA V H
Feeding area July–August 2006 408 275–400 1.0 2.9 96.1 0.0
Feeding area July–August 2007 204 250–375 3.0 8.3 88.7 0.0
Overwintering area October–November 2006 124 255–385 3.3 0.0 96.7 0.0
Spawning grounds February 2006 215 260–380 0.4 0.0 77.3 22.4
Spawning grounds February 2007 232 265–380 0.0 0.0 53.1 46.9
Spawning grounds February–March 2008 314 270–400 0.5 0.0 99.5 0.0
60°
65°
70°
75°(a)
66°
68°
70°
72°
74°
Lat
itu
de
(b)
15° 10° 5° 0° 5° 10° 15° 20°
10° 15° 20°
15° 10° 5° 0° 5° 10° 15° 20°
Longitude
60°
65°
70°
75°(c)
Fig. 1 Sampling location off the coast of Norway for NSS herring
during July–August (feeding season) 2006 (open diamond) and 2007
(solid circle) (a), October–November (overwintering) 2006 (opencircle) (b) and February (spawning season) 2006 (open square) 2007
(upward pointing triangle) and February–March 2008 (downwardpointing triangle) (c). Dashed rectangle (c) indicates location of b
Mar Biol (2011) 158:1287–1299 1289
123
A common criticism of K is that this variable shows a
length dependency with larger fish tending to have a higher
value of K. This was examined using common Pearson
correlation analysis in the current data sets for all years and
seasons independently. There was no significant correlation
between length and K in either of the feeding seasons.
However, there was a weak trend in the overwintering and
in the spawning season data in 2006, 2007 and 2008 (see
‘‘Results’’). Slotte (1999b) shows that the relative weight
loss during overwintering and migration is inversely pro-
portional to length in NSS herring. This indicates that the
weak positive correlation between length and K is a result
of greater weight loss, relative to body size, from feeding to
spawning rather than a statistical artefact and so is appro-
priate as a measure for weight at length for NSS herring.
Fecundity is determined by condition close to spawning
within a year (see ‘‘Results’’). In order to estimate whether
annual variations in condition can explain the annual
variations in fecundity, condition before spawning for the
population was quantified using the average weight of all
340-mm herring in the IMR CDB caught in January and
above 67�N for the years in question. Fecundity was cal-
culated using the fecundity-length equation from each year.
Weight at length decreases as herring migrate, thus, using
only fish from January and occupying north of 67�N gives
a representative estimate of condition between years
without the effect of including fish which had already
migrated large distances. The fecundity and weight of
340-mm herring were used for this comparison as it rep-
resents a length class that was about midway in the length
distributions of the repeat spawners ([320 mm) and thus
was considered representative of the whole repeat-spawner
part of the stock. To examine the differences in fecundity
within the two maturation cycles in the study, the mean
fecundity of a 340-mm fish was estimated using the
fecundity-length equations for each sampling period
(Table 2).
Estimation of atresia
The intensity of atresia was estimated in herring caught
during the spawning season that had a K \ 0.75 or with an
average oocyte diameter \1,200 lm. These criteria were
chosen because atresia rises sharply in herring with a
K \ 0.70 and is absent when the average oocyte diameter
is [1,200 lm (Oskarsson et al. 2002). In ovaries where
the average oocyte diameter was [800 lm, atresia was
estimated using whole mount preparations. Atretic oocytes
are distinguishable from normal oocytes as they are
irregular in shape, relatively smaller than normal oocytes
and have an uneven transparency (Oskarsson et al. 2002). Ta
ble
2T
he
fecu
nd
ity
–w
eig
ht
(F–W
),fe
cun
dit
y–
len
gth
(F–
L)
and
fecu
nd
ity
–le
ng
th–
Fu
lto
n’s
con
dit
ion
(F–
LK
)re
lati
on
ship
sfo
rN
SS
her
rin
gg
rou
ped
by
yea
ran
dse
aso
n,
wit
hth
en
um
ber
of
sam
ple
sin
the
rela
tio
nsh
ip(n
),th
er2
of
the
rela
tio
nsh
ipan
dth
eco
ntr
ibu
tio
no
fK
toth
er2
val
ue
(Kr2
)
Yea
rS
easo
nn
F–
Wre
lati
on
ship
r2F
–L
rela
tio
nsh
ipr2
F–L
Kre
lati
on
ship
r2K
r2
20
06
Fee
din
g3
98
F=
27
99
W-7
,96
80
.46
F=
77
09
L-1
.74
91
05
0.4
7F
=8
21
L?
61
,88
29
K-2
.45
91
05
0.4
8(0
.02
)
20
07
Fee
din
g1
87
F=
25
19
W-8
,35
60
.17
F=
56
19
L-9
.68
91
04
0.1
4F
=5
67
L?
66
,83
39
K-1
.66
91
05
0.1
6(0
.01
)
20
06
Ov
erw
inte
rin
g1
16
F=
26
29
W-1
6,7
17
0.8
6F
=7
04
9L
-1.7
09
10
50
.78
F=
65
7L
?1
04
,03
69
K-2
.40
91
05
0.8
5(0
.07
)
20
06
Sp
awn
ing
20
4F
=2
74
9W
-15
,85
10
.85
F=
70
49
L-1
.75
91
05
0.7
7F
=5
70
L?
98
,87
09
K-2
.03
91
05
0.8
5(0
.08
)
20
07
Sp
awn
ing
11
6F
=2
82
9W
-16
,09
80
.86
F=
76
49
L-1
.92
91
05
0.8
1F
=6
59
L?
71
,56
49
K-2
.10
91
05
0.8
5(0
.04
)
20
08
Sp
awn
ing
25
3F
=2
49
9W
-7,4
92
0.7
5F
=6
72
9L
-1.6
19
10
50
.72
F=
61
7L
?8
0,0
10
9K
-2.0
29
10
50
.78
(0.0
6)
Len
gth
(L)
=to
tal
len
gth
(mm
)an
dw
eig
ht
(W)
=to
tal
wei
gh
t(g
)
1290 Mar Biol (2011) 158:1287–1299
123
A minimum of 200 oocytes were counted, and the relative
intensity of atresia i.e. percentage of oocytes which were
atretic; 100 9 number of atretic oocytes/(number of nor-
mal and atretic oocytes) was calculated. Atresia was
estimated in ovaries containing oocytes \800 lm using
the profile counting method (Andersen 2003). A section of
the ovary was dehydrated in ethanol and embedded in
Technovit� resin. Several 4-lm sections were then cut and
stained with toluidine blue. To prevent the same oocytes
being present on different slides, the minimum distance
between each section was equal to the LC oocyte diame-
ter. The sections were examined under the microscope
with the total number of normal and atretic oocytes
counted (atretic oocytes were distinguished from normal
oocytes using the criteria from Hunter and Macewicz
(1985)), and the relative intensity was calculated. How-
ever, this intensity is an underestimation of the true
intensity of atresia as atretic oocytes are smaller than
normal oocytes so are less likely to be encountered in
histological sections. The relative intensity was then
adjusted using the equation from Gonzalez-Vasallo (2006)
who compared the intensity of atresia in herring ovaries
estimated using the profile counting method and the
unbiased physical disector method (Andersen 2003;
Kjesbu et al. 2010):
RIA ¼ 3:0881� A0:75ðr2 ¼ 0:93Þ
RIA, unbiased relative intensity of atresia; A, relative
intensity of atresia from profile counting. We considered
herring with an atretic intensity greater than 15% at the
time of sampling to be high because this level is outside the
range found in herring that are down regulating fecundity
during the autumn (Kurita et al. 2003).
Statistics
ln-transformed data were used for fitting linear regression
models between length and weight. Weight-, length- and
length-K-based models were fitted to un-transformed
fecundity data, as the assumption of linearity, normal dis-
tribution and homogeneity of variance between years was
met, for each sampling period and year using linear
regression. This was also done for the combined data from
the three spawning seasons. Variations in fecundity
between years were assessed using ANCOVA with either
length, weight or K as a covariate. A two-factor ANCOVA
was used to test the effect of ovary development stage on
fecundity in the summer season with length and LC oocyte
diameter as covariables.
The ability of the weight, length and length-K models
from the spawning season to accurately predict fecundity
was tested. A regression model was established using only
half the samples from each year (selected randomly using
the random function in Microsoft Excel), these were then
used to predict the fecundity of the remaining samples. The
observed fecundity was divided by the predicted fecundity.
The resultant values were plotted against their respective
predictor variable. To test the reliability of using previously
established relationships to predict fecundity for other years
where no year specific relationship is available, the length-
K model from the combined data was used to predict the
fecundity for the fish in Oskarsson et al. (2002) and Kurita
et al. (2003). The predicted values were then compared with
the actual fecundity estimated in the respective studies.
To examine the general effect of ovary development on
the strength of the fecundity-length/weight relationships,
all fish from the study were pooled and divided among ten
Table 3 Coefficient of determination (r2) values for the fecundity–
weight (W-r2), fecundity–length (L-r2) and fecundity–length ? Ful-
tons’s K (LK-r2) relationship and fecundity of a 340-mm (including
95% confidence intervals) NSS herring at different stages of ovary
development indicated by leading cohort (LC) oocyte diameter
LC oocyte diameter (lm) n W-r2 L-r2 LK-r2 K-r2 Fecundity
(thousands)
400–499 365 0.41 0.39 90 ± 2.2
500–599 148 0.38 0.33 0.41 0.08 76 ± 3.6
600–699 26 0.45 0.31 85 ± 13.0
700–799 22 0.80 0.57 0.81 0.24 74 ± 10.4
800–899 43 0.75 0.62 0.71 0.09 68 ± 4.9
900–999 53 0.88 0.81 0.85 0.04 66 ± 3.1
1,000–1,099 38 0.89 0.83 0.88 0.05 61 ± 4.2
1,100–1,199 168 0.83 0.76 0.83 0.07 68 ± 2.6
1,200–1,299 247 0.84 0.77 0.84 0.07 65 ± 1.3
1,300? 115 0.80 0.61 0.82 0.21 61 ± 2.1
Relationships are from pooled data for all sampling dates. A blank value for the LK-r2 indicates the addition of K to the regression was not
significant. K-r2 indicates the contribution of K in the LK relationship
Mar Biol (2011) 158:1287–1299 1291
123
groups according to LC oocyte diameter (Table 3) and the
fecundity of an average 340-mm herring was calculated for
each group. Differences in fecundity between groups were
tested using ANCOVA with length as covariate together
with a Scheffe post hoc test. The Scheffe post hoc test was
used due to unequal n between groups. Annual variations in
the average potential fecundity in the spawning season was
tested against the average weight of a 340-mm herring
from the IMR CDB using linear regression.
Results
Weight and age at length
There was no difference in weight at length, compared
using ln-transformed data, between the 3 years in the
feeding season or the 6 years in the spawning season
(ANCOVA; p \ 0.05), and these were best described using
linear regression (Table 4). The average length at age of
herring from age 5 (average length 310 mm (±10 mm))
increased by approximately 10 mm per year throughout the
period of the study.
All the herring caught during the summer had a
K greater than 0.70. There was no significant correlation
between length and K in either of the feeding seasons
(p [ 0.05). However, there was a weak trend in the over-
wintering (p = 0.006, r = 0.25) and in the spawning sea-
son data in 2006 (p \ 0.001, r = 0.50), 2007 (p = 0.006,
r = 0.48) and 2008 (p = 0.006, r = 0.28). These rela-
tionships were significantly different between years
(ANCOVA; p \ 0.0001).
Ovary development
The majority of the fish caught during the summer sam-
pling had clearly begun ovary development (Table 1) and
had an LC oocyte diameter between 350 and 600 lm
(Fig. 2a, b). However, several fish in the cortical alveoli
stage were also caught during the summer. The majority of
the fish caught in the overwintering grounds were in the
vitellogenic stage (Table 1) and had an oocyte diameter in
the range of 500–1,000 lm (Fig. 2c). On the spawning
grounds, the majority of the fish were either in the
vitellogenic stage or had began oocyte hydration (Table 1)
of the vitellogenic fish the oocytes were generally in the
range of 800–1,400 lm (Fig. 2d, e, f).
Ovary stage had a significant effect on fecundity with
highest fecundity at the beginning of vitellogenesis
(ANCOVA; p \ 0.0001). The general pattern showed that
fecundity decreased as ovary development progressed with
the greatest decreases occurring during early vitellogenesis
(Table 3; Fig. 3). There were no further significant
decreases in fecundity after the LC oocyte diameter
reached 600–699 lm (Table 5). There was, however, a
small but significant increase in fecundity between
900–999 and 1,000–1,099, followed by a decrease from
1,100–1,199 to 1,200–1,299 lm, but the fecundity at these
stages (1,000–1,099 and 1,100–1,199 lm) still remained
significantly less than the fecundity at the beginning of
ovary development (Table 5).
The explanatory power of weight and length on fecundity
was lowest at the beginning of ovary development and gen-
erally increased until the oocytes were around 900–1,099 lm,
it then showed a small decrease during the final part of ovary
development (Table 3). The effect of K on fecundity varied
throughout ovary development with no clear pattern.
Variation in fecundity
The linear regression models of fecundity-weight (Table 2)
had a tendency to systematically overestimate the fecundity
of herring in the lower weight range (Fig. 4a). However,
for the fecundity-length or the fecundity-length-K regres-
sions (Table 2), there was no systematic underestimation of
fecundity for herring in the lower length range (Fig. 4b, c).
There was a positive correlation between K and the
observed/predicted values from the fecundity-length
regression (p \ 0.001, r = 0.44) but not for the observed/
predicted values from the fecundity-weight or fecundity-
length-K regressions (p [ 0.05).
Fecundity in the feeding season was significantly higher
in 2007 than 2006, both when length and weight was a
covariate (ANCOVA; p \ 0.0001; Fig. 5). The LC oocyte
diameter was significantly lower in summer 2007 (mean =
431 lm, (SD = 61), n = 408) compared to summer 2006
(mean = 441 lm, (SD = 75), n = 206) (ANOVA; p \0.0001, Fig. 2), indicating a difference in ovary develop-
ment stage between years. As fecundity differences can be a
result of the development stage of the ovary the LC oocyte
diameter was included as a covariate in the ANCOVA
together with length/weight. This resulted in the year effect
on fecundity being insignificant (p [ 0.05).
There were significant differences in fecundity in the
spawning season between years when length, weight or
length together with K were used a covariates, both,
between years in the current study (Fig. 5) and between
Table 4 The weight (W; g)—length (total length, L; mm) relation-
ships for NSS herring grouped by season
Season n Relationship r2
Feeding 612 ln(W) = 2.59 9 ln(L) - 9.28 0.85
Overwintering 124 ln(W) = 3.23 9 ln(L) - 13.05 0.93
Spawning 761 ln(W) = 3.59 9 ln(L) - 15.26 0.92
1292 Mar Biol (2011) 158:1287–1299
123
years in the current study and years from previously pub-
lished studies (Oskarsson et al. 2002; Kurita et al. 2003)
(ANCOVA; p = 0.0001). The average fecundity of a
340-mm herring, calculated from the length fecundity
equations from the spawning seasons, varied between years
(ANOVA; p \ 0.0001), was lowest in 1999 and differences
between years were up to 18%. This variation was related
to the variation in the average weight of the 340-mm her-
ring taken from the IMR CDB i.e. the herring caught in
January and north of 67�N (linear regression; r2 = 0.73,
p = 0.031, Fig. 6), but was not correlated with the average
weight of the 340-mm herring used in the fecundity esti-
mates (linear regression; p [ 0.05).
The average fecundity of a 340-mm herring, calculated
from the length fecundity equations from the feeding and
spawning seasons, decreased significantly from 88 thou-
sand to 68 thousand over the maturation cycle starting in
summer 2006 and ending in spring 2007, a decrease of
23%. In the subsequent cycle, fecundity decreased from 93
thousand in summer 2007 to 68 thousand in spring 2008, a
decrease of 27%. The largest value of fecundity for a
340-mm herring in August 2006 and February 2007 was
129 thousand and 69 thousand, respectively, which equated
to a difference of 47%. For all length groups, weight-spe-
cific fecundity increased by 9.1% between October 2006
and February 2007 (ANCOVA; p \ 0.001) while length-
0
200
400
600
800
1000
1200
1400
1600
0
200
400
600
800
1000
1200
1400
1600L
C o
ocy
te d
iam
eter
(µm
)
(a) (b)
(c)
240 260 280 300 320 340 360 380 4000
200
400
600
800
1000
1200
1400
1600
240 260 280 300 320 340 360 380 400
Length (mm)
(d)
(f)(e)
Fig. 2 Leading cohort (LC)
oocyte diameter plotted against
length for NSS herring caught
on the feeding grounds in July–
August 2006 (a) and 2007 (b),
on the overwintering grounds in
October 2006 (c) and on the
spawning grounds in 2006 (d),
2007 (e) and 2008 (f). Points
marked with an x indicate fish
with an atretic intensity greater
than 15%. Dashed line at
250 lm indicates the threshold
for a fish to be considered to
have started ovary development
Mar Biol (2011) 158:1287–1299 1293
123
240 280 320 360 400
1300+
240 280 320 360 400
Length (mm)
1200-1299
240 280 320 360 4000
40
80
120
160
2001100-1199
1000-1099900-999
0
40
80
120
160
200
Po
ten
tial
fec
un
dit
y (t
ho
usa
nd
s)
800-899
700-799600-699
0
40
80
120
160
200500-599
0
40
80
120
160
200400-499
Fig. 3 Relation between length
and fecundity for NSS herring at
different stages of oocyte
development. Legend indicates
oocyte size (lm) class in the
graph. Linear regression lines
are shown
Table 5 Post hoc comparisons of fecundity at length (as covariate) between oocyte diameter groups
1 2 3 4 5 6 7 8 9
400–499 (1)
500–599 (2) ***
600–699 (3) *** 0.16
700–799 (4) *** *** 0.86
800–899 (5) *** *** 0.36 1.00
900–999 (6) *** *** 0.54 1.00 1.00
1,000–1,099 (7) *** *** *** 0.28 0.33 0.10
1,100–1,199 (8) *** *** *** 0.20 0.17 * 1.00
1,200–1,299 (9) *** *** 0.32 1.00 1.00 1.00 ** ***
1,300? (10) *** *** 0.84 1.00 0.97 1.00 *** *** 0.98
Values are p values with * p \ 0.05; ** p \ 0.001; *** p \ 0.0001
1294 Mar Biol (2011) 158:1287–1299
123
specific fecundity did not change (ANCOVA; p [ 0.05).
Weight at length decreased by 10% during the same period
(ANCOVA; p \ 0.001).
The resultant model from the combined fecundity data
from all three spawning seasons (2006–2008) was
F ¼ 611� Lengthþ 8:69� 104 � K � 2:07� 105
r2 ¼ 0:84; df ¼ 576; p\0:001
Using this equation to predict the fecundity in December
1996, January 1998 (Oskarsson et al. 2002) and February
1999 (Kurita et al. 2003) using the original length and weight
data gave an average underestimation of 7, 11 and 26%,
respectively, compared to the observed fecundity estimate
based upon gravimetric/Auto-diametric methodology.
Atresia
In 2006, 2007 and 2008, atresia was present in 16, 37 and
16% of the fish examined for atresia in the spawning
260 280 300 320 340 360 380 400
Length (mm)
0.00
1.00
2.00
3.00
Ob
serv
ed/p
red
icte
d
100 200 300 400 500
Weight (g)
0.00
1.00
2.00
3.00
260 280 300 320 340 360 380 400
Length (mm)
0.00
1.00
2.00
3.00
(a)
(b)
(c)
Fig. 4 The deviation from linear prediction of the fecundity and the
observed fecundity for fecundity versus weight (a) and length (b) and
length-K (c)
240 260 280 300 320 340 360 380 400
Length (mm)
0
40
80
120
160
200
Po
ten
tial
fec
un
dit
y (t
ho
usa
nd
s)
0
40
80
120
160
200 (a)
(b)
Fig. 5 Relation between length and fecundity, with regression lines
shown, for NSS herring caught in the feeding area during summer
1998 (open circle solid line), 2006 (open diamond dashed line) and
2007 (open square dash dot line) (a), and spring 2006 (open diamonddash dot line), 2007 (open square solid line) and 2008 (opendownward pointing triangle dashed line) (b)
Mar Biol (2011) 158:1287–1299 1295
123
seasons, respectively. Note that this result does not repre-
sent the prevalence in the whole population as these fish
were not selected randomly but due to a higher likelihood
that atretic oocytes would be present at that time of the
year. All fish, which had an atretic relative intensity greater
than 15%, which is considered to be high, had a
weight \180 g (Fig. 7), a length \ 305 mm and a K \0.72. The percentage of fish that had atresia accounted for
4, 2 and 4% of all the fish analysed for fecundity in the
2006, 2007 and 2008 spawning seasons, respectively.
These consisted of twenty 4-year-old fish and two 5-year-
old fish so are likely to be recruit spawners (ICES 2010).
Nine of these fish (eight 4-year-old and one 5-year-old) had
an atresia [95%.
Discussion
Skipped spawning is a common phenomena amongst tel-
eosts with the most common sub-group categories in
female wild fish being ‘resting’ (failure to begin ovary
development) and ‘reabsorbing’ (reabsorption of oocytes
through atresia) (Rideout et al. 2005). The resting category
is not prevalent in the NSS herring, as can be seen from the
fact that almost all herring caught in the feeding grounds
had begun ovarian development. This is probably because
all individuals were above the threshold value of K (0.70),
which guarantees the beginning of ovary development
(Kennedy et al. 2010). Even though some herring would be
above the threshold value of K when ovary development
begins, they may still not have accumulated sufficient
energy reserves to fully support ovarian development,
survive the winter and carry out extensive migrations.
However, after they have begun ovary development, her-
ring will feed for approximately another 5 months, which
may give them enough time to accumulate sufficient
reserves (Slotte 1999b; Kurita et al. 2003).
During early vitellogenesis, herring had a high fecun-
dity, which was poorly related with size or condition
(Table 3). As ovary development begins approximately
5 months before the end of the feeding period (Kurita et al.
2003), fecundity at that time cannot reflect the level of
energy reserves at the over wintering and spawning time,
because these have not yet been determined. Herring have
a determinate fecundity which means that after spawning
has commenced no more oocytes are recruited to the
developing cohort. For many determinate spawners,
including herring, there is a gap of several months between
the end of oocyte recruitment and spawning. This tempo-
rally restricted pulse of recruitment of a large number of
pre-vitellogenic oocytes to the developing pool allows
subsequent reductions of fecundity in order for it to reflect
the level of energy reserves present closer to the breeding
season. This allows the possibility of a higher fecundity
than would be achieved if fecundity was determined by the
energy reserves when the oocytes were initially recruited.
280 300 320 340 360
Weight (g)
45
50
55
60
65
70
75P
ote
nti
al f
ecu
nd
ity
(th
ou
san
ds)
1999
1997
1998
2006
20072008
Fig. 6 Average potential fecundity versus average weight for a
340-mm NSS herring. Numbers on the graph indicates year. Errorbars show 95% confidence limits. Line shows linear regression fit.
Data for 1997 and 1998 are from Oskarsson et al. (2002) and data for
1999 are from Kurita et al. (2003). Data for 1997 are from December
1996 but are applicable to the 1997 spawning season
100 200 300 400 500
Weight (g)
0
20
40
60
80
100
Rel
ativ
e in
ten
sity
of
atre
sia
(%)
Fig. 7 Relative intensity of atresia in relation to weight for NSS
herring caught on the spawning grounds between 2006 and 2008.
Dashed line at 15% indicates threshold above which intensity is
considered high
1296 Mar Biol (2011) 158:1287–1299
123
This down-regulation of fecundity occurs in other herring
populations (van Damme et al. 2009) and also seems to be
a common mechanism across other determinate spawners
too as it has been documented in, cod (Gadus morhua)
(Thorsen et al. 2006), plaice (Pleuronectes platessa)
(Kennedy et al. 2007) and Greenland halibut (Reinhardtius
hippoglossoides) (Kennedy et al. 2009).
As ovary development progresses, body size and con-
dition explain an increasing amount of the variation in
fecundity and fecundity down-regulation ceased during
overwintering. During overwintering, the rate of food
consumption by herring declines and they start to rely on
stored energy reserves (Slotte 1999b). After this point, it is
unlikely that the herring will gain any additional energy,
therefore fecundity is reduced to closely match body con-
dition. These results indicate that condition many months
before spawning plays an important role in the determi-
nation of fecundity in herring.
Our results showed a lower degree of down-regulation
compared to that found by Kurita et al. (2003), who
reported that fecundity decreased by 57% between July and
February, whereas our study showed a decrease of 23 and
27% between August and February in the years studied.
Kurita et al. (2003) estimated a higher potential fecundity
in July and a lower potential fecundity in February com-
pared to the present study. The range in the summer
fecundity from Kurita et al. (2003) is equivalent to the
variation in the fecundity seen in the current study. How-
ever, due to this high variation between individuals, a
larger number of samples are required to get a reliable
average for fecundity than was sampled in Kurita et al.
(2003), so Kurita et al. (2003) may have overestimated the
average fecundity which may explain some of the differ-
ence in the level of down-regulation. The lower fecundity
in February 1999 found by Kurita et al. (2003) is related to
the low condition of herring in that year and will also
account for some of the difference in down-regulation
between studies. This shows that fecundity differences
between years are brought about mainly by variation in the
degree of down-regulation of oocytes as opposed to vari-
ation in the number of oocytes beginning vitellogenesis.
The highest fecundity estimates for a 340-mm fish in
August 2006 (129,000) and February 2007 (69,000),
showed a difference of 47%, which is comparable to Kurita
et al. (2003)’s value of 57%. This leads us to conclude that
high levels of down-regulation are possible for individual
fish; however, these represent more of an extreme value in
individuals rather than the norm.
The largest part of the down-regulation in fecundity
occurred during early vitellogenesis. Between overwinter-
ing and spawning fecundity did not decrease despite further
decreases in body weight (Fig. 3). Kurita et al. (2003)
found that the largest decrease in fecundity occurred
between July and October, which is in agreement with the
current study. However, Kurita et al. (2003) state that the
fecundity continues to decreases between October and
January which is in contrast to the present study. The
reason for this difference in the two studies is not clear but
may represent flexibility in the fecundity regulation pro-
cess. In years of lower energy reserves or higher energy
depletion during overwintering, down-regulation may
occur for a greater part of the ovary development leading to
a lower fecundity; the weight of herring caught North of
67� in 1999 was the lowest of the 6 years studied (Fig. 6).
During the spawning season, there were many small fish
(\180 g) which exhibited high levels of atresia ([15%),
including some with relative intensities of [95% (Fig. 7).
It is likely that the all of these fish were recruit spawners as
deduced from their age. The herring with an atretic inten-
sity [95% would not have spawned in that season, prob-
ably due to insufficient energy reserves to complete the
maturation of their oocytes, thus abandoned ovary devel-
opment and spawning. These herring were probably
attempting to spawn for the first time as deduced from their
age, thus are not skipping spawning in the true sense of the
term (Rideout et al. 2005). Atretic intensities up to 100%
have previously been documented in herring caught close
to the spawning season (Oskarsson et al. 2002). These
consisted of herring with K less than 0.70, similar to the
current study. However, Oskarsson et al. (2002) did not
give details on the weight or age of these herring. Irre-
spective of that, it appears that this aborted maturation may
commonly occur in a small number of first-time spawners
each year. The reasons for this may be due to smaller
herring having insufficient energy reserves for spawning.
This could be a result of lower energy storage capacity due
to their small body size, smaller fish also have higher
weight-specific metabolic rates and swim less economi-
cally (Schmidt-Nielsen 1984). It is interesting to note that
the aborting of ovary development occurred very close to
the spawning season and on the spawning grounds indi-
cating the ‘decision’ not to spawn was made as far into
ovary development as was possible. It is currently unclear
whether the herring with atretic intensities between 15 and
60% would spawn or would go on to absorb the remaining
oocytes. The majority of these individuals had oocytes
between 400 and 1,000 lm, the stage in which the major
part of down-regulation occurs. However, the intensities
are higher than expected at that development stage (Kurita
et al. 2003), and their oocytes are less developed than the
other herring caught at the same time. It therefore seems
likely that these herring will not spawn and will go on to
reabsorb the remainder of their oocytes.
There were significant variations in fecundity, in the
spawning season, between years with a difference of up to
18% between years with this difference being significantly
Mar Biol (2011) 158:1287–1299 1297
123
correlated with change in body weight between years
(Fig. 6). Variations in the average potential fecundity of a
340-mm herring was better correlated with the average
body weight of 340-mm herring taken from the IMR CDB
than the average weight of the herring that were actually
involved in fecundity estimation. The weight of the herring
taken from the IMR CDB was limited to herring caught
from latitudes above 67�N. The herring above 67�N will be
mostly overwintering/early migrating herring and so give a
good reflection of condition before the start of the migra-
tion. The timing of sampling for fecundity during the
spawning season was not standardised between years and
the herring within a sampling period were also caught at
different stages of migration. This leads to a reduced ability
to accurately quantify the variability in condition between
years, and its effects on the fecundity, as herring which had
began migration, assuming they started with a similar
condition, will have a lower condition than those that had
not.
When estimated at a similar point in ovary development,
weight is generally considered to be the best predictor of
fecundity at the individual level (Koops et al. 2004;
Skjæraasen et al. 2006; Kennedy et al. 2007), provided
none of the fish have fallen below a critical energy point
where relative fecundity starts to fall (Kjesbu 2009).
However, weight-based fecundity linear models overesti-
mated the fecundity of herring in the lower weight range
(Fig. 4a). This is most likely due to the greater prevalence
and intensity of atresia seen in herring of this size leading
to a much lower fecundity. The best predictor of fecundity
at the individual level was a combination of length and
K. However, this equation did not prove useful for the
prediction of fecundity in other years with considerable
underestimations of fecundity when tested against observed
fecundity data from previous years. The reason for this is
likely due to variation between years in the migratory
distance the herring had undertaken before capture. This
would affect the energy reserves of the herring at the time
of sampling and so affect the predicted fecundity. Thus,
when using established fecundity models to backcalculate
total egg production for species that undertake spawning
migrations, it would be advisable to use the length-weight
relationships for individuals which have not began their
spawning migration.
The addition of K increased the explained variance in
fecundity in all sampling periods but the amount of vari-
ance explained varied through ovary development with no
distinct pattern (Table 3). Many previous studies have
found that measurements of energy reserves generally add
little to the explained variance in fecundity (see Rideout
and Morgan 2010 and references therein). Rideout and
Morgan (2010) described this as a problem of sampling
time which results in the masking of the effects of
condition i.e. sampling too early in development can mask
the effect of indices of condition if the effects of condition
on fecundity have not been fully expressed. On the other
hand, the effect of condition at the beginning of ovary
development on fecundity may not be expressed until close
to spawning, so sampling too close to spawning may mask
the effect as condition, both absolute and relative to other
fish, may have changed. As most of the down-regulation of
fecundity occurred during early development of the ovary
and there was no change in fecundity from overwintering
to the spawning season, it is clear, as mentioned earlier,
that energy reserves at the beginning of overwintering are
important for the determination of fecundity. However,
K may not be an accurate measure of energy levels in
herring which may be why it explains only a small and
varying amount of variance in the fecundity linear models
(Davidson and Marshall 2010).
Acknowledgments The study was funded by the Research Council
of Norway (NFR) project ‘‘Timing and determination of fecundity
and skipped spawning: implications for stock—recruitment theory of
determinate spawners’’ (173341/S40) and encouraged by discussion
with and the terms of references of the NAFO Working Group on
Reproductive Potential and COST Action Fish Reproduction and
Fisheries (FA0601). We would like to thank the crew and personnel
of the M/S Libas, M/S Gardar and R/S G.O. Sars for the collection of
samples. A warm thank you also to Anders Thorsen, Merete Fonn and
Bente Njøs Strand for help and advice in the analyses of samples and
to Cindy van Damme (IMARES, The Netherlands) and the anony-
mous readers and referees who gave valuable comments on earlier
drafts of the manuscript.
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