1914
Recruitment dynamics of the Gulf of Riga herring stock:
density-dependent and environmental effects
Tiit Raid, Georgs Kornilovs, Ain Lankov, Anne-Marin Nisumaa, Heli Shpilev, and Ahto Järvik
Raid, T., Kornilovs, G., Lankov, A., Nisumaa, A-M., Shpilev, H., and Järvik, A. 2010. Recruitment dynamics of the Gulf of Riga herring stock:
density-dependent and environmental effects. – ICES Journal of Marine Science, 67: 1914 – 1920.
The Gulf of Riga and open-sea stocks of the Baltic herring have displayed remarkably consistent inverse recruitment and stock development patterns since the 1970s: the open-sea stocks steadily declined, whereas the Gulf stock increased rapidly in the early 1990s,
reaching a peak abundance in the early 2000s and exceeding the level of the 1970s by a factor of 2 – 3. The increase was accompanied
by a decline in the mean weight-at-age and the condition factor. The estimated decline (by 30– 40%) in the average annual consumption rate per individual and changes observed in the zooplankton community suggest that density-dependent effects may have
increased since the 1970s. The current period of high stock sizes is also characterized by greater recruitment variability. Historical
fecundity investigations have established that the average egg production per individual has decreased in all age groups by 20 –
50%, along with a decrease in mean weight and condition. Yet, the effect on recruitment has been low so far, because lower fecundity
has been compensated by the greater abundance and population fecundity has been maintained at the original level. Recruitment
appears to be more influenced by environmental conditions than by spawning-stock biomass.
Keywords: Baltic herring, condition, consumption, density-dependence, fecundity, Gulf of Riga, recruitment.
Received 6 November 2009; accepted 18 June 2010; advance access publication 29 September 2010.
T. Raid: European Commission Joint Research Centre, Institute for the Protection and Security of the Citizen, Maritime Affairs Unit-FISHREG, Via
E. Fermi 1, I-21027 Ispra (VA), Italy. G. Kornilovs: Latvian Fish Resources Agency, Daugavgrivas 8, Riga LV-1048, Latvia. A. Lankov and H. Shpilev:
Estonian Marine Institute, University of Tartu, Lootsi 2a, EE-80012 Pärnu, Estonia. A-M. Nisumaa: Laboratoire d’Océanographie de Villefranche,
CNRS-Université, de Paris 6, BP 28, 06234 Villefranche-sur-mer Cedex, France. A. Järvik: Estonian Maritime Academy, Mustakivi 25, EE-13912
Tallinn, Estonia. Correspondence to T. Raid: tel: +39 0332 786597; fax: +372 671 8900; e-mail: [email protected].
Introduction
Baltic herring (Clupea harengus membras) demonstrate remarkable geographical variability. The 10 –12 local populations
(Ojaveer, 1981, 1989) are adapted to the highly variable environmental conditions, which are reflected in differences in morphology, growth patterns, and stock dynamics. However, tagging
experiments, observations on catch composition, and acoustic
surveys (Aro, 1989; Parmanne, 1990) have indicated a considerable
amount of spatial and temporal mixing, particularly during the
feeding period in the open-sea area. Moreover, the rate of
mixing is highly variable, which makes stock separation for assessment and management purposes problematic. Therefore, assessment and management of Baltic herring only partly follow the
established population structure. The Gulf of Riga (Subdivision
28.1) herring is an exception in this respect, and the trends in
the dynamics of this stock are well monitored.
The Gulf of Riga herring is slow-growing and characterized by
one of the lowest mean length- and weight-at-age in the Baltic,
quite different from the neighbouring stock in the central Baltic
(Subdivisions 25 –27, 28.2, 29, and 32), which represents essentially a complex of several populations. The Gulf of Riga population does not undergo major migrations into the open sea and
largely resides within the Gulf. Only a minor component of the
older herring may leave the Gulf during summer and autumn,
after the spawning season, but returns thereafter. The extent of
migration depends on stock size and on local feeding conditions.
In the 1970s and 1980s, when the stock was low, the number of
migrating fish was considered negligible. In the mid-1990s, the
migration rate increased, but since 2000, the catch of Gulf of
Riga herring in the central Baltic never exceeded 6% of the total
catch (ICES, 2009a). The herring fishery within the Gulf has
been prosecuted by Estonia and Latvia, using both trawls and
trapnets.
The Gulf of Riga and the central Baltic herring stocks have
exhibited a remarkably consistent inverse development since the
1970s: the latter decreased throughout the period, whereas the
Gulf stock started to increase in 1990s and remains at a high
level up to the present (ICES, 2009a).
Two distinct periods can be distinguished in the Gulf of Riga
herring over the past three decades (Figure 1a): a “low-stock”
period up to 1987–1989 and a “high-stock” period since then,
with the difference in the average abundance exceeding a factor
of 2. Around the same time, the mean weight-at-age dropped by
a similar factor (Figure 1b). This pattern is similar to the decrease
in growth exhibited by most Baltic herring stocks during the past
30 years (Rönkkönen et al., 2004). Focusing on the mechanisms
determining recruitment in Baltic herring, Cardinale et al.
(2009) suggest that climate and/or foodweb structure may
indirectly affect recruitment via prey availability, either for the
recruits or for the spawners. In addition, clear changes in diet
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1915
Recruitment dynamics of Gulf of Riga herring
Fecundity samples were collected from the trapnet catches
along the southern and the northeastern coasts of the Gulf of
Riga in 2005 and 2006. Gonads of three females per 0.5 cm
length class were collected and preserved in 70% alcohol. Total
length, weight, and age were also determined. Subsequently,
only gonads with non-ovulated oocytes were selected, and all
oocytes in one or two subsamples of 200 mg from each gonad
were counted and weighed to obtain an estimate of the total
number of oocytes in the ovary (absolute fecundity). These
data were used to calculate the population fecundity, which is
defined as the sum of eggs spawned annually by all age groups
comprising the spawning biomass (Serebryakov, 1990). We
assumed that all females in age group 2+ of length, L,
≥120 mm were mature. The 2005/2006 data by length class
were also used to estimate population fecundity for 2001–
2005. Historical information from the 1970s (Ojaveer, 1983,
1988) was used for population fecundity estimates for the early
1980s. Stock size estimates for the respective periods were
taken from ICES (2009a).
Consumption estimates
Figure 1. (a) Total abundance (N; ages 1+) and recruitment-at-age
1 (R); and (b) mean weight (W ) for ages 1– 5 and 6+, 1977 – 2007
(ICES, 2008).
and prey availability have been documented since the late 1980s
(Möllmann et al., 2000, 2004; Kornilovs et al., 2001).
Fecundity depends on size, weight, and body condition
(Anokhina, 1969; Rannak, 1970; Munthali and Ribbink, 1998;
Oskarsson and Taggart, 2006; Lambert, 2008), which in turn
reflect conditions for growth as determined by environmental
factors (Möllmann et al., 2003, 2005; Casini et al., 2004, 2006;
Checkley et al., 2009). Consequently, the sudden decrease in
mean weight-at-age observed in the late 1980s could be expected
to have been accompanied by a deterioration in feeding conditions, lower consumption rates, and lower fecundity.
Therefore, recruitment may have been affected as well. Our goal
was to explore the mechanisms affecting recruitment in the Gulf
of Riga herring within the context of possible changes in food consumption and fecundity.
Material and methods
Data
The basic biological information on stock development was
derived from ICES (2008, 2009a). To estimate the average
Fulton’s condition factor (CF; Nash et al., 2006) for the whole
year and population fecundity, data from Estonian and Latvian
commercial pelagic trawl catches of 1984– 1988 (11 808 individuals), 1991–1995 (17 033 individuals), and 2001–2005 (18 486
individuals) were used. Because pelagic trawls use a mesh size of
10 –20 mm, the effect of trawl selectivity on the size and weight
composition of catches was assumed marginal. For 1980–1983,
CF values were obtained from Latvian data; however, because
these only covered August –September, they were corrected for
the mean difference between the average value for these 2
months and the all-year mean.
The information on herring food composition, collected during
the main feeding period from May to November in 1994–1998,
was used to calculate consumption, based on the energy contents
of the major groups taken from the literature (Table 1). Stomach
samples were collected from daytime trawl-survey catches (haul
duration: 30 min; codend mesh size: 10 mm) in the northeastern
part of the Gulf of Riga (depth range: 6– 54 m). Samples were preserved in a 4% solution of buffered formaldehyde and analysed in
the laboratory using standard procedures (Cassie, 1971; Henroth,
1985).
Food consumption by the stock was calculated according to
Winberg’s (1970) bioenergetics model, using data available from
various sources (Ricker, 1973; Aneer, 1975, 1980; Chekunova
and Naumov, 1977; Green, 1978; Chekunova, 1979; Melnitchuk,
1980; Arrhenius and Hansson, 1993, 1995; Raid and Lankov,
1995), supplemented with information on growth and population
estimates. Annual consumption (C) is expressed by (Winberg,
1970):
C = Em + P + Pq + Eloss (kJ year−1 ),
(1)
where Em is the energy used in metabolism, P the energy stored
annually in growth, Pq the energy released as eggs, and Eloss the
energy losses. The mean temperature of the surface and mixed
layers (0–40 m) during the main feeding period of herring for
1998–2007 (from the Environmental Marine Information
System; http://emis.jrc.ec.europa.eu) was used to estimate
Krogh’s temperature coefficient for calculations of Em (Raid and
Lankov, 1995). Taking into account the mean duration of
spawning and wintering periods, when feeding intensity is
low, the average duration of the annual feeding period was
assumed to be 215 d. Energy used annually for growth was calculated from
P = cDW
(kJ year−1 ),
(2)
where DW is the annual growth in weight. An average value of 5.53
was used for c (Aneer, 1975).
1916
T. Raid et al.
Table 1. Average prey composition (% wet weight) by length class (cm) of herring (in parenthesis: number of stomachs analysed) and the
energy content used in calculating consumption.
Composition by length class
Prey groups
Copepoda
Cladocera
Ostracoda
Lamellibranchiata larvae
Zooplankton (sum)
Mysidae
Amphipoda + Isopoda
Fish larvae
<10 (544)
90.2
7.5
0.0
0.1
97.8
1.4
0.0
0.8
10 –12 (191)
87.0
9.3
0.0
0.2
96.6
1.0
0.9
1.6
12– 14 (742)
69.2
27.5
+
0.0
96.7
2.1
+
1.2
14 –16 (535)
58.2
31.9
0.0
0.0
89.9
7.7
+
2.2
≥16 (68)
56.0
15.4
0.0
0.0
71.3
28.1
0.6
0.0
Energy content (kJ g21), source
2.85,
3.35,
3.98,
5.12,
Laurence (1976)
Hakala (1979)
Hill et al. (1992)
Aneer (1975)
+, present
Energy released at spawning was calculated using unpublished
data on the fecundity –weight relationship (A-MN, pers. obs.):
F = 0.462W + 0.355,
(3)
where F is the fecundity (in ′ 000 eggs). Taking the diameter of an
egg as being equal to 1 mm and the ratio between dry and wet
weight as 0.24 (Green, 1978), gonad dry weight (GW) can be calculated from:
GW = 0.126F (g).
(4)
According to Green (1978), the mean energetic value of clupeoid
gonad dry weight is 21.94 kJ g21. Therefore, the equation of
energy annually released at the spawning of herring (Pq) reduces to
Pq = 2.76(0.462W + 0.355) (kJ year−1 ).
(5)
Results
The CF revealed a steady downward trend over the period, without
major breakpoints (p , 0.001; Figure 2a). The average annual
consumption estimates reveal that an average herring in the population consumed 25 –30% less in recent years than in the 1980s.
Consumption decreased steadily from 1990 to 1998 (i.e. after the
main stock increase) and it has fluctuated since then
(Figure 2b). Mean weights and CF were well correlated with the
estimated consumption rates in 1977–2007 (Figure 2c).
The estimates of average individual fecundity for 2005/2006
reveal a severe decline compared with the historical estimates in
the 1970s. Although the general shape of the length –fecundity
relationship has remained relatively unchanged, average fecundity
has decreased in most abundant length groups by 30 –45% and in
larger size groups by more than 50% (Figure 3). The fecundity estimates for 2005/2006 were also 5 –15% lower than those reported
by Kornilovs (1997) for 1995.
Recruitment plotted against stock size for the two periods
suggests that the annual variability of the former was higher
during the later period of high stock abundance (Figure 4a), and
particularly so during the 2000s (Figure 1). A similar graph for
the central Baltic herring displays essentially the same feature,
although in this case the most recent period was characterized
by less recruitment and lower recruitment variability
(Figure 4b). Although both sets suggest an almost linearly increasing stock –recruitment relationship, it is equally possible that in
both cases stock biomass followed a change in the level of recruitment, rather than recruitment following the biomass.
Figure 2. Trends in (a) mean condition factor (CF), 1980– 2008; (b)
total biomass (B) and mean annual consumption per individual (C),
1977 –2007; and (c) estimated relationships between mean weight
(W ) and mean annual consumption per individual (W ¼ 85.6C 2
0.9; r 2 ¼ 0.80) and between CF and C (CF ¼ 5.79 C + 5.00; r 2 ¼
0.63), 1980 –2007. All values for age groups 1– 6.
Regarding population reproductive output, the overall increase
in population abundance since the 1980s appears to have largely
compensated for the decline in individual fecundity (Table 2),
1917
Recruitment dynamics of Gulf of Riga herring
Table 2. Estimates of female stock size (Nfem), population
fecundity (Fecpop), realized recruitment (R), and recruitment
success (R/Fecpop) during selected years during the periods of low
and high stock sizes.
Figure 3. Fecundity– length (Fec, L) relationship for the Gulf of Riga
herring in the 1970s (Fec ¼ 0.78 L 3.66; r 2 ¼ 0.98; from Ojaveer, 1983,
1988) and in 2005 –2006 (Fec ¼ 3.41 L 2.90; r 2 ¼ 0.69).
Year
Nfem (3106)
Low stock size
1984
1 074
1985
1 405
1986
1 393
1987
1 330
1988
2 423
Average
1 525
s.d.
519.3
High stock size
2001
2 291
2002
3 348
2003
2 624
2004
3 811
2005
2 322
Average
2 879
s.d.
672.7
Fecpop (31012)
R (3109)
R/Fecpop
15.4
19.8
20.7
18.6
32.0
21.3
6.3
1.37
1.11
3.86
0.55
1.26
1.63
1.29
0.009
0.006
0.019
0.003
0.004
0.008
0.006
18.3
25.9
22.2
28.8
18.5
22.7
4.6
2.26
6.58
1.01
3.17
6.25
3.85
2.46
0.012
0.025
0.005
0.011
0.034
0.017
0.012
Figure 4. Relationship between spawning-stock biomass (SSB) and R
for (a) Gulf of Riga herring during 1978 – 1988 (low stock size) and
1989 –2007 (high stock size); and (b) central Baltic herring during
1975 –1989 (high stock size) and 1990 – 2006 (low stock size).
because population fecundity varied virtually in the same range
(15– 32 × 1012 eggs for 1984– 1988 vs. 18 –29 × 1012 eggs for
2001–2005). These estimates also suggest a well-defined positive
relationship between stock size and population fecundity during
both periods. Yet, the data suggest that the increase in population
fecundity per unit of stock size has been somewhat lower during
the “high-stock” period (Figure 5a).
Although the population fecundity did not change between
the two periods, the recruitment was approximately a factor
Figure 5. Relationships between (a) female stock abundance
(≥11 cm; Nfem) and population fecundity (Fecpop) under low
(1984 – 1988; y ¼ 0.121 x + 2883; r 2 ¼ 0.99) and high (2001 – 2005;
y ¼ 0.068 x + 3316; r 2 ¼ 0.98) stock size conditions; and (b)
population fecundity and recruitment (R) during the same periods.
of 2 higher in 2001–2005 (Figure 5b). On average, 0.008%
of the eggs produced (according to the estimated population
fecundity) appeared as recruits in 1984–1988, whereas the
corresponding value for 2001–2005 was 0.017% (Table 2).
1918
We interpret these results as supporting the view that recruitment was enhanced, whereas population fecundity (or reproductive potential) remained largely unchanged. Therefore, the
difference in recruitment level should not be sought in a
higher spawning-stock biomass as an index of reproductive
potential, but in a change in environmental conditions affecting
the survival of prerecruits.
Discussion
Several studies have established that the shift in zooplankton composition in the late 1980s to early 1990s (decrease in copepods and
increase in the proportion of cladocerans) has had major effects on
the feeding conditions of the pelagic stocks in the Baltic, and
herring stocks specifically (Möllmann and Köster, 1999;
Kornilovs et al., 2001; Raid et al., 2003; Möllmann et al., 2005;
Cardinale et al., 2009). Consequently, the dietary overlap
between herring and sprat increased substantially (Checkley
et al., 2009). In addition, in the Gulf of Riga, the biomass of
larger copepods (specifically Limnocalanus macrurus), which constituted a key part of the herring diet in the past, has decreased significantly since the 1980s (Sidrevics et al., 1993) and herring has
largely switched to feeding on cladocerans and smaller copepods
(Ojaveer et al., 1989, 1999). Our data on mean weights and condition factor correlated well with the estimated consumption
rates, and these data support a shift in the feeding conditions
around 1990 (Figure 2).
The processes governing recruitment may be tentatively split in
two important loops that can both be affected by the environment
(Figure 6). Environment-related factors, such as availability of
suitable spawning substrata, temperature and salinity conditions
on the spawning grounds, abundance, and composition of the
zooplankton and the temporal match or mismatch with secondary
production, affect the mortality at the early stages of development.
Likewise, stock-related factors such as condition of fish and
fecundity are also tuned by the environment. Consequently,
recruitment success represents the result of complex dynamic
interactions between stock and the environment.
In the Gulf, strong year classes are formed mainly in warm
springs after warm winters, which promote high production
during the period of larval development and favour survival
(Rannak, 1971; Ojaveer, 1988). A positive correlation between
zooplankton abundance and herring year-class strength was
established during the period of low stock size (Kornilovs,
1997), but this continued to apply during the recent period
T. Raid et al.
with high stock size and this relationship is still used for predicting recruitment (ICES, 2009a). The differences in recruitment
success between the two periods are apparently explained
largely by the temperature conditions. The period until the end
of 1980s is characterized by a series of rather cold winters that
were unfavourable for herring reproduction in the area. Since
the end of the 1980s, the majority of winters have been mild
and only three winters had permanent ice cover resulting in
poor year classes (ICES, 2009b).
The conflicting developments in recruitment and stock size of
the Gulf of Riga and central Baltic herring remain puzzling,
because the environmental factors have essentially been similar.
Nevertheless, the period of warmer winters and springs has not
favoured prerecruit survival of central Baltic herring. This may
be associated with competition for food with sprat. Both stocks
have exhibited reduced recruitment variability during the
periods of low stock size, suggesting that this feature is less
linked to environmental than to density-dependent factors.
Stock reproductive potential is of course a key stock-related
factor in recruitment processes (Winters et al., 1993; Oskarsson
and Taggart, 2006), so potential changes in individual fecundity
are important. Individual fecundity is largely determined by
body weight and body condition (Zijlstra, 1973; Horwood et al.,
1989; Kraus et al., 2000, 2002; Tomkiewicz et al., 2003). The
decreasing trend in mean weight- and condition-at-age observed
for the Gulf of Riga herring over recent decades is typical of
most Baltic herring stocks (ICES, 2009a), so severe declines in
individual fecundity might have been expected. Although the
recent increase in population abundance has largely compensated
for the decline in individual fecundity, recruitment, and consequently reproduction success, has doubled (Table 2). The lack of
a relationship between reproductive potential and realized recruitment between the two periods indicates that the differences should
be sought in environmental conditions.
Although the effects of the reduced growth rate and the
decrease in condition on fecundity of the Gulf of Riga herring
are currently compensated for by enhanced recruitment, the
results raise concern about the future perspectives of the stock
should recruitment fail for a few consecutive years. If the effects
on growth and condition are density-dependent, reproductive
potential might not change severely, although this would depend
on how fast the stock could respond. However, if the effects
persist, because of a regime shift that permanently changes the
food conditions, the future of the stock might be less rosy.
Figure 6. Some key elements of the recruitment formation process (see text).
Recruitment dynamics of Gulf of Riga herring
Acknowledgements
The study was partly financed by the Estonian Ministry of
Education and Research (Grant SF0180005s10) and by the
Estonian Science Foundation (Grant 6751).
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