Fecundity regulation in relation to habitat utilisation of two sympatric flounder (Platichtys flesus) populations in the brackish water Baltic Sea

Journal of Sea Research 95 (2015) 188–195

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Fecundity regulation in relation to habitat utilisation of two sympatric flounder (Platichtys flesus) populations in the brackish water Baltic Sea Anders Nissling a,⁎, Anders Thorsen b, Filipa F.G. da Silva b,c a b c

Ar Research Station, Department of Ecology and Genetics, Uppsala University, SE-621 67 Visby, Sweden Institute of Marine Research, P.O. Box 1870, Nordnes, N-5817 Bergen, Norway National Institute for Aquatic Resources, Technical University of Denmark, Jægersborg, Allé 1, DK-2920 Charlottenlund, Denmark

a r t i c l e

i n f o

Article history: Received 11 June 2013 Received in revised form 2 June 2014 Accepted 4 June 2014 Available online 13 June 2014 Keywords: Flounder Life-history traits Fitness Capital spawner Fecundity Atresia

a b s t r a c t Two populations of flounder (Platichtys flesus) with different life history traits inhabit the brackish water Baltic Sea. Both types share feeding areas in coastal waters during summer-autumn but utilise different habitats for spawning in spring, namely offshore spawning with pelagic eggs and coastal spawning with demersal eggs respectively. Fecundity regulation by atresia was assessed as prevalence (portion of fish with atresia) and intensity (calculated as the average intensity of atresia in these fish) during the reproductive cycle following start of gonad development in the autumn up to spawning in spring, and evaluated in relation to fish condition (Fulton's condition factor reflecting energy reserves of the fish) and feeding incidence of the respective population. Peaking in winter (December–February), fecundity regulation was significantly higher for coastal spawning flounder than for flounder spawning offshore. For coastal spawners, the prevalence was 45–90% with an intensity of 6.4–9.3% vs. 0–25% and an intensity of 2.1–3.4% for offshore spawners during winter. Further, fecundity regulation ceased prior to spawning for offshore spawners but continued for coastal spawners. For coastal spawners, the prevalence was 12–29% and an intensity of 2.5–6.1% during spawning. The change in fish condition was strongly related to feeding incidence and differed between populations. As feeding ceased, condition of offshore spawners decreased during winter up to spawning, whereas condition of coastal spawners decreased during autumn but was maintained as feeding started again prior to spawning. Thus, habitat utilisation according to spawning strategy affects the timing of fecundity down-regulation reflecting availability of resources, namely limited food resources in deep areas and higher availability in coastal areas. Offshore spawning flounder display characteristics typical for a capital spawner with ceasing of feeding and oocyte down-regulation well before spawning, whereas coastal spawning flounder can be characterised as intermediate between a capital and income spawner with feeding prior to and during spawning along with continuous fecundity-regulation. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Due to the specific requirements of early life-stages, reproduction in fish is restricted spatially and temporally in accordance with local conditions, both abiotic (e.g. temperature, salinity and oxygen) and biotic (e.g. availability of suitable food items for first feeding larvae). This means that adaptations have evolved and continue to evolve in response to local conditions which results in differences in habitat utilisation and life-history traits, amongst species and amongst populations within a species. As both biotic and abiotic conditions vary (e.g. Cushing, 1990; Hjort, 1914) and influence progeny survival, several commercial marine fishes like gadoids and pleuronectoids, flounder (Platichtys flesus) included, are iteroparous batch spawners, i.e. spawning over successive seasons and shedding eggs in several batches during the spawning season (Murua and Saborido-Rey, 2003). Obviously, high egg production over ⁎ Corresponding author. E-mail address: [email protected] (A. Nissling).

http://dx.doi.org/10.1016/j.seares.2014.06.003 1385-1101/© 2014 Elsevier B.V. All rights reserved.

a long period of time increases fitness in response to varying conditions during the spawning season within a year (cf. window of progeny survival) as well as between years (often several years between strong year-classes) (e.g. Cushing, 1990; Hjort, 1914). Thus, there is a trade-off between investment in gonad production and somatic growth influencing the current versus future reproductive potential (e.g. Kjesbu and Witthames, 2007; Stearns, 2000). For species distributed over large areas with discrepancies in environmental conditions, life-history traits such as investment in egg production may vary to maximise fitness. Bagenal (1966) hypothesised, based on studies on plaice Pleuronectes platessa, that size specific fecundity varies with lower fecundity in the centre and higher fecundity towards the edges of the distribution, as a response to less favourable conditions. However, this pattern has been questioned by Rijnsdorp (1991) and Rijnsdorp and Witthames (2005) arguing that fecundity of plaice is fairly constant with the exception of the Baltic Sea, where fecundity is considerably higher (Kändler and Pirwitz, 1957) due to brackish water conditions involving selection for high fecundity (e.g. Nissling and Dahlman, 2010).

A. Nissling et al. / Journal of Sea Research 95 (2015) 188–195

Energy allocation for both somatic and gonad growth follows a seasonal cycle, normally peaking in the summer-autumn (Rijnsdorp, 1990; Rijnsdorp and Witthames, 2005). Hence, timing of reproduction, normally occurring in the spring, and feeding season are to a large extent decoupled but vary amongst species and between populations within a species in accordance with local conditions. For a typical capital spawner, reproduction is fully covered by stored energy allocated prior to the reproductive investments, whereas for an income spawner the energy is gained directly from feeding. Most fishes, however, fit somewhere in between a fully capital and a fully income spawner, i.e. may be characterised as mainly capital or mainly income spawner. Irrespective of strategy, available energy resources will determine the final number of eggs produced. In principle, all fish down-regulate the number of maturing oocytes by atresia (resorption of vitellogenic oocytes) in relation to available energy resources, even if in high condition. A number of studies, however, have shown that both prevalence (the proportion of individuals displaying atresia) and intensity (the proportion of atretic cells in individuals displaying atresia) increase with decreasing fish condition (e.g. Kennedy et al., 2008; Kurita et al., 2003), with loss of fecundity ranging from negligible to substantial or even total loss as spawning is skipped (Armstrong et al., 2001; Nash et al., 2000; Rideout et al., 2000, 2005). Thus, the realised fecundity (number of eggs shed) differs from the potential fecundity (the stock of oocytes in the pre-spawning ovary), i.e. to estimate the reproductive potential of a stock, information about both the potential fecundity and occurrence

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of atresia is required. The timing and extent of oocyte down-regulation may vary, not only amongst species but amongst populations reflecting local environmental conditions such as feeding opportunities and spawning time. For example, in East-arctic cod (Gadus morhua), considered to be mainly a capital spawner, atresia may be pronounced both during vitellogenesis prior to spawning (Thorsen et al., 2006) and during the spawning (Kjesbu et al., 1991), whereas Baltic cod and Norwegian coastal cod display low levels of atresia prior to spawning but increased prevalence during spawning (Kjesbu et al., 1991; Kraus et al., 2008). Further, differences in the duration of the down-regulating period may affect the realised fecundity amongst populations. Van Damme et al. (2009), studying North Sea herring (Clupea harengus), found significant differences in the realised fecundity between autumn- and winter spawners due to down-regulation of oocytes over a longer period for individuals spawning in the winter despite only low levels of atresia. Flounder, P. flesus, inhabit the Eastern Atlantic, in both coastal and brackish waters of Western Europe, from the White Sea to the Mediterranean and the Black Sea (FishBase, 2011) including the brackish water Baltic Sea (Fig. 1). In the Baltic Sea two genetically distinct populations (Florin and Höglund, 2008; Hemmer-Hansen et al., 2007) with different spawning strategies occur. These two populations consist of flounder spawning in the higher salinity (~10–20 psu) deep basins in ICES subdivisions (SD; Fig. 1) 24, 25, 26 and 28, which produce pelagic eggs, and flounder in the less saline (~ 6–8 psu) coastal areas and banks of ICES SD 25-30 and SD 32 which produce demersal eggs (Nissling et al.,

Fig. 1. The Baltic Sea with ICES subdivisions (SD) and position of sampling locations; offshore spawners Bornholm basin (OSBB), offshore spawners Gotland basin (OSGB) and coastal spawners eastern Gotland (CSEG; two sites).

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A. Nissling et al. / Journal of Sea Research 95 (2015) 188–195

2002; Sandman, 1906; Solemdal, 1971). Both populations share feeding areas in coastal waters during summer-autumn and may co-occur in deeper areas during winter but utilise different habitats for spawning in spring (Aro, 1989). They therefore form sympatric populations. Marine fishes inhabiting the Baltic Sea have adapted to the less saline brackish water conditions with respect to salinity requirements for fertilisation and egg development (e.g. Nissling and Westin, 1997; Nissling et al., 2002; Solemdal, 1970; Thorsen et al., 1996) and thus form specific populations. The reproductive success of these populations, however, can vary spatially and temporally. Success is governed by highly irregular saline water inflow events, influencing salinity conditions as well as oxygen conditions (Nissling et al., 2002; Segerstråle, 1969; Ustups et al., 2013). These events affect stock abundance and distribution, including for flounder (Drews, 1999; Ojaveer et al., 1985). Consequently, to cope with varying brackish water conditions that affect egg survival, selection for high egg production in the Baltic Sea can be expected. In an earlier study of flounder inhabiting the Baltic Sea, differences in reproductive investment corresponding to the respective spawning strategy were revealed. Compared to the offshore spawning population, the coastal spawners had considerably higher size-specific potential fecundity and lower somatic growth (Nissling and Dahlman, 2010). The present study focuses on differences in fecundity regulation in these populations, by assessing the prevalence and intensity of atresia during the reproductive cycle from early autumn up to the spawning in the spring. The main aim was to reveal timing and extent of atresia, and potential effects of fish condition.

2. Material and methods 2.1. Sampling In flounder, vitellogenesis begins during the feeding season in September with spawning taking place in March–May for offshore spawning flounder and in April–June for coastal spawners (Bagge, 1981; own observation). Sampling was carried out between October and April (Table 1), with sampling for offshore spawners taking place in the Hanö Bight-Bornholm basin (OSBB) in ICES SD 25 (coastal spawning flounder not present in the western part of SD 25; Molander, 1954) and coastal spawners off eastern Gotland (CSEG) in SD 28 (Fig. 1). The offshore spawning type feeds in coastal areas during summer to early-autumn but migrates to deeper areas during autumn for wintering and subsequent spawning in the deep basins (Aro, 1989; Bagge, 1981). Thus, sampling of OSBB followed depth distribution according to season; at ~ 25–30 m depth in October and at ~ 65–80 m depth in March. Similarly, sampling of CSEG followed expected depth distribution; shallow waters during spring at 2–10 m depth, and somewhat deeper during winter, at 3–20 m depth. The coastal spawning type is known to not occur deeper than ~ 40 m depth during winter (Molander, 1954), although recent findings show that coastal spawners may occur deeper off Gotland in SD 28 (own observation). To reveal potential inter-area differences as well as discrepancies between years, additional sampling was conducted in 2012. Offshore spawners were sampled in the Gotland basin (OSGB) in SD 28 and coastal spawners in SD 28 during the winter in January–February and during

Table 1 Sampling locations, depth range and date of catches of coastal- (CSEG) and offshore spawning (OSBB and OSGB) flounder P. flesus in the present study. Number of fish screened (Ns) for occurrence of atresia and number of fish in total (Nt; also stomach content and Fulton's condition factor assessed). Sampling location

Acronym

ICES SD

Positions

Depth (m)

Date

Ns

Nt

Bornholm Basin

OSBB

25

N 55 24 E 14 18 N 55 40 E 14 43 N 55 21 E 14 55 N 55 20 E 14 56 N 57 20 E 19 07 N 57 35 E 19 22 N 57 35 E 19 21 N 57 20 E 19 07 N 57 14 E 18 40 N 57 14 E 18 40 N 57 35 E 18 49 N 57 35 E 18 48 N 57 35 E 18 48 N 57 35 E 18 48 N 57 27 E 18 53 N 57 26 E 18 54 N 57 33 E 18 50 N 57 26 E 18 55

~25–28

October 9, 2010

19

45

~35–40

December 6, 2011

20

36

~64–71

February 2, 2011

17

37

~67–81

March 14, 2011

20

42

~78–80

January 31, 2012

18

18

~79–80

February 7, 2012

~79–80

April 16, 2012

20

33

~79–80

April 19, 2012

~1–6

October 4, 2010

20

26

~3–6

December 7, 2010

20

28

~5–20

February 7, 2011

18

18

~2–4

March 21, 2011

20

30

~2–4

April 15, 2011

20

26

~2–4

May 5, 2011

17

17

~3–10

January 31, 2012

11

11

~3–10

February 7, 2012

~3–10

April 16, 2012

18

58

~3–10

April 19, 2012

Gotland Basin

Eastern Gotland

OSGB

CSEG

28

28

A. Nissling et al. / Journal of Sea Research 95 (2015) 188–195

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spawning in April. Fish were sampled using gill-nets as well as from the commercial trawl-fishery (deepest locations in SD 25). Positions of sampling sites, dates of sampling and depth range are given in Table 1 together with the number of fish analysed (for occurrence of atresia and in total).

considered as the largest present in the ovary. Only oocytes that were cut centrally with a visible nucleus were used.

2.2. Measurements

3.1. Timing of fecundity regulation

Fish for analyses were selected to cover the size distribution in catches. Total length (± 1 mm; Lt), somatic weight [± 1 g (intestine and gonad removed); Ws] and the average weight of otoliths (±0.0001 g; Otw) were measured. Fish condition (Cf) was calculated as Fulton's condition factor [(Ws/Lt3) * 100], reflecting energy reserves (e.g. Bromley, 1980; Costopoulos and Fonds, 1989; Lambert and Dutil, 1997). The Fulton's condition factor was considered representative for flounder in the Baltic Sea as the exponent in the length-weight relationship is estimated to 2.96 for female Baltic flounder (FishBase, 2011). Age was assessed from the relationship between age determined by otolith readings, using the stain and slice method (ICES, 2008), and average otolith weight (data from Nissling and Dahlman, 2010). The relationships used were: Otw = 2.525 × age + 7.792 (r2 = 0.778) for coastal spawners (CSEG) and Otw = 2.681 × age + 8.414 (r2 = 0.751) for offshore spawning flounder in SD 25 (OSBB). Individuals were then assigned an age class according to otolith weight of class midpoint ± 0.5 yr. For offshore spawners in SD 28 (OSGB) age was determined by otolith readings (ICES, 2008). Feeding incidence according to ecotype and sampling occasion was assessed by examination of stomach contents including intestines and calculated as the proportion of individuals with food items present. A gonad sub-sample (~0.1–0.2 g wet weight) was fixed in 3.6% phosphate buffered formaldehyde for assessment of atresia. In total 160, 214 and 51 fish were sampled from OSBB, CSEG and OSGB respectively, of these 76, 144 and 38 individuals respectively were screened for occurrence of atresia (Table 1). Data on Lt, Ws, Cf and Otw, are given as supplementary data (Appendix A).

Oocyte down-regulation by atresia began soon after the beginning of ovary development in October, peaked in December to February and decreased until spawning (Fig. 2). This was true with respect to both prevalence (Fig. 2a) and intensity (Fig. 2b) of atresia and irrespective of population. Prevalence and intensity of atresia were considerably higher for coastal spawning flounder than for the offshore spawning type; 45–90% prevalence with an intensity of 6.4–9.3% for coastal spawners, compared to 0–25% with an intensity of 2.1–3.4% for offshore spawners during the winter. Moreover, for offshore spawners, occurrence of atresia ceased in February, whereas atresia in coastal spawning flounder remained with a prevalence of 12–29% and an intensity of 2.5– 6.1% up to spawning, i.e. significantly higher occurrence of atresia at all sampling occasions (prevalence; df = 1, χ 2 = 17.29, p b 0.001 in December, χ2 = 15.15, p b 0.001 in February and χ2 = 3.67, p = 0.055 in March) except for early in the reproductive cycle in October (df = 1, χ2 = 0.12, p = 0.732). The pattern was the same irrespective of sampling year and sampling area (Fig. 2), i.e. the observed differences were population specific. The rate of oocyte growth was highest between October and December when oocytes increased from 220 to 400 μm. Oocyte growth then ceased, at the “germinal vesicle migration stage” (oocyte diameter 400–600 μm; Janssen et al., 1995) until the final maturation prior to ovulation and spawning in March–May (Fig 3). Atresia levels increased along with oocyte

3. Results

a)

CSEG1

100

OSBB

CSEG2

OSGB

90

2.3. Assessment of atresia Prevalence (%)

80 70 60 50 40 30 20 10 0

October

b)

December Jan/Feb

CSEG1

10

February

OSBB

March

CSEG2

April

May

OSGB

9 8

Intensity (%)

The fixed ovary samples were embedded in resin (Technovit, Kulzer), sectioned with a thickness of 4 μm, and stained with 2% toluidine blue and 1 % sodium tetraborate. Depending of the density of vitellogenic oocytes present, slides of 5–15 non overlapping photographs (QImaging 5 Mpx Micropublisher camera, resolution 0.846 px/μm) at 4 × magnification (Nikon Eclipse 80 i) were taken from each of the histological slides. The photographs were then screened for presence of atresia. Samples containing atresia were further analysed by profile counting (Kjesbu et al., 2010) using two categories of vitellogenic oocytes; normal and alpha atretic (Hunter and Macewicz, 1985; Witthames et al., 2003). Thereafter, the intensity of atresia, i.e. the percentage of atretic oocytes, was calculated. At least 150 vitellogenic oocytes were scored for each fish. Since atretic oocytes tend to be smaller than normal cells they will be underrepresented in profile counts (Kjesbu et al., 2010; Witthames and Greer Walker, 1995). To adjust for this bias the relationship between the profile and the more laborious dissector method (which is considered unbiased with respect to size and shape (Thorsen et al., 2006) presented in Kjesbu et al. (2010); Fig. 6) was used to correct the profile counting. The relationship obtained between the methods is shown as supplementary data (Appendix B). Flounder represents a group-synchronous determinate spawner, i.e. displays one stage of vitellogenic oocytes that mature towards the start of spawning (Janssen et al., 1995). The largest vitellogenic oocytes present in the ovary, the leading cohort (LC), increases in size towards the start of spawning and therefore provides a good measure of oocyte maturity (Kjesbu, 1994). Thus, the occurrence of atresia in relation to oocyte maturation was evaluated according to LC diameter. The LC diameter was estimated from the histological slides as the mean diameter of 5 oocytes that visually were

7 6 5 4 3 2 1 0

October

December

Jan/Feb

February

March

April

May

Fig. 2. a) Prevalence (portion of fish with atresia), and b) intensity (calculated as the on average intensity of fish displaying atresia), of offshore- (OSBB and OSGB) and coastal(CSEG; two sites) spawning flounder (P. flesus) during the reproductive cycle following gonad formation up to spawning.

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A. Nissling et al. / Journal of Sea Research 95 (2015) 188–195 CSEG1

OSBB

CSEG2

CSEG2 sp

OSGB sp

700 650

Diameter (µm)

600 550 500 450 400 350 300 250 200

Fig. 3. Diameter (μm) of oocyte leading cohort, with 95% confidence intervals, during the reproductive cycle following gonad formation up to spawning of offshore- (OSBB and OSGB) and coastal- (CSEG; two sites) spawning flounder (P. flesus) displaying atresia; sp refer to spawning fish.

growth from October to December and decreased after the oocytes had reached ~450 μm in diameter (during the “germinal vesicle migration stage”). 3.2. Atresia in relation to fish age and condition Comparison of condition, assessed as Fulton's condition factor (Cf), for coastal spawners (the ecotype which showed the highest atresia levels) indicated a discrepancy in Cf for fish with and without atresia (Fig. 4a). In December, when atresia was most pronounced, fish

a)

CSEG1 NA

CSEG1 A

CSEG2 NA

CSEG2 A

Fulton´s condition factor

1.3 1.2 1.1

3.3. Feeding habits and condition

1 0.9 0.8 0.7

b)

October December Jan/Feb

OSBB NA

February

OSBB A

March

OSGB NA

April

May

Table 2 On average (±standard deviation) condition (Fulton's condition factor) of different ageclasses of coastal- (CSEG) and offshore spawning (OSBB) flounder P. flesus at different sampling occasions during the reproductive cycle in 2010–2011.

1.2 1.1

CSEG

1 0.9 0.8 0.7

Fish condition (Cf) was higher for offshore spawning fish sampled in SD 25 (OSBB) compared to fish sampled in SD 28, irrespective of spawning strategy (OSGB and CSEG), indicating that fish condition is related to local conditions rather than to spawning strategy (Fig. 5a). For offshore spawning fish at OSBB in 2010–2011 Cf was high (1.146– 1.150) during October-December but then decreased considerably up to spawning (0.904). For coastal spawners (CSEG in 2010–2011) on the other hand Cf had decreased already during autumn from October

OSGB A

1.3

Fulton´s condition factor

displaying atresia were in poorer condition (df = 18, t = 2.62, p = 0.017; t-test). Also, in October and March Cf was on average lower for fish displaying atresia but the difference was not significant, p = 0.068 and p = 0.072, for October and March respectively. For offshore spawners, with low occurrence of atresia, no difference in Cf was detected during the period when atresia was most pronounced, p = 0.328 and p = 0.247, in October and December, respectively (Fig. 4b). The limited number of sampled fish does not allow for analysis of occurrence of atresia in relation to age at each of the respective sampling occasions. However, pooling (i.e. disregarding sampling occasion) of individuals into age classes (≥ 10 individuals per class) for coastal spawners covering the reproductive cycle in 2010–2011 suggests somewhat lower prevalence of atresia, 20–25%, in younger fish, age 3–6 yr corresponding to age at maturity (50% maturation at 3–4 yr and 100% at 6 yr for flounder off Gotland SD 28, with age determined by otolith readings according to ICES, 2008; Nissling and Florin, unpublished), compared to 31–58% (on average 47.3%) in older (7–21 years) fish. A RxC-table test showed, however, no significant differences between age groups, df = 7, χ2 = 8.407, p = 0.298, but comparing 3–6 yr old fish vs. 7–21 yr resulted in a significant difference, df = 1, χ2 = 5.590, p = 0.018. The higher prevalence of atresia in older fish was associated with significantly lower Cf, df = 1, F = 12.53, p = 0.001 (two-way ANOVA with age and sampling occasion as fixed factors; no interaction between age-group and occasion, p = 0.725) in older compared to younger fish (Table 2). A corresponding analysis of OSBB offshore spawners yielded no difference in Cf between age-groups (df = 1, F = 1.93, p = 0.169; no interaction between age-group and occasion, p = 0.292), and accordingly, similar levels of atresia, 9.1% for 3–6 yr old fish and 11.3% for 7–20 yr (df = 1, χ2 = 0.081, p = 0.776). For OSGB fish sampled in January–February a similar comparison suggested a higher prevalence of atresia in older fish 33.3% vs 0% in younger. The difference was however, not significant (p = 0.098; Fisher's exact test. N.B. n = 18) and the Cf was similar in the respective age group (df = 16, t =1.063, p = 0.303; t-test).

Sampling occasion

Age 3–6 yr

Age 7–21 yr

October December February March–April

1.113 0.970 0.889 0.866

1.030 0.885 0.846 0.822

± ± ± ±

0.089 0.088 0.054 0.077

± ± ± ±

0.161 0.077 0.049 0.058

OSBB October December Jan/Feb

February

March

April

May

Fig. 4. Condition (Fulton's condition factor), with 95% confidence intervals, of fish displaying (A) and not displaying (NA) atresia, of a) coastal- (CSEG; two sites) and b) offshore- (OSBB and OSGB) spawning flounder (P. flesus) during the reproductive cycle following gonad formation up to spawning.

Sampling occasion

Age 3–6 yr

Age 7–20 yr

October December February March

1.171 1.185 1.007 0.835

1.127 1.110 0.961 0.879

± ± ± ±

0.058 0.127 0.101 0.108

± ± ± ±

0.077 0.096 0.047 0.078

A. Nissling et al. / Journal of Sea Research 95 (2015) 188–195

a)

CSEG1

OSBB

CSEG2

OSGB

Fulton´s condition factor

1.3 1.2 1.1 1.0 0.9 0.8 0.7 0.6 October December Jan/Feb

b)

CSEG1

February

OSBB

March

CSEG2

April

May

OSGB

100

Feeding incidence (%)

90 80 70 60 50 40 30 20 10 0 October December Jan/Feb

February

March

April

May

Fig. 5. a) Condition (Fulton's condition factor) with 95% confidence intervals, and b) feeding incidence, of offshore- (OSBB and OSGB) and coastal- (CSEG; two sites) spawning flounder (P. flesus) during the reproductive cycle following gonad formation up to spawning.

(1.018) to December (0.913), but then levelled off and remained unchanged (on average 0.835) from February and onwards up to spawning in April–May. Feeding incidence differed between the populations (Fig. 5b) with the offshore spawning type feeding up to early winter (100% feeding incidence in October and December) but then ceased feeding up to spawning influencing the Cf. In contrast, coastal spawning flounder stop feeding during the autumn (feeding incidence 0% from October until February), but start to feed in the spring prior to spawning (feeding incidence, 21–91% in March-May), i.e. coinciding with decreasing condition in late autumn but maintained Cf during the spring up to spawning. 4. Discussion The annual total egg production of a population represents the reproductive potential affecting stock recruitment. Size specific fecundity varies amongst populations due to adaptations to local environmental conditions, both abiotic (e.g. salinity and temperature; Nissling and Dahlman, 2010; Thorsen et al., 2010) and biotic (food availability and population density; Nash et al., 2000; Kennedy et al., 2007), and temporally with fish size/age and condition, i.e. with the stock structure within a population (e.g. Marshall, 2009; Marshall et al., 2006), and accordingly varies between years (e.g. Kennedy et al., 2007; Kjesbu et al., 1998; Ndjaula et al., 2010). Fecundity is commonly assessed as the potential fecundity, although the realised fecundity, i.e. the number of eggs spawned, may differ considerably as the final number of eggs produced is a function of both the number of previtellogenic oocytes produced early in the maturation cycle and down-regulation of developing oocytes during the maturation process (Kennedy et al., 2007, 2008; Kurita et al., 2003). Inter-annual differences in the extent of fecundity

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regulation within a population, as well as discrepancies in timing of down-regulation between populations, may bias assessment of the reproductive potential and hamper both intra- and inter-population comparisons. In principle, all fish down-regulate oocytes by atresia, irrespective of condition. It may thus be difficult to establish a clear relationship between levels of atresia and fish condition, although the extent of down-regulation is related to available energy resources. For example, Skjæraasen et al. (2009) and Kurita et al. (2003), studying Northeast Arctic cod and Atlantic herring, respectively, found no relationship between the relative intensity of atresia and fish condition. However, Kennedy et al. (2008) showed that total atresia was correlated to the decrease in condition over time for plaice, and Kennedy et al. (2011) found for Atlantic herring that individuals with condition below a certain threshold value had a higher intensity of atresia compared to fish in higher condition. The findings of Kennedy et al. suggest that it is more likely to find atresia in fish in poorer condition. In accordance with this, coastal spawning flounder (the ecotype with the highest prevalence and intensity of atresia) displaying atresia appeared to, on average, be in poorer condition compared to those with no atretic oocytes present. This was evident in early winter, during the period when Cf decreased (Fig. 5a) and atresia levels were most pronounced (Fig. 4a), and was supported by the observed discrepancy in fish condition between young recruit-spawners and older fish (Table 2). The condition of sampled fish differed between sampling areas, being considerably higher for fish in ICES SD 25 (the Hanö Bight) than in SD 28 (off Gotland), irrespective of spawning strategy. This may reflect either stock abundance or quantity and quality of food items (or both), influencing availability of energy resources for the individual fish. Adult flounder feed upon a variety of faunal groups including bivalves, polychaetes, crustaceans, and small fishes (e.g. Summers, 1980; Westberg, 1997). In the Baltic Sea area, i.e. the area of the study, adult flounder consume mostly bivalves (Bonsdorff et al., 1995; Westberg, 1997; own observation), primarily the very abundant blue mussel, Mytilus edulis (L.), or Mytilus trossulus (Gould) according to later taxonomy. According to an ongoing study monitoring the condition of Mytilus spp. in the Baltic Sea (Kjell Larsson, Linné University, Sweden), weight/length relationship (quality) is at present (2010– 2011) somewhat lower in SD 25 (the Hanö Bight) compared to in SD 28 (off Gotland). Available CPUE-data (ICES, 2012) suggest considerably higher stock abundance of flounder in SD 28 compared to in SD 24–25 (~1100 no/h vs. ~ 200 no/h). Thus, high competition rather than poor quality of food might be the cause of differing condition of flounder in the respective area. Irrespective of area, however, changes in condition during the reproductive cycle differed between fish according to spawning strategy. Depending on habitat utilisation, feeding habits differ between the ecotypes (Fig. 5) in accordance with availability of preferred food items, Mytilus spp., being most abundant in the depth interval 3–12 m (Vourinen et al., 2002; Westerbom et al., 2002; ICES SD 29) or down to 20 m depth (see Wolowicz et al., 2006; ICES SD 26) although it may, depending on substrate, occur deeper. Feeding habits of offshore spawning flounder are in accordance with a typical capital spawner; feeding up to early winter but then ceasing feeding when migrating to deeper areas in the winter for subsequent spawning, i.e. to areas with limited food resources compared to the more productive coastal area (see Lassig and Leppäkoski, 1981). Coastal spawning flounder on the other hand, cease feeding already in the autumn, when migrating to deeper water, but start feeding again when migrating back to coastal areas for spawning (Aro, 1989; Molander, 1954), i.e. displaying less typical capital spawner characteristics. As typical for a determinate capital spawner (Kennedy et al., 2007; Kurita et al., 2003; Thorsen et al., 2006) onset of down-regulation by atresia in flounder occurred early in the reproductive cycle and was most pronounced whilst oocytes were still growing, i.e. the strategy is to abort primarily less developed oocytes to minimise energetic costs (Witthames and Greer-Walker, 1995). Nevertheless, in coastal spawning

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flounder abortion also of more developed (~450 μm in diameter) oocytes occurred, although at lower levels, despite that this involves both incorporation of yolk-material and then a subsequent breakdown. Evidently, habitat utilisation influencing feeding habits affects the timing of fecundity down-regulation, reflecting predictability of energy resources. For offshore spawning flounder, food availability is low following the migration to deep areas in autumn-early winter whereas for coastal spawning flounder feeding conditions are higher but probably also less predictable. The unpredictability may be caused by variability in temperature which again may influence quality of the main food item Mytilus spp. (Bayne and Widdows, 1978; Waldeck and Larsson, 2013) as well as food conversion (e.g. Brett, 1979). Thus, for offshore spawning flounder oocyte abortion occurs early in the reproductive cycle as typical for capital spawners (Kennedy et al., 2007; Kurita et al., 2003; Thorsen et al., 2006), whereas coastal spawning flounder display prolonged oocyte down-regulation up to spawning, in accordance with food resources. That is, if conditions (food and temperature) are favourable it can sustain a high fecundity. Furthermore, the extent of atresia differed also between populations; both higher prevalence and intensity occurred in coastal spawning flounder. This probably reflects egg survival probabilities of the respective spawning strategies, particularly with a selection for high fecundity for coastal spawning flounder. Although not yet fully elucidated, both fertilisation rates and egg survival can be expected to be lower for coastal spawning flounder due to the lower salinity conditions (Molander, 1954; Nissling et al., 2002; Solemdal, 1970). Coastal spawning flounder spawns at a salinity of 5–7 psu as opposed to 10–20 psu for the offshore spawning population. Furthermore, production of demersal eggs probably involves a higher mortality rate due to predation, infestation by bacteria etc. Accordingly, size specific potential fecundity is significantly higher for coastal spawning flounder that spawn demersal eggs, whereas offshore spawners with pelagic eggs, i.e. the same spawning strategy as flounderpopulations outside the Baltic Sea, display fecundities similar to populations in the Atlantic-North Sea area (Nissling and Dahlman, 2010). Thus, despite lower prevalence and intensity of atresia the offshore spawning type is less fecund, whereas coastal spawners, which have higher levels of atresia, still show higher specific potential fecundity. Hence, in order to maximise egg production, high initial oocyte production of coastal spawning flounder is down-regulated according to prevailing conditions in the particular year. High fecundity initially suggests that energy at least in some years may be available to cover maturation of the vast majority of developing oocytes resulting in a high realised fecundity. Evidently, the production of a high number of oocytes initially surpasses the risk of wasting energy by down-regulation of developed oocytes during the course of spawning in years when conditions are less favourable. When considering sustainable exploitation of fish stocks, attention is given to conservation of genetic diversity that enhances resilience of stocks to variable environmental conditions, including climate changes (e.g. Möllmann et al., 2009). We consider that population specific characteristics such as habitat utilisation of different life-stages (e.g. connectivity and natal homing; Secor et al., 2009; Svedäng et al., 2007, 2010) and reproductive potential (reproductive timing and size specific fecundity; Kjesbu, 2009; Marshall, 2009; Lowerre-Barbieri et al., 2011) may be important in this context. In the Baltic Sea opportunities for reproduction of flounder vary according to prevailing salinity and oxygen conditions, both spatially due to decreasing salinities from the south towards the north, and temporally due to irregularly occurring inflow events (Nissling et al., 2002; Ustups et al., 2013). Accordingly, information about the annual egg production in different areas is a prerequisite for understanding stock development mechanisms, and thus for setting appropriate management measures. Hence, to assess the spatial and temporal variability in the reproductive potential of each stock both the potential fecundity (Nissling and Dahlman, 2010) and oocyte down-regulation by atresia (present study) need to be considered. An implication of the discrepancy in timing of fecundity regulation between the populations is that the reproductive potential may be

accurately determined for offshore spawning flounder if estimated shortly prior to spawning whereas for coastal spawning flounder accurate estimates require additional assessment of atresia up to spawning. Further, given that vitellogenic oocytes are recruited in September according to body size (Kennedy et al., 2008) and that offshore spawners are subjected to oocyte down-regulation over a shorter period, and with lower prevalence and intensity of atresia compared to coastal spawners, the present study suggests that the variability in size specific fecundity may be lower for offshore spawning flounder than for coastal spawning flounder, reflecting differences in habitat utilisation. 5. Conclusions The present study has shown that respective spawning strategy of two sympatric flounder populations inhabiting the Baltic Sea involves differences in the potential fecundity (Nissling and Dahlman, 2010) and fecundity-regulation. These differences probably reflect egg survival probabilities and food availability related to habitat utilisation for spawning and feeding respectively. The present study reveals discrepancies in strategy of reproductive investment according to spawning strategy. Offshore spawning flounder represent a typical capital spawner for which feeding ceases and oocyte down-regulation occurs well before spawning. By contrast, coastal spawning flounder can be characterised as intermediate between a capital and income spawner, with feeding prior to and during spawning along with continuous fecundity-regulation up to spawning. The present study thus suggests that accurate inter-population comparisons of fecundity may be biased unless discrepancies in timing and extent of oocyte down-regulation are considered. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.seares.2014.06.003. Acknowledgements Many thanks to Bente Njøs Strand for analysis of samples and to Manuela de Gouveia, Rebecca Retz and Annette Asp for assistance during sampling. The investigation was financially supported by the WWF, the European Fisheries Fund (EFF) and the County Administrative Board Gotland. References Armstrong, M.J., Conolly, P., Nash, R.D.M., 2001. An application of the annual egg production method to estimate the spawning biomass of cod (Gadus morhua L.), plaice (Pleuronectes platessa L.) and sole (Solea solea L.) in the Irish Sea. ICES J. Mar. Sci. 58, 183–203. Aro, E., 1989. A review of fish migration patterns in the Baltic. Rapports et Procés-Verbaux des Réunions du Conseil International pour l'Exploration de, la Mer, 190, pp. 72–96. Bagenal, T.B., 1966. The ecological and geographical aspects of the fecundity of plaice. J. Mar. Biol. Assoc. U. K. 46, 161–186. Bagge, O., 1981. In: Voipio, A. (Ed.), Demersal fishes. The Baltic Sea. Elsevier Oceanographic Series No. 30. Elsevier Scientific Company, Amsterdam, pp. 320–323. Bayne, B.L., Widdows, J., 1978. The physiological ecology of two populations of Mytilus edulis L. Oecologia 37, 137–162. Bonsdorff, E., Norkko, A., Boström, C., 1995. Recruitment and population maintenance of the bivalve Macoma balthica (L.)—factors affecting settling success and early survival on shallow sandy bottoms. In: Eleftheriou, A., Ansell, A.D., Smith, C.J. (Eds.), Biology and ecology of shallow coastal waters. Proceedings of the 28th EMBS Symposium. Olsen & Olsen, Fredensborg, pp. 253–260. Brett, J.R., 1979. Environmental factors and growth. In: Hoar, W.S., Randall, D.J., Brett, J.R. (Eds.), Fish Physiology vol. VIII: Bioenergetics and Growth. Academic Press, NY, pp. 599–675. Bromley, P.J., 1980. Effects of dietary protein, lipid and energy content on the growth of turbot (Scophthalmus maximus L.). Aquaculture 19, 359–369. Costopoulos, C.G., Fonds, M., 1989. Proximate body condition and energy content of plaice (Pleuronectes platessa) in relation to condition factor. Neth. J. Sea Res. 24, 45–55. Cushing, D.H., 1990. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv. Mar. Biol. 26, 249–294. Drews, T., 1999. Population dynamics of flounder (Platichthys flesus) in Estonian waters. Proc. Est. Acad. Sci. Biol. Ecol. 48, 310–320. Florin, A.-B., Höglund, J., 2008. Population structure of flounder (Platichthys flesus) in the Baltic Sea: differences among demersal and pelagic spawners. Heredity 101, 27–38.

A. Nissling et al. / Journal of Sea Research 95 (2015) 188–195 Hemmer-Hansen, J., Nielsen, E.E., Grønkjær, P., Loeschcke, V., 2007. Evolutionary mechanisms shaping the genetic population structure of marine fishes; lessons from European flounder (Platichthys flesus L.). Mol. Ecol. 16, 3104–3118. Hjort, J., 1914. Fluctuations in the great fisheries of northern Europe reviewed in the light of biological research. Rapp. P.-v. Réun. Cons. Int. Explor. Mer., 20, pp. 1–228. Hunter, J.R., Macewicz, B.J., 1985. Rates of atresia in the ovary of captive and wild Northern Anchovy, Engraulis-Mordax. Fish. Bull. Fish B-Noaa 83, 119–136. ICES, 2008. Report of the he 2nd Workshop on Age Reading of Flounder (WKARFLO), 26-29 May 2008. Rostock, Germany: ICES CM 2008/ACOM , 38, (53 pp.). ICES, 2012. Report of the Baltic Fisheries Assessment Working Group 2012 (WGBFAS), 12-19 April 2012, Copenhagen, Denmark. ICES CM 2012/ACOM , 10, pp. 251–272. Janssen, P.A.H., Lambert, J.G.D., Goos, H.J.Th., 1995. The annual ovarian cycle and the influence of pollution on vitellogenesis in the flounder, Pleuronectes flesus. J. Fish Biol. 47, 509–523. Kändler, R., Pirwitz, W., 1957. Über die Fruchtbarkeit der Plattfische im Nordsee-Ostsee Raum. Kiel. Meeresforsch. 13 (1), 11–34 (in German). Kennedy, J., Nash, R.D.M., Slotte, A., Kjesbu, O.S., 2011. The role of fecundity regulation and abortive maturation in the reproductive strategy of Norwegian spring-spawning herring (Clupea harengus). Mar. Biol. 158, 1287–1299. Kennedy, J., Witthames, P.R., Nash, R.D.M., 2007. The concept of fecundity regulation in plaice Pleuronectes platessa L. Can. J. Fish. Aquat. Sci. 64, 587–601. Kennedy, J., Witthames, P.R., Nash, R.D.M., Fox, C.J., 2008. Is fecundity in plaice (Pleuronectes platessa L.) down-regulated in response to reduced food intake during autumn? J. Fish Biol. 72, 78–92. Kjesbu, O.S., 1994. Time of start of spawning in Atlantic cod (Gadus morhua) females in relation to vitellogenic oocyte diameter, temperature, fish length and condition. J. Fish Biol. 45, 719–735. 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.), Fish Reproductive Biology: implications foe assessment and management. Wiley-Blackwell, Oxford, UK, pp. 293–332. Kjesbu, O.S., Witthames, P.R., 2007. Evolutionary pressure on reproductive strategies in flatfish and groundfish: relevant concepts and methodological advancements. J. Sea Res. 58, 23–34. Kjesbu, O.S., Klungsøyr, J., Kryvi, H., Witthames, P.R., Walker, M.G., 1991. Fecundity, atresia, and egg size of captive Atlantic cod (Gadus morhua) in relation to proximate body-composition. Can. J. Fish. Aquat. Sci. 48, 2333–2343. Kjesbu, O.S., Witthames, P.R., Solemdal, P., Greer Walker, M., 1998. Temporal variation 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., Fonn, M., Gonzáles, B.D., Nilsen, T., 2010. Stereological calibration of the profile method to quickly estimate atresia levels in fish. Fish. Res. 104, 8–18. Kraus, G., Tomkiewicz, J., Diekmann, R., Köster, F.W., 2008. Seasonal prevalence and intensity of follicular atresia in Baltic cod Gadus morhua callarias L. J. Fish Biol. 72, 831–847. Kurita, Y., Meier, S., Kjesbu, O.S., 2003. Oocyte growth and fecundity regulation by atresia of Atlantic herring (Clupea harengus) in relation to body condition throughout the maturation cycle. J. Sea Res. 49, 203–219. Lambert, T., Dutil, J.-D., 1997. Can simple condition indices be used to monitor and quantify seasonal changes in the energy reserves of Atlantic cod (Gadus morhua)? Can. J. Fish. Aquat. Sci. 54, 104–112. Lassig, J., Leppäkoski, E., 1981. Benthic fauna of the Baltic Sea. In: Voipio, A. (Ed.), The Baltic Sea. Elsevier Oceanographic Series No. 30. Elsevier Scientific Company, Amsterdam, pp. 254–274. Lowerre-Barbieri, S.K., Ganias, K., Saborido-Rey, F., Murua, H., Hunter, J.R., 2011. Reproductive timing in marine fishes: variability, temporal scales, and methods. Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science, 3, pp. 71–81. Marshall, C.T., 2009. Implementing information on stock reproductive potential in fisheries management: the motivation, challenges and opportunities. In: Jakobsen, T., Fogarty, M.J., Megrey, B.A., Moksness, E. (Eds.), Fish Reproductive Biology: implications foe assessment and management. Wiley-Blackwell, Oxford, UK, pp. 395–420. Marshall, C.T., Needle, C.L., Thorsen, A., Kjesbu, O.S., Yaragina, N.A., 2006. Systematic bias in estimates of reproductive potential of an Atlantic cod (Gadus morhua) stock: implications for stock-recruit theory and management. Can. J. Fish. Aquat. Sci. 63, 980–994. Molander, A.R., 1954. Skrubbskäddan, Pleuronectes flesus (L.). In: Andersson, K.A. (Ed.), Fiskar och fiske i Norden. Natur och Kultur, Stockholm, pp. 135–140 (in Swedish). Möllmann, C., Diekmann, R., Müller-Karulis, B., Kornilovs, G., Plikshs, M., Axe, P., 2009. Reorganization of a large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea. Glob. Chang. Biol. 15, 1377–1393. Murua, K., Saborido-Rey, F., 2003. Female reproductive strategies of marine fish species of the North Atlantic. J. Northwest Atl. Fish. Sci. 33, 23–31. Nash, R.D.M., Witthames, P.R., Pawson, M., Alesworth, E., 2000. Regional variability in the dynamics of reproduction and growth of Irish Sea plaice, Pleuronectes platessa L. J. Sea Res. 44, 55–64. Ndjaula, H.O.N., Nash, R.D.M., Slotte, A., Johannessen, A., Kjesbu, O.S., 2010. Long-term changes in the total egg production of Norwegian spring-spawning herring Clupea harengus (L.)—implications of variations in population structure and condition factor. Fish. Res. 104, 19–26. Nissling, A., Dahlman, G., 2010. Fecundity of flounder, Pleuronectes flesus, in the Baltic Sea —reproductive strategies in two sympatric populations. J. Sea Res. 64, 190–198. Nissling, A., Westin, L., 1997. Salinity requirements for successful spawning of Baltic and Belt Sea cod and the potential for cod stock interactions in the Baltic Sea. Mar. Ecol. Prog. Ser. 152, 261–271.

195

Nissling, A., Westin, L., Hjerne, O., 2002. Spawning success in relation to salinity of three flatfish species, Dab (Pleuronectes limanda), Plaice (Pleuronectes platessa) and Flounder (Pleuronectes flesus), in the brackish water Baltic Sea. ICES J. Mar. Sci. 59, 93–108. Ojaveer, E., Kaleis, M., Aps, R., Lablaika, I., Vitins, M., 1985. The impact of recent environmental changes on the main commercial fish stocks in the Gulf of Finland. Finn. Fish. Res. 6, 1–14. Rideout, R.M., Burton, M.P.M., Rose, G.A., 2000. Observations on mass atresia and skipped spawning in northern Atlantic cod, from Smith, Newfoundland. J. Fish Biol. 57, 1429–1440. Rideout, R.M., Rose, G.A., Burton, M.P.M., 2005. Skipped spawning in female iteroparous fishes. Fish Fish. 6, 50–72. Rijnsdorp, A.D., 1990. The mechanism of energy allocation over reproduction and somatic growth in female North Sea plaice, Pleuronectes platessa L. Neth. J. Sea Res. 25, 279–290. Rijnsdorp, A.D., 1991. Changes in fecundity of female North Sea plaice (Pleuronectes platessa L.) between three periods since 1900. ICES J. Mar. Sci. 48, 253–280. Rijnsdorp, A.D., Witthames, P.R., 2005. Ecology of reproduction. In: Gibson, R.N. (Ed.), Flatfishes Biology and Exploitation. Fish and Aquatic Resources Series no. 9. Blackwell Science, Oxford UK, pp. 68–93. Sandman, J.A., 1906. Kurzer Bericht über in Finnland ausgefürte Untersuschungen über den Flunder, den Steinbutt und den Kabeljau. Rapp. P.-v. Réun. Cons. Int. Explor. Mer., 5, pp. 37–44 (in German). Secor, D.H., Kerr, L.A., Cadrin, S.X., 2009. Connectivity effects on productivity, stability, and persistence in a herring metapopulation model. ICES J. Mar. Sci. 66, 1726–1732. Segerstråle, S.G., 1969. Biological fluctuations in the Baltic Sea. In: Sears, M. (Ed.), Progress in Oceanography vol 5. Pergamon Press, Oxford & New York, pp. 169–184. Skjæraasen, J.E., Kennedy, J., Thorsen, A., Fonn, M., Njøs Strand, B., Mayer, I., Kjesbu, O.S., 2009. Mechanisms regulating oocyte recruitment and skipped spawning in Northeast Arctic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 66, 1582–1596. Solemdal, P., 1970. The reproductive adaptation of marine teleosts to water of low salinity. ICES CM 1970/F:30 ,. Solemdal, P., 1971. Prespawning flounders transferred to different salinities and the effects on their eggs. Vie et Milieu (suppl.) 22, 409–423. Stearns, S.C., 2000. Life history evolution: success, limitation, and prospects. Naturwissenschaften 87, 476–486. Summers, R.W., 1980. The diet and feeding behaviour of the flounder Platichthys flesus (L.) in the Ythan estuary, Aberdeenshire, Scotland. Estuar. Coast. Shelf Sci. 11, 217–232. Svedäng, H., Righton, D., Jonsson, P., 2007. Migratory behavior of Atlantic cod Gadus morhua: natal homing is the prime stock-separating mechanism. Mar. Ecol. Prog. Ser. 345, 1–12. Svedäng, H., André, C., Jonsson, P., Elfman, M., Limburg, K.E., 2010. Migratory behavior and otolith chemistry suggest fine-scale sub-population structure within a genetically homogenous Atlantic cod population. Environ. Biol. Fish 89, 383–397. Thorsen, A., Kjesbu, O.S., Fyhn, H.J., Solemdal, P., 1996. Physiological mechanisms of buoyancy in eggs from brackish water cod. J. Fish Biol. 48, 457–477. Thorsen, A., Marshall, C.T., Kjesbu, O.S., 2006. Comparison of various potential fecundity models for north-east Arctic cod Gadus morhua L., using oocyte diameter as a standardising factor. J. Fish Biol. 69, 1709–1730. Thorsen, A., Witthames, P.R., Marteinsdottir, G., Nash, R.D.M., Kjesbu, O.S., 2010. Fecundity and growth of Atlantic cod (Gadus morhua L.) along a latitudinal gradient. Fish. Res. 104, 45–55. Ustups, D., Müller-Karulis, B., Bergstrom, U., Makarchouk, A., Sics, I., 2013. The influence of environmental conditions on early life stages of flounder (Platichthys flesus) in the central Baltic Sea. J. Sea Res. 75, 77–84. van Damme, C.J.G., Dickey-Collas, M., Rijnsdorp, A.D., Kjesbu, O.S., 2009. Fecundity, atresia, and spawning strategies of Atlantic herring (Clupea harengus). Can. J. Fish. Aquat. Sci. 66, 2130–2141. Vourinen, I., Antsulevich, A.E., Maximovich, N.V., 2002. Spatial distribution and growth of the common mussel Mytilus edulis L. in the archipelago of SW-Finland, northern Baltic Sea. Boreal Environ. Res. 7, 41–52. Waldeck, P., Larsson, K., 2013. Effects of winter temperature on mass loss in Baltic blue mussels: implications for foraging sea ducks. J. Exp. Mar. Biol. Ecol. 444, 24–30. Westberg, V., 1997. Food and feeding habits of flounder Platichthys flesus (L.) in the NW Åland archipelago, northern Baltic Sea. (MSc Thesis) Åbo Akademi University (in Swedish, with English abstract). Westerbom, M., Kilpi, M., Mustonen, O., 2002. Blue mussels, Mytilus edulis, at the edge of the range: population structure, growth and biomass along a salinity gradient in the north-eastern Baltic Sea. Mar. Biol. 140, 991–999. Witthames, P.R., Greer Walker, M., 1995. Determination of fecundity and oocyte atresia in sole (Solea solea) (Pisces) from the Channel, the North Sea and the Irish Sea. Aquat. Living Resour. 8, 91–109. Witthames, P.R., Andersson, E., Greenwood, L.N., Lyons, B., Fonn, M., Kjesbu, O.S., 2003. Apoptosis in regressing follicles from Solea solea and Gadus morhua. Fish Physiol. Biochem. 28, 377–378. Wolowicz, M., Sokolowski, A., Bawazir, A.S., Lasota, R., 2006. Effects of eutrophication on the distribution and ecophysiology of the mussel Mytilus trossulus (Bivalvia) in the southern Baltic Sea (the Gulf of Gdansk). Limnol. Oceanogr. 51, 580–590. FishBase. Froese, R. and Pauly, D. (Editors), 2011. World Wide Web electronic publication. www.fishbase.org (12/2013) http://www.fishbase.org/summary/Platichthys-flesus. html.