Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?

MARSYS-02922; No of Pages 9 Journal of Marine Systems xxx (2016) xxx–xxx

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Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring? Nina Mikkelsen a, Torstein Pedersen a,⁎, Thassya Christina dos Santos Schmidt b,c, Inger-Britt Falk-Petersen a, Aril Slotte b a b c

Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway, NO-9037 Tromsø, Norway Institute of Marine Research (IMR), Box 1870 Nordnes, NO-5817 Bergen, Norway Department of Biology, University of Bergen, Box 7803, NO-5020 Bergen, Norway

a r t i c l e

i n f o

Article history: Received 1 March 2016 Received in revised form 6 December 2016 Accepted 15 December 2016 Available online xxxx Keywords: Clupea pallasii Clupea harengus Balsfjord herring Lake Rossfjord herring Life history characteristics

a b s t r a c t Herring from two unexploited fjord populations, Lake Rossfjord (LRH, n = 100) and Balsfjord (BFH, n = 420) in northern Norway, were sampled in 2014 and 2015. Life history characteristics were analysed and compared to the oceanic Norwegian spring-spawning herring (NSSH), and other Atlantic and Pacific herring stocks. Genetic studies have shown that LRH and BFH are ancestors evolved from Pacific herring that hybridized with Atlantic herring. This study shows that both LRH and BFH mature at a relatively early age, at 2–3 years and ca. 4 years respectively, compared to ca. 5 years for NSSH. The spawning stocks of LRH and BFH consist of small fish and contain relatively few age classes. Both fjord populations have slow growth after sexual maturity; LRH has a very low asymptotic length (L∞ = 19.8 cm), while that of BFH is higher (L∞ of 28.5 cm); both these values being lower than that of NSSH (L∞ of ca. 37 cm). The somatic relative fecundity of LRH is 176.6 oocytes g−1, while the somatic relative fecundity of recruit and repeat BFH spawners is 152.4 and 183.1 oocytes g−1, respectively. These estimates are lower than those for NSSH and other Atlantic herring fjord populations, but comparable with other Pacific herring. Due to the smaller body sizes of the spawners in the LRH and BFH populations, absolute fecundity is much lower than in NSSH. The gonadosomatic indices of prespawning fish are similar in LRH and BFH, being slightly higher compared to the NSSH, but lower than values reported for Pacific herring. The natural mortality rates of LRH and BFH (M = 0.64 year−1 and M = 0.76 year−1, respectively) are much higher than in NSSH (M = 0.15 year−1) and most other Atlantic herring populations, except the Lusterfjord herring. However, these high mortality rates are similar to those of several Pacific herring populations. It is concluded that LRH and BFH show low somatic growth and high natural mortality rate. These life history characteristics differ from those of NSSH, but are similar to some Pacific herring populations adapted to a coastal high-mortality risk environment. © 2016 Elsevier B.V. All rights reserved.

1. Introduction The two species of herring, the Atlantic herring (Clupea harengus) and the Pacific herring (Clupea pallasii), are both ecologically and commercially important planktivorous species in oceanic and coastal waters (Hay et al., 2008) and comprise many stocks. The ancestors of herring may have evolved in the Arctic Basin during the Paleogene (Svetovidov, 1952) and cannot have spread into the Pacific before the Bering Strait opened in the Pliocene about 3–5 mill years ago (Herman and Hopkins, 1980 in Grant, 1986). Herring populated both the western and the eastern side of the northern Pacific and northern Atlantic, respectively. Atlantic and Pacific herring are considered as distinct species (Grant, 1986). During postglacial warm periods (b 12,000 years), Pacific ⁎ Corresponding author. E-mail address: [email protected] (T. Pedersen).

herring may have invaded the Arctic north - eastern Atlantic and formed local populations in the Kara Sea and White Sea, and in some Norwegian fjords (Laakkonen et al., 2013, 2015). These herring populations are genetically similar to the Pacific herring and are considered to be Clupea pallasii populations (Laakkonen et al., 2013, 2015; Semenova et al., 2013). In northern Norway at 69°N, two neighbouring fjord populations with assumed Pacific ancestry have been identified by genetic methods in Balsfjord and in Lake Rossfjord (Jørstad et al., 1991; Laakkonen et al., 2015). Recent genetic studies indicate that these populations, to a varying degree, have hybridized with Atlantic herring (Laakkonen et al., 2015). Both the Balsfjord (BFH) and the Lake Rossfjord (LRH) populations may spatially overlap with juveniles from the highly migratory Norwegian spring-spawning herring (NSSH), which inhabit fjords and coastal areas in northern Norway but have different offshore spawning areas than the local fjord populations (Hognestad, 1994; Jørstad and

http://dx.doi.org/10.1016/j.jmarsys.2016.12.004 0924-7963/© 2016 Elsevier B.V. All rights reserved.

Please cite this article as: Mikkelsen, N., et al., Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?, J. Mar. Syst. (2016), http://dx.doi.org/10.1016/j.jmarsys.2016.12.004

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N. Mikkelsen et al. / Journal of Marine Systems xxx (2016) xxx–xxx

Pedersen, 1986). Vertebrae number is significantly lower in BFH and LRH than in NSSH (Hognestad, 1994; Kjørsvik et al., 1990). Although the genetic structure of the Norwegian fjord herring populations of Pacific ancestry have been investigated, life history characteristics such as individual growth, fecundity, reproductive effort, longevity and natural mortality rate are less known in these populations. Both Atlantic and Pacific herring have large interspecific life history diversity with a large range in individual growth patterns, age and size at maturity, and spawning periods (Hay et al., 2008; Jennings and Beverton, 1991; McQuinn, 1997). In the White Sea area, there are herring populations of assumed Pacific ancestry with different spawning periods (spring versus summer) and different growth patterns (Semenova et al., 2009). Along the Norwegian coast, south of 68°N, there are several identified local fjord Atlantic herring populations with varying life history patterns (Eggers et al., 2014; Pampoulie et al., 2015; Silva et al., 2013). Spawning site selection differs between Pacific herring populations that deposit their eggs on aquatic vegetation in the sublittoral zone (Alderdice and Hourston, 1985) and most Atlantic herring populations that deposit their eggs on gravel or rocks at deeper water coastally and on offshore banks (Geffen, 2009; Grant, 1986). BFH is a beachspawner depositing the eggs on macroalgae in very shallow waters (Jørstad, 1994; Kjørsvik et al., 1990), while LRH spawns on vegetation at 7–9 m depth (Hognestad, 1994). The main objective of this study was to investigate if the life history characteristics of BFH and LRH differ and to compare them to those of NSSH and other Atlantic and Pacific populations. The life history parameters studied were: length and age at maturity, vertebrae number, growth pattern, potential and relative fecundity, reproductive output, and natural mortality rate. We hypothesized that: (i) life history characteristics of BFH and LRH are similar to their Pacific ancestors, and (ii) life history characteristics of these two populations differ from NSSH and other Atlantic herring populations. The approach in the study was to

sample fish from the local populations in the field and estimate growth functions (von Bertalanffy's growth equation), instantaneous mortality rate from age frequency distribution of spawners, fecundity and reproductive effort measured as weight proportion of gonad mass relative to body weight.

2. Materials and methods 2.1. Study area and environmental conditions Both study sites are located in Troms County, northern Norway (Fig. 1). Balsfjord is a 68 km long fjord with a sill (35 m) that separates the fjord from the open coastal waters and limits the exchange of deep water. In the period from October to late April, the water column is vertically mixed and almost homogenous (Mankettikkara, 2013). The winter temperatures, at 100 m depth in the inner part of Balsfjord in the period 1980–2012, ranged 2.5–5.5 °C (Mankettikkara, 2013) with salinities in the range 32.6–33.8‰ (Fig. 479 in Mankettikkara, 2013). The mean temperatures in spring, at the same depth, ranged between 0.5 and 3.9 °C and the salinities ranged between 30.5 and 33.9‰ (Fig. 455 in Mankettikkara, 2013). At Holmenes (Fig. 1), the spawning ground of BFH, the water temperatures in April ranges from 1 to 4 °C (Lurås, 1994). Lake Rossfjord is approximately 8 km2 with a maximum depth of 60 m and is connected to the fjord of Malangen by a shallow 4 km long “river”, where high salinity water may enter the system at high tide. The surface lake water is fresh, but the salinity increases with depth to 16–18‰ at ca. 12 m depth. The water is anoxic from the bottom layer up to ca. 12 m depth and LRH is distributed from the surface down to the anoxic water (Hognestad, 1994). During winter, Lake Rossfjord is ice-covered and as the ice breaks, usually in early June, LRH spawns

Fig. 1. Map of the study areas, Lake Rossfjord and Balsfjord. Arrows show shallow sills. Holmenes is the main spawning site for Balsfjord herring. LR1 and LR2 are sampling locations for Lake Rossfjord herring.

Please cite this article as: Mikkelsen, N., et al., Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?, J. Mar. Syst. (2016), http://dx.doi.org/10.1016/j.jmarsys.2016.12.004

N. Mikkelsen et al. / Journal of Marine Systems xxx (2016) xxx–xxx

nearshore at several localities in the lake, at a salinity of 15–18‰ and temperature at 6–9 °C (Hognestad, 1994). 2.2. Fish sampling Trawl samples of BFH were provided by R/V Johan Ruud, UiT The Arctic University of Norway (Table 1). Gillnet samples were collected during several surveys in Balsfjord (2014 and 2015) and one survey in Lake Rossfjord in 2015 (Fig. 1, Table 1). The gillnets were 25 m long by 2 m deep with mesh sizes of 21, 25 and 28 mm (Table 1), except in Balsfjord where the smallest mesh size was not used. In accordance with observations by Lurås (1994), the nets were set at the spawning ground Holmenes in Balsfjord at approximately 5 m depth, in series of four (alternate 25 and 28 mm mesh size) at 19:00–20:00 h local time and hauled the next day (08:30–09:00 h). In Lake Rossfjord, samples were collected just as the ice was retreating on 27 May 2015. All icefree, shallow and near-shore areas along the lake at depths of 7–12 m were surveyed with an echo sounder (Humminbird 570 Sonar 60° Dual Beam 200/83 kHz) to detect aggregations of fish and the echo sounder recordings indicated the presence of herring at two locations, Langnesodden (LR1) and Solheim (LR2) (Fig. 1). Gillnets were placed at LR1 and LR2 in series of three at approximately 10 m depth. At LR1, gillnets were set at 00:30 h and hauled at 13:30 h, while at LR2 the nets were set at 12:30 h and hauled at 13:45 h. The County Governor of Troms, who manages Lake Rossfjord aiming to protect the anadromous fish passing through the lake, granted permission for the collection of herring by gillnets to UiT The Arctic University of Norway. Herring samples were frozen for analysis in the laboratory, where total length (TL; cm), weight (TW; gram) and gonadal weight (OW; gram) were measured, and the number of vertebrae (VS) was counted. In the samples from BFH (2015) and LRH (2015), one fresh subsample of ovaries was removed and preserved in 3.6% phosphate-buffered formaldehyde and the remaining part frozen. The maturity stage was recorded for all captured fish. The maturity stage was classified according to an 8-point scale: immature = 1 and 2, maturing–mature = 3–5, running/spawning = 6, spent = 7, recovering/resting = 8 (Mjanger et al., 2012). The sagittal otoliths were washed in clean water and stored in paper bags. All fish were aged from their scales using standard ageing techniques. The age compositions of the spring samples of BFH (2014) and BFH (2015) were compared to herring sampled in Balsfjord in spring 1988. 2.3. Growth Individual growth in BFH and LRH was assessed by fitting the von Bertalanffy growth model (VBGM) to data (data for BFH sampled at the spawning ground were pooled for 2014 and 2015); assuming growth is adequately described by the VBGM equation   Lt ¼ L∞ 1−e−K ðt−t 0 Þ

ð1Þ

Table 1 Herring samples collected in Balsfjord (BFH) and Lake Rossfjord (LRH) in northern Norway 69°N. Sampling gear, number of fish (N), sex (Females = F, Males = M), range for stage of maturity (Ma) and age. Sample

Date

Sampling gear

N

(F, M)

Ma

Age

BFH (2014) BFH (2014)a BFH (2015) BFH (2015) BFH (2015) LRH (2015)b

23.04.2014 26.09.2014 16.03.2015 20.03.2015 14.04.2015 27.05.2015

Gillnet (25, 28 mm) Trawl Trawl Gillnet (25, 28 mm) Gillnet (25, 28 mm) Gillnet (21, 25, 28 mm)

45 92 167 70 46 100

(27, 18) (51, 41) (68, 99) (38, 32) (22, 24) (69, 31)

4–8 3–4 2–7 4–6 4–7 1–7

3–7 3 2–8 4–11 4–8 2–10

a b

This sample was only used in consideration of age at maturity. LRH collected at LR1 and LR2 were pooled due to low sample size at LR2.

3

where Lt is the average length at age t, L∞ is the asymptotic maximum length, K is the von Bertalanffy growth coefficient and t0 was fixed to 0. Data were fitted to the VBGM model using nonlinear regression in SYSTAT 13.1. The estimated parameters L∞ and K were compared to previously published parameters of NSSH (Beverton et al., 2004). 2.4. Fecundity and reproductive output Only data collected prior-to-spawning in 2015 were used in BFH fecundity estimates. Fecundity estimates prior to spawning reflect the final fecundity, because no downregulation through atresia takes place during this period (Kurita et al., 2003). The autodiametric method was applied to estimate the mean oocyte diameter (OD, μm) (Thorsen and Kjesbu, 2001). Potential fecundity (FP) was determined by the oocyte packing density theory (Kurita and Kjesbu, 2009) and represented as FP = OW × 7.474 × 1010 × OD−2.584. Somatic relative potential fecundity (RFP) was calculated as FP divided by the somatic weight (TW − OW) (Ma et al., 1998). Published prior to spawning NSSH fecundity data (Óskarsson et al., 2002; Kurita et al., 2003) were used to compare both FP and RFP estimates with those of BFH and LRH. Reproductive output was measured by the gonadosomatic index (GSI) for females classified to stage 6 in the maturity scale. GSI was expressed as the ratio OW/ (TW − OW). 2.5. Mortality The total instantaneous mortality rate (Z) was estimated using the Chapman–Robson catch-curve estimator (Chapman and Robson, 1960), using the data on age frequencies for BFH and LRH. This method is considered to be a reliable mortality rate estimator (Dunn et al., 2002). The age classes used in each mortality estimation include the age class at peak abundance and older age-classes up to and including the oldest age-class with non-zero abundance in the sample. Based on literature values for BFH (Lurås, 1994) and for the Lusterfjord herring, western Norway (61°N, 7°E) (Aasen, 1952), Z was estimated with the Chapman–Robson estimator using the “chapmanRobson”-function in the package FSA implemented in R (www.r-project.org). 2.6. Statistical analysis If a variable was normally distributed, a two-sample t-test with unequal variance was applied for two groups and an analysis of variance was applied for three groups. If variables deviated from normality, Mann-Whitney (M-W) test was applied. Chi-square tests were applied to test for differences between groups in age composition. Analysis of covariance (ANCOVA) was used to test for differences in a variable (FP and RFP) between two groups and to test if the covariate (length) had a significant effect. A linear regression model was used to test if natural mortality rate (M) was affected by species (C. harengus or C. pallasii, categorical variable) and asymptotic length (L∞). A probability level of 5% was taken as indicating statistical significance. Statistical tests were performed using SYSTAT 13.1 and R version 3.2.3 (www.r-project.org). Data on asymptotic lengths given as standard length (SL, cm) were converted to total length (TL) using the relationship: TL = 0.776 + 1.223 × SL (Karpov and Kwiecien, 1988). 3. Results 3.1. Herring samples from Balsfjord (2014 and 2015) and Lake Rossfjord (2015) One sample of 92 three year old maturing herring (51 females, 41 males) was taken by bottom trawl in September 2014 outside the spawning area in Balsfjord and genetically identified as BFH using allozyme-electrophoretic methods (unpublished, Geir Dahle, Institute of Marine Research, Norway). A total of 328 herring were collected on

Please cite this article as: Mikkelsen, N., et al., Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?, J. Mar. Syst. (2016), http://dx.doi.org/10.1016/j.jmarsys.2016.12.004

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N. Mikkelsen et al. / Journal of Marine Systems xxx (2016) xxx–xxx

the spawning ground in Balsfjord, 45 herring in 2014 and 283 in spring 2015 (Table 1). The mean age was 5.6 years and 4.9 years in BFH (2014) and BFH (2015), respectively (Fig. 2a), while the corresponding mean length was 25.3 cm and 23.3 cm (Fig. 2b). The length at age did not differ between males and females for most age groups (Table 2). The maturity in BFH caught in spring ranged from stage 2 to 8 and the majority of herring sampled in April were in stage 6 both years (Table 1). The vertebral counts did not differ between 2014 and 2015 (t-test, p = 0.745), ranging from 52 to 57 (mean = 55.0, SD = 0.79). In Lake Rossfjord, most of the LRH were caught in gillnets of mesh size 25 mm and only one large herring (25.0 cm) was caught with mesh size 28 mm. The temperature at LR1 and LR2 ranged from 6.4 to 9.2 °C. One hundred LRH were captured (LR1: n = 90, LR2: n = 10), and were pooled in analysis. The total LRH sample consisted of 69 females and 31 males aged from 2 to 10 years (mean = 3.8 years, SD = 1.4) (Fig. 2c, Table 1) and with lengths between 16.5 and 25 cm (mean = 19.3 cm, SD = 1.0) (Fig. 2d). The maturity ranged from stage 1 to 7 (Table 1) and the majority of fish were in stages 5 and 6. There was only one immature fish in stage 1 in the sample. The vertebral counts ranged from 52 to 56 (mean = 54.2, SD = 0.87). VS was lower in LRH than BFH (t-test, p b 0.001).

Table 2 Length at age by sex (Females = F, Males = M) of herring in samples from Balsfjord (BFH (2014), BFH (2015)) and Lake Rossfjord (LRH (2015)). Test statistics for differences in length at age by sex, given by t-test (t stats, degree of freedom (df) and p value). Data source

BFH (2014)

BFH (2015)

LRH (2015)

3.2. Age at maturity and individual growth The sample of BFH caught in 2015 was dominated by four year old herring (Fig. 2a), while the BFH sample from September 2014 consisted of three year old herring that were in the maturing stage and spawned first time in spring 2015 as four year olds. This implies an age at maturity of approximately four years in BFH. In the sample of LRH, two year old fish were in stages 5 and 6, indicating an age at maturity of two years. The BFH (2014) sample consisted of significantly older and larger fish than the BFH (2015) sample, and fish in the LRH (2015) sample were significantly younger and smaller than in the BFH (2015) sample (Table 3). Data from Lurås (1994) for BFH (1988) showed few fish younger than six years and thus significantly older fish than BFH (2014) and BFH (2015) (Table 3). The VBGM estimated parameter for asymptotic length was longer in BFH (L∞ = 28.5 cm) than in LRH (L∞ = 19.8 cm); concurrent K was much higher in LRH (K = 1.21 year−1) than in BFH (K = 0.37 year−1) (Fig. 3a, Table 4). Growth in LRH and BFH were similar to the growth

a

Age

N

Length (cm)

t stats

df

p value

1 14 9 5

0.35 0.22 0.33 0.35

178

b0.001

34

0.039

4.512

25

b0.001

1.181 1.467 0.582 1.434 −0.164

2 4 6 15 2

0.35 0.20 0.58 0.17 0.88

F

M

Mean (SD) F

M

3 4 5 6 7

1 2 10 8 6

0 2 7 5 4

23.0 (−) 24.3 (0.35) 24.8 (1.27) 26.0 (0.96) 26.4 (0.38)

25.0 (0.71) 24.1 (0.85) 25.5 (0.79) 26.1 (0.48)

−1.432 1.274 1.018 1.025

3 4 5 6 7 8 10 11

2 86 1 23 0 13 1 0

1 97 1 19 13 15 0 1

21.0 (0.70) 22.3 (0.77) 28.0 (−) 26.0 (0.69)

19.5 (−) 21.5 (0.97) 25.0 (−) 25.5 (0.84) 26.2 (0.80) 25.9 (0.84)

a

2 3 4 5 6 7 10

10 34 3 17 3 1 1

3 5 10 11 2 0 0

18.2 (0.42) 19.3 (0.65) 19.2 (0.58) 19.9 (0.34) 19.7 (0.76) 19.5 (−) 25.0 (−)

27.2 (0.63) 28.0 (−)

5.855 a

2.149 a

31.5 (−) 17.5 (1.0) 18.8 (0.76) 18.9 (0.99) 19.6 (0.54) 19.8 (0.35)

Insufficient data for test.

of NSSH up to the age of maturity, but decreased after age of maturity in both LRH and BFH (Fig. 3b). 3.3. Fecundity and reproductive output Two groups of spawners were observed in BFH herring: recruit spawners and repeat spawners. This differentiation was based on body length and age of BFH females, i.e., recruit spawners (TL between 20 and 24.5 cm, age = 4) and repeat spawners (TL ≥ 25 cm, age ≥ 6). FP differed significantly between BFH and LRH (t-test; p b 0.001). No significant difference was found in RFP (t-test; p = 0.07). Differences between BFH recruit and repeat spawners were found for both fecundity estimates (t-test; p b 0.001).

Fig. 2. Age and length distribution of herring samples. (a) and (b) Balsfjord (BFH (2014), BFH (2015)). (c) and (d) Lake Rossfjord (LRH (2015)).

Please cite this article as: Mikkelsen, N., et al., Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?, J. Mar. Syst. (2016), http://dx.doi.org/10.1016/j.jmarsys.2016.12.004

N. Mikkelsen et al. / Journal of Marine Systems xxx (2016) xxx–xxx Table 3 Tests for differences in age and length between samples from Balsfjord (BFH (2014), BFH (2015)) and Lake Rossfjord (LRH (2015)), given by Mann-Whitney (M-W), U test statistics (U), degrees of freedom (df) and p value. For tests between age-composition data from Lurås (1994) (BFH 1988) and other groups, frequencies in 2 × 5 tables with age classes ≤4, 5, 6, 7, and ≥8 were tested using χ2-tests. Variable

Data source

Test

Test statistic

df

p value

Age

BFH (2014) vs BFH (2015) BFH (2015) vs LRH (2015) BFH (2014) vs BFH (2015) BFH (2015) vs LRH (2015) BFH (1988) vs BFH (2014) BFH (1988) vs BFH (2015)

M-W M-W M-W M-W χ2 χ2

U = 8685 U = 19.230 U = 9630 U = 27.724 χ2 = 75.0 χ2 = 320

1 1 1 1 4 4

b0.001 b0.001 b0.001 b0.001 b0.001 b0.001

Length Age

Potential fecundity had a positive and significant correlation with total length (Fig. 4a). In general, BFH produced more eggs than LRH (Fig. 4a), and BFH repeat spawners produced more eggs than recruit spawners (Fig. 4a and b). With regard to RFP, LRH showed the highest mean production of oocytes (176.6 oocytes g− 1) followed by BFH (165.7 oocytes g−1), with repeat BFH spawners showing higher relative fecundity compared to recruit BFH spawners (183.1 oocytes g− 1, 152.4 oocytes g− 1, respectively). There was no significant effect of

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Table 4 Von Bertalanffy growth parameters (L∞, K) of herring populations: Balsfjord (BFH), Lake Rossfjord (LRH) and Norwegian spring-spawning herring (NSSH). Herring stock

L∞ (cm)

K (year−1)

Source

BFH LRH NSSH

28.5 19.8 36.8

0.37 1.20 0.28

This study This study Beverton et al. (2004)

length on RFP in LRH RFP (p = 0.75), but the relationship was positive (Fig. 4c). A slight increase in RFP in BFH was observed, mainly between recruit and repeat spawners (Fig. 4c). Comparing these two populations with previous NSSH reported data (Kurita et al., 2003; Óskarsson et al., 2002), the number of eggs produced per female by NSSH is higher compared to these local populations (Fig. 4b), although the number of eggs produced per gram of females (RFP) was similar among BFH, LRH, and NSSH (Fig. 4d). The reproductive output given by mean GSI for females in Balsfjord was 0.236 (SD ± 0.09) and 0.213 (SD ± 0.07) for 2014 and 2015, respectively (Table 5), but the difference was not significant (M-W, U = 187.5, df = 1, p = 0.372). In Lake Rossfjord, the mean GSI was 0.225 (SD ± 0.06) (Table 5). Overall, GSI values were not significantly different among BFH (2014), BFH (2015), and LRH (2015) (K-W, χ2 = 1.672, df = 2, p = 0.433) and were all higher than reported for NSSH (Table 5). 3.4. Mortality rate The total mortality rate (Z) for BFH in 2014 and 2015 was 0.77 and 0.74 year− 1, respectively. For LRH in 2015, Z was estimated as 0.64 year− 1 (Table 6). The Z-values estimated from literature data were 0.63 year−1 for the Balsfjord herring in 1988 and 0.85 year−1 for the Lusterfjord herring in 1949–1950 (Table 6). Average M for C. pallasii populations (Table 5) was higher (M = 0.66 year−1) compared to C. harengus (M = 0.34 year−1), (t = 2.36, df = 12, p = 0.036). The regression model for M revealed a close to significant negative effect of increasing L∞ (t = 2.08, df = 11, p = 0.06), a significant lower intercept for C. harengus than for C. pallasii (t = 3.0, df = 11, p = 0.012) (Fig. 5). The regression model was M = 1.33– 0.0221 × L∞ for C. pallasii and M = 0.96–0.0221 × L∞ for C. harengus, and r2 was 0.51 (Fig. 5). 4. Discussion 4.1. Adaptations to environmental conditions in LRH and BFH

Fig. 3. Length at age in herring stocks. (a) Total length at age of herring caught in Balsfjord (BFH) in 2014 and 2015 (white circles) and in Lake Rossfjord (LRH) in 2015 (black circles). Lines show von Bertalanffy growth model fitted to data (BFH: solid line, LRH: dashed line). (b) Length at age in BFH, LRH and Norwegian spring-spawning herring (NSSH). Arrows indicate approximate age at maturity.

The vertebrae number estimated for LRH in 2015 was very similar to the values measured during 1971–1973 (Hognestad, 1994), but slightly lower than those for BFH. VS for NSSH is reported to be ca. 57.2 (Eggers et al., 2014; Runnstrøm, 1941) which is higher than in LRH and BFH. This supports the previous morphometric and genetic studies showing that local populations differ from NSSH. The clear difference in growth patterns and age at maturity between the BFH, LRH and NSSH, suggest that they have adapted to very different environmental conditions. The water masses in Balsfjord are characterized by cold water that is vertically mixed in winter with salinity N 32.5‰ (Mankettikkara, 2013), while LRH experiences water masses with higher temperatures, but lower salinity (Hognestad, 1994). Environmental conditions in Lake Rossfjord in spring 2015 were similar to the conditions reported by Hognestad (1994) in the 1970s, and the lack of schooling behaviour in LRH could be an adaptation to the low levels of oxygen because schooling might cause hypoxic conditions in itself (Domenici et al., 2007). Higher salinity than in Lake Rossfjord and higher temperatures than in Balsfjord characterize the water masses where NSSH is distributed in winter (Nøttestad et al., 1996).

Please cite this article as: Mikkelsen, N., et al., Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?, J. Mar. Syst. (2016), http://dx.doi.org/10.1016/j.jmarsys.2016.12.004

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N. Mikkelsen et al. / Journal of Marine Systems xxx (2016) xxx–xxx

Fig. 4. (a) Potential fecundity and (c) relative somatic fecundity versus total length from Balsfjord and Lake Rossfjord prior to spawning. Mean (±SD) of (b) potential fecundity and (d) relative somatic fecundity of Balsfjord, Lake Rossfjord, and reported data of Norwegian spring-spawning herring (Kurita et al., 2003; Óskarsson et al., 2002). Data from Óskarsson et al. (2002) represents mean and standard error in females at 31 cm. Mean and SD are based on females at 19 cm length class in LRH, 22 cm length class for recruit BFH, 26 cm length class for repeat BFH, and 34 cm length class for NSSH in Kurita et al. (2003). Symbols used in panels a and c are presented in panel a, whereas symbols in panels b and d are presented in panel b. Average potential fecundity (black triangle, b) was not provided in Óskarsson et al. (2002). Note that the y-axis scales are different.

4.2. Age and length-distributions and age at maturity The age at maturity for LRH in 2015 seemed to be between 2 and 3 years, which is slightly lower than the age of maturity of 3 years estimated by Hognestad (1994). Hognestad (1994) concluded that the maximum life span of LRH was 5 years, while fish aged 6, 7 and 10 years old were collected in this study, using the same maximum mesh size. Our results indicate that longevity has increased slightly since the 1970s. This result is also supported by the ban on gillnet fishery in Lake Rossfjord since 1994. Longevity of Balsfjord herring may have decreased since 1988 because Lurås (1994) found significantly older fish than 8 years compared to our samples from 2014 and 2015. However, Lurås (1994) used gillnets with mesh size ca. 30 mm, which may have biased the size distribution towards larger and older fish than found in 2014 and 2015 when mesh sizes were 25 and 28 mm. Also, the samples from the spawning areas in 1988 comprised no 4 year old fish, and fewer 5 than 6 year old fish (Lurås, 1994), suggesting that the median age of maturity was at least 5 years in 1988. This indicates that the age of maturity may have decreased from 5 to 4 years in BFH in the period from 1988 to 2014/2015. The age at maturity in both BFH and LRH is lower than in NSSH, which has a median age of maturity of ca. 5 years (Toresen and Østvedt, 2000). Since the mesh sizes of 25 and 28 mm were used in both Balsfjord and Lake Rossfjord, and most fish were caught in the intermediate mesh size (25 mm) gillnet in Lake Rossfjord, length differences between LRH and BFH are not due to gillnet selectivity.

Johannessen et al. (2014) caught herring in a wide size range (25– 38 cm) using gillnets with a mesh size of 26 mm; thus we assume that herring longer than 32 cm would have been caught in our study areas if they were present at the locations. 4.3. Individual growth The comparison of BFH growth curve in 2014 and 2015 with 1988 data (Lurås, 1994) showed a lower L∞ (28.5 vs 35.5 cm) and a higher K (0.37 vs 0.24 year−1) in 2014–2015. This change may be a consequence of the earlier age at maturity recorded in 2014–2015. The growth in LRH in the 1970s was very variable between years and herring with lengths from 22 to 24 cm were frequent in the samples (Hognestad, 1994), while few herring larger than 22 cm were caught in 2015. Despite these interannual variations in growth patterns, L∞ in LRH may be characterized as very low and intermediate for BFH when compared to other C. pallasii and C. harengus populations (Table 5). NSSH has one of the highest L∞ among the herring populations (Hay et al., 2001). The Lusterfjord herring from western Norway, which is a C. harengus population (Pampoulie et al., 2015), had a low and similar L∞ to LRH (L∞ = 21 cm) (Aasen, 1952; Beverton and Holt, 1959), and most other Atlantic herring populations with low L∞ and high K reported so far live in the Baltic Sea (Thurow, 1976). In the Pacific herring populations found in the White Sea and the south-eastern Barents Sea, the length at age of old herring differ markedly between stocks suggesting that L∞

Please cite this article as: Mikkelsen, N., et al., Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?, J. Mar. Syst. (2016), http://dx.doi.org/10.1016/j.jmarsys.2016.12.004

N. Mikkelsen et al. / Journal of Marine Systems xxx (2016) xxx–xxx

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Table 5 Natural mortality rate M (year−1), von Bertalanffy growth model parameters for asymptotic length (L∞) and growth coefficient (K) and wet gonadosomatic index (GSI, where GSI = ovarian mass/somatic mass) for herring populations. Herring origin

M (year−1)

L∞ (cm)

K (year−1)

C. pallasii BFH (2014 and 2015) BFH (1988) BFH (2014) BFH (2015) LRH Canada, BC Canada, BC Japan Pacific Beaufort Sea

0.761 0.631 0.771 0.741 0.641 a 0.463 1.084 0.206 0.565 0.864

28.51 35.52

0.371 0.242

C. harengus NSSH North Sea North Sea Lusterfjord Baltic north Baltic south Irish Sea Celtic Sea

0.157 0.2510 0.2311 0.851 0.3514 0.3614 0.206 0.3015

19.81

1.211

27.05 38.56 26.35 d 33.616

0.196 0.365

36.88 30.010

c 0.288 0.3810

21.013 19.414 27.714 29.56 b 30.116

0.6513 0.4014 0.4814 0.396

GSI

0.241 0.211 0.231 a 0.393

0.295 0.144 0.209 0.1912

1. This study, 2. Lurås (1994), 3. Tanasichuk (2000), 4. Tanasichuk et al. (1993), 5. Gunderson and Dygert (1988), 6. Beverton (1963), 7. Toresen and Østvedt (2000), 8. Beverton et al. (2004), 9. Silva et al. (2013), 10. Beverton and Holt (1959), 11. Cushing and Bridger (1966), 12. Hickling (1940), 13. Aasen (1952), 14. Thurow (1976), 15. Denney et al. (2002), 16. Hay et al. (2001). a GSI and M estimated for 6 year old herrings. b Value taken from largest mean length at age 9 for Celtic Sea. c Parameters estimated for 5 year old herrings. d Total length converted from standard length.

may vary from b20 cm to above 30 cm (Semenova et al., 2009). The true Pacific populations have in general a similar range of L∞ values as Atlantic herring. The western Pacific and the northern populations in the Bering Sea are characterized by high L∞ and low K, while there is a strong latitudinal trend in the eastern Pacific towards lower L∞ and higher K in the southern populations (Hay et al., 2008). The small body size at maturation, low age at maturity, high K and low L∞ of LRH compared to the intermediate values for BFH, and contrasting late maturing NSSH with a low K and large L∞, are combinations of characters that are consistent with patterns expected from trade-offs between reproduction and somatic growth (Roff, 1984). These interpopulation differences in maturation length and age and growth pattern have wide-reaching effects on size and age-distribution of the spawning stocks. 4.4. Fecundity and GSI Prespawning LRH potential fecundity for 2015 ranged from 2 to 12 thousand eggs, while Hognestad (1994), using a counting method, recorded a fecundity between 4 and 7000 eggs, and associated this small egg production with environmental conditions inside Lake Rossfjord.

Table 6 Estimates of total mortality rates (Z) for herring using the Chapman‐Robson catch-curve estimator, with lower and upper range for 95% confidence intervals given in brackets. Age classes used refers to the age classes from age of peak abundance that are used in the estimation and N is the total number of fish in those age-classes. Data source

N

Age classes used (year)

Z (year−1)

Balsfjord (2014) Balsfjord (2015) Balsfjord (1988)a Lake Rossfjord (2015) Lusterfjord (1949–50)b

40 270 232 87 570

5–7 4–11 6–10 3–10 5–10

0.77 (0.47, 1.06) 0.74 (0.42, 1.05) 0.63 (0.38, 0.88) 0.64 (0.39, 0.90) 0.85 (0.66. 1.04)

a b

Lurås (1994). Aasen (1952).

Fig. 5. Asymptotic length L∞ and natural mortality rates for stocks of Pacific herring (open symbols) and Atlantic herring (filled symbols). Lines (stippled line C. pallasii, solid line C. harengus) show predicted values from a linear regression model with different intercepts for the two species.

A positive correlation between potential fecundity and length was found in BFH and LRH, likewise in other herring populations (Kennedy et al., 2011; Óskarsson and Taggart, 2006). Even though the BFH repeat spawners produced 43.3% more eggs than recruit spawners, these local populations produced 58.9–85% fewer eggs compared to the oceanic NSSH. Therefore, due to the much smaller body size of mature LRH and BFH, fish from these two populations had much smaller absolute potential fecundity than had NSSH. The number of eggs produced per gram (RFP) of female, however, was analogous among BFH, LRH and NSSH. It has been suggested that local Atlantic herring populations have lower costs for migration and movement than large oceanic populations and thus direct more energy towards gonad production (Silva et al., 2013; Slotte, 1999). The average relative fecundities for LRH and BFH (RFP) were similar to values reported for herring in the north-eastern Pacific where relative fecundity was estimated as 220 oocytes g−1 for a stock in California, 200 oocytes g−1 in Br. Columbia and 150 oocytes g− 1 in Alaska (Hay et al., 2008). However, it should be taken into account that the relative fecundity for Pacific herring was estimated based on total body weight, not somatic weight as used here. In the Pacific, there is a decrease in size-specific fecundity with increasing latitude (Hay, 1985). Based on the number of eggs produced per gram, we can suggest that BFH and LRH invest more energy in reproductive purposes, probably as an attempt to guarantee high egg survival due to the adverse conditions found in these fjords. In addition, both LRH and BFH have a short life span, as reported in this study and as previously documented (Hognestad, 1994; Lurås, 1994). The GSI values in the range 0.21–0.23 for LRH and BFH were slightly above the GSI of 0.20 reported for NSSH, but were lower than the GSI values for other Norwegian local herring populations ranging from 0.26 to 0.30 (Silva et al., 2013). For Pacific herring, a high value of 0.38 was reported for 6 year old female herring from southern British Columbia (Tanasichuk, 2000), while a much lower GSI of 0.18 was recorded for a high latitude population (70°N) in the Beaufort Sea (Tanasichuk et al., 1993). Thus, the GSI values for LRH and BFH are intermediate in the lower range of the values for C. pallasii and C. harengus, and suggest a moderate gonad production compared to many other herring populations. 4.5. Natural mortality rate The natural mortality rate of ca. 0.7 year−1 for LRH and BFH is much higher than the value of 0.15 year−1 reported for NSSH (Toresen and Østvedt, 2000), and this difference largely corroborates the patterns in growth, and age and length at maturity. The estimates of mortality

Please cite this article as: Mikkelsen, N., et al., Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?, J. Mar. Syst. (2016), http://dx.doi.org/10.1016/j.jmarsys.2016.12.004

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rates for LRH and BFH were based on relatively few year classes and varying year-class strength may have affected the precision of estimates to some degree. However, the mortality estimates for BFH from three years of sampling were similar, indicating moderate variability in M. Since there is no commercial fishery on the LRH and BFH populations, the M values equal the Z values. The Lusterfjord herring had an M value similar to the LRH and BFH estimates, suggesting that some Atlantic fjord herring populations may also have higher M than oceanic populations. Despite the fact that the M values for LRH and BFH are among the highest values reported for adult herring, they are in the lower range of M values for other fish species of similar body size in fjord environments in northern Norway. The M value for shorthorn sculpin (Myoxocephalus scorpius) was estimated as 0.94 year−1 for females and 1.20 year−1 for males (Luksenburg and Pedersen, 2002). Similarly, M values in the range of 0.6–1.8 year−1 were estimated for 1 and 2 year old Atlantic cod (Gadus morhua) (Larsen and Pedersen, 2002; Pedersen and Pope, 2003). The value of M for several populations of adult herring was higher in Pacific herring compared to Atlantic herring. Estimates of M tended to decrease with increasing L∞. This is consistent with McGurk (1993) results, where north-eastern Pacific herring populations had higher M at a given size than Atlantic herring. The relatively high M values for LRH and BFH cluster with the other Pacific populations and the Lusterfjord herring. In British Columbia, Tanasichuk (2000) found that M for mature herring increased with age and suggested that the major cause of natural mortality in old herring is senescence. The natural mortality rate of a herring population in Canada fluctuated between ca. 0.4 to 1.0 year−1 over a 60 year period (Schweigert et al., 2010). Thus, natural mortality rate may be more dynamic and is probably estimated with larger uncertainty than the growth and reproduction parameters. Despite this, we believe that the values presented here show the broad picture, and that the M values for LRH and BFH resemble those of other Pacific herring populations, being higher than most Atlantic populations at similar body size. 4.6. Association between life history parameters Inter-population variability in the natural mortality rate and L∞ in herring confirm with the pattern expected from life history theory, i.e. high M associated with low L∞. The values for age and length at maturity for LRH, BFH, and NSSH corroborate the trend in M and L∞. Despite their high M values, LRH and BFH had low relative fecundity and intermediate GSI values compared to most other herring populations. Therefore, contrasting with other local Atlantic herring populations along the Norwegian coast that have higher relative fecundity and also considerably higher GSI than NSSH in the pre-spawning stage, indicating a higher reproductive effort in these local herring stocks (Silva et al., 2013). Somatic growth is very low after maturation in BFH and especially in LRH, implying that the surplus production after sexual maturity in most BFH and nearly all LRH is directed towards production of gonads. Genetic studies indicate that the populations of C. pallasii in the Atlantic have evolved from invaders to the Atlantic from the Asian and Beringian lineage of C. pallasii (Laakkonen et al., 2013). The Asian and Beringian lineage differ genetically from the north-eastern Pacific herring populations (Grant and Utter, 1984). The fact that the local LRH and BFH have evolved and adapted to the local environment, being sympatric and even hybridizing with Atlantic herring, suggests that they possessed some traits that were advantageous in their environment. When occurring in sympatry in Balsfjord, BFH has a deeper vertical distribution than NSSH (Jørstad and Pedersen, 1986), while LRH does not school as is common in other herring populations (Hognestad, 1994). This indicates an intraspecific population schooling behaviour and that these local populations have specific behavioural adaptations. Predatory fish like Atlantic cod (Gadus morhua) and saithe (Pollachius virens) are abundant in both Balsfjord and Lake Rossfjord (Hognestad, 1994). The coastal environment, with a suite of coastal

predators feeding on herring such as demersal fish, seabirds and mammals (Pedersen et al., 2016), may have higher mortality risk than the more oceanic environment, and thus the life histories of Pacific herring populations may have been adapted to a higher natural mortality rate than the oceanic Atlantic herring populations. The LRH and BFH populations are among the herring populations with the northernmost spawning areas in the world and they may experience a shorter feeding season and lower temperatures than most other herring populations. Trade-offs between growth, reproduction, and mortality risk have been shown to change with latitude in other fish species towards the priority of high growth rate potential in northern populations (Billerbeck et al., 2000). The herring in the Beaufort Sea has a higher L∞ and lower values for M and GSI than stocks further south in British Columbia. The Beaufort stock lives at even colder temperatures than the BFH (Tanasichuk et al., 1993), but has a high natural mortality rate similar to BFH. In contrast to NSSH and most Atlantic herring, BFH and LRH as well as other C. pallasii populations deposit their eggs on vegetation in very shallow water, which may be advantageous in fjordic environments with low wave exposure and few hard substrates. Baltic herring (C. harengus) also deposits eggs on the vegetation (Hay et al., 2001) and lives in a similar brackish water environment as Lake Rossfjord herring. However, Baltic herring does not seem to be genetically close to LRH and BFH (Jørstad et al., 1991). Compared to the nearest oceanic herring stock, NSSH, the environments for BFH and LRH may be considered as extreme with regard to temperature (BFH) and oxygen level (LRH), but environments in these areas have been sufficiently stable over time to permit population adaptations. 4.7. Conclusions It is concluded that the local herring populations in Lake Rossfjord and Balsfjord show similar life history characteristics (e.g., low somatic growth after maturity, high natural mortality rate) to many Pacific herring populations, but differ from the geographically close living Norwegian spring-spawning herring and also most other Atlantic herring stocks. Acknowledgements We thank Frode Gerhardsen for assistance with sampling and Jostein Røttingen, Bjørn Vidar Svendsen, and Jan de Lange for assistance with analysis of herring. The third author thanks the National Council of Scientific and Technological Development (CNPq – Brazil Grant no. 240467/2012-4) for the PhD funding. We thank Karen Rouen for linguistic assistance. References Aasen, O., 1952. The Lusterfjord herring and its environment. Fiskerdirektoratets Skrifter Serie Havundersøkelser vol. 10, pp. 1–64. Alderdice, D.F., Hourston, A.S., 1985. Factors influencing development and survival of Pacific herring (Clupea harengus pallasi) eggs and larvae to beginning of exogenous feeding. Can. J. Fish. Aquat. Sci. 42, 56–68. Beverton, R.J.H., 1963. Maturation, growth and mortality of clupeid and engraulid stocks in relation to fishing. J. Cons. Int. Explor. Sea 154, 44–67. Beverton, R.J.H., Holt, S.J., 1959. A review of the lifespans and mortality rates of fish in nature, and their relation to growth and other physiological characteristics. CIBA Foundation, Colloquium on Ageing vol. 5, pp. 147–177. Beverton, R.J.H., Hylen, A., Østvedt, O.-J., Alvsvaag, J., Iles, T.C., 2004. Growth, maturation, and longevity of maturation cohorts of Norwegian spring-spawning herring. ICES J. Mar. Sci. 61, 165–175. Billerbeck, J.M., Schultz, E.T., Conover, D.O., 2000. Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside. Oecologia 122, 210–219. Chapman, D.G., Robson, D.S., 1960. The analysis of a catch curve. Biometrics 16, 354–368. Cushing, D.H., Bridger, J.P., 1966. The stock of herring in the North Sea and changes due to fishing. Fishery Investigations, London, Series II vol. 25, pp. 1–123. Denney, N.H., Jennings, S., Reynolds, J.D., 2002. Life–history correlates of maximum population growth rates in marine fishes. Proc. R. Soc. Lond. B Biol. Sci. 269 (1506), 2229–2237.

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Please cite this article as: Mikkelsen, N., et al., Are life histories of Norwegian fjord herring populations of Pacific ancestry similar to those of Atlantic or Pacific herring?, J. Mar. Syst. (2016), http://dx.doi.org/10.1016/j.jmarsys.2016.12.004