Reduced size composition and fecundity related to fishery and invasion history in the introduced red king crab (Paralithodes camtschaticus) in Norwegian waters

Fisheries Research 121-122 (2012) 73–80

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Reduced size composition and fecundity related to fishery and invasion history in the introduced red king crab (Paralithodes camtschaticus) in Norwegian waters Ann Merete Hjelset a,b,∗ , Einar M. Nilssen b,a , Jan H. Sundet a a b

Institute of Marine Research, NO-9294 Tromsø, Norway Faculty of Biosciences, Fisheries and Economics, University of Tromsø, NO-9294 Tromsø, Norway

a r t i c l e

i n f o

Article history: Received 11 May 2011 Received in revised form 25 November 2011 Accepted 8 January 2012 Keywords: Fecundity Inter-annual variability Reproduction Spatial variability Size structure

a b s t r a c t The introduced red king crab (Paralithodes camtschaticus) in the Barents Sea is abundant in the coastal waters of eastern Finnmark and supports a valuable fishery. In this paper we look at the development in size span among ovigerous females in the period between 1995 and 2010. We identify variations in individual fecundity in three fjords in Finnmark from 2000 to 2007. All the analyses were performed using regression and general linear models. We found that the size range decreased during this period. A decline in individual fecundity was observed. Individual egg weight (IEW) varied among fjords and years, and displayed a tendency to decline during the period of investigation, but the IEW was not affected by crab size. Increased fishing pressure on large males may have caused both a decline in size range of ovigerous females as well as a decline in fecundity. Reduced IEW however is likely to be due to limited available food. We attempted to compare individual fecundity in the invasive crab with fecundity results from populations in native areas. This comparison was inconclusive, due to differences in sampling season, size range and the methods employed. © 2012 Elsevier B.V. All rights reserved.

1. Introduction The red king crab (Paralithodes camtschaticus), which was deliberately introduced to the Barents Sea by Russian scientists in the 1960s, has increased in abundance over the past 40 years, and the population is now regarded as self-sustaining (Kuzmin et al., 1996). Its success may be generally due to high ecosystem productivity in the new region and to its escape from co-evolving predators or parasites in its native areas. Life history traits such as size at maturity, number and size of offspring, and reproductive lifespan affect the population growth rate of invasive species (Tibbets et al., 2010). During the initial period of establishment of the population, fishing pressure was low, due to strict regulations. A male-only fishery for the crab has been carried out in Norwegian waters since 1994, and this species is now a valuable fishery resource (Falk-Petersen et al., 2011). Until recently a “3S” (sex, size and season) (Otto, 1986; Kruse, 1993) regime was applied as a management tool; only males with a carapace length (CL) greater than 137 mm could be legally harvested during the autumn fishing season. All females and undersized males were to be returned to the water (Otto, 1986; Dew, 2008). In 2008, the Norwegian authorities (Ministry of

∗ Corresponding author at: Institute of Marine Research, P.O. Box 6404, NO-9294 Tromsø, Norway. Tel.: +47 77 60 9745. E-mail address: [email protected] (A.M. Hjelset). 0165-7836/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2012.01.010

Fisheries and Coastal Affairs) permitted catch of females larger than 137 mm CL. The reproductive strategies of a species play a major role in population dynamics (Ramirez-Llodra, 2002). Fecundity is defined as the number of eggs produced by a female, and is directly related to life-history traits such as size and age at maturity, life-span and egg size (Stearns, 1992; Ramirez-Llodra, 2002). In the red king crab population in Norwegian waters, female size at maturity, that is the size at which 50% of the females carry eggs, is 109–111 mm CL, depending on sampling area, and this is larger than in other populations in their native areas (Hjelset et al., 2009). The red king crab reproduces annually and incubates the eggs for 10–12 months (Stevens and Swiney, 2007a). In crustaceans, egg size is directly related to the maternal investment in reproduction, and is the result of a tradeoff between the size of the egg and the number of eggs produced (Ramirez-Llodra, 2002). The quality and quantity of food available to a female crab may also influence the size of her eggs (Sastry, 1983; Ramirez-Llodra, 2002). The many variables required to adequately describe the fecundity of a species or population can make comparisons across stocks somewhat complex (Sastry, 1983). The fecundity of a population may decline because of reduced abundance of spawners but may also be due to a skewed sex ratio (Murua et al., 2003). The fishery for many valuable crustaceans alters the population demographic structure, because only large males are harvested (Wahle, 2003). The reproductive success of the red king crab depends on males and females being on the mat-

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Fig. 1. Map of our study area in county of Finnmark, situated in northern Norway, shaded area represent current distribution of red king crab (Paralithodes camtschaticus) in Norwegian waters.

ing grounds at the same time (Wallace et al., 1949; Powell et al., 1974). Male size is an important factor in mating efficiency, due to the handling and guarding behaviour exhibited by male crabs during mating (Paul and Paul, 1997). Large females, which produce the highest number of eggs, are most successfully fertilised by large males (Schmidt and Pengilly, 1990; Kruse, 1993). Females mating with small males with less sperm capacity have lower fertilisation success than females that mate with larger males (Paul and Paul, 1990a,b, 1997; Sato and Goshima, 2006). Other studies report that large females are sometimes observed without broods or with reduced brood sizes (Powell et al., 1973), which may be due to unsuccessful mating with smaller males. Adult males that moult before a mating season do not participate in that mating season (Rodin, 1990). This may further reduce the number of large males present on spawning grounds (Dew and McConnaughey, 2005). Since the male-only harvest may skew the sex ratio in the population and thereby reduce the reproductive potential of females (McMullen, 1969), it is important to monitor fecundity at population level. Stock–recruitment relationships are poorly understood for most commercially important crab and lobster species (Wahle, 2003), but it is well known that egg production plays a critical role in crustacean population dynamics and recruitment (Botsford, 1991). A general shortcoming of previous studies is that longterm data on fecundity are scarce. Information regarding how fecundity in an introduced species evolves after settling and spreading in a new geographic area has not been previously presented. In this study we investigated individual fecundity in red king crab in three large Norwegian fjords during an eight-year period, beginning 34 years after the species was first recorded in the region (Orlov and Ivanov, 1978). We studied spatial and temporal variations in the size structure of ovigerous females, and individual

fecundity, including egg size, in the Norwegian red king crab stock, and compared our findings on fecundity with studies performed in the species’ native areas. 2. Materials and methods 2.1. Data collection and sampling area A total of 12,117 ovigerous female king crabs with carapace lengths (CL) ranging from 74 mm to 192 mm were caught in the course of autumn scientific cruises in northern Norway between 1995 and 2010. The crabs were collected using baited traps and a beam trawl, at depths that ranged from 25 to 400 m. Egg samples from 905 female crabs were collected from three large inlet fjords; Varangerfjorden (first invaded), Tanafjorden and Laksefjorden (last invaded), from 2000 until 2007. During the sampling period, the distribution area of the species has increased as the crab has spread westward along the coast of Finnmark in northern Norway (Fig. 1). The CL of all the females caught was measured to the nearest 1.0 mm. Clutches were collected from between one and ten individuals in each 10 mm size group in order to ensure a representative selection from the available range of sizes (93–186 mm CL) in each year and fjord. Sampling was restricted to females with full clutches, and we avoided sampling females with lost or reduced legs, or showing signs of stress or egg loss. All samples were collected from females that had spawned during the previous reproductive season, since the red king crab reproductive cycle (hatching, moulting, extrusion and fertilization) is synchronous and lasts for about 12 months (Marukawa, 1933; Stevens and Swiney, 2007a). No estimates of clutch fullness were made, as we assumed that the crabs would not suffered any significant reduction in egg masses due to factors related to the mating event. In order to

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separate the egg clutch from the abdomen, each of the five pleopods at the base of the inner ramus was removed and kept frozen in zip-lock bags for analysis with eggs still attached.

Tegg versus CL regressions were fitted using the linearized form of power curve expression

2.2. Laboratory procedures

and the results from each fjord and year are presented in Table 1. The results of the Tegg –CL relationship are presented for Varangerfjorden, Tanafjorden and Laksefjorden, using the back-transformed Eq. (2) for the period 2004–2007.

Egg masses were thawed for 12 h at temperatures around 2–4 ◦ C before fecundity estimates were made. Eggs were then gently stripped from each pleopod using forceps and pooled in a pre-weighed drying pan. Three subsamples were taken from the smallest pleopod to ensure comparable stages of development among samples and counted under a dissecting microscope. Clutches (including subsamples) were dried to constant weight (60 ◦ C for >24 h). All weighing was done on microbalances with an accuracy of 0.1 mg for subsamples and 0.01 g for the complete egg masses. Subsample weights and counts were included in the total sums of weights and counts. During the counting of the subsamples, possible unfertilised eggs and non-viable eggs were identified on the basis of their difference in appearance from the rest of the egg mass. 2.3. Size composition and standard sized female In order to present an overview of several years of data on ovigerous female size composition, the 5th and 95th percentile and median values of CLs were calculated for each year and fjord for the sampling period 1995–2010. To visualise the development in fecundity, a standard-sized ovigerous female was defined by taking the average CL of all ovigerous females (n = 12,117; CL = 125 mm) sampled from 1995 to 2010. The standard female was also used in comparisons with fecundity from native areas. 2.4. Fecundity (Tegg ) and individual egg weight (IEW) Fecundity was defined as the total number of eggs (Tegg ) attached to the pleopod setae at the time of sampling. Individual dry egg weight (IEW) was estimated as the sum of dry weights from three subsamples divided by the number of eggs in the subsamples. Dry egg mass weight (Weggmass ) includes the entire egg mass after drying (including weights of subsamples). An estimate of Tegg , was then given by Weggmass /IEW. 2.5. Statistical analysis The data were divided into two subsets for the analysis of Tegg and IEW. One set comprised data from Varangerfjorden and Tanafjorden from 2000 to 2007, and one from Varangerfjorden, Tanafjorden and Laksefjorden, 2004–2007. All the statistical analyses, tests and graphical presentations were performed in R software (R Development Core Team, 2009). Outliers were classified as such on the basis of visual inspection using graphical tools available in R; this procedure was performed for each analysis. Statistical significance was set at 0.05. 2.5.1. Models of fecundity In order to meet the assumptions of normality and homogeneity of variance in linear regression models, we performed log10 transformation of both the response (Tegg ) and explanatory variables (CL). The log transformation stabilized the variance and linearized the relationship between the explanatory and response variables (Somers, 1991). An analysis of covariance (ANCOVA) was performed in a Tegg versus CL regression in order to test whether there were significant differences between years, within fjords or the interactions between these.

log10 (Tegg ) = log10 (a) + b × log10 (CL)

Tegg = aCLb

(1)

(2)

In both Eqs. (1) and (2), a and b are the regression constant and regression coefficient, respectively. In order to visualise the development in fecundity at individual level, Tegg (±1SE) was estimated for a standardized female (CL = 125 mm) for each year and fjord from Eq. (1). 2.5.2. Models of IEW Analysis of covariance (ANCOVA) was used to test for temporal and spatial differences in IEW. The analysis was run for the two subsets, Varangerfjorden and Tanafjorden 2000–2007, and Varangerfjorden, Tanafjorden and Laksefjorden 2004–2007. Mean values of IEW (±1SE) relative to year and fjord are shown for the two data subsets. 3. Results 3.1. Size composition of ovigerous females 1995–2010 Common to all areas is that the size range of ovigerous females narrowed from 1995 to 2010 (Fig. 2). In Varangerfjorden, the value of the 95th percentile shows that there was higher proportion of large females at the beginning of the period, and that around 1999–2001 they were at their maximum size. Since then the range has become narrower. The range of sizes narrowed in Tanafjorden, with a sudden decrease of the 95th percentile from 173 mm CL to 140 mm in 1999–2000, and continued to decrease until 2010. The size range of all ovigerous females in Laksefjorden did not change significantly in the course of the four-year sampling period, but since 2007, the range of sizes has become narrower there too. The 5th percentile and the median show no particular trend in the three fjords between 1995 and 2010. 3.2. Fecundity Tegg The total number of eggs per crab ranged from 23,000 to 560,000 in females from Varangerfjorden, with a mean (±SD) of 176,000 ± 82,000 eggs, and a mean (±SD) CL of 129 ± 19 mm (2000–2007). In Tanafjorden, the total number of eggs ranged from 18,000 to 474,000, with a mean of 192,000 ± 93,000 for a mean female of 130 ± 20 mm CL (2000–2007). In the westernmost fjord, Laksefjorden, the number of eggs ranged from 55,000 to 477,000 with a mean of 219,000 ± 84,000. The mean CL of females in Laksefjorden was 131 ± 16 mm CL (2004–2007). The number of eggs per ovigerous female significantly increased with CL in each fjord and year examined (p < 0.001). No differences in regression coefficients (slope) were detected between fjords or year, indicating that the basis for comparisons of elevation (fecundity = height of regression line) in the ANCOVA was fulfilled. 3.2.1. Temporal and spatial variation in subsets 2000–2007 and 2004–2007 ANCOVA identified size-dependent variation in fecundity between Varangerfjorden and Tanafjorden in the period 2000–2007 (F1,717 = 9.3, p = 0.002), with Tanafjorden having the highest fecundity at comparable sizes. Among years we found

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Table 1 Overview of sampled ovigerous red king crab (Paralithodes camtschaticus) females from Varangerfjorden, Tanafjorden and Laksefjorden in 2000–2007 used in fecundity analysis. Calculated model for single years and for the pooled period 2004–2007. Log(a) = regression constant, b = regression coefficient, SEb = standard error of b, r2 = adjusted coefficient of determination, F = Fisher value. Fecundity data Year

Model parameters Mth

Varangerfjorden 2000 Aug 2001 Aug 2002 Aug 2003 Sep 2004 Aug 2005 Aug 2006 Aug 2007 Aug 04–07 Fig. 3 Tanafjorden 2000 Aug 2001 Sep 2002 Sep 2003 Aug 2004 Aug 2005 Sep 2006 Aug/Sep 2007 Aug 04–07 Fig. 3 Laksefjorden 2004 Sep 2005 Sep 2006 Sep 2007 Sep 04–07 Fig. 3

Mean CL

CL range

N

Log(a)

b

SE

F value

r2

p value

133 141 126 131 128 126 126 121 125

99–173 98–183 103–155 104–170 99–161 100–150 93–155 98–144 93–161

33 46 47 42 45 48 52 43 192

−0.2152 −0.5044 −0.0792 −0.3437 0.0036 −0.5881 −1.0505 −0.3996 −0.8390

2.5958 2.7241 2.5227 2.6437 2.4661 2.7475 2.9566 2.6516 2.8593

0.2163 0.1523 0.2166 0.2025 0.2582 0.3145 0.3427 0.2892 0.1627

144.0 319.9 135.7 170.4 91.2 76.3 74.5 84.1 309.0

0.82 0.88 0.75 0.81 0.67 0.62 0.59 0.66 0.62

<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001

143 143 140 129 127 126 122 121 124

106–178 97–186 109–184 101–162 102–166 96–156 96–153 105–144 96–166

40 45 32 42 44 51 52 36 187

−0.5713 −0.1349 0.7422 −0.5052 −0.5746 −0.6373 −0.2390 −1.5671 −0.9414

2.7740 2.5617 2.1601 2.7431 2.7589 2.7789 2.5768 3.1933 2.9149

0.1259 0.1205 0.1830 0.1875 0.1599 0.1993 0.1884 0.5601 0.1336

485.1 452.2 139.4 214.1 297.7 194.4 187.2 32.5 475.9

0.93 0.91 0.82 0.84 0.87 0.80 0.79 0.48 0.72

<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001

129 133 135 128 132

105–158 108–166 101–170 99–170 101–170

24 42 54 56 179

−1.5179 −0.1010 −0.7656 −1.5774 −0.8895

3.2373 2.5669 2.8695 3.2419 2.9279

0.2285 0.2010 0.2272 0.1972 0.1218

200.7 163.0 159.5 270.4 577.8

0.90 0.80 0.75 0.83 0.76

<0.001 <0.001 <0.001 <0.001 <0.001

a negative trend in fecundity in Varangerfjorden (F7,358 = 2.9, p = 0.005) and in Tanafjorden (F7,341 = 9.9, p < 0.001). Fecundity models for each year and fjord are presented in Table 1. Analysis showed that size-dependent fecundity differed significantly among the three fjords studied in the period 2004–2007

(F2,562 = 36.7, p < 0.001), Laksefjorden having the highest fecundity and lowest in Varangerfjorden. There were no annual differences in Varangerfjorden during the 2004–2007 period (F3,186 = 1.3, p = 0.27), while weak negative trends across the years were observed in Tanafjorden (F3,181 = 5.1, p = 0.002) and Laksefjorden

Fig. 2. Size distribution of ovigerous female red king crab (Paralithodes camtschaticus) presented by percentile (5 and 95%) and median values for carapace length (CL) from 1995 to 2010, in Varangerfjorden, Tanafjorden and Laksefjorden. Grey boxes show the sampling period for fecundity data.

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Fig. 3. Power models of size fecundity relationship for red king crab (Paralithodes camtschaticus) from Varangerfjorden, Tanafjorden and Laksefjorden. Pooled data from years 2004 to 2007. Fig. 5. Mean individual egg weight (IEW) with standard error bars from Varangerfjorden, Tanafjorden and Laksefjorden in years 2000–2007.

(F3,175 = 3.9, p = 0.010). Pooled data sets for 2004–2007 for each fjord are presented in Fig. 3 and regression models are shown in Table 1. 3.2.2. Fecundity (Tegg ) in a standard sized female The total number of eggs carried by the standard sized female fell in all the fjords between 2000 and 2007 (Fig. 4). The largest decrease was observed in Tanafjorden, with a fall of about 50,000 eggs, while the reductions in Varangerfjorden and Laksefjorden were around half as great (about 30,000 and 25,000 eggs respectively). 3.3. Temporal and spatial variation in individual egg weight (IEW) Differences in IEW were found between Varangerfjorden and Tanafjorden during the 2000–2007 period (F1,697 = 64.2, p < 0.001), with Tanafjorden having higher IEW. Within each fjord, IEW was not influenced by the female size in either Varangerfjorden (F1,356 = 1.0, p = 0.3) or Tanafjorden (F1,340 = 0.6, p < 0.4). There were annual variations in egg weight in both Varangerfjorden (F7,356 = 8.2, p < 0.001) and Tanafjorden (F7,340 = 11.5, p < 0.001). Fig. 5 shows that mean egg weight fell during the first part of the period in both Varangerfjorden and Tanafjorden, with the lowest

levels in 2004 and 2005 for Varangerfjorden, before rising again, even though it never reached the same level as in 2000. Analysis of IEW for 2004–2007 showed that a mean egg weight each year for all crab sizes (CL) (F1,547 = 1.3, p = 0.2) within each fjords can be obtained. However, there were differences in mean egg weight among fjords (F2,547 = 25.5, p < 0.001) and among years (F3,547 = 4.4, p = 0.005). The mean egg weight estimates for Laksefjorden were higher than those for the other two fjords, and the mean IEW value rose during the study period (Fig. 5). ANCOVA of the two data subsets (2000–2007 and 2004–2007) revealed no variation in IEW related to crab size (CL) (Table 2). A common mean egg weight could therefore be established for each year for all crab sizes within each fjord. 3.4. Other results Dead eggs (white, non-fertilised and non-viable eggs) were observed in 220 samples, and the number of dead eggs ranged from 0.6 to 11% of the total number of eggs. We concluded that our population of red king crab did not produce a large proportion of dead or unfertilised eggs. Small amphipods and bivalves were also observed in a few clutches, but these were not systematically recorded. 4. Discussion In the course of the 34 years that have passed since king crabs were first recorded in Varangerfjorden (Orlov and Ivanov, 1978) the Table 2 ANCOVA of individual egg weight (IEW) versus listed parameters from Varangerfjorden and Tanafjorden in the period 2000–2007, and for the period 2004–2007 from Varangerfjorden, Tanafjorden and Laksefjorden.

Fig. 4. Estimated number of eggs (from regression models) for a standard sized female (CL = 125 mm) from Varangerfjorden, Tanafjorden and Laksefjorden, vertical bars are standard error bars.

Period

Parameters

Model parameters df

F value

p value

2000–2007

Year Fjord Year × Fjord CL Residuals

7 1 7 1 697

16.0 64.2 3.4 0.3

<0.001 <0.001 0.002 0.5

2004–2007

Year Fjord Year × Fjord CL Residuals

3 2 6 1 547

4.4 25.5 3.2 1.3

0.005 <0.001 0.004 0.2

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stock has grown in numbers and range (Fig. 1), confirming that the king crab has become a successful invasive species in its new environment. The size composition of ovigerous females in the fjords has changed during the sampling period (Fig. 2). The narrowing of the range of sizes observed in all three fjords may be due to increasing catches of large males, and the differences among fjords are due to differences in the catch history of males. Female survival may be influenced by the abundance of large males, since females are dependent on males during their moulting period. Being inactive and vulnerable immediately after moulting, they may be at greater risk of predation or cannibalism, due to a lack of large males to protect them (Paul and Paul, 1990b; Kruse, 1993; Kruse et al., 2000). The Pacific cod (Gadus macrocephalus) is an important predator on soft-shelled females in the Bering Sea (Blau, 1986; Otto, 1986). Handling of females caught during fishing may also increase mortality caused by injuries (Kruse, 1993). In summary, a combination of factors may have influenced the size span of ovigerous females and thereby shortened their reproductive life-span. A moulting increment of 5 mm for ovigerous females (Nilssen and Sundet, 2006) means that the reduced size range seen in this study is equivalent to a conservative estimate of four to six years of mating opportunities, which is lost for many females during the last part of the period studied. In 2002, the harvest rate of large males in the Norwegian fishery significantly rose. Any fishery based on a minimum legal size may change the stock structure in the course of time (Ennis et al., 1988; Sato et al., 2005; Enberg et al., 2009). Because there was a minimum legal size on large males only, the harvest targeting for the largest, and thus the largest mature, males (Enberg et al., 2010). Several studies have revealed that the number of matings by one male influence on the fertilization success in females (Powell and Nickerson, 1965; Paul and Paul, 1990a,b, 1997). The significance of such behaviour in the wild has not been determined, but Paul and Paul (1997) assumed that most large males can fertilize three females successfully in nature. No evidence of reduced fertilization was seen in red king crab in our study area, but non-ovigerous adult females and/or females with only partly full clutches have been observed in other areas, and this has been explained by the lack of large males due to harvesting (Powell et al., 1974; Johnson et al., 2000). A continuous high fishery pressure for large males in our waters may have similar consequences in the future. A positive correlation between size and fecundity has been demonstrated by many studies on decapods (Somers, 1991), and we found a significant positive relationship between the number of eggs carried and the size of the female. However, the level of fecundity may vary between areas and years in female crabs of the same size. A female red king crab caught in Laksefjorden carried more eggs than females of the same size from Varangerfjorden and Tanafjorden, and this difference is characteristic for the whole sampling period and all sizes (Fig. 3). The estimated fecundity of a standard-sized female in our population was different between years and fjords, and fecundity diminished during the period of study (Fig. 4). The number of eggs is morphologically limited, since the hard exoskeleton limits the physical space available on the abdomen for carrying eggs (Ramirez-Llodra, 2002). In many species, there is a trade-off between growing large before first maturity and producing many offspring through a limited number of years, while others mature at smaller size, resulting in many spawning events, with fewer eggs in each time period (Ramirez-Llodra, 2002). Hjelset et al. (2009) showed that size at 50% maturity (OL50 ) was the same in Varangerfjorden and Tanafjorden, but significantly higher in Laksefjorden. The difference in fecundity between the fjords can thus be related to the dissimilarity in size at first reproduction. Larger body size in females in Laksefjorden at first reproduction results in higher initial fecundity.

Differences in fecundity between fjords and years may be due to differences in year-class strengths. Primiparous females are less fecund than multiparous ones (Dew and McConnaughey, 2005; Swiney et al., 2010). In live catches, it is impossible to distinguish between primiparous and multiparous females, and most studies in which it was possible to distinguish the two forms were performed in controlled laboratory environments (Stevens and Swiney, 2007a,b). Abundant year classes of primiparous females will reduce population fecundity, since they are less fecund than multiparous individuals of the same size. We can reasonably assume that red king crabs utilised unexploited food resources as they spread along the Norwegian coast and also experienced little competition for food at the beginning. Crab foraging affected benthic communities after the population was well established (see Falk-Petersen et al., 2011, for a review). Oug et al. (2010) documented changes in the soft bottom fauna in Varangerfjorden after the introduction of red king crabs. A change in the availability and/or quality of food during the sampling period may therefore have affected the number of eggs carried and thus explain the decrease in fecundity. The amount of energy invested in an egg determines its size, and larger eggs produce larger offspring, which will be more competitive and better adapted for feeding (Sastry, 1983). We have shown that the mean egg weight decreased in the course of the sampling period in Varangerfjorden and Tanafjorden (Fig. 5). One explanation for this might be that the females have less energy to invest in the production of eggs, since the quality and quantity of their food may be reduced during the sampling period (RamirezLlodra, 2002). Fecundity is one of the life-history parameters that respond most rapidly to changes in the environment (RamirezLlodra, 2002), and our results confirm this, with changing fecundity and IEW among fjords and years. Ovigerous females continually attempt to optimise the temperature conditions for their eggs during the incubation period (Stone et al., 1992). Another factor that determines egg size may therefore be sea temperature. However, Eilertsen and Skarðhamar (2006) showed that bottom temperatures vary less than surface temperature in the course of the year in a fjord in Finnmark, and in the depth range used by the crab, the seasonal variation is less than 3 ◦ C. There is therefore no reason to believe that temperature had any effect on either fecundity or egg weight in our study. Our findings also showed that mean egg weight was independent of female red king crab size, in agreement with findings made by Johnson et al. (2000). Fecundity was estimated using dry weights of egg and egg masses, as this provides a more accurate measure of the content of oogenic material in the egg, and favours comparison between stocks, areas and seasons (Ramirez-Llodra, 2002). Although our sampling was carried out at the same time every year, the dry weight was used to allow comparisons to be made with other red king crab stocks. Using wet weights may jeopardise comparison between different areas due to seasonal changes in the water content of the egg clutch. Counting eggs is time-consuming, costly and tedious, but does give the best estimate of fecundity, and is the most frequently utilised monitoring method (Ramirez-Llodra, 2002; Tallack, 2007). Egg loss during sampling or counting may occur, but in this study it did not cause serious problems for the size-specific fecundity estimates. Dead eggs were identified as being white or yellow coloured among live eggs, which are purple, purple-brown or brown (Donaldson and Byersdorfer, 2005). The female crabs that we studied carried only small numbers of dead eggs, but this could change in the future, and should therefore be monitored. We did not visually check clutch fullness during sampling (Donaldson and Byersdorfer, 2005), which is a standard procedure during stock assessment surveys in Alaska (Swiney et al., 2010). Reduced clutch sizes have been reported in large females (Powell et al., 1973) and

Hjelset et al. 178d

Hjelset et al. 148d

143d

Paul and Paul (1996) Rodin (1990) McMullen (1969) Hjelset et al. 136d

95–438d 101–170

e

c

d

From Table 8, adjusted mean of eggs in Otto et al. (1990). Increase in mean number of egg from a north to south. Read from graph. Estimated from model. Egg clutch volume in milliliter. a

Laksefjorden, Norway

Tanafjorden, Norway

5. Conclusions

b

2.92 179 Log10 transformed

−0.89

0.76

69–339d 96–166 2.91 187 Log10 transformed

−0.94

0.72

44–210e 62–296d 103–168 93–161 0.62 2.86 192

79

were explained as reproductive senility or senescence, which is common and natural among large females (Somers, 1991). Some of our outliers were probably a result of reduced clutch fullness, but this is not regarded as a major problem in our stock. Swiney et al. (2010) showed that onboard visual inspection of clutch fullness is not a reliable estimator of fecundity. Another component which may reduce fecundity is related to brood mortality due to symbionts (Kuris, 1991), but our egg clutches did not appear to have problems with this. A study carried out in Varangerfjorden in 1999 showed that red king crab has various symbionts associated with their eggs, but these appeared to be harmless to the clutch (Haugen, 1999). Studies of red king crab fecundity and direct comparisons of fecundity data are difficult due to differences in sampling season, limited time series and different size ranges. Moreover, different models have been employed in different studies. Swiney et al. (2010) present a model that was used only on multiparous females, and therefore limited the generalisability of the data analysed. In the data-set of Otto et al. (1990), the maximum female size was 130 mm CL. Both studies are based on data collected in June and July, and the standardized female (CL = 125 mm) was more fecund than ours. In a laboratory study carried out in the spring by Paul and Paul (1996), the estimated number of eggs is lower, although the range of sizes of the crabs is similar to ours. Table 3 provides an overview of the differences in other studies done on fecundity. In crustacean fisheries females can easily be distinguished from males and can therefore be returned to the sea (Donaldson and Donaldson, 1992). This conservative approach is used in most crustacean fishery management in order to protect the production of offspring (Miller, 1976; Botsford, 1991). The importance of egg production for recruitment is associated with much uncertainty, because environmental variability appears to have a major effect on this relationship (Botsford, 1991). After hatching, larval survival is mainly determined by prey availability and the presence of predators, both of which factors are related to physical and biological processes (Jennings et al., 2001). The benefit of protecting ovigerous females is that the production of eggs and larvae is maintained. Size-specific fecundity decreased in the course of the study period for all sizes and fjords. The change in the stock structure and a fishery that targets large males and females, seem to have had negative impact on the stock. However, females appear to be capable of reproducing as much as five times before they reach the legal capture size (Nilssen and Sundet, 2006). In recent years, the size distribution of female crabs shows that large females have almost disappeared after two years of female catch quotas.

179 60, 78, 118, 150, 220b 20–348 110–161 0.36 115

Linear regression – Linear regression Log10 transformed Lab experiment, Alaska, USA West Kamchatka Kodiak Island, Alaska, USA Varangerfjorden, Norway

Norton Sound, Alaska, USA

– 1968, April/May 2004–2007, August/September 2004–2007, August/September 2004–2007, August/September

106 Loge transformed

−0.84

3.53 −4.59

3.7

3.54 −4.84

−326.6

Otto et al. (1990) 256d 73–85 17–157 65–118

∼205c ∼205c ∼150c 210d 210 203 161–213 90–107a 101–287 – – 26–169 105–145 105–145 105–150 79–130 r

0.51 0.75 0.51 0.84 87 97 25 110

n

2007, June/July 2008, June/July 2008, June/July 1982, 1983, 1985, pooled data 1982, 1985, pooled data Bristol Bay, Alaska, USA Bristol Bay, Alaska, USA Barlow Cove, southeastern Alaska Bristol Bay, Alaska, USA

Linear regression Linear regression Linear regression Loge transformed

a

b

0.78

Swiney et al. (2010) Swiney et al. (2010) Swiney et al. (2010) Otto et al. (1990)

Source No eggs in female = 125 mm CL Mean number of eggs × 1000 Egg range (×1000) CL range (mm) 2

Model parameters Model Year/mth Area

Table 3 Overview of selected fecundity studies on the red king crab (Paralithodes camtschaticus) and number of eggs in a female of CL = 125 mm. a = regression constant, b = regression coefficient, r2 = adjusted coefficient of determination.

A.M. Hjelset et al. / Fisheries Research 121-122 (2012) 73–80

This study of a newly established stock has shown that there was a significant reduction in the proportion of large females during the sampling period. We have shown that red king crab females underwent a considerable reduction in fecundity related to size, over the years and in the fjords studied. There were also temporal and spatial changes in individual egg weight during the same period. Fecundity monitoring should be prioritised along with the study of other population parameters, especially now that there is a fishing quota for large female crabs as well as an increased quota on males. The priority for the future should be to identify the consequences of the observed changes in fecundity on recruitment. Acknowledgements This project was funded by the Institute of Marine Research. We are grateful for the contributions of Ellen Dølvik Eliassen, Kristin Windsland and Maria Jenssen, who assisted in the counting of the

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