Temporal variations in the fecundity of Arcto-Norwegian cod (Gadus morhua) in response to natural changes in food and temperature

ELSEVIER

Journal of Sea Research 40 (1998) 303–321

Temporal variations in the fecundity of Arcto-Norwegian cod (Gadus morhua) in response to natural changes in food and temperature O.S. Kjesbu a,Ł , P.R. Witthames b , P. Solemdal a , M. Greer Walker b b

a Department of Marine Environment, Institute of Marine Research, P.O. Box 1870, N-5024 Bergen, Norway Centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory, Pakefield Road, Lowestoft, Suffolk NR33 OHT, UK

Received 20 November 1997; accepted 9 March 1998

Abstract Sexually mature Arcto-Norwegian female cod, Gadus morhua, were sampled off northern Norway either during spawning migration (Vestera˚len) or at spawning sites (Lofoten) from 1986 to 1996. This period comprised a dramatic, nearly cyclical change in the Barents Sea ecosystem. The stock of the main food item, viz. the Barents Sea capelin Mallotus villosus villosus, changed from a low (1986), to a high (1991) and again to a low (1994) level of abundance while the climate changed from a cold (1989) to a warm regime. The relative annual potential fecundity (i.e. number of vitellogenic oocytes per g prespawning fish) increased by approximately 40% from 1987 to 1991. However, information from a back-calculation technique calibrated in the laboratory using spawning fish indicated that this change might have been as high as 80 to 90%. Ovaries were analysed by the gravimetric, the automated particle counting and the stereometric method (modified to use with ovaries too large to section whole). All three methods gave similar fecundity estimates. The latter method was applied to quantify atresia of developing oocytes in the good-condition year of 1991. Atresia was rare, occurring in only 30% of the ovaries and where it was present in only 1 to 4% of the vitellogenic oocytes. Spawning females sampled from 1991 to 1996 gradually produced fewer eggs and demonstrated clear interannual variations in vitellogenic oocyte mean size and distribution thought to reflect a delicate reproductive tactic to minimise negative nutritional effects on egg size and egg quality. Estimates of annual potential fecundity for the duration of the study were significantly positively correlated with environmental temperature and the availability of capelin during vitellogenesis.  1998 Elsevier Science B.V. All rights reserved. Keywords: cod; fecundity; atresia; energy allocation; fish egg counter; stereometry

1. Introduction There is increasing awareness that the reproductive potential of the individual fish within the spawning stock affects recruitment (Damas, 1909; Nikolsky, 1962; Rothschild, 1986; Rijnsdorp et al., 1991; Marshall, 1995; Ulltang, 1996; Kjesbu et al., 1996a; Ł Corresponding

author. E-mail: [email protected]

Trippel et al., 1997). However, as yet, data on maternal and paternal effects are insufficient to construct a commencing hypothesis (Rijnsdorp et al., 1991). For Arcto-Norwegian cod (ANC), Gadus morhua, we presently question the underlying assumption in recruitment studies of a constant relative fecundity (number of vitellogenic oocytes per g fish) among years (Serebryakov, 1990), covering in the analysis the period from 1986 to 1996. Existing information

1385-1101/98/$ – see front matter  1998 Elsevier Science B.V. All rights reserved. PII: S 1 3 8 5 - 1 1 0 1 ( 9 8 ) 0 0 0 2 9 - X

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on ANC fecundity is very limited: Sorokin (1957) examined 8 specimens selected between 1949 and 1951, and Serebryakov et al. (1984) examined 110 specimens collected in 1971 and 1972, pooled and grouped by age. An overview of fecundity studies undertaken on Atlantic cod stocks has recently been presented by Westrheim (1996). Inter-year variability in relative fecundity in the order of 10 to 20% has been demonstrated for several species, e.g. mackerel, Scomber scombrus (Walsh et al., 1990), plaice, Pleuronectes platessa (Rijnsdorp, 1991) and orange roughy, Hoplostethus atlanticus (Koslow et al., 1995). A much more noticeable example is, however, the variation of 1.75 found in northwest North Sea autumn-spawning herring, Clupea harengus (Bailey and Almatar, 1989). No obvious reason for this considerable change was, however, found. Logically, to quantify the full range in relative fecundity, the stock under observation should undergo large-scale natural changes in environmental conditions during the period of study. Long-term studies (i.e. lasting over several decades) may be confounded by possible genetic drift overlying phenotypic responses (Jørgensen, 1990; Rijnsdorp, 1993). The ANC stock inhabits the Barents Sea ecosystem but undertakes yearly migrations to Norwegian coastal waters to spawn, the main spawning grounds being located off Lofoten where the season lasts from mid-March to mid-April (Pedersen, 1984; Bergstad et al., 1987; Nakken, 1994). Landings of ANC have varied considerably historically but the mean level since 1946 appears to be as high as 700 thousand metric tonnes (Nakken, 1994; Anonymous, 1997). However, in the mid-1980s the stock of the main prey, the Barents Sea capelin Mallotus villosus villosus, collapsed (and subsequently recovered) at the same time as a cold climatic regime and low zooplankton production prevailed (Skjoldal et al., 1992). A low abundance of capelin was recorded again from 1994 (Anonymous, 1996a), while the environmental water temperature was above normal between 1989 and 1995 (Anonymous, 1996b). Thus, the present sampling of ANC ovaries was undertaken over a period of time with profound, nearly cyclical changes in the Barents Sea ecosystem. Within the framework of annual changes in relative fecundity, we wanted to address methodology.

Estimating fecundity in prespawning Atlantic cod is in principle simple as the oocyte size distribution shows a clear distinction between previtellogenic and vitellogenic oocytes, i.e. determinate fecundity (Kjesbu et al., 1990). However, we tested the premise that the presumably 1 to 10 million vitellogenic oocytes per individual ANC were homogeneously packed in the ovary by varying the subsample size by two orders of magnitude. Next, we aimed to show if all of the potential fecundity was subsequently spawned or whether some vitellogenic oocytes aborted development and were resorbed into the body by the atretic process, studying the 1991 material stereometrically. The role of atresia in the regulation of oocyte production has been suggested to occur in the sole, Solea solea (Witthames and Greer Walker, 1995) and was also reviewed recently in several species (Tyler and Sumpter, 1996). To investigate the dynamics of this production more closely we also collected data on the fillet and liver weight and the associated development of oocytes measured as size distribution by an automated particle counter. In vitro studies were also undertaken on spawning females from 1991 onwards to examine annual variation in final oocyte size distribution and to back-calculate potential fecundity by a new method developed in Section 3. Tank experiments with spawning fish were initially undertaken to calibrate this method. Thus, the potential fecundity was estimated directly in prespawning fish in the period from 1986 to 1991 and thereafter by back-calculation with parameters estimated from the ovaries of spawning fish.

2. Materials and methods 2.1. Sampling of wild fish Sampling was limited to cod caught off northern Norway prior to and during spawning (Table 1). Sexually mature females were taken randomly and stratified by length off Vestera˚len (about 69ºN) from 4 to 13 March 1986–1989 and on spawning grounds in Vestfjorden, Lofoten (about 68ºN) from 18 to 21 March 1991. Additional, unstratified, random samples were collected at the same spawning location in the period 25 March to 4 April 1992–1996. No

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Table 1 An overview of the prevailing environmental conditions, the sampling protocol and the methods used to measure the dependent variables during the present study Year

Prevailing environmental conditions

Method d

Sampling protocol

temperature capelin biomass ANC biomass geogr. loc. in maturity (in 1000 t) b (in 1000 t) c Norw. waters status (ºC) a 1985 e 1986 1987 1988 1989 1990 1991

– 3.5 3.6 3.3 3.2 4.6 4.5

822 115 100 427 872 5834 7096

996 (201) 1242 (161) 1081 (143) 779 (145) 912 (168) 974 (296) 1518 (649)

Vestera˚len Vestera˚len Vestera˚len Vestera˚len – Lofoten

1992

4.4

5150

2017 (852)

Lofoten

1993

4.3

796

2721 (748)

Lofoten

1994

3.9

199

2619 (625)

Lofoten

1995 1996

4.2 ¾ D3.8

193 –

2431 (570) –

– Lofoten Bergen laboratory

Prespawning Prespawning Prespawning Prespawning – Prespawning and spawning

otolith reading Single Single Duplicate Duplicate – Single

dependent variables

Fecundity Fecundity Fecundity Fecundity None Fecundity Atresia Developing oocyte size distribution Prespawning Single Fecundity f and spawning Fillet weight Fresh vitellogenic oocyte diameter Spawning Single Fresh vitellogenic oocyte diameter Spawning Single Fresh vitellogenic oocyte diameter – None Spawning Single Fresh vitellogenic oocyte diameter Spawning (fish not killed) Egg production in captive specimens

G G G G – APC; S S APC APC; G FW B B B – B T

a Mean water temperature in the section Vardø-North (71–76ºN, 32ºE), Barents Sea between 50 and 200 m depth for a 6-month period (September–March) prior to sampling of the fish (H. Loeng, Institute of Marine Research, Bergen, pers. commun.). b Total Barents Sea capelin stock biomass (age 1C) on 1 October (Anonymous, 1996a). c Total stock biomass (age 3C), total spawning stock biomass is given in parentheses (Anonymous, 1997). d The abbreviations used for each method are listed in brackets as follows: gravimetric method (G); automated particle counter (APC); stereometric method (S); fillet method (FW); binocular microscope (B); and tank experiments (T). e Data included to show situation prior to start of project. f Tests on methodology only.

relevant studies were undertaken in 1990 and 1995. In 1986–1989 only prespawning (vitellogenic) specimens were collected. From 1991 onwards the sample was taken at a time and location which ensured that many fish were in different stages of spawning (Pedersen, 1984). In 1991 (calendar week 12) both prespawning and spawning fish were sampled while only the latter category of fish, except for a few in 1992, were included in the 1992–1996 samples (calendar week 13–14). As the 9-year protocol aimed to include several reproductive and methodological aspects the full sampling scheme turned out to be rather complex

(Table 1). Every female was recorded for total length (to the nearest 1 cm) and whole wet body weight (to the nearest 0.1 kg in 1986–1988 and to the nearest 1 g since 1989). The ovary was removed, weighed (since 1989) and, provided it was classified as prespawning, frozen for subsequent estimation of fecundity using the gravimetric method (for fecundity methods see Section 2.6). In 1991 ovarian subsamples of both prespawning and spawning fish were preserved for stereometric analyses and for the automated particle counter. In addition to estimates of fecundity the former method enabled us to estimate the level of atresia while the latter method enabled

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us to describe the oocyte size frequency distribution. Limited numbers of samples were collected in 1992 to compare the automated particle-counter method and the gravimetric method. In 1992–1996 special attention was given to studies of interannual changes in vitellogenic oocyte size and distribution. The long and short axes of 50 fresh oocytes from each female were shortly after capture measured and averaged under a binocular microscope (mag. 50ð) in iso-osmolar 1.07% NaCl. The wet weights of liver and viscera (gut and stomach) were recorded from 1989. Sagittal otoliths were removed from all fish for stock separation and age determination (Rollefsen, 1933, 1934). All sampling was undertaken at low air temperature (about 5ºC). In the laboratory, every ovary intended for gravimetric analysis was thawed and weighed (to the nearest 0.1 g). Small subsamples were weighed (to the nearest 1 mg) and preserved in a sucrose–formaldehyde-based fixative (Kjesbu and Holm, 1994). Fresh and thawed ovary weights showed negligible differences (¾1%). 2.2. Stock classification and age reading precision

2.3. Definitions (1) (Annual) potential fecundity (F): number of vitellogenic oocytes in the ovary just prior to spawning. (2) Residual fecundity (Fresidual ): number of vitellogenic oocytes still remaining in the ovary at the time of observation during the spawning period. (3) Batch fecundity: number of hyaline or ovulated oocytes due to be spawned in the immediate future. (3) Relative fecundity: F divided by the whole wet body weight. (4) Somatic relative fecundity: F divided by the ovary-free whole wet body weight. (5) Atresia: resorption of vitellogenic oocytes. (6) Relative intensity of atresia: percentage of atretic vitellogenic oocytes in relation to the total number of normal and atretic vitellogenic oocytes found in the ovary at the time of examination. Only atretic oocytes in the early α-stage (Hunter and Macewicz, 1985; Witthames and Greer Walker, 1995) were counted. 2.4. Stage of spawning calibration

Present catches probably contained both ArctoNorwegian cod (ANC) and Norwegian Coastal cod (CC) (Dahle, 1995). Exclusion of any CC individuals was considered relevant because of possible stockspecific differences in variables examined (Kjesbu, 1988). Duplicate, independent readings of otoliths selected from the years 1988 and 1989 (Table 1), however, showed examples of individuals which were classified differently each time, i.e. changed from CC to ANC or vice versa. This unknown type represented 20.5 and 22% of the total number of females examined in 1988 (n D 78) and 1989 (n D 150), respectively. No significant difference in the potential fecundity vs. total length relationship existed between these fish and the type recorded as ANC twice. However, to adopt a similar protocol for all years combined, only females classified as ANC in the first series of otolith readings in 1988 and 1989 were considered in the further analyses. Similar tests on precision in recording of fish age showed that about 1=3 of the records varied between duplicate readings, in 92 to 95% of the cases by 1 year only, and maximally by 2 years.

In 1996 an experiment was undertaken using captive ANC (Table 1) to relate the above observed automated particle-counter data on oocyte size frequency distribution to the progress through spawning quantified by the portion of the total number of eggs spawned (PES) at the time of sampling of each wild fish. This stage system ranges from 0 to 100% corresponding to prespawning and spent fish, respectively. Previous reports on CC have shown that the size distribution of vitellogenic oocytes is unimodal and becomes narrower throughout spawning (Kjesbu et al., 1990). Consequently, PES is negatively linearly correlated with the standard deviation of the diameter of vitellogenic oocytes (SD). These equations were intended to be calibrated for ANC. The fish for the experiment were sampled near Bear Island in the middle of the Barents Sea (i.e. obviously ANC) in October 1993 and transported to the laboratory. The analytical protocol was identical to Kjesbu et al. (1996a). As every batch of eggs spawned was collected from each of three naturally spawning females (two recruit spawners of 68 and

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Fig. 1. Change in batch fecundity in relation to residual fecundity during the spawning period represented by PES (portion of total number of eggs spawned).

307

in the very beginning (n D 6) and end of spawning (n D 4) were selected. The early-season ovaries showed small vitellogenic oocytes (minimum and mean diameter found to be <520 and 710 µm, respectively) and were set at PES D 5% (Kjesbu et al., 1990, 1991). The late-season ovaries were set at PES D 95% based on an evaluation of Fresidual and batch size. Equations to back-calculate F from Fresidual and PES for the years 1991–1994 and 1996 are presented in Section 3. For 1991 individual Fresidual and PES values were used while mean Fresidual and mean PES were used for the following years. The latter mean was set similar to that reported for 1991. This assumption was based on the fact that egg surveys in the Lofoten showed that the time of peak spawning of ANC was very stable among years: viz. 1 April (standard deviation D 2.2 days) (Pedersen, 1984). 2.5. Estimation of organ ratios and muscle mass The gonosomatic index (GSI) was defined as:

73 cm total length, and one repeat spawner of 95 cm total length) during the whole spawning period, both the batch fecundity=residual fecundity ratio and PES could be found and correlated. This complex relationship was explored empirically using 6th order polynomial regression .r 2 D 0:926, P < 0.001) (Fig. 1). An almost identical curve was found using distance weighted least squares smoothing (Wilkinson et al., 1992). Also, all three females showed similar patterns. In wild fish where the automated particle counter had shown well-defined batches to be present, this calibration included calculation of the ratio of batch fecundity=residual fecundity followed by assessment of PES from Fig. 1. Thus, the relationship between SD and PES in 1991 was indicated (presented below as Eq. 4). By applying this equation on the remaining material all specimens in 1991 were finally listed with PES values. In 1993 further analyses were undertaken to test: (1) if it was possible to develop a field method to estimate the progress through spawning based on measurements of 50 oocytes only (see method above); and (2) if there existed any interannual variation in the assumed linear PES–SD regression. ANC females judged macroscopically to be

GSI D 100 ð OW=.W

OW/ .%/

where OW is ovary weight (in g) and W is whole body weight (in g). The hepatosomatic index (HSI) was calculated as: HSI D 100 ð LW=.W

OW/ .%/

where LW is liver weight (in g). The Fulton’s condition factor (K) was: K D 100 ð W=L3 where L is total length (in cm). The total muscle wet weight (MW, in g) in individual females was estimated using the following simple equation: MW D W

.OW C LW C VW C SB/

(1)

where VW is wet weight of viscera (in g) and SB is total wet weight of skin and bones including head (in g). It was hypothesised that SB was approximately constant at a given total length. To test this, SB was recorded for fish of different L and K (range: 0.76– 1.41, mean: 1.04) after filleting and scraping off flesh from the remains of the fish. The relationship between SB and L (natural logarithmic transformed data) was as follows: SB D 1:707 ð 10

3

ð L3:183

(n D 12, r D 0:962, P < 0.001; Fig. 2). 2

(2)

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0.39 millions, respectively (n D 119, two subsamples).

Fig. 2. A comparison in ANC females between the amount of skin and bones with respect to the whole body weight in relation to total length.

2.6. Estimation of fecundity 2.6.1. Gravimetric method The gravimetric method was used only on ovaries free from large, hyaline oocytes because their presence would complicate representative subsampling (Kjesbu, 1989). All vitellogenic oocytes (n D 600 to 1000) in subsamples of 150 to 250 mg were counted under the binocular microscope, and the number counted raised to the whole ovary weight (50 to 3050 g). As in the other fecundity methods, sampling design was based on the assumption of a uniform packing density of oocytes in the whole cod ovary (Kjesbu and Holm, 1994). A total of four subsamples were taken from the middle part of the right ovary lobe of each female. In most females only two subsamples were counted. Three or four subsamples were examined in cases where the coefficient of variation (CV) for two or three subsamples was larger than 5%. The final mean fecundity estimate and the corresponding standard deviation were noted for each female. Tests on a representative group of females (n D 147) gave an overall CV of 4%. Large and small ovaries showed similar CV values. The fecundity of a typical small, medium and large ovary was given with a precision (mean š 95% confidence limits) of 0.50 š 0.01, 5.00 š 0.19 and 10.00 š

2.6.2. Automated particle-counter method An automated particle analyser (Millers Systems Ltd.) connected to a Hiac Criterion PC 2500 sensor, operated as described in Witthames and Greer Walker (1987), was used to count and size particles >200 µm released from ovary tissue subsamples (8–24 g) digested in Gilson’s fluid (Simpson, 1951; Kjesbu et al., 1991). Whole ovary weights ranged from 170 to 4700 g. The sensor was calibrated by passing through it manually measured oocytes and recording the oocyte counts generated as voltage pulses on a channel array of a pulse-height analyser interfaced with a personal computer. For each subsample, the upper and lower thresholds for the vitellogenic oocyte mode were determined. The same procedure was used for any final maturation (final growth) and hyaline oocytes (Kjesbu et al., 1990). In total about 9000 to 63,000 developing oocytes were counted and measured from each female by this method. The relevant fecundity was integrated from these counts between these limits and multiplied by the raising factor (ovary weight divided by subsample weight). As all vitellogenic oocyte diameter data in the years following 1991 were fresh values measured under the binocular microscope in calendar week 13, all 1991 data collected from the automated particle counter needed to be properly transformed, based on the following three-step procedure: (1) Estimates of mean diameter from the same subsample (n D 6) given by the binocular microscope (y) and by the automated particle counter (x) were regressed against each other: y D 1:072 ð x

19:0

(3)

.r D 0:983, P < 0:001; 390 µm < x < 630 µm). (2) The degree of shrinkage in Gilson’s fluid was corrected for by multiplying observed vitellogenic oocyte diameter in prespawning fish by 1.275 and in spawning fish by 1.335 (Kjesbu et al., 1990). The standard deviation of diameters of fresh vitellogenic oocytes was calculated from the general statistical law that SD .ax C b/ D jaj ð SD.x/. Thus, under point (1) multiplying by 1.072 and under the present point by 1.275 or 1.335. 2

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309

(3) Any relevant change occurring between calendar week 12 (1991) and 13 was adjusted for by establishing relationships between the dependent variable in question and PES as the independent variable assuming from the tank experiment described above that the latter increased by 15% over this period of time (data not presented). 2.6.3. Stereometric method A stereometric method (Emerson et al., 1990; Greer Walker et al., 1994) was modified to estimate the number of normal and atretic vitellogenic oocytes in a random selection of all the fish collected in 1991. Because ovaries were generally too large (same size range as observed for the previous method) to produce whole-ovary histological crosssections, the original method was modified to estimate the number of relevant cells in weighed tissue subsamples. In each case all oocytes in an ovary subsample (5–13 g) were fixed in cacodylate-buffered glutaraldehyde (Forberg, 1982), infiltrated with Historesin (Leica, UK) and finally polymerised in one or two blocks (depending on the subsample weight) formed by a Poly-tetra-fluoro ethylene mould. Each block was sectioned at 5 µm and stained with toluidine blue to estimate the oocyte partial volume (Pv) and number per unit volume (Nv) as in the original method. The total volume sampled in each stereometric estimate was calculated from the product of the mean cross-section area and the depth of oocytes (forming a discrete layer at the base) in the block or blocks. It was found necessary to analyse up to 85 fields (each field refers to a replicated subunit, 1:75 ð 1:71 mm2 , of the section area taken from three to six sections of one or two blocks, respectively) working from the base of the block to give stable mean values of Nv per field (Fig. 3). The number of normal and atretic oocytes in each subsample was raised to the whole ovary weight.

Fig. 3. Running, normalised mean of vitellogenic oocyte profiles per unit volume for three ANC females with increasing fields scored. The final, stable profile estimate was set at zero and taken as the reference.

differed when contrasted within the same fish (Table 2). Similarly, no important differences were observed between the automated particle-counter method and the stereometric method. In relation to the automated particle-counter method, the gravimetric method and the stereometric method showed fecundity estimates which were on average 1.020 (n D 3, CV D 4.7%) and 1.035 times (n D 27, CV D 26.7%) higher, respectively. 3.2. Interannual variation in potential fecundity in prespawning fish For the years analysed (1986–1989 and 1991) there existed a strong, positive relationship between potential fecundity (F) and total length, and between Table 2 Comparison of fecundity estimates obtained by two methods: gravimetric and automated particle counter, for three ANC females Female No.

3. Results

Fecundity (millions) gravimetric

automated

absolute

method

method

difference

0.775 (0.729–0.812) 1.667 (1.525–2.079) 4.594 (4.405–4.844)

0.721 1.677 4.635

0.054 0.010 0.041

3.1. Comparison of fecundity methods

1 2 3

Estimates of the number of vitellogenic oocytes in the whole ovary found by the gravimetric method and the automated particle-counter method hardly

Values in parentheses give observed range for four estimates. Absolute difference refers to mean gravimetric fecundity estimate and single, automated fecundity estimate.

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Fig. 4. Relationship between annual potential fecundity and total length in 1986–1989 and 1991 (Ž). For 1991 residual fecundity in spawning fish is also included (C). Ovaries collected in 1986–1989 were examined by the gravimetric method and in 1991 by the automated particle counter.

F and whole body weight (Fig. 4). The regression analysis (Table 3) showed consistently higher coefficients of determination .r 2 / for the relation with body weight than with body length. Regressions of F on somatic weight (i.e. ovary-free whole body weight) or total muscle weight (1989 only) gave values of r 2 in between those listed for F on whole body weight and total length. Fish age did not contribute significantly as a second independent variable

(P > 0.05, multiple regression analysis). However, a similar type of statistical test showed a positive significant effect (P < 0.001) of liver weight (Table 3). Corresponding HSIs ranged from 4 to 12%. Relative fecundity and total length were positively correlated with r D 0.324 (P D 0.022), 0.580 (<0.001), and 0.345 (<0.001) in 1986, 1988 and 1989, respectively. However, this was not seen for samples lacking large fish (1987) or containing few

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311

Table 3 Regression formulae for annual potential fecundity for each single year examined n

r2

P

Fecundity vs. total length 1986 F D 1.23 ð 10 7 L3.764 1987 F D 2.61 ð 10 7 L3.541 1988 F D 6.14 ð 10 8 L3.908 1989 F D 8.04 ð 10 7 L3.357 1991 F D 1.68 ð 10 5 L2.693

50 46 49 111 8

0.888 0.786 0.916 0.920 0.817

<0.001 <0.001 <0.001 <0.001 0.002

Fecundity vs. whole body weight 1986 F D 3.32 ð 10 1 W1.119 1987 F D 3.29 ð 10 1 W1.019 1988 F D 2.57 ð 10 1 W1.240 1989 F D 3.60 ð 10 1 W1.115 1991 F D 4.83 ð 10 1 W0.937

50 23 49 110 8

0.924 0.871 0.955 0.943 0.852

<0.001 <0.001 <0.001 <0.001 0.001

Fecundity vs. total length and liver weight 1989 F D 6.74 ð 10 6 L2.448 LW0.329 111

0.933

<0.001

Year

Regression

F D annual potential fecundity (in millions); L D total length (in cm); W D whole body weight (in kg); LW D liver weight (in g). All data were natural logarithmic transformed before analysis.

observations (1991) (P > 0.50). In 1986, 1988 and 1989 the relative fecundity of a fish of length 120 cm compared to one at 50 cm was found to be 36, 81 and 30% higher, respectively. Correlations with somatic relative fecundity on the y-axis instead showed significance levels similar to those presented, while the increase from 50 to 120 cm length was 52, 86 and 32%, respectively. The above results indicate that size-specific F varied significantly over time. To achieve overlap in length range among years the analyses were limited to fish 90 cm (Fig. 5). Regressions of whole body weight on total length varied significantly both in slope (P D 0.001) and intercept (P < 0.001) (ANCOVA). For F, intercepts were found to be significantly different (P < 0.001) but not slopes (P D 0.159). For fish at total length 50, 70 and 90 cm, estimated F in 1987 (defined as a poor-condition year; Table 1) was found to be 45, 44 and 44% lower than in 1991 (good-condition year), respectively. This apparently general reduction in F over length was less obvious in 1988 as the larger fish seemed to recovered more quickly from the situation in the previous year. Note, however, the above statistical information of no significant differences in slopes among years.

Fig. 5. Whole body weight (upper panel) and annual potential fecundity (lower panel) vs. total length for ANC females with recorded lengths of between 50 and 90 cm sampled in 1986– 1989 and 1991.

A more detailed examination of the annual changes in both whole body weight and F of a standard fish of 70 cm total length (i.e. at the above length-range midpoint) demonstrated that the relative fecundity varied significantly over time (Fig. 6). The lowest value (327 oocytes g 1 ) was recorded in 1987 and the highest (460 oocytes g 1 ) in 1991; an increase of 41%. Using instead a general fecundity regression for all years combined (i.e. pooled data, cf. the above cited ANC work of Serebryakov et al., 1984) no such clear pattern appeared (Fig. 6). However, as both these and the previous relative fecundity figures were found by putting together separate re-

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sults from various regressions, we finally took full account of individual variation by using directly estimated values. The percentage change in relative fecundity over time at 70 cm was found to be identical to that reported above although each estimate was noted to be generally slightly higher (10 oocytes g 1 ). 3.3. Interannual variation in ovarian and oocyte size in spawning fish Spawning specimens (n D 149) demonstrated significant yearly variations in mean and standard deviation of vitellogenic oocyte size, GSI, and weight at length but not in HSI (Fig. 7). The P-value for HSI was 0.206 (Kruskal–Wallis test), <0.05 for oocyte diameter and standard deviation and GSI (based on examples of non-overlapping confidence limits), and 0.364 for slope and 0.027 for intercept in weight=length regressions (ANCOVA). The year 1996 appeared to be exceptional, i.e. contained thinner fish, because there were no significant differences if this year was omitted (slope: 0.231; intercept: 0.080). Also, mean GSI in 1996 was extremely low. To circumvent problems with size-dependent effects, all statistical analyses of the present Section were restricted to fish >75 cm. 3.4. Stage of spawning, atresia and back-calculation of potential fecundity Spawning ANC females analysed using the automated particle counter (1991 data) showed a significant negative relationship between standard deviation of vitellogenic oocyte diameter (SD, in µm) and portion of eggs spawned (PES, in percentage): SD D 124:7

0:660 ð PES

(4)

Fig. 6. Variation among years (1986–1989 and 1991) in whole body weight (upper panel), annual potential fecundity (middle panel) and relative fecundity (per g whole body weight) (lower panel) of a standard fish of total length 70 cm. Vertical bars are 95% confidence limits (any noticed asymmetry is due to backcalculation from natural logarithmic transformed data). Relative fecundity was calculated both on a year-specific and pooled basis (i.e. using a general fecundity–weight regression for all years combined).

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Fig. 7. Mean fresh vitellogenic oocyte diameters, their standard deviations, and GSI and HSI values (%) recorded for spawning specimens collected in 1991–1994 and 1996. Vertical bars are 95% confidence limits.

(n D 13, r 2 D 0:947, P < 0:001, 15% < PES < 95%; Fig. 8). One outlier was excluded as the batch fecundity in this fish was probably underestimated because of loss of running eggs. As both SD and PES were subjected to errors, the above regression was contrasted with geometric-mean regression finding negligible differences, i.e. absolute difference in predicted SD being 0.6 µm. Maximum SD in prespawning fish was similar to SDs observed in early spawning fish. In the further fecundity analysis no systematic differences were found in the 1991 material between those females used to establish Eq. 4 and those where PES was found by inverting the same equation. The relationship between SD and PES varied

noticeably between years. Correcting for different methodologies, the SD at PES was found to be significantly lower in 1993 than in 1991 (Fig. 8). The exceptionally large range in SD at PES D 95% for 1993 determined under the binocular microscope was found to be due to examples of incomplete separation of vitellogenic oocytes and oocytes in early final maturation (note that only 50 oocytes were measured in 1993). As for 1991, the large range at the very beginning of the spawning period was, however, assumed to be correlated with short-term differences in rapid ovarian development and growth (Kjesbu et al., 1991). Combining individual estimates of PES and residual fecundity (Fresidual ), potential fecundity could be

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ANCOVA applied on the overlapping length range showed the intercept to be significantly higher (P D 0.001) in back-calculated specimens than in fish that had not yet started to spawn, but their slopes were not statistically different (P D 0.868). At 70 cm length the prespawning category showed F ³ 1.6 million, while the spawning category showed Fbackcal ³ 2.5 million. The combined data gave a fecundity (Fcombined ) of about 2.3 million using the following regression: Fcombined D 6:79 ð 10

Fig. 8. Seasonal change in standard deviation of fresh vitellogenic oocyte diameter measured using the automated particle counter (1991) and the binocular microscope (1993). The regression line refers to spawning fish in 1991. The vertical bars are the observed range around the mean value. PES D portion of eggs spawned.

found by back-calculation (Fbackcal ): Fbackcal D 100 ð Fresidual ð .100

PES/

1

(5)

Power regression for Fbackcal (in millions) on total length (L) was: Fbackcal D 5:66 ð 10

6

ð L3:061

(6)

(n D 47, r 2 D 0:687, P < 0:001; Fig. 9).

Fig. 9. Back-calculated annual potential fecundity (spawning specimens: C) and observed annual potential fecundity (prespawning specimens: Ž) in relation to total length in 1991. The curve given is based on back-calculated data (C) only.

6

ð L3:002

(7)

(n D 55, r 2 D 0:647, P < 0:001/. Liver weights were contrasted to indicate condition. The following multiple regression formula was found for the spawning fish in 1991: LW D 14:48 ð L

4:55 ð PES

509

(8)

(n D 47, r 2 D 0:753, P < 0:001) with both L and PES clearly contributing significantly: P < 0.001 and P D 0.002, respectively. The equation is valid for L > 65 cm only. The combined 1991 sample showed a mean PES of 47% (mean L D 82.3 cm). The corresponding figure for the spawning fish only was 55% (82.2 cm). Mean liver weight and length of the prespawning fish was 474 g and 82.5 cm, respectively. At similar length and maturity status, i.e. setting PES D 0% in Eq. 8, the spawning fish showed a liver weight of 686 g, i.e. 1.45 times as high. For further comparison among years, a prespawning female of 82.5 cm in 1989 showed an estimated liver weight of 307 g (n D 113, r 2 D 0:838, P < 0.001). No similar prespawning data were available for 1987, i.e. for the year in which the liver weight was probably lowest. The majority of females examined in 1991 demonstrated no sign of atresia (Fig. 10). Also, of the 30% ovaries showing this phenomenon the relative intensity of atresia was generally low (mean: 2.5%). Atresia was restricted to prespawning fish and to fish in the first half of the spawning period. The average diameter of the normal oocytes was <800 µm, i.e. relatively small. Observations made of atresia could not be significantly correlated (P × 0.05) to variations in fish condition represented by K. For samples collected in 1992–1994 and 1996, Fresidual could be estimated with high precision using

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315

Fig. 10. Observed relative atretic intensity in 1991 in relation to mean fresh vitellogenic oocyte diameter (left panel) and PES (right panel). Both prespawning and spawning specimens are included.

ovary weight (OW), mean vitellogenic oocyte diameter (D) and standard deviation (SD) as independent variables: Fresidual D 1:11 ð 103 ð OW1:062 ð D

2:971

ð SD1:359 (9)

(n D 47, r 2 D 0:910, P < 0.001). All 1991 data included to establish Eq. 9 showed a wide range in numerical values: OW, 182 to 4700 g; D, 693 to 876 µm; SD, 63 to 120 µm. 3.5. Synthesis The final analysis, including all years where ANC fecundity was either observed (prespawning fish) or back-calculated (spawning fish), used the potential fecundity for a fish of standard length 90 cm (F90 cm ) as the dependent variable. This standard length was approximately the midpoint in truncated length distribution for spawning fish. For 1991 only back-calculated values were used (see Section 4). To back-calculate F90 cm it was assumed that the time of peak spawning (i.e. mean PES) was stable among years and OW was estimated from GSI. For the duration of the study F90 cm demonstrated a clear temporal pattern (Fig. 11). F90 cm was significantly positively correlated with the environmental temperature and the amount of capelin available (Fig. 12). More specifically, the regression of F90 cm

Fig. 11. Synthesis of indicated variation in annual potential fecundity for a standard ANC female of 90 cm total length over a 10-year period of time (1986–1996). Arrows indicate that back-calculated potential fecundity was based on the assumption that the group of fish analysed spawned at the same time in the year as noticed for the fish in 1991.

on the 6-month mean temperature in the Vardø-North section yielded an r 2 value of 0.702 (P D 0.005) and on the ratio of Barents Sea capelin biomass and ANC spawning biomass an r 2 value of 0.623 (P D 0.019). There were, however, indications that environmental temperature and amount of capelin available were also correlated with each other (P D 0.118).

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Fig. 12. Estimated annual potential fecundity for a standard ANC female of 90 cm total length in relation to mean environmental temperature and amount of food during the period of vitellogenesis. The latter variable is represented by the ratio of biomass of Barents Sea capelin and ANC spawning stock biomass, for further information consult Table 1.

4. Discussion Relative fecundity in prespawning ANC varied among years (1986–1989 and 1991) by as much as 40%. This percentage was found by selecting the value for the poor-condition year 1987 as denominator and the value for the good-condition year 1991

as numerator. However, this percentage is considered to be an underestimate because the back-calculation technique used on the spawning fish in 1991 showed an extraordinarily high potential fecundity for these individuals; the phenotypic variability may have been as high as 80 to 90% (Table 4). Such marked medium-term responses in relative fecun-

Table 4 Approximate mean relative fecundity (number of vitellogenic oocytes per g prespawning whole body weight) ranked in order of increasing size found in previous and present studies on Atlantic cod inhabiting Norwegian waters, i.e. Arcto-Norwegian (ANC) and Norwegian Coastal cod (CC) Stock

Year

Feeding ration a

Spawning experience

Length (cm)

Relative fecundity (oocytes per g)

Study

ANC CC CC CC CC CC CC

1986–1991 1986–1987 1959 Experimental Experimental Experimental Experimental

Wild fish, northern Norway Wild fish, northern Norway Wild fish, western Norway Starved and low (6 months) Low and high (6 and 12 months) Starved and high (2 and 6 months) High (6 months)

Recruit=repeat Recruit=repeat Recruit=repeat Repeat Recruit Recruit Repeat

70 70 70 50–75 40–45 40–45 55–75

325–450 (600) b 450 800 950 [400] c 1100 1100 1300 [800] c

Present Kjesbu (1988) Botros (1962) Kjesbu et al. (1991) Kjesbu and Holm (1994) Karlsen et al. (1995) Kjesbu et al. (1991)

For experiments listed the single relative fecundity value indicates that no significant difference was noted between the two groups tested and that their pooled value is used. Note, however, that repeat spawners were more sensitive to food variations than recruit spawners. In cases where somatic relative fecundity was listed in the published literature the presently defined relative fecundity was found by multiplying by 0.90. a The value(s) in parentheses give(s) the length of exposure to each of the two different feeding rations, respectively. b The value in parentheses is that found by back-calculation in 1991 (i.e. using Eq. 7). c The values in parentheses show realised relative fecundity (i.e. number of eggs spawned per g prespawning body weight).

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dity under natural environmental fluctuations are to our knowledge new in the cod literature. Our results should be considered in the light of the large range in environmental fluctuations in the Barents Sea ecosystem over the time period in question, i.e. from a cold to a warm climatic regime and from a collapsed to a recovered capelin stock (prey). Indeed, we found a positive relationship between these environmental descriptors and estimates of potential fecundity. Another relevant issue is the fact that maturing ANC migrate over a very long distance to the spawning grounds and thereby could be particularly sensitive to variations in accumulated body reserves. To complete the picture, there were no obvious negative density-dependent effects operating that could possibly explain an observed 20% change in relative fecundity for North Sea cod between 1970–1971 and 1987–1988 (Rijnsdorp et al., 1991). Both the maximum and minimum relative fecundity presented for ANC are assumed to be realistic input values in future model work. Adopting the principles of oogenesis seen for CC in combined tank and field studies (Table 4), it seems clear that the physiological potential for a much higher value does exist. Thus, the fish might with a plentiful food supply, such as tabled, allocate significantly more energy to gonads prior to spawning than is often believed. Nevertheless, the present indicated maximum figure of 600 oocytes g 1 (L D 70 cm) is likely to be correct. This supposition is based on the extremely high liver index or fish condition found in 1991 and supported by detailed studies of a relevant subset (1985–1996) of the about 70-year-long Russian liver data base (Marshall et al., 1998). Similarly, focusing on the lower range in relative fecundity, a value of about 300 oocytes g 1 is probably close to a physiological minimum below which the fish might skip spawning to avoid further depletion of body reserves (Rijnsdorp, 1990, North Sea plaice; Kjesbu et al., 1991). Specimens which fail to produce eggs will most likely not invest energy in spawning migration either, and thereby still remained in the Barents Sea area at the time of sampling (Oganesyan, 1993; Marshall et al., 1998). Stated in another way, the present specimens were probably taken from those in a relatively better condition and therefore do not properly reflect the adult population as a whole. Larger females demonstrated a higher relative fecun-

317

dity than smaller ones, implying a higher level of depletion of body reserves during spawning (Kjesbu et al., 1996a). Cod >80 cm feed almost entirely on fish (incl. conspecifics) (Nakken, 1994). In the mid1980s, more precisely 1986 and 1987, the situation was, however, exceptional as the main prey, capelin, was practically unavailable (Table 1). This series of arguments might explain why there were no large fish (>90 cm) in any of our catches taken in the poor-condition year of 1987. Logically, several of them were still alive, as large specimens of relevant size reappeared the year after. Evidence suggests that ANC fecundity varied among years in an interrelated manner. Including back-calculated values, the potential fecundity changed in a near-unimodal fashion over the decade studied. As stated, the described pattern closely followed reported environmental fluctuations, thereby also indirectly supporting the given back-calculated values. As used, this technique relied upon the assumption that the peak of spawning was the same for all years, which seems reasonable (see citations above). The relative fecundity in 1988 appears to be lower than expected from the condition of the fish. This might be due to the documented poor situation in the previous year which possibly affected early oogenesis negatively (Kjesbu et al., 1996a). Taken together, it appears, at least for ANC, that fecundity comparisons based on data collected within a short period will tend to fail to demonstrate any interannual variation. An implication of this is that an analysis of possible fecundity differences between stocks of the same species should best be done within the same year (Witthames et al., 1995, Dover sole) or, ideally, over a similar period of years. Whole body weight was found to be the most powerful predictor of potential fecundity in ANC. As the body of maturing fish can be viewed as consisting of different compartments, viz. fillet, liver and ovary, which are coupled together in terms of transport of organic matter from the first two towards the latter (Smith et al., 1990; Kjesbu et al., 1991; Jobling, 1995), it is not surprising, at least in retrospect, that the combined weight of all three turned out to be the best predictor. Oosthuizen and Daan (1974) reached a similar conclusion although they did not weigh muscle and liver separately. Moreover, fish age did not contribute significantly when included as a sec-

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ond independent variable in a multiple-regression analysis. Note, however, that age appears to be important for fecundity in very long-lived species such as orange roughy, which may become 100 years old or more, and also in egg and larval quality studies (Kjørsvik et al., 1990; Solemdal et al., 1995; Kjesbu et al., 1996a; Trippel et al., 1997). In the latter respect it is, however, more specifically the maturation rate which in turn determines how quickly a recruit spawner becomes a repeat spawner (Marshall et al., 1998). Another confirmatory finding is that the intercept rather than the slope in cod fecundity length regressions varies among years (Pinhorn, 1984). Thus, the total production of oocytes changes among years, but fish of different lengths respond proportionally in a similar way, except possibly in 1988 when the larger ANC specimens seemed to respond faster in terms of growth in fecundity at the very beginning of the capelin stock recovery. Finally, the present fecundity regressions were all characterised by a higher coefficient of determination than normally found in the relevant literature. One partial explanation is the wide range in values presented on the x-axis. A pilot study based on the 1989 material showed that r 2 dropped considerably (from 0.920 to 0.533) by excluding successively the larger fish from the data base (using a length range of 50 to 125 cm and 50 to 70 cm, respectively), while there were no detectable changes in P-value (<0.001 in both cases). Very little or, in most cases, no atresia was seen in the prespawning and spawning ANC ovaries examined by the stereometric method. Obviously, this is to some extent because this examination was limited to fish classified as being in extremely good condition; relative intensity of atresia and fish condition (K) have been found to be inversely correlated in tank experiments (Kjesbu et al., 1991). The intensity of atresia appeared to be oocyte-size-specific with the underlying mechanism resembling the one indicated for sole (Witthames and Greer Walker, 1995) and CC (first and second author, unpubl. data); smaller vitellogenic oocytes undergo resorption which modulates fecundity but as a consequence a gap or hiatus develops between previtellogenic and vitellogenic oocytes which terminates further vitellogenic oocyte recruitment. Removing the smaller vitellogenic oocytes instead of the larger ones seems logical because of the

lesser energy invested in each and the thinner, more fragile chorion (Kjesbu and Kryvi, 1989). Further quantitative studies are, however, needed to discover how atresia operates in spawning ANC in poor condition (e.g. in years such as 1987) whereby the realised fecundity may become significantly lower than the potential fecundity. Information of this type is highly relevant in attempts to refine yearly estimates on total egg production of the stock (Marshall et al., 1998). The methodology presently developed for estimation of atresia in large ovaries should facilitate further studies on this topic in cod and other fish with small, numerous vitellogenic oocytes. This version of the stereometric method gave on average accurate results, but within-sample tests demonstrated a lower precision than in the gravimetric and automated particle-counter methods. Present and published information (Table 4) suggests that the overall oocyte production prior to spawning is more balanced energetically in wild than in captive specimens. As tabled for CC, realised rather than potential fecundity in captive fish was similar to potential fecundity in wild fish. It appears that CC, and probably also ANC, in a captive situation generally produce too many vitellogenic oocytes prior to spawning (i.e. both at low and high ration). This superfluous production is subsequently resorbed during the spawning season but significantly more eggs are spawned by fish in good condition than in poor condition. Detailed examinations of spawning ANC revealed significant interannual variations (1991–1994 and 1996) in both vitellogenic oocyte size and distribution and ovarian size. These measurements also show that females spawning late in the season (1991) demonstrate a lower size-specific potential fecundity. The observed differences in ovarian morphometrics imply that the method using the portion of the total number of eggs spawned, i.e. Eq. 4, used to backcalculate potential fecundity, needs to be separately calibrated in each year of study. The new finding that mean vitellogenic oocyte diameter and SD varied among seasons might reflect a delicate reproductive tactic to guarantee that eggs of normal size are produced even at times of poor nutritional situations. Contrasting for example 1991 and 1994 shows that GSIs and mean oocyte diameters (D) were approximately similar, but because in 1994 oocytes were

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generally more uniform in size (i.e. demonstrating a significantly lower SD) the corresponding number of oocytes present was much lower, supporting the statement of Wootton (1990) that GSI alone does not properly reflect reproductive investment. The fecundity multiple-regression equation used in this respect, i.e. Eq. 9, including D and SD as well as ovarian size as independent variables, appeared to work remarkably well. Based on the principles outlined for oocyte growth in Kjesbu et al. (1996b), a lower SD at a similar point in the maturation cycle should reflect a shorter spawning period (i.e. at the individual level) but not necessarily a shorter spawning season (i.e. at the population level). However, the spawning season in 1994, i.e. at the time of minimum mean SD, was observed to be extremely short in the Lofoten region (third author, pers. obs.). Out of the 5 years analysed for spawning fish, those collected in 1996 stand out as being in the poorest condition based on the low GSI and residual fecundity. Furthermore, the extremely large range in SD for that year indicates examples of abnormal maturity cycles. Statistical analyses of weights-at-length data suggest that the fish spawning in 1996 were in poor condition, but caution should be exercised in comparison of the condition of spawning fish among years. Assuming from the above discussion that fish in good condition invest more in reproduction, it follows that they should also lose more body weight in absolute terms during the spawning season and thereby approach the corresponding poor-condition fish in body characteristics (cf. surplus production allocation model for spawning fish in Rijnsdorp, 1990). It is striking that the case study in the 1991 season showed that prespawning specimens produced fewer eggs and were in poorer condition than the simultaneously taken spawning specimens. The cause of the delay in spawning time for the former category is unclear; it might be that temperatures were lower during vitellogenesis (Kjesbu, 1994), or that they belonged to another subpopulation (Witthames et al., 1995, Dover sole), or both. Observed differences in condition are considered to be too small to be of importance in this respect (Kjesbu, 1994). Nevertheless, collection of prespawning fish during the main spawning season seems unwise if the purpose is to study potential fecundity only (i.e. risk of getting biased samples).

319

We conclude that the dynamics of vitellogenic oocyte production in ANC varies among years, not only prior to spawning but also during spawning. Ideally, to obtain a broader picture, these topics of research should be expanded to include a higher number of females sampled at different geographical locations each year.

Acknowledgements This 10-year study has been supported financially by several projects of the Institute of Marine Research and also by the Norwegian Research Council (NFR) (formerly the Norwegian Fisheries Research Council) including a 6-month guest scholarship (1991–1992) at CEFAS (formerly the Fisheries Laboratory), Lowestoft, England, for training within the field of stereometry=histology (O.S.K.). The experimental work in 1996 was supported by the European Union contract FAIR-CT-95-0084. The writing up of this paper was part of the NFR project (No. 108153=110) ‘Population Dynamics Model for Northeast Arctic cod’. We thank everybody who assisted in sampling and analysing the material used. Per Bratland and Barbara Coleman are thanked specially for technical help with the gravimetric fecundity and histological analyses, respectively. We are also grateful to C.T. Marshall, T. Jørgensen and the three referees (two identified themselves as Adriaan Rijnsdorp and Ronald L. Smith) for valuable comments.

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