Introduction. ICES Journal of Marine Science, 58: doi: /jmsc , available online at

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1 ICES Journal of Marine Science, 58: doi: /jmsc , available online at on An application of the annual egg production method to estimate the spawning biomass of cod (Gadus morhua L.), plaice (Pleuronectes platessa L.) and sole (Solea solea L.) in the Irish Sea M. J. Armstrong, P. Connolly, R. D. M. Nash, M. G. Pawson, E. Alesworth, P. J. Coulahan, M. Dickey-Collas, S. P. Milligan, M. F. O Neill, P. R. Witthames, and L. Woolner Armstrong, M. J., Connolly, P., Nash, R. D. M., Pawson, M. G., Alesworth, E., Coulahan, P. J., Dickey-Collas, M., Milligan, S. P., O Neill, M. F., Witthames, P. R., and Woolner, L An application of the annual egg production method to estimate the spawning biomass of cod (Gadus morhua L.), plaice (Pleuronectes platessa L.) and sole (Solea solea L.) in the Irish Sea. ICES Journal of Marine Science, 58: The spawning biomass of cod (Gadus morhua), plaice (Pleuronectes platessa) and sole (Solea solea) in the Irish Sea in 1995 was estimated by means of the annual egg production method (AEPM). The area surveyed corresponded to ICES assessment area VIIa. This paper describes the sampling design, methods of analysis, estimates of biomass, and sources of error in the estimates. Estimates are also presented for spatially separated spawning grounds of cod and plaice in the eastern and western Irish Sea, the first time that information at this scale has been available. The AEPM estimates of spawning biomass of cod, sole and plaice exceeded the corresponding estimates from Virtual Population Analysis of data from commercial fisheries and trawl surveys by factors of 2.3, 2.7 and 4.3 respectively. The sources of these large discrepancies are not yet resolved. Key words: egg production method, cod, plaice, sole, Irish Sea, spawning stock biomass. Received 6 September 1999; accepted 1 September M. J. Armstrong and M. Dickey-Collas: Agricultural and Environmental Sciences Division, Department of Agriculture and Rural Development, Newforge Lane, Belfast BT9 5PX, Northern Ireland; P. Connolly: Marine Fisheries Services Division, the Marine Institute, Abbotstown, Dublin 15, Ireland; M. F. O Neill: Dept of the Marine and natural Resources, Sea Fisheries Division, Leeson Lane, Dublin 2, Ireland; R. D. M. Nash: University of Liverpool, School of Biological Sciences, Port Erin Marine Laboratory, Port Erin, Isle of Man; E. Alesworth: formerly University of Liverpool; M. G. Pawson, S. P. Milligan, P. R. Witthames, and L. Woolner: Centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory, Lowestoft, Suffolk NR33 0HT, England; P. J. Coulahan: Dept of Environmental Resource Management, Faculty of Agriculture, University College Dublin, Dublin 4, Ireland. Correspondence to: M. J. Armstrong, mike.armstrong@dardni.gov.uk Introduction The spawning stock biomass (SSB) of an exploited species is an important variable in the management of fisheries. It is usually monitored using some form of sequential population analysis (SPA) of annual catch-atage data, tuned using time-series of relative abundance estimates from surveys and/or commercial catch rates. Egg production surveys provide a method of estimating SSB independent of any data on commercial catches, and may provide insights into the accuracy of SPA estimates. Time-series of egg production surveys offer the potential to track changes in SSB of individual stocks more accurately than can be obtained using commercial catches which may represent mixed stocks. They may also provide valuable data for tuning SPAtype assessments. Egg production surveys have been applied to a variety of pelagic and demersal species /01/ $30/0

2 184 M. J. Armstrong et al. including anchovies (Lasker, 1985; Armstrong et al., 1988), sardines (Lo et al., 1996), mackerel (Lockwood et al., 1981; Greer-Walker et al., 1987) and flatfishes (Heessen and Rijnsdorp, 1989; Anon., 1992; Lo et al., 1992; Horwood, 1992, 1993a). Three methods of estimating SSB from egg production have been devised to cope with the patterns of fecundity in different types of fish as well as the cost and logistics of mounting surveys. The annual egg production method (AEPM) uses estimates of the total annual production of planktonic eggs and the annual fecundity of the stock, and requires a series of plankton surveys throughout the spawning season (Lockwood et al., 1981). The daily fecundity reduction method (DFRM) estimates egg production and decline in population fecundity over part of the spawning season (Lo et al., 1992). The daily egg production method (DEPM) requires a single survey to estimate the mean daily egg production and fecundity of the stock at or near the annual peak of spawning (Parker, 1980). The first two methods are designed for species with determinate annual fecundity, i.e. those in which all the eggs to be spawned during the year are present and identifiable in the ovary immediately prior to spawning. DEPM surveys are designed for batchspawning fish with indeterminate annual fecundity (e.g. anchovy). This paper presents the results of an AEPM survey of cod, plaice and sole in the Irish Sea (ICES Division VIIa) in The assessments carried out in 1994 by ICES indicated that the spawning biomass of these stocks would decline close to or below historical low values by 1995 (Anon., 1995). In view of the very low SSB forecasts (ca t for each stock), and the implications for management of the fisheries, it was considered that AEPM surveys could provide valuable independent information on SSB. The method is considered appropriate for cod and plaice as there is strong evidence that they are determinate spawners. Immediately prior to spawning, a large hiatus in size distribution develops between the advanced yolk-filled oocytes and the precursor pre-vitellogenic oocytes (Kjesbu et al., 1990; Urban, 1991). Although Horwood (1990) considered the possibility of indeterminate spawning in plaice, his samples were collected several months prior to spawning and hence would have exhibited a less distinct gap between the size distributions of the two groups of oocytes. In sole, the size distribution of developing oocytes is less distinct than in cod and plaice. However, studies by Horwood and Greer-Walker (1990) and Witthames and Greer-Walker (1995) suggest that fecundity in this species may be determinate. The area chosen for the egg surveys encompasses a major spawning population of sole, distributed mainly in the eastern Irish Sea, and populations of cod and plaice with spatially separated spawning components in the western and eastern Irish Sea. Smaller spawning sites occur in other regions of the Irish Sea, particularly in Cardigan Bay. Data from all spawning components of each species are combined in the annual stock assessments carried out by ICES. Tagging studies have shown comparatively low rates of movement of plaice and sole between the Irish Sea and surrounding assessment areas (Griffith, 1966; Macer, 1972; Williams, 1965). Hence, the AEPM and SPA estimates of biomass of these species represent the same stocks and are directly comparable. Although there is evidence of seasonal migrations of mature cod between the western Irish Sea and the Celtic Sea (Brander, 1975), tagging studies in the 1990s have shown a low incidence of Irish Sea cod in catches taken in the Celtic Sea (P. Connolly, Marine Fisheries Research Services Division, Marine Institute, Dublin, unpublished data). Materials and methods Biomass model Spawning biomass was estimated using the following equations: SSB=AEP/(Fr.R.10 6 ) Fr=Fg AT AT=SD.I atr.p atr /D atr where SSB is the spawning biomass (t), AEP is the annual egg production at age zero (millions of eggs), Fr is the mean realised annual fecundity (eggs g 1 ),Ris the mean ratio of biomass of mature females to total SSB, Fg is the mean potential annual fecundity (eggs g 1 ), AT is the mean annual losses of eggs due to atresia (eggs g 1 ), SD is the mean spawning duration of individual females (days), I atr is the intensity of atresia (geometric mean atretic oocytes g 1 in females with atresia), P atr is the prevalence of atresia (mean proportion of mature females with atretic oocytes), D atr is the duration of atretic oocytes (number of days when atretic eggs are identifiable). The coefficient of variation (CV) of the estimate of SSB was calculated as: CV 2 (SSB)=CV 2 (AEP)+CV 2 (Fr)+CV 2 (R) The covariances were assumed to be small and were not estimated. The methods of sampling and analysis employed in the 1995 surveys are summarised below.

3 Annual egg production in the Irish Sea 185 Egg surveys Eleven ichthyoplankton surveys of between 51 and 106 stations were carried out from February June 1995 [Table 1(a)]. Eggs were sampled using high-speed plankton samplers with 76 cm diameter non-encased frames fitted with 40 cm diameter conical nose cones (Nash et al., 1998). Nets were constructed with 270-μm aperture mesh. A 400-μm net was used when signifciant clogging occurred, together with a 30 cm diameter nose cone if clogging persisted. Both nets had sufficiently small mesh to retain all sizes of fish eggs. Calibrated flowmeters were mounted internally and externally. Double oblique tows from the surface to 2 m from the seabed were carried out at a ship s speed of 4.5 knots. The sea temperature, integrated over the water column, was recorded at each station. Three different survey grids A C were applied as the spawning season progressed, according to expected distribution of eggs of plaice, cod and sole (Nichols et al., 1993; Figure 1). Sampling strata were specified as 1/8 ICES statistical rectangles (approximately 28 km 16 km). Two plankton stations were sampled in each rectangle in areas where high egg densities were expected. A survey design with the same spatial coverage as grid B, but with only one station per rectangle, was available to allow maximum coverage in the event of sampling difficulties (referred to as grid D in subsequent text). Eggs were identified on the basis of morphology (Russell, 1976). Whilst this method was considered accurate for plaice and sole, early stage eggs of cod are not distinguishable morphologically from those of haddock (Melanogrammus aeglefinus) which also occur in the Irish Sea. The relative production of eggs of the two species was inferred using data on late stage eggs, which can be identified from patterns of embryo pigmentation. The biochemical method isoelectric focusing (IEF; Mork et al., 1983) was applied at selected stations to investigate the relative abundance of early-stage eggs of gadoids. Embryonic development The number of eggs at each stage of embryonic development was recorded for each plankton sample. The eggs of cod and plaice were classified into one of six morphological stages (1A, 1B, 2, 3, 4, and 5) following the criteria described for plaice (Simpson, 1959) and simplified by Thompson and Riley (1981) for cod. Sole larvae hatch at the end of stage 4, and hence were allocated to the five stages 1A to 4 (Riley, 1973). Stages 1B and 2 of each species were combined for analysis as an exchange of eggs between laboratories showed a greater inconsistency in allocation of eggs between these two short stages than was the case for other stage transitions. The duration and median age of stages 1A, 1B/2, 3, 4 and 5 were determined from the relationships between temperature and rate of embryonic development given in Table 2 for North Sea stocks (Riley, 1973; Ryland and Nichols, 1975; Thompson and Riley, 1981). Estimation of daily egg production The density of eggs at each stage in a rectangle was estimated using standard formulae for raising the sampler catch-rates to numbers m 2. The density estimate was multiplied by the area of the rectangle represented by the station, and divided by expected stage duration to give the average number surviving in each rectangle per day s spawning. Stage duration was calculated from the appropriate temperature development relationships using the depth-integrated temperature at the station. The mean daily production for each stage over the whole survey area was obtained by summing over rectangles. Non-sampled rectangles were assumed to have a density of eggs equivalent to the arithmetic mean of the adjacent sampled rectangles. The total annual production per stage (average numbers after mortality) was calculated as the sums of products of average daily production in each survey and number of days of spawning for which the survey estimate was considered representative. Annual egg production was estimated for all stages of embryonic development considered fully represented in the plankton. The variance of the mean was calculated assuming log-normal distribution of production estimates and a constant coefficient of variation for each rectangle, using an analysis of variance of data from the rectangles with replicate stations (Pope and Woolner, 1984). An estimate of daily egg mortality rate Z was calculated for each species according to the pattern of decline over time in the annual production estimates for each stage. In the absence of further information, a simple exponential model of mortality was assumed, and estimates of Z and production at age zero (AEP) were estimated by maximising the likelihood function: where X(I) is the predicted annual production of eggs of stage I at average age t conditional on a given combination of AEP and Z. The variables N(I) and SE(I) are the survey estimate of production of stage I eggs and its standard error respectively. The expected mean age of eggs at each stage was calculated for each value of Z, as the median overestimates the average age of eggs in the sea. The estimated annual abundance of stage 1A eggs, for which the median age was less than one day, was also considered as a minimum estimate of AEP independent of any estimate of Z which could be biased.

4 186 M. J. Armstrong et al. Table 1. Sources of data and samples for estimating egg production and adult spawning parameters. See acknowledgements for laboratory acronyms. (a) Ichthyoplankton surveys Cruise code Dates Vessel Laboratory Grid Stations RV Feb RV Cirolana CEFAS A 100 RV Feb RV Cirolana CEFAS A 91 RV Mar RV Lough Beltra and Roagan MI/PEML D 51 RV Mar RV Lough Foyle QUB A 104 RV8 30 Mar 6 Apr RV Corystes CEFAS A 106 RV9/RV Apr RV Lough Beltra and Roagan MI/PEML A 106 RV Apr RV Lough Foyle QUB A 106 RV12 30 Apr 7 May RV Lough Foyle QUB B 105 RV May MFV Philomena PEML B 87 RV May RV Cirolana CEFAS B 97 RV Jun RV Roagan PEML C 60 (b) Adult sampling Cruise Code Dates Vessel Laboratory Type of sampling RV1 31 Jan 9 Feb RV Corystes CEFAS Beam trawl survey RV Feb RV Cirolana CEFAS Otter trawl RV Mar RV Corystes CEFAS Beam trawl survey RV May RV Cirolana CEFAS Beam trawl CC Feb MFV Bonafide QUB Mid-water trawl charter CC2 26 Mar 7 Apr MFV Celestial Shore QUB Mid-water trawl charter CC3 8 9 May MFV Philomena PEML Beam trawl charter CO1 25 Jan 5 Feb MFV Ocean Monarch QUB Mid-water trawl (observers) CO2; CO7 5 8 Feb; 6 10 May MFV Irish Rose MI Otter trawl (observers) CO3 CO6; CO8 31 Mar 16 May Belgian beam trawl fleet RSZV Beam trawl (observers) PS1; PS2 Various dates MI, CEFAS Port sampling

5 Annual egg production in the Irish Sea N Proportion of SSB comprising females, and mean size of mature females Catch-rates of mature cod in research trawl surveys of the Irish Sea have been low throughout the 1990s, and such surveys were considered inadequate for estimating population parameters in any one year. Hence, population parameters of cod were estimated from catches taken by commercial otter-trawlers and mid-water trawlers between late January and April 1995 [Figure 2(a); Table 1(b)]. Cod-end mesh sizes were generally 80 mm, effectively retaining all mature cod. In one case, a commercial mid-water trawler was chartered during March and April to carry out a survey of the western and eastern Irish Sea. Each trawl catch in each sampling exercise was assumed to provide a random sample of the cod population in the area fished. The mid-water and otter trawls gave different estimates of population parameters, presumably due to variations in the vertical distribution of cod. It was not possible to determine which method was least biased. Hence, the mean values of parameters from each sampling exercise were treated as independent point estimates and were averaged without any form of weighting. Population parameters of plaice and sole were estimated from stratified surveys of the whole Irish Sea in February and March 1995, carried out using a 4-m beam trawl deployed from a research vessel [Figure 2(b)]. The beam trawl was towed at 4 knots for h at each station. Each catch was taken to represent a random sample of the population in each survey stratum. Means and variances of population parameters were obtained for each survey stratum using standard ratio estimators. Overall survey means and variances were calculated using weighting factors for each stratum, specified as the product of stratum area and mean catch rate (kg h 1 for proportion female, numbers h 1 for mean weight of females) N Grid A Grid B 55 N Potential fecundity Females that were ripe but not yet spawning were collected randomly from catches, and their ovaries were preserved in buffered formaldehyde solution. Additional fish were collected on a length-stratified basis. Standard gravimetric techniques were adopted to estimate the total number of vitellogenic oocytes in cod and plaice after suspension in Gilson s preservative, with histological screening to exclude fish with post-ovulatory follicles (Greer-Walker et al., 1986). A stereometric method (Emerson et al., 1990; Witthames and Greer-Walker, 1995) was used to estimate fecundity in sole. The mean Grid C 3 W Figure 1. Station positions for estimation of mean daily egg production during ichthyoplankton surveys of the Irish Sea at different times of the spawning season in 1995 (see Table 1 for grid used in each survey).

6 188 M. J. Armstrong et al. Table 2. Parameters of relationships expressing the age of eggs at end of each stage of embryonic development as a function of temperature (ages in days, temperature in C), published for stocks from the North Sea. Cod Sole Plaice Stage a b a b k t 0 D 0 1A B Cod: age=e at+b (Thompson and Riley, 1981). Sole: age=e sln(t)+b (Riley, 1973). Plaice: age=k/(t t 0 ) D 0 (Ryland and Nichols, 1975). 55 N (a) 55 N (b) Cumbrian coast Western Irish Sea Liverpool Bay Cardigan Bay W W Figure 2. (a) Areas sampled for cod population parameters in Hatched area: port sampling (PSI) and cruises CC1, CO1, C02 and C07. Dashed line indicates area of mid-water trawl survey CC2 [Table 1(b)]. (b) Stations and strata for estimation of plaice and sole population parameters during beam trawl surveys RV1 and RV7. fecundity of females F i in each survey stratum i was predicted from a linear regression of fecundity against fish weight (whole weight for plaice and sole, gutted weight for cod), according to the mean weight of mature females Wf i. Relative potential fecundity Fg i was obtained as F i /Wf i. Armstrong et al. (1988) show that the variance estimation may be simplified by specifying, for each sampling area, a new variable Q=Wf/F (i.e. the inverse of Fg). The squared coefficient of variation of Q, which will be equivalent to that of Fg, is given as (dropping area subscripts for convenience): V(Q)/Q 2 =[(MS/n F,W )+S 2 b(wf Wfs) 2 ]/F 2 +{[1 (b.q)]/ F} 2.V(Wf)/Q 2 where MS is the mean squared deviation from the regression, n F,W is the number of observations in the regression, S 2 b is the variance of the slope b of the regression, Wfs is the mean weight of females in the regression, and b is the regression slope. The first term gives the variance associated with the regression whilst the second term reflects the variance of Wf and the covariance of Wf and F. The mean and variance of Fg for the total population were obtained as weighted averages over survey strata. The weighting factors were the product of stratum area and mean catch rate of mature females in numbers. For cod, mean size of mature females was estimated only for the western Irish Sea because of the small sample sizes for the eastern region. Estimates of mean female size and Fg for plaice and sole were obtained from the beam trawl surveys by stratum. Spawning duration An estimate of the duration of spawning by individual fish is required for calculating annual losses of eggs due to atresia. Samples of mature fish were collected regularly throughout the spawning season, and the maturity

7 Annual egg production in the Irish Sea 189 stages (verified histologically when necessary) were recorded. The spawning duration in plaice and cod was estimated as the time elapsed between 50% of females at stage V (oocytes transparent due to hydration, but not yet ovulated) to 50% at stage VII (spent) and stage II (recovering spent) (Iles, 1964). This method could not be implemented for sole because sampling finished before the end of the spawning season. For this species, the median value of residual fecundity (number of eggs g 1 not yet spawned) was estimated for successive sampling events over the spawning season. The median was adopted as a robust estimate of the central tendency in the population, because of the large variability of estimates and relatively small sample sizes. The median values were regressed against time, and the completion date of spawning was estimated as the predicted time at which residual fecundity was equivalent to the estimated batch fecundity. Atresia of oocytes Fifty or more mature fish of each species were sampled at random from research or commercial hauls on at least two occasions at one or more of the regions of high spawning activity. Ovaries were examined using histology to select spawning or spent fish and to assess the prevalence of atresia, P atr (proportion of mature females with early alpha-atretic oocytes in the ovary) and the intensity of atresia, I atr (the geometric mean of the numbers of early alpha-atretic oocytes g 1 fish weight, in fish with atresia). The geometric mean was used to reduce the influence of some unrealistically high individual values, at the expense of introducing some bias. The early alpha-atretic stage has been described in sole (Witthames and Greer-Walker, 1995) and cod (Kjesbu et al., 1991), and these criteria were applied to plaice. Annual losses due to atresia in cod and plaice (AT, eggs g 1 ) were calculated using expression (3) (Anon., 1996). For plaice and sole, duration of the atretic stage (D atr ) was assumed to be nine days (Horwood, 1993a,b). For cod, a value of ten days was used (Kjesbu et al., 1991). Estimates of AT were obtained for a series of sampling periods covering the spawning duration of the fish, and a weighted average was obtained using the duration of the sampling periods as weighting factors. In the case of sole, where very high levels of atresia were observed, daily losses (calculated as I atr.p atr /D atr ) were found to decline linearly with time, and the annual losses were calculated by integrating under the regression line between the start date of spawning and the date when losses reach zero. Variance of the annual loss due to atresia was estimated from the variances and covariances of the regression parameters. (Note that the incidence of atresia on a particular sampling date reflects the mean of the preceding nine days.) Realised fecundity F r The realised fecundity (eggs g 1 ) was calculated as the difference between potential fecundity Fg and annual losses due to atresia, AT. Results Identification of eggs The size range of late-stage eggs of cod, identifiable from embryo pigmentation, was mm. Of these eggs, 98% were within the size range mm used for classification of early-stage eggs of cod in the preserved samples. Some unusual spikes were apparent at the lower end of this size range, particularly in samples from the Liverpool Bay area of the eastern Irish Sea. This indicated possible mis-identification of eggs of species such as witch (Glyptocephalus cynoglossus) and whiting (Merlangius merlangus). Although most of the eggs of these species are smaller than 1.24 mm, the size ranges overlap with that of cod. The potential over-estimation of cod SSB in the eastern Irish Sea, caused by mis-identification of eggs, is discussed later. The size range of late stage eggs of haddock ( mm) was similar to that of cod. However, this species comprised only 2% of late-stage eggs identified as cod and haddock on the basis of pigmentation. Although the sampling for IEF proved too limited for reliable estimation of species composition of early stage eggs, more than 95% of eggs in the size range mm were identified as cod. The egg production estimates for cod were reduced by 2% to allow for the occurrence of haddock eggs, based on relative abundance of late stage eggs. Spatial and temporal pattern of spawning The distribution of eggs of the three species followed the pattern observed in earlier surveys (Nichols et al., 1993). Figure 3(a) (c) show the distribution of stage 1 eggs at, or close to, the peak of the spawning period for each species. Eggs of cod were most abundant off the Irish coast, the south west coast of the Isle of Man, and in the eastern Irish Sea [Figure 3(a)]. Spawning by plaice was mainly confined to the shallow sandy regions close to the Irish Coast and in the eastern Irish Sea [Figure 3(b)], whilst spawning by sole was mainly in the eastern Irish Sea and to the south and southwest of the Isle of Man [Figure 3(c)]. Densities of eggs at the periphery of the survey grids were generally very low, indicating that drift of eggs into or out of the area surveyed may have been a comparatively small fraction of the total annual production. Figure 4(a) (c) show the seasonal pattern of egg production of each egg stage, for the survey area

8 M. J. Armstrong et al. 55 N 54 (a) Daily production ( 10 9 ) (a) Plaice Feb 03 Mar 02 Apr 02 May Date 01 Jun N (b) Scotland Daily production ( 10 9 ) (b) Cod Feb 03 Mar 02 Apr 02 May Date 01 Jun 54 Ireland N Northern Ireland (c) Irish Sea Isle of Man Wales England Daily production ( 10 9 ) (c) Sole Feb 03 Mar 02 Apr 02 May Date excluding Cardigan Bay where sampling did not take place later in the survey period. Some spawning of cod and plaice was recorded during the first survey in February. Daily production of stage 1A plaice eggs reached a peak in March, whilst cod spawning peaked in the first week of April. Spawning by cod and plaice was effectively completed by May. In contrast, spawning by sole was at very low levels prior to the middle of March, peaked between mid-april and late May, and had not been completed by the final survey in June. Spawning by sole appeared to commence earlier in Liverpool Bay than off the coast of Cumbria. Egg mortality and annual egg production 01 Jun Figure 4. Seasonal pattern in mean daily egg production, by stage of development., stage 1A;, stage 2;, stage 3;, stage 4;, stage 5. The estimated annual production of eggs of each species is given by area and stage of development in Table 3, W Figure 3. Distribution of stage 1 eggs near the peak of spawning: (a) cod, April (cruise 9); (b) plaice, March (cruise 6); (c) sole, 30 April 7 May (cruise 12). Contours are eggs m 2.

9 Annual egg production in the Irish Sea 191 Table 3. Estimated annual abundance of eggs ( 10 9 ) by stage of embryonic development. Coefficients of variation of the estimates are in parentheses. Stage 1A Stage 1B/2 Stage 3 Stage 4 Stage 5 (a) Cod Western Irish Sea (0.187) (0.206) (0.175) (0.484) (0.215) Eastern Irish Sea (0.235) (0.234) (0.201) (0.278) (0.182) Cardigan Bay (0.753) (0.474) (0.404) (0.937) (0.828) Total Irish Sea (0.144) (0.151) (0.129) (0.409) (0.165) (b) Plaice Western Irish Sea (0.437) (0.406) (0.255) (0.220) (0.256) Eastern Irish Sea (0.200) (0.204) (0.176) (0.167) (0.191) Cardigan Bay (94) (0.643) (00) (0.649) (0.919) Total Irish Sea (0.188) (0.180) (0.141) (0.154) (0.232) (c) Sole Western Irish Sea (0.159) (0.145) (0.120) (0.657) Eastern Irish Sea (0.114) (0.120) (0.092) (0.160) Cardigan Bay (0.477) (0.438) (0.300) (1.100) Total Irish Sea (0.102) (0.107) (0.082) (0.159) together with coefficients of variation. In most cases the estimates of annual production of each stage of eggs did not differ significantly from the simple exponential mortality curve fitted by maximum likelihood (Figure 5). Data for plaice eggs in the western Irish Sea conformed particularly closely to the exponential model, although the precision of the individual production estimates was comparatively poor. The production of cod eggs of stages 1A, 3, 4, and 5 conformed to the exponential model whilst production of stage 1B/2 eggs appeared higher than expected and was largely weighted out of the analysis. This could reflect errors in identification of early-stage eggs, an under-estimate of the duration of the combined stage 1B/2, or even real variations in mortality rate at different stages of development. The estimate of mortality (Z) for cod eggs in the eastern Irish Sea ( d 1, Table 4) was significantly larger than obtained for the western region ( d 1 ). This reflected the unexpected large number of early stage eggs in the eastern region, particularly at the lower end of the size range used for cod. Unfortunately, IEF sampling in the eastern Irish Sea was too limited to provide identification of early-stage eggs. The estimates of Z for plaice eggs in the western and eastern Irish Sea were similar at d 1 and d 1 respectively and were close to the estimate for western Irish Sea cod. Mortality of sole eggs was estimated only for stages 1 3 because spawning was not completed by the final plankton survey, contributing to a very low estimate of abundance of stage 4 eggs. The mortality rate of d 1 was high compared with the estimates for cod and plaice. The maximum likelihood estimates of annual egg production for cod, plaice and sole at age zero exceeded the stage 1A abundance estimates by 19 43%, 32 34% and 40% respectively (Table 4). Hence there is potential for large errors in the AEP estimates if the assumption of a constant rate of mortality throughout the embryonic period is incorrect. Population structure Sampling of cod was confined mainly to the western region where most commercial fishing for this species in the Irish Sea takes place. Five mid-water trawl hauls were made in the eastern Irish Sea in April, but the data were considered unreliable because only one haul took cod in sufficient numbers. Hence, the population parameters estimated for the western spawning population were assumed to apply also to the eastern region. Estimates of mean weight of mature female cod and

10 192 M. J. Armstrong et al. Egg production ( 10 9 ) 4000 Westen Irish Sea cod Age (d) Egg production ( 10 9 ) 2000 Westen Irish Sea plaice Age (d) Egg production ( 10 9 ) 4000 Eastern Irish Sea cod Age (d) Egg production ( 10 9 ) 2000 Eastern Irish Sea plaice Age (d) Egg production ( 10 9 ) 4000 Whole Irish Sea cod Age (d) Egg production ( 10 9 ) 2000 Whole Irish Sea plaice Age (d) Egg production ( 10 9 ) Whole Irish Sea sole Age (d) Figure 5. Mortality curves fitted to estimates of annual production of eggs ( 2 s.e.) at the average age in each stage of development. Table 4. Estimates of daily mortality (Z), annual egg production at age zero (AEP) and annual abundance of stage 1A eggs ( 10 9 ). Standard errors in parentheses. Cod Plaice Sole West East Whole West East Whole Whole Z (0.030) (0.028) (0.023) (0.032) (0.015) (0.017) (0.030) AEP (324) (341) (494) (159) (148) (243) (287) Stage 1A (286) (281) (410) (178) (162) (249) (202)

11 Annual egg production in the Irish Sea 193 Table 5. Estimates of population parameters for cod (proportion of mature stock comprising females, by number and by weight; mean length of mature females and males), for different methods of capture. Standard errors in parentheses. Method of capture Area Dates No. hauls R (weight) R (Nos.) Lf (cm) Lm (cm) Wf. (g) (1) Otter trawl West 13 Jan 24 Apr PS1 (0.036) (0.036) (1.4) (2.7) (227) (2) Otter trawl West 5 8 Feb CO2 (0.076) (0.060) (2.5) (2.3) (402) (3) Mid-water West 25 Jan 5 Feb CO1 (0.023) (0.014) (0.9) (1.0) (156) (4) Mid-water West Feb CC1 (0.030) (0.029) (1.3) (1.5) (234) (5) Mid-water West 26 Mar 7 Apr CC2 (0.045) (0.055) (0.9) (1.9) (147) (6) Mid-water East 5 Apr CC2 (0.023) (0.016) (2.8) (3.1) (400) (7) Groundfish survey Whole Irish Sea March: per survey (n/a) Mean (1 5) West Jan Apr (0.028) (0.041) (1.9) (2.4) (286) proportion of SSB comprising mature females (R) varied according to method of capture, and tended to be greater in mid-water trawl catches than in otter trawl catches (Table 5). Averaged over all commercial sampling exercises in the western Irish Sea, the mean proportion female by number in catches of mature cod was only slightly less than 50% (Table 5). However, females comprised more than 50% of the catch weight of mature cod. The sensitivity of the SSB estimate to using population parameter estimates only from otter trawl or mid-water trawl samples is considered later. The distribution of mature male plaice in the beam trawl survey RV1 was more patchy than that of females, resulting in poor precision in estimates of R in each stratum [Table 6(a)]. The estimate of R for the Cumbrian coast ( ) was substantially higher than the estimate for Liverpool Bay ( ), although the weighted mean for the eastern Irish Sea was very close to 0. The mean weight of mature female plaice off Cumbria was almost 50% larger than in Liverpool Bay. The estimates of R for the western Irish Sea and Cardigan Bay were similar. Data from the March beam trawl survey RV7 were not used for plaice because of potential errors in discriminating immature fish from spent fish. Both beam trawl surveys RV1 and RV7 provided data for estimation of sole population parameters. The overall biomass indices for mature males and females were very similar between the two surveys, as were the estimates of Wf and Lf [Table 6(b),(c)]. Estimates of R were more variable, with some strata containing relatively few males. Population estimates were obtained as simple averages of the estimates from the two surveys. The final estimate of R= reflects the greater size reached by female sole compared with males. Potential fecundity The fecundity weight relationships were linear for all stocks in all areas (Figure 6, Table 7). Whilst the intercepts in each case were not significantly different from zero, they were negative in all cases. Regressions of Fg against fish length or weight had slopes significantly greater than zero at the 5% error level. Hence, it was necessary to estimate the mean weight of females in the population in order to estimate mean fecundity. Samples for cod were derived mainly from the western Irish Sea (only ten ovaries were collected from the eastern region). Mean potential fecundity in the population was estimated to be eggs g 1 gutted weight based on a mean weight of mature females of 4829 g. This estimate was adopted for the western and eastern Irish Sea. If mean weights are calculated using only the otter or pelagic trawl estimates in Table 5, the mean Fg is 845 or 861 eggs g 1 respectively. Fecundity of plaice in the western Irish Sea was lower than in the eastern region [Figure 6(b) (e)]. For a nominal fish weight of 300 g, estimates of Fg in the eastern Irish Sea and Cardigan Bay were similar at eggs g 1 and significantly higher than the figure of 196 eggs g 1 for the western Irish Sea. This is also reflected in the mean Fg per survey stratum [Table 6(a)]. The stereometric estimates of fecundity in sole were consistently larger (9% on average) than those obtained

12 194 M. J. Armstrong et al. Table 6. Population parameters of plaice and sole estimated during beam trawl surveys RV1 and RV7. Biomass indices are mean survey catch-rates of mature males or females multiplied by area of stratum. Cumbria Liverpool bay Irish Sea West Cardigan Bay Total mean s.e. mean s.e. mean s.e. mean s.e. mean s.e. (a) Cruise RV1: Plaice Survey area (km 2 ) Biomass index: females Biomass index: males Wf (g) Lf (cm) R Fg (eggs g 1 ) (b) Cruise RV1: Sole Biomass index: females Biomass index: males Wf (g) Lf (cm) R (c) Cruise RV7: Sole Biomass index: females Biomass index: males Wf (g) Lf (cm) R

13 Annual egg production in the Irish Sea 195 F ('000 eggs) (a) F ('000 eggs) 500 (b) Wf (g) Wf (g) F ('000 eggs) 500 (c) F ('000 eggs) 500 (d) Wf (g) Wf (g) F ('000 eggs) 500 (e) F ('000 eggs) (f) Wf (g) Wf (g) F ('000 eggs) (g) Wf (g) Figure 6. Regressions of total potential fecundity (F) against female weight (Wf: gutted weight for cod, whole weight for plaice and sole), by species and sampling area. (a) Cod whole Irish Sea; (b) Plaice Cumbrian Coast; (c) Plaice Liverpool Bay; (d) Plaice western Irish Sea; (e) Plaice Cardigan Bay; (f) Sole eastern Irish Sea; (g) Sole western Irish Sea. Table 7. Parameters regressions of potential fecundity (eggs female 1 ) against female weight (whole weight for plaice and sole, gutted for cod; g) estimated during 1995 in the Irish Sea. Wfs=mean fish weight in regression data; MS=mean squared deviation from the regression. Species Area Wfs Slope s.e. (slope) Intercept MS N. obs Cod Whole Irish Sea Plaice Cardigan Bay West. I. Sea Cumbria Liverpool Bay Sole Eastern I. Sea Western I. Sea Common slope fitted by ANCOVA.

14 196 M. J. Armstrong et al. Table 8. Estimates of potential and realised fecundity in sole, with standard errors. Area Weighting Wf 2 factor 1 g Fg eggs g 1 s.e. AT 3 eggs g 1 s.e. Fr eggs g 1 s.e. Eastern Irish Sea Western Irish Sea Total From combined biomass indices for mature females in cruises RV1 and RV7. 2 Weighted mean estimates from RV1 and RV7. 3 AT estimates for eastern Irish Sea applied to western region. for the same fish using the gravimetric method. This was partly caused by the effect of the different chemical treatment of the ovarian tissue on distinguishing between vitellogenic and pre-vitellogenic oocytes. It was not possible to decide which method was least biased. The stereometric method was adopted for estimating population mean fecundity, which was examined separately for fish collected off Cumbria, in Liverpool Bay and in the western Irish Sea. Total potential fecundity increased linearly with fish weight in the three areas. A general linear models procedure estimating a common slope but different intercepts to data from the western Irish Sea and the combined eastern Irish Sea strata provided the best fit to the data [Table 7, Figure 6(f),(g)]. Relative fecundity Fg was weakly correlated with female weight (p<0.02). The mean Fg for the Irish Sea was eggs g 1 (Table 8). Spawning duration and oocyte atresia Spawning duration of individual cod was approximately 40 d [Figure 7(a)]. However, atresia was found to be infrequent and of very low intensity, and was recorded mainly in spent fish at the end of the spawning season. A prevalence of 15 17% was recorded in March and April with geometric mean intensity of only eggs g 1, resulting in an annual loss of potential fecundity of only 2 eggs g 1. Spawning duration of plaice in Liverpool Bay and off Cumbria was very similar to the estimate for the western Irish Sea and Cardigan Bay, although both estimates were much lower than expected [13 14 d; Figure 7(b),(c)]. Of the 116 samples screened for atresia, only four had atretic oocytes present and these were all spent fish with advanced atresia. Prevalence and intensity of atresia in spawning and pre-spawning fish was estimated to be zero, and realised fecundity of plaice was therefore equivalent to potential fecundity. The Iles method could not be applied to estimate spawning duration in sole because sampling ceased before 50% of the females were recorded as spent. Median values of residual fecundity (eggs g 1 ) were calculated from samples collected in Liverpool Bay on Percentage Percentage Percentage (a) Western Irish Sea cod Jan 0 30 Jan 1 Mar 31 Mar Date (b) Eastern Irish Sea plaice Feb 14 Feb 1 Mar Date 30 Apr 16 Mar (c) Western Irish Sea and Cardigan Bay plaice Feb 3 Mar Date 17 Mar Figure 7. Spawning duration of cod and plaice: seasonal trends in the proportion of females that are mature but not yet spawning (ovary stages 3 and 4; hatched), in the process of spawning (stages 5 and 6; open) or spent or spent/recoverying (stages 7 and 2; stippled). 14 and 29 April and 15 May. Although only three observations were available, a linear regression was fitted [Figure 8(a)]. A spawning duration of 59 d was calculated as the time elapsed from 2 April (t=92 d), when 50% of females had ovaries with fully hydrated oocytes (stages 5 and 6), and the time when the Fg(res)

15 Annual egg production in the Irish Sea 197 Fg (res) (eggs g 1 ) AT (eggs g 1 d 1 ) (a) (b) Fg (res) = t R 2 = t (days from 1 January) AT = t R 2 = 0.92 t (days from 1 January) Figure 8. (a) Spawning duration of sole: decline in median residual fecundity (Fg(res)) over time; (b) decline in mean daily losses of eggs due to atresia over the spawning period (AT), given as averages over all mature female sole sampled in Liverpool Bay. regression gave a value equivalent to the batch fecundity of 20 eggs g 1. Levels of atresia in sole were high and variable during the spawning season. From the beginning of April to mid-may, the prevalence of mature females with atretic oocytes varied between 56 94%. The geometric mean number of atretic oocytes in the samples declined from 95 eggs g 1 near the commencement of spawning to 5 eggs g 1 at the end of the spawning season when residual fecundity was low. Daily losses of eggs through atresia, averaged over all mature females sampled in Liverpool Bay, declined from 9 eggs g 1 to zero within 44 days of the commencement of spawning [Figure 8(b)]. Integrating under the regression line gave a total loss of eggs g 1 over the spawning period. This represents an annual loss due to atresia of 28% of total potential annual egg production. Only one sample of sole from the western Irish Sea, collected on 1 May, was screened for atresia. The loss of eggs from all mature females in this sample was estimated at 2.3 eggs d 1 compared with the regression prediction of 2.9 eggs d 1 for sole from the eastern Irish Sea on 1 May. It was concluded that rates of atresia in the western Irish Sea were comparable with those in the east, and hence that 28% of total annual egg production would be lost in this region. Estimates of potential fecundity, atresia losses and realised fecundity in Irish Sea sole are summarised in Table 8. AEPM estimates of biomass Distinct spawning grounds in the western and eastern Irish Sea were observed for cod and plaice, whereas sole spawning was located mainly in the central and eastern region. Total SSB of cod was estimated to be 8.5 kt [CV=15%; Table 9(a)]. The estimate was split almost evenly between the eastern and western Irish Sea with negligible biomass in Cardigan Bay. Basing the estimate only on population parameters from mid-water trawl samples gave SSB=7.9 kt compared with 9.5 kt using samples from otter trawls only. Total egg production of plaice in the eastern Irish Sea was double that estimated for the western Irish Sea [Table 9(b)]. However, the higher mean fecundity and sex ratio estimated for the eastern region resulted in an estimated SSB only 24% higher than in the west, although the precision of the estimate for the western region was poor. Total SSB was estimated to be 16.0 kt (CV=17%). The regional composition of the SSB estimate was as follows: 52% in the eastern Irish Sea, 42% in the western Irish Sea and 6% in Cardigan Bay. The estimated SSB of sole for the whole Irish Sea, including Cardigan Bay, was kt [CV=14%; Table 9(c)]. Discussion Comparison of population parameters with previous estimates The relationship between fecundity and length in plaice sampled in Cardigan Bay in the present project is similar to that given by Horwood (1990) for the same region. The estimates of fecundity in the eastern Irish Sea are also similar to estimates given by Horwood (1993b) for the northern Celtic Sea. The published fecundity size relationship for Irish Sea sole sampled in Liverpool Bay (Witthames and Greer-Walker, 1995) is based on fish length, whereas fish weight was used in the present study. However, the results appear to be similar. Whilst there are no previous estimates of fecundity for Irish Sea cod, data from other stocks show considerable regional variation. No previous estimates of spawning duration were available for Irish Sea cod and plaice. The estimate of spawning duration of 14 d for plaice was consistent between the western and eastern Irish Sea but much lower than the estimate of 35 d given by Rijnsdorp (1989) for plaice in the North Sea. Individual plaice from the Irish Sea have been observed to spawn over periods well in excess of 14 d in aquaria (R. D. M. Nash, Port Erin Marine Laboratory, unpublished). This suggests that the beam trawl surveys may not provide representative samples of all maturity stages of plaice. In contrast, the estimate of spawning duration of 40 d for cod is comparable with the average

16 198 M. J. Armstrong et al. Table 9. Estimates of variables and coefficients of variation for calculation of spawning stock biomass of cod, plaice and sole in the Irish Sea by means of the annual egg production method. Whole Irish sea includes Cardigan Bay. Whole Irish Sea Western Irish Sea Eastern Irish Sea Variable Mean CV (%) Mean CV (%) Mean CV (%) (a) Cod AEP ( 10 9 eggs) SD (days) AT (eggs g 1 ) Fg (eggs g 1 ) Fr (eggs g 1 ) R Wf (g) gutted factor IEF correction SSB (kt) (b) Plaice AEP ( 10 9 eggs) SD (days) AT (eggs g 1 ) Fg (eggs g 1 ) Fr (eggs g 1 ) R Wf (g) SSB (kt) (c) Sole AEP ( 10 9 eggs) SD (days) 59 AT (eggs g 1 ) Fg (eggs g 1 ) Fr (eggs g 1 ) R Wf (kg) SSB (kt) spawning duration of 50 d recorded in laboratory reared Norwegian cod (Kjesbu, 1989). The estimated spawning duration of sole of 59 d was consistent with the estimate of 60 d obtained for North Sea sole in 1991 (Anon., 1992). No previous estimates of atresia in Irish Sea cod and plaice are available, although atresia has been recorded in other areas. Captive Norwegian cod fed on moderate rations showed a linear relationship between intensity of atresia and proportion of eggs spawned, with losses due to atresia of 36% of potential fecundity (Kjesbu et al., 1991). Plaice kept in the laboratory by Horwood et al. (1989) had low rates of atresia even when fed small rations. The present study showed insignificant levels of atresia in wild cod and plaice captured in the Irish Sea in In contrast, 28% of the potential annual fecundity of sole captured in the Irish Sea in 1995 was lost through atresia. The estimate of 31% given by Horwood (1992) for Celtic Sea and Bristol Channel sole assumed a spawning duration of 40 d, and would equate to an annual loss of 46% of potential fecundity with a spawning duration of 59 d. Witthames and Greer-Walker (1995) found high prevalence of atresia in North Sea sole (45% 57%) causing an annual loss of 12% of potential fecundity over 60 d spawning. The high rates of atresia in this species introduces a considerable additional demand for sampling, requiring the estimation of four additional variables over a period of up to two months. The inherent assumptions and potentially high sampling error in estimates of atresia limit the effectiveness of