- Email: [email protected]
Condition of cod (Gadus morhua) off Greenland during 1982–1998
Fisheries Research 48 (2000) 79±86
Condition of cod (Gadus morhua) off Greenland during 1982±1998 Josep Lloreta,*, Hans-Joachim RaÈtzb a
Institut de CieÁncies del Mar Ð CSIC, Passeig Joan de Borbo sn, E-08039 Barcelona, Catalonia, Spain b Institut fuÈr See®scherei, Palmaille 9, D-22767 Hamburg, Germany Received 1 June 1999; received in revised form 31 August 1999; accepted 27 November 1999
Abstract An analysis of the condition (Fulton's K) of cod (Gadus morhua) off Greenland during autumn in the period 1982±1998 is presented. The paper addresses the interannual variations in condition and attempts to relate these to variations in water temperature. No size, age, sex, maturity nor geographical differences were observed. Condition of cod was positively related to water temperature. Mean condition factor calculated from total weights for the entire period was 0.89. Hepatosomatic and gonadosomatic indices are also presented for year 1998. Overall, the condition of cod off Greenland was among the lowest observed in natural populations of this species. # 2000 Elsevier Science B.V. All rights reserved. Keywords: Atlantic cod; Gadus morhua; Greenland; Condition factor; Fulton's K; Hepatosomatic index; Gonadosomatic index
1. Introduction Since 1982, the demersal ®sh assemblage in Greenlandic waters has undergone fundamental changes in species composition and abundance, with the collapse of the ecologically and economically important cod (Gadus morhua) and golden red®sh (Sebastes mentella) stocks which almost disappeared from survey catches (RaÈtz, 1997). Other species inhabiting the area like American plaice (Hippoglossoides platessoides), Atlantic wolf®sh (Anarhichas lupus) and starry skate (Raja radiata) displayed a less pronounced decrease in abundance but decreased in biomass by more than 50% (RaÈtz, 1997). The cod stock, for a long time being considered the main commercial and biological spe*
Corresponding author. Tel.: 34-93-2216416; fax: 34-93-2217340. E-mail address: [email protected] (J. Lloret)
cies of the area, already collapsed at the end of the 1960s decade and remained at a very low level since then (Anon, 1996). Fishing activities appeared to have been the main responsible factor for the observed declines (Lloret, 1997; RaÈtz et al., 1999). In addition to this major anthropogenic effect, studies on climatic and oceanographic conditions around Greenland (Buch and Stein, 1989) revealed concomitant interannual changes in the ocean and atmosphere which have in¯uenced ®sh biomass production in this area (Buch et al., 1994; Stein and Lloret, 1995; RaÈtz et al., 1999). Simple condition indices (e.g. Fulton's K condition factor, hepatosomatic index and gonadosomatic index) have been demonstrated to be a measure of the energy reserves of ®sh, e.g. Atlantic cod (Lambert and Dutil, 1997b), cod with a low condition index presumably resulting from adverse environmental, poor feeding conditions or parasitic infections
0165-7836/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 5 - 7 8 3 6 ( 0 0 ) 0 0 1 1 1 - 9
80
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
(Lambert and Dutil, 1997b; Yaragina and Marshall, 2000). Condition indices of cod have been shown to follow interannual variations and seasonal cycles, with lower energy reserves occurring during spawning (Dambergs, 1964; Jangaard et al., 1967a,b; Eliassen and Vahl, 1982; Taggart et al., 1994; Shelton and Lilly, 1995; Lilly, 1996; Lambert and Dutil, 1997a). Poor condition (i.e. lower available energy reserves) can have several consequences for stocks (Lambert and Dutil, 1997a). Reproductive success can be reduced through lower fecundity and reduction in egg quality (Kjesbu et al., 1992; Lambert and Dutil, 1998; Marshall et al., 1999). Poor condition may also lower the chances of survival of big ®sh, leading to an increase of natural mortality (Love, 1958; Wilkins, 1967; Krivobok and Tokareva, 1972). Fulton's K condition factor is one of various formulations used to evaluate the weight±length relationship in ®sh (Bolger and Connolly, 1989). It was selected because of its simplicity of calculation and because it converts a twodimensional weight±length relationship into a single statistic that gives a simple indication of the ``wellbeing'' of a ®sh (Lambert and Dutil, 1997b). The major disadvantage of Fulton's K condition factor is the assumption of an isometric growth in ®sh (b3 in the formula K W=Lb ). If this assumption is seriously violated, problems of correlation between condition factor and length could arise. The aim of this study was to examine the annual condition of cod during the period 1982±1998 from samples obtained during German annual ground®sh surveys, and to test the in¯uence of interannual water temperature ¯uctuations on it. Age, size, sex, maturity and geographical differences in condition are also tested, and we describe the hepatosomatic and the gonadosomatic indices of cod during the survey in 1998. The condition values of cod off Greenland are compared with those of other stocks. 2. Materials and methods Weight and length measurements of individual cod were derived from annual German ground®sh surveys covering shelf areas and the continental slope off west and east Greenland. The surveys, which were performed in autumn, commenced in 1982 and were primarily designed for the assessment of cod. The
standard gear used was the 140 ft bottom trawl with a 22 m horizontal opening rigged with heavy ground gear and equipped with a small mesh liner inside the cod end. The towing time was 30 min. The survey covered shelf areas and the continental slope at the 3 mile offshore line. Due to a pronounced heterogeneity of cod distribution (RaÈtz, 1996), the survey area was subdivided into different geographic and depth strata, with seven geographic strata which were split into two depth strata covering the 0±200 and 201± 400 m zones (Fig. 1). The strategy applied included a distribution of the sampling effort according both to the stratum areas and to cod abundance. Consequently, 50% of the hauls were allocated proportionally to stratum by stratum area while the other 50% were apportioned on the basis of a review of historical mean cod abundance. The hauls were randomly distributed within trawlable areas of the various strata. Nontrawlable areas were mainly located inshore. During 1982±1998, 2418 successful sets were carried out. Further information on the ®shing strategy is given by RaÈtz (1997). Fork length (cm) and total (whole body) weight (5 g) of all individual cod in the catch were measured yearly since 1982. Sex and maturity were determined. Three maturity stages were used to identify the reproductive state of ®sh in autumn. Males and females having nearly transparent testis/ovaries were classi®ed as stage 1 (immature), while those with whitish testis or reddish ovaries (but without running milt or visible eggs, respectively) were classi®ed as stage 2 (mature-resting). When testis were white with running milt (males) or eggs were visible (females), individuals were classi®ed as stage >2 (mature-spawning). Age determinations was done by the staff of the Institut fuÈr See®scherei (Hamburg) from the otoliths collected each year during the period 1982±1998, according to the methodology described by RaÈtz (1994). Data were not available during years 1983± 1986, and in 1988. Gutted (carcass) weight (5 g) was also measured since 1992. Table 1 shows the annual number of ®sh sampled by area, sex and maturity stage, and the annual mean total weight, length and age. During the 1998 survey, liver and digestive tract (stomach and intestine) weights (5 g) were also taken from the 85 cod captured, while gonad weight was measured in 76 of them.
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
81
Fig. 1. Survey area and stratification as specified in Section 2.
Fulton's K condition factor and the hepatosomatic index (HSI) were used as main indicators of the condition of cod. The gonadosomatic index (GSI) was used as a complementary index of the condition. Interannual variations in the condition of cod since 1982 were assessed by calculating for each year the Fulton's K condition factor from all samples of length and weights. The K condition factor was expressed as W K 100 3 L where W is the total weight (g) and L is the fork length (cm). The stated formula, with the constant3, assumes an isometric growth in ®sh, and thus a heavier weight for a given length corresponds to a better condition. However, the use of gutted (carcass) weight or somatic weight (total weight less gonad and stomach content weights) instead of total weight would have provided a more precise re¯ection of condition since feeding intensity and gonad maturation can vary signi®cantly between years of individuals (Lambert and Dutil, 1997a). Unfortunately, data on gutted and somatic weights were available only from 1992 onwards and in 1998, respectively. Comparisons between total and gutted weights and between the resulting condition factors calculated from them were
done for ®sh captured since 1992, while comparison between total and somatic weights and the resulting condition factors calculated from them were done for ®sh captured in 1998 to investigate the difference between the different methods of calculation. The HSI was calculated for all samples taken in 1998 as LW HSI 100 W where LW and W represent liver and somatic weights, respectively. The GSI was calculated for all samples taken in 1998 as: GW GSI 100 W where GW and W represent gonad and somatic weights, respectively. The in¯uence of size, age, sex, maturity and area (East±West Greenland) on condition factor, HSI and GSI values was also investigated (sex and area information were transformed into numerical format). The relationships between length and total, somatic, gonad and liver weights were calculated using simple exponential regressions whose equations were calculated by converting the non-linear models into linear
82 Table 1 Annual number of fish sampled by area (E: east Greenland, W: west Greenland), sex (U: undetermined, M: male, F: female) and maturity stage, and annual mean (S.D.), total weight (TW), length (L), age (A), condition factor (K) and water temperature (T)a Total
Area E
1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 S
Sex W
U
Maturity stage M
373
373
0
1
198
180
1154
465
689
0
553
601
2833 2050 1423 160 435 91 460 164 329 204 9676
1852 1422 743 0 320 26 417 91 306 122 6137
981 628 680 160 115 65 43 73 23 82 3539
1 14 55 1 1 27 0 0 3 10 113
1381 989 661 97 219 30 222 77 158 93 4672
1451 1047 707 62 215 34 238 87 168 101 4891
Mean (S.D.) a
F
Empty (year) cells indicate that information was not available.
1 217
531 552 762 146 213 73 322 128 88 125 3157
2 140
1921 76 287 12 222 18 137 36 233 79 3161
TW (g)
L (cm)
A (year)
K
T (8C)
2451 (2192)
62.0 (17.4)
5.1 (2.0)
0.82 (0.15)
2009 (2579)
50.8 (22.4)
4.2 (2.5)
0.95 (0.17)
2173 (2187) 2204 (2064) 1801 (1692) 296 (320) 1327 (1714) 1191 (1879) 1989 (2433) 1613 (1862) 2554 (1606) 1408 (1953)
57.7 56.6 52.4 30.8 46.5 38.8 50.6 48.9 61.8 39.8
4.9 5.2 5.2 2.3 3.7 3.0 4.0 3.8 4.6
0.84 0.91 0.92 0.82 0.86 0.85 0.92 0.93 0.94 0.91
3.14 3.01 2.70 4.18 4.14 3.78 3.96 3.29 3.46 3.56 3.49 3.60 3.62 3.86 4.71 4.19 5.18
2016 (2121)
54.2 (19.4)
>2 15
376 0 1 1 0 0 1 0 7 0 401
(17.5) (18.7) (16.9) (7.2) (17.3) (21.3) (23.0) (17.4) (13.3) (25.8)
(1.6) (1.6) (1.8) (1.0) (1.8) (1.8) (2.2) (1.5) (1.1)
4.7 (1.9)
(0.12) (0.20) (0.12) (0.10) (0.10) (0.17) (0.11) (0.11) (0.12) (0.14)
0.89 (0.15)
(1.69) (1.38) (1.39) (1.06) (0.91) (0.97) (1.09) (1.28) (1.13) (1.06) (1.17) (1.28) (1.01) (0.89) (1.02) (0.80) (1.05)
3.76 (1.32)
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
Year
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
ones by taking the logarithm of raw data. Non-linear models were chosen because they presented lower residual standard errors than linear models. As a standard procedure, near bottom temperatures were measured directly before or after trawling in the vicinity of the swept area by a CTD-sonde with a precision of 1008C. During the 15 year time series, a total of 1394 measurements were made. Annual weighted mean temperatures of the near bottom layers were calculated from 1982 to 1998 using the stratum areas as weighting factor, and were compared with the annual mean condition factor by means of linear regression analysis. 3. Results 3.1. Condition factor and temperature Total weight was strongly related to gutted and somatic weight (r20.99, P<0.05, n1728 and r2 0.99, P<0.05, n85, respectively), and thus condition factors calculated from total weights and those calculated from gutted and somatic weights were also strongly related (r20.69, P<0.05, n1802 and r2 0.91, P<0.05, n85, respectively). Therefore, the values of total weights were used to calculate condition factors as they allowed us to construct a longer time series than gutted or somatic weights did, providing a reliable indicator of somatic and gutted condition. Condition factor was independent of size, age, sex, maturity and area. Although signi®cant relationships (P<0.05, n9676) were observed between condition factor and the stated variables, a very low value of the coef®cient of determination was found in all cases (r2<0.01). Therefore, it was decided to make no distinction between sizes, ages, sexes, maturity stages and area in the analysis of their condition factor. Moreover, the underlying assumption of an isometric growth associated with the use of Fulton's condition factor is respected, as the slope of the regression between total weight and length for all samples (log-transformed data) was 3.04 (r20.98, P<0.05, n9676). Annual mean condition factors were calculated for the period 1982±1998 (Table 1), showing clear interannual variations (Fig. 2). Condition was high during
83
Fig. 2. Interannual variations in temperature and the condition factor (calculated with total weights) of the 9676 cod captured during autumn (September±November) groundfish surveys between 1982 and 1998 off Greenland. 1983±1986 and 1988 data on condition factor were not available.
years 1987, 1990±1991 and 1995±1998, and low in 1982, 1989 and 1992±1994. Overall, condition factor ranged close to an average value of 0.9, with a maximum of 0.95 in 1987 and a minimum of 0.82 in 1982 and 1992. From 1992 to 1997, an upward trend was observed which did not continue in 1998. Mean condition factor calculated from total weights for the entire period 1982±1998 was 0.89 (S.D.0.15; n 9676), which corresponds to estimated mean values of 0.75 and 0.85 if condition factor would have been calculated from gutted and somatic weights, respectively. Since 1982, only 20% of cod reached condition factor values above 1.00 (which corresponds to estimated values of 0.82 and 0.95 in the gutted and somatic condition factors, respectively). Annual weighted mean temperatures of the near bottom layer by stratum area were calculated to indicate the overall ambient temperature (Table 1, Fig. 2). Since 1982, the overall mean temperature variation ranged between 2.7 and 5.18C. A very cold event around 38C was identi®able for the period 1982± 1984 followed by a warming to an overall mean of 48C. During 1987±1989, there was a less pronounced cooling. Subsequently, there was an increasing trend exceeding 48C in the most recent years. The estimated near bottom temperature for 1996±1998 indicates the warmest conditions during the entire survey period, with the 1998 estimate (5.18C) being the highest since 1982. Annual mean condition factor values were positively correlated with annual weighted mean temperatures (r20.28, p0.07, n12). Only the 1998 data,
84
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
when temperature exceeded 58C, were an obvious outlier in the regression. 3.2. Liver and HSI HSI was dependent of size (r20.20, aÿ1.351, b0.119, P<0.05, n85; Fig. 3), but independent from age, sex, maturity and area (r2<0.03, P>0.05). The relationship between liver weight and length was described using a simple exponential regression model whose equation was calculated by converting the model into a linear one by taking the logarithms of data (Fig. 3). 3.3. Gonad and GSI GSI was independent of size, age, sex and maturity, as no signi®cant relationships were observed between GSI and these variables (r2<0.03, P>0.05). Although GSI was signi®cantly (P<0.05) related to the area, a very low coef®cient of determination was found (r20.07). Therefore, it was decided to make no distinction between sizes, ages, sexes, maturity stages and area in the analysis of their GSI. Mean GSI for the samples taken in 1998 was 1.131 (S.D.0.671, n76). The relationship between gonad weight and length was described using a simple exponential regression model whose equation was calculated by converting the model into a linear one by taking the logarithm of data (Fig. 3). 3.4. Length±weight relationships The relationships between length and somatic weight for 1998 samples (Fig. 3) and length and total weight for 1982±1998 samples (Fig. 3) were described using simple exponential regression models whose equations were calculated by converting the models into linear ones by taking the logarithms of data.
Fig. 3. Relationships between HSI, liver weight (LW), gonad weight (GW), somatic weight (SW) and length (L) for cod captured in October 1998 and between total weight (TW) and L for cod
captured during autumn (September±November) groundfish surveys between 1982 and 1998 off Greenland. Estimated values were obtained from the linear regression HSIÿ1.35140.1186L (r20.18, P<0.01, n85) and the exponential regressions LW 0.00000174L4.3523 (r20.70, P<0.01, n85), GW0.0000226 L3.3005 (r20.51, P<0.01, n76), SW0.0033410L3.2265 (r2 0.97, P<0.01, n85) and TW0.0074721L3.04114 (r20.99, P<0.01, n9676).
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
4. Discussion Maximum annual levels of condition factor and HSI for several cod stocks have been demonstrated to occur from September to December (Dambergs, 1964; Jangaard et al., 1967a,b; Eliassen and Vahl, 1982; Taggart et al., 1994; Dutil et al., 1995; Lilly, 1996; Lambert and Dutil, 1997a). By contrast, GSI for cod has been shown to peak during spawning season, i.e. spring, while minimum values were found from September to December (Lambert and Dutil, 1997a). Therefore, the K condition factor and HSI calculated for cod off Greenland should represent the maximum level at their seasonal pattern while the GSI index should represent the lowest level of the year. However, the values of the GSI should be interpreted carefully since samples were obtained during autumn when all mature ®sh were resting (Table 1). When comparing the condition factor for cod off Greenland during the period 1982±1998 with that of northern Gulf of St. Lawrence stock for the period 1984±1996 (samples also taken during fall) presented by Lambert and Dutil (1997a), it is observed that the former has been usually in a poorer condition than the later. Our analyses reveal that the most frequent values of condition indices for cod off Greenland since 1982 are about the same magnitude or even lower than those obtained for cod of northern Gulf of St. Lawrence during fall 1993 and 1994, a level which was demonstrated by the authors to be signi®cantly lower than the level at which cod could be quali®ed as being in very good condition on the basis of laboratory experiments. Values of HSI and GSI indices and somatic, liver and gonad weights at a given length for cod off Greenland during fall 1998 were also lower than those of cod of northern Gulf of St. Lawrence during fall 1993 and 1994, which were comparable with those of cod dying from exhaustion (Lambert and Dutil, 1997a). Southern Gulf (Dutil et al., 1995), Nova Scotia (Jangaard et al., 1967a) and cod off eastern Newfoundland (NAFO Div. 2J3KL; Shelton and Lilly, 1995) can regularly reach higher condition factor values too. Overall, condition in cod off Greenland was among the lowest observed in natural populations of this species. Thus, in the long term, cod off Greenland might present a lower reproductive potential than that of other stocks from the Atlantic. Not only are
85
condition indices in the Greenland stock low, but also weights at age are low compared with other stocks in the North Atlantic. For instance, 4 year old cod off Greenland average 1.8 kg compared with 7.3 kg in the Celtic Sea (Brander, 1995). These observations reveal that the cod stock off Greenland has a much lower condition and productivity than other cod stocks. The fact that temperature has been observed to be an important factor controlling recruitment and growth (RaÈtz et al., 1999) and condition (this paper) of cod off Greenland indicates that this environmental variable might be limiting the productivity of this stock and increasing its fragility, especially when other than natural factors intervene (e.g. ®sheries). Acknowledgements The authors would like to thank Prof. A.D. McIntyre for his comments on the manuscript. We also thank Prof. Dr. G. Hubold and Dr. Jordi Lleonart for supporting us in our ideas. This research project was funded in part by the Deutsche Forschungsgemeinshaft (DFG) Ð Consejo Superior de Investigaciones Cientõ®cas (CSIC) exchange program. Josep Lloret bene®ted also from a grant of the D.G. Research of the Government of Catalonia.
References Anon, 1996. Report of the North-Western Working Group. ICES CM Assess 15, 377 pp. Bolger, T., Connolly, P.L., 1989. The selection of suitable indices for the measurement and analysis of fish condition. J. Fish. Biol. 34, 171±182. Brander, K.M., 1995. The effect of temperature on growth of Atlantic cod (Gadus morhua L.). ICES J. Mar. Sci. 52, 1±10. Buch, E., Horsted, S.A., Hovgard, H., 1994. Fluctuations in the occurrence of cod in Greenland waters and their possible causes. ICES Mar. Sci. Symp. 198, 158±174. Buch, E., Stein, M., 1989. Environmental conditions off west Greenland, 1980±1985. J. Northwest Atlantic Fish. Sci. 9, 81±89. Dambergs, N., 1964. Extractives of fish muscle IV: seasonal variations of fat, water-solubles, protein, and water in cod (Gadus morhua L.) fillets. J. Fish. Res. Board Can. 21, 703± 709. Dutil, J.-D., Lambert, Y., Chouinard, G.A., FreÂchet, A., 1995. Fish condition: what should we measure in cod (Gadus morhua)? DFO Atl. Fish. Res. Doc. No. 95/11.
86
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
Eliassen, J.E., Vahl, O., 1982. Seasonal variations in biochemical composition and energy content of liver, gonad and muscle of mature and immature cod, Gadus morhua L. from Balsfjorden, northern Norway. J. Fish. Biol. 20, 707±716. Jangaard, P.M., Brockerhoff, H., Burgher, R.D., Hoyle, R.J., 1967a. Seasonal changes in general condition and lipid content of cod from inshore waters. J. Fish. Res. Board Can. 24, 607± 612. Jangaard, P.M., Ackman, R.G., Sipos, J.C., 1967b. Seasonal changes in fatty acid composition of cod liver, flesh, roe, and milt lipids. J. Fish. Res. Board Can. 24, 613±627. Kjesbu, O.S., Kryvi, H., Sundby, S., Solemdal, P., 1992. Buoyancy variations in eggs of Atlantic cod (Gadus morhua) in relation to chorion thickness and egg size: theory and observations. J. Fish. Biol. 41, 581±599. Krivobok, M.N., Tokareva, G.I., 1972. Dynamics of weight variations of the body and individual organs of the Baltic cod during the maturation of gonads. Trudy VNIRO 85, pp. 45±55 (translated from Russian by Trans. Ser. Fish. Res. Board Can. No. 2722, 1973). Lambert, Y., Dutil, J.-D., 1997a. Condition and energy reserves of Atlantic cod (Gadus morhua) during the collapse of the northern Gulf of St. Lawrence stock. Can. J. Fish. Aquat. Sci. 54, 2388±2400. Lambert, Y., Dutil, J.-D., 1997b. Can simple condition indices be used to monitor and quantify seasonal changes in the energy reserves of Atlantic cod (Gadus morhua)? Can. J. Fish. Aquat. Sci. 54 (1), 104±112. Lambert, Y., Dutil, J.-D., 1998. Energetic consequences of reproduction in Atlantic cod (Gadus morhua) in relation to pre-spawning level of energy reserves. In: Abstracts of Oral and Poster Presentations NAFO Symposium: Variations in Maturation, Growth, Condition and Spawning Stock Biomass Production in Groundfish, Lisbon, 9±11 September 1998. Northwest Atlantic Fisheries Organization, Darmouth, Nova Scotia, Canada, 45 pp. Lilly, G.R., 1996. Growth and condition of cod in subdivision 3Ps as determined from trawl surveys (1972±1996) and sentinel surveys (1995). DFO Atl. Fish. Res. Doc. No. 96/69.
Lloret, J., 1997. Population dynamics of American Plaice (Hippoglossoides platessoides) off west Greenland, (NAFO Divisions 1B±1F), 1982±1994. NAFO Sci. Coun. Studies 30, 89±107. Love, R.M., 1958. Studies on the north sea cod III: effects of starvation. J. Sci. Food Agric. 9, 617±620. Marshall, C.T., Yaragina, N.A., Lambert, Y., Kjesbu, O., 1999. Total lipid energy as a proxy for total egg production by fish stocks. Nature. 402, 288±290. RaÈtz, H.-J., 1994. Assessment of the migration of Atlantic cod (Gadus morhua L.) between the stocks off west and east Greenland in 1984±1986 by means of Otolith typing. J. Northw. Atl. Fish. Sci. 16, 7±18. RaÈtz, H.-J., 1996. Efficiency of geographical and depth stratification in error reduction of groundfish survey results: case study Atlantic cod off Greenland. NAFO Sci. Coun. Stud. 28, 65±71. RaÈtz, H.-J., 1997. Structures and changes of the demersal fish assemblage off Greenland and trends in near bottom temperature, 1982±1996. NAFO SCR 97/5, N2830, 32 pp. RaÈtz, H.-J., Stein, M., Lloret, J., 1999. Variation in growth and recruitment of Atlantic cod (Gadus morhua) off Greenland during the second half of the 20th century. J. Northw. Atl. Fish. Sci. 25, 161±170. Shelton, P.A., Lilly, G.R., 1995. Factors influencing weight at age of cod off eastern Newfoundland (NAFO Divisions 2J3KL). Theme Session on Causes of Observed Variation in Fish Growth. ICES CM 1995/P:14, 29 pp. Stein, M., Lloret, J., 1995. Stability of water masses-impact on cod recruitment of west Greenland? Fish. Oceanogr. 4 (3), 230±237. Taggart, C.T., Anderson, J., Bishop, C., Colbourne, E., Hutchings Lilly, G., Morgan, J., Murphy, E., Myers, R., Rose, G., Shelton, P., 1994. Overview of cod stocks, biology, and environment in the Northwest Atlantic region of Newfoundland, with emphasis in northern cod. ICES Mar. Sci. Symp. 198, 140±157. Wilkins, N.P., 1967. Clupea harengus L., survival and some gross biochemical changes. Comp. Biochem. Physiol. 23, 503±518. Yaragina, N.A., Marshall, C.T., 2000. Tropic Influences on interannual and seasonal variation in the liver condition index of northeast Arctic cod (Gadus morhua), ICES J. Mar. Sci. 56, in press.
Condition of cod (Gadus morhua) off Greenland during 1982±1998 Josep Lloreta,*, Hans-Joachim RaÈtzb a
Institut de CieÁncies del Mar Ð CSIC, Passeig Joan de Borbo sn, E-08039 Barcelona, Catalonia, Spain b Institut fuÈr See®scherei, Palmaille 9, D-22767 Hamburg, Germany Received 1 June 1999; received in revised form 31 August 1999; accepted 27 November 1999
Abstract An analysis of the condition (Fulton's K) of cod (Gadus morhua) off Greenland during autumn in the period 1982±1998 is presented. The paper addresses the interannual variations in condition and attempts to relate these to variations in water temperature. No size, age, sex, maturity nor geographical differences were observed. Condition of cod was positively related to water temperature. Mean condition factor calculated from total weights for the entire period was 0.89. Hepatosomatic and gonadosomatic indices are also presented for year 1998. Overall, the condition of cod off Greenland was among the lowest observed in natural populations of this species. # 2000 Elsevier Science B.V. All rights reserved. Keywords: Atlantic cod; Gadus morhua; Greenland; Condition factor; Fulton's K; Hepatosomatic index; Gonadosomatic index
1. Introduction Since 1982, the demersal ®sh assemblage in Greenlandic waters has undergone fundamental changes in species composition and abundance, with the collapse of the ecologically and economically important cod (Gadus morhua) and golden red®sh (Sebastes mentella) stocks which almost disappeared from survey catches (RaÈtz, 1997). Other species inhabiting the area like American plaice (Hippoglossoides platessoides), Atlantic wolf®sh (Anarhichas lupus) and starry skate (Raja radiata) displayed a less pronounced decrease in abundance but decreased in biomass by more than 50% (RaÈtz, 1997). The cod stock, for a long time being considered the main commercial and biological spe*
Corresponding author. Tel.: 34-93-2216416; fax: 34-93-2217340. E-mail address: [email protected] (J. Lloret)
cies of the area, already collapsed at the end of the 1960s decade and remained at a very low level since then (Anon, 1996). Fishing activities appeared to have been the main responsible factor for the observed declines (Lloret, 1997; RaÈtz et al., 1999). In addition to this major anthropogenic effect, studies on climatic and oceanographic conditions around Greenland (Buch and Stein, 1989) revealed concomitant interannual changes in the ocean and atmosphere which have in¯uenced ®sh biomass production in this area (Buch et al., 1994; Stein and Lloret, 1995; RaÈtz et al., 1999). Simple condition indices (e.g. Fulton's K condition factor, hepatosomatic index and gonadosomatic index) have been demonstrated to be a measure of the energy reserves of ®sh, e.g. Atlantic cod (Lambert and Dutil, 1997b), cod with a low condition index presumably resulting from adverse environmental, poor feeding conditions or parasitic infections
0165-7836/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 5 - 7 8 3 6 ( 0 0 ) 0 0 1 1 1 - 9
80
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
(Lambert and Dutil, 1997b; Yaragina and Marshall, 2000). Condition indices of cod have been shown to follow interannual variations and seasonal cycles, with lower energy reserves occurring during spawning (Dambergs, 1964; Jangaard et al., 1967a,b; Eliassen and Vahl, 1982; Taggart et al., 1994; Shelton and Lilly, 1995; Lilly, 1996; Lambert and Dutil, 1997a). Poor condition (i.e. lower available energy reserves) can have several consequences for stocks (Lambert and Dutil, 1997a). Reproductive success can be reduced through lower fecundity and reduction in egg quality (Kjesbu et al., 1992; Lambert and Dutil, 1998; Marshall et al., 1999). Poor condition may also lower the chances of survival of big ®sh, leading to an increase of natural mortality (Love, 1958; Wilkins, 1967; Krivobok and Tokareva, 1972). Fulton's K condition factor is one of various formulations used to evaluate the weight±length relationship in ®sh (Bolger and Connolly, 1989). It was selected because of its simplicity of calculation and because it converts a twodimensional weight±length relationship into a single statistic that gives a simple indication of the ``wellbeing'' of a ®sh (Lambert and Dutil, 1997b). The major disadvantage of Fulton's K condition factor is the assumption of an isometric growth in ®sh (b3 in the formula K W=Lb ). If this assumption is seriously violated, problems of correlation between condition factor and length could arise. The aim of this study was to examine the annual condition of cod during the period 1982±1998 from samples obtained during German annual ground®sh surveys, and to test the in¯uence of interannual water temperature ¯uctuations on it. Age, size, sex, maturity and geographical differences in condition are also tested, and we describe the hepatosomatic and the gonadosomatic indices of cod during the survey in 1998. The condition values of cod off Greenland are compared with those of other stocks. 2. Materials and methods Weight and length measurements of individual cod were derived from annual German ground®sh surveys covering shelf areas and the continental slope off west and east Greenland. The surveys, which were performed in autumn, commenced in 1982 and were primarily designed for the assessment of cod. The
standard gear used was the 140 ft bottom trawl with a 22 m horizontal opening rigged with heavy ground gear and equipped with a small mesh liner inside the cod end. The towing time was 30 min. The survey covered shelf areas and the continental slope at the 3 mile offshore line. Due to a pronounced heterogeneity of cod distribution (RaÈtz, 1996), the survey area was subdivided into different geographic and depth strata, with seven geographic strata which were split into two depth strata covering the 0±200 and 201± 400 m zones (Fig. 1). The strategy applied included a distribution of the sampling effort according both to the stratum areas and to cod abundance. Consequently, 50% of the hauls were allocated proportionally to stratum by stratum area while the other 50% were apportioned on the basis of a review of historical mean cod abundance. The hauls were randomly distributed within trawlable areas of the various strata. Nontrawlable areas were mainly located inshore. During 1982±1998, 2418 successful sets were carried out. Further information on the ®shing strategy is given by RaÈtz (1997). Fork length (cm) and total (whole body) weight (5 g) of all individual cod in the catch were measured yearly since 1982. Sex and maturity were determined. Three maturity stages were used to identify the reproductive state of ®sh in autumn. Males and females having nearly transparent testis/ovaries were classi®ed as stage 1 (immature), while those with whitish testis or reddish ovaries (but without running milt or visible eggs, respectively) were classi®ed as stage 2 (mature-resting). When testis were white with running milt (males) or eggs were visible (females), individuals were classi®ed as stage >2 (mature-spawning). Age determinations was done by the staff of the Institut fuÈr See®scherei (Hamburg) from the otoliths collected each year during the period 1982±1998, according to the methodology described by RaÈtz (1994). Data were not available during years 1983± 1986, and in 1988. Gutted (carcass) weight (5 g) was also measured since 1992. Table 1 shows the annual number of ®sh sampled by area, sex and maturity stage, and the annual mean total weight, length and age. During the 1998 survey, liver and digestive tract (stomach and intestine) weights (5 g) were also taken from the 85 cod captured, while gonad weight was measured in 76 of them.
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
81
Fig. 1. Survey area and stratification as specified in Section 2.
Fulton's K condition factor and the hepatosomatic index (HSI) were used as main indicators of the condition of cod. The gonadosomatic index (GSI) was used as a complementary index of the condition. Interannual variations in the condition of cod since 1982 were assessed by calculating for each year the Fulton's K condition factor from all samples of length and weights. The K condition factor was expressed as W K 100 3 L where W is the total weight (g) and L is the fork length (cm). The stated formula, with the constant3, assumes an isometric growth in ®sh, and thus a heavier weight for a given length corresponds to a better condition. However, the use of gutted (carcass) weight or somatic weight (total weight less gonad and stomach content weights) instead of total weight would have provided a more precise re¯ection of condition since feeding intensity and gonad maturation can vary signi®cantly between years of individuals (Lambert and Dutil, 1997a). Unfortunately, data on gutted and somatic weights were available only from 1992 onwards and in 1998, respectively. Comparisons between total and gutted weights and between the resulting condition factors calculated from them were
done for ®sh captured since 1992, while comparison between total and somatic weights and the resulting condition factors calculated from them were done for ®sh captured in 1998 to investigate the difference between the different methods of calculation. The HSI was calculated for all samples taken in 1998 as LW HSI 100 W where LW and W represent liver and somatic weights, respectively. The GSI was calculated for all samples taken in 1998 as: GW GSI 100 W where GW and W represent gonad and somatic weights, respectively. The in¯uence of size, age, sex, maturity and area (East±West Greenland) on condition factor, HSI and GSI values was also investigated (sex and area information were transformed into numerical format). The relationships between length and total, somatic, gonad and liver weights were calculated using simple exponential regressions whose equations were calculated by converting the non-linear models into linear
82 Table 1 Annual number of fish sampled by area (E: east Greenland, W: west Greenland), sex (U: undetermined, M: male, F: female) and maturity stage, and annual mean (S.D.), total weight (TW), length (L), age (A), condition factor (K) and water temperature (T)a Total
Area E
1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 S
Sex W
U
Maturity stage M
373
373
0
1
198
180
1154
465
689
0
553
601
2833 2050 1423 160 435 91 460 164 329 204 9676
1852 1422 743 0 320 26 417 91 306 122 6137
981 628 680 160 115 65 43 73 23 82 3539
1 14 55 1 1 27 0 0 3 10 113
1381 989 661 97 219 30 222 77 158 93 4672
1451 1047 707 62 215 34 238 87 168 101 4891
Mean (S.D.) a
F
Empty (year) cells indicate that information was not available.
1 217
531 552 762 146 213 73 322 128 88 125 3157
2 140
1921 76 287 12 222 18 137 36 233 79 3161
TW (g)
L (cm)
A (year)
K
T (8C)
2451 (2192)
62.0 (17.4)
5.1 (2.0)
0.82 (0.15)
2009 (2579)
50.8 (22.4)
4.2 (2.5)
0.95 (0.17)
2173 (2187) 2204 (2064) 1801 (1692) 296 (320) 1327 (1714) 1191 (1879) 1989 (2433) 1613 (1862) 2554 (1606) 1408 (1953)
57.7 56.6 52.4 30.8 46.5 38.8 50.6 48.9 61.8 39.8
4.9 5.2 5.2 2.3 3.7 3.0 4.0 3.8 4.6
0.84 0.91 0.92 0.82 0.86 0.85 0.92 0.93 0.94 0.91
3.14 3.01 2.70 4.18 4.14 3.78 3.96 3.29 3.46 3.56 3.49 3.60 3.62 3.86 4.71 4.19 5.18
2016 (2121)
54.2 (19.4)
>2 15
376 0 1 1 0 0 1 0 7 0 401
(17.5) (18.7) (16.9) (7.2) (17.3) (21.3) (23.0) (17.4) (13.3) (25.8)
(1.6) (1.6) (1.8) (1.0) (1.8) (1.8) (2.2) (1.5) (1.1)
4.7 (1.9)
(0.12) (0.20) (0.12) (0.10) (0.10) (0.17) (0.11) (0.11) (0.12) (0.14)
0.89 (0.15)
(1.69) (1.38) (1.39) (1.06) (0.91) (0.97) (1.09) (1.28) (1.13) (1.06) (1.17) (1.28) (1.01) (0.89) (1.02) (0.80) (1.05)
3.76 (1.32)
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
Year
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
ones by taking the logarithm of raw data. Non-linear models were chosen because they presented lower residual standard errors than linear models. As a standard procedure, near bottom temperatures were measured directly before or after trawling in the vicinity of the swept area by a CTD-sonde with a precision of 1008C. During the 15 year time series, a total of 1394 measurements were made. Annual weighted mean temperatures of the near bottom layers were calculated from 1982 to 1998 using the stratum areas as weighting factor, and were compared with the annual mean condition factor by means of linear regression analysis. 3. Results 3.1. Condition factor and temperature Total weight was strongly related to gutted and somatic weight (r20.99, P<0.05, n1728 and r2 0.99, P<0.05, n85, respectively), and thus condition factors calculated from total weights and those calculated from gutted and somatic weights were also strongly related (r20.69, P<0.05, n1802 and r2 0.91, P<0.05, n85, respectively). Therefore, the values of total weights were used to calculate condition factors as they allowed us to construct a longer time series than gutted or somatic weights did, providing a reliable indicator of somatic and gutted condition. Condition factor was independent of size, age, sex, maturity and area. Although signi®cant relationships (P<0.05, n9676) were observed between condition factor and the stated variables, a very low value of the coef®cient of determination was found in all cases (r2<0.01). Therefore, it was decided to make no distinction between sizes, ages, sexes, maturity stages and area in the analysis of their condition factor. Moreover, the underlying assumption of an isometric growth associated with the use of Fulton's condition factor is respected, as the slope of the regression between total weight and length for all samples (log-transformed data) was 3.04 (r20.98, P<0.05, n9676). Annual mean condition factors were calculated for the period 1982±1998 (Table 1), showing clear interannual variations (Fig. 2). Condition was high during
83
Fig. 2. Interannual variations in temperature and the condition factor (calculated with total weights) of the 9676 cod captured during autumn (September±November) groundfish surveys between 1982 and 1998 off Greenland. 1983±1986 and 1988 data on condition factor were not available.
years 1987, 1990±1991 and 1995±1998, and low in 1982, 1989 and 1992±1994. Overall, condition factor ranged close to an average value of 0.9, with a maximum of 0.95 in 1987 and a minimum of 0.82 in 1982 and 1992. From 1992 to 1997, an upward trend was observed which did not continue in 1998. Mean condition factor calculated from total weights for the entire period 1982±1998 was 0.89 (S.D.0.15; n 9676), which corresponds to estimated mean values of 0.75 and 0.85 if condition factor would have been calculated from gutted and somatic weights, respectively. Since 1982, only 20% of cod reached condition factor values above 1.00 (which corresponds to estimated values of 0.82 and 0.95 in the gutted and somatic condition factors, respectively). Annual weighted mean temperatures of the near bottom layer by stratum area were calculated to indicate the overall ambient temperature (Table 1, Fig. 2). Since 1982, the overall mean temperature variation ranged between 2.7 and 5.18C. A very cold event around 38C was identi®able for the period 1982± 1984 followed by a warming to an overall mean of 48C. During 1987±1989, there was a less pronounced cooling. Subsequently, there was an increasing trend exceeding 48C in the most recent years. The estimated near bottom temperature for 1996±1998 indicates the warmest conditions during the entire survey period, with the 1998 estimate (5.18C) being the highest since 1982. Annual mean condition factor values were positively correlated with annual weighted mean temperatures (r20.28, p0.07, n12). Only the 1998 data,
84
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
when temperature exceeded 58C, were an obvious outlier in the regression. 3.2. Liver and HSI HSI was dependent of size (r20.20, aÿ1.351, b0.119, P<0.05, n85; Fig. 3), but independent from age, sex, maturity and area (r2<0.03, P>0.05). The relationship between liver weight and length was described using a simple exponential regression model whose equation was calculated by converting the model into a linear one by taking the logarithms of data (Fig. 3). 3.3. Gonad and GSI GSI was independent of size, age, sex and maturity, as no signi®cant relationships were observed between GSI and these variables (r2<0.03, P>0.05). Although GSI was signi®cantly (P<0.05) related to the area, a very low coef®cient of determination was found (r20.07). Therefore, it was decided to make no distinction between sizes, ages, sexes, maturity stages and area in the analysis of their GSI. Mean GSI for the samples taken in 1998 was 1.131 (S.D.0.671, n76). The relationship between gonad weight and length was described using a simple exponential regression model whose equation was calculated by converting the model into a linear one by taking the logarithm of data (Fig. 3). 3.4. Length±weight relationships The relationships between length and somatic weight for 1998 samples (Fig. 3) and length and total weight for 1982±1998 samples (Fig. 3) were described using simple exponential regression models whose equations were calculated by converting the models into linear ones by taking the logarithms of data.
Fig. 3. Relationships between HSI, liver weight (LW), gonad weight (GW), somatic weight (SW) and length (L) for cod captured in October 1998 and between total weight (TW) and L for cod
captured during autumn (September±November) groundfish surveys between 1982 and 1998 off Greenland. Estimated values were obtained from the linear regression HSIÿ1.35140.1186L (r20.18, P<0.01, n85) and the exponential regressions LW 0.00000174L4.3523 (r20.70, P<0.01, n85), GW0.0000226 L3.3005 (r20.51, P<0.01, n76), SW0.0033410L3.2265 (r2 0.97, P<0.01, n85) and TW0.0074721L3.04114 (r20.99, P<0.01, n9676).
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
4. Discussion Maximum annual levels of condition factor and HSI for several cod stocks have been demonstrated to occur from September to December (Dambergs, 1964; Jangaard et al., 1967a,b; Eliassen and Vahl, 1982; Taggart et al., 1994; Dutil et al., 1995; Lilly, 1996; Lambert and Dutil, 1997a). By contrast, GSI for cod has been shown to peak during spawning season, i.e. spring, while minimum values were found from September to December (Lambert and Dutil, 1997a). Therefore, the K condition factor and HSI calculated for cod off Greenland should represent the maximum level at their seasonal pattern while the GSI index should represent the lowest level of the year. However, the values of the GSI should be interpreted carefully since samples were obtained during autumn when all mature ®sh were resting (Table 1). When comparing the condition factor for cod off Greenland during the period 1982±1998 with that of northern Gulf of St. Lawrence stock for the period 1984±1996 (samples also taken during fall) presented by Lambert and Dutil (1997a), it is observed that the former has been usually in a poorer condition than the later. Our analyses reveal that the most frequent values of condition indices for cod off Greenland since 1982 are about the same magnitude or even lower than those obtained for cod of northern Gulf of St. Lawrence during fall 1993 and 1994, a level which was demonstrated by the authors to be signi®cantly lower than the level at which cod could be quali®ed as being in very good condition on the basis of laboratory experiments. Values of HSI and GSI indices and somatic, liver and gonad weights at a given length for cod off Greenland during fall 1998 were also lower than those of cod of northern Gulf of St. Lawrence during fall 1993 and 1994, which were comparable with those of cod dying from exhaustion (Lambert and Dutil, 1997a). Southern Gulf (Dutil et al., 1995), Nova Scotia (Jangaard et al., 1967a) and cod off eastern Newfoundland (NAFO Div. 2J3KL; Shelton and Lilly, 1995) can regularly reach higher condition factor values too. Overall, condition in cod off Greenland was among the lowest observed in natural populations of this species. Thus, in the long term, cod off Greenland might present a lower reproductive potential than that of other stocks from the Atlantic. Not only are
85
condition indices in the Greenland stock low, but also weights at age are low compared with other stocks in the North Atlantic. For instance, 4 year old cod off Greenland average 1.8 kg compared with 7.3 kg in the Celtic Sea (Brander, 1995). These observations reveal that the cod stock off Greenland has a much lower condition and productivity than other cod stocks. The fact that temperature has been observed to be an important factor controlling recruitment and growth (RaÈtz et al., 1999) and condition (this paper) of cod off Greenland indicates that this environmental variable might be limiting the productivity of this stock and increasing its fragility, especially when other than natural factors intervene (e.g. ®sheries). Acknowledgements The authors would like to thank Prof. A.D. McIntyre for his comments on the manuscript. We also thank Prof. Dr. G. Hubold and Dr. Jordi Lleonart for supporting us in our ideas. This research project was funded in part by the Deutsche Forschungsgemeinshaft (DFG) Ð Consejo Superior de Investigaciones Cientõ®cas (CSIC) exchange program. Josep Lloret bene®ted also from a grant of the D.G. Research of the Government of Catalonia.
References Anon, 1996. Report of the North-Western Working Group. ICES CM Assess 15, 377 pp. Bolger, T., Connolly, P.L., 1989. The selection of suitable indices for the measurement and analysis of fish condition. J. Fish. Biol. 34, 171±182. Brander, K.M., 1995. The effect of temperature on growth of Atlantic cod (Gadus morhua L.). ICES J. Mar. Sci. 52, 1±10. Buch, E., Horsted, S.A., Hovgard, H., 1994. Fluctuations in the occurrence of cod in Greenland waters and their possible causes. ICES Mar. Sci. Symp. 198, 158±174. Buch, E., Stein, M., 1989. Environmental conditions off west Greenland, 1980±1985. J. Northwest Atlantic Fish. Sci. 9, 81±89. Dambergs, N., 1964. Extractives of fish muscle IV: seasonal variations of fat, water-solubles, protein, and water in cod (Gadus morhua L.) fillets. J. Fish. Res. Board Can. 21, 703± 709. Dutil, J.-D., Lambert, Y., Chouinard, G.A., FreÂchet, A., 1995. Fish condition: what should we measure in cod (Gadus morhua)? DFO Atl. Fish. Res. Doc. No. 95/11.
86
J. Lloret, H.-J. RaÈtz / Fisheries Research 48 (2000) 79±86
Eliassen, J.E., Vahl, O., 1982. Seasonal variations in biochemical composition and energy content of liver, gonad and muscle of mature and immature cod, Gadus morhua L. from Balsfjorden, northern Norway. J. Fish. Biol. 20, 707±716. Jangaard, P.M., Brockerhoff, H., Burgher, R.D., Hoyle, R.J., 1967a. Seasonal changes in general condition and lipid content of cod from inshore waters. J. Fish. Res. Board Can. 24, 607± 612. Jangaard, P.M., Ackman, R.G., Sipos, J.C., 1967b. Seasonal changes in fatty acid composition of cod liver, flesh, roe, and milt lipids. J. Fish. Res. Board Can. 24, 613±627. Kjesbu, O.S., Kryvi, H., Sundby, S., Solemdal, P., 1992. Buoyancy variations in eggs of Atlantic cod (Gadus morhua) in relation to chorion thickness and egg size: theory and observations. J. Fish. Biol. 41, 581±599. Krivobok, M.N., Tokareva, G.I., 1972. Dynamics of weight variations of the body and individual organs of the Baltic cod during the maturation of gonads. Trudy VNIRO 85, pp. 45±55 (translated from Russian by Trans. Ser. Fish. Res. Board Can. No. 2722, 1973). Lambert, Y., Dutil, J.-D., 1997a. Condition and energy reserves of Atlantic cod (Gadus morhua) during the collapse of the northern Gulf of St. Lawrence stock. Can. J. Fish. Aquat. Sci. 54, 2388±2400. Lambert, Y., Dutil, J.-D., 1997b. Can simple condition indices be used to monitor and quantify seasonal changes in the energy reserves of Atlantic cod (Gadus morhua)? Can. J. Fish. Aquat. Sci. 54 (1), 104±112. Lambert, Y., Dutil, J.-D., 1998. Energetic consequences of reproduction in Atlantic cod (Gadus morhua) in relation to pre-spawning level of energy reserves. In: Abstracts of Oral and Poster Presentations NAFO Symposium: Variations in Maturation, Growth, Condition and Spawning Stock Biomass Production in Groundfish, Lisbon, 9±11 September 1998. Northwest Atlantic Fisheries Organization, Darmouth, Nova Scotia, Canada, 45 pp. Lilly, G.R., 1996. Growth and condition of cod in subdivision 3Ps as determined from trawl surveys (1972±1996) and sentinel surveys (1995). DFO Atl. Fish. Res. Doc. No. 96/69.
Lloret, J., 1997. Population dynamics of American Plaice (Hippoglossoides platessoides) off west Greenland, (NAFO Divisions 1B±1F), 1982±1994. NAFO Sci. Coun. Studies 30, 89±107. Love, R.M., 1958. Studies on the north sea cod III: effects of starvation. J. Sci. Food Agric. 9, 617±620. Marshall, C.T., Yaragina, N.A., Lambert, Y., Kjesbu, O., 1999. Total lipid energy as a proxy for total egg production by fish stocks. Nature. 402, 288±290. RaÈtz, H.-J., 1994. Assessment of the migration of Atlantic cod (Gadus morhua L.) between the stocks off west and east Greenland in 1984±1986 by means of Otolith typing. J. Northw. Atl. Fish. Sci. 16, 7±18. RaÈtz, H.-J., 1996. Efficiency of geographical and depth stratification in error reduction of groundfish survey results: case study Atlantic cod off Greenland. NAFO Sci. Coun. Stud. 28, 65±71. RaÈtz, H.-J., 1997. Structures and changes of the demersal fish assemblage off Greenland and trends in near bottom temperature, 1982±1996. NAFO SCR 97/5, N2830, 32 pp. RaÈtz, H.-J., Stein, M., Lloret, J., 1999. Variation in growth and recruitment of Atlantic cod (Gadus morhua) off Greenland during the second half of the 20th century. J. Northw. Atl. Fish. Sci. 25, 161±170. Shelton, P.A., Lilly, G.R., 1995. Factors influencing weight at age of cod off eastern Newfoundland (NAFO Divisions 2J3KL). Theme Session on Causes of Observed Variation in Fish Growth. ICES CM 1995/P:14, 29 pp. Stein, M., Lloret, J., 1995. Stability of water masses-impact on cod recruitment of west Greenland? Fish. Oceanogr. 4 (3), 230±237. Taggart, C.T., Anderson, J., Bishop, C., Colbourne, E., Hutchings Lilly, G., Morgan, J., Murphy, E., Myers, R., Rose, G., Shelton, P., 1994. Overview of cod stocks, biology, and environment in the Northwest Atlantic region of Newfoundland, with emphasis in northern cod. ICES Mar. Sci. Symp. 198, 140±157. Wilkins, N.P., 1967. Clupea harengus L., survival and some gross biochemical changes. Comp. Biochem. Physiol. 23, 503±518. Yaragina, N.A., Marshall, C.T., 2000. Tropic Influences on interannual and seasonal variation in the liver condition index of northeast Arctic cod (Gadus morhua), ICES J. Mar. Sci. 56, in press.