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ICES Journal of Marine Science: Journal du Conseil 2003 60(4):780-786; doi:10.1016/S1054-3139(03)00024-9
© 2003 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
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Winter and spring changes in condition factor and energy reserves of wild cod compared with changes observed during food-deprivation in the laboratory

Jean-Denis Dutil*, Yvan Lambert and Denis Chabot

Ministère des Pêches et des Océans, Institut Maurice-Lamontagne CP 1000, Mont-Joli, Quebec, Canada G5H 3Z4

*Correspondence to J.-D. Dutil; tel: +1 418 775 0582; fax: +1 418 775 0740. e-mail: dutiljd{at}dfo-mpo.gc.ca.

Atlantic cod were food-deprived for a period of 84 days at three temperatures (2, 6, 10°C), and changes in the liver, gonads and somatic weights, and muscle and liver water contents were monitored and compared with changes observed in wild cod over winter in the northern Gulf of St. Lawrence. Total lack of food during the period January–April would have caused condition to decline to a level at which very high mortality takes place. Actual changes in condition in wild cod were less than predicted from the laboratory experiments except during the period April–May at the onset of spawning. Thus, wild cod were able to meet part of the metabolic costs during winter through occasional feeding, as confirmed by stomach content data. We conclude that previous estimates of natural mortality associated with poor condition in spring were not biased by the selective mortality of poor-condition fish in winter.

Keywords: Atlantic cod, Gadus morhua, natural mortality, condition, energy, growth, maturation

Received 11 April 2002; accepted 18 February 2003.


   Introduction
Top
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Following the severe decline in the abundance of Atlantic cod (Gadus morhua) in eastern Canada, natural mortality (M) has been estimated to be higher than previously considered (Sinclair, 2001). Fishery biologists generally assume a fixed value (0.2, 18%) for M. While M can be assessed readily in stocks, which are not exploited, partitioning M into its major components is not a trivial task. This is even more complex in situations where stocks are exploited, particularly in large ecosystems. Thus, we have a limited understanding of natural mortality, its variability in space and time and its response to changes in the ecosystem. Two aspects of natural mortality in juvenile and adult cod have been examined in association with groundfish decline: predation by seals (Hammill and Stenson, 2000) and starvation (Dutil and Lambert, 2000).

Climatic variations and changes in marine ecosystems that have a negative impact on fish condition may also increase the risk of mortality. Declining condition may, for instance, decrease metabolic and swimming capacities of cod (Martínez et al., 2003) and hence their ability to seize prey and avoid predation. Such a situation has been assessed recently in the Gulf of St. Lawrence, where cod have experienced a period of changing environmental conditions. The cooling of the cold intermediate water layer in the Gulf of St. Lawrence started in the 1980s (Gilbert and Pettigrew, 1997). In the northern Gulf, cod moved to deeper waters and shifted their latitudinal distribution, possibly to avoid being exposed to colder waters (Castonguay et al., 1999). Nevertheless, both size-at-age and individual energetic condition declined throughout the 1980s and early 1990s (Dutil et al., 1999). Individual fish experience marked seasonal changes in condition both in the northern (Lambert and Dutil, 1997b) and southern Gulf (Schwalme and Chouinard, 1999) with levels of energy reserves being minimal during the spring period when spawning takes place. Females in poor condition invested less energy in maturation, but in relation to available energy reserves, energy expenditures were greater than in females in good condition (Lambert and Dutil, 2000). As a result, energy invested in reproduction by poor-condition females, as well as low energy levels in reproductive and non-reproductive individuals, increased their risk of mortality (Dutil and Lambert, 2000).

The range of potential values for several variables indicative of cod condition has been determined experimentally (Lambert and Dutil, 1997b; Dutil and Lambert, 2000). The proportion of wild cod with energy reserves as low as observed in starved cod in the laboratory experiments has been determined by comparing field and laboratory observations. The degree of overlap between frequency distributions was used as an estimate of natural mortality that is directly attributable to lack of food (Dutil and Lambert, 2000). However, there are two potential drawbacks to such a method. Firstly, fish in the wild may die before critical thresholds are reached, because life is more demanding in the wild than in the laboratory, i.e. critical thresholds may differ in the wild and in the laboratory. Secondly, mortality associated with poor condition may be underestimated when condition approaches critical thresholds, i.e. dead fish are not sampled representatively. To investigate whether our estimates of M associated with poor condition had been underestimated (case 2), we compared changes in physiological condition observed in the wild to changes predicted in unfed fish kept at three temperatures.


   Materials and methods
Top
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Laboratory experiments
Cod of two size categories (38–48 and 48–58 cm) were deprived of food for 84 days at three temperatures (mean±s.d.), 2.06±0.33°C (group 1), 6.14±0.15°C (group 2) and 9.97±0.12°C (group 3), from early-November 1995 to late January 1996. There were two tanks for each combination of size and temperature. One tank held 25 fish. These fish were measured (±1 mm) and weighed (±1 g) after 21, 42, 63 and 84 days: a random sample of 10 cod was used for dissection after 84 days. The other tank held 32 fish. A random sample of 10 fish was used for dissection after 21, 42 and 63 days. Twenty fish were sampled and dissected at the start of the experiment (group 4). Forty cod held in two other tanks, one tank for each size category, were maintained at 6.05±0.19°C, and were fed capelin to satiation once a week for a period of 63 days. They were measured and weighed and then used for dissection (group 5). All fish were measured, weighed and double-tagged (Visible implant tags, Northwest Marine Technology, Shaw Island, Washington, DC) at the start of the experiment. Capture sites, handling methods and tank setup were as described in Dutil et al. (1998). Condition factor (K), somatic condition factor (Ks), liver-somatic index (LSI), gonad-somatic index (GSI) and muscle (MW) and liver (LW) water contents were measured and calculated as described in Dutil and Lambert (2000).

Temperature and size category effects on changes in the condition factor over 84 days ({Delta}K84d) were tested with a two-way factorial ANOVA without replication (Zar, 1996). Time course changes in body weight were described with linear regressions and tested with analysis of covariance (based on observations after 21, 42, 63 and 84 days). Changes in the condition factor and somatic condition factor over 84 days ({Delta}K84d and {Delta}Ks84d, respectively) were described with a linear model pooling fish from the two size categories at each level of temperature and using fork length (Li) and initial condition or somatic condition factor (Ki and Ksi, respectively) as covariates.

The number of fish with GSI below and above 3% was calculated for each tank, and differences in their proportions between tanks (i.e. size categories) were tested within each group (groups 1, 2, 3 and 5) using the {chi}2-test for independent samples. There was no tank (size category) effect (P>0.05), and thus we pooled the data for small and large fish to examine GSI and LSI at the start (group 4), after feeding (group 5) and after food-deprivation (groups 1, 2, 3), and for cod with GSI below and above 3%, separately. GSI was compared using the Kruskal–Wallis one-way ANOVA by ranks followed by a posteriori Tukey multiple comparisons. Group effects on the proportion of fish with GSI values below and above 3% were tested using the {chi}2 test for independent samples. The small number of females (10%) precluded a separate analysis for males and females. As no replicate tanks were available, group effects should be interpreted cautiously.

Liver-weight/somatic-weight relationships were analyzed using linear regressions and the analysis of covariance. Relationships between LW, MW and Ks were fitted with a segmented quadratic model with a plateau representing the minimal liver or muscle water contents (Gauss–Newton method). Then a polynomial regression model adapted from Lambert and Dutil (1997a) fitted to the non-linear portion of the relationships was used to assess LW and MW from Ks. The analyses are based on observations made after 21, 42, 63 and 84 days.

Field–laboratory comparisons
Field samples were obtained from the estuary and northern Gulf of St. Lawrence in 1994 (Dutil and Lambert, 2000). Fish size varied among samples, but our analyses were restricted to a common size range (32–64 cm): January 20, mean length=41.0±5.2 cm (n=145); April 7, 37.1±4.0 cm (n=60); May 5, 47.4±6.9 cm (n=554); June 5, 39.7±4.3 cm (n=139). Ks and fork length were not correlated (P>0.05 and r2<0.02 in any of the four samples). The length of cod averaged 44.5±7.2 cm overall for field samples compared with 48.0±3.8 cm in the laboratory experiments.

Changes in condition in the laboratory were modeled for a standard 48-cm fish and compared with changes in condition observed in field samples. For three-temperature (2, 6, 10°C) representative of cod geographic distribution (Brander, 1995), we tested whether changes in Ks observed in 1994 cod differed from those expected ({Delta}Ks) for unfed cod in the laboratory experiments. The hypothesis for the period January–April was:


Formula

where KsJ and KsA are the somatic condition factors observed in January and April, respectively, and {Delta}Ks represents the expected change in the somatic condition factor for a 48-cm fish with a somatic condition factor at the start of the food-deprivation period equal to KsJ. The expected frequency distribution for the somatic condition factor in April was constructed by translation assuming a normal distribution with mean (KsAP):


Formula

KsJ and KsAP were assumed to have equal coefficients of variability. Predicted (KsAP) and observed (KsA) somatic condition factors were compared by the t-test. This procedure was repeated for the three periods (January 20–April 7, April 7–May 5, and May 5–June 5) and three temperatures (see Equations (4)–(6) in Section "Results").

Variability in the predicted somatic condition factor in May (2 and 6°C) was further examined. The change in somatic condition factor from April to May ({Delta}Ks28d) was calculated from Equations (4) and (5) (in Section "Results") using the median length of the fish in the May sample (47.3 cm). The expected frequency distribution for the somatic condition factor in May was constructed by translation assuming a normal distribution. The variance (Var) was calculated as:


Formula

where Cov (Ksi, {Delta}Ks84d) is the covariance between Ksi and {Delta}Ks84d.

Differences in LSI, LW and MW among the four field samples were tested with Kruskal–Wallis one-way ANOVA by ranks followed by a posteriori Tukey multiple comparisons due to non-normal distributions, particularly in the May and June samples, and heterogeneous variances (P<0.001). The t-tests were used to compare LSI, LW and MW between cod sampled in January and cod in group 4. Normality was tested using Shapiro–Wilk's W and skewness (symmetry) following D'Agostino (in Zar, 1996).

Feeding activity
Stomachs were collected to assess feeding activity in the field. In January and August–September 1994, cod were caught using bottom trawls during depth-stratified random surveys covering most of the winter and summer distribution of northern Gulf of St. Lawrence cod. An additional survey was conducted in May 1994 that covered most of the spawning aggregation. For each set where cod were caught, three non-empty stomachs were taken for each 10-cm length-class. Empty stomachs were counted for each length-class until three non-empty stomachs were collected. In addition, the stomach of 56 cod collected in April 1994 near Sept-Iles, Quebec, and of 140 cod caught in June 1994 near Matane, Quebec, were weighed. For each stomach, a fullness index was calculated by dividing the mass of stomach content by the fork length raised to the third power, and the result was multiplied by 10 000 (Lilly, 1991). These analyses were restricted to cod measuring between 32 and 64 cm.


   Results
Top
 Introduction
 Materials and methods
 Results
Discussion
 References
 
Laboratory observations
The decline in condition factor over 84 days ({Delta}K84d) was influenced by size and temperature (P<0.05; Figure 1). Weight loss over time was linear in all size and temperature combinations (P<0.01, r2>0.95), but daily weight loss was slightly greater from day 0 to day 21 than in the period from day 21 to day 84.


Figure 1
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  		Figure 1 Decrease in the condition factor (mean and s.d.) of Atlantic cod in two size categories over an 84-day food-deprivation period at three temperatures.

 
When the two size categories were combined and fish length introduced as a covariate, {Delta}K84d was influenced by fish length and initial condition factor (Table 1), with fish of a small size and in better condition experiencing larger decreases in condition factor. Li had a significant effect at all temperatures (r>0.42), whereas Ki was significant at 2°C (r=–0.42) and 6°C (r=–0.20), but not at 10°C. Li and Ki showed a poor correlation.


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  		Table 1 Correlation coefficients between initial length (Li), condition factor (Ki) and decline in condition factor ({Delta}K84d) of Atlantic cod over an 84-day food-deprivation period at three temperatures. *indicates significant relationships with {Delta}K84d (P<0.05). Statistics for the multiple linear regression are shown.

 
{Delta}K84d is described by the following equations:


Formula 1

(1)


Formula 2

(2)


Formula 3

(3)
where fork length is in millimeter. Removing Ki in the analyses at 10°C had no influence on the statistics in Table 1. GSI averaged 1.2% (n=20) at the start of the experiment. This value was used to obtain the initial somatic condition factor (Ksi):


Formula 4

(4)


Formula 5

(5)


Formula 6

(6)

GSI varied considerably among individuals particularly at the end of the experiment, with some fish having large gonads and others having smaller gonads lacking any sign of maturation (Table 2). Mean GSI was greater in food-deprived cod at 2°C as a larger proportion of the fish matured during the experiment. The proportion of maturing cod was similar in fed (63 days) and food-deprived (84 days) cod at 6°C, but mean GSI was much greater in fed cod. Slow maturation was associated with low energy reserves in the liver. LSI was greater in more mature fish (1.62±1.01% and 2.86±1.35% when GSI was smaller than 3% and larger than 3%, respectively). LSI was also greater in fed cod (6.24±1.48%) than in cod sampled at the start of the experiment (4.63±1.20) and much greater than in food-deprived cod (2.87±1.28, 2.29±1.32 and 1.62±1.18% at 2, 6 and 10°C, respectively).


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  		Table 2 Gonad-somatic index (GSI,%) of Atlantic cod before (S) and after 63 days of feeding at 6°C (F) or 84 days of food-deprivation at three temperatures (n=20). Numbers of fish, GSI and fork length (mean±s.d.) are shown for cod with GSI under (I) or over (M) 3%. Values with the same letter column-wise are not different (P>0.05).

 
Liver weight correlated positively with somatic weight, but the relationships were different at 2, 6 and 10°C (analysis of covariance, P>0.05 for slopes and P<0.05 for elevations):


Formula 7

(7)


Formula 8

(8)


Formula 9

(9)
where LWt is liver weight and SWt is somatic weight. LW and MW correlated negatively with Ks. Water content reached minimum asymptotic values of 22.2% in the liver and 80.1% in the muscle, based on the quadratic model with a plateau, for Ks values above 0.93 and 1.04, respectively. Water content was higher at lower Ks values:


Formula 10

(10)


Formula 11

(11)

Field observations
The condition of cod declined from January to May, but improved from May to June. Ks differed significantly among the four samples (P<0.001). January and May differed from all other samples (Tukey HSD, P<0.05), but April and June were not significantly different (P>0.05). Ks was normally distributed for each monthly sample (Shapiro–Wilk, P>0.05) and the four variances were homoscedastic (Bartlett, P>0.05; Table 3). This change in Ks is shown in Figure 2 for a theoretical population of 1 million fish assuming a normal distribution and using means and s.d. in Table 3. The proportion of cod with Ks values below 0.75, for instance, would be 36.2% in January, 70.1% in April, 90.1% in May and 80.8% in June.


Figure 2
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  		Figure 2 Frequency distribution of the somatic condition factor for Atlantic cod sampled in January, April, May and June 1994 assuming a normal distribution and a population of 1 million fish. The means and standard deviations (s.d.) of Table 3 were used.

 


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  		Table 3 Somatic condition factor (Ks, mean±s.d.) of Atlantic cod in 1994 in the estuary and northern Gulf of St. Lawrence. P is the Shapiro–Wilk probability statistic.

 
LSI, LW and MW differed among samples (P<0.001; Table 4). LW increased from January to April and further increased into May and June. MW, in contrast, did not change from January to April, reached a high value in May and then declined slightly in June.


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  		Table 4 Mean (n) and 95% confidence interval for the liver-somatic index (LSI, %) and liver (LW, %) and muscle (MW, %) water contents of Atlantic cod in 1994 in the estuary and northern Gulf of St. Lawrence.

 
Expected vs observed distributions
From January to April, Ks in wild fish decreased much less than expected based on the declines observed in unfed fish in the laboratory for all three temperatures (P<0.001; Tables 3 and 5—April). Had the wild cod not fed between January and April (76 days between sampling events) or had feeding only made up for greater activity costs in the wild compared to the laboratory, a large proportion of the fish would have been threatened (Table 5—April). From April to May, observed and predicted declines did not differ at 2 or 6°C (P>0.05), but differed at 10°C (P<0.01). From May to June, condition actually improved and hence the observed and predicted values differed at all three temperatures (P<0.001).


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  		Table 5 Predicted somatic condition factor (Ks), liver-somatic index (LSI, %), liver water (LW, %) and muscle water (MW, %) contents for Atlantic cod in April and May 1994, and percentage of fish expected to reach two critical thresholds described in Dutil and Lambert (2000). Predicted values for April and May were calculated from the January and April observations, respectively, assuming no feeding took place.

 
As the observed and predicted declines in Ks over the period April–May were similar (Tables 3 and 5—May), our May sample could have been biased as it may have missed fish, which died from energy exhaustion during that critical period. The laboratory experiments do not support this possibility. The percentage of fish below two critical thresholds described in Dutil and Lambert (2000) were not markedly different for the observed distribution in May (0.3 and 28.8% for Ks<0.54 and Ks<0.66, respectively) compared with the predicted distribution at 2 and 6°C (Table 5—May). Furthermore, Ks distribution did not depart from normality in May, although Ks and LSI observations were positively skewed (P<0.01) and LW observations negatively skewed (P<0.02).

LSI, as estimated from predicted Ks was close to values actually observed in April, particularly at 6°C (Equations (7)–(9), somatic weights calculated for a 48-cm fish; Tables 4 and 5). LW and MW on the other hand were much greater (Equations (10) and (11); Tables 4 and 5). In contrast, LSI estimated from predicted Ks was slightly higher than actually observed in May (Tables 4 and 5). Similarly, LW was slightly lower than actually observed, although MW was slightly higher. There was no difference in LSI between wild cod in January and cod sampled at the start of the experiment (4.26±1.61% and 4.63±1.20%, respectively, mean and s.d., P>0.05). Differences in LW (27.58±7.67% and 32.06±7.67% in January and group 4 cod, respectively) and MW (80.33±0.64% and 80.81±0.58% in January and group 4 cod, respectively) were slight but significant (P<0.05 and P<0.01, respectively).

Feeding activity
The percentage of empty stomachs was greatest in January, decreased in May and further decreased in late summer (Table 6). Fullness index and weight of stomach contents were also lowest in January and increased to levels that were similar in May and late summer. These results may be taken as representative of the feeding activity of the stock. Cod were caught in 115 of 123 sets in January (stomachs sampled from 95 sets), 67 of 71 in May (55 sets sampled) and 83 of 198 in late summer (62 sets sampled). Two additional samples were collected in April and June. The cod sampled in April had all fed, whereas feeding activity was lower in June than in May. These two samples may not be representative of feeding activity for the whole stock as they were obtained from discrete areas and contained fewer fish than the other samples.


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  		Table 6 Feeding activity of Atlantic cod in 1994 in the estuary and northern Gulf of St. Lawrence. Proportion of empty stomachs is expressed as a percentage of the total number of stomachs examined. Stomach fullness index is described in the Section "Materials and methods". The average weight of stomach contents (g) is given with empty stomachs included (1) or excluded (2).

 

   Discussion
Top
 Introduction
 Materials and methods
 Results
 Discussion
References
 
Earlier estimates of natural mortality associated with low condition factor and energy reserves in cod were reconsidered in the present study. The mortality of emaciated cod was hypothesized to occur during the winter leading to a biased estimate of poor condition and resulting mortality in the spring in the northern Gulf of St. Lawrence. The condition of cod steadily declined over the winter in 1994 (Lambert and Dutil, 1997b; Schwalme and Chouinard, 1999), suggesting that energy gains did not match energy costs. From January to April, however, wild cod exhibited a much smaller decline in condition factor than the food-deprived cod in the laboratory experiments. Other indicators of nutritional condition were consistent with this finding. Wild cod in May had smaller livers and higher LW contents than predicted from the laboratory experiments, but LSI (>2%) and LW content (<60%) suggested that liver was still a primary source of energy. Smaller livers and higher LW contents in the May sample may reflect a greater demand for energy in the pre-spawning period than could be estimated in our laboratory experiments. The laboratory experiments were conducted in the fall period at the onset of sexual maturation in cod (Lambert et al., 1994; Karlsen et al., 1995). Results may have been different had the laboratory experiments been conducted in the period January–May when the energy demands for maturation and mating increase. Food-deprived cod may also spend more energy on activity in the wild than in the laboratory. Greater activity costs in the laboratory, however, would have resulted in fish being in an even worst projected condition in spring. Temperature effects should be interpreted cautiously. The experimental design did not include replicate samples (tanks) for each level of temperature at the end of the experiment (day 84). Tank effects may not lead to an underestimate of minimal survival costs, but they may result in an overestimate at any given temperature. This would make our comparisons between actual and observed changes in the condition factor conservative. Thus, we reject our hypothesis and conclude that our earlier estimates of mortality were not biased (Lambert and Dutil, 1997b; Dutil and Lambert, 2000). Additional experiments would be required to better estimate weight loss–temperature relationships.

While mid-winter in the northern Gulf of St. Lawrence appears to be a period of relative food shortage, as shown by the decline of condition in the field samples, part of the energy costs of cod are met through occasional feeding during mid-winter. Southern Gulf cod contained substantial food quantities only during the period from May to November, whereas a majority of empty stomachs and a reduction of stomach fullness occurred in the winter (Schwalme and Chouinard, 1999). This is consistent with stomach content data for northern Gulf cod in 1994. Few cod had fed in January, and a substantial proportion of empty stomachs were found in the cod sampled in a spawning aggregation in May (Ouellet et al., 1997) and in the St. Lawrence estuary in June, when spawning was not yet over. Nevertheless, stomach samples collected in April and May indicated that some fish had actually resumed feeding before spawning occurred.

Temperature and food availability in the fall and winter may explain variations in reproduction in the spring period. Wild fish classified as being emaciated in Dutil and Lambert (2000) had a much larger gonad to liver dry weight ratio than non-emaciated fish. Dutil and Lambert (2000) suggested that two groups of fish, early and late spawners, might participate in reproduction, with early spawners having lower fat reserves earlier in the spring period. Alternately, poor- and good-condition fish may participate in reproduction with poor-condition fish being in a difficult position to meet the energy demand of maturation and spawning once committed to reproduction. Maturation is initiated early in the fall (Lambert et al., 1994; Karlsen et al., 1995). The marked decline in condition factor, which occurs in autumn and winter (Lambert and Dutil, 1997b; Schwalme and Chouinard, 1999) suggests that food shortage does occur during maturation right up to spawning in both northern and southern Gulf cod. Feeding level has been shown to affect the size of the liver (Karlsen et al., 1995) and the size of the gonads (Lambert et al., 1994) early in the process of maturation. Temperature has a marked incidence on metabolic rates and costs and thus can also potentially interfere with the process of maturation in food-deprived cod. In our study, lower GSI and smaller proportions of maturing to non-maturing fish were observed at higher temperatures suggesting that food-deprivation may be more detrimental to maturation at higher temperatures. Gulf cod inhabit warmer waters in winter than in summer, but individual cod are found in a range of temperatures in winter (2–6°C) (Swain et al., 1998; Castonguay et al., 1999). Temperature selection by individual cod during the winter may thus be critical in terms of both survival and reproduction in situations of food shortage and may have an incidence on individual variations observed in spawning patterns in the spring (Ouellet et al., 1997; Dutil and Lambert, 2000).


   Acknowledgements
 
We thank Y. Gagnon, S. Chouinard and M. Péloquin for their assistance in the field and in the laboratory. We also thank R. Miller, M.-F. Beaulieu, L. Chénard, L. Perreault and L. Girard for their work in analysing stomach samples. Thanks to R. Miller for her review of an earlier version and to H. Bourdages for his help with data analysis. The Department of Fisheries and Oceans funded this work under two projects: "Programme multidisciplinaire de recherche sur la morue du nord du Golfe Saint-Laurent (IML)" and "Partitioning the total mortality of Atlantic cod stocks".


   References
Top
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

    Brander K.M. (1995) The effect of temperature on growth of Atlantic cod (Gadus morhua). ICES Journal of Marine Science 52:1–10.[Abstract/Free Full Text]

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