© 2005 International Council for the Exploration of the Sea
Effect of temperature and food availability on reproductive investment of first-time spawning male Atlantic cod, Gadus morhua
a Tohoku National Fisheries Research Institute Shinhama, Shiogama 985-0001, Japan
b Fisheries Research Services Marine Laboratory PO Box 101, Victoria Road, Aberdeen AB11 9DB, Scotland, UK
*Correspondence to M. Yoneda: tel: +81 22 365 1191; fax: +81 22 367 1250. e-mail: myoneda{at}fra.affrc.go.jp.
This study demonstrates how temperature and food availability affect growth, maturation, and sperm production in first-time spawning male cod in captivity. Cod, prior to the onset of maturation, were held under four different varying temperature and feeding regimes between November 2002 and March 2003. Lower food availability resulted in poor growth and body condition. Decreasing temperature partly led to slower growth in fish that matured during the experiment. Low temperature resulted in lesser proportions of mature fish relative to the higher temperature treatments. Higher temperature and food availability resulted in higher sperm production (testicular weight and gonadosomatic index). Our findings suggest that variation in food availability would mainly affect the growth and condition and the level of gamete production whilst variation in temperature would affect the proportion of males that mature. These results are contrasted with similar data for female cod.
Keywords: cod, food, growth, maturation, temperature
Received 5 July 2004; accepted 27 April 2005.
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Introduction |
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Environmental variability in factors such as food availability and temperature can have important consequences for the energy allocated to somatic growth and reproduction, because of the effect on metabolism and surplus energy (Wootton, 1990). Favourable feeding conditions could lead to individuals maturing earlier (Kjesbu, 1994) and producing more gametes (Lambert and Dutil, 2000). However, as changes in food intake and metabolic rate are associated with changes in temperature (Jobling, 1993), unfavourable temperature could reduce energy investment in growth and reproduction indirectly by a reduction in food consumption. In addition, temperature has a direct effect on the synthesis and secretion of hormones influencing gametogenesis (Van Der Kraak and Pankhurst, 1997). As such, variation in temperature could affect the timing of the maturational decision and spawning season. However, low temperatures appear to have less of an influence on testicular maturation than on ovarian development (Cyr et al., 1998; Pawson et al., 2000).
Males generally utilize less energy for gonad maturation for a given weight than do females (Jonsson et al., 1991), since sperm represent a small cytoplasmic investment (Wootton, 1990). As such, there may be a sex-related difference in the rate of energy accumulation at the critical time when individuals decide to mature or postpone maturation (Thorpe, 1994; Jacobsen and Ajiad, 1999). This is likely to reflect the general findings that male fish mature earlier than females (Wootton, 1990). In addition, experiments on some marine fish have indicated that food manipulation may not affect the proportion of mature males and the weight of the testes, but can affect ovarian investment (Karlsen et al., 1995; Bromley et al., 2000). This implies that the allocation pattern of energy resources into gonads may differ between males and females (Diana and Mackay, 1979; Rijnsdorp and Ibelings, 1989). Thus, there could be sex-related differences in the reproductive responses to environmental variability.
Atlantic cod, Gadus morhua (Linnaeus, 1758), is a long-lived multiple spawner that reproduces annually over a protracted spawning season (Hislop, 1984). Relative to females, there is little information about the effect of environmental conditions on reproductive characteristics of male cod. Atlantic cod spawning stocks in British waters have been younger with a result of the intense fishing pressure for a long time (Cook et al., 1997), and have also been subject to large changes in environmental conditions in the last few decades (O'Brien et al., 2000). An understanding of the effect of environmental change on reproductive potential in younger fish is therefore becoming increasingly important for the implementation of proper stock assessment. The purpose of this study is to examine how temperature and feeding regime influence the growth, maturity, and reproductive output of first-time spawning male cod (2 years old) using three varying temperature regimes designed to mimic the range of natural variation experienced by wild cod. We also contrast these findings with similar work on female cod (Yoneda and Wright, 2005).
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Material and methods |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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Male and female juvenile cod (2 years old in the year of spawning) were obtained from the SEAFISH hatchery at Ardtoe (SEAFISH) on the west coast of Scotland; either they had been reared at that facility or had been transferred to the FRS Aultbea rearing facility. Additional cod were caught by handline in the waters off the east coast of Scotland (MacDuff and Stonehaven). Only 2-year-old wild cod, as verified by otolith-based age estimates, were used to avoid using any repeat spawners in the experiment. The experiment was conducted at the Fisheries Research Services, Marine Laboratory (Aberdeen, UK) between November 2002 and March 2003. Prior to the experiment, fish were kept in circular tanks (5.7 m3) under ambient temperature and artificial lighting with a natural photoperiod cycle for 2–4 months, and fed to satiation with commercial dry pellets (C0-7 EUROPA 18%, TROUW ESPANA; Protein 50%, Oil 18%, Ash 11.5%, Fibre 0.6%, Phosphorus 1.8%). At the end of October, cod were starved for 2–3 days to ensure that their stomachs were empty. Cod were then anaesthetized in MS-222 (75 mg/l), measured (±0.5 cm), weighed (±1 g), and individually marked with both internal (Trovan® Pitt Tags) and external (Elastomer marks, Northwest Marine Technology, Inc.) tags.
Fish randomly selected from each source of the collection were transferred into four different tanks and subjected to one of the following temperature and feeding regimes; low temperature/high feeding (LT/HF), ambient temperature/high feeding (AT/HF), high temperature/high feeding (HT/HF), and high temperature/low feeding (HT/LF) (Table 1). To examine the effect of temperature on biological characteristics, the first three treatments (LT/HF, AT/HF, HT/HF) were compared whilst the food effect was examined, based on the comparison of the two treatments HT/HF and HT/LF. All tanks were supplied with re-circulated water and subjected to the ambient photoperiod cycle, although the three temperature-controlled tanks (LT/HF, HT/LF, and HT/HF) had artificial lighting. There were no significant differences in the total body weight (BW, g)–total length (TL, cm) relationship between sexes, treatment groups, and sampling locations at the onset of the experiment (n = 120; r2 = 0.928; TL: p < 0.001; sex: p = 0.16; treatment: p = 0.21; location: p = 0.88; generalized linear model, gamma family, log-function). Temperature in each tank was recorded every 20 min using a data logger (Minilog-12bit, VEMCO). The HT and LT in the inside tanks were aimed to keep the gradients within ±3°C of the AT in the outside tank throughout the experiment. The temperature in all treatments followed or paralleled the local ambient seasonal decline from December to late February, after which it increased gradually, although some fluctuations in weekly/daily temperature could not be avoided (Figure 1). Temperature regimes in the HT/HF and HT/LF treatments were practically identical (±0.1°C) throughout the experiment, so no temperature effects should exist between the two groups. The mean temperatures in all treatments between November and December were significantly higher than between January and March (p < 0.001; Mann–Whitney U-test). Fish on high feeding ration in LT/HF, AT/HF, and HT/HF were fed daily to satiation with pellets (0.42–0.75% BW in each treatment per day), and any leftovers were removed after feeding. The rations in such treatments were gradually reduced from 0.75% BW as the leftover appeared to increase with decreasing temperature. The mean rations given throughout the experiment LT/HF, AT/HF, and HT/HF were 0.49%, 0.51%, and 0.53% of BW, respectively. The final ration in the low feeding treatment (HT/LF) was 0.24% BW per day (Kjesbu, 1994), and no leftovers were detected after feeding.
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From January to February repeated measurements were taken on TL, BW, and testicular development. Testicular development was assessed by either applying slight pressure along the abdominal cavity towards the genital pore and/or catheterization every 15 days. All fish were sacrificed by 29 March, corresponding to the end of the main spawning season in wild cod (Hislop, 1984). Running males were sacrificed for future analysis of evaluation of sperm quality. All experimental work was carried out under Home Office license "Estimating fish growth and reproductive investment" (PPL 60/3020).
After sacrifice, TL of all specimens was measured to the nearest centimetre. BW was determined to the nearest g, while testicular weight (TW) and liver weight (LW) were measured to the nearest 0.1 g.
The gonadosomatic index (GSI), hepatosomatic index (HSI), and somatic condition factor (KS) were calculated in the following manner:
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The specific growth rate, in terms of the percentage daily increment in body weight (SGR), was evaluated according to Svåsand et al. (1996).
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Sexually mature males were defined on the basis of testes having large amounts of spermatozoa in the lumina of the testicular lobules and main sperm duct, and developing spermatids and few spermatocytes, if any. In males with mature stage testis, milt was easily collected from the genital pore by applying slight pressure. Immature fish were defined as the testis having only spermatogonia, including one testis containing spermatogonia and developing spermatocytes.
Non-parametric statistic tests (Kruskal–Wallis test and Mann–Whitney U-test) were used as some data sets (<12) did not provide enough data to test the normality assumptions (GraphPad, 2001). To examine the temperature effect, the Kruskal–Wallis test, if necessary, followed by Dunn's multiple-comparison test was used to compare each SGR, HSI, KS, TW, and GSI among the LT, AT, and HT treatments. Meanwhile, the U-test was used to compare such values between HT/HF and HT/LF treatments to determine the food effect. Fisher's Exact test was used to compare the proportion mature and the timing of maturation during the experiment between treatments. Condition indices were incorporated into generalized linear models (GLM), with TL as the first predictor in order to examine whether the nutritional state could explain variation around the TW–TL relationship. The GLM incorporates a gamma-response distribution coupled with a log-link function (Y = eax+b) to connect the mean to the linear predictors. An additional measure of model fit was based on a pseudo-coefficient of determination (r2), which was the fraction of the total variation explained by the model:
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To remove the influence of different potential spawning experience and locations of birth on biological characteristics (Svåsand et al., 1996) and given that the majority of fish came from the west coast, statistical analyses were also made using only the specimens from this region. Due to the likely importance of temperature on growth and condition, separate analyses were conducted for the warmer early period up to January and the colder late period of each experiment (see Figure 1).
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Results |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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Growth and condition
The SGR of mature males in HT/HF during the early period was significantly higher than those from the HT/LF treatment (Figure 2; p < 0.05; U-test). However, for the late period there was no significant difference in SGR of mature males between the two treatments (p = 0.26), because of a significant decline in the growth rate in all treatments (p < 0.01; U-test). There were no significant differences in SGR during the experiment among the LT, AT, and HT treatments, indicating that temperature had no appreciable effect on growth (early: p = 0.41; late: p = 0.59; Kruskal–Wallis test). In immature males, there was no significant difference in SGR between the two periods for all the treatments combined (p = 0.19), with immature males having lower SGR during the early period than mature males in all treatments (p < 0.01; Dunn's test) except for the HT/LF treatment (p > 0.05).
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There were no significant differences in HSI and KS in mature specimens between LT, AT, and HT treatments, indicating no temperature effect on condition (Figure 3; n = 39; HSI: p = 0.44; KS: p = 0.39; Kruskal–Wallis test). Between HT/LF and HT/HF there was a significant difference in HSI in mature specimens (n = 27, p < 0.05; U-test) but not in KS (p = 0.24).
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The variations in SGR, HSI, and KS for all individuals were also found when only specimens from the west coast were considered.
Maturity
All males in AT/HF and HT/HF became mature during the experiment, with the exception of one fish in HT/HF, resulting in higher proportions of mature fish in such groups than in LT/HF and HT/LF (Table 2). The effect of temperature on the proportions of mature fish was significant when only the data from the west coast in the three temperature treatments were combined (LT vs. AT and HT = 0.70 vs. 1.00; n = 30, p < 0.05; Fisher's Exact test), but this was only marginally significant when all the data from the two different regions were considered (n = 43, p = 0.08). No significant effect of food on the mature proportion was found (HF vs. LF: all specimens: n = 32, p = 0.34; west coast: 1.00 vs. 0.79; n = 25, p = 0.23). Contrasting mature fish between the January–February and March periods, specimens within the two treatments where feeding and temperature were not limited appeared to mature earlier than in the LT or LR treatments. However, there were no significant effects of temperature and food on the timing of testicular maturation among and between the treatments (LT vs. AT and HT: n = 39, p = 0.28; HF vs. LF: n = 27, p = 0.25; Fisher's Exact test). The same pattern was seen when only the data from the west coast were used (temperature: n = 27, p = 0.41; food: n = 22, p = 0.66).
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Sperm production
There was no significant difference in the TW of mature specimens among the three temperature treatments (n = 39, p = 0.77; Kruskal–Wallis test). However, the feeding treatment did have a significant effect on TW (n = 27, p < 0.05; U-test), with the HT/HF mature males having larger testes than those from the HT/LF treatment. Similar variation was found in the case of GSI (Figure 3; temperature treatment: p = 0.62; food treatment: p < 0.05). Similar variation in the TW and GSI was found when only specimens from the west coast were considered (temperature: n = 27; TW: p = 0.54; GSI: p = 0.27; food: n = 22; TW and GSI: p < 0.05).
HSI in mature fish from the three temperature treatments and the two food treatments explained some of the variation in TW in addition to TL (temperature: n = 39, r2 = 0.60; TL: p < 0.001; HSI: p < 0.05; food: n = 27, r2 = 0.74; TL: p < 0.001; HSI: p < 0.05; GLM), but KS did not significantly influence the two models (temperature: p = 0.20; food: p = 0.99).
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Discussion |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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The present study demonstrates that maturation and the level of reproductive investment in male cod are related to growth rate, with mature cod initially growing faster than those that delay maturation. However, the allocation of surplus energy into reproduction by mature males in the 2 months preceding spawning leads to growth rates comparable with those that do not mature during this period. This suggests that first-time spawning cod have a minimal level of growth that must be maintained if males are to invest in reproduction. This pattern of energy allocation was consistent with that found in first-time spawning female cod subjected to the same environmental manipulations (Yoneda and Wright, 2005). A similar relationship between growth and maturation in wild Atlantic cod has also been inferred using otolith back-calculation of the growth of mature and immature fish (Trippel et al., 1995). By manipulating either temperature or food we were able to identify how these two factors influence growth and reproductive investment. Although we were unable to control for individual food intake, the variation in individual growth trajectories and reproductive investment seen in this study should be a function of their net food intake for a given temperature regime.
As the temperature regimes in the present study reflect the maximum and minimum seasonal ranges that the studied cod population is likely to experience (G. Slesser and W. Turrell, pers. comm.), environmental results should be of relevance to the field situation. Our study showed that the cold temperatures experienced by males in the low temperature treatment had a significant effect on the proportion of males that matured when only the specimens from the same origin were considered. Conversely, manipulation experiments on cod and sea bass Dicentrarchus labrax (Linnaeus, 1758) found that temperature had little influence on testicular maturation (Cyr et al., 1998; Pawson et al., 2000). Cyr et al. (1998) found similar seasonal variations in gonadosomatic index, the level of plasma testosterone and 11-keto-testosterone of cod between two groups held at different constant temperatures. Low temperatures can reduce energy investment in reproduction indirectly by a reduction in food consumption. However, the temperature manipulations used in this study did not appear to cause a significant constraint on growth and condition and, by inference, food intake. As such, the different responses to the effect of temperature on testicular maturation of cod may be due in part to different temperature manipulations in the experiments, since short-term varying of temperature within the lower range experienced by the populations may lead to some physiological stress (Fry, 1971; Pickering, 1998). It is likely that annual variations in temperature may be expected to lead to changes in sexual maturity in males. A similar case was also reported for wild cod from Smith Sound, Newfoundland, in Canada (Rideout et al., 2000). They suggested that the cold water (temperature < 3°C) might be directly responsible for the undeveloped testes since there was no evidence for a nutritional effect. However, such temperature extremes are unlikely to be relevant to temperate cod stocks.
Once males commit to maturation they appear to allocate energy to reproduction partly on the basis of food intake since males with unrestricted food availability had larger testes than those on the restricted diet for a similar temperature regime. Lower feeding regime resulted in poor growth in mature fish during the early period of the experiment compared with the high feeding regime group. However, no feeding regime differences in growth rate were found during the late period because of a significant within treatment reduction in SGR between the periods. The decline in somatic growth in the later period could be explained by the combination of the seasonal decline in temperature (Jobling, 1993) and increasing investment in gonad maturation (Hutchings, 1993). The lack of a feeding effect on SGR in the late period may reflect the higher reproductive investment in this treatment.
Sex-related differences in energy allocation to reproduction might arise under the same environment as a consequence of differences in the endogenous control of appetite (Diana, 1983) and lower energy required for sperm production (Wootton, 1990). Comparing results from this study with the responses of female cod to the same treatments (Yoneda and Wright, 2005) provides a means of identifying sex-related differences. In contrast to the males examined in this study, there was evidence for a temperature effect on gonadal maturation in females, with the low temperature leading to an arrest in the onset of vitellogenesis, resulting in the occurrence of females that postponed spawning (Yoneda and Wright, 2005). Therefore, cold temperatures may have a greater impact on females than males.
Consistent with the studies by Kjesbu and Holm (1994) and Karlsen et al. (1995), Yoneda and Wright (2005) found that first-time spawning females produced relatively similar fecundity independent of food availability prior to the first spawning season. This suggests that first-time spawning female Atlantic cod invest in reproduction relative to their size, so that any surplus energy is invested in somatic growth. This clearly affects body size and survival rate during that season which in turn influences fecundity in the following season (Kjesbu et al., 1991; Lambert and Dutil, 2000; Yoneda and Wright, 2005). In contrast, male investment appears to maximize current reproduction as the condition of the liver, the main storage for lipids in cod (Lambert and Dutil, 1997) significantly influenced testicular weight of mature males. These sex-related differences may reflect the importance of body size to reproductive success, because while fecundity is related to size, larger body size in males is not necessarily related to higher spawning success under experimental conditions (Rakitin et al., 2001).
In conclusion, our study has clarified the influence of temperature and food on reproductive investment in first-time spawning male cod. Variation in food availability would mainly affect the growth performance and enhance sperm production in males, whilst variation in temperature would affect the proportions that matured. As such, this study demonstrates that changes in temperature will most likely lead to changes in the proportion of spawning males, while food availability will affect the relative reproductive investment of males.
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Acknowledgements |
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We are grateful to Iain and Fiona Gibb for helping in measurement of specimens, to Ben Williamson, Rory Long, and Peter Gibson for skilful husbandry of the experimental fish, and to two anonymous reviewers for constructive comments. We acknowledge a grant to M. Y. from the "Japan Society for the Promotion of Science for Research Abroad" in 2002. This work was conducted as part of a contract with the Scottish Executive MF0462.
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References |
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