SEARCH

SEARCH BY CITATION

Keywords:

  • energy density;
  • gonadal allocation;
  • parr;
  • proteins;
  • smolts;
  • somatic allocation

Abstract

  1. Top of page
  2. Resumen
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

Abstract –  Lipid density appears to influence life-history decisions in salmonid fishes. This study shows that parr and smolts of anadromous Atlantic salmon from a south Norwegian river have on average between 30 and 40% higher energy level than corresponding brown trout in spring and summer, which may explain differences in life-history traits between the two species. The higher energy density of young salmon was chiefly due to a 1.8 times higher lipid density in parr and 2.4 times higher lipid density in smolts. The difference was smaller among immature parr in the autumn, with only 1.4 times higher lipid density in salmon than trout. The reason for the decreased difference was probably that the more energy rich salmon parr had attained maturity at the time. Among mature male parr, the somatic energy density was approximately 10% higher in trout than salmon. However, the gonadal energy content was more than twice as high in salmon than in trout. The higher somatic energy allocation in parr of Atlantic salmon probably influences protein growth of the two species in fresh water, and increases the ability of salmon relative to trout to undertake long distance feeding migrations and make large investments in reproduction.

Resumen

1. Probablemente los animales mantienen un control regulador de los patrones de ubicación de energía para ser capaces de completar las actividades que demandan energía, tales como la migración y la reproducción. Planteamos como hipótesis que el almacenaje de energía lipídica debe ser mayor en juveniles de Salmo salar que en Salmo trutta dado que las distancias migratorias son mucho mayores en los primeros que en los segundos.

2. Este estudio muestra que tanto individuos en estadios de ‘‘parr’’ y ‘‘smolt’’ de S. salar anádromo de un río del sur de Noruega tienen en primavera y verano, unos niveles medios de energía lipídica 30–40% mayores que los correspondientes de S. trutta, lo que explica diferencias en las características biológicas entre ambas especies. La mayor densidad de energía en S. salar fue debida a 1.8 veces mayor densidad lipídica en los individuos en estadio ‘‘parr’’ y 2.4 veces mayor en los individuos en estadio ‘‘smolt’’. La diferencia fue menor entre individuos ‘‘parr’’ inmaduros en otoño con solo 1.4 veces mayor densidad lipídica en S. salar que en S. trutta. La razón para una menor diferencia es probablemente que los individuos ‘‘parr’’ de salmón, mas ricos en términos energéticos, alcanzan la madurez al mismo tiempo. Entre los individuos ‘‘parr’’ machos maduros, la densidad de energía somática fue aproximadamente un 10% mayor en S. trutta que en S. salar.

3. Por otro lado, el contenido en energía gonadal fue más de dos veces mayor en S. salar que en S. trutta. Una mayor ubicación de energía somática en los individuos ‘‘parr’’ de S. salar probablemente influencia el crecimiento en proteínas de ambas especies en agua dulce e incrementa la habilidad de S. salar, relativo a S. trutta, para desarrollar migraciones alimenticias a larga distancia y hacer grandes inversiones en reproducción.


Introduction

  1. Top of page
  2. Resumen
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

In salmonids, there are interesting life-history differences among closely related species, such as anadromous Atlantic salmon and brown trout (Salmo trutta L.). For instance, male parr of brown trout which attain maturity in their presmolt stage, usually fail to smolt later in life (Jonsson 1985; Dellefors & Faremo 1988). Mature male parr of Atlantic salmon, on the other hand, can spawn in the autumn and smolt and move to sea during the subsequent spring, together with previously immature smolts (Österdahl 1969; Hansen et al. 1989), although at a lower frequency than immature parr (Whalen & Parrish 1999). Furthermore, Atlantic salmon migrate to high seas in the North Atlantic Ocean for feeding (Hansen et al. 1993; Holm et al. 2000; Hansen & Jacobsen 2003), brown trout feed mainly in fjords and along the coast in the vicinity of their home river (Jensen 1968; Pemberton 1976; Jonsson 1985; Berg & Berg 1987), although large individuals may move out into the open ocean (Knutsen et al. 2004). Because of such differences in ecology between the species, it is reasonable to assume that energy allocations will differ between the similar life stages of the two, preparing for migration or spawning.

Sexual maturation and spawning as well as smolting and seaward migration are energy demanding processes, and lipid energy reserves are the major energy sources (Van den Thillart et al. 2002; Jonsson & Jonsson 2003). For instance, adult salmon and trout may spend 50% or more of their total energy on reproduction (Glebe & Leggett 1981; Jonsson & Jonsson 1997; Jonsson et al. 1998), and the lipid content of salmon smolts exhibits a trend towards depletion during smolting and the seaward migration from the river, through the fjord and into the ocean (Stefansson et al. 2003), supporting this contention. Probably, variation in life-history decisions among fish species can be regulated through differences in lipid depositions, as seen within the same species (Kadri et al. 1995, 1996; Simpson et al. 1996; Crossin et al. 2004).

Thus, we expected differences in lipid energy reserves between parr of anadromous Atlantic salmon and brown trout, which was indicated by Berg & Bremset (1998). They measured higher energy concentration in salmon than trout parr, especially in September. However, they did not differentiate between immature and mature parr, or investigate energy contents of smolts, ready for migration. We hypothesised that the lipid energy storage is higher for smolts of Atlantic salmon than brown trout, and immature and maturing parr ready for spawning. If so, we also predicted that male parr in salmon have relatively larger gonads than trout. We tested this on Norwegian anadromous brown trout and Atlantic salmon from southern Norway.

Methods

  1. Top of page
  2. Resumen
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

Atlantic salmon were sampled in the River Imsa, south-western Norway. The smolts were sampled on their way to sea in a downstream trap situated 100 m above the estuary of the river, in May 1995. Male parr were sampled with electric fishing gear in the river (1600 V DC unloaded) on 2 June 1997, and at the commencement of the spawning period in late October/early November 1997–1999. The parr and smolts were 1–2 years of age.

Brown trout were sampled with electric fishing gear in three streams, Helldalsbekken, Skagestadbekken and Vesbekken, south Norway. The smolts were sampled at the mouth of the river on their way downstream in late April. The parr were sampled from June to August, and immature and mature parr were sampled on the spawning grounds at the beginning of the spawning period in October 1992 and 1994. The parr and smolts were 1–3 years of age.

The fish were sealed in polyethylene bags and frozen immediately after capture. While still partly frozen, the fish were dissected. For each fish gonads and soma were treated separately. Partly frozen, somatic and gonadal tissues of each fish were weighed before they were ground in a mincer and homogenised in a microcutter. Between each sample, the mincer and microcutter were cleaned, washed and dried.

The energy density (kJ 100 g−1 wet mass) of each fish was estimated by adding the energy in protein, lipid and carbohydrates in the gonadal and somatic tissues. The caloric coefficients for making energy estimates from proximate composition data were 17 kJ for protein and carbohydrate and 38 kJ for lipids (Craig et al. 1978). Protein was determined by the Kjeldahl method (Anonymous 1981), and lipid content was determined after hydrolysis in hydrochloric acid and extraction with diether (Anonymous 1987). The carbohydrate content, estimated by measuring glucose following hydrolysis of tissue with sulphuric acid (Mason 1983), was negligible (mean values 0.01–0.1 g 100 g tissue−1). The energy contents of soma and gonads of the fish were calculated as mean energy content of the tissue (kJ g−1) times their masses. Water was measured by drying 6 g samples at 105 °C until constant mass was obtained.

Results

  1. Top of page
  2. Resumen
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

Somatic energy, lipid and protein densities in smolts of Atlantic salmon were higher than those in smolts of brown trout (Table 1). In trout, the individual energy density varied between 280 and 429 kJ 100 g−1, with an estimated mean of 352 kJ 100 g−1 wet mass. The comparable values for salmon were 408, 526 and 464 kJ 100 g−1 respectively. The main reason for the higher energy density in smolts of salmon than trout is that the lipid density was almost three times higher in salmon. In addition, protein density was also significantly higher in salmon than trout. Thus, Atlantic salmon smolts have lower water content and higher somatic energy reserves than brown trout, when they start their ocean migration in spring.

Table 1.  Sample sizes and densities of somatic lipid, protein, water (g 100 g−1 wet mass), and energy densities (kJ 100 g−1 wet mass) of freshwater stages of anadromous Atlantic salmon and brown trout.
 SalmonTrout
SampleLipidProteinWaterEnergySampleLipidProteinWaterEnergy
  1. Student's t-tests were used when testing for significant differences between salmon and trout in similar developmental stages.

  2. ***P < 0.001, **P < 0.01, *P < 0.05.

Smolts  Age 1–3  April to May214.1 ± 0.8***18.1 ± 0.6***74.1 ± 0.7***464 ± 32***241.7 ± 0.816.9 ± 0.578.1 ± 1.2352 ± 36
Parr  Age 1–2  June to August178.0 ± 0.9***17.3 ± 0.4***72.3 ± 0.8***597 ± 35***544.5 ± 0.916.8 ± 0.676.0 ± 1.2454 ± 39
Immature parr  Age 1–3  October to November84.6 ± 0.6***18.7 ± 0.7***74.1 ± 0.7***493 ± 30***543.2 ± 1.117.8 ± 0.576.7 ± 1.0425 ± 41
Mature male parr  Age 1–3  October to November242.2 ± 1.1**17.6 ± 1.0***76.7 ± 2.0*389 ± 51**602.9 ± 1.418.6 ± 1.375.7 ± 2.2427 ± 64

In summer, somatic energy and lipid densities of parr were higher in salmon than trout (Table 1). On average, it was almost 600 kJ 100 g−1 with individual minimum and maximum values of 559 and 691 kJ 100 g−1 in salmon and c. 450 kJ 100 g−1 with minimum and maximum values of 280 and 529 kJ 100 g−1 in trout. Furthermore, the lipid density was almost twice as high in salmon as in trout, and protein density was also higher in salmon.

But in the autumn, just prior to spawning, somatic energy, as well as lipid and protein densities of mature male parr were lower in salmon than trout (Table 1). Mean somatic energy density in salmon was c. 390 kJ 100 g−1, with minimum and maximum values of 283 and 472 kJ 100 g−1. In trout, the mean energy density was approximately 10% higher, with minimum and maximum values of 335 and 624 kJ 100 g−1.

The energy, lipid and protein densities of immature parr in autumn were higher in salmon than trout (Table 1). In trout, mean energy density was 425 kJ 100 g−1, with respective minimum and maximum values of 353 and 496 kJ 100 g−1. In salmon, the corresponding values were 493 and between 418 and 533 kJ 100 g−1. Thus, in both species somatic energy and lipid densities were higher in immature than mature parr. The water content was higher in mature male salmon parr than in mature male trout parr. In all other stages investigated, the concentration of water was higher in trout than in salmon.

Total gonadal energy content increased linearly with somatic energy content in both species (Fig. 1). Mean male gonadal energy was more than twice as high in Atlantic salmon than in similar-sized anadromous brown trout (comparison of slopes: F1,95 = 2.76, P = 0.1; comparison of elevation: F1,96 = 113.4, P < 0.0001). This means that the mature males have allocated a large part of their lipid energy surplus in gonadal development, and salmon more so than trout.

image

Figure 1. Total gonadal energy content (Y kJ) on somatic energy content (X kJ) of mature male parr of anadromous brown trout Salmo trutta, age 1–3 years (x: —–; Ytrout = 0.053 Xtrout − 3.92, r2 = 0.81; d.f. = 60; F = 261.0; P < 0.001) and Atlantic salmon Salmo salar, age 1–2 years (•: ------; Ysalmon = 0.079 Xsalmon + 2.78; r2 = 0.58; d.f. = 35; F = 49.23; P < 0.001).

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Resumen
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

As hypothesised, juvenile Atlantic salmon in fresh water allocated relatively more energy into somatic reserves than corresponding brown trout, meaning that they invested relatively less in protein growth. We have data on Atlantic salmon from only one population, so it might be argued that it is difficult to judge the generality of the results. However, the energy density of lacustrine Atlantic salmon parr from Newfoundland caught in early September is close to the estimated mean of the immature parr caught in summer and late autumn in our study (Dempson et al. 2004). Furthermore, higher lipid and energy densities in trout than salmon parr were also indicated by Berg & Bremset (1998). Our summer and autumn estimates for salmon, however, were higher than those found by these authors in a stream in mid-Norway. We assume that this difference is real and not because of random variation, and may be at least partly due to the different location of the two salmon rivers.

The postsmolt ecology of Atlantic salmon appears to change with latitude and distance between the home river and the marine feeding area. Rivers in south Norway are located farther from the oceanic feeding areas in the North Atlantic than those in mid-Norway. The smolts may therefore need larger somatic energy reserves to reach these habitats quickly. In south Norway, Atlantic salmon smolts appear not to delay in coastal waters for feeding, but move quickly to sea, contrasting findings from north and mid-Norway (Jonsson et al. 1993; Rikardsen et al. 2004). In the south, the postsmolts use their stored energy reserves on their way out to sea (Stefansson et al. 2003). Smolts from rivers in north and mid-Norway, on the contrary, start marine feeding as they leave the river mouth and are found to be delayed near the coast before moving farther out to sea (Levings et al. 1994; Rikardsen et al. 2004).

The main feeding area of all Norwegian salmon is in the North Atlantic between Greenland and Norway north of the Faroese Islands and south of Spitsbergen (Holm et al. 2000; Hansen & Jacobsen 2003). The northern and southern limits are probably temperature dependent and appear to vary among years (L.P. Hansen, personal communication).

The marine feeding migration of brown trout is probably less energy demanding than that of Atlantic salmon. Anadromous brown trout feed in fjords and coastal waters, from the river estuary onwards, whether they originate from rivers in north or south Norway. Few individuals move farther away from the river mouth than 100 km (Jensen 1968; Jonsson 1985; Berg & Berg 1987; Jonsson et al. 1995), so little reserve energy is needed when they start marine feeding, and the observed energy density of the smolts was accordingly not much higher than that of the exhausted adults after spawning (cf. Jonsson et al. 1997).

The low energy density of brown trout smolts is similar to those found in masu salmon (Oncorhynchus masou Brevoort) (Henderson & Tocher 1987) and coho salmon [Oncorhynchus kisutch (Walbaum)] (Woo et al. 1978) in the North Pacific. Pacific salmon may also stay some time for feeding in the estuary, before moving out into the ocean (Fisher & Pearcy 1995; Kline & Willette 2002). However, a similar behaviour is not found for chinook salmon [Oncorhynchus tshawyscha (Walbaum)] at the southern end of their distribution in California, where the postsmolts have evolved an ocean-type life history and move directly into the ocean (MacFarlane & Norton 2002). We do not know if there are differences in the amount of stored energy in smolts from southern and northern populations of this species, although this might very well be the case, as indicated by the present study of Atlantic salmon. Estuarine feeding is reasonable if the growth opportunities for postsmolts are good, and/or the risk of predation relatively low.

Male Atlantic salmon parr allocate large amounts of their energy reserves in reproduction, compared with male trout parr. This is seen both from the reduction in energy density from summer to autumn, and the much higher gonadal investment in salmon. The difference may have evolved because of the much larger size difference between parr and anadromous males in Atlantic salmon than in brown trout. The somatic energy content of the anadromous trout males is approximately one order of magnitude larger than that of the mature parr males, in Atlantic salmon it is often two orders of magnitude larger. In male anadromous brown trout, gonadal energy content is approximately 3% of the somatic energy (Jonsson & Jonsson 1997), in anadromous salmon, it is approximately the same or slightly more (Gage et al. 1995; Fleming 1996; Jonsson & Jonsson 2003). Thus salmon parr often compete for fertilisation of eggs with fish producing much more milt than most trout parr do. There is a positive association between spermatocrit and the energy content of the milt, meaning that males with large gonads produce more sperm than those with smaller ones (Vladic et al. 2002). Hence, when parr males reproduce as sneakers (Gross 1985; Hutchings & Myers 1988; Moran et al. 1996), salmon may increase their success relative to that of their dominant rivals by partitioning relatively more energy for sperm production. This is not performed by brown trout, where the anadromous conspecifics have less milt than salmon (Jonsson & Jonsson 1997).

Salmon parr may also allocate more energy to gonadal development than trout because their spawning mortality is higher, so their chance of survival is low. Parr are targets of aggression from anadromous males and females as they are potential egg predators and male competitors for fertilisation of eggs (Jones & King 1952; Jordan & Youngson 1992; Jones & Hutchings 2001, 2002). If caught, parr may be fatally injured (Hutchings & Myers 1987), or even eaten by the anadromous adults (Fleming 1996). As the size difference between anadromous and parr males is much larger in salmon than trout, mortality during reproduction may be highest in salmon.

Somatic energy density at the time of spawning is lower in salmon than trout, but still many mature male salmon parr move to sea during the subsequent spring (Österdahl 1969; Hansen et al. 1989; Whalen & Parrish 1999). Salmon parr may feed at low temperature during winter (Finstad et al. 2004). In early winter, salmon parr with a low lipid content have an enhanced appetite (Simpson et al. 1996), and in spring, the spent parr males are found to have similar high somatic energy density as the immature salmon parr (Jonsson & Jonsson 2003), and much higher than the values we have measured for parr of brown trout (this study). The high priority for building lipid reserves, probably allows previously mature male parr to go through smolting in the subsequent spring. Obviously, trout are not doing the same, maybe because the fitness gain by going to sea is small, and smaller for previously mature than immature male parr.

The mechanism by which fish regulate their storage of lipid versus protein growth is virtually unknown. In endotherms, leptin, a hormone secreted from adipose tissue, influences body composition (Siervogel et al. 2003), and acts as a signal triggering puberty (Chehab et al. 1997). In ectotherms, leptin has been found to regulate energy metabolism of fence lizard, Sceloporus undulates (Niewiarowski et al. 2000), but has not yet been discovered from fish.

This study shows that the somatic energy densities of immature parr and smolts are higher in Atlantic salmon than brown trout. Obviously, storage of somatic reserve energy has higher priority in salmon where the distance to the feeding grounds at sea is much longer. The different energy storage pattern allows parr of Atlantic salmon to allocate more energy into gonadal development relative to somatic protein growth, compared with brown trout.

References

  1. Top of page
  2. Resumen
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References
  • Anonymous 1981. Determination of Kjeldahl nitrogen content with Kjeltec auto system 1, 2, 3, and 4. Teactor Application Note AN 30: 14.
  • Anonymous 1987. Determination of total crude fat in plant materials and feeding stuff with the Soxtec Hydrolyzing system. Tecator Application Note AN 92: 16.
  • Berg, O.K. & Berg, M. 1987. Migration of sea trout (Salmo trutta L.) from the Vardnes River in northern Norway. Journal of Fish Biology 31: 113121.
  • Berg, O.K. & Bremset, G. 1998. Seasonal changes in the body composition of young riverine Atlantic salmon and brown trout. Journal of Fish Biology 52: 12721288.
  • Chehab, F.F., Mounzih, K., Lu, R.H. & Lim, M.E. 1997. Early onset of reproductive function in normal female mice treated with leptin. Science 275: 8890.
  • Craig, J.F., Kenley, M.J. & Talling, J.F. 1978. Comparative estimators of the energy content of fish tissue from bomb calorimetry, wet oxidation and proximate analysis. Freshwater Biology 8: 585590.
  • Crossin, G.T., Hinch, S.G., Farrell, A.P., Higgs, D.A., Lotto, A.G., Oakes, J.D. & Healey, M.C. 2004. Energetics and morphology of sockeye salmon: effects of upriver migratory distance and elevation. Journal of Fish Biology 65: 788810.
  • Dellefors, C. & Faremo, U. 1988. Early sexual maturation in males of wild sea trout, Salmo trutta L., inhibits smoltification. Journal of Fish Biology 33: 741749.
  • Dempson, J.B., Schwarz, C.J., Shears, M. & Furey, G. 2004. Comparative proximate body composition of Atlantic salmon with emphasis on parr from fluvial and lacustrine habitats. Journal of Fish Biology 64: 12571271.
  • Finstad, A.G., Næsje, T.F. & Forseth, T. 2004. Seasonal variation in the thermal performance of juvenile Atlantic salmon (Salmo salar). Freshwater Biology 49: 14591467.
  • Fisher, J.P. & Pearcy, W.G. 1995. Distribution, migration, and growth of juvenile chinook salmon, Oncorhynchus tshawytscha, off Oregon and Washington. Fishery Bulletin 93: 274289.
  • Fleming, I.A. 1996. Reproductive strategies of Atlantic salmon: ecology and evolution. Reviews in Fish Biology and Fisheries 6: 379416.
  • Gage, M.J.G., Stockley, P. & Parker, G.A. 1995. Effects of male mating strategies on characteristics of sperm production in Atlantic salmon (Salmo salar): theoretical and empirical investigations. Philosophical Transactions of the Royal Society London B 350: 391399.
  • Glebe, B.D. & Leggett, W.C. 1981. Latitudinal differences in energy allocation and use during the freshwater migrations of American shad (Alosa sapidissima) and their life history consequences. Canadian Journal of Fisheries and Aquatic Sciences 38: 806820.
  • Gross, M.R. 1985. Disruptive selection for alternative life histories in salmon. Nature London 313: 4748.
  • Hansen, L.P. & Jacobsen, J.A. 2003. Origin and migration of wild and escaped farmed Atlantic salmon, Salmo salar L., in oceanic areas north of the Faroe Islands. ICES Journal of Marine Science 60: 110119.
  • Hansen, L.P. Jonsson, B., Morgan, R.I.G. & Thorpe, J.E. 1989. Influence of parr maturity on emigration of smolts of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 46: 410415.
  • Hansen, L.P., Jonsson, N. & Jonsson, B. 1993. Oceanic migration of homing Atlantic salmon. Animal Behaviour 45: 927941.
  • Henderson, R.J. & Tocher, D.R. 1987. The lipid composition and biochemistry of freshwater fish. Progressive Lipid Research 26: 281347.
  • Holm, M., Holst, J.C. & Hansen, L.P. 2000. Spatial and temporal distribution of post-smolts of Atlantic salmon (Salmo salar) in the Norwegian Sea and adjacent areas. ICES Journal of Marine Science 57: 955964.
  • Hutchings, J.A. & Myers, R.A. 1987. Escalation of an asymmetric contest: mortality resulting from mate competition in Atlantic salmon, Salmo salar. Canadian Journal of Zoology 65: 766768.
  • Hutchings, J.A. & Myers, R.A. 1988. Mating success of alternative maturation phenotypes in male Atlantic salmon, Salmo salar. Oecologia 75: 169174.
  • Jensen, K.W. 1968. Seatrout (Salmo trutta L.) on the river Istra, western Norway. Institute of Freshwater Research Drottningholm Report 48: 187213.
  • Jones, M.W. & Hutchings, J.A. 2001. The influence of male parr body size and mate competition on fertilization success and effective population size in Atlantic salmon. Heredity 86: 675684.
  • Jones, M.W. & Hutchings, J.A. 2002. Individual variation in Atlantic salmon fertilization success: implication for effective population size. Ecological Applications 12: 184193.
  • Jones, J.W. & King, G.M. 1952. The spawning of the male salmon parr (Salmo salar Linn. Juv.). Proceedings of the Zoological Society of London 122: 615619.
  • Jonsson, B. 1985. Life history patterns of freshwater resident and sea-run migrant brown trout in Norway. Transactions of American Fisheries Society 114: 182194.
  • Jonsson, N. & Jonsson, B. 1997. Energy allocation in polymorphic brown trout. Functional Ecology 11: 310317.
  • Jonsson, N. & Jonsson, B. 2003. Energy density and content of Atlantic salmon:variation among developmental stages and types of spawners. Canadian Journal of Fisheries and Aquatic Sciences 60: 506516.
  • Jonsson, N., Hansen, L.P. & Jonsson B.. 1993. Migratory behaviour and growth of hatchery-reared post-smolt Atlantic salmon Salmo salar L. Journal of Fish Biology 42: 435443.
  • Jonsson, N., Jonsson, B., Aass, P. & Hansen, L.P. 1995. Brown trout Salmo trutta released to support recreational fishing in a Norwegian fjord. Journal of Fish Biology 46: 7084.
  • Jonsson, N., Jonsson, B. & Hansen, L.P. 1997. Changes in proximate composition and estimates of energetic costs during upstream migration and spawning in Atlantic salmon, Salmo salar. Journal of Animal Ecology 66: 425436.
  • Jonsson, N., Jonsson, B. & Hansen, L.P. 1998. Density-dependent and density-independent relationships in the life cycle of Atlantic salmon, Salmo salar. Journal of Animal Ecology 67: 751762.
  • Jordan, W.C. & Youngson, A.F. 1992. The use of genetic marking to assess the reproductive success of mature male Atlantic salmon parr (Salmo salar L.) under natural spawning conditions. Journal of Fish Biology 41: 613618.
  • Kadri, S., Metcalfe, N.B., Huntingford, F.A. & Thorpe, J.E. 1995. What controls the onset of anorexia in maturing adult female salmon. Functional Ecology 9: 790797.
  • Kadri, S., Mitchell, D.F., Metcalfe, N.B., Huntingford, F.A. & Thorpe, J.E. 1996. Different patterns of feeding and resource accumulation in maturing and immature Atlantic salmon, Salmo salar. Aquaculture 142: 245257.
  • Kline, T.C. & Willette, T.M. 2002. Pacific salmon (Oncorhynchus spp.) early marine feeding patterns base don N-15/N-14 and C-13/C-12 in Prince William Sound, Alaska. Canadian Journal of Fisheries and Aquatic Sciences 59: 16261638.
  • Knutsen, J.A., Knutsen, H., Olsen, E.M. & Jonsson, B. 2004. Marine feeding of anadromous brown trout (Salmo trutta L.) during winter. Journal of Fish Biology 64: 8999.
  • Levings, C.D., Hvidsten, N.A. & Johnsen, B.O. 1994. Feeding of Atlantic salmon (Salmo salar L.) postsmolts in a Norwegian fjord in central Norway. Canadian Journal of Zoology 72: 834839.
  • MacFarlane, R.B. & Norton, E.C. 2002. Physiological ecology of juvenile Chinook salmon (Oncorhynchus tshawytscha) at the southern end of their distribution, the San Francisco Estuary and Gulf of the Farallones, California. Fisheries Bulletin 100: 244257.
  • Mason, M.J. 1983. Determination of glucose, sucrose, lactose and ethanol in foods and beverages, using immobilized enzyme electrodes. Journal of the Association of Official Analytical Chemistry 66: 981984.
  • Moran, P., Pendas, A.M., Beall, E. & Vazquez, E.G. 1996. Genertic assessment of the reproductive success of Atlantic salmon precocious parr by means of VNTR loci. Heredity 77: 655660.
  • Niewiarowski, P.H., Balk, M.L. & Londraville, R.L. 2000. Phenotypic effects of leptin in an ectotherm: A new tool to study the evolution of life histories and endothermy? Journal of Experimental Biology 203: 295300.
  • Österdahl, L. 1969. The smolt run of a small Swedish river. In: Northcote, T.G. ed. Symposium on salmon and trout in streams. H.R. MacMillan lectures in fisheries. Vancouver: University of British Columbia, pp. 205215.
  • Pemberton, R. 1976. Sea trout in North Agryll sea lochs, populations, distribution and movements. Journal of Fish Biology 9: 157179.
  • Rikardsen, A.H., Haugland, M., Bjørn, P.A., Finstad, B., Knudsen, R., Dempson, J.B., Holst, J.C., Hvidsten, N.A. & Holm, M. 2004. Geographical differences in marine feeding of Atlantic salmon post-smolts in Norwegian fjords. Journal of Fish Biology 64: 16551679.
  • Siervogel, R.M., Demerath, E.W., Shubert, C., Remsberg, K.E., Chumlea, W.C., Sun, S., Czerwinski, S.A. & Towne, B. 2003. Puberty and body composition. Hormone Research 60: 3645.
  • Simpson, A.L., Metcalfe, N.B., Huntingford, F.A. & Thorpe, J.E. 1996. Pronounced seasonal differences in appetite of Atlantic salmon parr, Salmo salar: effects of nutritional state and life-history strategy. Functional Ecology 10: 760767.
  • Stefansson, S.O., Bjørnsson, B.T., Sundell, K., Nykammar, G. & McCormick, S.D. 2003. Physiological characteristics of wild Atlantic salmon post-smolts during estuarine and coastal migration. Journal of Fish Biology 63: 942955.
  • Van den Thillart, G., Vianen, G. & Zaagsma, J. 2002. Adrenergic regulation of lipid mobilization in fishes; a possible role in hypoxia survival. Fish Physiology and Biochemistry 27: 189204.
  • Vladic, T.V., Afzelius, B.A. & Bronnikov, G.E. 2002. Sperm quality as reflected through morphology in salmon alternative life histories. Biology of Reproduction 66: 98105.
  • Whalen, G.K. & Parrish, D.L. 1999. Effect of maturation on parr growth and smolt recruitment of Atlantic salmon. Canadian Journal of Fisheries and Aquatic Sciences 56: 7986.
  • Woo, N.Y.S., Bern, H.A. & Nishioka, R.S.J. 1978. Changes in body composition associated with smoltification and premature transfer to seawater in coho salmon (Oncorhynchus kisutch) and king salmon (O. tshawytscha). Journal of Fish Biology 13: 421428.