The costs of becoming nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic Salmon
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1 Functional Ecology 1997 The costs of becoming nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic Salmon N. H. C. FRASER and N. B. METCALFE Fish Behaviour and Ecology Group, Division of Environmental and Evolutionary Biology, Graham Kerr Building, IBLS, Glasgow University, Glasgow G12 8QQ, UK Summary 1. Most animals are active by day or by night, but not both; juvenile salmonids are unusual in that they switch from being predominantly diurnal for most of the year to being nocturnal in winter. They are visual foragers, and adaptations for high visual acuity at daytime light intensities are generally incompatible with sensitive night vision. Here we test whether juvenile Atlantic Salmon Salmo salar are able to maintain their efficiency of prey capture when switching between diurnal and nocturnal foraging. 2. By testing the ability of the fish to acquire drifting food items under a range of manipulated light intensities, we show that the foraging efficiency of juvenile salmon is high at light intensities down to those equivalent to dawn or dusk, but drops markedly at lower levels of illumination: even under the best night condition (full moon and clear sky), the feeding efficiency is only 35% of their diurnal efficiency, and fish will usually be feeding at less than 10% (whenever the moon is not full, skies are overcast or when in the shade of bankside trees). Fish were unable to feed on drifting prey when in complete darkness. 3. The ability of juvenile salmon to detect prey under different light intensities is similar to that of other planktivorous or drift-feeding species of fish; they thus appear to have no special adaptations for nocturnal foraging. 4. While winter drift abundance is slightly higher by night than by day, the difference is not enough to compensate for the loss in foraging efficiency. We suggest that juvenile salmon can nonetheless switch to nocturnal foraging in winter because their food requirements are low, many individuals adopting a strategy in which intake is suppressed to the minimum that ensures survival. Key-words: Fish vision, foraging, invertebrate drift, Salmo salar, winter Functional Ecology (1997) Ecological Society Introduction Most animals can be classified as being either diurnal, nocturnal or crepuscular, since adaptations for activity at one light level tend to reduce efficiency at another. This is especially true for visual adaptations: diurnal species tend to show adaptations to increase spatial and temporal acuity and colour sensitivity, whereas nocturnal species may compromise on these aspects in order to enhance their visual sensitivity at low light intensities (Douglas & McGuigan 1989; Douglas & Hawryshyn 1990; Munz 1990). The greatest problem may therefore be faced by the limited number of species that switch between diurnal and nocturnal activity patterns. Juvenile salmonids were long considered to be predominantly crepuscular or diurnal foragers, since early studies showed that most of their food was obtained during the day with peaks just after dawn and at dusk (e.g. Hoar 1942; Higgins & Talbot 1985; Sagar & Glova 1988; Thorpe et al. 1988; Angradi & Griffith 1990). However, it has recently been demonstrated that they switch to being almost exclusively nocturnal in winter (Heggenes et al. 1993; Riehle & Griffith 1993; Contor & Griffith 1995; Fraser et al. 1995). This switch is dependent on temperature: as soon as water temperatures drop below about 10 C the fish start to shelter in streambed crevices during the day (Rimmer, Paim & Saunders 1983; Cunjak 1988) but emerge to feed at night (Fraser, Metcalfe & Thorpe 1993; Fraser et al. 1995). One possible reason for this highly unusual switch is an increase in the predation risk associated with daytime foraging in winter. Declining temperatures result in the fish becoming increasingly sluggish (Webb 1978; Johnson, Bennett & McLister 1996) and so less able to escape from warm-blooded predators such as piscivorous birds, which are predominantly diurnal. The tendency 385
2 386 N. H. C. Fraser & N. B. Metcalfe in winter to shelter in crevices during the day may thus be an antipredator behaviour (Fraser et al. 1993). Stream-living species such as the Atlantic Salmon Salmo salar L. rely almost entirely on vision to detect their prey (which is mostly in the form of drifting invertebrates): the fish dart out from a vantage position to intercept items of drift being carried past in the current (Keenleyside 1962; Stradmeyer & Thorpe 1987). Do salmon maintain their ability to detect prey items when they switch from diurnal to nocturnal foraging? This paper addresses this question by (1) measuring the night-time light intensities that are typically experienced by Atlantic Salmon in winter and (2) measuring the ability of the fish to detect and consume food items at these light levels. Methods NIGHT-TIME LIGHT INTENSITIES The natural range of light intensities experienced by juvenile salmon on winter nights was measured by recording light levels in west Scotland (56 N) at a location far from anthropogenic light sources (1 km from the nearest village). To obtain representative data from the more extreme conditions of night-time light intensity, measurements were only made if the sky was either fully clear or fully overcast, and if the lunar cycle was within 3 days of either full moon or no moon. Readings were taken on 37 different nights between 6 October 1995 and 3 February 1996; measurements were made usually once but occasionally twice during a single night (with at least 1 h between successive records), and up to five times (at 10-min intervals) during a single dawn or dusk (defined as from 1 h before to 20 min after sunrise, and from 20 min before to 1 h after sunset). Atlantic Salmon have a spectral sensitivity similar to that of humans (Ali 1961), and so a photometer (luxmeter) was the most relevant form of sensor since it measures light intensity as perceived by the human eye. Each measurement consisted of recording the level of illuminance (using a Skye Instruments SKL300 photometer, range lx, Skye Instruments Ltd, Llandrindod Wells, UK) in air both in the open and in the shade cast by a group of trees; normally the sensor was pointed vertically upwards, but on clear nights with a full moon it was also pointed directly at the moon to obtain the maximum reading. FEEDING EFFICIENCY IN RELATION TO LIGHT INTENSITY The experiments were carried out between 1 April and 23 May 1994 on 26 yearling parr, selected at random from a stock tank in which they had previously been reared under routine hatchery conditions of ambient temperature, natural light and excess food. The fish (mean forklength ± 0 13 mm, mean weight ± 0 49 g) were individually marked with alcian blue dye spots and then placed in a 1-m tangential flow grey fibreglass tank inside a lightproof constanttemperature cabinet; this maintained water temperature at 8 C throughout the experiment. The water depth in the tank was maintained at 30 cm (similar to the depth of water typically selected by this size of salmon; Heggenes 1990). To test the ability of the fish to detect and intercept food items moving in the water column (since drifting invertebrate food forms the majority of their diet; Keenleyside 1962; Maitland 1965; Stradmeyer & Thorpe 1987), we adopted the technique of Jørgensen & Jobling (1990, 1992) and prevented the fish from taking stationary or slowly moving food on the floor of the tank by holding them in a 60 x 30 cm 2 net enclosure suspended 10 cm above the tank floor. Our aim was to compare the feeding efficiency of the fish under different light intensities. We subjected them to a 12L:12D photoperiod where the intensity of illumination was kept constant during the day throughout the experiment but at night it varied between trials; food (commercial salmon pellets) was only provided at night. The daytime illumination was provided by a fluorescent strip light (450 lx). At night, the tank was lit by a 400 W metal halide lamp (Thorn Kolorarc MBIF Daylight, Thorn EMI Ltd, UK) positioned 1 5 m above the tank. This lamp produced light across a very broad spectrum (as indicated by the high colour rendering index, R a =90), similar to that of moon- or starlight. The light provided by this lamp was varied between trials (see below) by neutral density filters. Light levels were recorded as the mean of readings taken at 10 different points just above the water level across the width of the tank, using the same photometer as used for measurements of natural night-time light levels; light intensities experienced by the fish would be little different from those measured in air, given the shallow water depth. Food was dispensed by an automatic feeder that dropped a continuous trickle of pellets onto the water surface; these slowly sank through the moving water column before dropping through the bottom of the net out of the reach of the fish. Water velocity through the net enclosure was 5 10 cm s 1, similar to that selected at night by foraging salmonids in winter (Heggenes et al. 1993; Riehle & Griffith 1993). The food pellets were dark brown, and so at low light intensities provided a similar degree of contrast against the light grey background of the tank wall as many natural prey items. The feeder was adjusted to deliver less than the maximum potential daily food intake of the group so that fish would not cease feeding during a trial due to satiation. Food intake was measured using the X-radiography technique described in detail elsewhere (Talbot & Higgins 1983; Jørgensen & Jobling 1992; McCarthy et al. 1993). A sample of the normal food was mixed with tiny ballotini lead glass marker beads (size 9, Jencons
3 387 Nocturnal feeding efficiency in salmon Ltd, Leighton Buzzard, UK; 7% by weight) and repelleted; the ballotini beads are inert but are radioopaque and so show up in the digestive tract when the fish is subsequently X-rayed. The number of beads can then be converted to an estimate of the amount of food eaten by first X-raying known weights of the labelled food to produce a calibration regression. The experiment was run on a 1-week cycle: the fish experienced an intermediate night-time illumination (0 1 lx) for 3 days, during which the feeder operated at night; the feeder was then switched off for 3 days (to ensure that the fish were motivated to feed). The feeder then dispensed the labelled food for the last 4 h of darkness during the final test night, when light levels were fixed at one of eight settings ranging from complete darkness (0 lx) to sunrise with a clear sky (200 lx), presented in a random sequence. The fish were immediately anaesthetized and X-rayed (using a Todd Research TR80 kv/20 ma portable X-ray machine, Todd Research Ltd, Chelmsford, UK) at the end of this test night. Gut evacuation times are greater than 4 h at the test temperature of 8 C (Higgins & Talbot 1985), and so the X-ray plates recorded the entire intake of food for each fish during the test night. The feeder was weighed before and after this period of feeding to determine the amount of food delivered to the fish. Owing to mortality, the number of fish tested at any one light intensity ranged from 21 to 26. Results NIGHT-TIME LIGHT INTENSITIES Light intensities for a given state of moon and sky condition were relatively stable from 1 h after sunset until 1 h before sunrise; values were therefore pooled over this period, which was defined as the night. This produced sample sizes of 4 11 readings per category of sky condition (clear or overcast, full or no moon, open or shade). For readings taken in the open, the light level at night was consistently below the sensitivity of the meter (i.e. < 0 01 lx) in all overcast conditions (regardless of the state of the moon) and when the sky was clear with no moon. When there was a clear sky with a full moon the median-recorded light intensity was 0 03 lx, or 0 15 lx if the photometer was pointed directly at the moon. Night-time light levels in the shade were always below 0 01 lx regardless of the state of the moon or sky. Light intensities at dawn were similar to those at dusk, and so both times have been pooled for presentation (Fig. 1). Intensities at this time moved through approximately four orders of magnitude in under 1 h regardless of sky conditions or whether open or shaded (Fig. 1). However, readings in the open were consistently around 10 times higher than those in the shade. For instance, at sunrise/sunset the mean recorded values with clear skies were 190 lx in the open and 22 3 lx in the shade, while when overcast the corresponding readings were 55 8 lx and 4 6 lx. FEEDING EFFICIENCY IN RELATION TO LIGHT INTENSITY Fig. 1. Change in ambient light intensities during dawn and dusk on days when the sky was (a) clear and (b) overcast, plotted separately for readings taken in the open (open symbols) and under the shade of trees (filled symbols). Data for dawn and dusk have been combined and are medians of readings taken on 22 different days; time is plotted so that negative values represent the period before sunrise or after sunset. Readings below the sensitivity of the photometer (0 01 lx) have been plotted as lx. There was a strong influence of illumination on feeding efficiency: the percentage of fish within the group that obtained food was highly correlated with light level (Fig. 2a; Spearman s rank correlation r s = 0 905, n = 8 light intensities, P < 0 01).The relationship between light intensity and the probability of a fish feeding showed an excellent fit to a logistic regression (equation given by P(feeding) = x/(1 + x), where x=e 0.693log(y) and y = light intensity (set to lx for trial in complete darkness); Improvement χ 2 = 52 14, P < 0 001). At light intensities equivalent to sunrise around 90% of fish obtained food, but the success rate dropped rapidly so that under full moon conditions only 20 40% of fish were feeding, and none fed in complete darkness. A similar relationship with light was found for the mean amount of food
4 388 N. H. C. Fraser & N. B. Metcalfe only those individuals that obtained some food are included, and if calculations are based on medians rather than means (since the distributions were not normal), the amount of food obtained per fish shows no decrease (Fig. 2c; Spearman s rank correlation on median values, r s = 0 107, n = 7, NS). This indicates that a few fish were able to maintain their intake even on relatively dark nights, presumably because they were positioned close to where the food fell through the tank. However, there was no consistent pattern in the relative amount of food obtained by different individuals between trials (Kendall s Coefficient of Concordance, W = 0 126, n = 6, NS), nor was there any indication that food was limiting in any trial: the feeder delivered g of food over 4 h on test nights, of which a maximum of less than 30% was consumed. Fig. 2. Food intake of juvenile Atlantic Salmon during a 4-h period in relation to the prevailing light intensity. (a) The percentage of fish that obtained food (based on sample sizes of fish per trial); also shown is the line of the logistic regression relating the percentage of fish feeding to light intensity (see text for details of the regression equation). (b) The mean amount of food obtained per fish, expressed as a percentage of body weight to control for slight variations in body size between fish. (c) The median amount of food (% of body weight) obtained per fish; only salmon that obtained some food (n = 6 24 per trial) are included in calculations of the medians. obtained per fish (Fig. 2b; Spearman s rank correlation based on mean values, r s = 0 704, n = 8 light intensities, P < 0 05). This latter relationship is, however, slightly misleading since the calculations include those fish that obtained no food (i.e. the majority of the sample at the lower light intensities). If Discussion The results demonstrate that juvenile Atlantic Salmon are not particularly efficient at foraging in low light conditions, with less than 50% of the fish obtaining food at 1 lx, and minimal feeding rates below 0 01 lx. A similarly rapid decrease in foraging efficiency over the same range of light intensities has been noted for other species of fish feeding on planktonic prey (e.g. Minnow Phoxinus phoxinus (Harden Jones 1956), Coho Salmon Oncorhynchus kisutch (Brett & Groot 1963), Threadfin Shad Dorosoma petenense (Holanov & Tash 1978), Bream Abramis brama (Townsend & Risebrow 1982), Cutthroat Trout Oncorhynchus clarkii and Dolly Varden Salvelinus malma (Henderson & Northcote 1985) and Herring Clupea harengus (Batty, Blaxter & Richard 1990)). The same phenomenon has also been documented for the piscivorous Largemouth Bass Micropterus salmoides (McMahon & Holanov 1995), even though it is feeding on much larger prey items. While some species such as the herring are known to switch to filter-feeding at very low light levels (Batty et al. 1990), this is unlikely to be an option for stream-living salmonids because to encounter prey the fish would have to hold station in (rather than just adjacent to) areas of high current; the energetic costs of so doing would probably far exceed the energy gained (see Fausch 1984). In our experiment the fish were held off the bottom of the tank by a mesh false floor. Jørgensen & Jobling (1990, 1992) have shown that both Atlantic Salmon and Arctic Charr Salvelinus alpinus can feed effectively in complete darkness, but only if they are allowed access to pellets on the tank floor. This is rather an unnatural situation. Food pellets in a hatchery tank create a high density of prey items moving slowly across a smooth uniform surface virtually into the mouths of the resting fish; the resulting high rates of chance encounters are far greater than those between wild fish and potential benthic prey species. Wild fish in winter do not change their strategy from
5 389 Nocturnal feeding efficiency in salmon that of a sit-and-wait forager to hunting actively for prey hidden in the benthos (Fraser et al. 1993; Heggenes et al. 1993). Therefore, it is likely that benthic foraging is relatively unimportant and that wild fish must continue to rely on visual detection of drifting items for the majority of their food. At low light intensities relatively few fish obtained any food, but the amount acquired by these successful fish was comparable to that obtained at higher light levels. Since potential intake rates are closely related to the distance over which prey items can be detected, which is strongly influenced by light intensity (Henderson & Northcote 1985), the likely explanation for these results is that at high light levels fish could see the food pellets from any point in the net enclosure; all fish could exploit the food regardless of their position within the tank. In contrast, when light levels were much lower, only those fish that happened to be holding station in the direct path of the moving pellets were able to detect them. Such fish achieved a high intake whereas fish holding station a short distance away were oblivious to the food. There was no consistent ranking in the amount of food obtained by each individual, which indicates that the food source was not being monopolized or defended by particular fish. We have previously shown that while salmon are aggressive and attempt to defend feeding territories during the day, they exhibit virtually no aggression at night (Fraser et al. 1993), presumably because the radius of the defended area shrinks with the prey detection range. No fish fed when tested in complete darkness, indicating that salmon require some light to detect water-borne prey items (see also Jørgensen & Jobling 1992). To evaluate the extent to which salmon could be constrained by their inability at low light levels to feed effectively on drifting prey, we must first establish the range of ambient light intensities experienced by wild salmon. The measurements of night-time illuminance in this study are similar to those reported elsewhere: dusk was measured at 5 10 lx by Contor & Griffith (1995), while full moonlight has consistently been recorded as lx and starlight as lx (Harden Jones 1956; Brett & Groot 1963; Contor & Griffith 1995; McMahon & Holanov 1995). However, all of these previous studies appear to have made their measurements in the open and on clear nights, and our data show that light levels are generally one order of magnitude less in the shade, and are significantly lower when the sky is overcast. Since in northern latitudes winter skies are more frequently overcast than clear, and natural streams are often shaded by bankside trees, the lowest values in the recorded range of light intensities are perhaps the most appropriate. From 1 h after sunset until 1 h before sunrise, wintering juvenile Atlantic Salmon are at best (when lit by bright moonlight) able to feed on drifting prey at c. 35% of their maximal efficiency, and more typically are feeding at less than 10% efficiency. This reduction in foraging capability is offset for part of the year by a greater availability of food, since in general both the total quantity of drift and the average size of the prey species increases at night (e.g. Elliott 1965, 1967, 1970, 1973; Sagar & Glova 1988). From spring until autumn, when stream salmonids are active (and potentially able to feed) throughout the diel cycle, most studies of wild fish have found peaks in feeding at dawn and/or dusk (when light intensities are not constraining and drift abundance is higher than the daytime level) but rather little and less selective foraging during the night itself (Elliott 1970, 1973; Jenkins, Feldmeth & Elliott 1970; Sagar & Glova 1988; Angradi & Griffith 1990; Riehle & Griffith 1993; Forrester, Chace & McCarthy 1994). However, in winter the situation is different, since fish usually only emerge from daytime refuges when the light intensity is already low (Contor & Griffith 1995), so forcing them to use an inefficient foraging strategy. Moreover, the diversity of prey species available in winter may be reduced (Cunjak 1988), and the increase in drift food abundance at night is small or non-existent: the mean ratio of night:day drift abundance from December to February ranges from 1 05 ± 0 34 (n = 3 sampling months; data from Table 4 in Heggenes et al. 1993) to 2 21 ± 0 37 (n = 9 sitemonths; data from Elliott 1967: Figures 9 11). Even a 2 5-fold increase in prey availability at night could not offset the observed reduction in feeding efficiency of 65 90%. Salmonids exhibit a temperature-dependent shift in visual pigments, with a greater proportion of porphyropsin (as opposed to rhodopsin) in the retina at low temperatures (Allen et al. 1973; Tsin & Beatty 1977). It has been suggested that this may enhance their nocturnal foraging capability in winter (Fraser et al. 1993). Foraging success in the current study was measured at a temperature which should have induced the winter proportion of pigments (see Allen et al. 1973: Figure 2), so that their nocturnal capability would be at a maximum. However, many juvenile Atlantic Salmon exhibit a suppressed appetite over winter, insufficient to maintain body mass or reserves even in the presence of excess food (Metcalfe, Huntingford & Thorpe 1986; Metcalfe & Thorpe 1992; Bull, Metcalfe & Mangel 1996; Simpson et al. 1996), so a low foraging efficiency may be of little consequence since such individuals only require a minimal amount of food per day. The switch to nocturnal behaviour in winter therefore appears not to be driven by feeding efficiency, but may instead be a means of combating the dangers of ice formation (Cunjak 1988; Heggenes et al. 1993) or the increased daytime risk of predation in winter (Fraser et al. 1993). However, those salmon adopting the alternative life-history strategy of migrating to sea at their first opportunity (when aged 1-year old) attempt to maintain their food intake rates at a high level throughout the winter (Higgins & Talbot 1985;
6 390 N. H. C. Fraser & N. B. Metcalfe Metcalfe, Huntingford & Thorpe 1988). We would therefore expect that these fish would face the greatest cost of a poor night-time foraging efficiency; they may thus be forced to make occasional daytime sorties out of their refuges in order to maintain a desired growth rate. Acknowledgements We thank V. Cameron for fish husbandry, C. D. Bull for advice on X-radiography, BOCM Pauls for provision of fish food, and two referees for helpful comments on the manuscript. This work was funded by NERC grant GR3/9225 to NBM. References Ali, M. (1961) Histophysiological studies on the juvenile Atlantic salmon (Salmo salar) retina. Canadian Journal of Zoology 39, Allen, D.M., McFarland, W.N., Munz, F.W. & Poston, H.A. (1973) Changes in the visual pigments of trout. Canadian Journal of Zoology 51, Angradi, T.R. & Griffith, J.S. 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(1984) Profitable stream positions for salmonids: relating specific growth rate to net energy gain. Canadian Journal of Zoology 62, Forrester, G.E., Chace, J.G. & McCarthy, W. (1994) Diel and density-related changes in food consumption and prey selection by brook charr in a New Hampshire stream. Environmental Biology of Fishes 39, Fraser, N.H.C., Metcalfe, N.B. & Thorpe, J.E. (1993) Temperature-dependent switch between diurnal and nocturnal foraging in salmon. Proceedings of the Royal Society of London B 252, Fraser, N.H.C., Heggenes, J., Metcalfe, N.B. & Thorpe, J.E. (1995) Low summer temperatures cause juvenile Atlantic salmon to become nocturnal. Canadian Journal of Zoology 73, Harden Jones, F.R. (1956) The behaviour of minnows in relation to light intensity. Journal of Experimental Biology 33, Heggenes, J. 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(1978) Particulate and filter feeding in threadfin shad, Dorosoma petenense, at different light intensities. Journal of Fish Biology 13, Jenkins, T.M.Jr., Feldmeth, C.R. & Elliott, G.V. (1970) Feeding of rainbow trout (Salmo gairdneri) in relation to abundance of drifting invertebrates in a mountain stream. Journal of the Fisheries Research Board of Canada 27, Johnson, T.P., Bennett, A.F. & McLister, J.D. (1996) Thermal dependence and acclimation of fast start locomotion and its physiological basis in rainbow trout (Oncorhynchus mykiss). Physiological Zoology 69, Jørgensen, E.H. & Jobling, M. (1990) Feeding modes in Arctic charr, Salvelinus alpinus L.: the importance of bottom feeding for the maintenance of growth. Aquaculture 86, Jørgensen, E.H. & Jobling, M. (1992) Feeding behaviour and effect of feeding regime on growth of Atlantic salmon, Salmo salar. Aquaculture 101, Keenleyside, M.H.A. (1962) Skin-diving observations of Atlantic salmon and brook trout in the Miramichi River, New Brunswick. Journal of the Fisheries Research Board of Canada 19, Maitland, P.S. (1965) The feeding relationships of salmon, trout, minnows, stoneloach and three-spined sticklebacks in the River Endrick, Scotland. Journal of Animal Ecology 34, McCarthy, I.D., Houlihan, D.F., Carter, C.G. & Moutou, K. (1993) Variation in individual food consumption rates of fish and its implications for the study of fish nutrition and physiology. Proceedings of the Nutrition Society 52,
7 391 Nocturnal feeding efficiency in salmon McMahon, T.E. & Holanov, S.H. (1995) Foraging success of largemouth bass at different light intensities: implications for time and depth of feeding. Journal of Fish Biology 46, Metcalfe, N.B. & Thorpe, J.E. (1992) Anorexia and defended energy levels in over-wintering juvenile salmon. Journal of Animal Ecology 61, Metcalfe, N.B., Huntingford, F.A. & Thorpe, J.E. (1986) Seasonal changes in feeding motivation of juvenile Atlantic salmon (Salmo salar). Canadian Journal of Zoology 64, Metcalfe, N.B., Huntingford, F.A. & Thorpe, J.E. (1988) Feeding intensity, growth rates, and the establishment of life-history patterns in juvenile Atlantic salmon. Journal of Animal Ecology 59, Munz, W.R.A. (1990) Stimulus, environment and vision in fishes. The Visual System of Fish (eds R. H. Douglas & M. B. A. Djangoz), pp Chapman & Hall, London. Riehle, M.D. & Griffith, J.S. (1993) Changes in habitat use and feeding chronology of juvenile rainbow trout (Oncorhynchus mykiss) in fall and the onset of winter in Silver Creek, Idaho. Canadian Journal of Fisheries and Aquatic Sciences 50, Rimmer, D.M., Paim, U. & Saunders, R.L. (1983) Autumnal habitat shift of juvenile Atlantic salmon (Salmo salar) in a small river. Canadian Journal of Fisheries and Aquatic Sciences 40, Sagar, P.M. & Glova, G.J. (1988) Diel feeding periodicity, daily ration and prey selection of a riverine population of juvenile chinook salmon, Oncorhynchus tshawytscha (Walbaum). Journal of Fish Biology 33, 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, Stradmeyer, L. & Thorpe, J.E. (1987) Feeding behaviour of wild Atlantic salmon, Salmo salar, L., parr in mid- to later summer in a Scottish stream. Aquaculture & Fisheries Management 18, Talbot, C. & Higgins, P.J. (1983) A radiographic method for feeding studies on fish using metallic iron powder as a marker. Journal of Fish Biology 23, Thorpe, J.E., Morgan, R.I.G., Pretswell, D. & Higgins, P.J. (1988) Movement rhythms in juvenile Atlantic salmon, Salmo salar L. Journal of Fish Biology 33, Townsend, C.R. & Risebrow, A.J. (1982) The influence of light level on the functional response of a zooplanktivorous fish. Oecologia 53, Tsin, A.T. & Beatty, D.D. (1977) Visual pigment changes in rainbow trout in response to temperature. Science, Wash. 195, Webb, P.W. (1978) Temperature effects on acceleration in rainbow trout (Salmo gairdneri). Journal of the Fisheries Research Board of Canada 35, Received 29 April 1996; revised 20 September 1996; accepted 10 October 1996
Chinook salmon (photo by Roger Tabor)
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