Behavioural aspects of predation by juvenile Atlantic salmon (Salmo salar L.) on particulate, drifting prey

Anita. Behav., 1981, 29, 557-571

BEHAVIOURAL ASPECTS OF PREDATION BY JUVENILE ATLANTIC SALMON (SALMO SALAR L.) ON PARTICULATE, DRIFTING PREY BY J. W. J. WAI~KOWSKI Department of Agriculture and Fisheries for Scotland, Freshwater Fisheries Laboratory, Faskally, Pitlochry, Scotland

Abstract. A recirculatory flume tank simulating a simplified stream environment was used to study the feeding behaviour of juvenile Atlantic salmon (Salmo salar L.), 5.1 to 9.4 cm in fork length (from tip of snout to fork of tail), on artificial particulate prey passively drifting in the water current. Changes in feeding behaviour at two different times of the year and when fish were presented with prey of different sizes are described and quantified. Responsiveness to food was greatly reduced in autumn as compared to summer. The maximum distances at which prey elicited a response decreased in autumn to 40 % of the summer value, and the maximum distances which fish traversed in order to capture prey decreased by 80 % over the same period. During the peak growing season, the response to a range of prey sizes from 0.013 to 0.102 x fish fork length was directly related to prey size and could be accounted for on the basis of visual theory alone. Capture distances were closely related to fixation distances. Maximum capture distance increased to a peak value for prey of between 0.025 and 0.069 x fork length, while larger prey were never captured and the smallest prey rarely evoked a response. Prey size selectivity also operated after capture, through rejection versus retention of the prey. Introduction The freshwater residential phase of the Atlantic salmon's (Salmo salar L.) life cycle has long been regarded purely as a feeding and growth stage prior to the animals becoming smolts and migrating seaward. If this is correct, then the primary function of pre-smolt behaviour must be the acquisition of adequate food, for which efficient exploitation of available food sources is necessary. The fish-carrying capacity of streams and rivers is partly dependent on benthic productivity but is also greatly enhanced by input of material of terrestrial origin (Hasler 1975). A considerable quantity of material is being carried as drift by the current at any one time, and this represents a significant source of food for stream fishes (reviewed by Waters 1969). The utilization of drift prey has several advantages, including independence from local productivity and the potential elimination of the hunting and active searching component of energy expenditure normally associated with food acquisition (Schoener 1969). Wafikowski & Thorpe (1979a) found that the distribution of juvenile Atlantic salmon was closely related to the maximum locally available current velocity and thus to drift abundance. Drift feeding was the predominant method of food acquisition, although foraging on substrateassociated prey also took place where fish were closely associated with the substrate as a consequence of high cun'ent velocities. Other recent

studies (Bisson 1978; Symons & Heland 1978; Ringlet 1979) have confirmed these findings in S. salar and other salmonids. From the predictions of available predatorprey models (e.g MacArthur & Pianka 1966; Emlen 1968; Pulliam 1974), predators should minimize costs associated with locating, pursuing, capturing and ingesting prey. At the same time, benefits, in terms of net energy gain derived from prey consumption, should be maximized. Predators are therefore expected to be selective consumers, preying selectively on specific items rather than choosing prey in proportion to abundance. Salmonid fish have been shown to exhibit a high degree of selectivity based on prey body size. Various studies have produced different results, selectivity sometimes being shown to be biased towards the largest or the smallest available prey, or to be related to the body size of the fish predator (reviewed in Wafikowski & Thorpe 1979b). If prey selectivity is a mechanism for maximizing foraging efficiency, it follows that in the case of immature fish it also constitutes a mechanism for maximizing somatic growth, as opposed to gonadal growth. The importance of the relationship between the body sizes of fishes and their prey, from the point of view of the efficiency of energy acquisition, has been demonstrated mathematically by Paloheimo & Dickie (1966) and Kerr (1971), and experimentally in salmon by Wafikowski & Thorpe (1979b). The latter study 557

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demonstrated unequivocally that all sizes of juvenile Atlantic salmon fed on pelleted feed diets show significantly better growth on particle diameters between 0.022 and 0.026 x fish fork length than on a range of larger or smaller particle size categories. It has been well established that juvenile salmonids are predominantly visual predators (see e.g. All 1961; Protasov 1968; Ware 1973; Ringler 1979). Previous investigations (Wafikowski & Thorpe 1979a) have shown that juvenile Salmo spp. generally feed while holding station in a water current, and that both substrate-oriented and drift feeding take place. Substrate-oriented feeding consists either of bouts of foraging amongst the substrate or of isolated attack and capture sequences involving one particular prey item. Two types of drift feeding behaviour were observed: (i) A rapid burst of swimming directly towards the prey and interception of the item, followed by return to the original station. In this case capture almost always took place upstream of the station held by the fish. (ii) Material passing within 1 or 2 cm of a fish was occasionally captured by means of rapid side-to-side snapping movements of the head. The objectives of the present work were to study the responses of juvenile Atlantic salmon to drifting particulate prey and, having established basic response patterns, to investigate prey size selectivity. Using information obtained in a study of wild populations of the species (Wafikowski & Thorpe 1979a), laboratory experiments were devised such that the experimental conditions simuIated the most common type of environment in which juvenile Atlantic salmon were found. Simple prey, of uniform colour and shape, were presented in the current flow to individual fish in a simulated stream environment. Problems associated with pre-conditioning on a particular prey size were minimized by feeding a wide range of prey sizes to stock fish and by enforcing a 7-day period of food deprivation immediately prior to each experiment. Response and capture zones were recorded as twodimensional areas in the horizontal plane, the scope for movement of prey and fish in the vertical plane being small owing to the configuration of stream environments.

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Methods Experimental Material Juvenile Atlantic salmon from known pairings were reared from the alevin stage in 2-m-diameter radial flow tanks (Minaur 1973) under ambient environmental conditions at Pitlochry. Complete details of stock fish feeding and holding regimes are given in Wafikowski & Thorpe (1979b). The fish used during the June experimental series were in their second year and those used in August and September in their first year. Each were the progeny of a single cross. Prey particles were obtained by sieving crumbled Ewos salmon feed, using a set of closetolerance test sieves, into discrete limited-range size classes. The resulting particles were nearspherical, dark red-brown in colour, and slightly denser than water. Apparatus The apparatus consisted of a recirculatory flume tank, remotely-controlled feed particle dispensers, overhead illumination, and an overhead camera. The flume tank consisted of a rectangular box, slightly tapered at each end, 4.0 m long • 1.0 m wide x 0.4 m deep, constructed of 1.5-cm plywood (Fig. 1). The interior of the flume was painted a pinky-grey colour and baffles were of blackened stainless steel wire mesh. The experimental compartment was one metre square and the water depth was maintained at 0.22 m. Water recirculation was accomplished using a 7-kW in-line centrifugal pump with a ball valve fitted in parallel to the flume to control flow volume. Standard velocities within the experimental compartment were achieved at the half and three-quarters open positions of the valve. The arrangement of baffles produced a nearrectilinear flow over the entire width and length of the experimental compartment (Fig. 2). Suspended air bubbles were eliminated using the fine aperture baffle Q and the outlet cover plate H which prevented the formation of a suction vortex. Twenty-three equally spaced feed dispensers, controlled manually, were mounted on a frame suspended within the flume tank (Fig. 1). Each dispenser consisted of a 20-cmZ actuating syringe connected by fine-bore polythene tubing to a 5-cm 3 syringe cylinder and piston assembly mounted horizontally above the water surface and over a vertical guide tube (K, Fig. 1). Each actuating syringe was individually operated, the displaced air causing the piston in the dispenser

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to push a food particle out of the cylinder, dropping through the guide tube into the current flow. A typical particle trajectory is shown in Fig. 3. Salmon juveniles had been observed to feed in the wild under surface irradianee from 1 x 10 -1 to 1 x 102 W m -z, and showed no change in particle size selectivity within the range 1 x 10.2 to 1 x 102 W m -2. The light source used in the experiments consisted of eight 1.2-m, 40-W 'warm-daylight' fluorescent tubes, providing a resultant irradiance of 0.233 x 101 W m -~ measured at the flume bottom with the tank empty. In order to restrict illumination to the experimental area only and to eliminate reflection from the water surface, the light sources were surrounded by a system of reflectors. Light intensity was uniform over the bottom of the experimental compartment, while the sides and the upstream baffles and feed dispensers were in shadow.

A 35 m m Nikon F2 motor-driven 250-frame camera system, fitted with a 50 m m f 1.4 lens, was mounted 1 m above the centre of the experimental compartment, and run at a firing speed of 4.3 frames s-1. Sequential data showing fish and prey positions, feeding m o v e m e n t s and behaviour were obtained by projection of the negatives.

The Optical Environment The optical transmittance of the water within the experimental compartment, under standard operating conditions, was found to be 0.22 m -z, uncorrected for wavelength. This was measured using a 1.0-m path length 21% Transmissometer (Hydro Products, U.S.A). Wavelength-corrected transmittance was determined spectrophotometrically on small, staticwater samples using a path length of 0.01 m. Minimum attenuation was found to occur at 650 nm. In order to minimize the variation of

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contrast with viewing distance due to wavelength-dependent differential attenuation, it was decided to use prey pigmented in such a way that the peak wavelengths of reflected light would lie in the part of the visible spectrum where attenuation due to the optical properties of the water was lowest. The prey particles used were therefore pigmented a deep red colour with the dye Amaranth, the reflectance maximum of which was found spectrophotometrically to lie between 600 and 700 nm. Gross changes in the background against which fish viewed prey items were avoided by using only those fish which took up station in the characteristic position on the bottom and immediately in front of baffle S. From this position, prey could only be viewed against a vertical background and not against the water surface or tank base. All vertical backgrounds were in deep shadow, owing to the positioning of reflector screens. To determine whether possible differences in background had any substantial effect on the responses of experimental fish, the results of prey presentation to the left and right of each fish were compared. Since no overall differences were found the analysis of the results was undertaken as described. Standard operating conditions were those of maximum attainable clarity, defined as those under which the operator could distinguish a 0.1-cm diameter prey particle at the far side of the tank. A 12L:12D lighting schedule was maintained and all testing was accomplished between the fifth and eleventh hours of 'daylight'.

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Experimental Procedure Fifteen fish of mean fork length (from tip of snout to fork of tail) approximately equal to that of the stock population, were placed in the holding compartment of the flume. The fish were held and deprived of food for 8-10 days, depending on when they were used. Different fish were therefore deprived of food for varying periods; those remaining longest obtained limited quantities of waste food from the experimental compartment during days 8, 9 and 10. The pump was switched on after the first five days, during which water throughflow was provided by the ball-cock and standpipe arrangement only, and current velocities were gradually increased during the sixth day by increasing the valve aperture to the half or three-quarters open position as required. Fish were left to acclimate during the seventh day and experiments commenced on the eighth. One fish at a time was transferred without being netted through the hatchway in baflte S (Fig. 1) and allowed four hours to acclimatize to Top view

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WAIqKOWSKI: PREDATION BY SALMON ON DRIFTING PREY the experimental compartment and take up a fixed station. Those fish holding station to the rear of the compartment were then tested for feeding response. If this proved positive then the experiment commenced; if not, the fish was replaced. One food particle was placed in each dispenser prior to the transfer of fish, which were not disturbed during acclimatization and the experimental period. Each trial consisted of the release of one food particle and the filming of subsequent events until the prey was either ingested or rejected, or until it passed out of the experimental compartment. A period of 5-10 min was allowed between trials and dispensers were actuated in a random order. The end of one 250-frame film represented the termination of the trial series on that particular fish, which was then removed from the tank and measured for fork length. Three series of experiments were conducted and are listed in Table I. Those in August and September provided data on the response of the same stock to the same relative particle size during and after the growing season. The growing season was taken to end at the beginning of September, since at this time water temperatures dropped from 16 C to 7.5 C, subsequently remaining below 11 C and slowly falling (Wafikowski & Thorpe 1979b). The particle sizes used were the closest available to those found in prior experiments to give the best growth rate (Wafikowski & Thorpe 1979b) and were equivalent to 0.31-0.37 x mean fish fork length in August and 0.29-0.34 x mean fish fork length in September. The three-quarters open valve position was used since it had been found to provide a current velocity profile (A, Fig. 2) against which fish maintained stations on the flume bottom without actively swimming, and against which they were able to swim freely. The June experimental series demonstrated differences in response elicited by a variety of particle sizes. Wafikowski (1979) has demonstrated that internal mouth breadth limits the size of prey that can be ingested by Atlantic salmon juveniles. Five prey particle sizes were chosen, and are listed in Table I, ranging from larger than mean mouth breadth (0.60 cm) to smaller than that on which fish of this size showed maximum growth (Wafikowski & Thorpe 1979b). Over the experimental period, a total of 10 fish from two batches of 15 were used. Each fish was tested with two feed sizes assigned to alternate feed dispensers. One of the two sizes was carried over to the following series

561

of trials, on the next fish, such that a new size was carried over each time. In addition, in order to standardize any effect on the motivational state of the fish caused by the first prey captured, it was arranged that first capture was always of the 'new' size, after which dispensers were activated in a random order. The half-open valve position (B, Fig. 2) was used, differences in absolute current velocity between the June and August/ September experiments being necessitated by differences in fish size and season. Results The resting station held by all the experimental fish had the same orientation to the current flow, and therefore to the direction of feed presentation. In analysing the results of each experimental series these stations are plotted as one position, allowing all other points to be plotted in relation to a single initial station (Figs 4 and 5). Positions of prey at the first overt response from the fish (fixation), and at the point of prey capture, are drawn in the horizontal plane only. Each point represents one fish-prey interaction. All points originally to the left of the fish have been transposed to the right. Distances were measured from the centre of the fish's head. The results of each experiment are presented as a scatter diagram of prey positions at first fixation response by the fish, irrespective of subsequent events, and the area represented is designated the fixation zone. A similar scatter is plotted for the prey positions at interception. The outermost boundary of this scatter defines the maximum extent of the capture zone. The first overt response was always fixation on the prey by turning the head towards the prey position (except when prey were presented directly upstream of the fish, when the first recorded response was the movement of the fish towards interception). Fish that did not move off towards the prey immediately after first fixation returned to an upstream-facing posture. Fish which swam towards the prey but abandoned the capture attempt before interception returned to their original resting station, as did fish which successfully intercepted prey. Finally, captured prey were either ingested or rejected. These responses are summarized in Tables II and III and Fig. 6. The scattering of prey positions at first fixation may in part be explained by the recording technique used. The camera took 4.3 frames s-1 at current velocities between 10 and 20 cm s-1, which generates an error of 2.3--4.6 cm.

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WAlqKOWSFd: PREDATION BY SALMON ON DRIFTING PREY The premise that points of first fixation and capture might reflect the order of prey presentation through changes in satiation of the fish (e.g. Beukema 1968), was examined by inspection of response sequences and prey release order. No pattern with prey release order could be established. Experiments involving feeding to satiation showed that at 15 C, 8.0-cm fish starved for one week consumed in excess of twenty 0.23%0.280 cm diameter food particles, before rejecting any item offered.

The Influence of Season on Response Comparison of Figs 4a and 4b shows that during August, fish responded to prey at far greater distances than in late September. In August, fish of 5.36 cm mean fork length fixated on and captured potential prey presented up to 0.53 m either side of the fish's mid-line, a

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Fig. 4. Responses of juvenile Atlantic salmon to prey of near optimum size for growth during the growing season (11-14 August) and after cessation of growth in autumn (21-28 September). The figures show positions of prey at first fixation and at point of prey capture, release positions of prey eliciting no response, and the configuration of fixation and capture zones. Results of left-hand and right-hand responses have been transposed to the right of the figures, the outer boundaries of the zones so defined are shown on the left. Both zones extend to left and right of the fish as mirror-images, but for simplicity they have been indicated on the left-hand side only.

563

distance equivalent to 9.9 fish body lengths (bl). However, in late September, fish (from the same parental stock) of 8.08 cm mean fork length fixated only on prey presented at distances of less than 0.32 m, and captured only those prey presented within 0.15 m. These distances are equivalent to only 4.0 and 1.9 bl respectively, and represent a reduction in capture zone area from 4880 cm 2 in August to only 130 cm e in late September. This substantial decrease in the maximum distance traversed by fish in order to capture a prey item occurred despite a reduction in relative current velocity from 2.52 to 1.67 bl s-1. In August there was a clear-cut boundary (except for one out o f 50 prey presented) between the zone of positive response and the area in which no response was elicited. However, in late September, there was no such clear-cut boundary: one third of the prey passing through the fixation zone eIicited no response. On the basis o f a chisquared test this is a significant difference (P < 0.001, Z ~ = 86.57) between the two periods. The situation regarding capture of prey which had elicited a fixation response was not clear. In August, 32 out of 38 such prey were captured, while the corresponding figures for September were 9 out of 14, a significant difference at the P < 0.05 level only (X 2 = 5.25). Only 43 % o f prey passing through the fixation zone in September were captured, as compared to 82.1 7o in August. This difference seems to be due both to a lack of initial fixation response and to subsequent suppression of capture. The former could be explained by a failure to visually detect some prey items within the fixation zone, while the latter implies a choice not to attempt capture following initial fixation.

Prey Size Selectivity and Response Behaviour Fish showed very restricted and erratic responses to the smallest (0.013 • fish fork length) prey size; consequently, little photographic information on first response and capture was obtained. However, additional observations confirmed that the capture zone for this prey size was restricted to about 1.5 bl arc radius f r o m the station held. The proportion of the prey presented in the flume which elicited a fixation response was only 18% for prey of 0.013 • fork length, but was between 73 % and 84 700 for the four larger prey sizes (Table III). The proportion of these prey that were subsequently captured (Fig. 6) was between 96 and 100 7o for all prey sizes except the

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largest (0.102 • fork length), when fish moved towards only five of the 21 presentations which elicited a fixation response, and intercepted none of them. Table III indicates that fixation zone breadth and the associated capture zone breadth, where appropriate, increased with increase in prey size to a maximum for prey of 0.025 • fork length, and thereafter decreased gradually. However, from Fig. 5 it can be seen that this result could be an artefact resulting from the spatial constraints of the apparatus, which apparently prevented fish from utilizing the full extent o f their fixation zones with the larger prey sizes. The maximum distance at which a particular prey item can be detected visually depends on the predator's visual acuity and on the optical constraints of the environment, which affect the apparent contrast between prey and background. If the apparent visual acuity of the fish under the experimental conditions is known, then the maximum distance at which fish would be expected to respond to a prey item of a particular diameter, can be calculated. Acuity is normally measured in terms of the lowest limits of resolution, and is consequently defined as the angle, measured at the eye, subtended by the smallest detail which produces a detectable difference in retinal stimulation by comparison with the surrounding field (Pirenne 1962). Measurement of visual acuity using this strict definition was not attempted, since the maximum visual angle subtended by prey particles on which fish fixated was considered to provide an adequate base for the type of predictions required. Using results from the 0.018 • fork length prey size, the minimum visual angle was found to be eight minutes of arc. This is within the range 4.2 to 53.0 minutes measured for a variety of visually-feeding fish species (Yamanouchi 1956; Tamura 1957; O'Connell 1963; Protasov 1968). The mean transmittance of static water samples between 600 and 700 nm (the reflectance peak of the pigment used in the feed particles) was measured spectrophotometrically and found

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Current directionfromtop to bottomof figure Fig. 5. Responses of juvenile Atlantic salmon to prey o f five size categories. The figures show positions of prey at first fixation and at point of prey capture, release positions of prey eliciting no response, and the configuration o f fixation and capture zones. a: 0.100-0.118-cm-diameter prey (0.013 • fork length). b: 0.140--0.170-cm-diameter prey (0.018 x fork length).

c: 0.200--0.236-cm-diameter prey (0.025 • fork length) 9 d: 0.400-0.475-cm-diameter prey (0.051 • fork length) 9 e: 0.800-0.950-cm-diameter prey (0.102 • fork length). Results of left-hand and right-hand responses have been transposed to the right half o f the figures; the outer boundaries o f the zones so defined are shown on the left. Both zones extend to left a n d right o f the fish as mirror images, but for simplicity they have been indicated on the left-hand side only.

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to be 0.64 m -1. To maintain the contrast between prey and background, one must compensate for this loss :of 36 % of transmitted light per metre path length. Since the amount of light reflected from a: target is directly proportional to its area, a simple compensation (effective within the limits of the short distances being considered) can ibe accomplished by increasing the target area by 36 % per metre distance from the observer. Compensation was therefore calculated from the formula: L ' -= L(1.36) (r - ral2) where L is the prey diameter at fixation distance r,, and L ' is the derived prey diameter, based on the minimum visual angle and corrected for optical attenuation, at a distance r. Figure 7 compares this derived relationship between prey diameter and maximum fixation distance with that measured in the experiment. Divergence between the calculated and measured distanceprey-size relationship is almost certainly due to the spatial limitations of the apparatus, restricting maximum fixation distance for the two largest prey sizes. Selectivity on the basis of prey size is further demonstrated by the proportions of prey eliciting a fixation response that were subsequently captured, ingested or rejected after capture (see Fig. 6). The results demonstrate one threshold prey size, between 0.025 and 0.051 x fork

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length, below which almost all captured prey were ingested and above which almost all were rejected; and a second threshold size between prey 0.051 and 0.102 • fork length above which prey were never taken and below which virtually all prey were captured. Clearly there must be threshold prey sizes outside which prey physically cannot be captured. With regard to an upper size threshold, experimental work reported elsewhere (Warikowski 1979) demonstrated that, since salmon ingest items whole and do not bite pieces

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Fig. 7. The variation with prey size of measured and calculated maximum fixation distances. The calculated maximum fixation distance is derived from measurements using the 0.018 x fork length prey size corrected for optical attenuation with viewing distance by increasing the target area by 36 % per metre path length, where the target area is the cross-sectional area of the prey item at right angles to the line of sight. The maximum fixation distance possible for 8.62-cm fish in the experimental tank was 1.16 m.

WAlqKOWSKI: PREDATION BY SALMON ON DRIFTING PREY out of large items, internal mouth breadth serves as the extreme upper limit to the accessible prey size range. Thus, while experimental fish occasionally began an attempt to capture prey larger than mean internal mouth breadth, they abandoned this attempt at some point before interception. Prey size selection in juvenile Atlantic salmon was therefore found to operate on three levels. Large prey are seen at greater distances than smaller prey, the maximum distance at which prey may be fixated being therefore directly related to prey size; prey larger than a certain threshold size, probably related to maximum internal mouth breadth of the fish, are not intercepted; and prey may be rejected after capture. Discussion On the basis of visual theory and simple stimulus-response behaviour, it would be expected that points of first overt response would form a part-sphere represented in the Figures as an arc in front of the fish with the head of the fish as its centre. The radius of the are would thus depend on visual acuity, the apparent contrast (Duntley 1962) between prey and background, and motion. In fact, points of first response formed a fan-shaped scatter, which often departed radically from this hypothetical arc. Departure from this arc directly in front of the fish (see Figs 4 and 5) may be explained by considering the nature of the response measured. There is evidence that prey velocity influences the response o f fish predators (Boulet t960; Ware 1973; Kislalioglu & Gibson 1976). The angular velocity of prey decreased the closer the prey release point was to the resting fish, although linear velocities remained uniform. Therefore, the closer to the resting fish that a prey particle was released, the greater the real distance it travelled in order to appear to experience the same displacement. If the fixation response is to some extent dependent on the apparent displacement of moving prey, then prey the trajectories of which passed close to the fish would not be expected to elicit a response until they had traversed a greater distance (i.e. were closer to the fish) than prey the trajectories of which passed further away from the fish. Furthermore, since the recorded response when prey were presented directly in front of the fish was not first fixation but movement towards the prey, it might be expected that this part of the fixation zone would appear depressed. A functional explanation for depression of the fixation zone directly

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upstream of the fish would be that a prey item approaching from this direction would have a very high probability of certain interception; the fish may therefore afford to wait until the item is very close. In some instances (Figs 5e, d and e), departure from this hypothetical arc can also be accounted for purely on the basis of spatial constraints imposed by the apparatus, particularly in the case of the sharp cut-off in points of first fixation about 0.1 m downstream of the feed dispenser array. The space within which a visual predator responds to prey depends in the first instance on the maximum distance at which the predator can see the prey. Three classes of factor influence this distance directly: environmental characteristics; the predator's visual system; and prey characteristics. Primary environmental factors are incident light intensity (Hemmings 1966; Protasov 1968), turbidity (Tyler & Preisendorfer 1962; Moore & Moore 1976), and the inherent contrast between the prey and the background against which it is seen (Duntley 1962; Hemmings 1966). In considering the predator's visual system, only visual acuity and colour perception are likely to affect the distance at which prey are visible to the predator. Tamura (1957) and Hester (1968) have shown that the probability of detection is highest in the binocular part of the visual field of certain fish. The distribution of retinal pigments in fish would seem to indicate that the demands of contrast are directly opposed to those of colour sensitivity (Lythgoe 1966); the resultant compromise presumably depends on the particular requirements and visual environment of the species. The visual appearance of a prey item can be defined by its colour, shape, size, and behaviour. Since salmonids can discriminate between colours (e.g. All 1961), a primary effect on visual location would be that of colour-dependent inherent contrast (demonstrated to be an important factor in rainbow trout predation, by Ginetz & Larkin 1973). The shape of an object may also affect visibility: for example, a diffuse shape (e.g. an insect body, with many thin projections) may appear smaller at a distance than a compact shape of similar overall size (see e.g. Zaret 1972). A direct, but species-specific, relationship between prey size and response distance has been found in horse mackerel, Trachurus sp. (Protasov 1968), cod, Gadus morhua (Brawn 1969), rainbow trout Saline gairdneri (Ware

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1972), bluegill sunfish, Lepomis macrochirus (Werner & Hall 1974), and flounder Platiehthys flesus (Moore & Moore 1976). Prey behaviour likely to affect overall accessibility of prey has been shown to fall into two categories: concealment (Ivlev 1961; Stein 1977), and mobility and escape reactions (Moore & Moore 1976). The use of living prey to study the feeding responses of fish is subject to certain limitations. A fundamental problem is that of finding a standard prey. Different species of prey organisms exhibit characteristic concealment and avoidance behaviour as well as continuous movement associated with a variety of functions. Shape, colour and visibility also vary between species and often between life stages within one species. Investigation of the response to different body size categories is restricted by the difficulty of obtaining a wide range of otherwise identical organisms (see e.g. Le Brasseur 1969). Therefore, for the present study, it was decided to use easily available pelleted feeds, the composition and particle size of which could be rigidly controlled. This circumvented the specific objections above, since the prey were simple, non-motile particles drifting passively along a simple trajectory. On recognition of a suitable prey item, the predator has the choice between attempting capture or continuing to search. In order for an animal to survive and grow, feeding activity must yield a net energy gain. This clearly places limitations both on the distance that can be travelled in order to capture prey and on the size of prey taken. These factors are clearly interrelated, since increased prey size compensates for an increased capture distance. Optimal foraging theory predicts four categories of foraging choice (see e.g. Pyke et al. 1977). These four categories are concerned with foraging location, allocation of time to particular locations, patterns of foraging movement withing locations, and diet. In the present instance, S. salar juveniles have been shown to choose locations of high current velocity and concomitant drift concentration, to choose a particular foraging movement pattern, and to select prey on the basis of size. Allocation of time to particular locations has not been investigated in this study. The present experiments concern the feeding behaviour of juvenile salmon held in a flatbottomed tank under a non-turbulent nearrectilinear flow regime. This environment closely approximated to the conditions under which large concentrations of juvenile salmon were

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found in the wild. Wafikowski & Thorpe (1979a) reported such concentrations over flat bedrock, over level substrates of fine gravel, and in open water. Since juvenile salmon always held feeding stations which afforded a wide upstream field of view, water clarity was the only environmental constraint likely to affect fixation distances. Fish maintained in the experimental flow regime showed the same position-holding and feeding behaviour as fish of a similar size in the wild during the same part of the year (June, August and September; Wafikowski & Thorpe 1979a). That is, they faced directly upstream and maintained station on the bottom of the tank. This position was held by adopting a characteristic posture in which the pectoral fins act as hydroplanes exerting a downward force and the fish rests on the pectoral and caudal fins. In this posture, fish of 8.62, 5.36 and 8.08 cm mean fork length were subjected to mean current velocities of 2.33, 2.52 and 1.67 body lengths per second (bl s-1) respectively. These velocities are well within the range 0.0-8.3 bl s-1 experienced in the wild (Wafikowski & Thorpe 1979a). The foraging pattern of juvenile Atlantic salmon resident in streams and rivers is unusual in that they generally prey on drifting material by holding position in a water current as described above, and make individual forays from that position to capture single prey items. Since the prey drifts passively in the water current (the component of movement of motile prey organisms is likely to be very small in comparison with the water current velocities under consideration) and the predator actively maintains position against that current, it can be considered that the immediate environment of the predator, containing the prey, is stationary and that the predator swims at a constant velocity through it. There is therefore no element of pursuit involved in the capture of prey, merely intersection of the prey trajectory by the predator. Similarly, the searching component of predation is much simplified in comparison with classical predator strategies. Provided an individual fish locates an area of high drift abundance (assuming the available drift to contain suitable food), then searching for prey consists only of maintaining station in the current flow and visually scanning the surrounding environment. Station is commonly maintained by reference to stationary elements of the environment outside the water current, such as features of the substrate or river bank (Arnold 1974). Energy expenditure directly associated with feeding in

WAlqKOWSKI: PREDATION BY SALMON ON DRIFTING PREY the present instance is therefore limited to that used in maintaining a searching station and moving to intercept prey, and in the subsequent manipulation, ingestion and digestion of the prey. Energy expenditure in maintaining a searching station may be considerably greater than that of active searching under some conditions, for example low current velocities. Wafikowski & Thorpe (1979a) found that Atlantic salmon juveniles sometimes avoided maintenance of a station against a current flow by remaining in low-velocity conditions immediately adjacent to the areas of high velocity and high drift abunddance within which feeding took place. Pyke et al. (1977) reviewed published results on optimal diet choice and concluded that in theory: an animal should never specialize on a 'less preferred' food type; if a food type is included in an optimal diet it should be consumed whenever encountered, and if it is excluded it should never be consumed; and increased food abundance should lead to greater food specialization. Wafikowski & Thorpe (1979b) found that 0.022-0.026 x fish fork length was the optimum food particle diameter for growth maximization in juvenile salmon; that is 0.19-0.23 cm in the case of fish of 8.62 cm mean fork length, and prey size categories larger and smaller than this resulted in significantly reduced growth. The present results demonstrate that prey larger and smaller than this optimum size are less likely to be consumed. In the case of larger-than-optimum size categories, fish chose either not to attempt capture or to reject almost all captured items, while smaller-than-optimum s i z e categories elicited reduced fixation distances or were not responded to. However, non-optimal sizes were not completely excluded from the diet, except when size precluded ingestion. Wafikowski (1979) compared optimum prey size in S. salar derived from growth and behaviour experiments with that implied from examination of size-frequency distributions of the stomach contents of wild fish. He found that the experimental optimum prey size corresponded precisely with the most common size category of natural prey found in fish of comparable size. The experiments considered above were performed in June, a period of characteristically rapid growth during the early part of the short salmonid growing season (e.g. Alien 1969), when maximization of food intake would be expected. Rapid growth characteristically continues

569

through to August, declining in September (Brett et al. 1969; Elliott 1976). This decline in growth rate occurs independently of ration level (Brett et al. 1969; Elliott 1975). The present work demonstrated that responses to prey of nearoptimal size for growth were greatly reduced in September, both in intensity and with distance, in comparison to those in August (and June); a result consistent with reduced energy demands. The zone within which fish fixated on prey was reduced in relative breadth by 60 ~o and the zone within which prey were captured by 80~. Furthermore a significantly lower proportion of prey passing through the fixation zone elicited a response, and a smaller proportion of these were captured after the end of the growing season than during its height. Reduced metabolic efficiency due to decreasing water temperatures would be expected to restrict activity and so the reduced capture distances observed may simply be a direct function of temperature. Alternatively, given the environmental constraints imposed on the metabolism and behaviour of the fish during autumn and winter, it may be that feeding in the reduced capture zone was most profitable, and that reduced efficiency made feeding outside this zone unjustified in terms of energetics. During the experiment prey abundance was comparable between the August and late September series, while in the natural environment, abundance decreases during autumn and winter. If, as according to theory, increased food abundance should lead to greater food specialization, then the converse should be true: decreased food abundance should lead to reduced specialization. Although the present results indicate reduced responses to optimum prey size, Wafikowski & Thorpe (1979b) demonstrated that during the late autumn and winter seasons, maxlmum growth was elicited by a comparatively wider range of prey sizes, implying reduced specialization.

Acknowledgments The author wishes to thank the staff of Shared Technical Services, University of Stifling, for the construction of various pieces of equipment, and Messrs I. Irvine and A. McQueen for their care of stock fish. Particular thanks are extended to Dr J. E. Thorpe, Dr P. Tytler, and Ms K. R. Perry for their support, criticism and discussion throughout the work, and during preparation of the manuscript. The study was in part funded by the Natural Environment Research Council.

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(Received 25 January 1980; revised 17 June 1980; MS. number: 1976)