The effect of prey type on the predatory behaviour of the fifteen-spined stickleback, Spinachia spinachia (L.)

Anita. Behav., 1992, 43, 147-156

The effect of prey type on the predatory behaviour of the fifteen-spined stickleback, Spinachiaspinachia(L.) M I C H E L J. K A I S E R * , R O B I N N. GIBSONI" & R O G E R N. H U G H E S * *Functional and Evolutionary Biology Group, School of Biological Sciences, University of Wales, Bangor, Gwynedd LL57 2UW, U.K. ~Dunstaffnage Marine Laboratory, PO Box 3, Oban, Argyll PA34 4AD, U.K. (Received28 December1990; initial acceptance26 February1991; final acceptance 7 June 1991;MS. number:3702)

Abstract. The fifteen-spined stickleback, preying on the mysid, Neomysis integer, and the amphipod,

Gammarus Iocusta, maximized its energy intake by adjusting its predatory behaviour to the prey being attacked. The escape speed of Neomysis placed an upper constraint on the size of the prey available to fish of a given size. The increase in importance of Neomysis in the natural diet of larger sticklebacks reflected size-dependent limitations of the fast-start performance in these fish. The escape speed of Gammarus did not limit its availability to the sticklebacks; the limiting factor for this prey was its cross-sectional area. The fish expended 20 times more energy attacking Neomysis than Gammarus, but Gammarus took up to 159 times longer to ingest. Neomysis always responded to an attack with a tail-flip, which usually resulted in movement at an angle of approximately 90 ~ to the direction of attack. Although Gammarus occasionally used a tail-flip response, it was never used to escape a fish attack. Adoption of a stationary C-shape often deterred the fish from attacking Gammarus. Many foraging models have assumed that prey can be ranked in order of profitability, determining which prey should be included in the diet (Werner & Hall 1974; Elner & Hughes 1978; Hughes 1980, 1988; Dunkin & Hughes 1984). Diet selection is influenced by many factors including hunger level (Beukema 1968; Croy & Hughes 1991a), risk of predation (Croy & Hughes 1991b), and experience and learning (Thomas 1977; Milinski 1979; Cunningham & Hughes 1984; Croy & Hughes 1990). In particular, the latter two factors may determine the methods used by a predator to catch prey (Nyberg 1971; Elner 1979; Webb & Skadsen 1980; Cunningham & Hughes 1984). Morphological aspects (Werner 1977; Wankowski 1979; Kaiser et al. 1990) and prey-capture performance (Webb 1976, 1984) of predators, however, place upper and lower constraints on the size of prey captured (Hart & Harmin 1990; Sih & Moore 1990). Prey recognition is an important factor in diet selection in fishes (Jacobs 1965; Protasov 1970; Kislalioglu & Gibson 1976; Holmes & Gibson 1986). Various factors, such as body shape (de Groot 1971; Holmes & Gibson 1986) and movement (Kislalioglu & Gibson 1976; Holmes & Gibson 1986), all elicit feeding responses in predatory species. 0003 3472/92/010147+10 $03.00/0

The fifteen-spined stickleback is an ambush predator (Croy 1989), consuming both benthic and pelagic invertebrates. Mysids and amphipods are usually the most important food items in the diet (Kislalioglu & Gibson 1977; present study), and there is a logarithmic relationship between the stickleback's length and the size of prey eaten (Kislalioglu & Gibson 1976, 1977; M. J. Kaiser, unpublished data). Amphipods maintain a high level of dietary importance throughout the ontogeny of the fish, whereas mysids become progressively more important with increasing fish size (Kislalioglu & Gibson 1975; present study). The amphipod Gammarus locusta tends to be cryptic, hiding under stones and between fronds of weed whereas the mysid Neomysis integer shoals within 1 m of the substratum (O'Brien & Ritz 1988). Neomysis have large conspicuous eyes and a discrete set of pereopods (thoracic limbs) in the region of the carapace, whereas Gammarus have small, indistinct eyes and conspicuous appendages along most of the body (Fig. 1). These external visual characteristics allow sticklebacks to differentiate between the two prey types (M. J. Kaiser, unpublished data). The present study investigates the ability of sticklebacks to make fine adjustments 9 1992The Association for the Study of Animal Behaviour 147

Animal Behaviour, 43, 1

148 Gornrnarus

species were kept in the same aquarium conditions as the fish.

Video-recording Technique J

Neomysis

Spinach/a

Figure 1. The anaphipod, Gammaruslocusta, the mysid, Neomysis integer and the fifteen-spined stickleback, Spinachia spinachiaL. showing centre of mass (C), which is found 0.40+ 0.013 ()7+ sE) standard body length from the tip of the smout. Scale bars: 1 cm.

to its predation technique on the basis of these characteristics. Attack behaviour in sticklebacks is a sequence of inter-related steps: searching, orientation towards prey, prey fixation, S-bend (describing the fish's body posture prior to a strike), capture and ingestion, each step differing in duration (Croy & Hughes 1990). We used this sequence to elucidate which factors might influence selective predation over the short time from the S-bend (Fig. 2a) to the moment of prey capture. The escape responses of Neomysis and Gammarus were also examined, in relation to specific prey recognition and the fine adjustment of predatory tactics.

METHODS

Animal Collection and Maintenance We collected sticklebacks from Dunstaffnage Bay, near Oban, Scotland, by seine or push-netting, from July 1989 to March 1990. They were held in circular 36-1itre opaque tanks with a running seawater supply at 15_. I~ in constant light conditions. Neomysis were collected in a small stream at Dunstaffnage Bay by push-netting at low-water. Gammarus were collected from beneath stones and fucoid algae in the intertidal zone. Both prey

The video-recording technique described by Batty (1983) was used in all experiments to record the attack and escape sequences of the predator and prey, respectively, with fluorescent lights providing background illumination. Infra-red light from a light-emitting diode was focused by a Fresnel lens onto a JVC TK-S310 television camera fitted with an infra-red transmitting filter. The diode was strobed in synchrony with the video field pulse. This technique produces sharp, unsmeared silhouette images, allowing accurate frame-by-frame analysis. A frame rate, of 50/s, gave sufficient resolution for analysis. A glass aquarium measuring 90 x 37 • 37 cm was mounted on a stand between the condenser lens and the camera, such that the light from the diode was free to pass through the base of the tank. The water depth in the tank was 10 cm and held at 15 + 1~ An arena 25 cm in diameter and made of plastic sheet was placed in the aquarium to restrict both the fish and prey within the infra-red illuminated arena, during filming.

Videotape Analysis The reference points used to determine movement between frames were: (1) the fish's mouth, as it is the distance from the mouth to the prey that is most relevant in this study; (2) the third abdominal segment of Neomysis, as this is the point of flexion during a tail-flip response; (3) the centre of the Gammarus body during a flip response; and (4) the anterior of the Gammarus head during linear swimming. Sequential displacement every 0.02 s was measured by plotting the position of the reference points onto acetate sheet fixed to a monitor screen.

Escape Responses of Prey We designed an experiment to simulate predator attacks on prey while recording the responses of the prey. This allowed us to determine maximum escape velocities, and other anti-predator behaviour, for later comparison with fish fast-start performance and predatory tactics. Gammarus or Neomysis were placed in the arena and allowed to settle for 5 min. The head region was then approached with a hand-held glass probe to stimulate an escape response. Sticklebacks most commonly attack the head of the prey, validating the

Kaiser et al.: Stickleback predatory behaviour

149

Gammarus

Neomys~

[Q)

{b)

{d)

Figure 2. Stickleback attacking Neomysis and Gammarus. (a) S-bend prior to a fish strike; (b) preparatory stroke; (c) main propulsive stroke; (d) fish decelerating after an attack. The time elapsed between each frame is 0-02s. above procedure (Kislalioglu & Gibson 1976; Croy & Hughes 1991c; personal observations). Prey were grouped into size classes to investigate any effect on escape ability. Individual prey (51 Neomysis and 78 Gammarus) were stimulated at a low frequency of once every minute for 5 min to reduce effects of habituation and fatigue. The velocity of escape was estimated by measuring the distance moved by the predetermined points on the prey's body every 0.02 s. Fish Predation Ten sticklebacks ranging from 85 to 115 mm in total length were used. Before a trial, the fish were food-deprived for 24 h to standardize their hunger state. Individual Neomysis ( N = 52) or Gammarus ( N = 19) were placed in the arena behind the fish's caudal fin, allowing the prey to settle. Videorecording ceased after the fish had captured and eaten the prey, or after 5 min had elapsed. The trailing-edge amplitude and body curvature (chord) were measured from a video monitor, as they are directly related to the thrust and provide a comparable measure of burst-swimming performance (Webb 1978). Body curvature was measured as the chord of the curve from the trailing-edge of the caudal fin to the fish's centre of mass (Webb 1978). Trailing-edge amplitude was defined as the distance

from the flexed caudal fin to a line passing through the centre of mass parallel to the direction of movement (Webb 1978). Centre of Mass Before trailing-edge amplitude or body curvature could be measured the centre of mass had to be determined. Five fish between 70 and 115 mm total length were killed in MS 222 and then blotted dry to remove excess water. Each fish was cut into 5-mm segments and each segment weighed to two decimal places. A cumulative plot of segment weight (g) from the snout and from the caudal fin allowed the centre of mass to be estimated. Natural Diet A sample of 115 sticklebacks that had been caught at Tralee Bay, near Oban, Scotland, between June 1986 and December 1989, were dissected and their stomach contents identified. The length of any intact animals was used as a measure of prey size. Frequency of occurrence was used as a measure of relative importance of prey type in the diet. Ingestion Time Two groups of five sticklebacks of mean+_sE standard length 102-5 + 2.5 and 85.7 +_2.5 m m were

150

Animal Behaviour, 43, 1

60 15-I6 m m

13-14ram "

30

0.04

o

9~

60

-

T

~

I0-I~ m m

0.08

O-IZ

0.08

-i 7-14mm 5-6 mm 0-12

(b)

Z E

30

~ 0

~ O.04 Time ( s /

Figure 3. Cumulative displacement measured from analysis of video recordings. (a) The responses of Neomysis 10-12, 13-14, and 15-16 mm in length to a probe (O) and sticklebacks attacking Neomysis (lI). (b) The responses of Gammarus 5-6 and 7-14 mm in length to a probe (O) and sticklebacks attacking Gammarus( I ) allowing for the 0.02 s lag in the prey's response to fish attack.

both fed Neomysis and Gammarus of mean_sE length 13.5+ 1.3 and 8-1+0.8 mm, respectively. Prey of these sizes were used because they are approximately equal in energy value, so allowing the effect of prey morphology to be studied independently of energy yield (A. P. Westhead, unpublished data). The time from the moment that the prey was seized in the mouth to the moment of swallowing was recorded using a stopwatch.

RESULTS

Escape Responses of Prey Neomysis The flip response of mysids was highly consistent. During the initial 0.02 s of the escape response,

0-02 s after the fish began their attack, the body flexed at the third abdominal segment, producing maximum displacement (Fig. 2c). By the end of the first 0"02 s the body was folded in half and had a streamlined shape, the head trailing furthest behind, i.e. closest to the fish's mouth (Fig. 2c). During the following 0.06 s the body maintained its streamlined shape until the mysid came to rest, continually decelerating (Figs 2c, 3a). The cumulative distance moved during the flip response increased with body size, and the differences between the 10-12, 13-14 and 15-16ram size classes were all significant (Fig. 3, ANOVA: F 2 = 63-49, P<0-0001). The tail-flip response moved the mysid away from the fish's mouth, most frequently at an angle of approximately 90 ~ to the angle of attack (Fig. 4, chi-squared test: Z~ = 12.04, P<0.05).

Kaiser et al.: Stickleback predatory behaviour

151

Table I. The mean_+sE and maximum velocities (m/s) attained during Neomysis and Gammarus escape responses when attacked by a probe

60

50

Velocity Length of prey (mm)

40

3o

20

I0

I

0o

90 ~ Escape angle

Figure 4. Numbers ofmysids escaping at 90~ and 0 ~ to the line of attack by a stickleback (N = 72).

Gammarus Occasionally Gammarus used a flip response similar to that of Neomysis (9-6% of the trials, N = 390). Propulsion was initiated by a C-shaped flexing, unlike the complete folding observed in Neomysis. The resultant displacement was much less than that observed in Neomysis. As in Neomysis, the cumulative distance m o v e d during the flip response increased with body size (Fig. 3). The most c o m m o n escape response used by all sizes of Gammarus was simple swimming. The resultant velocities were slower than those produced during the flip response (Table I), and decreased with amphipod size, which suggests that drag factors and body mass have a significant effect on swimming speed (Table I). When Gammaruswere persistently attacked they adopted a stationary C-shaped posture, increasing their height:length ratio.

Fish Attack The following data refer to sticklebacks of mean length 94.5 ram, range 87.5-105.0 ram. After approaching the prey, the fish hovered a fixed distance from it (Fig. 2a, Table II). This behaviour probably allows the fish to fixate a particular point on the body and adopt the S-bend

X_+ SE

Maximum

Neomysis fast-start (flip response) 10 0.568 _+0.025 I1 0.606+0.037 12 0.606+0.030 13 0.788 +0.041 14 0-802 __+0.040 15 0.988 + 0.054 16 1.006 __+0.052

1.230 1.120 1.150 1.480 1.580 1.580 1.660

Gammarus fast-start (flip response) 5/6 0.155_+ 0.020 7/8 0.303 __+0.030 9/10 0.317__+0.028 11/12 0'334_+ 0.020 13/14 0.340 __0.020

0.275 0.557 0.543 0'645 0.629

Gammarus linear swimming 5/6 O'116 __+0.006 7/8 0'116__+0.008 9/10 0.105__+0.005 11/12 0'081 __+0'006 13/14 0.080__ 0"003

posture required to propel the fish towards the prey (Fig. 2a-c). The distance from the m o u t h to the prey did not depend on prey size ( A N O V A : F 1 = 3 ' 3 4 , P>0"05). Fish hovered at a greater distance from Neomysis than from Gammarus ( A N O V A : F 1 = 35.26, P<0.0001, Table II). During the first 0-02s when a stickleback attacked Neomysis, the chord was less, and the trailing-edge amplitude was greater than when attacking Gammarus (ANOVA: F1 = 342'23, P < 0"0001, Table II, Fig. 2b). After 0-04 s the chord and trailing-edge amplitude observed in attacks on both prey types were not significantly different ( A N O V A : F 1 = 2.83, P > 0.05, Table II, Fig. 2c). When attacking both Neomysis and Gammarus, the fish reached peak velocity after 0-04 s, thereafter decelerating until the fish came to rest (Fig. 2c~1). The velocity achieved during an attack on Neomysis (X+_SE= 0'720 ___0"030 m/s, maximum of 0.991m/s) was greater than that of an attack on Gammarus (0.128_+0'020m/s, maximum of 0-218 m/s; A N O V A : F 1 = 7.88, P < 0.007). The mean velocity achieved by sticklebacks during attacks on Gammarus was less than the

Animal Behaviour, 43, 1

152

Table II. The distance from the stickleback's mouth, and the orbit of the eye, to the head of the prey (hover distance), and kinematic measurements of body curvature (chord) and trailing-edge amplitude for the preparatory and propulsive strokes

Distance offish mouth to prey (mm)

Prey

Mean -+SE

N

P

Neomysis Gammarus

6.23 + 0' 37 3.51 • 0.28

19

< 0.0001

32.10-+0.90 ~

19

Neomysis Gammarus

30.08-+0.19 36.03 -+0.29

19

<0.0001

Neomysis Gammarus

19.45_+0.39 6.66 _ 0-29

19

<0.0001

Neomysis Gammarus

35.92-+0.28 35.68+0.38

19

NS

Neomysis Gammarus

3"08+0.09

19

<0.0001

Angle of attack on Neomysis Kinematic measurements (nun) Preparatory stroke Body curvature (chord, mm)

Trailing-edge amplitude (mm) Propulsive stroke Body curvature (chord, mm) Trailing-edge amplitude (ram)

Table IIl. The ingestion times (s) of Neomysis (X+SE length= 13.5+ 1.3 ram) and Gamrnarus (8'1 -+0"8 mm) eaten by small (85.7 + 2.5 mm) and large (102-5 +_2.5 ram) sticklebacks

3"13+_O"11

The total work done, W, in accelerating the fish forwards is given by

W=KI Small fish (~ + SE)

Large fish (~?_+SE)

t-Test P

0'98-I-0-28 2-21_+0.32 0.023

0"008 0.0002

[U2 +(2ax)~

+O.6M(U2-U~)(1)

"JO

where K 1 is a constant equal to

K~ =0.50Sw[O.35(L/v) -~ Neomysis 2-61 + 0.35 Gammarus 415.00_+66.77 t-Test P

0.0002

(2)

Kinetic viscosity (v) is given by v = 0-0122 (salinity = 34%o, temperature = 15~ density, p = 1.023 kg/m 3)

mean velocity achieved by the smallest Gammarus during a flip response, but was greater than any Gammarus velocity achieved during linear swimming (Table I). Although Gammarus quite clearly demonstrated the ability to perform a flip response, it was never observed in any trial involving a fish attack.

Wetted surface area (Sw) is given by S w= 0"4L 2 where L = length offish (0.0945 m) i.e. mean length offish in this study) Sw=0.003572 m E

Work Done During Fast-start

L = l e n g t h of fish (m); Uo=initial velocity (m/s); U = f i n a l velocity (m/s); a = acceleration (m/s2); x = distance moved (m); and M = mass of fish (g).

During the fast-start, energy is expended to overcome drag and to propel the fish forwards (Webb 1975). Knowing the maximum velocities achieved during attacks on Neomysis and Gammarus, an estimate of the work done during a fish strike can be made.

The equations are taken from Webb (1975). Substituting into equation (2), K 1 = 2.29 x 1 0 - 6 and is a constant during attacks on Neomysis and Gammarus. Hence when attacking Neomysis, a fish 0'945 m total length, expends 6.92 • l0 -7 J overcoming drag, and 1.51 • 1 0 - 3 J propelling itself

Kaiser et al.: Stickleback predatory behaviour

I

5

5

7

9

It

15

15

5

5

7 . 9

II

15

15

50

0

20

I0

o

6l-8O

81-1oo IO1-12o Length (mm)

121-14o

Figure 5. The percentage occurrence of (a) Neomysis in Loch Etive in January and February (taken from Mauchline 1971) and (b) Neomysis in the stomachs of sticklebacks of total length 87-5-105 mm from January to February. (c) Lengt~frequency distribution of sticklebacks in the sampled population in January and February (Kaiser & Croy 1991). forwards. However, a fish attacking an amphipod expends 2.42 x 10 9 j overcoming drag, and 7.64 x 10- 5 j propelling itself towards the prey.

Ingestion Time Large and small sticklebacks took 2.25 times and 159 times longer to ingest Gammarus than Neomysis, respectively (Table III). DISCUSSION

Predator-Prey Interactions In the first 0.02 s o f a strike at Neomysis, the fish travel the mean hover distance (Table II). During

153

the following 0.02 s they reach their peak velocity, as do Neomysis. The second 0.02 s of the strike is the critical stage when the mysid is actually captured. Neomysis most commonly moved at an angle of approximately 90 ~ to the line offish attack (Fig. 4). If the attack were to be in a straight line, mysids would evade the zone of interception as described by Hart & Hamrin (1990). Sticklebacks, however, tend to angle their attack approximately 32 ~ towards the anticipated direction of mysid escape (Table II), increasing capture rate. Kislalioglu & Gibson (1976) suggested that sticklebacks fixate the head region of Neomysis because of its prominence. During a Neomysis flip response, the head is posterior to the centre of mass and consequently closest to a predator's mouth. By fixating on the prey's head the predator thereby increases the probability of prey capture. The cumulative distance moved by the fish by the end of 0.04 s is similar to that moved by 14-mm Neomysis (Fig. 3). Analysis of the stomach contents of wild sticklebacks of similar length to those used in the present study revealed that the largest mysids eaten measured 14 mm (Fig. 5). Sticklebacks of this size (mean, 94-5 ram) are most frequent in January and February (Fig. 5; Kaiser & Croy 1991) when mysids up to 16 mm long are present in the population (Mauchline 1971). Although Neomysis availability is not limited by the mouth dimensions of the fish (Fig. 6), the fast-start capabilities of sticklebacks, in this study, exclude Neomysis of more than 14 mm from the diet. As sticklebacks increase in length, their fast-start capabilities improve (Webb 1978), possibly explaining why mysids increase in dietary importance as the fish become larger (Fig. 7). Concomitantly, amphipods decrease in importance, which may imply that mysids are a more profitable food source for larger fish. Kislalioglu & Gibson (1976) found that the optimal mysid length for a 90-mm stickleback was 10.5 mm. The present study has shown that Neomysis of this size are within the predatory capabilities of sticklebacks (Fig. 3, Table I). Although Gammarus was able to give a flip response, the velocity achieved was much less than that produced by Neomysis during a strike by a stickleback (Fig. 3), and this escape mode was rarely used (9.6% of trials, N=390). Gammarus most commonly escaped by simple linear swimming, which achieved a mean velocity 34% as fast as the flip response (Table I). The mean velocity attained by the fish striking at Gammarus was

154

Animal Behaviour, 43, 1

15

-g E ,o

O_

O

I

20

I

40

I

I

I

I

I

60 80 I00 120 140 Fish length (ram) Figure6. The maximumprey size available to sticklebacksof a givensizedetermined from the comparison of mouth and prey cross-sectionalarea (mm2). 9 Neomysis; [] : Gamrnarus. 50

4O so t9

o

20

o~ IO o

Gammarus

Neom.vsis

Figure7. The percentage occurrence of Gammarus and Neomysis in the diets of three sizeclasses of sticklebacks(N= 115 fish). I : 0-50 mm; []: 51 100mm; D: 101-150mm. 10% greater than the highest Gammarus swimming velocity. Although Gammarus are able to produce an escape response, we never saw them use it when they were attacked by sticklebacks, suggesting that Gammarus detect approaching fish inefficiently. This may also explain why sticklebacks hover closer to Gammarus than Neomysis (Table II). Gammarus used a third anti-predator response to probe attacks, which we saw during the predation trials. Persistent strikes by a predator induced Gammarus to adopt a motionless, curled-up, Cshape, increasing the height :length ratio above 1: 5, which caused the fish to lose interest in the prey. A motionless Gammarus will be well camouflaged against a coarse substratum. Visual predators, such as fish, find stationary prey less attractive than

moving prey (Kislalioglu & Gibson 1976; Holmes & Gibson 1986; Croy & Hughes 1991c). Although Gammarus were easier to catch than Neomysis, above a certain threshold size they took much longer to ingest (Table III), which may be explained by their higher height:length ratio than Neomysis, the adoption of the C-shape, and their prominent appendages. Evolution

of Prey

Behaviour

The escape responses of Neomysis and Gammarus have probably evolved as adaptations to predation pressures and to their respective habitats. Neomysis shoaling behaviour (Mauchline 1971) will minimize predation risk by reducing the encounter rate with

Ka&er et al.: Stickleback predatory behaviour predators (Bertram 1978), and possibly lead to the predator being confused (Milinski 1979). The transparent body of Neomysis will act as effective camouflage in mid-water, although once encountered, a shoal of Neomysis remains vulnerable to attack, as it does not use natural cover to avoid predators, hence necessitating a rapid escape response. Gammarus tend to be cryptic, hiding among stones and seaweed, where body colour is most effective as camouflage. A flip response, as used by Neomysis, may be inappropriate in a cryptic habitat, because of spatial constraints.

Fast-start of Other Species The velocity measured for fifteen-spined sticklebacks is comparable to that of other species (Webb 1978). Taylor & McPhail (1986) found that freshwater and anadromous three-spined sticklebacks, Gasterosteus aculeatus, attained maximum velocities of 0.90m/s and 0.66m/s respectively, compared to 0.99 m/s measured for fifteen-spined sticklebacks in this study. Three-spined sticklebacks appear to have a similar fast-start velocity to fifteen-spined sticklebacks, which may reflect their comparable habitats and predatory behaviour. However, Taylor & McPhail (1986) used electrical stimuli to induce fast-start in three-spined sticklebacks, whereas the present study has examined natural predatory sequences, which may affect the reliability of this comparison. The Role of Prey Recognition Nyberg (1971) showed that the largemouth bass, Micropterus salmoides, varies its attack velocity according to the type and mobility of prey to be captured. Sticklebacks also modify their attack strategy according to prey type, suggesting the ability to recognize and distinguish prey. Kislalioglu & Gibson (1976) found that sticklebacks responded differently to various parts of mysid bodies, and work with model prey indicates that these fish can distinguish mysid and amphipod shapes (M. J. Kaiser, unpublished data), thereby facilitating learning and increasing handling efficiency (Kislalioglu & Gibson 1976; Croy & Hughes 1990). Sticklebacks convincingly demonstrate the importance of prey recognition, leading to fine tuning of attack methods. Maximizing Net Rate of Energy Intake Sticklebacks can recognise specific prey types and adjust their method of strike accordingly. The

155

maximum velocity achieved during an attack on Neomysis was 4.5 times greater than an attack on Gammarus. Consequently, when attacking Neomysis, the energy expended propelling the fish forwards and overcoming drag was 20 and 286 times greater, respectively, than when attacking Gammarus. The energy expended overcoming drag in both cases in 104 less than that expended in acceleration, and can be ignored, as suggested by Webb (1975). Sticklebacks often have to make more than one attempt to catch Neomysis (personal observations), further increasing energy expenditure and decreasing profitability per unit mass ingested. Although the sticklebacks expended 20 times as much energy catching Neomysis, the greater ingestion time and consequent reduction in net rate of energy intake make Gammarus the less profitable prey.

ACKNOWLEDGMENTS Dr Rob Batty made helpful comments on an earlier version of this manuscript. Andrew Westhead kindly supplied energetic data for Neomysis and Gammarus. This work was conducted while M.J.K. was in receipt of a NERC/CASE studentship.

REFERENCES Batty, R. S. 1983. Observation of fish larvae in the dark with television and infra-red illumination. Mar. Biol., 76, 105 107. Bertram, B. C. 1978. Living in groups: predators and prey. In: Behavioural Ecology: an Evolutionary Approach (Ed. by J. R. Krebs & N. B. Davies), pp. 64-96. Oxford: Blackwell. Beukema, J. 1986. Predation of the three-spined stickleback (Gasterosteus aculeatus): the influence of hunger and experience. Behaviour, 31, 1-126. Croy, M. I. 1989. Characteristics of learning associated with feeding in marine predators. Ph.D. thesis, University of Wales, Bangor. Croy, M. I. & Hughes, R. N. 1990. The combined effects of learning and hunger in the feeding behaviour of the fifteen-spined stickleback Spinachia spinachia L. In: Behavioural Mechanisms of Food Selection (Ed. by R. N. Hughes), pp. 214 234. Berlin: Springer-Verlag. Croy, M. I. & Hughes, R. N. 1991a. The role of learning and memory in the feeding behaviour of the fifteenspined stickleback, Spinachia spinachia L. Anim. Behav., 41, 149-160. Croy, M. I. & Hughes, R. N. 1991b. The influence of hunger on feeding behaviour and on the acquisition of learning foraging skills in the fifteen-spined stickleback, Spinachia spinachia. Anirn. Behav., 41, 161 170. Croy, M. I. & Hughes, R. N. 1991c. Hierarchical response to prey stimuli and associated effects of hunger and

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