Anim. Behav., 1988, 36, 986 990

Size-specific protection against predation by fish in swarming waterfleas, Bosmina longispina

PER JOHAN JAKOBSEN & G E I R H E L G E JO H N S EN Department of Animal Ecology, Museum of Zoology, University of Bergen, 5000 Bergen, Norway

Abstract. When feeding on non-swarming waterflea prey, sticklebacks, Gasterosteus aculeatus, selected larger items. However, when feeding on swarming prey, the fish fed mainly at the edges of the swarms and smaller items were consumed. This selection of small prey items can be explained by the fact that when attacked by a stickleback the waterfleas escaped towards the centre of the swarm, larger individuals more quickly than smaller ones, thus leaving the stickleback with smaller than average prey at the edge of the swarm.

Several studies have shown clumping of prey to be important as an antipredator mechanism (e.g. Milinski 1979). However, the possibility that swarm members may be differentially protected depending on their position within the swarm is often overlooked. Milinski (1977b) found Daphnia magna at low densities at edges of simulated swarms to be more susceptible to predation than those at higher densities, and Jennings & Evans (1980) found individuals at the periphery of bird flocks to be more vigilant than those in the flock's centre. Hamilton's (1971) geometrical model showed that each individual could reduce the size of its own domain of danger by positioning itself nearer to another animal and thus reducing the likelihood of being the prey individual nearest to the predator. This may result in a compact group from which it is more difficult for the predator to obtain a particular victim. The evasion tactics of such groups to an approaching predator are dis- cussed by Pitcher (1986).

It pays small and large fish in shoals to make different decisions about joining, leaving or remaining with their shoal fellows. Thus the shoal- ing responses of individual fish depend on their own size. The different size classes do better when completely separated, but shoaling fish hedge their bets by remaining in the same area to allow close schooling when required (Pitcher et al. 1986).

However, information about whether differently sized prey within groups differ in their ability to escape from a predator is still needed. Our aim in this study was therefore to evaluate the conse- quences of swarming on a predator's choice of differently sized prey, and to investigate whether behavioural differences of individual prey influence

the predator's prey choice. This was done by comparing the diet of three-spined sticklebacks, Gasterosteus aculeatus, feeding freely on swarming and non-swarming waterfleas, Bosmina longispina. The behaviour of differently sized B. longispina during disturbance was recorded in order to evalu- ate possible differences in escape rate within the swarms. Bosmina longispina typically forms dense compact swarms (Huitfeldt-Kaas 1906). In addi- tion, it is frequently preyed upon by sticklebacks in nature. Jakobsen & Johnsen (1987) found that during the day in summer, swarms of B. longispina were under attack from sticklebacks 57% of the time.

T H E E F F E C T OF S W A R M I N G

Methods

The sticklebacks were starved for 24 h before any of the experiments were run. Littoral B. longispina were collected in Lake Kvernavatn, western Nor- way, with a plankton net and were transferred to a tank measuring 1-1 x 1-1 m 2 and 0-3 m deep. The tank was filled with lake water, which had been filtered through a net with a mesh size of 90 pm. Illumination was provided by two 40-W fluores- cent light tubes placed 1.7 m above the tank surface.

When illuminated, B. longispina formed tightly packed balls in the tank. Seen from above, these swarms were recognized as dark spots, and we were not able to see the bottom of the tank through them. Swarm size varied from 10 to 25 cm in diameter. Kept under identical conditions, densit- ies varied between 16 and 39 400 individuals per

986

Jakobsen & Johnsen: Different protection in swarms

litre ()?_+ SD = 8684 + 17 489; Jakobsen & Johnsen 1988).

To investigate how swarming of the prey influenced their choice of feeding place and prey sizes, four sticklebacks were allowed to feed on swarms of B. longispina in the tanks. These swarms were very distinct, so that it was easy to recognize where the sticklebacks were feeding. Each of the 20 trials lasted for 15 min, and different fish were used in each trial. Behaviour of the fish was classified as either feeding or swimming only in one of three possible places: between swarms, edge of swarms or inside swarms. Between swarms was defined as areas with no shadowing from the B. longispina to the bottom of the tank. The swarm edge was defined as areas where the bottom of the tank was diffusely overshadowed by B. longispina. These areas were between 1 and 4 cm in width and were always found in connection with a swarm. Inside swarms was defined as areas where the bottom was completely overshadowed by B. longispina. Changes in behaviour were continuously recorded, and in this way a time budget for the feeding behaviour of the sticklebacks was constructed.

The size distribution of B. longispina in the diet was measured by examining the stomach contents of 10 fish from 10 different trials. This was done by opening the stomachs and washing out the con- tents. The size distribution of B. longispina avail- able to the foraging sticklebacks was measured from a transect of six samples within the tank, taken independently of swarm localization. Numbers of B. longispina in the samples ranged from 76 to 29 800 individuals per litre (,~'+SD= 6038_ 11 751).

A test of the preferred size selection by stickle- backs when feeding on non-swarming B. longispina was performed using a 10-1itre glass bottle contain- ing lake water and 2500 B. longispina per litre. The bottle had a diameter of 30 cm, was illuminated by a 40-W light bulb 1.7 m above the bottle, and reflective aluminium foil under the bottle kept light conditions inside even. The even light conditions and the small bottle size inhibited swarming. Variation in B. longispina density was not detect- able under these conditions. Single sticklebacks were carefully transferred to the bottle, and allowed to feed for 5 rain. The time was started when the first item was consumed. Both stomach contents of 10 sticklebacks and the food available to them were examined to determine length distri- bution of B. longispina.

987

Table I. Time budget (.~-+ SD) for sticklebacks feeding on dense swarms of B. longispina (60 sticklebacks, 15 trials and 225 min)

Feeding Swimming only

Between swarms 46.2+29% 37.3_+29% Edge of swarms 14.3+ 12% 2.1 -+3% Inside swarms 0.1 -+0.3% - -

When sticklebacks were feeding on both swarm- ing and non-swarming prey, prey density was very high. Hence, we assume that there was no competi- tion for the same prey target. The fact that four fish were feeding together on swarming prey while single fish fed on non-swarming prey should there- fore not influence the prey size selection.

Results

All the sticklebacks preferred to feed between swarms of B. longispina, but they also fed on the edges of the swarms 14% of the time. Single sticklebacks were found within the dense swarms only 0-1% of the time (Table 1). The size distribu- tions of B. longispina (Fig. l) indicate that fish predation was concentrated on average and smaller than average individuals in swarms (X2= 140.6, dr= 9, P < 0-001). Individual fish did not show any difference with respect to the size distribution of their prey (P>0-05, Student t-test.) When the sticklebacks were allowed to feed on non-swarming B. longispina, they selected the larger ones (Fig. 2, Z2=66-8, dr= 10, P<0.001).

S W I M M I N G S P E E D OF T H E P R E Y

Methods

Swimming speeds of both disturbed and undis- turbed B. longispina were recorded as a function of body length to investigate whether there was a size- related difference and whether frightening influenced their swimming speed. Swarms were frightened by a dead stickleback mounted on a rod moved slowly towards the swarm, and the swim- ming speed and size of individuals within the swarm recorded. We also recorded the size-specific swimming speed of undisturbed B. longispina within a swarm.

The experimental arena consisted of a Plexiglas

988 Animal Behaviour, 36, 4

40 t 30

a

40

30

a

LLI 0 Z LLI r r

2 0

10

0 0.4 0.5 0.6 0.7 0.8

O O O 4 0

30"

20"

10.

0

b

0.4 0.5 0.6 0.7 0.8 L E N G T H (mm)

Figure 1. Length distribution of Bosmina longispina in (a) the tank (six samples, N=382 individuals), and (b) stomachs of sticklebacks (10 sticklebacks, N=364 indi- viduals) when the prey were swarming. Mean values for the distributions are indicated by the closed circles.

IJJ 0 Z 1.11 n- 0::

20 __L 10- - I

I I i = - 0

1

0.4 0.5 0.6 0.7 0.8

40

o~ 30

20-

b

10-

0 0.4 0.5 0.6 0.7 0.8 LENGTH (ram)

Figure 2. Length distribution of Bosmina longispina from (a) the experimental bottle (three samples, N= 120 indi- viduals), and (b) stomachs of sticklebacks (10 stickle- backs, N=266 individuals) when the prey were not swarming. Mean values for the distributions are indicated by the closed circles.

box measuring 50 x 25 x 1-5 cm 3, with millimetre paper mounted on the back wall. Il lumination came from a light tube placed behind the top of the box. The swimming patterns of B. longispina were therefore not influenced by different light condi- tions. The cladocera preferred to swarm just beneath the light tube. They were allowed to stay at this site for 10 min before each trial was run. A video camera was used to record their swimming behaviour. Only the B. longispina that were in focus by the camera were used for measuring and estimation of swimming speed. These organisms swam perpendicular to the camera, and length of the specimens and their swimming speeds were measurable in two dimensions. To ensure that the individuals to be measured were selected randomly,

never more than two measurements were taken from each of 20 replicates. Densities of B. longis- pina varied between 7 and 24 individuals per cm 3 in the investigated parts of the swarms which is comparable to natural swarm densities (Jakobsen & Johnsen 1988).

Results

Larger B. longispina always swam faster than smaller ones, both when disturbed and when undisturbed (Fig. 3). However, when attacked by a stickleback, the swimming speed was doubled and the difference between large and small individuals was further increased. Reaction distance of B.

Jakobsen & Johnsen." Different protection in swarms 989

, ~ 1.5"

E 0

1

u.I I l l

0.5

O9

1

0

O5 1 LENGTH (mm)

Figure 3. Size-related swimming speed of Bosmina longis- pina when disturbed (a) and when undisturbed (b). Lines represent equations (1) and (2).

longispina to the stickleback was never more than 5 cm. Thus, no escape of the swarm as a whole was observed. The relation between the body size (mm) of undisturbed and disturbed B. longispina and their swimming speed (cm/s) is represented by equations (1) and (2) respectively.

Speed = 0.677 x length + 0.29 (r=0.58, N=31) (1)

Speed = 1 . 0 9 5 x l e n g t h + 0.50 (r =0"74, N=31) (2)

D I S C U S S I O N

When feeding, sticklebacks fed most of the time between the swarms. We did not control for feeding efficiency in different feeding sites. Selection for smaller than average prey could therefore have occurred between swarms. However, there was no correlation between number of B. longispina and their mean size in the six samples from the tank. Thus, size of B. longispina was equal at all feeding sites before the sticklebacks were introduced. Furthermore, the sticklebacks showed a clear abi- lity to select the largest B. longispina when these were evenly distributed. In addition, if densities were too low to make them prefer the larger ones, they should show no preference for any size, as found for bluegill sunfish, Lepomis macrochirus (Werner & Hall 1974). Hence, prey smaller than

medium size must be eaten at the edges of the swarm rather than between swarms.

The fact that four sticklebacks fed together on the swarms, while they fed singly on the non- swarming prey, could also have influenced prey selection. Milinski (1984) showed differences between individual fish dependent on their com- petitive ability. However, in this experiment, we found no difference between individual fish, prob- ably because of the high densities of prey. Thus, there was no competition for the same targets.

If frequently attacked by a predator, swarming individuals are safer in dense parts of the swarm (Welty 1934; Radakov 1958; Neill & Cullen 1974; Milinski 1977a). When frightened by a predator, the swarm members swam faster and away from the frightening stimulus. This behaviour is also observed for swarming copepods, escaping in a synchronized movement away from the predator (Hamner & Carleton 1979). A difference, however, was that only the part of the B. longispina swarm nearest to the stickleback swam vigorously. The rest of the swarm remained undisturbed. This seeking of shelter towards the centre of the group is an example of Hamilton's (1971) selfish herd effect.

Larger individuals swam faster than smaller ones, making them better able to escape a frighten- ing stimulus. Sticklebacks prefer to attack the edge of the swarms (Milinski 1977a; this study) and should therefore experience a predominance of smaller swarm members at the point where they are feeding. This is supported by the gut analyses reported here, but the sticklebacks still had the ability to select larger items among the available prey at the edge of the swarm.

Radakov (1973) found that individuals in fish schools remained in the same position within the school when frightened. In our experiments, how- ever, large individuals escaped more quickly, leav- ing the smaller ones at the edge near to the predator. Larger individuals thus benefited more than the small ones by staying in the swarm, since they are not so endangered by being at the edge of the swarm. Hence, smaller individuals benefit most by staying in large swarms, where the edge of the swarm is small in relation to the volume of the swarm. Milinski (1977b) showed that peripheral individuals are more endangered than central ones in a swarm, but not as much as stragglers. This could explain the sharp boundaries of such swarms. Occasional visits to the outer parts of the swarm, however, might increase the amount of food eaten

990 Animal Behaviour, 36, 4

by each individual, since food deplet ion within dense swarms can be high. This is indicated by a negative corre la t ion between n u m b e r of B. longis- pina and algal conten t in the same water sample when measured in the field ( Jakobsen & Johnsen 1988).

A C K N O W L E D G M E N T S

We t h a n k Eva and Atle K a m b e s t a d for their assistance in recording the behav iour of the feeding sticklebacks, Randi Lund for count ing and mea- suring the zoop l ank t on samples and Ka thy Smayda for correct ing the English. Manf red Milinski has made valuable comments on the manuscript . The work is suppor ted by BP-Norway and the Universi ty of Bergen.

R E F E R E N C E S

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(Received 1 December 1986; revised 8 September 1987; MS. number: 2934)