The development and ecological significance of feeding techniques in the reed warbler (Acrocephalus scirpaceus)

Anita. Behav.,1976,24, 213-229

THE DEVELOPMENT AND ECOLOGICAL SIGNIFICANCE OF FEEDING TECHNIQUES IN THE REED WARBLER (A CROCEPHAL US SCIRPd CEUS) BY N. B. DAVIES & R. E. GREEN*

Edward Grey Institute, Department of Zoology, Oxford and 24, Park Parade, Cambridge Abstract. Wild reed warblers use several techniques to capture their insect prey (mainly Diptera). Different techniques are used for different prey and so vary with prey activity. Independent young birds pick stationary prey from foliage more frequently than adults, which often catch prey in mid-air. This is not because the young need time to develop feeding skills, Captive birds which did not have experience of flies until fully grown were no worse at capturing them than birds which had had continuous experience from an early age. Adults probably use more energy-demanding techniques in'order to collect enough food for their young as well as themselves. However, rapid learning of prey handling ability is restricted to a sensitive period early in development, before structural maturation of the bill is completed. the initial field observations of the different feeding techniques and then the development of these techniques in young captive birds with different experience of prey, Finally an attempt is made to relate the variety of feeding techniques to the behaviour of the prey.

A predator may use a variety of techniques to capture its prey. Recent interest in the feeding behaviour of birds has mainly been concerned with differences between species in relation to competition (Lack 1971; Cody 1974). There have been few attempts to relate feeding techniques within a species to the behaviour and ecology of the prey, as Kruuk (1972) has done for a predatory mammal. Many feeding techniques appear to involve considerable skill and several studies of wild birds have shown that the young are less successful at capturing prey than adults (terns, Dunn 1972; Buckley & Buckley 1974; herons, Recher & Recher 1969; Siegfried 1972; pelicans, Orians 1969). This is apparently because it takes the young some time to develop these hunting skills. For example young oystercatchers (Haematopus ostralegus) take 3 years to become as efficierft as adults at eating edible mussels (Norton-Griffiths 1968). The lower efficiency of feeding of young birds may partly explain their higher mortality and deferred reproduction (Lack 1968). The reed warbler (Acrocephalus scirpaceus) is an insectivorous passerine which is a summer visitor to Europe. Field observations begun in 1972 at Wicken Fen andUpware, Cambridgeshire, England, showed that they used several feeding techniques to capture prey and that there were marked differences in the feeding techniques of young and adults. In 1974 the reasons for these differences were studied in the laboratory using hand-reared individuals. More detailed observations were also made of the circumstances in which the different feeding techniques were used. This paper firstly describes *Present address: Broom's Barn Experimental Station, Higham, BurySt. Edmunds,Suffolk.

The Feeding Techniques of Wild Reed Warblers Methods Reed warblers forage mainly in bushes but also in reeds and other herbage (Green & Davies 1972; Catchpole 1973). They are most easily watched in bushes, and most of our observations refer to this habitat. Feeding birds were watched through binoculars and aged by plumage, the adults having old feathers worn at the edges by activity during the breeding season and the young just out of the nest having clean new ones. Three classes were distinguished, adults (usually feeding young), juveniles receiving food from their parents, and juveniles independent of their parents. Observations were made throughout the day during July to September 1972 and July to August 1973. Although individual birds could not be distinguished observations were made over a large area of fenland, and the results probably refer to at least fifty individuals in each age class. Movements made by the birds as they hopped between perches or along a perch were categorized by comparison with their body length into those less than 15 cm, 15 to 60 cm, and greater than 60 cm. The time for which an individual was in view was measured with a stopwatch. Food samples were collected throughout the day from five broods of nestlings, 5 to 8 days old, in June 1974. The nests were in reeds and the 213

ANIMAL BEHAVIOUR,

214

parents were foraging in willow (Salix) and hawthorn (Crataegus) scrub. The nestlings were fitted with circular neck collars made from sections of pipe cleaner for periods of 30 min at a time which prevented food, given to them by the parents, being swallowed. There are objections to this technique, the main one being that nestlings may be able to swallow small food items but not large ones, thus biasing the sample (Orians 1966) In this study only large balls of food, containing both large and small insects, were found in the throats of the nestlings. The unswallowed food was collected and preserved in 50 per cent ethanol. Nineteen such collections were made and the samples identified under a binocular microscope. Results Food. Dipteran imagines formed a large part

of the prey (Table I). Observation of adults feeding themselves, and also of independent juveniles later in the season, showed that adult Diptera were the most important prey items. Feeding techniques. When looking for food in bushes and other open vegetation, reed warblers flit between perches, pausing regularly and often Table I. Food Brought by Parents to Nestling Reed Warblers

Prey

Per cent of total items

Mollusca

0.8

Araneae

5.8

Odonata, Agriidae

1.7

Hemiptera, Aphididae Psyllidae Delphacidae

1:7~ 10"9 6.7]

Coleoptera

5'0

Trichoptera

7.5

Lepidoptera larvae

3"3

Diptera, Tipulidae Chironomidae Culieidae Rhagionidae Dolichopodidae Empididae Trypetidae Chloropidae Scatophagidae Muscidae

3.3" 29"2 0.8 7-5 3.3 65.0 7-5 0.8 1.7 6.7 4.2 Total 120 items

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holding the head and body horizontal while making head movements at the rate of about one per second. In this way they appear to be scanning nearby vegetation for resting and flying insects. They catch prey in the following ways. (1) Stand picking: the bird picks up prey from a twig or leaf without moving from its perch. (2) Hover picking: the bird picks up prey from a twig or leaf while hovering. (3) Leap picking: the bird leaps towards prey resting on a nearby twig or leaf and either picks it up or catches it in mid-air just as it takes off. (4) Leap catching: the bird leaps towards flying prey, catches it in mid-air and then lands on another perch beyond. (5) Fly catching: the bird sallies out from a perch taking flying prey on the wing, often returning to the same perch. With this method the bird often makes several wing beats to reach the prey, whereas when leap catching the wings are only half raised and most of the power comes from the legs. Leap picking and hover picking were rarely seen, forming less than 0-5 per cent of the captures observed, and are included in Table II with stand picking. In the wild, foliage often conceals insects, and a bird rarely sees resting prey from far enough away to~warrant,a leap pick. There were marked differences between age groups in the proportions of the techniques used. With increasing age there was a progressive increase in the incidence of leap catching from 23 per cent in juveniles fed by parents to 68 per cent in the parents themselves. However, there was no increase in leap catching in independent juveniles over the period July to September. There was a corresponding decline in the proportion of picking attempts with age. Flycatching was relatively unimportant in all age groups. The table summarizes information from a large but unknown number of birds and therefore the statistical significance of the results is difficult to estimate. However, a similar difference exists in a smaller sample of birds individually recognizable because of plumage differences, mainly produced by different patterns of body moult. Twelve independent juveniles used a significantly smaller proportion of leap catching and fly catching attempts (median 50 per cent, range 26 to 80 per cent) than nine adults feeding young (median 71 per cent, range 59 to 91 per cent; MannWhitney U-test, two-tailed, P < 0.05). Juveniles

DAVIES & GREEN: REED WARBLER FEEDING TECHNIQUES

215

Table IL Feeding Teelmiques and Size of Movements when Feeding in Wild Reed Warblers of Different Ages

Size of movements (per cent frequency)

Feeding techniques (per cent freqnency)

Age class

Total capture attempts

Juveniles fed by parents

78

74

23

3

568

25

71

4

Juveniles independent of parents (July-August)

229

50

48

2

2160

8

79

13

Juveniles independent of parents (September)

734

47

52

1

.

1078

26

68

6

931

73

18

Adults feeding young

Stand Leap picking catching

fed by their parents also made the smallest proportion of large movements (greater than 60 cm), while independent juveniles made fewer than adults. Birds feeding largely by aerial methods often appeared to be deliberately disturbing foliage with their wings and bodies, perhaps to flush resting insects. Some species such as flycatchers (Hubbard & Hubbard 1970) and gnatcatchers (Root 1967) use wing flicking and tail flicking, rather than leaping about, to disturb prey and thereby make it more visible. Aggression when foraging. Reed warblers feed to a large extent outside their breeding territories (Lack 1946; Catchpole 1972). At Wicken Fen many birds fed in bushes around the edge of the reed bed and some would travel 150 m to collect food for the young. They did not defend any permanent feeding territories but vigorously defended the bushes in which they were feeding at the time against conspecifics and also against sedge warblers (Acrocephalus schoenabaenus) and other species. Foraging birds often met and the original bird would immediately chase away the newcomer, making snapping noises with the bill. Defence of a temporary territory in this way may be important for a species feeding on disturbable prey. When foraging, reed warblers often make large jumps between the branches of the bush, and by shaking the foliage and twigs in this manner they disturb insects which are then immediately captured by leap catching. A fly may be more easily captured soon after takeoff than when it has been in the air for some time (Davies, in preparation). The presence of other reed warblers in the same bush at the same time may be disadvantageous in that many prey items would be disturbed at once and therefore

Fly Total catching movements < 15 cm

.

. 9

15-16cm > 60 cm

.

become less available. The presence of other species would also have a similar effect if these were moving through the foliage, and aggression during foraging both to conspecifics and other species may be to minimize interference (see also Goss-Custard 1970). It is interesting that the sedge warbler, which feeds by quietly picking items in the foliage, is much less aggressive while foraging than the reed warbler (Green & Davies 1972) and this may be because it is not so dependent on disturbabte prey. When insect prey density is very low and search becomes the main limiting factor, some species may forage in flocks. Mixed species flocks form around leader species which flush insects as they move through the canopy and make them available to others in the flock (Brosset 1969). Fogden (1972) found that assemblages of insectivorous birds in Sarawak were at their maximum size during the lean season, and this increased their foraging efficiency. Therefore the aggression and solitary feeding shown by the reed warbler may only be adaptive for feeding on highly mobile prey at relatively high densities, where capture of the prey is more critical than searching for it. Discussion

The observations on wild birds present two main questions. Firstly, why is there a difference in the feeding techniques of young and old birds ? Secondly, why do reed warblers use such a variety of feeding techniques to capture their prey ? The increase in the proportion of aerial capture techniques with age could be due to maturation or learning of a skill, but the lack of any change in the proportion of these techniques used by independent juveniles over the period

216

ANIMAL

BEttAVIOUR,

July to September suggest that an ecological factor may be involved. These two questions will be examined in the next two sections.

Development of Feeding Techniques in Captive Reed Warblers Methods The factors responsible for the differences between juvenile and adult feeding techniques in the wild were studied using hand-reared birds. In July 1974 fourteen young reed warblers from five broods, 5 to 9 days old, were taken from their nests in Cambridgeshire. They were divided into two groups and kept in separate cages so that they were visually isolated from each other. One group of eight birds ('experienced') was given continuous experience of flies from their day of collection from the wild, and the other group of six ('naive') was not given any such experience until 30 to 40 days later when fully grown. Ideally, each brood should have been split so as to contribute individuals to both groups, but in practice this was not convenient because the broods were small and taken at different dates. However, each group contained individuals from three broods. The nestlings were placed in small, open cardboard boxes lined with cloth, inside a 90 cm3 wire cage. When the birds were small each group was kept in a single cage, but when they were larger, at 20 to 35 days of age, and more active, they were split so that each cage contained two or three individuals only. The cages were covered in fine terylene netting which prevented flies in the cages escaping from one group or entering to the other. The netting had the additional advantage of concealing the observer, so the birds could be watched without disturbing them. Each cage was provided with five perches spanning the cage at various heights. Each bird was weighed and measured daily at dawn and dusk during its early development. Weight changes were similar to those recorded in the wild (Dyrcz 1974) and all reached a final weight of 10.5 to 11 g. The birds were fed by forceps on small balls of minced meat rubbed in cod-liver oil and dipped into a homogenized powder consisting of three measures of Saval puppy food, one of Bemax wheat germ, one of chick meal, and one of Lowe's cat meat. This diet was supplemented with crushed flies. After each feeding, two drops of water containing Abidec multivitamin solution and Bifuran antibiotic were given by pipette. Nestlings were fed every 45 min from

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05.00 to 21.00 hr. All birds gaped when hungry and accepted two or three balls of food each meal. When they left the cloth nest, they were fed through the bars of the cage whenever they begged, each taking one meat ball every 20 rain. When all the birds were independent they fed from dishes of the dry powder and minced meat placed in their cages, and water was provided in drinking fountains. The birds were marked individually with colour rings or non-toxic dye on the underparts. Activity changed regularly in relation to feeding. When the birds were hungry they stood still on a perch and called persistently a loud 'chack'. After feeding there followed a period of about 10 min during which they would sleep and preen, huddled together on the same perch touching each other. Then would follow a period of activity during which the birds hopped about the cage and explored their surroundings. A similar sequence was noted by Barraud (1961) with young band-reared chaffinches (Fringilla coelebs). Observations were made of behaviour during these periods of activity for 1-min intervals. The following were noted; which bird, number of movements, number of pecks and, for the experienced group, the number and success of their attempts at capturing flies. For quantification of the feeding methods, the same categories were used as for the wild birds, namely stand pick, leap pick, leap catch, and fly catch. In addition, two more methods were distinguished: 'stand catch', in which the bird remains in the same position on a perch and catches flying prey, and 'hop pick,' in which the bird hops over to the prey and picks it up. This differs from leap picking, when the prey is picked up after one leap. Movements were divided into small hops along a perch and larger movements between perches.

Results General changes in behaviour with age. While still in the nest the birds spent most of the time sleeping. After each feeding session they immediately shuffled to the nest edge and defaecated over the rim. At 8 to 9 days they perched shakily on the nest rim for short periods, and preened, wing stretched and wing flapped. They left the nest at 10 to 11 days which is the same as in the wild (Brown & Davies 1949), when the wing feathers were only half grown and the tail feathers in quill (Fig. 1). The tarsi were full grown at 8 days, and on leaving the

DAVIES & GREEN: REED WARBLER FEEDING TECHNIQUES

217

7 0 84

"

9

SO

9

50

:-':"

t

Oo

{ Wing

o

o ~,Tail

0 O

9 .. 9 ~ el 9

40

o~

E

oo o

~o 3o

9l ~'

o9

~' 20 o o 10

o ~

;

lb

o

1;

io

A

a'o

~

20

4'5

Age, days

Fig. 1. Growth of wing and tail feathers of hand-reared reed warblers. Points from fourteen birds.

12

~

1c

~o~

e3 09

> 0

6 ~

30~E~

4

20"E E

O

~o

12

14

~6

18

20

22

2a

26

28

Age, days Fig. 2. Changes with age in movement rate, solid circles, and size, open circles, in captive young reed warblers. Means and sE for the fourteen birds in both experiencedand naive groups. nest the birds were adept at clinging to the walls of the cage. Their first reaction on leaving the nest was to climb up to the top of the cage and beg. They were nmch less stable on horizontal perches, tended to overbalance and sometimes fell off the perch when preening or being fed. Both rate and size of movements increased rapidly at first and then levelled off at 20 to 25 days (Fig. 2). At fledging the birds were capable only of short flights of less than 30 cm but by 20 days they could fly across the full length of the cage. At 2I days wing flicking and tail flicking occurred as they hopped about the cage, and the birds appeared to move much faster from perch to perch. Postural stability and ability to land

accurately on perches also improved during the first week. At first, if the birds were given food when they were not hungry they turned away, but at 11 to 12 days they pecked at offered food with a closed bill. From this age they began to peck at a wide variety of objects in the cage including each other, their perches, the cage wall and droppings. Exploratory pecking at first occurred when the birds were satiated, and when hungry they begged for food (Hinde 1959). Through exper~eoce they came to recognize certain items of food. Individuals ignored their own faeces after 1 day's handling experience but rapidly learned to pick up food which dropped from the dishes.

218

ANIMAL

BEHAVIOUR,

They began to actively take food from the forceps rather than passively beg. If food was placed in the bill tip it was usually dropped. Mandibulation improved with experience so that by 16 days the birds could swallow some meat balls placed in the bill tip, by either making small bill dabbling movements with the head tilted back, or by wiping the bill against the perch and pushing food further into the mouth. At 16 days they started picking up dropped food and other debris in the cage. A similar sequence of behaviour was noted by Newton (1972) in young cardueline finches. The change from dependent to independent feeding was gradual. The first food was taken from the food dishes at 16 to 18 days, soon after the start of exploratory pecking. By 21 days they were regularly taking food by themselves and often backed away and showed fear of the forceps and offered food. They would, however, beg and snatch food from each other. Sometimes they approached the food in the dish, briefly begged towards it with quivering wings, and then suddenly picked some up and swallowed it. This begging preliminary eventually disappeared at 25 to 30 days and the last food from the forceps was accepted at this age. Barraud (1961) noted similar conflict behaviour during the change to independent feeding in young hand reared chaffinches and great tits

(earus major).

Changes with age in reaction to flies in the experienced group. Blowflies (Calliphora erythrocephala) were introduced into the cage of the experienced group and numbers maintained at

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20 to 30 by replacing those that died. Sugar solution was provided and the flies remained active. By making head movements or sometimes movements of the whole body, the birds visually tracked flies as they flew around the cage and walked along the perches and up the walls. Even when still in the nest at 8 days of age, the nestlings would stretch up and follow the movements of flies buzzing over their heads. Soon after fledging, at 10 to 11 days, the birds spent most of the time sitting still on a perch watching the flies and gaping at them if they passed nearby, as they did to all moving objects. At 12 days they began to chase the flies, hopping over to where one had landed or was walking on the ground. The flies always flew off well before the bird arrived. They also attempted to stand catch flies which flew past them, but again they missed by a long margin. All the first capture attempts were made at moving flies and stationary and dead flies were ignored even if they were right under the bird's feet. As the birds became more agile and quicker at hopping over to the flies they managed to hit some with their bills before they escaped. At 16 days some were picked up by the legs or wings and held for 1 to 2 s before they escaped or were dropped. The first flies were swallowed at 19 to 24 days and this is the age at which the bill attains full length (Impekoven 1962). There was then a sharp increase in the attempt rate and an equally marked decrease in the rate of pecking at non-edible objects, such as the cage wall and perches. Such a change did not occur in

6.0

"7 .=

Naive group 5'0

Inedible objects

E .E 4'0 o

o. 3.0 O

Experienced group 2.0

Flies

1.0 ~'----,0"~15

17

i

,

,

19

21

23

~"'~. 25

Inedible objects 27

29

Age, days

Fig. 3. Changes with age in rate of pecking at inedible objects in captive young reed warblers. Comparison between experienced group and naive group. Means and SEfor eight experienced and six naive birds.

DAVIES & GREEN: REED WARBLER F E E D I N G TECHNIQUES

219

100-

Stand catch Stand pick Hop pick

e~

~50Leap pick

!j!i

|

Leap catch Fly catch

1'1

3

15

19 21 23 Age, days Fig. 4. Changes with age in feeding techniques of eight captive young reed warblers. Experienced group with Calliphoraas prey. Shaded areas represent per cent frequency use of the different feeding techniques.

the naive group (Fig. 3) which carried on pecking at various items in the cage. Immediately after swallowing their first flies, the experienced birds began to pick up stationary, resting flies. At this stage the proportion of attempts made by stand catching had decreased, as various other techniques such as hop picking, leap picking and fly catching were used. Leap catching was the last method to appear at 20 days, presumably because it required the greatest co-ordination of movement (Fig. 4). The success of capture attempts suddenly increased after the first fly was swallowed and reached 75 to 90 per cent within a day or two. This was because the birds changed their feeding techniques and greatly increased the proportion of attempts they made by picking as opposed to catching. The success of picking increased suddenly, though that of catching did not change and remained low (Fig. 5). Impekoven (1962) also hand-reared young reed warblers and noted that they showed interest in flies at 11 days old, swallowed their first flies at 18 days and were regularly catching flies at 22 days. Handling performance also suddenly changed after the first fly was swallowed. The handling time, defined as the time taken from capturing a fly to swallowing it, decreased markedly. At first the flies were held by the legs or wings and were frequently dropped. Often pieces of leg or wing were broken off during handling. The first

17

25

27

swallowing often took much longer than subsequently and the birds rapidly began to hold the flies by the body rather than by the appendages. Handling times decreased in some birds even on the first day, and after the second day there was no further improvement (Table HI). Comparison between the experienced group and naive group in their reaction to flies. Because the success with Calliphora was so high, and also because of an unexpected decrease in supply from cultures, a change was made to the house fly (Musea domestica) which is smaller and more active. The birds, all now fully grown and feeding for themselves, were provided with the dry mix food ad libitum and placed into six cages with two or three birds in each cage. The naive and experienced birds were kept in different cages and were visually isolated from each other. Testing occurred every 1 to 2 days at 12.00 hours. About fifty Musca were introduced into each cage in turn and the following were noted: which bird, method of capture attempt, success and handling time. The recording session lasted from 15 to 40 min for each cage. The experienced group were given four tests over 8 days before the naive group were first tested. The naive group were given their first experience of flies at 31 to 43 days of age. Both groups were then tested for a further seven tests given over a period of 8 days.

220

ANIMAL

BEHAVIOUR,

24,

1

.~ lOO

Picking techniques

80

~

20

_{,

Catching techniques

-- -- --9

-6 -3 0 Days before and after first swallowing of a fly', day 0

+3

+21

Fig. 5. Changes with age in capture success of Caltiphora by captive young reed warblers. Experienced group, mean and sE of eight birds.

(a) Capture success. (i) Musca. When presented with their first flies all the birds in the naYve group showed no hesitation and immediately began to capture and eat them. The first attempts of four of the six birds in this group were all by leap catching, one of the more difficult methods of capture, and all were successful. There was no significant daily change in method of capture, nor of capture success in either group, and the data are presented for all days combined in Table IV. No difference was found between the naive and experienced groups in methods of capture, although there was considerable individual variation within both groups. The difference in total capture success between the two groups was small and again the i~adividual variation was great. The total success of the naive group was greater than that of the experienced group, and for the individual feeding techniques considered separately the naive group were more successful at leap picking and leap catching but not for the other techniques. Table HI. Changes with Age in Handling Times of Calliphora. Captive Birds, Experienced Group

Handling time (s) Day 1 Mean • sE for seven birds Total handlings

Subsequentdays

19'84 ! 6.34

5"81 4- 0'75

28

57

Day 1 is the day on which a Calliphorawas first swallowed. Wilcoxon matched pairs test between the mean handling time on day 1 and that on subsequent days for the seven birds, P < 0.05.

The four birds with the highest success in the naive group were also the four oldest birds, being 6 days older than the oldest in the experienced group. Their greater success may therefore have been due to their greater age. This may explain why they were better than the others only in the two leaping techniques where motor co-ordination in capture may be most critical. However, three of these birds were from the same brood, and the small differences may be due to interbrood variability. (ii) Calliphora. After the test with Musca, three birds in each group were also tested wffh Calliphora. There was no difference in capture success between the experienced birds (86.0 zk 9-9 per cent, N----39) which had continuous experience of this species during early development, and the naive birds presented with this fly for the first time (84.5 :k '4'8 per cent, N = 133; Mann-Whitney U-test, two-tailed, P

0-05).

(b) Handling ability. In marked contrast to their proficiency at capturing flies, the naive group were worse than the experienced group at handling the prey once captured. They dropped Calliphora more often than the experienced birds, but not Musca, which is smaller and therefore more easily managed. Handling times for both Calliphora andMusca were much greater in the naive group (Table V). There was some slow improvement with experience in the naive group's handling of Musca (Fig. 6) but even after 6 days' experience they were still worse than t h e e x p e r i e n c e d group, w h o s e handling times remained constant throughout the test period. Three of the experienced group were given Calliphora 10 days after their early

DAVIES & G R E E N : REED W A R B L E R F E E D I N G TECHNIQUES

221

Table IV. Comparison Between the Naive and Experienced Groups of Captive Birds in Feeding Techniques and Capture Success with g u s c a . Both Groups were 30--45 days old Feeding technique Stand catch

Stand pick

Hop pick

Leap pick

Leap catch

Fly catch

7"1 • 0-9 5.5 :~ 1.6

0.6 • 0.3 0.6 ~ 0.6

23.8 • 2.7 19.9 • 3.6

45.8 ~: 1.9 50.5 :~ 7.1

3.8 _-t=1"6 3.9 • 0.9

Total attempts

PER CENT ATTEMPTS

Experienced group Naivegroup

18"9 =t= 1.9 19.7 • 5.0

1376 677 TOTAL PER

CENT SUCCESS

PEP. C E N T S U C C E S S

Experienced group Naivegroup

57"2 • 4.2 75"0 :~ 7.6 55"2 • 11"9 76.5 • 8.2

70'8 -I- t7.2 60.6 ~ 3'4 75"8 i 6.1 P < 0-05

39.7 • 3.2 52"2 • 3"0

40.8 i 7.6 24.3 • 5'2

P < 0"05

50.7 i 2"1 59.9 ~ 2"8 P < 0'05

Means and SE for eight experienced and six naive birds. Significant differences using the Mann-Whitney U-test, two-tailed, are shown.

Table V. Comparison Between the Naive and Experienced Groups of Captive Birds in Handling Ability of Calliphora and Musca Per cent captures dropped Number of handlings

Calliphora

Musca

Handling time (s)

Calliphora

Musea

Experienced group

848

52.1 • 1.1

9'4 ! 2"1

8"0 • 1"4

2.1 ~ 0.1

Naive group

400

75.6 • 7.0

11.9 ~ 5.1

37.9 dc 2.4

3.6 • 0.5

P < 0.05

P < 0.001

P < 0.05

Means and SE for eight experienced and six naWe birds. Significant differences using the Mann-Whitney U-test, twotailed are shown.

B-o 4.0

9~E-3.0

~

Navie group Expee rinced group

e-

9~r-- 2.o .-r 1.o

~ ~ ~ ~ a ~ ~ ~i'oi'I

Tesdtays

Fig. 6. Comparison between the experienced and naive groups of captive reed warblers in handling times of Musca. Naive group had their first experience of flies on test day 6. Means and SE for eight experienced and six naive birds.

222

ANIMAL

BEHAVIOUR,

continuous experience of this species, and then again 6 days later. Their handling times were greater than before (17-5 4-2.9 s, compare with Table V) but still less than those of the naive group tested on the same days. Discussion

(a) Capture success. The early stage of development at which young reed warblers fledge is probably an adaptation to reduce predation on whole broods in the nest (Catchpole 1972). At each stage the complexity of behaviour shown by the young birds is limited by their degree of maturation and growth. Both changes in postural control and opportunities for pecking probably contributed to the early improvement in capture success in the experienced group (Cruze 1935). Simple picking methods appeared first, and more complex techniques such as leap catching appeared when the birds were older. The techniques used were not related to their success until the birds swallowed their first flies, which did not occur until the bill was fully grown. The subSequent sudden increase in both rate and success of attempts suggest that the main factor limiting their capture performance was the recognition that the flies were food, rather than the ability to perform the movements involved in capturing them. While the exploratory pecking of the experienced group decreased suddenly when they began to swallow the flies, the naive group continued to peck at a wide variety of objects in the cage, at least up to 30 days, when observation of this behaviour was discontinued. They certainly recognized some items, such as dropped meat balls, as food but continued to peck at other inedible objects. It may be that unlike the experienced group, they were not presented with an easily recognizable specific stimulus like the flies, to which they could devote all their attention, the debris on the floor of the cage being rather homogenous in appearance and non-mobile. Similarly, in imprinting studies with young chicks, the most effective objects are those that are the most conspicuous to the human eye, moving stimuli being among the most effective (Bateson 1966). The results from the captive birds suggest that the large differences in feeding techniques noted between adult and independent immature reed warblers in the wild cannot be accounted for by differences in ability to capture flies. Firstly, once the experienced birds were fully

24,

I

grown, there was no further marked improvement in ability to capture flies. Secondly, the naive group were just as successful as the experienced group in capturing Musca and Calliphora during their first exposure. This suggests that the motor patterns used in hopping about the cage are very similar to those used in capturing flies. Some indication of this was seen when one of the naive group began a partial moult at the age of 25 days. As it hopped around the cage, small feathers dropped from its body and these were accurately caught in mid-air by two of the other birds, using methods identical to those used in leap catching flies. Small improvement may occur after full growth is attained due to maturation, which may explain why the older birds, even though comparatively inexperienced, were the most successful at fly capture. Young chaffinches choose smaller seeds than adults for some time after they are fully grown and Kear (1962) suggested that this may be due to continuing maturation of the muscles of the head and bill. We conclude that the difference in feeding techniques between wild adult and immature birds is probably due to a difference in food requirements. The observations of the adults were made on individuals feeding young, and their greater use of the leap catching technique was probably due to increased need to collect food. Root (1967) found that adult gnatcatchers (Polioptila caerulea) with young made more aerial captures of prey than adults without young, who tended to take prey which could be captured with less effort. (b) Handling ability. Although just as efficient as the experienced group at capturing flies, the naive group were much worse at handling the prey once caught. The age of first experience of flies markedly affected the speed of learning to handle them efficiently. The experienced group at 20 days of age improved their handling performance of Calliphora after a single day's experience and after this were immediately efficient at handling the smaller Musca. The improvement of the naive group, which were first tested at 30 to 40 days of age, was much slower. They were still not as good as the experienced group after 6 days testing with Musca and were also worse at handling Calliphora. This suggests that the mandibulative skills used in holding and swallowing flies must be different from those involved in handling meat balls, at which both groups were proficient. Some of the early handling improvement was

DAVIES & GREEN: REED WARBLER FEEDING TECHNIQUES due to learning to hold the flies by the body rather than by the legs and wings, and this resulted in their dropping the prey less often (Blest 1957). However, all the naive group held the prey by the body during the first day of testing, and there must be further improvement in mandibulation of flies once they are held firmly in the bill. Vince (1960, 1961) found that young great tits were more curious than adults and were more successful at learning to pull up food suspended from a perch by a piece of string, partly due to the greater variety of methods they tried. Similarly, young reed warblers may learn to handle flies by trial and error quicker than older birds because they try a wider variety of methods of mandibulation. Structural differences may also be relevant here. Young passerines have flexible bills and their wide gapes enable the parents to feed them large meals. In order to save energy in visits to the nest, parents often bring larger items to the young than they eat themselves (Root 1967, Royama 1970). When the young begin to feed themselves they may be physically better able to mandibulate large items than older birds whose bills and associated musculature are more mature and less adaptable. This may partly explain why the experienced group were less good at handling Calliphora when they were older. Although the break in experience was probably also a contributing factor to the longer handling times, there was no rapid improvement after a few trials comparable to that which occurred when the birds were younger. Therefore it is possible that young birds are better able to make a wide variety of small mandibulative movements and so learn to handle prey items efficiently in a much shorter time than older birds. Sensitive periods have been described for several learning processes including the following responses of nidifugous birds (Bateson 1966) the development of song in the chaffinch (Thorpe 1958) and the impaling techniques of shrikes (Smith 1972). Similarly the rapid learning of handling ability in the reed warbler seems to be restricted to a period early in development, probably before structural maturation of the bill is complete. (c) Other factors. Two factors which may be important in the development of feeding behaviour which were not studied here, are interaction with the parent birds and the ability to search for prey. Interaction with parents is important for learning hunting skills in several predatory mammals (Schaller 1972). In birds,

223

prolonged parental care may be correlated with the use of highly skilled feeding techniques (Ashmole & Tovar 1968). However, in most cases the young do not seem to learn feeding skills from the parents, although there are some exceptions (Norton-Griffiths 1967, 1969; Bent 1940, 1942; Meinertzhagen 1954), and observational learning of feeding methods has been reported in the laboratory situation (Dawson & Foss 1965). In the wild, young reed warblers do not follow their parents and do not get the opportunity to watch them feeding. The period of parental care ends when they are fully grown at 20 to 26 days (Brown & Davies 1949) and this corresponds to the time needed by our captive birds to learn by trial and error to capture prey by themselves. Therefore in this species as in some others (Smith 1973; Kear 1962) the influence of the parents is probably unimportant for the development of feeding techniques. In some birds parental or other social interaction may be important in learning where to feed and what to feed on, rather than how to capture prey (Turner 1964; Newton 1972). In this study flies were presented to the captive birds in far greater densities than those which they would encounter in the wild, and they did not have to search for the prey in the bare cages. Capture of the prey was quickly perfected during growth, and similarly experience plays little role in prey attack and killing behaviour in shrikes (Smith 1973) and kestrels (Falco sparverius) (Mueller 1974). However, in the wild, the most important factor limiting the feeding rate may be search or selection of suitable prey items, and for this, improvement with experience may be considerable.

The Ecological Significance of the Different Feeding Techniques Reactions to different prey species. The handreared captive birds from both groups were used at 35 to 40 days of age to study feeding techniques with different species of prey. Feeding techniques and successes for three calypterate Diptera are presented in Table VI. Musca and Lucilia were more active flies and spent more time flying round the cage than Calliphora, and the birds used catching techniques more often for these two species. Picking techniques were more successful for the sluggish Calliphora than for Musca which often escaped capture by flying off as the bird attempted to pick them up. There were no differences in picking success

224

ANIMAL

BEHAVIOUR,

24,

1

Table VI. Feeding Techniques and Capture Success for Three Species of Diptera by tbe Captive Birds

Species

Total number capture attempts

Per cent attempts by catching techniques

Per cent success By picking techniques

By catching techniques

Per cent success by all techniques

Calliphora

506

7-7 • 1"4

78'7 • 4.5

29.0 ~ 12-8

75"8 • 4.8

Lucilia

173

55.7 • 11.2

65"8 • 7.1

48'1 =b 4'6

53"4 • 2'5

Musca

2051

68"4 • 2"9

64.8 • 3.0

47.7 •

56'4 • 6.5

P < 0.01 P < 0'05 between Calliphora between and each of Calliphora the others and Musca

2"8

P < 0'01 between

Calliphora

and Musca

Means and SE for fourteen birds. Significant differences using Wilcoxon tests are shown. between Musca and Lueilia, nor were there any differences in the success of the catching technique for the three species. For total success, including all capture methods, Calliphora was more easily captured than Musca through there were no other differences. When they were 40 days old, three individuals were presented with five wasps (Vespa vulgar• These were the first that they had seen, the only prey they had previously experienced being the three fly species. All three birds immediately showed great interest in the wasps, peered at them and then made some half hearted attempts at capture. They appeared to be in conflict and wiped their bills against the perch, occasionally jumped into the air, or flew towards the wasps and snapped their bills 2 to 3 cm away without touching them. After 15 rain four Calliphora were introduced and these were immediately picked up and eaten without hesitation within 2 rain. The birds continued to ignore the wasps, and after a further.5 min another wasp painted with methylene blue dye was introduced as well. Within 20 s one bird jumped down and picked up the blue wasp, holding it in the bill for 4 s before dropping it, whereupon another bird picked it up and held it for 2 s. All wasps were then ignored for a further 20 rain after which they were removed. The next day eight wasps were presented, all having had the stings removed to avoid injury to the birds. Four of these were painted blue and four were normally coloured. All birds showed the same approach-avoidance conflict as the day before and ignored the normal wasps. However, one bird pecked three times at a blue wasp and picked up another on two occasions for brief periods of 1 to 2 s. After 30 rain ten Lucilia were released into the cage

and all were caught and eaten within 4 rain. The wasps were then ignored, and were removed after a further 20 rain. It could be argued that early experience with flies had resulted in the formation of a preference for familiar food items. Rabinowitch (1969) has shown that finches form stable seed preferences due to early experience and Coppinger (1969, 1970) has emphasized the importance of novelty as a factor in prey rejection. However, white butterflies (Pieris brass• were given to these three birds the day before the wasp test and although these were novel and quite unlike any prey they had seen before and caused great excitement, they were immediately attacked and pecked at. Hover flies (Diptera: Syrphidae) were also given for the first time on the day of the wasp test and were caught and eaten. Although these bore little detailed resemblance to the wasps, they were similarly coloured a striking black and yellow. The normal wasps were probably rejected on the basis of both colour and shape and the rejection of the blue wasps after a brief handling experience may have been due to the distasteful venom (Leipelt 1963) or some textural quality of the body (Gwinner 1961). Reactions to changes in activity of the prey.

Some flies encountered by birds in the wild were resting on leaves and twigs, while others were in flight. The relationship between success and frequency of use of the different techniques is shown in Fig. 7 for the fourteen captive birds from both groups at 30 to 40 days of age, with Musca as prey at 21 to 25~ Stand picking, stand catching and leap picking were the most successful methods. In all three of these techniques either the bird, or the fly, or both were

DAVIES & GREEN: REED WARBLER FEEDING TECHNIQUES

225

I 0 0 9n013 0 0

00 80

o

9 @

0

0

0 o

0 9

o

~0

@9 9 0 0

0

@0

0 @

o Stand pick

0 ~o

@0

9 9

@

8

40

0

9

o Leap pick

p@

9

@

9

9 Stand catch

@

9 Leap catch

o. (_)

20

Fly catch

.@

20

40

60

80

100

Attempts, per cent

Fig. 7. Relationship between success and frequency of use of different feeding techniques in fourteen captive reed warblers with Musca as prey. stationary, and there is presumably less scope for error in the movements involved in capture. However, at this temperature most of the flies were active and in flight, and the birds mainly used leap catching, which was a less successful technique but enabled them to capture flies at a greater rate. Fly catching was the least successful of all the techniques and was also used the least. Fly activity changes with temperature, and below a threshold the flies are sluggish and unable to take off, (Taylor 1963). At Wicken Fen, bushes frequented by feeding reed warblers were examined, and early in the morning, at low temperatures, many flies were seen resting on the foliage. They were much tess active and their presence less obvious to a human observer than in the heat of the day when many were in flight and active. In the wild, adult reed warblers change their feeding tactics with temperature and there is an increase in the rate of catching techniques and a decrease in the rate of picking techniques as the temperature increases. Independent immatures show a similar change in behaviour (Fig. 8) although they use the catchilag technique less frequently than the adults. Most of the observations were made early in the

day, so as expected, these changes also correlate significantly with time of day. Partial regressions show that the increase in rate of the catching techniques is explained best by temperature variation for both adults and immatures, while the decrease in picking rate is best explained by temperature for the immatures and time of day for the adults (Table VII). In the wild it is often not possible to see if the birds are successfid with their capture attempts, so this change in behaviour was studied in more detail with the captive birds, at 35 to 40 days old, using Musca as prey. The birds were kept in cages outside, and feeding techniques and successes were compared between days which were cold (15 ~ shade temperature), warm (21 to 25~ and hot (29~ There was no difference in the techniques used between 21 to 25~ and 29~ and although fewer attempts were by catching techniques at 15~ the difference was not significant (Table VIII). This was not very surprising because there are several differences between the cage and the wild. The birds were given food ad libitum, and the flies were not important as a food source, so a bird was not at a disadvantage if it attempted to capture only the few flies

226

ANIMAL

BEHAVIOUR,

24,

1

A

20

y = - 0 . 1 5 x + 6.89 1

y=-O-23x+8-81

20

--

15 I(

--

9

--

10

o~

----2_-'.

_ ~ ~ 1 7 6 1 ~7 6-~ " oo

-(3 (D

9

"~

I~

~ ~

oc

I 5

..C

~

10

15

%

~

"~

13

13 13

I

I

20

25

":_-

5--

9

. 9

..

_:__.

30 2:3

B ~3

k~

-E

y = 0 - 4 0 x + 5-13 ~, <

10

"z3

25--

15

" -20

25

30

D

c~

y = 0"52x -1"81

O

20--

O f

O

I --

9

15

o

n 9

15L--

9 AO~

'/ll'

0

10

-

A

F1

lo[ ." :

9

/.~../D

9

% o

9

5i

9

9

9

~

oOO 9

9

O

O

p ..'...,S.... -." ..-, 9

9

1

l

I

1

10

15

20

25

L 30

5

J--I

. 10

l= 15

l 20

25

30

Temperature ~ Fig. 8. Rates of capture attempts by two feeding techniques in wild reed warblers relative to shade temperature. Adults, A. Picking. B. Leap catching and fly catching. Different symbols refer to different individual birds. Independent immatures, C. Picking. D. Leap catching and fly catching. Fitted regression lines. Temperature ~

that happened to pass near it. Also, resting flies were not concealed and were sitting on the walls of the cage or the perches, whereas in the wild they were often out of sight under leaves. Finally, the wild birds are feeding on a wide variety of insect species and only one fly species was used in the experiments. However, capture success did change markedly with temperature. Total success was one and a

half to two times greater at 15~ t h a n at 21 to 25~ where success was in turn greater than at 29~ Success of the catching techniques was greater at 15~ than at 21 to 25~ but there were no differences between 21 to 25~ and 29~ Flies fly faster at higher temperatures (Johnson 1969) and may therefore be more likely to evade capture. Success of the picking techniques was greater at lower temperatures.

DAVIES & GREEN: REED WARBLER FEEDING TECHNIQUES

227

Table VII. Partial Regressions of the Changes in Rate of Picking and Catching Techniques with Time of Day and Temperature in Wild Reed Warblers

Adults feeding young

Independentjuveniles

SE

Significance of difference from 0

Partial b

sE

Significance of difference from 0

--0"21

0"22

NS

--0"26

0"09

P < 0'01

temperature

--0.38

0'23

NS

--0.07

0"15

NS

Picking techniques/100 s on temperature

time

--0.31

0.15

P < 0.05

--0'03

0.08

Ns

Catching techniques/100 s on temperature

time

+0"70

0'15

P < 0.001

+0.70

0"13

P < 0.001

Variables

Variable excluded

Partial b

Picking techniques/100 s on time

temperature

Catching techniques/100 s on time

Table VIII. Feeding Techniques and Capture Success of Musea at Different Ambient Temperatures by the Captive Birds

Ambient temperature 15~

21-25~ 29~

Total number of capture attempts

Per cent attempts by catching techniques

Per cent success By picking techniques

by catching techniques

Per cent success by all techniques

112

58.8 ~ 16.6

75.6 4- 9.2

80'0 :1: 12-2

84"0 4- 3"6

2053

70.9 -4- 2.8

69"8 4- 3"8

48.7 ::k 2"3

54-6 -4- 2"1

487

70.9 A: 3.4

35"5 -4- 4"9

39"6 • 4-6

38"6 • 3"7

P < 0"01 between 15~ and 21-25~

P < 0"01 between 21-25~ and 29~

P < 0'01 between 21-25~ and 29~

Means and sE for fourteen birds. Significant differences using Wilcoxon tests are shown.

The only individual feeding technique whose success changed with temperature was leap picking which was m o r e successful at 21 to 25~ than at 29~ (Wilcoxon test P < 0.01). At 21 to 25~ leap picking was a more successful technique than leap catching and total picking methods were more successful than total catching methods (Wilcoxon test P < 0.01 in b o t h cases), but at 29~ these differences disappeared. These results are consistent with the view that in w a r m t h flies are better able to evade capture by taking off as the bird attempts to pick them up. A similar result was obtained when we ourselves tried to capture mediumsized flies in the field using a mouth-operated suction trap or pooter, and success greatly decreased as the temperature increased (Green & Davies 1972).

Discussion

The range of feeding methods used by the reed warbler enable it to exploit b o t h sluggish and highly mobile prey. The available prey changes throughout the day due to diurnal flight .periodicities (Lewis & Taylor 1964) and changes m activity with temperature. The birds alter their feeding tactics to match these changes. At low temperatures their feeding rate m a y be limited by their ability to search for stationary prey hidden in the foliage. Fewer meals are brought to nestlings early in the morning, perhaps because insects are less active and more difficult to find than later in the day when the temperature increases. A t higher temperatures the capture success of highly mobile prey m a y become more critical. Similar changes in prey activity influence the feeding behaviour o f other

ANIMAL

228

BEHAVIGUR,

species (Miller 1931; D u r a n g o 1951; GossC u s t a r d 1969). In the wild, reed warblers e n c o u n t e r a great variety o f prey, a n d the results with the captive birds feeding o n three species o f flies show that different feeding techniques are used for different p r e y species. However, reed warblers do n o t a t t e m p t to c a p t u r e all the prey they encounter. I n n a t e rejection o f d a n g e r o u s p r e y , such as the wasps, which were refused by t h e captive reed warblers on their first presentation, is o f considerable advantage. I f the bird was stung this c o u l d p r o v e fatal or at least prevent feeding for some time (Leipelt 1963). M o s t l e r (1935) c o n c l u d e d t h a t learning is i m p o r t a n t in wasp rejection for several passerine species, b u t there is p r o b a b l y some individual v a r i a t i o n and, in general, birds which regularly feed o n wasps show specializations a n d often have innate p a t t e r n s o f t r e a t m e n t to render t h e m harmless before swallowing (Birkhead 1974).

Acknowledgments W e t h a n k the N a t u r e C o n s e r v a n c y Council for a p e r m i t to keep birds in captivity, Peter R o b e r t s h a w a n d A n n N a y l o r for help in handrearing t h e m a n d D r P. P. G. B a t e s o n a n d M r R a y Rice for facilities at M a d i n g l e y , C a m b r i d g e . D r P. P. G. Bateson, D r E. K. D u n n a n d D r I. N e w t o n helped us i m p r o v e early drafts and the m a n u s c r i p t was t y p e d b y M r s M e r l e Harris. P a r t o f the w o r k was financed b y a N . E . R . C . studentship.

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Catchpole, C. K. (1972). A comparative study of territory in the reed warbler, Acrocephalus scirpaceus, and the sedge warbler, Acroeephalus sehoenobaenus. J. Zool. Lond., 166, 213-231. Catchpole, C. K. (1973). Condition of co-existence in sympatric breeding populations of Aerocephalus warblers. J. Anita. Ecol., 42, 623-635. Cody, M. L. (1974). Competition and the Structure of Bird Communities. Princeton University Press. Coppinger, R. F. (t969). The effect of experience and novelty on avian feeding behaviour with reference to the evolution of warning colouration in butterflies. I. Reaction of wild caught adult blue jays to novel insects. Behaviour, 35, 45-60. Coppinger, R. F. (1970). II. Reaction of naive birds to novel insects. Am. Nat., 104, 323-337. Cruze, W. W. (1935). Maturation and learning in chicks. J. comp. psychol., 19, 371-409. Dawson, B. V. & Foss, B. M. (1965). Observational learning in budgerigars. Anita. Behav., 13, 470474. Dunn, E. K. (1972). Effect of age on the fishing ability of Sandwich terns, Sterna sandivicensis. Ibis., 114, 360-366. Durango, S. (1951). Om tornskatans, Lanius collurio, L., spetsning av bytesdjur. Var Fagelvarld, 10, 49-65. Dyrcz, A. (1974). Factors affecting the growth rate of nestling great reed warblers and reed warblers at Milicz, Poland. Ibis, 116, 330-339. Fogden, M. P. L. (1972). The seasonality and population dynamics of equatorial forest birds in Sarawak. Ibis, 114, 307-343. Goss-Custard, J. D. (1969). The winter feeding ecology of the redshank, Tringa totanus. Ibis, 111, 338-356. Goss-Custard, J. D. (1970). Feeding dispersion in some overwintering wading birds. In: Social Behaviour in Bird~ and Mammals (Ed. by J. H. Crook), pp. 3-34. London: Academic Press. Green, R. E. & Davies, N. B. (1972). Feeding ecology of reed and sedge warblers. Wieken Fen Group Report, 4, 8-14. Gwinner, E. (1961). Uber die Entstachelungshandlung des Neuntoters, Lanius eollurio. Vogelwarte, 21, 36-47. Hinde, R. A. (1959). Behaviour and speciation in birds and lower vertebrates. Biol. Rev., 34, 85-128. Hubbard, J. P. & Hubbard, C. L. (1970). Foraging behaviour in the blue flycatcher. Auk, 87, 154-156. Impekoven, M. (1962). Die Jugendentwicklung des Teichrohrsangers, Aeroeephalus scirpaceus. Rev. Suisse Zool., 69, 77-191. Johnson, C. G. (1969). Migration and Dispersal of Insects by Flight. London: Methuen. Kear, J. (1962). Food selection in finches with special reference to interspecific differences. Proe. zool. Soe. Lond., 138, 163-204. Kruuk, H. (1972). The Spotted Hyena. Chicago. Univ. Chicago Press. Lack, D. (1946). Sedge warblers and reed warblers collecting food outside their territories. Br. Birds, 39, 87. Lack, D. (1968). Ecological Adaptations for Breeding in Birds. London: Methuen. Lack, D. (1971). Ecological Isolation in Birds. Blackwell. Leipelt, W. (1963). Zur schutzwirkung des Stachelgiftes von Bienen und Wespen gegenuber Trauerfliegenschnapper und Gartenrotschwarz. Zool. Jb. Physiol., 70, 167-176.

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blue herons, Florida caerulea. Anim. Behav., 17, 320-322. Root, R. B. (1967). The niche exploitation pattern of the blue grey gnatcatcher. Ecol. Monogr., 37, 317-350. Royama, T. (1970). Factors governing the hunting behaviour and selection of food by the great tit, Parus major L. J. Anim. EeoL, 39, 619-5668. Schaller, G. B. (1972). The Serengeti Lion. Chicago. Univ. Chicago Press. Siegfried, W. R. (1972). Aspects of the feeding ecology of cattle egrets, Ardeola ibis, in South Africa. J. AnOn. EcoL, 41, 71-78. Smith, S. M. (1972). The ontogeny of impaling behaviour in the loggerhead shrike, Lanius ludovicianius L. Behaviour, 42, 232-247. Smith, S. M. (1973). A study of prey attack behaviour in young loggerhead shrikes, Laniu~" ludovicianius L. Behaviour, 44, 113-141. Taylor, L. R. (1963). Analysis of the effect of temperatttre on insects in flight. J. Anim. Ecol., 32, 99-117. Thorpe, W. I-I. (1958). The learning of song patterns by birds with special reference to the song of the chaffinch, Fringilla coelebs, lbis, 100, 535-570. Turner, R. A. (1964). Social feeding in birds. Behaviour, 24, 1--46. Vince, M. A. (1960). Developmental changes in responsiveness in the great tit, Parus major. Behaviour, 15, 219-243. Vince, M. A. (1961). Developmental changes in learning capacity. In: Current Problems in Animal Behaviour (Ed. by Thorpe & Zangwill). Cambridge University Press. (Received 28 February 1975; revised 12 May 1975; MS. number: 1409)