(144) REACTIONS OF SOME PASSERINE BIRDS TO A STUFFED CUCKOO. II. A DETAILED STUDY OF THE WILLOW-WARBLER.
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1 (144) REACTIONS OF SOME PASSERINE BIRDS TO A STUFFED CUCKOO. II. A DETAILED STUDY OF THE WILLOW-WARBLER. BY GEORGE EDWARDS, ERIC HOSKING AND STUART SMITH IN a previous paper {British Birds, Vol. xlii, pp ) we described the reactions of various small passerine birds to a stuffed Cuckoo (Cuculus canorus) placed in their nesting territories. These experiments, which were exploratory in nature, raised a number of interesting problems, and it became evident that if we were to obtain answers to certain of them, it would be necessary to give close study to a single species during the whole of the breeding period. We chose for this study the Willow-Warbler (Phylloscopus trochilus) because it is a common bird whose nest is not very difficult to find, and one which reacts strongly to a stuffed Cuckoo. It can be shown mathematically that if one assumes a probability of at least 0.05 (one in twenty) to be desirable, then at least 10 experiments on one species must be carried out to obtain significant results from which sound deductions can be made. Altogether we found, and did experiments at, 14 nests of the Willow-Warbler, whilst in addition, experiments were tried in 6 territories of cock birds of this species, from the day of their arrival in mid-april until the beginning of nest construction. The results relating to the period of territory formation, therefore, are not so significant as those obtained at the nests. During this intensive study we attempted, among other things, to answer the following questions : (a) What effect has the stage reached in the breeding cycle on the reactions of the birds? (b) Has any particular part of the Cuckoo a specially high significance in evoking attack? (c) Is the Cuckoo " recognized " as such by the Willow-Warblers, and can they differentiate one dummy from another? These questions, and the experimental data obtained during their elucidation, are dealt with below. (a) Effect of stage reached in breeding cycle. It is convenient to divide the breeding cycle into four periods, namely, (i) from the arrival of the cock birds to the start of nest construction ; (ii) the period including nest-construction, clutchcompletion, and incubation ; (iii) the period during which the brood is in the nest; and (iv) the post-fledging period. (i) The first cock Willow-Warblers arrived in their territories in the North Cheshire area in mid-april, and experiments were started on the day of their arrival. There were two cocks singing vigorously on the 13th, three on the 14th, and five on the 18th. The sixth did not
2 VOL. XLIII.] REACTIONS TO A STUFFED CUCKOO. 145 arrive until April 24th. The method of experimentation at this stage was to use stuffed Cuckoos specially prepared for us in which a stout wire protruded through the belly. This wire was thrust down the hollow inside of a 10 foot bamboo cane, and the Cuckoo could then be lifted nearly 20 feet into the tree in which a bird might be singing. Animation could be give to the Cuckoo by slightly rotating the cane in either direction. The birds reacted at once to this, even though an observer held the cane in his hand, but once a bird's attention had been drawn by such methods to the Cuckoo, the cane was normally thrust into the ground and reactions observed from a distance. In general, during this period, the following may be taken to summarize average reaction to the dummy, though there were individual variations between different cocks. The results are based on 42 hours of watching and experimenting in the six territories. Immediately on arrival and for a period afterwards (which is variable and which probably corresponds to that before the hens arrive) the cock Willow-Warblers respond to the Cuckoo by posturing at it with " flicking " wings and very loud and sustained song. Occasonally the chittering " chee-chee " note, which is such a feature of later display, is used against the dummy, but not at all frequently. On no single occasion was an actual attack made on the dummy, the chief features being a close approach and vigorous and sustained singing. As soon as a hen bird arrived and one of the cocks had paired with her, reaction of that cock to the Cuckoo diminished quickly. In two instances, paired cock Willow-Warblers ceased altogether to react to the Cuckoo, although they continued to sing in their territories and attack other Willow-Warblers which ventured in. Reaction to the Cuckoo during territory formation, seems strongest in the region of the song-post, but thereafter it is strongest in the area of the nest. It seems probable that during this stage when the cock birds are forming their territories, the Cuckoo has no very great " valence " for the Willow-Warbler, and that reaction to it may take place more because of the high general level of aggressive potential within the birds, than from specific reaction to the dummy as a Cuckoo. Cock birds which were merely passing through on migration did not react to the Cuckoo at all, although they sang whilst resting in areas as yet untenanted by other Willow-Warblers. Thus in one case, the behaviour of a cock bird which was singing in one area puzzled us at first because, whenever the Cuckoo was presented to it, the bird flew away to a distance. Next day, however, this bird had disappeared and was evidently a passing migrant. (ii) Experiments were conducted at three nests during the building stage, at four nests during laying and incubation of the eggs, and at seven nests with young in various stages of development. In only one case were the three stages of building, laying and incubation, and rearing of the young, investigated consecutively at
3 146 BRITISH BIRDS. [VOL. XLIII. one and the same nest, since at two of the three nests found in the building stage, the experiments resulted in the birds abandoning the nest before it was completed. This desertion of nests at the building stage, if experiments are attempted, was also noted by Lack to occur with three Robins (Erithacus rubecula), (Life of the Robin, Witherby, London, 1943). It should be noted, however, that in the case of the nest at which experiments were carried out through all three stages, the reaction at any one stage duplicated exactly that obtained at other nests at which only one, or sometimes two stages were investigated. The general picture, allowing for small individual variations from pair to pair, is fairly constantly as follows. During the nestbuilding period the Willow-Warbler reacts to the Cuckoo with chittering and wing-flicking, but not with an attack. At one nest, completed externally but not lined, a stuffed Cuckoo placed in a bush a yard above the nest evoked loud chittering and wing-shaking from the pair. This brought in other Willow-Warblers until there were six birds of this species in the small bush, all demonstrating against the Cuckoo. There was no attack, however, although occasionally two of the cocks would sing a snatch of song and then attack one another. While the six birds were in the bush, a live Cuckoo came to a tree 20 yards away and called. Two of the Willow-Warblers then left the bush and flew to the tree, where they chittered and demonstrated against the live Cuckoo. Later, this nest was deserted, as was one other at which experiments were done during the building stage. As soon as egg-laying starts, reaction to the Cuckoo becomes more violent. At a nest with four fresh eggs of an incomplete clutch, the hen bird returned soon after a dummy Cuckoo had been placed just above the nest. She demonstrated by chittering and flicking her wings, but did not attack. When the cock arrived three minutes later, he attacked at once and the hen joined in, and the combined attack was violent enough to knock over the dummy. After incubation has started, violent attack by both birds of the pair is general, and accompanied by the usual chittering and wingflicking. (iii) With young in the nest, reaction to the Cuckoo is immediate, violent, and sustained, and does not seem to vary with the degree of development of the young. (iv) In the post-fledging period, experimental work is difficult and uncertain, especially after the young have scattered, but at two nests at which we were able to experiment on the day the young were leaving, or had just left, the nest, the adult birds persisted in attacking the Cuckoo so long as the young remained near to the site of the nest. On the following day, however, when the young were more scattered, the adults no longer attacked the Cuckoo, even though it was placed in its previous position immediately over the
4 VOL. XLIII.] REACTIONS TO A STUFFED CUCKOO. 147 nest. The young were by this time scattered over a radius of about 20 yards from the nest-site, and the adult birds merely chittered at the Cuckoo and flicked their wings. This marked diminution in aggressive behaviour after the young are well clear of the nest duplicates what we observed at a Nightingale's {Luscinia megarhyncha) nest, where violent attack on a dummy ceased quickly a few minutes after the young had scattered into the undergrowth around the nest. Although violent attacks on the Cuckoo occur in the area immediately surrounding the nest during the incubation and fledging periods, the cock Willow-Warblers will react to the Cuckoo by cluttering and wing-flicking at any point within their territories. Indeed, it is possible to obtain a fairly clear idea of the extent of any territory by studying the reaction of the cock birds to a Cuckoo. Thus our friend, Edward Bradbury, experimented with a Willow-Warbler which had a territory in a field adjoining his garden. When he appeared in the field with the stuffed Cuckoo in his hand, the cock Willow-Warbler would fly towards him calling with the chittering note. It would then follow him down one hedge-side and half way along another hedge until a small oak tree was reached. Beyond this point the bird refused to go, and reaction ceased as he passed into the next bird's territory. This experiment was exactly repeated on five separate occasions. Conversely, one of us (S.S.) was able to find the whereabouts of two Willow-Warblers' nests by moving a Cuckoo about in the territories and noting the violence of the reaction from the birds. On many occasions we have placed stuffed Cuckoos at random in woods, coppices and gardens and invariably they attract a variety of birds, amongst which Willow-Warblers are always prominent with their chittering note and wing-flicking. Only when they have a nest very near to the position of the Cuckoo does any attack take place. (b) Has any particular part of the Cuckoo a special significance? Almost without exception, the area of attack on the Cuckoo dummies (and for that matter on any dummy which evokes attack) is the head and especially the eyes, crown and nape. We therefore investigated experimentally the question of the valence of different parts of the Cuckoo's body. We made first of all a wooden form, roughly shaped like a bird's body and having holes and slits cut into it so that a tail, wings, and head and breast could be independently attached to it. Fig. i shows the wooden body, and Figs. 2 and 3 show first the tail and wings attached, and then in addition, the head. At four separate nests, containing young in all stages of growth, we tried the following sequence : wooden body alone ; body plus tail; body plus tail plus wings; body, tail, wings and head. General reaction was as follows. With the wooden body alone, the birds took very little notice, although they obviously saw
5 148 BRITISH BIRDS. [VOL. XLIII. it and usually flitted around uneasily for a short while before feeding the young. Reaction to the body with tail, and then with tail plus wings added, was more obvious than to the body alone. In one case the hen called once or twice with the fear note (" hewie ") ; in two other cases, where the pair arrived with food together there was a little chittering and wing-flicking but no attack. As soon as the head was added, however, in all cases violent and immediate attacks were made on it. We also tried, at one nest with small young, the wooden body with head alone added, and got an immediate attack (Fig. 4). We next tried the effect of the head alone, with no body attached, at three other nests with young at which experiments had not previously been tried. At each one, the head and a few breast feathers were wired on to a stick and placed near to the nest. Very violent attacks occured in each case. Figs. 5 and 6 show the Willow- Warblers attacking this wired-up head. In one case we fixed pieces of tape over the eyes of the head and found reaction was diminished so that no actual attack occurred, but we put this fact forward with reserve as only one experiment was carried out in this way to test the significance of the eyes. It is interesting to note that a carved wooden Cuckoo-shaped bird with metal tail and wings, and correctly coloured glass eyes (Fig. 7) failed completely to evoke an attack by Willow-Warblers with young. Later the same birds readily attacked the feathered head of a Cuckoo attached to a stick. It seems evident from these experiments that the part of the Cuckoo having the highest significance or " valence" for the Willow-Warblers is the head, and Hartley (An Experimental Analysis of Interspecific Recognition, 1949, in press) has summarized other examples which confirm that the head or face of a bird are of prime importance in the processes of recognition. (c) " Recognition " of the Cuckoo. Previous experiments (vide antea, Vol. xlii, p. 19) had indicated that several species of passerine birds could differentiate a stuffed Cuckoo from a stuffed Jay (Garrulus glandarius) or hen Sparrow-Hawk (Accipiter nisus), but we were anxious to go more fully into this question with our Willow-Warblers. We therefore arranged a series of tests with the following dummies : (a) the composite Cuckoo described above ; (b) a whole Cuckoo; (c) a hen Sparrow-Hawk; (d) a cock Sparrow-Hawk standing over prey ; (e) a Red-footed Falcon (Falco vespertinus). The order of presentation of these dummies was varied, both from trial to trial, and from nest to nest. We had previously noticed that change from one type of reaction to another, when the birds were presented successively with two different dummies, was rarely immediate. The birds appeared to go through a stage of indecision in which one type of reaction slowly faded and its place was taken gradually by the other. As an example, we frequently got both the " chittering" and " hewie " notes
6 VOL. XLIII.] REACTIONS TO A STUFFED CUCKOO. 149 immediately after removing a Cuckoo and substituting a Sparrow- Hawk, and only after several minutes did the birds go over completely from an aggressive to a fear reaction. It was as though the visual " imprinting " of the image of the first dummy was overlaid by that of the second, and that as the latter increased in strength the former slowly died away. We therefore decided on a very quick change round of the dummies. As soon as the birds had given one typical reaction (e.g., the chittering call followed by one attack) we changed to the next dummy. This gave us remarkably clear-cut, and almost immediate, changes in reaction, and also by changing our dummies round rapidly we could make a large number of observations in a comparatively short time. Typical of our results at five different nests may be cited the following, which represent work at one nest which contained young just ready to leave. We placed a stout stick in the ground and fixed the dummies to it in various orders. In all, five trials were carried out, each starting in turn with a different dummy, and following with the others in the order given below. The reactions observed were recorded and were as follows. Dummy Wooden Cuckoo with Reaction tail and wings. Fear reaction ; " hewie " note. Wooden Cuckoo with tail Aggressive reaction, " chittering " note and wings, plus head Whole Cuckoo. and attack. Violent aggressive reaction. " Chittering " note and attack on dummy whilst held in hand. Hen Sparrow-Hawk. Fear reaction : " hewie " note. Red-footed Falcon. Aggressive rea'ction : " chittering " and attack. Cock Sparrow-Hawk with Very strong fear reaction: "hewie" raised wings, standing note and spasmodic fluttering of on prey. wings. These reactions were clear-cut, and repeatable for the five orders of presentation of the dummies that we tried. Experiments at this nest lasted about 4 hours. The reaction to the Red-footed Falcon is of great interest, since although the hooked beak of the raptor was there, the general colouration and shape of head of this stuffed bird approximated to those of the Cuckoo. It is fairly certain from these experiments that Willow-Warblers have a visual concept of " cuckoo " associated with a head which is blue-grey in colour, and that they have a specific reaction to this concept which is aggressive in character, and typified by a specific, chittering " chee-chee " note, accompanied by wing-flicking and by actual physical attack on the head. Although, in most of the trials, we were able to change the dummies very quickly, there were one or two instances where we did not
7 150 BRITISH BIRDS. [VOL. XLIII. do this quickly enough to get the change of reaction quite clear-cut. Thus, in going from whole Cuckoo to hen Sparrow-Hawk we once or twice got the chittering note just after the change over, when this had taken us longer to accomplish than some others. To demonstrate the extremely high retention of the visual image, we left a Cuckoo head in place at one nest for 9 minutes during which both birds made violent attacks on it. We then removed it but left in position the perch on which it had been fixed. The Willow- Warblers continued to fly to the perch and to " chitter " and flick their wings for 30 minutes after the removal of the dummy (Fig. 8). This persistence of visual image after removal of the object causing it, is a common feature of bird behaviour, and explains such apparently abnormal behaviour as the return of a bird to the spot in midair where a sawn-off branch, containing its nest, had previously been sited. Finally we wish to acknowledge the help we have received from various ornithologists during the course of this work. Mr. Peter Hartley, of the Edward Grey Institute at Oxford, helped us to crystallize our ideas on the psychological aspects of the work at a critical stage and made several valuable suggestions for experimental work. He also carved for us the complete wooden Cuckoo. Mr. A. Hazlewood, of the Bolton Museum, was instrumental in getting for us a number of Cuckoo skins from a taxidermist's old stock, and went to considerable trouble to stuff these specially with peat and to insert stout wires for our convenience. Mr. R. Wagstaffe, Keeper of the Yorkshire Museum, also supplied us with stuffed specimens under the British Trust for Ornithology Study-Material Service.
8 British Birds, Vol. xliii, PI. 26. Fig. 2. EXPERIMENTS WITH DUMMY CUCKOOS. Fig. i. BODY OF SECTIONAL CUCKOO. SECTIONAL CUCKOO WITH TAIL AND WINGS ATTACHED. (Photographed by ERIC HOSKING).
9 British Birds, Vol. xliii, PI. 27. Fig. 3^ EXPERIMENTS WITH DUMMY CUCKOOS. SECTIONAL CUCKOO WITH HEAD, TAIL AND WINGS. Fig. 4. WILLOW-WARBLER (Phylloscopus trochilus) ATTACKING HEAD OF CUCKOO ATTACHED TO WOODEN BODY. (Photographed by ERIC HOSKING).
10 British Birds, Vol. xliii, PI. 28. EXPERIMENTS 'WITH DUMMY CUCKOOS. Fig. 5. WILLOW-WARBLER ATTACKING HEAD OF DUMMY CUCKOO. (Photographed by ERIC HOSKING).
11 British Birds, Vol. xliii, PI. 29. Fig. 6. EXPERIMENTS WITH DUMMY CUCKOOS. WILLOW-WARBLERS ATTACKING HEAD OF DUMMY CUCKOO. (Photographed by ERIC HOSKING).
12 British Birds, Vol. xliii, PI. 30 Fig. 7. EXPERIMENTS WITH DUMMY CUCKOOS. CARVED CUCKOO WITH EYES AND METAL TAIL AND WINGS. Fig. 8. WILLOW-WARBLER DEMONSTRATING WITH WING-FLICKING AND WITH CHITTERING NOTE ON STICK FROM WHICH THE CUCKOO HEAD HAS BEEN REMOVED. {Photographed by ERIC HOSKING).
13 British Birds, Vol. xliii, PI. 31. PINTAIL {Anas acuta) : NEWLY HATCHED NESTLINGS, NORFOLK, MAY 14TH, (SEE PAGE 159). {Photographed by ROBIN M. HARRISON).
14 British Birds, Vol. xliii, PI. 32. Upper : FULMAR (Fulmarus glacialis) SUN-BATHING, GREAT SALTEE ISLAND, Co. WEXFORD. (SEE PAGE 160). (Photographed by A. G MASON). Lower : RING USED BY ROYAL DUTCH HAWKING CLUB FOR MARKING HERONS. (SEE LETTER, PAGE 165). (Photographed by M. J. TEKKE).
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