acta neurobiol. exp

ACTA NEUROBIOL. EXP. 1975, 35: 517-528

Memorial Paper in Honor of Jerzy Konorski

?fHE BIOLOGICAL SIGNIFICANCE OF DUETTING AND ANTIPHONAL SONG

W. H. THORPE

Sub-Department of Animal Behaviour Madingley, Cambridge. England

Abstract. Duetting plays a very important part in the signal system between male and female in a large number of bird species, in particular species that inhabit tropical regions. These elaborate song patterns show many interesting features, of which only a few have been discus- sed here. Perhaps the most interesting result of our investigations of duetting is the light cast on the heretofore little appreciated precision and synthesizing power of avian aural perception, the great precision of response time and the equally great exactness of control of the vocal organs. The use of these vocal powers for individual recognition is in line with observations made over the past decade by B. Tschanz, C. G. Beer, myself and others. This work has shown that in many co- lonial nesting birds (for example auks, terns, gulls, gannets and pen- guins) brief calls of a half-second duration or less can have enough acoustic detail not only to serve as labels identifying the calling species but also to label the individual caller.

Every ornithologist is aware of the almost universal occurrence amongst birds of elaborate ritualised mutual displays between male and female. It is in connecti~n with these displays, in fact one might say a necessary part of them, that the remarkable and in same cases gro- tesqce and fantastic evolution of sexual dimorphism of plumage has occurred. Some outstanding examples are known to everyone, e.g. the peacock's tail, the exquisitely beautiful male plumages of many species

518 nT. H. THORPE

of pheasants and the bizarre display of the bustards; some of which, when in full display, turn themselves "inside out" into an object hardly recognisable as a bird! It has long been realised that such visual displays, all of which involve an elaborate series of species-specific action-patterns, not only in the male but to a lesser extent in the female also, are essential in the process of pair formation, in maintenance of the pair bond once formed, and in the mutual coordination of the sexual cycles. This coordination is essential for the successful completion of the reproductive cycle to the point at which the young eventually reach indepen- dence. Such displays then are often mutual between male and female, are closely coordinated and may endure for the whole of the breeding season and in some cases throughout t h e year.

Song is of course a recognised element in the display of the male in an enormous number of species of birds, particularly those grouped under the general heading of Oscines. Moreover vocalisations of one kind or another are commonly found to be incorporated in the process of the male's display to his potential or actual mate. In most birds the females themselves do not "sing"; but very often simple vocalisations may be produced by the female while the mutual visual displays are in progress. When this happens it is probable that the vocalisations of males and females together will be coordinated in the same manner as are their display gestures. To this extent it can be said that such species "duet". All examples of mutual vocalisation between pairs, whether simple, brief and poorly organised or lengthy elaborate and precisely organised can be included under the term "duetting". Where the performance involves one member of the pair starting the song and the other completing it, it is usual to employ the term "antiphonal song" as a par-

(a) Ant+hona/ (6) Polyphonic

(c) unison (d) Overlapping (polyphonic)

Fig. 1. Types of duet singing.

THE BIOLOGICAL SIGNIFICANCE OF DUETTING d l 9

ticular kind of duetting. So antiphonal song and duetting may include exact alternation, polyphonic performances (when the two birds sing at the same time, each coordinating its individual song pattern with the other) and rather more unusually, unison singing when both birds produce exactly the same pattern of notes a t the same moment. Finally of course the two contributions may be different in pattern but overlap each other, again with precise coordination. Figure 1 shows in the form of musical examples, a, a characteristic antiphonal song and b, c, and d, polyphonic duets. Example c, is a song in complete unison while d, shows an instance of simple overlapping; in essence, polyphony because the long upper note is sounding during the performance of the lower notes.

The existence of this first type of mutual singing between mated pairs was first recognised by ornithologists working in tropical regions. Thus G. A. Fischer and A. Reichenow (1878, 1879) mentioned its occurrence in the Laniidae (Genus 1,aniarius) in East Africa. N. A. Cobb made a similar observation in Australia in 1897 referring to an uncertain species of the Genus Cracticus (Family Cractidae); and W. H. Hudson (1892) described mutual vocalisations as part of the display of the spur-winged plover Noploxypterus (Vanellus) cayanus in South America. Early observations in this century include those of Fuertes (1916) and Huxley (1919). Stoneham (1928) was the first to provide precise observations on duetting of some of the Shrikes (Laniarius) jn East Africa.

Since then both observations and experiments have proceeded apace and the more important studies up to the year 1971 have been summarised by myself and associates (Thorpe 1972).

The present position is that the existence of species showing habitual antiphonal song is known in approximately 33 families of birds. Of these 33 no less than 23 are families either restricted to or at least characteristic of the tropical areas of the world. Where the families are not restricted to the tropics we find, as in the wrens (Troglodytidae) that it is almost exclusively the tropical species which display this type of behaviour. Of the 23 families mentioned as displaying antiphonal song there are some nine in which we find the habit most fully developed and in which the timing and coordination of the duetting is most fully perfected. These nine families are the Megapodae (the mound builders), the Phasanidae (pheasants, quails and francolins), the Rallidae (rails and crakes), the Formicariidae (the ant birds and ant shrikes), the Tro- glodytidae (the wrens), the Turdidae (the thrushes including the Robin Chat Cossypha heuglini), the Sylviidae (the warblers), the Laniidae (the shrikes) and the Meliphagidae (the honey eaters of Australia and New 6 uifiea).

520 W. H. THORPE

The last family but one mentioned above is that in which the tropical representatives in Africa have the most perfect examples of duetting and which have so far been the most thoroughly studied. Thus in the genus Laniarius it is established that all 15 species, ranging throughout tropical Africa, exhibit this behaviour.

Of these 15 species we studied three, Laniarius aethiopicus, the African Bell-Shrike, or Tropical Bou-bou Shrike, Laniarius erythrogaster, the Black Headed Gonolek, and L. funebris, the Slate-coloured Bou- bou. This work has all been reported in full in the reference above given, so it is not necessary to recount all the details here. However we have reason to believe that the work on these three, particularly that of the first mentioned L. aethiopicus, gives a number of clues as to the origin and function of this duet and antiphonal singing. The conclusions that arise from this work are that, apart from the callnotes, the vocalisations usually consist of antiphonal singing between the members of a mated pair; and that the male is usually, but not necessarily, the leader. Usual- ly the duet pattern (which in this species consists of a series of typically six or seven clear flute-like notes uttered with great exactness of timing the whole pattern completed within a period of 1 or 2 sec is produced in bouts of about 5 or 10 repetitions at regular intervals of about 4 or 5 sec. Sometimes, however, the bouts of antiphonal song are much more extended; consisting perhaps of 20 to 40 or more repetitions of the pattern without any break. On occasion birds may sing the whole of a given pattern in exact synchrony, the performance thus being in unison, and we also found that either bird alone could sing the whole duet pattern by itself. That is, using its own notes and those of its partner correctly. This device can apparently be used as a means for calling the absent mate back to his or her territory. It was also shown that while there are many duet patterns common to most if not all pairs in a given area, the repertoire of each pair is likely to be distinct from that of its neighbours, and that the individual repertoire, and to some extent the individual voice quality, can be used as a means of individual recognition by the birds. This vocal repertoire is worked out and developed between members of the mated pair; isolated birds seem unable to produce any complexity of vocalisation pattern. Studies of captive birds have shown that crowding of the birds, particularly if they cannot see one another, leads to great but temporary elaboration of duet patterns; and there is some evidence that in crowded areas, where the territories are small, duet patterns are more complex than in regions where the population is sparser.

Our study of the harmonic aspects of the antiphonal song of L. aethiopicus has yielded evidence of considerable interest from the musical

THE BIOLOGICAL SIGNIFICANCE OF DUETTING 521

point of view. Besides being dealt with in the monograph the salient facts have also been summarised by Thorpe (1973). They are outside the scope of the present paper and so are not further referred to here.

From our studies on the shrikes we were forced to the conclusion that the functions of antiphonal song in these species are four. First, location and maintenance of contact with the mate; second, mutual sti- mulation between two birds of a pair, as a part of or a substitute for the ordinary methods of visual display; third, aggressive maintenance of territory and fourth, mutual reassurance after disturbance. There are reasons for thinking that these functions will apply satisfactorily to the great majority of known examples of antiphonal song particularly those occurring in the tropics. In many cases the most perfect examples of antiphonal song occur in the species which live in the very dense tropical vegetation, where it must be difficult for the two members of the pair to keep in sight of each other. In such a setting the birds would find a vocal pair-bond useful, if not essential. Moreover in all the species of Laniarius, male and female are of identical appearance. This again is peculiarly frequent, indeed almost invariable, in the nine families above mentioned. Not only do these Shrikes, and a great many other tropical birds, live in dense vegetation, particularly those of tropical rain forests; they also show very little sign of migratory movements and it seems probable that the Shrikes remain paired for life and main- tain their territories for the greater part of the year, perhaps for their entire lives.

Now it is important to realise that in the Earth's temperate zones, seasonal changes in the length of the day provide the most important of the cues that initiate the secretion of birds' sex hormones and so bring potential pairs into the breeding condition. In the Tropics, the day- length cue, is very slight if not completely absent. Moreover other pos- sible "seasonal" cues (such as variations in humidity, rainfall, degree of cloud cover and light) tend to be unpredictable and to give little ad- vance warning. I t follows that if birds in the tropics are to take full advantage of the period when breeding conditions are at an optimum, both males and females must be in constant contact so that their behaviour and their reproductive cycles are fully coordinated and ready to take immediate advantage of good conditions when they arise.

Our experiments in tropical avaries in Cambridge yielded many interesting new facts about duet production. Thus we were able to confirm our field observation that, if one member of a pair was absent, the bird remaining in the territory tends to sing the whole duet pattern by itself; both its own contribution and its mate's. When the mate returns however a period of unison singing is not uncommon. The duet in

522 W. H. THORPE

unison would last for a few seconds; thereafter the pair resume antiphonal song as before. These Shrike studies evidently confirm a theory put forward by Konrad Lorenz to the effect that "whole duet" vocalisation in a partner's absence may be intended to secure the partner's re- turn. It is almost as if one bird were using the characteristic vocal performance of the other as a "name", that might serve as a recall.

A series of separation experiments in the aviaries yielded the fol- lowing conclusions: First, separation initially leads to an increase in the amount of vocalisation by the deserted bird. In contrast, a bird which is moved to a new "territory" tends to decrease its vocalisation. Second, if the bird remaining in the territory is a male he employs all his usual vocalisations and in addition some of those of his missing partner. Third, if two members of a pair are separated for a long period, there is sooner or later a tendency to show a regression of vocalisation which can re- duce the performance to what amounts to a juvenile condition.

If an isolated male hears a playback of his mate's voice, he will reply with the appropriate item from his own repertoire. The male is much less likely to respond to his own voice, however, and does so only by repeating the song which has just been played. This finding during our aviaries studies confirms still another conclusion based on field work: even though notes of the Bell-Shrike are very uniform in acoustic struc- ture they may be sufficiently different to be recognized on the basis of their vocal quality as well as by the musical pattern which they form. Again in aviary experiments we found that the female Bell-Shrike in the aviary will answer such notes of her own male as she may be able to hear but will not answer the notes of any neighbouring pairs. In one set of experiments an extra male was kept in association with a duetting pair. The outside male was never heard to vocalise until the resident male was removed. When the removal took place, however, it became clear that the outside male had at least in part learned not only his rival male's repertoire but also that of the female. The resident female will respond to the educated outside male song although she would not respond to the songs of strangers.

It was not at all unusual during our studies of birds in the wild to find examples of antiphonal singing in which three birds took part. Sometimes the third bird would be simply duplicating one or more of the notes of the mated pair but at other times it would contribute one or two original notes to the pattern which the pair had already worked out. When this happened, the pair took no apparent objection to the addition; indeed, they sometimes went so far as to alter the timing of their pattern to allow for the interpolation of the third bird's notes. The trio then established might be repeated many times. This was difficult to

THE BIOLOGICAL SIGNIFICANCE OF DUETTING 523

4

prove with some species but was clear with L. funebris. The production of trios could take place almost instantaneously as we found when we had a number of newly imported individuals in the laboratory close together, but screened from sight of one another. These trios and indeed sometimes quartets, which developed under these artificial conditions, were coordinated with extreme precision for a short series of repetitions and then abandoned not to be heard again. This was in strong contrast to the relative permanence of trios heard in the wild.

Trios of this kind were usually brought about under natural conditions in the margins of territories where one member of an adjacent pair, sex unknown, joined in with a duetting pair. We have also fairly good evidence that a well grown young bird will sometimes combine in duetting with its parents and perhaps in this way obtain its first prac- tical experience in learning the niceties of the performance. Also in tho wild one may sometimes hear well coordinated song patterns between four birds. These quartets are perhaps most likely to occur when there are two well-grown young of a pair in the neighbourhod and they can also be heard at the point of contact between adjacent occupied territories; in this case the four adult birds may produce a bout of quartet singing with little or no evidence of aggression. However, one may at times hear fierce interruptions of one pair's duetting by the voices of a neighbouring pair, though it is more usual for the two pairs to sing their un- changed duet patterns in alternation, resulting in agonistic counter duetting.

This phenomenon of trio and quartet singing can merge into rather con- fused group singing which is not a1 all well understood. Some particularly interesting examples of this are provided by Grass Warblers of the Genus Cisticola. This genus contains a huge assemblage of 40 species and 153 races of birds widespread throughout tropical and sub-tropical Africa. Out of all these forms 4 species are duettists, yet they are duettists of the highest precision. These 4 species are nigriloris, discolor, chub- bz and Itunteri. Discolor Is confined to the Cameroon mountain district, both the peak and the highlands. I t has been recorded; but the remoteness of its habitat and the scarcity of workers in that area have so far prevent- ed any detailed studies. The last two species, chubbi and hunteri, have complex duets with high-pitched notes of extreme rapidity and extraordinary precision. Figure 2 shows a schematised sonographic picture of the duet motif of a pair of Cislicola hunteri at Ngong, Kenya. The diagram makes clear the contributions of the birds X and Y, but the sex of these two is uncertain though it is thought probable that X represents the female and Y the male. Quartet singing is also heard in this species but here it seems to be an effect of counter duetting between

W. H. THORPE

Duet motif kHz( l-

1

0 0.5 Time 0 sec Fig. 2. Schematised sonagraphic picture of the duet motif of a pair of Cisticola hunteri at Ngong, Kenya. Sa and Ual-Ua4, contribution of bird X T and Val-Val9, the contribution of bird Y. The sex of birds X and Y is uncertain but it is thought

probable that X = 9 and Y = $. From Todt (1970).

neighbouring pairs with a very good temporal coordination both between individuals and between pairs. Todt who has done the most thorough work on this species find that pairs respond to playbacks of their own duets first by male and female making vocal contact; second, by mutual aggressive approach to the loudspeaker and third, a loud counter duet. When this happens the responding pair generally use that duet pattern of their repertoire which is being played to them at the moment. Com- munal singing is very characteristic of this species but here again it seems that it is made up of several discrete and consistently duetting pairs. If one plays the duet of one of these pairs to a communally singing group the only pair to emerge from the undergr,owth and reply to the recorder is the one whose duet has been reproduced.

The precision of duetting in hunteri and chubbi is prodigious. In chubbi I have recorded a series of six consecutive duets, in this case the birds being within sight c~f one another, the mean response time being 396 msec with a remarkably small standard deviation of 2.9 msec, i.e.. about 118th the error which a man would make under similar circum- stances.

C. nigriloris is an equally precise performer and notes of discernible pitch are more evident than in the duets of the other three species. The birds are unique in their ability to transpose the entire duet pattern from its original range to at least two different pitch levels whilst re-

THE BIOLOGICAL SIGNIFICANCE OF DUETTING ,523

taining the original relationships between the constituent notes. This is the more remarkable because the duet comprises a rapid 4-note pattern, repeated many times, and each bird appears to contribute only one note a t a time. These birds also produce strange creaking noises as an accompaniment to the pitched sounds.

This case of the genus Cisticola raises a puzzling question. Why, as seems almost certain, is antiphonal song restricted to these four species only? One would think that a great many of the other species must be equally in need of this form of communication in the dense vegetation in which they almost all live. There is certainly no clear answer to this puzzle but one interesting explanation has been suggested. All these four species are restricted to high altitudes where dense mist and cloud often prevail for long periods. It may well be that this additional hin- drance to the maintenance of visual contact gives antiphonal song a significant selective advantage over and above that provided by a habitat of dense vegetation.

One final example of an African duetting species may be mentioned namely the Whitebrowed Robin Chat (Cossypha heuglini). Here again, as in all the other species mentioned in this paper, the sexes are identical in appearance - another feature which sets a premium upon a vocal means of recognition. The curious thing about the genus Cossypha is that of the 15 species occurring in Africa, all of them living under similar conditions only one has been established for certain as a duettist. This one has the widest distribution of them all ranging from Eritrea and the highlands of Ethiopia and the Sudan in the north, south to Southern Rhodesia and the eastern Transvaal and west to the Lower Congo and Angola. In different parts of its range it overlaps geographically with all the other species!

The Whitebrowed Robin-Chat is found at all altitudes up to about 2,000 m where there is dense vegetation. In general it is an excessively shy bird which spends most of its time securely hidden in the under- growth, feeding largely on the ground and rarely seen at any height in trees except when singing. It is however exceedingly pugnacious and aggressive counter duetting is quite common. The song is usually given under conditions of low visibility at dawn and dusk and the duet-pattern is a long one, lasting 5 sec or more. It starts with male solo phrases showing a gradual crescendo (Fig. 3). Aparticularly interesting point is that when the loudness reaches a certain critical level it appears to provide the signal for the female to join in. The birds then proceed together, continuing the crescendo and with the pitch slowly rising; although after the female takes part the male tends to cut out his higher notes giving a lower pitched accompaniment to the females downward glissandos. All

W. H. THORPE

d I I

0 1.0 2.0 sec Fig. 3. A and B, consecutive duets from a pair of wild birds. Note that the regular relationship between d and $2 parts changes with the change of a" phrase a t s tart

of B and returns at the end. (From Thorpe 1972.)

species of this genus are exceptionally fine singers but the song of heuglini is remarkable in its dramatic intensity and extraordinary crescendos. Each repetition is slightly louder and more rapidly uttered than the last, conveying the impression that the bird is labouring under an intolerable stress.

There is however one remarkable and puzzling phenomenon which has become established and which shows that duetting is not always a matter of maintenance of the pair-bond - this is the occurrence of interspecific duetting. Laniarius funebris not infrequently duets with L. erythrogaster (Thorpe, p. 129) and Wickler (1972ab) has reported duetting between L. funebris and the Drongo Dicrurus adsirnilis.

In attempting to summarise this subject, one must resist giving the impression that antiphonal song, even of the most precise timing, is restricted to the tropics. The recent paper by Hall-Craggs (1974) on the duetting of the Whooper Swan (Cygnus cygnus) has shown the performance to be far more precisely coordinated than was previously thought.

In conclusion we can say that duetting constitutes a very important part of the signal system between male and female in a large number of bird species, particularly those that inhabit tropical regions. Lack of space prevents reference in this article to more than a few of the remarkable features which these studies have revealed. Perhaps the most interesting basic result of our investigations of duetting is the light cast on the heretofore little appreciated precision and synchronising power of avian aural perception, the great exactness of response time and the equally fine control of vocal organs. These are aspects of the study which would have been of particular interest to Professor Konorski and

THE BIOLOGICAL SIGNIFICANCE OF DUETTING 52 7

i t has been a great privilege to be able to make this small contribution to the memory of a friend of long standing and a very great behavioural physiologist. It is much to be hoped that the famous research school which he founded will continue to develop and thus constitute a lasting memorial to him.

Finally most of the facts here summarised will be found in the Mo- nograph (op. cit.) but, since its publication, a number of new studies have appeared and references to some of the more significant of these in relation to African and South American birds are appended. Of particular note are Wickler's (1972~) studies of L. funebris and those which establish the behaviour in families of birds where it was not previously recsgnized. These are von Helversen and Wickler (1971) for the Drongo Dicrurus adsimilis (Family Dicruridae) and Snow (1973) for the Hairy Hermit, Glaucis hirsuta (Family Trochilidae).

It was been suggested that autochthonous rhythms of sound production, which must be of widespread occurrence in birds, are an important element in the performance of precisely timed examples of duetting and antiphonal song (Payne 1971). The evidence seems all against this view as far as the examples described in this article are concerned. How- ever in the Barbets (Capjtonidae) autochthonous rhythms seem fairly conspicuous in non-duetting forms and it may be the case that, as argued by Payne and Skinner (1970), some of the examples of apparently precise duetting in this family are dependent on the preexistence of these rhythms.

FISCHER, G. A. and REICEENOW, A. 1878, 1879. Briefliche Reiseberichte aus Ost-Afrika. J. Ornithol. 26 and 27.

FUERTES, L. A. 1916. Impressions of the voices of tropical birds. Ann. Rept. Smiths Inst. 1916: 299-323.

HALL-CRAGGS, J. ,1974. Controlled antiphonal calling by Whooper Swans (Cyg- nus cygnus). Ibis 116: 228-231.

HUDSON, W. H. 1892. The naturalist in L a Plata. London (Dent). HUXLEY, J. S. 1919. Some points in the sexual habits of the little grebe, with

a note on the occurrence of vocal duets in birds. Brit. Birds 13: 155-158. PAYNE, R. B. 1971. Duetting and chorus singing in African birds. Ostrich, Suppl.

9: 125-146. PAYNE, R. B. and SKINNER, N. J. 1970. Temporal patterns of duetting in African

barbets. Ibis 112: 173-183. SNOW, B. K. 1973. Social organisation oi' the hairy hermit (Glaucis hirsuta. Tro-

chilidae). Ardea 61: 94-105. STONEHAM, H. F. 1928. Field notes on a collection of birds from Uganda. Ibis 12

(Ser. 4): 252-285.

528 W. H. THORPE

THORPE, W. H. 1972. Duetting and antiphonal song in birds. Its extent and significance. (In collaboration with J. Hall-Craggs, B. Hooker, T. Hooker and R. Hutchison). Behaviour, Suppl. 18: 1-197.

THORPE, W. H. 1973. Duet-singing birds. Sci. Amer. 229: 70-77. TODT, D. 1970. Die antiphonen Paargesange der ostafrikanischen Grassangers Cis-

ticola hunteri priniotdes. J. Ornithol. 111: 332-356. von HELVERSEN, D. and WICKLER, W. 1971. Uber den Duettgesang des afrika-

nischer Drongo (Dicrurus adsirnilis) Z. Tierpsychol. 29: 301-321. WICKLER, W. 1972a. Aufbau und Paarspezifitat des Gesangsduettes vor Lania-

rius funebris. Z. Tierpsychol. 30: 464-476. WICKLER, W. 197223. Duettieren zwischen artverschiedenen Vijgeln im Freiland.

Z. Tierpsychol. 31: 98-103.

Received 25 October 1974

W. H. THORPE, Department of Zoology, Sub-Department of Animal Behaviour, University of Cambridge, Madingley, Cambridge CB3 8AA, England.

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