R. M. KILNER, D. G. NOBLE & N. B. DAVIES
Nature 397, 667 - 672 (1999) © Macmillan Publishers Ltd.
Department of Zoology, University of
Cambridge, Downing Street, Cambridge CB2 3EJ, UK
Nestling birds present vivid gapes and produce loud calls as they solicit food, but the complexity of the display is poorly understood. Here we explain the function of reed warbler begging signals and show how they are exploited by the common cuckoo, Cuculus canorus, a brood parasite. Reed warbler parents integrate visual and vocal signals from their young to adjust their provisioning rates, and the two signals convey more accurate information about offspring need than either does alone. The cuckoo chick has a particularly striking begging display which has been suggested to be irresistible to host parents. However, we show that the cuckoo, reared alone in the nest, presents a deficient visual display, and elicits the same amount of care as a reed warbler brood only by compensating with its exaggerated vocal display. Therefore the cuckoo succeeds not through mimicry of the host brood begging signals, but by tuning into the sensory predispositions of its hosts.
Many animal displays are highly complex1,2, often built from several component signals of different sensory types3,4. For example, nestling birds beg with a combination of brightly coloured gapes5 and repetitive begging calls6. Despite their ubiquity, and a range of theoretical models7,8,9,10,11, empirical understanding of multicomponent displays is limited12. Here we explain why the nestling begging displays of reed warblers (Acrocephalus scirpaceus) and their brood parasite, the common cuckoo (Cuculus canorus), include both visual and vocal components. Our experiments show that reed warbler parents use both signals to adjust their provisioning rates at the nest. Together, these signals provide parents with more information about their offsprings' need than is available from either signal alone. Moreover, we show that reed warblers follow exactly the same integration rule when provisioning a single cuckoo in their nest as when feeding a brood of their own young. The way in which parents integrate two nestling signals illuminates the function of the cuckoo's extraordinarily rapid begging call13. Rather than whipping parents into a feeding frenzy at the nest14,15, the supernormal begging call instead serves to persuade parents to work at their normal rate by compensating exactly for the cuckoo's subnormal visual display of a single gape.
Information carried by begging signals
We studied a population of reed warblers at Wicken Fen, Cambridgeshire, UK, in the summers
of 1996-1998. Nestling reed warblers solicit food from their parents by exhibiting a
bright yellow gape and calling repeatedly. Although previous work with other species has
established that the various components of the begging display are individually correlated
with nutritional state5,16,17, it is not known how they combine to signal food
requirements. We investigated whether gape area and begging call rate convey distinct
information about the extent of food deprivation (see Methods).
Chicks were temporarily removed from the nest at a range of different ages (day 3/4 and
day 6/7) in broods of four (the modal brood size). They were fed with chick-rearing mix
until they stopped begging, and then kept warm but unfed. Every 10 min, for the next
110 min, we stimulated the brood to beg, recording the begging behaviours on video
and audiotape (see Methods). We found that total gape area
displayed and begging call rate each varied significantly with both the extent of food
deprivation and chick age (Fig. 1). Hence, the different elements of the begging display
carried 'multiple messages'11,
each element reflecting both age and hunger10,11.
Moreover, because the two elements in the begging display each explained different
components of variance, for both chick age and food deprivation, they also functioned as
'back-up' signals (Fig. 1)11.
Figure 1 Effect of food deprivation. Effect of food deprivation
on a, the total gape area displayed by all chicks (see Methods) and b, the
rate of calling by broods of four reed warblers, on day 3/4 (open circles;
s.e.m. The data were analysed with a repeated-measures
ANOVA, with two within-factors (food deprivation time and type of begging signal) and one
between-factor (chick age). There was a significant effect of food deprivation (
We checked the robustness of our conclusions by using a separate
analysis of a larger data set with a different measure of offspring need, namely the
amount of food required to cause the nestling reed warblers to stop begging. Nestlings
were temporarily removed from the nest at a range of different ages (day 2 to day 8) and
in broods of one (
Parental response to multiple signals
Do parents regulate their provisioning rate in relation to both the rate at which the
brood calls and the total gape area displayed? We tested this possibility by
subjecting the parents of broods of two and four nestlings, aged 6/7 days old, to
playback of begging calls which were broadcast through a small speaker, attached to the
side of the nest, every time the nestlings gaped for food. The three treatments were: no
playback, playback of one chick calling and playback of four nestlings calling (see Methods). Clearly, the effects of these playbacks on the parents would
be confounded if they affected the behaviour of the nestlings. To examine this, we
recorded the duration of the brood begging display during each treatment, because in
another species this is influenced by sibling vocalizations18. There was no indication that the playback of begging
calls affected this aspect of chick begging behaviour (22
= 1.63
Figure 2 Effect of playback treatments. The effects of the
playback treatments at broods of two (2RW; s.e.m. Each pair of parents was subjected to three treatments:
no playback, playback of one reed warbler chick calling (playback 1RW) and playback of
four reed warbler chicks calling (playback 4RW). The data were analysed with a
repeated-measures ANOVA with one within-factor (playback treatment) and one between-factor
(brood size). There was a significant effect of brood size (
In a different analysis, we used data from 59 brood-size
manipulations and 52 playback manipulations (see Methods) to
investigate the separate effects of visual and vocal signals on provisioning rates to
chicks aged 6/7 days old. We used field recordings of broods manipulated to be different
sizes to check that the calling rate of individual chicks was not affected by
altering the brood size. A strong positive linear relationship between brood size and
brood call rate (
We found that reed warbler parents combined multiple signals from
their young to adjust their provisioning rate at the nest. There were significant
independent effects of the maximum number of gapes displayed per nest (
The regression equation explains parental provisioning rate in terms
of the number of chicks displaying visually and vocally 6/7 days after hatching. We
studied whether the equation could be expressed more generally to explain provisioning
rates to reed warbler nestlings of different ages and in different brood sizes. To
generalize the equation from day-6/7 chicks to young of all ages, we divided the 'gape'
coefficient by the mean gape area of a day-6/7 reed warbler chick (140 mm2),
and divided the 'calls' coefficient by the mean number of calls per 6 s given by an
unmanipulated day-6/7 reed warbler chick in the field (12.95 calls/6 s). The
regression equation thus derived was: feeds delivered per
It may seem remarkable that parental provisioning rates for broods of one to eight young, from one to eight days after hatching, can be explained simply as a response to the gape area displayed and the brood calling rate. However, the results of our experiments with chicks in the laboratory indicate that both signals can convey accurate information about chick age, brood size and nutritional state, so perhaps it is not surprising that two signals alone can explain so much of the variance in parental provisioning rate. We suggest that the visual display may provide parents with a crude estimate of how frequently to feed their young, because it is correlated with brood size and chick age, whereas the vocal display may enable parents to fine-tune their provisioning in relation to the brood's level of hunger, because this signal provides more finely graded information about nutritional need. For example, in day-6/7 chicks the visual signal reaches a plateau 60 min after being fed to satiation, whereas the vocal signal continues to change (Fig. 1).
In theory, the amount of food supplied by parents to young is likely to be the source of a conflict of interests between the two parties, because investment patterns that are optimal for parents can be suboptimal for offspring19,20. Recent theoretical work has suggested that the conflict may be resolved in the parents' favour if provisioning rates are based on costly, and hence reliable, nestling signals of need21,22. The two regression equations that we have derived experimentally (first to relate chick need to their begging signals, and second to relate the begging signals to parental provisioning) allow us to link chick need quantitatively with parental provisioning rates. In principle, this provides a way in which to measure the outcome of parent-offspring conflict, and to test the prediction that parents supply chicks with exactly the food that they demand. At present, this analysis is beyond our reach, because the units of each regression equation are not the same.
Exploitation by cuckoo chicks
The reed warblers at Wicken Fen are parasitized by the common cuckoo, a brood parasite
that relies entirely on its hosts to incubate its eggs and rear its young to independence23. Shortly after hatching, the cuckoo
nestling evicts all of the reed warbler eggs and chicks from the nest24, and so becomes the sole beneficiary
of parental care. Apparently oblivious to the destruction of their own reproductive
success, the pair of warblers then feeds the imposter, even as it grows to eight
times their own body weight. By 2 weeks of age, the cuckoo overflows the tiny nest, and
the warblers seem to risk being devoured themselves as they perch on the cuckoo's back in
order to bow deep into the enormous gape with food.
Our observations show that the rate at which parents provision a single cuckoo chick closely matches the rate at which they provision a brood of four of their own young, of equivalent mass, the modal brood size in this species (Fig. 3). The food brought to the cuckoo is also the same as for their own young25. Previous experiments have established that the cuckoo's success at eliciting care cannot be attributed simply to its relatively large size. When we placed in a reed warbler nest a single blackbird (Turdus merula) or song thrush (T. philomelos) chick of the same mean mass as a cuckoo nestling, the Turdus nestlings were fed at a significantly lower rate. However, their rate of being fed improved markedly when their own begging display was augmented by cuckoo nestling begging calls broadcast from a small speaker at the side of the nest13.
Figure 3 Relationship between nestling mass and feeding rate.
The relationship between the mass of young in the nest and the number of feeds delivered
per hour by both parents to the nest, for cuckoos (open circles, solid line,
Analysis of a larger data set than presented previously13 shows that the Turdus
nestlings accompanied by cuckoo begging calls obtained significantly more food than
cuckoos (unpaired
At 6-8 days of age, a cuckoo nestling's begging call closely matches the rate of calling of a brood of four reed warblers13. However, as the cuckoo grows, its begging call becomes increasingly more rapid, far faster than the rate of calling achieved by a brood of four reed warblers (Fig. 4a). Conversely, despite its enormous gape, the total gape area displayed by the single cuckoo is much less than that of a brood of four reed warblers, and the difference becomes more pronounced with increasing chick mass (Fig. 4b). This is an inevitable consequence of the fact that adult cuckoos have relatively small bills in relation to mass compared with adult reed warblers26, so a single cuckoo will never match the gape area of four reed warblers of the same total mass (Fig. 5).
Figure 4 Relationship between nestling mass and begging call
rate or gape area. The relationship between nestling mass and a, begging call rate,
for cuckoos (
Figure 5 Chick gapes. a, A nestling cuckoo, day 11/12; b, a brood of four reed warblers, day 6/7. The two pictures are at roughly the same magnification.
If reed warblers follow the same integration rule when feeding a
cuckoo as when feeding their own young, we can use our regression equation to test whether
the increasingly supernormal begging call of older cuckoo nestlings serves to compensate
exactly for their increasingly subnormal visual stimulus, compared with a brood of four
reed warblers. Using the equation: feeds delivered per
When we compared our predictions with measurements of unmanipulated cuckoo begging call rates in the field, we found no significant difference between the two (Fig. 6). Therefore reed warblers do indeed use exactly the same provisioning rules when feeding cuckoos and when feeding their own brood (Fig. 7). The increase in the cuckoo's calling rate with age is exactly what we would expect if it is to offset the disadvantage of displaying a single gape. Furthermore, the close match between our predictions and observations (Figs 6, 7) indicates that any cues other than gape area and call rate must play a minor role in determining host provisioning rate. For example, our experiments show that gape colour has no effect on provisioning rate27. A key point is that the cuckoo does not mimic the begging displays of a brood of reed warblers precisely, but instead tunes into the way in which the host parents integrate visual and vocal cues from their young28, exaggerating the latter to compensate for deficiencies in the former. There is an analogy here with the way in which males can exploit female sensory systems in mate choice29. This sensory exploitation differs from the deception practised by aggressive mimics such as Photurus fireflies and Bolas spiders30 which, respectively, mimic exactly the visual or chemical cues of their prey.
Figure 6 Comparison of observed and predicted begging call
rates. Observed cuckoo begging call rate (open circles, solid line) is compared with the
predicted cuckoo begging call rate (filled circles, dashed line) that should accompany the
display of a particular gape area, assuming that reed warblers use the same rules to feed
both a cuckoo nestling and their own young. Numbers refer to sample sizes of cuckoos
measured at each age. Both lines increase significantly in relation to gape area (
Figure 7 Comparison of predicted and observed provisioning
rates. Predicted provisioning rates, derived from our experiments with reed warbler
nestlings, are shown by the plane, which represents the regression equation: feeds
delivered per hour
Theoretically, we would expect the cuckoo to demand a much higher provisioning rate than a brood of reed warblers, because it has no genetic stake in the future breeding success of the parents31,32. However, far from being an irresistible narcotic lure14, the cuckoo chick apparently struggles to induce parents to feed it at the rate at which they would provision a brood of their own young. Rather than demanding a higher provisioning rate, the cuckoo instead exploits hosts by forcing them to provide care for longer (17 days in the nest plus 16 days after fledging, compared with 11 days in the nest plus 12 days after fledging for reed warbler young)33. Parents can certainly be made to work much harder in the short term25, so why don't cuckoos solicit a higher rate of provisioning? It has previously been argued that this would not benefit the cuckoo because it might exhaust hosts before the end of the cuckoo's dependent period25. But the data shown here suggest another explanation. By evicting the reed warbler chicks from the nest at the start of its nestling life, the cuckoo gains the benefit of receiving all the food brought to the nest, but pays the cost of being solely responsible for dictating the rate at which it is provisioned. Constrained by its visual display of a single gape, the cuckoo may be unable to solicit a higher rate of feeding, perhaps because there is an upper limit to the rate at which calls can be produced or perceived.
Other species of brood parasite that are reared alongside the hosts' own young may show a different solution to the same problem. These species might suffer the cost of sibling competition for food at each nest visit34,35, but at least they gain the benefit of assistance in soliciting a high visit rate. In short, the constraints of eliciting a high provisioning rate alone, or of losing food in sibling competition, may mean that we never see brood parasites being fed at the high rate we might predict.
Methods
Measurement of nestling gape area, mass and call rate in the field. For all
species, we used Vernier callipers to measure the distance between the proximal outer
corners of the mouth flange to the nearest 0.05 mm (gape width), and the distance
between the proximal corner and the tip (gape length) and calculated the product (gape
area, assuming the usual fully open gape). For broods, total gape area displayed was the
sum of the individual gapes. We found it impossible to handle cuckoo chicks older than day
11 and be certain that they would settle back in the nest. Therefore gape areas for cuckoo
chicks on days 13 and 15 were estimated from the extrapolated polynomial regression of
gape area on nestling weight, using published masses of common cuckoos in reed warbler
nests at these ages32. We
measured nestling mass in the field to the nearest 0.25 g using a 50 g Pesola
spring balance, and in the laboratory to the nearest 0.005 g using a Sartorius
electronic balance. We recorded the vocalizations emitted by unmanipulated cuckoos at
different ages and reed warblers of different ages and in different brood sizes onto
digital audiotape (DAT), using a Sony ECM-T6 tie-clip microphone attached to the side of
the nest, and then recorded these calls onto a Macintosh computer. We scored the number of
calls produced during the first 6 s of each nest visit (the shortest nest visit
duration) using the sonograms produced by the application Canary 1.2.1.
Measurement of begging displays and food consumption in the
laboratory. To standardize levels of food deprivation, we recorded the begging
displays of chicks in the laboratory in June-July 1996-1998. Chicks were temporarily
removed from the nest at a range of different ages (reed warblers day 2-8, cuckoos day
2-11) and in broods of one (reed warblers
Parental response to nestling visual and vocal signals. In
June-July 1996-1998, we performed 111 treatments using 63 different pairs of parents when
chicks were 6/7 days old. For each treatment we scored total feeds delivered per hour at
the nest by both parents. Data were collected either by using a video camera (
Manipulation of brood size. We manipulated brood sizes so
that they ranged from one to eight nestlings (
Playback manipulation. We broadcast the vocalizations of
either a single reed warbler chick (
Received 11 November 1998;
accepted 13 January 1999.
References
Acknowledgements. We thank NERC for funding the
research; the National Trust for allowing us to work at Wicken Fen; C. Thorne and the
Wicken Fen Group for research facilities; M. de L. Brooke for assistance in finding
nests; M. de L. Brooke, F. Hunter, R. Johnstone and N. Langmore for comments on the
manuscript; and B. Grenfell for producing
Correspondence and requests for materials should be addressed to R.M.K. (e-mail: rmk1002@zoo.cam.ac.uk).
Nature © Macmillan Publishers Ltd
1999 Registered No. 785998 England.