Rebecca M. Kilner

Begging the question: are offspring solicitation behaviours signals of need?

Throughout the animal kingdom, distinctive behaviour by offspring commonly precedes and accompanies their provisioning by parents. Here, we assess empirical support for the recent theory that begging advertises offspring need, that parents provision young in relation to begging intensity, and that the apparently costly nature of begging ensures the reliability of the signal. While there is some support for the predictions of honest signalling models, empirical work has also revealed a host of complexities (such as the use of multiple signals) that existing theoretical analyses have only begun to address.

Signals of need in parent-offspring communication and their exploitation by the common cuckoo

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.

The evolution of egg colour and patterning in birds

Avian eggs differ so much in their colour and patterning from species to species that any attempt to account for this diversity might initially seem doomed to failure. Here I present a critical review of the literature which, when combined with the results of some comparative analyses, suggests that just a few selective agents can explain much of the variation in egg appearance. Ancestrally, bird eggs were probably white and immaculate. Ancient diversification in nest location, and hence in the clutchs vulnerability to attack by predators, can explain basic differences between bird families in egg appearance. The ancestral white egg has been retained by species whose nests are safe from attack by predators, while those that have moved to a more vulnerable nest site are now more likely to lay brown eggs, covered in speckles, just as Wallace hypothesized more than a century ago. Even blue eggs might be cryptic in a subset of nests built in vegetation. It is possible that some species have subsequently turned these ancient adaptations to new functions, for example to signal female quality, to protect eggs from damaging solar radiation, or to add structural strength to shells when calcium is in short supply. The threat of predation, together with the use of varying nest sites, appears to have increased the diversity of egg colouring seen among species within families, and among clutches within species. Brood parasites and their hosts have probably secondarily influenced the diversity of egg appearance. Each drives the evolution of the others egg colour and patterning, as hosts attempt to avoid exploitation by rejecting odd‐looking eggs from their nests, and parasites attempt to outwit their hosts by laying eggs that will escape detection. This co‐evolutionary arms race has increased variation in egg appearance both within and between species, in parasites and in hosts, sometimes resulting in the evolution of egg colour polymorphisms. It has also reduced variation in egg appearance within host clutches, although the benefit thus gained by hosts is not clear.

Escalation of a coevolutionary arms race through host rejection of brood parasitic young

Cuckoo nestlings that evict all other young from the nest soon after hatching impose a high reproductive cost on their hosts. In defence, hosts have coevolved strategies to prevent brood parasitism. Puzzlingly, they do not extend beyond the egg stage. Thus, hosts adept at recognizing foreign eggs remain vulnerable to exploitation by cuckoo nestlings. Here we show that the breach of host egg defences by cuckoos creates a new stage in the coevolutionary cycle. We found that defences used during the egg-laying period by host superb fairy-wrens (Malurus cyaneus) are easily evaded by the Horsfields bronze-cuckoo (Chrysococcyx basalis), a specialist fairy-wren brood parasite. However, although hosts never deserted their own broods, they later abandoned 40% of nests containing a lone Horsfields bronze-cuckoo nestling, and 100% of nests with a lone shining bronze-cuckoo nestling (Chrysococcyx lucidus), an occasional fairy-wren brood parasite. Our experiments demonstrate that host discrimination against evictor-cuckoo nestlings is possible, and suggest that it has selected for the evolution of nestling mimicry in bronze-cuckoos.

Primary and secondary sex ratio manipulation by zebra finches

Wild zebra finches, Taeniopygia guttata, breed opportunistically when there is sufficient food available, often rapidly mobilizing their reproductive systems in response to an ephemeral boom in grass seed production. For females in captivity, fecundity, attractiveness to mates and survival to reproduction are all correlated with their fledging weight. By contrast, for males, only attractiveness is related to fledging weight; the relationship between fledging weight and male mortality is much weaker and that for male fecundity is unknown. Previous work thus suggests that how much food nestlings receive will have a profound impact on their reproductive success, and that this effect may be more marked for females than for males. I manipulated the food available to domesticated breeding zebra finches to test Trivers & Willards (1973, Science, 179, 90-92) hypothesis of adaptive sexual investment. When food availability was restricted, clutch sex ratios were significantly more male biased than when food was available in excess. Within clutches, daughters hatched sooner than sons and first-hatched chicks fledged at higher weights than those that hatched last. Chick mortality was female biased when food availability was low but male biased when food availability was unrestricted. I compared the song output of brothers of differing weight at independence, but found no significant difference between them. These data suggest that zebra finches manipulate both their primary and secondary sex ratios in relation to food availability to invest adaptively in sons and daughters, and support Trivers & Willards hypothesis. Copyright 1998 The Association for the Study of Animal Behaviour.

NESTLING CUCKOOS, CUCULUS CANORUS, EXPLOIT HOSTS WITH BEGGING CALLS THAT MIMIC A BROOD

Nestling cuckoos, Cuculus canorus, eject host eggs or young from the nest and are then raised alone by the hosts. Using reed warblers, Acrocephalus scirpaceus, as hosts, we investigated how the single cuckoo chick can command the same provisioning rate as a whole brood of host young. Large size alone is not sufficient to stimulate adequate provisioning because single blackbird, Turdus merula, or song thrush, T. philomelos, chicks of the same mass as a cuckoo were fed at a lower rate. Our experiments show that the key stimulus is the cuckoo chicks rapid begging call (‘si, si, si, si ...’), which sounds remarkably like a whole brood of host chicks, and which it matched in calling rate. When single blackbird or song thrush chicks were accompanied by loudspeakers that broadcast either cuckoo begging calls or calls of a brood of reed warblers, the hosts increased their provisioning rate to that for a cuckoo chick. We suggest that the cuckoo needs vocal trickery to stimulate adequate care to compensate for the fact that it presents a visual stimulus of just one gape.

Negotiations within the family over the supply of parental care

Adults provisioning dependent young are in conflict with their partners, who would prefer a greater level of effort, and with their offspring, who would prefer a greater supply of food. To what extent, then should adults negotiate their provisioning behaviour with other family members? We used experimental manipulations of brood size, and targeted playback of begging calls to determine the extent to which adult great tits Parus major adjust their provisioning rates in response to the behaviour of their partner and their brood. We found that males and females behaved similarly, both responding more to each others behaviour than to chick calling. We also found that the degree to which adults negotiated their provisioning rates with each other varied between years. A review of the literature suggests that the extent of negotiation over provisioning is likely to vary not only between species of diverse taxa, but also between and within (this study) populations of the same species. We suggest that provisioning behaviour lies on a ‘negotiation continuum’, which describes the extent to which parents respond to the actions of other family members. We argue that an individuals location on the ‘negotiation continuum’ is determined partly by the extent to which it can physically respond to the behaviour shown by other members of the family and partly by the quality of information on offer.

Parent-Offspring Conflict and Coadaptation

Speak to Me, Mama Maternal effects are effects of the mother (for example, hormones) on her offspring that are independent of genetic inheritance, but related to the mothers phenotype and her environment. Despite their universal occurrence, little is known about the evolutionary influence of maternal effects. Hinde et al. (p. 1373; see the cover) modeled maternal effects in birds and showed that nestling begging, as well as provoking feeding, also provides parents with information about offspring vigor. Conversely, maternal effects provide information to the unborn offspring about parental quality. Experimental studies with canaries provided support for the theoretical predictions, and together these studies show that parent-offspring conflict (that is, the conflict between the offspring for its immediate needs and the need of the parent to conserve resources for any future offspring) is resolved by the reciprocal exchange of information before and after birth. Hormonal signaling ensures a match between parental capacity for resource provisioning and offspring behavior and development after hatching that meet the mothers capacity to provide resources. Prenatal hormonal signaling can match a mother bird’s capacity to provide food with her offsprings’ expectations. The evolution of family life has traditionally been studied in parallel by behavioral ecologists and quantitative geneticists. The former focus on parent-offspring conflict and whether parents or offspring control provisioning, whereas the latter concentrate on the coadaptation of parental supply and offspring demand. Here we show how prenatal effects on offspring begging can link the two different approaches. Using theoretical and experimental analyses, we show that when offspring control provisioning, prenatal effects primarily serve the parent’s interests: Selection on parents drives coadaptation of parent and offspring traits. In contrast, when parents control provisioning, prenatal effects primarily serve the offspring’s interests: Selection on the offspring drives coadaptation of parent and offspring traits. Parent-offspring conflict may thus be responsible for the selective forces that generate parent-offspring coadaptation.

Conspicuous, ultraviolet-rich mouth colours in begging chicks

There is as yet no clear consensus on the function of vivid mouth colours in begging chicks. A major obstacle to our understanding has been that no studies have measured gape colours independently of human colour perception. Here, we present the first study, to our knowledge, to use UV-VIS spectrometry to quantify the gape colour, background nest colour and nest light environment of eight European passerines. Both mouths and the surrounding flanges show striking and previously unreported peaks of reflectance in the ultraviolet, coupled with high long-wavelength reflectance responsible for the human-visible appearance of the gape. High ultraviolet reflectance is likely to have an important effect on the conspicuousness of nestling mouths, since contrast with the nest background is maximal in the ultraviolet. Furthermore, the dual-peak nature of the spectra suggests that gapes are avian non-spectral colours analogous to human purple.

Visual mimicry of host nestlings by cuckoos

Coevolution between antagonistic species has produced instances of exquisite mimicry. Among brood-parasitic cuckoos, host defences have driven the evolution of mimetic eggs, but the evolutionary arms race was believed to be constrained from progressing to the chick stage, with cuckoo nestlings generally looking unlike host young. However, recent studies on bronze-cuckoos have confounded theoretical expectations by demonstrating cuckoo nestling rejection by hosts. Coevolutionary theory predicts reciprocal selection for visual mimicry of host young by cuckoos, although this has not been demonstrated previously. Here we show that, in the eyes of hosts, nestlings of three bronze-cuckoo species are striking visual mimics of the young of their morphologically diverse hosts, providing the first evidence that coevolution can select for visual mimicry of hosts in cuckoo chicks. Bronze-cuckoos resemble their own hosts more closely than other host species, but the accuracy of mimicry varies according to the diversity of hosts they exploit.