Reliable Information Content and Ontogenetic Shift in Begging Calls of Grey Warbler Nestlings

The most critical assumption of communication models regarding parent–offspring conflict is that food solicitation displays of genetic offspring are honest signals to elicit beneficial parental care. A critical requirement of honesty is the reliable change of perceivable aspects of begging calls with physiological needs. We experimentally tested whether and how the acoustic structure and begging call rate of individual Grey Warbler Gerygone igata nestlings change with hunger level and age. We also examined a rarely documented component of chick begging calls, namely the temporal dynamics of acoustic modulation after nestlings heard parental feeding calls. Begging call structure narrowed in frequency range and, surprisingly, decreased in amplitude as chick hunger levels increased. We also found that begging calls changed with chick age, with the frequency increasing and the duration decreasing for older chicks. These results indicate that the acoustic properties of nestling Grey Warbler begging calls are complex and may be used to signal several aspects of nestling traits, including hunger level and age (or size, a correlate of age). Overall, begging calls of Grey Warbler chicks appear to be honest, implying that parents are likely to benefit from relying on the acoustic features of their progeny’s calls which predict chick need. Our results have important implications regarding the reliability and information content of nestling solicitation signals for the brood parasite shining cuckoo Chrysococcyx lucidus exploiting Grey Warbler parental care, in that these begging‐call mimetic specialist cuckoos might also need to match closely the dynamics of acoustic features of their host chicks’ calls.     

Acoustic signalling of hunger and thermal state by nestling tree swallows

The begging displays used by altricial nestling birds to solicit care from parents include vigorous movements and loud calling. These begging signals have attracted considerable interest, mainly because their intensity seems excessive for the function of transmitting information about nestling need to parents. However, how information on need is encoded in the various components of the signal, especially its acoustic components, is poorly understood. We examined how begging calls of large and small nestling tree swallows, Tachycineta bicolor, changed during a short period of food deprivation and cooling, as a first step in determining the role that various call characteristics played in advertising nestling need. In contrast to previous studies, we examined several call variables, and related them not only to need for food but also need for warmth. When nestlings were deprived of food, their calls increased in rate and length. Large nestlings also increased the amplitude of their calls. When nestlings were cooled during food deprivation, they decreased the frequency of their calls and their call rate. The latter trend was especially evident in small nestlings. Our results suggest that begging calls carry information not only on the overall hunger level of broods, as emphasized in previous studies, but also on the size, hunger and thermal need of individual nestlings. Further tests are needed to determine whether parents use this information and whether begging calls are optimally designed to convey it. Copyright 2001 The Association for the Study of Animal Behaviour.     

Begging in the absence of sibling competition in Wilson’s storm-petrels, Oceanites oceanicus

Begging displays of nestlings in multichick broods can signal both hunger and competitive ability. Studies of begging in species with single-chick broods exclude the influence of nestling competition and may provide especially useful models for the study of signalling during parent-offspring conflict. However, there is no evidence that chicks signal hunger by begging in the absence of sibling competition. I tested predictions of signalling models in a species with single-chick broods, the Wilson's storm-petrel. Chicks used two types of begging calls, ‘rhythmic’ calls and ‘long’ calls. I found that chicks conveyed information about their current body condition by begging. When their body condition was low, chicks increased the number and frequency of long begging calls, as well as the frequency of rhythmic calling. Parents responded to increased begging by regurgitating larger meals. The study thus demonstrates that the begging system can work in the absence of nestling competition. Chicks also called in the absence of their parents, but in this context they used only rhythmic calls and there was no correlation with current body condition. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Begging and cowbirds: brood parasites make hosts scream louder

Avian brood parasites have evolved striking begging abilitythat often allows them to prevail over the host progeny in competitionfor parental resources. Host young are therefore selected bybrood parasites to evolve behavioral strategies that reducethe cost of parasitism. We tested the prediction that the intensityof nestling begging displays functioning to attract parentalcare increases across species with the frequency of parasitismby the brown-headed cowbird (Molothrus ater). This was expectedbecause host young should try to prevail over highly competitiveparasitic broodmates in scramble interactions, act more selfishlywhen frequency of parasitism is high because brood parasitesoften affect more severely host condition than conspecific broodmates,and discount the kin selection costs of subtracting resourcesto unrelated parasites. Across 31 North American host species,begging loudness positively covaried with parasitism rate inPasserines, and such effect was stronger in species with smallcompared with large clutches. Begging loudness increased withbrood parasitism and nest predation among the most suitablehost species. These results held after controlling for concomitantecological factors and for common ancestry effects. Our resultssupport the hypothesis that avian brood parasitism has playeda role in the evolution of begging behavior of host young.     

Oxidative stress mediates physiological costs of begging in magpie (Pica pica) nestlings

Background

Theoretical models predict that a cost is necessary to guarantee honesty in begging displays given by offspring to solicit food from their parents. There is evidence for begging costs in the form of a reduced growth rate and immunocompetence. Moreover, begging implies vigorous physical activity and attentiveness, which should increase metabolism and thus the releasing of pro-oxidant substances. Consequently, we predict that soliciting offspring incur a cost in terms of oxidative stress, and growth rate and immune response (processes that generate pro-oxidants substances) are reduced in order to maintain oxidative balance.

Methodology/Principal Findings

We test whether magpie (Pica pica) nestlings incur a cost in terms of oxidative stress when experimentally forced to beg intensively, and whether oxidative balance is maintained by reducing growth rate and immune response. Our results show that begging provokes oxidative stress, and that nestlings begging for longer bouts reduce growth and immune response, thereby maintaining their oxidative status.

Conclusions/Significance

These findings help explaining the physiological link between begging and its associated growth and immunocompetence costs, which seems to be mediated by oxidative stress. Our study is a unique example of the complex relationships between the intensity of a communicative display (begging), oxidative stress, and life-history traits directly linked to viability.     

Age-Related Changes in Signalling of Need by Nestling Tree Swallows (Tachycineta bicolor)

Despite a large literature on the ontogeny of behaviour, few studies have examined how the function of juvenile behaviour changes during development. One of the most widespread and important juvenile behaviours is begging, the display used by young animals to solicit food from their parents. Begging signals generally vary reliably with offspring need for food and have served as models for understanding the evolution of honest signalling. Little is known, however, about whether the relationship between begging and need varies over the period of rapid juvenile development. Here, we examine whether tree swallow, Tachycineta bicolor, begging calls consistently reflect hunger levels across the 20 d nestling period. We recorded begging calls at 5, 10 and 15 d post‐hatch, during an hour of food deprivation, and related call features to time without food (i.e. hunger) at each age. The overall correlation between call structure and hunger, as measured by canonical correlation, was consistent across ages. The particular features that correlated with hunger varied, however. Call rate and length increased with hunger at all ages, but call amplitude and frequency range increased with hunger at days 10 and 15 only. The results of our study suggest that begging calls consistently convey information about offspring hunger throughout the nestling period, with the number of call features encoding hunger increasing with nestling age. This change may enhance the ability of parents to assess offspring hunger levels by adding redundancy to the signal.     

Are acoustical parameters of begging call elements of thin-billed prions related to chick condition?

Chicks of burrowing petrels use begging calls to advertise their hunger levels when parents arrived at the nest. In a previous study, adult thin-billed prions Pachyptila belcheri responded to higher begging call rates of their single chick by regurgitating larger meals. We tested whether acoustic parameters of begging call elements may also be involved in signalling. To describe variation in begging, we determined begging session parameters, namely the duration, number of calls and the mean and maximum rate of calling. We then digitised calls and carried out a semi-automatic extraction of six acoustic parameters of call elements, including mean and maximum acoustic frequency, the length of call elements and the location of the maximum frequency and amplitude within calls. Chicks showed strong individual differences in all parameters. While the session parameters were correlated with body condition and with the meal size the chick received, none of the acoustic parameters were related to body condition and provisioning. A cross-fostering experiment showed the same pattern, as only session parameters changed related to an experimentally altered body condition, while acoustical cues appear to play no role in signalling hunger levels. We suggest that this may be explained by the absence of sibling competition in these birds. As parents do not need to decide which chick to feed, immediate information on condition at the time of adult arrival may not be required.     

Hopeless solicitation? Host-absent vocalization in the common cuckoo has no effect on feeding rate of reed warblers

Begging behavior of nestlings can signal both hunger and competitive ability. Studies of begging in evicting avian brood parasites exclude the influence of nestling competition and may provide new insights into the host–parasite conflict and the evolution of signaling. Apart from the begging call, common cuckoo Cuculus canorus nestlings use special vocal displays in the absence of their hosts, termed here host-absent vocalization (HAV). Since these conspicuous calls can increase the risk of predation and require energy, their costs should be balanced by some benefits, such as increased food provisioning. However, there has been no evidence that chicks convey information about their hunger by HAV. We therefore tested experimentally whether cuckoo chicks use HAV as an additional signal to enhance food-delivery rate by their hosts. We used playback of HAV recorded from cuckoo nestlings to determine whether their hosts, reed warblers Acrocephalus scirpaceus, increase their provisioning in response to an apparent increase in HAV. Older chicks spent more time in HAV than younger chicks, suggesting that HAV is not caused by inaccurate discrimination of host arrival stimuli. Negative correlation of HAV with feeding rate and mass gain between the two experiments suggested that hunger was the motivation of HAV. The playback experiment, however, did not prove that HAV affects host provisioning rate. We discuss possible reasons for this result and provide alternative explanations for HAV, such as creating a bond between the hosts and the parasitic young used later in the postfledging care.     

IBERIAN AZURE-WINGED MAGPIE CYANOPICA (CYANA) COOKI NESTLINGS BEGGING CALLS: CALL CHARACTERIZATION AND HUNGER SIGNALLING

ABSTRACT

Nestling begging behaviour has long been seen as a signal by which nestlings solicit care from parents and most of the existing evidence provides some support for it being an honest signal. Begging is a multicomponent signal in which both sound and vision components are usually important. Although it is known that begging encodes information about nestling hunger the present knowledge about the specific behavioural features that convey the information is still scarce. The aim of this study was to describe begging calls of Iberian Azure-winged Magpie Cyanopica (cyana) cooki nestlings and examine how information on nestling hunger might be encoded in the begging calls. Nestlings were experimentally submitted to different periods of food deprivation and the call variation within individuals was studied. The young were individually tested and stimulated to beg by simulating parental visits. When subject to increasing food deprivation periods, nestlings increased the response level to simulated parental visits. The study also found that for the studied size differences, nestlings did not differ in their response level. Results confirmed that information on nestlings' hunger might be encoded in parameters of the calling behaviour. When the food deprivation periods increased, nestlings tended to start begging earlier, begged more often, extended their calling bout and increased the call duration, changing both at the level of the call and vocal begging bout. Overall the results support the view of begging as an honest signal, namely that begging should reflect nestling hunger and that only some call features might encode information about hunger.     

Condition-dependent effects of corticosterone on a carotenoid-based begging signal in house sparrows

Begging is a complex display involving a variety of different visual and auditory signals. Parents are thought to use these signals to adjust their investment in food provisioning. The mechanisms that ensure the honesty of begging displays as indicators of need have been recently investigated. It has been shown that levels of corticosterone (Cort), the hormone released during the stress response, increase during food shortage and are associated with an increased begging rate. In a recent study in house sparrows, although exogenous Cort increased begging rate, parents did not accordingly adjust their provisioning rate. Here, we tested the hypothesis that Cort might affect the expression of other components of begging displays, such as flange color (a carotenoid-based trait). We experimentally increased levels of circulating Cort and investigated the effects of the treatment on (1) the flange coloration of the nestlings, (2) the behavioral response and (3) the parental allocation of food and (4) nestling condition and cell-mediated immune response. We found that Cort affected flange coloration in a condition-dependent way. Cort-injected nestlings had less yellow flanges than controls only when in poor body condition. Parental feeding rate was also affected by the Cort treatment in interaction with flange color. Feeding rate of Cort-injected nestlings was negatively and significantly correlated with flange color (nestlings with yellower flanges receiving more food), whereas feeding rate and flange color were not correlated in control chicks. We also found that nestlings injected with Cort showed a weaker immune response than controls. These results suggest that, indeed, Cort has the potential to affect multiple components of the begging display. As Cort levels naturally raise during fasting, parents have to take into account these multiple components to take a decision as to optimally share their investment among competing nestlings.     

Vocal matching and intensity of begging calls are associated with a forebrain song circuit in a generalist brood parasite

Vocalizations produced by developing young early in life have simple acoustic features and are thought to be innate. Complex forms of early vocal learning are less likely to evolve in young altricial songbirds because the forebrain vocal‐learning circuit is underdeveloped during the period when early vocalizations are produced. However, selective pressure experienced in early postnatal life may lead to early vocal learning that is likely controlled by a simpler brain circuit. We found the food begging calls produced by fledglings of the brown‐headed cowbird (Molothrus ater), a generalist avian brood parasite, induced the expression of several immediate early genes and early circuit innervation in a forebrain vocal‐motor pathway that is later used for vocal imitation. The forebrain neural activity was correlated with vocal intensity and variability of begging calls that appears to allow cowbirds to vocally match host nestmates. The begging‐induced forebrain circuits we observed in fledgling cowbirds were not detected in nonparasitic passerines, including species that are close relatives to the cowbird. The involvement of forebrain vocal circuits during fledgling begging and its association with vocal learning plasticity may be an adaptation that provides young generalist brood parasites with a flexible signaling strategy to procure food from a wide range of heterospecific host parents. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 615–625, 2016     

Innate development of acoustic signals for host parent–offspring recognition in the brood‐parasitic Screaming Cowbird Molothrus rufoaxillaris

Young birds communicate their need to parents through complex begging displays that include visual and acoustic cues. Nestlings of interspecific brood parasites must ‘tune’ into these communication channels to secure parental care from their hosts. Various studies show that parasitic nestlings can effectively manipulate host parental behaviour through their begging calls, but how these manipulative acoustic signals develop in growing parasites remains poorly understood. We investigated the influence of social experience on begging call development in a host‐specialist brood parasite, the Screaming Cowbird Molothrus rufoaxillaris. Screaming Cowbird nestlings look and sound similar to those of the primary host, the Greyish Baywing Agelaioides badius. This resemblance is likely to be adaptive because Baywings discriminate against fledglings unlike their own and provision nests at higher rates in response to Baywing‐like begging calls than to non‐mimetic begging calls. By means of cross‐fostering and playback experiments, we tested whether the acoustic cues that elicit recognition by Baywings develop innately in Screaming Cowbird nestlings or are acquired through social experience with host parents or nest mates. Our results suggest that begging call structure was partially modulated by experience because Baywing‐reared Screaming Cowbird and host nestlings were acoustically more similar as age increased, whereas acoustic similarity between cross‐fostered and Baywing‐reared Screaming Cowbird nestlings decreased from 4–5 to 8–10 days of age. Cross‐fostered Screaming Cowbirds developed begging calls of lower minimum frequency and broader bandwidth than those of Baywing‐reared Screaming Cowbirds by the age of 8–10 days. Despite the observed differences in begging call structure, however, adult Baywings responded similarly to begging calls of 8‐ to 10‐day‐old cross‐fostered and Baywing‐reared Screaming Cowbirds, suggesting that these were functionally equivalent from the host's perspective. These findings support the idea that, although rearing environment can influence certain begging call parameters, the acoustic cues that serve for offspring recognition by Baywings develop in young Screaming Cowbirds independently of social experience.     

Signalling of Nutritional Need by Magpie Nestlings

The relationship between begging behaviour, chick nutritional state, and parental distribution of food within broods was studied in 4- and 5-chick magpie Pica pica broods under natural conditions. Three components of the begging display (duration, latency, and posture) were highly correlated with each other and also with the emission and duration of begging calls. Begging performance was strongly influenced by the food intake of nestlings during the preceding 1-h interval, indicating that begging may reliably reflect the nutritional need of nestlings. Daily growth during the preceding day, as well as average cumulative food intake by the brood during the preceding 24 h, seemed not to affect begging in a similar way. Begging signals employed by hungrier nestlings involved a higher degree of muscular activity, thus supporting the prediction that nestlings in greater need should employ more costly signals. Overall, those nestlings who begged more tended to obtain more food, but the relationship between feeding success and begging behaviour was weak due to a high variation between broods in the way that parents seemed to respond to variations in begging behaviour. Possible causes for this variation, and its implications for the evolution of reliable begging displays, are discussed.     

Parental Distribution of Resources in Relation to Larval Hunger and Size Rank in the Burying Beetle Nicrophorus vespilloides

In altricial birds, the parents' distribution of resources within the brood is influenced by variation in at least two components of nestling condition: hunger level and size rank. Here, we examine whether variation in larval hunger and size rank had similar influences on the parents' distribution of resources in the burying beetle Nicrophorus vespilloides . To this end, we analyzed hitherto unpublished data on parental resource distribution among individual larvae derived from three previous experiments. Our first experiment showed that resource distribution was biased towards hungry larvae at the expense of control larvae, but that actively begging hungry larvae were as likely to obtain resources from parents as actively begging control larvae. Thus, resource distribution was biased towards hungry larvae because hungry larvae spent more time begging than control larvae. Our second experiment showed that actively begging senior larvae (i.e. larvae that were older and larger) were more likely to obtain resources than actively begging junior larvae, suggesting that senior larvae had a competitive advantage or were treated preferentially by the parents. Our third experiment found no evidence that the interaction between larval hunger and size rank had an effect on parental resource distribution, suggesting that hunger level had a similar effect on resource distribution to seniors and juniors. We conclude that offspring hunger and size rank have remarkably similar effects in the burying beetle N. vespilloides as reported in studies on altricial birds.     

Parent-offspring conflict and the coordination of siblings in gulls

Offspring solicit food from their parents by begging behaviours. Studies on birds suggest that these displays are 'honest signals of need' and adults provide food according to the begging level. However, siblings may compete for parental resources and the begging intensity is expected to change with brood size. Here, we show that in the black-headed gull (Larus ridibundus) an increase of the numbers of siblings can result in a decrease of individual begging cost through nestlings' synchronized signalling. This is in accordance with some mathematical models. As parents respond to the total solicitation emerging from the nest, the probability to get food increases with the number of chicks begging together. The more siblings there are, the more they coordinate their begging while decreasing the number of individual begging bouts. Intra-brood synchronization of begging enables chicks to reduce their effort and hence exerting an important role in parental-offspring negotiation.     

Calling at a cost: elevated nestling calling attracts predators to active nests

Begging by nestling birds has been used to test evolutionary models of signalling but theory has outstripped evidence. Eavesdropping predators potentially impose a cost on begging that ensures signal honesty, yet little experimental evidence exists for such a cost at active nests because the use of artificial nests, long playback bouts and absence of parents may have exaggerated costs. We broadcast short periods (1 h) of either nestling vocalizations or background noise at active white-browed scrubwren, Sericornis frontalis, nests. Nestlings called naturally during both treatments, allowing us to test whether elevated calling increases risk, a key but rarely tested assumption of evolutionary models. Predators visited nests exclusively during periods of elevated calling. Furthermore, playbacks affected neither adult visits nor nestling activity, suggesting that calling alone attracted predators. Adults gave alarm calls and nestlings usually called less when predators approached nests. Predation risk to broods is, therefore, likely to fluctuate substantially over short periods of time, depending on nestling hunger and whether adults or young have detected predators. This study confirms a present-day cost of nestling begging, demonstrates that this cost can be incurred over short periods and supports the importance of parent-offspring antipredator strategies in reducing predation risk.     

Birth order, individual sex and sex of competitors determine the outcome of conflict among siblings over parental care

Success in competition for limiting parental resources depends on the interplay between parental decisions over allocation of care and offspring traits. Birth order, individual sex and sex of competing siblings are major candidates as determinants of success in sib-sib competition, but experimental studies focusing on the combined effect of these factors on parent-offspring communication and within-brood competitive dynamics are rare. Here, we assessed individual food intake and body mass gain during feeding trials in barn swallow chicks differing for seniority and sex, and compared the intensity of their acoustic and postural solicitation (begging) displays. Begging intensity and success in competition depended on seniority in combination with individual sex and sex of the opponent. Junior chicks begged more than seniors, independently of satiation level (which was also experimentally manipulated), and obtained greater access to food. Females were generally weaker competitors than males. Individual sex and sex of the opponent also affected duration of begging bouts. Present results thus show that competition with siblings can make the rearing environment variably harsh for developing chicks, depending on individual sex, sex of competing broodmates and age ranking within the nest. They also suggest that parental decisions on the allocation of care and response of kin to signalling siblings may further contribute to the outcome of sibling competition.     

Signalling of hunger when offspring forage by both begging and self-feeding

Studies on vertebrate species in which the offspring obtain food only from their parents have shown that offspring begging conveys information on offspring hunger. It is unclear whether begging can also convey information on hunger in partially begging species, in which the offspring, from hatching, obtain food partly through begging for food from the parents and partly through self-feeding. In partially begging species, offspring hunger state could reflect the amount of food obtained by self-feeding in addition to the amount obtained from the parent, and the offspring could respond to hunger by self-feeding instead of begging. To test whether begging reflected the current hunger state of offspring in the partially begging beetle Nicrophorus vespilloides, we subjected larvae to two deprivation treatments: no access to any food for 2 h (i.e. food-deprived larvae) and no food provided by the parent (i.e. self-feeding larvae). Larvae of both treatments spent more time begging than did control larvae, which had access to food both from the parents and by self-feeding. Furthermore, the amount of begging differed between the treatments, with food-deprived larvae spending more time begging than the self-feeding ones. We conclude that, in partially begging species, food obtained through both foraging strategies, i.e. begging for food from parents and self-feeding, contribute to the offspring's current hunger state, and that begging can convey information about it.     

Host–parasite coevolution beyond the nestling stage? Mimicry of host fledglings by the specialist screaming cowbird

Egg mimicry by obligate avian brood parasites and host rejection of non-mimetic eggs are well-known textbook examples of host-parasite coevolution. By contrast, reciprocal adaptations and counteradaptations beyond the egg stage in brood parasites and their hosts have received less attention. The screaming cowbird (Molothrus rufoaxillaris) is a specialist obligate brood parasite whose fledglings look identical to those of its primary host, the baywing (Agelaioides badius). Such a resemblance has been proposed as an adaptation in response to host discrimination against odd-looking young, but evidence supporting this idea is scarce. Here, we examined this hypothesis by comparing the survival rates of young screaming cowbirds and non-mimetic shiny cowbirds (Molothrus bonariensis) cross-fostered to baywing nests and quantifying the similarity in plumage colour and begging calls between host and cowbird fledglings. Shiny cowbirds suffered higher post-fledging mortality rates (83%) than screaming cowbirds (0%) owing to host rejection. Visual modelling revealed that screaming cowbirds, but not shiny cowbirds, were indistinguishable from host young in plumage colour. Similarly, screaming cowbirds matched baywings' begging calls more closely than shiny cowbirds. Our results strongly support the occurrence of host fledgling mimicry in screaming cowbirds and suggest a role of visual and vocal cues in fledgling discrimination by baywings.     

Stimuli for nestling begging in blue tits Cyanistes caeruleus: hungry nestlings are less discriminating

In altricial birds, nestlings usually respond to the sound and appearance of the provisioning adults by begging for food when the adults arrive at the nest. Nestlings can, however, also beg incorrectly on hearing misleading sounds in the environment and fail to beg when the adult arrives. This study uses the blue tit Cyanistes caeruleus to test the hypotheses that nestling begging strategies are influenced by the reliability of the stimulus to beg, and that nestling motivational state affects the response to different stimuli. Here, we show experimentally that nestling hunger strongly influences the response to stimuli that vary in their reliability. While hunger increases begging rate, it also increases the likelihood that nestlings will beg when the parent is absent. This is in agreement with both the predictions of signal detection theory and recent empirical work on other species. We found, however, no evidence that age-related perceptual constraints influence the begging response of ten day old nestlings to different stimuli.