Equivocal Responses of Feeding Parents to Experimental Brood Sizes in a Hawk–Cuckoo Host: Brood Size as a Reference for Parental Provisioning Decisions?

The number of offspring surviving until independence is the fundamental drive in the evolution of parental care. Because of the related costs, parental investment must be balanced with essential resources for parents themselves, among the resources available in the environment under the current parental condition. It is advantageous for parents to adjust their level of investment to the number of offspring; however, there is little evidence that parents employ numerical competence in adjusting their investment level. We investigated how parents respond to experimentally manipulated brood sizes in a passerine species, known as a host of a brood parasitic cuckoo whose chicks presumably deceive their hosts numerically. Parents reduced their provisioning to broods of reduced sizes, whereas parents did not increase provisioning to enlarged broods compared to that in the control condition. These parental responses can be attributed to the response of chicks to the experimental treatments compared to that in the control: chicks lowered begging intensity in the reduced condition, while they did not intensify being in the enlarged condition. Further analyses revealed that eagerness of parents to respond to chick begging intensity differed between the experimental treatments: strong parental response was detected toward begging chicks only in the reduced condition. We propose that the detected equivocality of parental responses might be related to the difference in the number of chicks between the unmanipulated and experimentally manipulated broods, the former reflecting the initial parental decision on the amount of resources to allocate to the brood.     

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.     

Darwin's Finch Begging Intensity Does Not Honestly Signal Need in Parasitised Nests

Parental care should be selected to respond to honest cues that increase offspring survival. When offspring are parasitised, the parental food compensation hypothesis predicts that parents can provision extra food to compensate for energy loss due to parasitism. Chick begging behaviour is a possible mechanism to solicit increased feeding from attending parents. We experimentally manipulated parasite intensity from Philornis downsi in nests of Darwin's small ground finch (Geospiza fuliginosa) to test its effects on chick begging intensity and parental food provisioning. We used in‐nest video recordings of individually marked chicks to quantify nocturnal parasite feeding on chicks, subsequent diurnal chick begging intensity and parental feeding care. Our video analysis showed that one chick per brood had the highest parasite intensity during the night (supporting the tasty chick hypothesis) and weakest begging intensity during the day, which correlated with low parental care and rapid death. We observed sequential chick death on different days rather than total brood loss on a given day. Our within‐nest video images showed that (1) high nocturnal larval feeding correlated with low diurnal begging intensity and (2) parent birds ignored weakly begging chicks and provisioned strongly begging chicks. Excluding predation, all parasite‐free chicks survived (100% survival) and all parasitised chicks died in the nest (100% mortality). Weak begging intensity in parasitised chicks, which honestly signalled recent parasite attack, was not used as a cue for parental provisioning. Parents consistently responded to the strongest chick in both parasitised and parasite‐free nests.     

Individual benefits of nestling begging: experimental evidence for an immediate effect, but no evidence for a delayed effect

The evolutionary stability of honest signalling by offspring is thought to require that begging displays be costly, so the costs and benefits of begging--and whether they are experienced individually or by the whole brood--are crucial to understanding the evolution of begging behaviour. Begging is known to have immediate individual benefits (parents distribute more food to intensely begging individuals) and delayed brood benefits (parents increase provisioning rate to the brood), but the possibility of delayed individual benefits (previous begging affects the current distribution of food) has rarely, if ever, been researched. We did this using playback of great tit Parus major chick begging and a control sound from either side of the nest. Male parents fed chicks close to the speaker more when great tit chick begging, but not other stimuli, was played back. In contrast, there was no effect of playback at the previous visit on the chicks that male parents fed. We have thus demonstrated an immediate individual benefit to begging, but found no evidence of a delayed individual benefit in this species.     

Chick begging as a signal: are nestlings honest?

Begging by dependent avian offspring is known to correlate withhunger level, and parents use this as a signal of brood demandto adjust their chick feeding behavior. While there is informationon how each chick adjusts its begging to its own condition,little is known of how chicks adjust to the state of their nestmates. In two experiments we manipulated the competitive environmentof individual European starling (Sturnus vulgaris) chicks byaltering the state of nest mates while holding the state oftarget chicks constant In the first experiment we placed thetarget chick's nest mates in neighboring nests with brood sizesof two, five, or eight chicks. Following the manipulation wereturned them to their own nests and recorded begging behavioron videotape. In the second experiment we separated a targetchick from its siblings and manipulated feeding level in thelaboratory. The siblings were fed at one of three levels; meanwhile,all the target chicks were fed at the intermediate level. Afterthe manipulation we placed the target chicks with their siblingsand recorded their begging in response to an artificial stimulus.In neither experiment was the begging effort of the unmanipulatedtarget chicks affected by the changes in begging behavior oftheir siblings. This result supports the view that begging isa reliable signal of individual chick state and does not involveresponses to the effort of nest mates.     

European starling chicks benefit from high yolk testosterone levels during a drought year

Avian egg yolk contains androgenic hormones, such as testosterone, of maternal origin. Experimental elevation of yolk testosterone levels enhances growth of canary chicks. Success in sibling competition, due to increased begging, is presumed to underlie this growth enhancement, because canary hatchlings from testosterone-treated eggs beg longer in response to vibrational stimuli than controls. Furthermore, experimental elevation of both yolk androstenedione and testosterone increased chick growth and begging in black-headed gulls. We measured daily growth of European starling (Sturnus vulgaris) chicks hatching from testosterone-treated or vehicle-treated (control) eggs until 14 days of age, and measured begging behavior at hatching and at 5 days of age. A temporary drought caused relatively high levels of early brood reduction for this population; 2- and 3-day-old chicks were most likely to starve. We found that chicks from testosterone-treated eggs were less likely to starve than control chicks, and were heavier on the days when most brood reduction occurred. However, chicks from testosterone-treated eggs begged less than control chicks on the day of hatching, and begged similarly at 5 days of age. Thus, while yolk testosterone did increase growth during periods of (presumably) high competition, increased begging does not appear to mediate this effect. Instead, testosterone may induce more efficient energy use, for example, by decreasing ineffective begging. While our results indicate that elevated yolk testosterone enhances survival, and thus offspring and parental fitness, further evidence regarding the fitness consequences of yolk androgens are vital to understanding their role in avian life history.     

Differences in the nestling begging calls of hosts and host-races of the common cuckoo, Cuculus canorus

We compared nestling begging calls of four hosts (reed warbler, Acrocephalus scirpaceus; great reed warbler, A. arundinaceus; dunnock, Prunella modularis; and meadow pipit, Anthus pratensis) and the respective host-races of the common cuckoo. Note structure varied between host species, but not between cuckoo host-races, so cuckoos did not vary their call note structure to match that of their hosts' chicks. Call rate increased with age, but there were marked differences between both host species and cuckoo host-races. Dunnock-cuckoos called more rapidly than reed warbler-cuckoos despite growing at the same rate. We suggest this difference reflects how cuckoos tune into the way these host species respond to begging signals from their own young, because dunnock chicks called much more rapidly than reed warbler chicks. Great reed warbler-cuckoos called at a lower rate than reed warbler-cuckoos when young, but at a greater rate when older than 8 days. This could also result from the cuckoo chicks tuning into differences in the way these hosts respond to begging signals. However, great reed warbler-cuckoos grew at a faster rate than the other cuckoo host-races, so they may also call faster to demand higher provisioning rates from this larger host. To test these hypotheses critically, data are needed on how the different host species integrate visual and vocal begging signals from their own broods. We discuss how differences in cuckoo begging might develop, given that cuckoo host-races are restricted to female cuckoo lineages. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Effects of begging on growth rates of nestling chicks

We investigated whether an increase in begging levels delaysgrowth of chicks. In experiment 1, we hand-reared nine pairsof ring dove squabs, divided into a control and a begging group.All squabs received similar amounts of food, but those in thebegging group had to beg for a prolonged period in order tobe fed, while squabs in the control group received food withoutbegging. Squabs stopped responding to the treatment after 10days and, at that time, there was no effect of induced beggingon their body mass. In experiment 2, we hand-reared 27 pairsof magpie chicks for 3 days. The design of experiment 2 wassimilar to that of experiment 1. Daily food intake and beggingaffected growth rates. On average, chicks in the begging groupgrew 0.8 g/day less than control chicks, which represents adecrease of 8.15% in growth rate. Because growth is usuallypositively associated with expected fitness, this demonstratesthat begging is a costly behavior, an assumption routinelymade in models of begging behavior.     

Feeding experience and relative size modify the begging strategies of nestlings

The offspring of birds and mammals use a combination of movementsand vocalizations, known as begging, to solicit food from theirparents. A widespread interpretation of begging is that itconstitutes an honest signal of offspring need. But we knowthat in the house sparrow (Passer domesticus) the intensityof begging calls reflects the past experience of offspringin addition to their need. Here we show that this result generalizesto other species. An experiment with hand-reared magpies (Pica pica) and great spotted cuckoos (Clamator glandarius) indicates that the begging strategies depend on the past experience ofchicks and the composition of their brood. In asynchronoustwo-magpie broods, both chicks begged at the same intensitywhen the large chick obtained food more easily than its sibling,but the large chick begged at higher intensity when it was easier for the smaller chick to obtain food. Cuckoo chicks beggedat higher intensity than magpies.     

Sibling competition and siblicide in asynchronously-hatching broods of the cattle egret Bubulcus ibis

Feeding behaviour and sibling competition were observed in nine families of the cattle egret (Bubulcus ibis) from blinds during 1359 nest-h throughout the nestling period. During days 0–19, size differences among siblings were clear; begging behaviour of chicks changed with time. At least one parent always attended the nest. Food boluses regurgitated early within a feeding period were received by senior chicks more often than by juniors. When any two siblings begged for food at the same time, the elder and younger received the first bolus on 65% and 35% of occasions respectively. Between days 20 and 39, the frequency of begging reached a peak. Begging behaviour became intense and stereotyped. The number of boluses received per begging declined rapidly, especially for junior chicks. In large broods, the success rate of begging was lower and fights occurred among siblings, especially among juniors. Out of 256 dyadic fights, the elder sibling won 85, lost one, and tied 171. The youngest chick died in two broods, apparently as the result of these fights (siblicide). No parents interfered in fights among their offspring. After day 40, the frequency of begging decreased gradually and ceased by day 80, No chicks died in the last period, although the frequency of fights in all large broods remained high.     

Imperfect mimicry of host begging calls by a brood parasitic cuckoo: a cue for nestling rejection by hosts?

Coevolutionary interactions between avian brood parasites and their hosts often lead to the evolution of discrimination and rejection of parasite eggs or chicks by hosts based on visual cues, and the evolution of visual mimicry of host eggs or chicks by brood parasites. Hosts may also base rejection of brood parasite nestlings on vocal cues, which would in turn select for mimicry of host begging calls in brood parasite chicks. In cuckoos that exploit multiple hosts with different begging calls, call structure may be plastic, allowing nestlings to modify their calls to match those of their various hosts, or fixed, in which case we would predict either imperfect mimicry or divergence of the species into host-specific lineages. In our study of the little bronze-cuckoo (LBC) Chalcites minutillus and its primary host, the large-billed gerygone Gerygone magnirostris, we tested whether: (1) hosts use nestling vocalizations as a cue to discriminate cuckoo chicks; (2) cuckoo nestlings mimic the host begging calls throughout the nestling period; and (3) the cuckoo begging calls are plastic, thereby facilitating mimicry of the calls of different hosts. We found that the begging calls of LBCs are most similar to their gerygone hosts shortly after hatching (when rejection by hosts typically occurs) but become less similar as cuckoo chicks get older. Begging call structure may be used as a cue for rejection by hosts, and these results are consistent with gerygone defenses selecting for age-specific vocal mimicry in cuckoo chicks. We found no evidence that LBC begging calls were plastic.     

Responses of breeding Cory's shearwater Calonectris diomedea to experimental manipulation of chick condition

We studied the regulation of provisioning in Cory's shearwaterat Selvagem Grande during the chick rearing period. Provisioningwas examined in terms of feeding frequency and amount of fooddelivered to chicks. Two groups of chicks were subjected toshort-term contrasting manipulations of their nutritional status:one group of chicks was given a food supplement of about 30g, and another group was deprived of up to 30 g of food. Adultstending deprived chicks increased the frequency of feedingvisits (but not the size of feeds), which resulted in an increasein the net rate of food delivery. At the end of this study,deprived chicks were growing at the same rate as fed chicks. Parents attending fed chick did not change their provisioningrates in response to the treatment. Our results indicate thatCory's shearwaters are able to adjust their provisioning ratein response to short-term variation in the nutritional statusof their chicks. We also examined the change in the beggingrate of fed and deprived chicks in response to the treatment.There was no relationship between the begging rate and thecondition of chicks, which is taken to be a measure of thechick's physiological condition, related to its ability towithstand imposed periods of fasting. However, fed chicks decreasedtheir begging rate after the increase in their condition dueto supplementary food. Conversely, deprived chicks, which wereonly able to sustain their condition before the onset of thetreatment, maintained high levels of begging. To some extent,these results suggest that parental provisioning can be influencedby the begging behavior of chicks.     

Experimental evidence for offspring learning in parent-offspring communication

The offspring of birds and mammals solicit food from their parents by a combination of movements and vocalizations that have come to be known collectively as 'begging'. Recently, begging has most often been viewed as an honest signal of offspring need. Yet, if offspring learn to adjust their begging efforts to the level that rewards them most, begging intensities may also reflect offsprings' past experience rather than their precise current needs. Here we show that bird nestlings with equal levels of need can learn to beg at remarkably different levels. These experiments with hand-raised house sparrows (Passer domesticus) indicated that chicks learn to modify begging levels within a few hours. Moreover, we found that the begging postures of hungry chicks in natural nests are correlated with the average postures that had previously yielded them parental feedings. Such learning challenges parental ability to assess offspring needs and may require that, in response, parents somehow filter out learned differences in offspring signals.     

Food restricted Tufted Puffin (Fratercula cirrhata) nestlings increase vocal activity during handling without modulating total or free corticosterone

In some species, corticosterone (CORT) appears to play a role in the control of begging behavior. Because of the potentially high costs associated with chronic elevation of CORT, it has also been proposed as a mechanism to ensure begging is an honest signal. We determined the effects of moderate food restriction (50% of high calorie treatment) on vocal behavior during handling, and on baseline levels of both total and ‘free’ unbound CORT in Tufted Puffin (Fratercula cirrhata) nestlings. Chick vocalizations during handling were similar to begging calls, and we assumed they were representative of begging behavior. We also measured total and free CORT in free-living Tufted Puffin chicks to determine if hormone levels in our experiment were comparable to natural levels. We found no effect of caloric restriction on either total or free baseline CORT, yet food-restricted nestlings vocalized more intensely during handling than chicks in the high calorie group. Mean plasma concentrations of total and free CORT in experimentally manipulated birds did not differ from levels in free-living nestlings. These results suggest that CORT does not play a role in modulating begging behavior in this species.     

Nestling competition,rather than supernormal stimulus,explains the success of parasitic brown-headed cowbird chicks in yellow warbler nests

Interspecific parasitic chicks are usually fed more than the smaller host young with whom they share the nest. This could be due to parasitic chicks having evolved exaggerated features that are preferred by the adults to the features present in their own young (the supernormal stimulus hypothesis). Alternatively, the success of parasitic chicks could be due to them being better competitors. We tested these hypotheses by studying the interaction between brown-headed cowbird chicks, Molothrus ater, and a common small host, the yellow warbler, Dendroica petechia. Parasitic chicks begged more intensively than the host''s young and received most of the feeds. The relative height reached by the begging chicks of both species was the most important variable in determining their feeding success. Being larger and begging intensively, brown-headed cowbirds were better able to reach higher than the host''s young, but at equal heights parasitic chicks were no better than the host''s young at gaining feeds. It is suggested that the success of the brown-headed cowbirds when parasitizing yellow warblers is due to them physically out-competing the smaller young of their hosts, and not to them evoking a stronger response from the hosts by being a supernormal stimulus.     

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.     

An immunological cost of begging in house sparrow nestlings

Parent–offspring conflict predicts that offspring should demand a greater parental investment than is optimal for their parents to deliver. This would escalate the level of offspring demand ad infinitum, but most of the models on the evolution of parent–offspring communication predict that begging must be costly, such costs limiting the escalation and defining an optimal level of begging. However, empirical evidence on this issue is mixed. A potential begging cost that remains to be accurately explored is a decrease in immunocompetence for offspring begging fiercely. This study experimentally analyses this cost in house sparrow (Passer domesticus) nestlings. A group of nestlings was forced to beg fiercely for a prolonged time while a control group begged at low levels, both groups receiving the same quantity of food. At the same time, the nestling response to an antigen (phytohaemagglutinin) was measured. Nestlings forced to beg fiercely showed a reduction in immunocompetence with respect to control chicks, but the two groups showed no difference in growth rate. The largest and the smallest nestlings in each brood showed a similar response to the treatment. These results strongly suggest a trade-off between begging and immunocompetence in this species. This trade-off may be a consequence either of resources from the immune system being reallocated to begging behaviour, or of adaptive immunosuppression in order to avoid oxidative stress. Steroid hormones are proposed as mediators of such a trade-off.     

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.     

Wing-shaking and wing-patch as nestling begging strategies: their importance and evolutionary origins

Avian chicks use different begging strategies when soliciting parental care. A novel begging strategy was recently observed in Horsfield’s hawk-cuckoo Hierococcyx hyperythrus (=Cuculus fugax). Chicks of this brood-parasitic species raise and shake their wings and display to fosterers a gape-coloured patch on the undersides of their wings. Although the gape-coloured wing-patch may be a unique trait of Horsfield’s hawk-cuckoo, wing-shaking in the context of begging is virtually universal in both brood parasites and their hosts. A simple qualitative comparison across different avian taxa suggests that wing-shake begging is most probably an ancestral feature of cuckoos and perhaps all altricial birds. The wing-shaking may be an honest signal of chick quality. It could also reduce the risk of predation if wing-shaking was coupled with reduced loudness of begging. Horsfield’s hawk-cuckoo chicks could have exploited the universal pre-existing host responsiveness to wing-shake begging. Evolution could have then further proceeded by making the wing-shaking more conspicuous by addition of another stimulus—the unique colourful wing-patch. I also hypothesize that wing-shake begging may have evolved from pre-fledging restlessness and is used secondarily in courtship displays, threatening postures, and distraction displays by adults. Further discussions and tests of these hypotheses may facilitate research into the so far unstudied phylogenetic history of avian chick-begging strategies. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Nest‐dwelling ectoparasites reduce begging effort in Pied Flycatcher Ficedula hypoleuca nestlings

Parasitized nestlings might be expected to increase begging effort to obtain additional resources to compensate for those sequestered by their parasites. However, begging is costly and chicks harbouring parasites may find it more difficult to attain high begging levels. Consequently, we predicted that, for the same level of nutritional need, nestlings that are parasitized will invest less in begging than those that are not parasitized. We tested this prediction by measuring begging in Pied Flycatcher Ficedula hypoleuca nestlings parasitized with haematophagous mites Dermanyssus gallinoides and Dermanyssus gallinae and blowfly larvae Protocalliphora azurea, and subjected to different levels of food deprivation in order to control for short‐term nutritional need. Nestlings from nests with ectoparasites spent less time begging than those from nests without parasites, especially when very hungry, although there was no association with latency to beg or begging intensity. Our results suggest that time invested in begging may indicate not only the level of need, but also nestling parasitism status.