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.     

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.     

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.     

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.     

Great spotted cuckoos respond earlier to the arrival of feeding foster parents and perform less erroneous begging when hungry than their magpie host nest‐mates

In many bird species, parents usually feed the first nestling that starts to beg before its nest‐mates. The pressure to avoid missed feeds could trigger nestlings to perform in erroneous begging in absence of parents, which has the same costs as begging in the presence of parents but without any reward. So, nestlings should try to minimize both erroneous begging and missed feeds simultaneously. The threshold to start begging is predicted to be lower for hungry nestlings and for nestlings that are unrelated to their nest‐mates, because they suffer lower inclusive fitness costs when depriving nest‐mates of food. In line with this idea, we found that brood parasitic great spotted cuckoo nestlings responded sooner than their magpie nest‐mates when an adult arrived to the nest. Under laboratory conditions, nestlings of both species rarely incurred in erroneous begging when food was abundant, but under conditions of restricted food, magpie nestlings increased erroneous begging while cuckoo nestlings did not. Highly conspicuous begging in cuckoos results in an increased predation risk, which could have resulted in stronger selection pressures on cuckoos to avoid erroneous begging, probably resulting in better developed perceptual abilities, allowing cuckoos to perform better than their host nest‐mates.     

Begging to differ: scrubwren nestlings beg to alarm calls and vocalize when parents are absent

Nestling birds face a dilemma: they can increase parental provisioning by begging more intensively, but by doing so may also increase their risk of predation. Nestlings could deal with this dilemma by reducing begging intensity after parents have warned them of a nearby predator. We therefore tested experimentally whether nestling scrubwrens, Sericornis frontalis, increase begging intensity with hunger but reduce it after adult alarm calls. Single 5- and 8-day-old nestlings were temporarily taken into the laboratory for playback experiments. Over a 90-min period of food deprivation we simulated parental visits every 10 min by playing back adult feeding calls. Hungrier nestlings begged louder and longer to simulated parental visits, but contrary to expectation did not beg less if they had previously heard playback of alarm calls, and even begged to the alarm calls themselves. The results were similar for both ‘mobbing’ and ‘flee’ alarm calls. Nestlings also gave distinctive calls in the 10-min interval between simulated parental visits, and the number of these calls increased with hunger and after playback of alarm calls. We suggest that nestlings acquire the ability to respond appropriately to alarm calls late in the nestling period and that therefore parents might be selected to avoid alarm calling when defending young nestlings.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Relative performance of hybrid nestlings in Ficedula flycatchers: a translocation experiment

Ecological speciation predicts that hybrids should experience relatively low fitness in the local environments of their parental species. In this study, we performed a translocation experiment of nestling hybrids between collared and pied flycatchers into the nests of conspecific pairs of their parental species. Our aim was to compare the performance of hybrids with purebred nestlings. Nestling collared flycatchers are known to beg and grow faster than nestling pied flycatchers under favorable conditions, but to experience higher mortality than nestling pied flycatchers under food limitation. The experiment was performed relatively late in the breeding season when food is limited. If hybrid nestlings have an intermediate growth potential and begging intensity, we expected them to beg and grow faster, but also to experience lower survival than pied flycatchers. In comparison with nestling collared flycatchers, we expected them to beg and grow slower, but to survive better. We found that nestling collared flycatchers indeed begged significantly faster and experienced higher mortality than nestling hybrids. Moreover, nestling hybrids had higher weight and tended to beg faster than nestling pied flycatchers, but we did not detect a difference in survival between the latter two groups of nestlings. We conclude that hybrid Ficedula nestlings appear to have a better intrinsic adaptation to food limitation late in the breeding season compared with nestling collared flycatchers. We discuss possible implications for gene flow between the two species.     

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.     

Barn owl (Tyto alba) siblings vocally negotiate resources

Current theory proposes that nestlings beg to signal hunger level to parents honestly, or that siblings compete by escalating begging to attract the attention of parents. Although begging is assumed to be directed at parents, barn owl (Tyto alba) nestlings vocalize in the presence but also in the absence of the parents. Applying the theory of asymmetrical contests we experimentally tested three predictions of the novel hypothesis that in the absence of the parents siblings vocally settle contests over prey items to be delivered next by a parent. This 'sibling negotiation hypothesis' proposes that offspring use each others' begging vocalization as a source of information about their relative willingness to contest the next prey item delivered. In line with the hypothesis we found that (i) a nestling barn owl refrains from vocalization when a rival is more hungry, but (ii) escalates once the rival has been fed by a parent, and (iii) nestlings refrain from and escalate vocalization in experimentally enlarged and reduced broods, respectively. Thus, when parents are not at the nest a nestling vocally refrains when the value of the next delivered prey item will be higher for its nest-mates. These findings are the exact opposite of what current models predict for begging calls produced in the presence of the parents.     

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.     

Benefits of Extra Begging Fail to Compensate for Immunological Costs in Southern Shrike (Lanius meridionalis) Nestlings

Theoretical models aimed at explaining the evolution of honest, informative begging signals employed by nestling birds to solicit food from their parents, require that dishonest signalers incur a net viability cost in order to prevent runaway escalation of signal intensity over evolutionary time. Previous attempts to determine such a cost empirically have identified two candidate physiological costs associated with exaggerated begging: a growth and an immunological cost. However, they failed to take into account the fact that those costs are potentially offset by the fact that nestlings that invest more in begging are also likely to obtain more food. In this study, we test experimentally whether a 25% increase in ingested food compensates for growth and immunological costs of extra begging in southern shrike (Lanius meridionalis) nestlings. Three nestmates matched by size were given three treatments: low begging, high begging-same food intake, and high begging-extra food intake. We found that, while a higher food intake did effectively compensate for the growth cost, it failed to compensate for the immunological cost, measured as T-cell mediated immune response against an innocuous mitogen. Thus, we show for the first time that escalated begging has an associated physiological net cost likely to affect nestling survival negatively.     

Dark nests and conspicuousness in color patterns of nestlings of altricial birds

Nests of altricial birds exhibit variable spectral properties that may affect the efficacy (conspicuousness) of the colored begging traits that a nestling displays to its parents. Here we explored whether selection for efficient perception has favored the evolution of nestling color designs that maximizes nestling detectability in variable light environments. Visual models were used to estimate how parents perceive the coloration of mouths, flanges, heads, and breasts of nestlings within their nest in 21 species of European birds. We show that the largest chromatic and achromatic contrasts against the nest background appeared for nestling mouths and flanges, respectively. Nestlings of open-nesting species showed a larger general achromatic contrast with the nest than did nestlings of hole-nesting species. However, nestlings of hole nesters showed a more evident achromatic contrast between flanges and other traits than did nestlings of open nesters. In addition, species with larger clutch sizes showed larger general achromatic contrasts with the nest. Gaping traits of open-nesting species contrasting with the nest background were better perceived under rich light regimes than under poor ones. These findings are consistent with a scenario in which selection for nestling detectability in dark environments has favored the evolution of particular achromatic components of gape coloration but also nestling traits that enhance signal efficacy by maximizing color contrasts within a nestling.     

Begging and the risk of predation in nestling birds

Theoretical models of the evolution of begging in nestling passerinesassume that begging is costly, either energetically or in termsof predation. However, few empirical measures of these costsexist. We examined whether nestling begging calls could attractpredators to nests by comparing predation rates at artificialnests with and without playbacks of tree swallow begging calls.Nests were baited with quail eggs and placed in pairs on theground or in modified nest-boxes. Nests with playbacks of beggingcalls were depredated before control nests significantly moreoften in both the ground and nest-box trials, suggesting thatpredators may use begging calls to locate nests. These resultssuggest that the risk of nest predation may be increased becauseof calling by nestlings and provide further support for theassumption that conspicuous begging is costly in terms of predation     

Begging in the absence of parents: a "quick on the trigger" strategy to minimize costly misses

Nestling begging in the absence of parents may reflect "falsealarms" due to cognitive constraints or signaling activity towardnest mates (sibling negotiation). According to signal detectiontheory, cognitive constraints should result in both false alarms(begging in the absence of parents or to inappropriate stimuli)and misses (failure to beg during parental visits). In our studyof house sparrows, nestling begging in the absence of parentscomprised up to 50% of the begging events at the nest and wasmore frequent at an early age and among hungrier (lower ranked)nestlings. In contrast, the probability of begging during parentalvisits was constantly high (80% or more), suggesting that therate of misses must have been low even at an early age. Theseresults have 2 main implications. First, the observation thatbegging in the absence of parents decreases with nestling agefavors the cognitive constraints hypothesis over functionalexplanations such as the sibling negotiation hypothesis. Second,the low proportion of "misses" among young nestlings suggeststhat nestling respond to their cognitive constraints by usinglow decision criteria (a "quick on the trigger" strategy) thatincreases the frequency of false alarms but minimizes costlymisses.     

Nestling testosterone is associated with begging behaviour and fledging success in the pied flycatcher, Ficedula hypoleuca

Animal signals are hypothesized to be costly in order to honestly reflect individual quality. Offspring solicitation signals given by nestling birds are thought to have evolved to advertise either need or individual quality. We tested the potential role of testosterone (T) in controlling the intensity of these signals by measuring begging behaviour as: (i) duration of the begging display and (ii) maximum height of the begging stretch, and by sampling endogenous T levels in nestling blood. We tested nestling pied flycatchers (Ficedula hypoleuca) using well-established experimental paradigm involving transient food deprivation to encourage begging behaviour and then blood-sampled nestlings at the end of these tests for T levels. Our results show that individual nestlings with the most intense begging displays had the highest circulating levels of T immediately after testing. In addition, we found substantial differences between broods in terms of circulating T. Finally, we found evidence that broods with higher levels of T showed increased fledging success, indicating a benefit for increased T production in nestlings. The potential trade-offs involved in T-mediated begging behaviour are discussed.     

A Long-Term Experimental Study Demonstrates the Costs of Begging That Were Not Found over the Short Term

Parent–offspring conflict theory predicts that begging behaviour could escalate continuously over evolutionary time if it is not prevented by costliness of begging displays. Three main potential physiological costs have been proposed: growth, immunological and metabolic costs. However, empirical evidence on this subject remains elusive because published results are often contradictory. In this study, we test for the existence of these three potential physiological costs of begging in house sparrow (Passer domesticus) nestlings by stimulating a group of nestlings to beg for longer and another group for shorter periods than in natural conditions. All nestlings were fed with the same quantity of food. Our study involves a long-term experimental treatment for begging studies (five consecutive days). Long-term studies frequently provide clearer results than short-term studies and, sometimes, relevant information not reported by the latter ones. Our long-term experiment shows (i) a clear effect on the immune response even since the first measurement (6 hours), but it was higher during the second (long-term) than during the first (short-term) test; (ii) evidence of a growth cost of begging in house sparrow nestlings not previously found by other studies; (iii) body condition was affected by our experimental manipulation only after 48 hour; (iv) a metabolic cost of begging never previously shown in any species, and (v) for the first time, it has shown a simultaneous effect of the three potential physiological costs of begging: immunocompetence, growth, and metabolism. This implies first, that a multilevel trade-off can occur between begging and all physiological costs and, second, that a lack of support in a short-term experiment for the existence of a tested cost of begging does not mean absence of that cost, because it can be found in a long-term experiment.     

Nestling testosterone controls begging behaviour in the pied flycatcher, Ficedula hypoleuca

Begging signals and endogenous testosterone (T) levels of young birds have been shown to be positively correlated. If T is causally involved in controlling the level of begging effort, an endocrine control mechanism could explain the evolution of begging as a costly signal reflecting need. We tested experimentally whether elevated circulating T levels enhanced begging behaviour in nestling pied flycatchers, Ficedula hypoleuca. A pilot study confirmed that nestling T levels could be elevated within a natural physiological range using an oral dose of T. After T-dosing, nestling begging behaviour was measured as: i) the duration of begging displays and ii) the maximum height of begging stretches. Our results show that nestling T levels were elevated at 90 min post dosing and that at this time point both measures of begging behaviour were performed more intensely by T-dosed nestlings than controls. Nestling begging displays in response to dosing varied between individuals, which in part was explained either by the date in the breeding season or nestling mass. The results of this study confirm the causal nature of T in controlling nestling begging signals and suggest that it may be part of the mechanism that controls begging behaviour in nestling birds.     

Does testosterone mediate the trade-off between nestling begging and growth in the canary (Serinus canaria)?

Nestling birds solicit food from their parents with vigorous begging displays, involving posturing, jostling and calling. In some species, such as canaries, begging is especially costly because it causes a trade off against nestling growth. Fitness costs of begging like this are predicted by evolutionary theory because they function to resolve conflicts of interest within the family over the provision of parental investment. However, the mechanism that links these costs with nestling behaviour remains unclear. In the present study, we determine if the relationships between nestling androgen levels, nestling begging intensities and nestling growth rates are consistent with the hypothesis that testosterone is responsible for the trade-off between begging and growth. We test this idea with a correlational study, using fecal androgens as a non-invasive method for assaying nestling androgen levels. Our results show that fecal androgen levels are positively correlated with nestling begging intensity, and reveal marked family differences in each trait. Furthermore, changes in fecal androgen levels between 5 and 8 days after hatching are positively associated with changes in nestling begging intensity, and negatively associated with nestling growth during this time. Although these correlational results support our predictions, we suggest that that experimental manipulations are now required to test the direct or indirect role of testosterone in mediating the trade-off between begging and growth.     

Facultative adjustment of pre‐fledging mass recession by nestling chimney swifts Chaetura pelagica

In species susceptible to mass‐dependent flight costs, mass recession prior to fledging may ensure that fledglings have appropriate wing loading. Our objectives were to determine if mass recession by chimney swift Chaetura pelagica nestlings is intrinsically controlled or facultatively adjusted by nestlings, and if mass recession is driven by changes in parental (i.e. reduced provisioning rates) or nestling (i.e. reduced begging) behavior. Nestling swifts (n = 50 in 17 broods) were divided into three treatment groups: controls, half‐weighted, or weighted. Half‐weighted and weighted nestlings had 0.6–0.7 or 1.2–1.3‐g lead weights, respectively, glued to body feathers on their backs during the period from 16 to 26 d post‐hatching. Weighted nestlings lost more mass than control and half‐weighted nestlings. After accounting for the added weights, control nestlings also had a higher wing loading than weighted nestlings. Video recordings revealed that provisioning rates of adult swifts did not vary throughout the nestling period, but the percent time nestlings spent begging increased slightly with age. Differences in mass recession among nestlings in different treatment groups resulted in convergence toward similar wing loading values likely optimal for flight efficiency. Mechanism(s) involved in this process remain unclear because provisioning rates were similar (from day 12 to 26 post‐hatching) whereas percent begging time by nestlings tended to increase with nestling age. However, weighted nestlings may have lost more mass than control nestlings by soliciting less food from adults than siblings, being more active, losing more water due to tissue maturation, or through some combination of two or more of these factors.     

Manipulation of hunger levels affects great spotted cuckoo and magpie host nestlings differently

Brood parasitic nestlings usually exhibit an exaggerated begging behaviour, which is mainly attributed to reduced inclusive fitness costs since they typically share the nest with unrelated individuals. However, energetic costs also constrain begging expression and accordingly a relation between food requirements and intensity of begging behaviour could also exist in brood parasites, just as in nesting bird species. Here, we tested this hypothesis in the great spotted cuckoo Clamator glandarius and its main host, the magpie Pica pica, by studying the effect of an appetite enhancer, cyproheptadine hydrochloride, on nestling provisioning and development (size, body mass and cell‐mediated immune response). To study nestling provisioning, neck‐collars were meticulously placed around nestling necks allowing normal respiration but avoiding the ingestion of food delivered by adult magpies during ca 2.5 h. Loss in body mass during neck‐collar trials was used as a proxy for energetic begging costs, while the amount of food received during these trials and growth during the whole nestling period were used as variables reflecting short‐ and long‐term effects of the experimental treatment. During neck‐collar trials, we found that experimental nestlings of both species received more food than control nestlings. However, experimental magpies, but not cuckoos, lost more body mass than control nestlings. These results suggest a short‐term beneficial effect of an escalated begging behaviour in both species that would be energetically cheaper for cuckoos than for magpies. We found positive long‐term effects of the appetite enhancer only in magpies (in terms of tarsus and wing length at fledging, but not in terms of immune response and body mass); suggesting that exaggerated begging would be beneficial for hosts only. We discuss the possible effect of begging behaviour on the risk of predation and on inclusive fitness, but also the possibility that our results may be explained by some kind of limitation in the capability of food assimilation by parasitic species.