Partial begging: an empirical model for the early evolution of offspring signalling

Species where, from birth, the offspring feed themselves in addition to begging for food from the parents can be described as 'partially begging'. Such species provide a unique opportunity to examine the evolution of offspring begging from non-signalling offspring foraging strategies. We used the partially begging burying beetle Nicrophorus vespilloides to test specific hypotheses concerning the coexistence of begging and self-feeding. We first tested whether the cessation of larval begging coincided with an increase in the efficiency of self-feeding. As predicted, begging ceased when the efficiency of self-feeding reached the point where the larvae grew just as well without as with access to food provided by the parent. We next tested whether the transition to nutritional independence was under parental or offspring control. The parent did not change its behaviour towards the larvae over time, while the larvae changed their behaviour by reducing the time spent begging in the presence of the parent. Food allocation during the transition to nutritional independence was therefore under offspring control. Our results on partial begging provide a starting point for new theoretical models for the origin of begging. We suggest that these should be constructed as scramble-competition models because the offspring control food allocation.     

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.     

Behavioral dynamics between caring males and females in a beetle with facultative biparental care

In families in which both parents care for multiple offspring,the amount of care a parent provides can be simultaneously influencedby multiple social interactions (i.e., parent-parent and parent-offspring).In this study, we first tested for sex differences in the parents'contribution to care and then used path analysis to addressthe simultaneous impact of parent-parent and parent-offspringinteractions on male and female care in the burying beetle,Nicrophorus vespilloides. In this species, both parents provisiontheir offspring predigested carrion from a vertebrate carcass,and the larvae beg for food from their parents. We found thatfemales were more involved in direct care for the larvae andspent more time than did males provisioning the larvae withfood. By using path analysis, we found a negative relationshipbetween male and female provisioning, suggesting that parentsadjust their behavior to that of their mate. Furthermore, wefound that both social interactions (i.e., larval begging) andnonsocial factors (i.e., brood size) significantly influencedmale provisioning, but had no significant effect on female provisioning.We suggest that the difference in the relative contributionof the two sexes to the care of the offspring explains why onlymales seemed to adjust their care to variation in social andnonsocial factors. For example, females may be less able toadjust their care to variation in larval begging and brood sizebecause they were already working near their maximum capacity.     

Does resource availability affect offspring begging and parental provisioning in a partially begging species?

In species where parents repeatedly provide their offspring with food, the offspring often communicate their need to the parents. Burying beetles, which breed on a wide size range of carcasses of small vertebrates, are interesting model systems to test theories on begging, because the larvae show partial begging, that is, they obtain food through both signalling to their parents (begging) and feeding directly from the carcass. We manipulated resource availability inNicrophorus vespilloides by providing parents with mouse carcasses spanning a wide size range, and allowing them to rear the larvae that hatched, so that both the amount of resources and the number of siblings varied. Time spent begging by each larva was strongly influenced by the time parents spent near the larvae. Brood size had a nonlinear effect on larval begging, with begging increasing with brood size for relatively smaller broods and decreasing again for larger broods. Carcass size and number of parents present had no effect on begging. Time spent provisioning the larvae by the parents was strongly associated with the time spent begging by each larva. Parents spent more time provisioning under biparental care than under uniparental care, while brood size and carcass size had no significant effect. These findings suggest that the larvae adjust their begging to the behaviour of their parents and the number of siblings, but not to the amount of resources. Furthermore, parents adjust the time spent provisioning to the average amount of begging by each larva in the brood, and not to the availability of resources.     

Flexible communication within bird families—The consequences of behavioral plasticity for parent–offspring coadaptation

Offspring are selected to demand more resources than what is optimal for their parents to provide, which results in a complex and dynamic interplay during parental care. Parent–offspring communication often involves conspicuous begging by the offspring which triggers a parental response, typically the transfer of food. So begging and parental provisioning reciprocally influence each other and are therefore expected to coevolve. There is indeed empirical evidence for covariation of offspring begging and parental provisioning at the phenotypic level. However, whether this reflects genetic correlations of mean levels of behaviors or a covariation of the slopes of offspring demand and parental supply functions (= behavioral plasticity) is not known. The latter has gone rather unnoticed—despite the obvious dynamics of parent–offspring communication. In this study, we measured parental provisioning and begging behavior at two different hunger levels using canaries (Serinus canaria) as a model species. This enabled us to simultaneously study the plastic responses of the parents and the offspring to changes in offspring need. We first tested whether parent and offspring behaviors covary phenotypically. Then, using a covariance partitioning approach, we estimated whether the covariance predominantly occurred at a between‐nest level (i.e., indicating a fixed strategy) or at a within‐nest level (i.e., reflecting a flexible strategy). We found positive phenotypic covariation of offspring begging and parental provisioning, confirming previous evidence. Yet, this phenotypic covariation was mainly driven by a covariance at the within‐nest level. That is parental and offspring behaviors covary because of a plastic behavioral coadjustment, indicating that behavioral plasticity could be a main driver of parent–offspring coadaptation.     

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.     

Interaction between parental care and sibling competition: parents enhance offspring growth and exacerbate sibling competition

Species with elaborate parental care often also show intense sibling competition over resources provided by parents, suggesting joint evolution of these two traits. Despite this, the evolution of elaborate parental care and the evolution of intense sibling competition are often studied separately. Here, we examine the interaction between parental food provisioning and sibling competition for resources through the joint manipulation of the presence or absence of parents and brood size in a species with facultative parental care: the burying beetle Nicrophorus vespilloides. The effect of the interaction between the presence or absence of parents and brood size was strong; brood size had a strong effect on growth when parents provided care, but no effect when parents were absent. As in previous studies, offspring grew faster when parents were present than when parents were absent, and offspring grew faster in smaller broods than in larger broods. Our behavioral observations showed that brood size had a negative effect on both the amount of time parents spent providing resources to individual offspring and the offspring's effectiveness of begging, confirming that the level of sibling competition increased with brood size. Furthermore, offspring in larger broods shifted more from begging toward self-feeding as they grew older compared to offspring in small broods. Our study provides novel insights into the joint evolution of parental care and sibling competition, and the evolution of offspring begging signals. We discuss the implications of our results in light of recent theoretical work on the evolution of parental care, sibling competition, and offspring begging signals.     

Provisioning control during maternal care by the earwig Anisolabis maritima (Dermaptera: Anisolabididae): Do mothers adjust provisioning according to offspring need?

Provisioning offspring is an important form of parental care for the improvement of offspring survival and growth. Because provisioning can be costly for parents, parents may change their investment levels in response to offspring need and begging signals. Anisolabis maritima is a cosmopolitan species of earwig that shows subsocial behavior. Females progressively provision their young in soil burrows. The present study investigated whether A. maritima mothers carry food to the nest for their offspring (nymphs) and whether the mothers adjust the amount of food carried to the burrow according to the degree of the nymphs’ hunger. Through laboratory experiments, I found that mothers carried food to sites where more nymphs were present, and more food to broods of more hungry nymphs. These results have revealed that mothers recognize the presence of offspring and the degree of their hunger. This study, therefore, indicates the presence of offspring begging signals in A. maritima.     

Tadpole begging reveals high quality

Parents can benefit from allocating limited resources nonrandomly among offspring, and offspring solicitation (i.e. begging) is often hypothesized to evolve because it contains information valuable to choosy parents. We tested the predictions of three ‘honest begging’ hypotheses – Signal of Need, Signal of Quality and Signal of Hunger – in the tadpoles of a terrestrial frog (Oophaga pumilio). In this frog, mothers provision tadpoles with trophic eggs, and when mothers visit, tadpoles perform a putative begging signal by stiffening their bodies and vibrating rapidly. We assessed the information content of intense tadpole begging with an experimental manipulation of tadpole condition (need/quality) and food deprivation (hunger). This experiment revealed patterns consistent with the Signal of Quality hypothesis and directly counter to predictions of Signal of Need and Signal of Hunger. Begging effort and performance were higher in more developed and higher condition tadpoles and declined with food deprivation. Free‐living mothers were unlikely to feed tadpoles of a nonbegging species experimentally cross‐fostered with their own, and allocated larger meals to more developed tadpoles and those that vibrated at higher speed. Mother O. pumilio favour their high‐quality young, and because their concurrent offspring are reared in separate nurseries, must do so by making active allocation decisions. Our results suggest that these maternal choices are based at least in part on offspring signals, indicating that offspring solicitation can evolve to signal high quality.     

Features of begging calls reveal general condition and need of food of barn swallow (Hirundo rustica) nestlings

Altricial offspring of birds solicit food provisioning by complexbegging displays, implying acoustic and visual signals. Differentcomponents of begging behavior may function as reliable signalsof offspring state and thus reproductive value, on which parentsbase optimal parental decisions about allocation of criticalresources (e.g., food). We experimentally manipulated componentsof general condition of nestling barn swallows (Hirundo rustica)by (1) altering brood size by cross-fostering an unbalanced number of nestlings between pairs of synchronous broods andthus manipulating the level of within-brood competition forfood, (2) injecting some nestlings with a harmless immunogen,simulating an infection, and (3) preventing part of the nestlingsfrom receiving food for a short period while establishing controlgroups. We recorded rate of begging response by individual nestlings as parents visited the nest and recorded begging calls usinga DAT recorder to analyze six sonagraphic features of vocalizations.Our factorial experiment revealed that nestlings deprived offood begged more frequently when parents visited the nest comparedto their non—food-deprived nest mates. Food deprivationincreased duration of syllables forming begging calls, whereas brood size enlargement resulted in increased latency of responseto parental calls. Heavy nestlings in good body condition vocalizedat a relatively low peak frequency. To our knowledge, thisis the first study in which begging rate and sonagraphic structureof begging calls are shown to reliably reveal a diverse setof components of offspring general state, on which parental decisions may be based.     

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.     

Parent–Offspring Conflict over the Transition to Independence in Nicrophorus vespilloides: Parental Chemical Cues and Offspring Begging

In species where parents provide their offspring with food, the offspring must undergo a transition from nutritional dependency to independence. Parent–offspring conflict theory predicts that the optimal timing for this transition will differ between parents and offspring and that the realised timing depends on each party’s ability to control the transition. The burying beetle Nicrophorus vespilloides is an excellent species for studying conflict over the transition to independence; the larvae beg for pre‐digested carrion from their parents until they cease begging around 72 h after hatching. The cessation of begging is not associated with changes in parental behaviour, suggesting that the transition is mostly under offspring control. However, recent work has demonstrated that caring parents express distinct chemical cues that stimulate larval begging, the expression of which varies between breeding and non‐breeding beetles, suggesting that parents might exert control over the transition to independence by altering these cues throughout development. If so, we predict that begging larvae should behave differently towards parental chemical cues from different stages of development and that larvae of different ages should behave similarly towards parental chemical cues from the same stage of development. We found no evidence for either prediction: begging larvae did not behave differently towards parental chemical cues from different stages of development, and larvae of different ages still behaved differently towards parental chemical cues from the same stage of development. Our results provide no support for the hypothesis that parents can control the transition to nutritional independence by altering their chemical profiles.     

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.     

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.     

Species divergence in offspring begging intensity: difference in need or manipulation of parents?

Conflicts over the delivery and sharing of food among family members are expected to lead to evolution of exaggerated offspring begging for food. Coevolution between offspring begging intensity and parent response depends on the genetic architecture of the traits involved. Given a genetic correlation between offspring begging intensity and parental response, there may be fast and arbitrary divergence in these behaviours between populations. However, there is limited knowledge about the genetic basis of offspring solicitation and parental response and whether these traits are genetically correlated. In this study, we performed a partial cross-fostering experiment of young between pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) and recorded the behaviour of individual offspring and their (foster)parents. We found that nestling collared flycatchers reached a higher phenotypic quality, estimated both as mass at fledging and as intensity of their T-lymphocyte-mediated immune response when raised by heterospecific foster parents. However, although collared flycatchers begged relatively more intensively, we found no evidence of corresponding higher resistance (i.e. lower feeding rate) of adult collared flycatchers than of adult pied flycatchers. Thus, the difference in offspring begging intensity between the two species seems not to be a result of a difference in escalation of the parent-offspring conflict. Instead, the species' divergence in exaggeration of offspring begging intensity 'honestly' matches a difference between the species in offspring need. This interpretation is strengthened by the fact that the difference in begging intensity between the two species increased as the season progressed, coinciding with the higher sensitivity of nestling collared flycatchers to the seasonal decline in food availability. Thus, the behavioural differentiation appears to be a direct consequence of a life-history differentiation (offspring growth patterns).     

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.     

Effects of inbreeding on behavioural plasticity of parent–offspring interactions in a burying beetle

Inbreeding depression is defined as a fitness decline in progeny resulting from mating between related individuals, the severity of which may vary across environmental conditions. Such inbreeding‐by‐environment interactions might reflect that inbred individuals have a lower capacity for adjusting their phenotype to match different environmental conditions better, as shown in prior studies on developmental plasticity. Behavioural plasticity is more flexible than developmental plasticity because it is reversible and relatively quick, but little is known about its sensitivity to inbreeding. Here, we investigate effects of inbreeding on behavioural plasticity in the context of parent–offspring interactions in the burying beetle Nicrophorus vespilloides. Larvae increase begging with the level of hunger, and parents increase their level of care when brood sizes increase. Here, we find that inbreeding increased behavioural plasticity in larvae: inbred larvae reduced their time spent associating with a parent in response to the length of food deprivation more than outbred larvae. However, inbreeding had no effect on the behavioural plasticity of offspring begging or any parental behaviour. Overall, our results show that inbreeding can increase behavioural plasticity. We suggest that inbreeding‐by‐environment interactions might arise when inbreeding is associated with too little or too much plasticity in response to changing environmental conditions.     

The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care.

The coevolution of parental investment and offspring solicitation is driven by partly different evolutionary interests of genes expressed in parents and their offspring. In species with biparental care, the outcome of this conflict may be influenced by the sexual conflict over parental investment. Models for the resolution of such family conflicts have made so far untested assumptions about genetic variation and covariation in the parental resource provisioning response and the level of offspring solicitation. Using a combination of cross-fostering and begging playback experiments, we show that, in the great tit (Parus major), (i) the begging call intensity of nestlings depends on their common origin, suggesting genetic variation for this begging display, (ii) only mothers respond to begging calls by increased food provisioning, and (iii) the size of the parental response is positively related to the begging call intensity of nestlings in the maternal but not paternal line. This study indicates that genetic covariation, its differential expression in the maternal and paternal lines and/or early environmental and parental effects need to be taken into account when predicting the phenotypic outcome of the conflict over investment between genes expressed in each parent and the offspring.     

A chemical signal of offspring quality affects maternal care in a social insect

Begging signals of offspring are condition-dependent cues that are usually predicted to display information about the short-term need (i.e. hunger) to which parents respond by allocating more food. However, recent models and experiments have revealed that parents, depending on the species and context, may respond to signals of quality (i.e. offspring reproductive value) rather than need. Despite the critical importance of this distinction for life history and conflict resolution theory, there is still limited knowledge of alternative functions of offspring signals. In this study, we investigated the communication between offspring and caring females of the common earwig, Forficula auricularia, hypothesizing that offspring chemical cues display information about nutritional condition to which females respond in terms of maternal food provisioning. Consistent with the prediction for a signal of quality we found that mothers exposed to chemical cues from well-fed nymphs foraged significantly more and allocated food to more nymphs compared with females exposed to solvent (control) or chemical cues from poorly fed nymphs. Chemical analysis revealed significant differences in the relative quantities of specific cuticular hydrocarbon compounds between treatments. To our knowledge, this study demonstrates for the first time that an offspring chemical signal reflects nutritional quality and influences maternal care.     

Food limitation in asynchronous bluethroat broods: effects on food distribution, nestling begging, and parental provisioning rules

Scramble competition models of begging predict that junior nestlingswill be more affected by food limitation than seniors. Thesemodels assume that food allocation is under offspring controland, hence, predict that this change in food distribution iscaused by a differential behavioral response by seniors andjuniors. By using the bluethroat (Luscinia svecica svecica)as our model species, we induced food limitation by removingthe male parent temporarily. We found that, as predicted, fooddistribution became more biased in disfavor of juniors whenfood was limited. However, there was no significant differencein the behavioral responses of seniors and juniors (i.e., positioningin the nest or begging postures) to food limitation that couldexplain the change in food distribution. Hence, there was noevidence that seniors controlled food distribution. As predictedif parents preferentially fed seniors, nestling rank affectedfood distribution when controlling for variation in nestlingbehaviors. Furthermore, as expected if the increased skew infood distribution under food limitation was caused by activefood allocation by parents, nestling rank had a greater effecton food distribution under food limitation than under normalconditions. The present study suggests that food distributionin passerine birds is determined not only by nestling behaviors(begging posture and positioning) alone but also by parentalpreferences for seniors based on nonsignaling cues, such asbody size.