On the coadaptation of offspring begging and parental supply—a within-individual approach across life stages

Parental care is often characterized by complex behavioral interactions between offspring soliciting for food and parents providing food. During this interplay both behaviors, offspring begging and parental provisioning, can exert a selective pressure on the expression of the other. It has, therefore, been predicted that traits involved in this interplay may coevolve and ultimately become (genetically) correlated. Such covariation has—at least at the phenotypic level—been found in a number of cross-fostering studies, including evidence from the canary (Serinus canaria), our model species. However, a common challenge for these studies has been to establish a genetic covariation given the difficulty to disentangle the relative contribution of genetic and maternal effects, as the latter may act already before cross-fostering. We addressed this problem by studying within-individual covariation between begging (expressed at the nestling stage) and provisioning (expressed at the adult stage). In addition, we estimated the degree of heritability of these behaviors using parent-offspring regressions, as inheritance forms a prerequisite for any genetic correlation. Both traits showed a low to moderate non-significant heritability, similar to those previously reported in other bird species. However, offspring begging and parental provisioning did not covary at the intra-individual level. Thus, individuals begging intensively as nestlings were not necessarily individuals that provided more food as adults or vice versa. These findings provide important insights for our understanding of coadaptation, suggesting that factors other than genes such as maternal effects may play a role in adjusting offspring begging to the levels of parental provisioning.     

Provisioning rules and chick competition in asynchronously hatching common terns (Sterna hirundo)

Interactions between nestling birds and their parents are models for examining parent–offspring communication and sibling competition. Most studies have focused on species where young are restricted to a nest. However, offspring of many species are mobile and fed by parents for an extended period post-hatch. These chicks mobility may provide an opportunity to examine the role of signalling and physical competition on parental feeding decisions. We examined parental provisioning rules in relation to offspring behaviour and hatching order (i.e., competitive ability) in a species with mobile young, the common tern. We determined that about 95% of feedings were directed to the first chick to reach the parent when it landed with food. We developed a probabilistic model to predict the likelihood of a chick reaching the parent first, and thus receiving food. Our model showed that begging intensity, feeding history, and the interaction between begging intensity and relative proximity to the parent best predicted which chick would arrive first. Increased begging was associated with arriving first significantly more when a chick was relatively further from the parent than when it was closer than its siblings. Independently of these factors, larger, earlier-hatched chicks were more likely to be fed than smaller, later-hatched chicks. Additional analyses showed that parents landed closer to more intensively begging chicks, however, increased begging did not explain the advantage of earlier-hatched chicks because begging intensity did not vary with hatching order. Instead, earlier-hatched chicks were more likely to outrun later-hatched siblings and reach the parent first.     

Parent-absent signalling of need and its consequences for sibling competition in the barn swallow

In species with parental care, competition among siblings for access to limited parental resources is common. Sibling competition can be mediated by begging behaviour, a suite of different visual and acoustic displays by which offspring solicit parental care. These are mostly addressed to the parents upon food provisioning, but can also be performed in the absence of the attending parents. This so-called parent-absent begging (PAB) may function as an intrabrood communication signal and potentially affect intrabrood competition dynamics for access to food. We investigated the role of PAB in moulding sibling interactions and its effect on food intake among altricial barn swallow (Hirundo rustica) nestlings, both under normal and experimentally reduced food intake. Frequency of PAB increased after food deprivation. Nestlings that had performed PAB increased their begging intensity upon the subsequent parental feeding visit, while siblings reduced their own begging level, but only when they had not been food-deprived. As a consequence, nestlings which had performed PAB before parental arrival had larger chances of receiving food. However, nestlings did not benefit from displaying PAB when competing with food-deprived siblings. Our findings show that PAB reliably reflects need of food, indicating that a nestling will vigorously compete for the subsequent food item. By eavesdropping siblings' PAB displays, nestlings may optimally balance the costs of scrambling competition, the direct fitness gains of being fed and the indirect fitness costs of subtracting food to needy kin. However, large asymmetries in satiation between competitors may lead individual offspring to monopolize parental resources, irrespective of PAB displays.     

Provisioning rules in tree swallows

Conflict between parents and offspring may result in offspring exaggerating their needs and parents devaluing their begging signals. To determine whether this occurs, it is first necessary to establish the link between need, begging and parental response. The purpose of our study was to examine these relationships in tree swallows (Tachycineta bicolor). Parents preferentially fed nestlings that begged sooner, reached higher and were closer to the front of the nestbox (Fig. 1). Begging intensity of both individuals and entire broods increased with relatively long periods between feeding visits. Within broods, parents responded to increased begging intensity by increasing their feeding rate, although this effect was relatively weak. Large and small nestlings did not differ in their begging behavior and all nestlings, regardless of size, were fed at similar rates. Despite the overall equity in feeding, male parents preferentially fed larger nestlings while female parents fed smaller nestlings. Nestlings did not increase their begging intensity in response to begging by nestmates. Our results suggest that begging is related to need in this species and that parents respond to variation in begging intensity. Received: 4 May 1995/Accepted after revision: 17 December 1995     

Parentally biased favouritism in relation to offspring sex in zebra finches

Family conflicts over parental care result in offspring attempting to exert control using solicitation behaviours, whilst the parents are potentially able to retaliate through provisioning rules. However, the evolutionary interests of one parent may not necessarily support the evolutionary interests of the other parent, and such conflicts of interest may be expressed in how the two parents allocate the same form of parental care to individual offspring. Theory suggests that such parentally biased favouritism is a universally predicted outcome of evolutionary conflicts of interest, and empirical evidence suggests that parentally biased favouritism occurs in relation to offspring size and solicitation behaviours. However, unequivocal empirical evidence of parentally biased favouritism in relation to offspring sex is absent, due to being strongly confounded by sex differences in size and solicitation behaviours. Here, we present strong evidence for parentally biased favouritism in relation to offspring sex in zebra finches (Taeniopygia guttata), independent of the effects of chick size and begging intensity. Mothers preferentially provisioned sons over daughters, whilst fathers showed no bias, meaning that sons received more food than daughters. Parentally biased favouritism in relation to offspring sex facilitates parental control over evolutionary conflicts of interest and is probably more widespread than previously realised.     

Rising costs of care make spiny chromis discerning parents

When the costs of parental care do not scale with the number of offspring being cared for, inclusion of non-descendant young into broods can be advantageous, leading to systems of alloparental care. However, if the cost of care scales with the number of offspring, selection may act against misdirected parental care. The spiny chromis, Acanthochromis polyacanthus, is a marine fish with extended biparental care, and broods that increase in size over the care period strongly suggest that alloparental care occurs in this species. However, A. polyacanthus parents directly provision their offspring by producing ectodermal mucus for their fry to feed on. The costs of such provisioning may scale with brood size, potentially increasing the costs of parental care. Using wild A. polyacanthus pairs, we tested whether foreign offspring are accepted into established broods, and measured how brood defence effort and mucal feeding scale with brood size. We found that A. polyacanthus discriminate between their own and foreign young, vigorously expelling experimentally introduced foreign offspring. Although defensive effort did not scale with brood size, mucal feeding was strongly dependent on brood size, and this increasing cost of care likely acts as the primary selective force on parental discrimination and rejection of foreign fry in A. polyacanthus.     

Begging affects parental effort in the pied flycatcher, Ficedula hypoleuca

It has been suggested that nestlings use begging to increase their share of parental resources at the expense of current or future siblings. There is ample evidence that siblings compete over food with nestmates by begging, but only short-term effects of begging on parental provisioning rates have been shown. In this study, we use a new experimental design to demonstrate that pied flycatcher (Ficedula hypoleuca) nestlings that beg more are able to increase parental provisioning rates over the major part of the nestling period, thus potentially competing with future siblings. Parents were marked with microchips so that additional begging sounds could be played back when one of the parents visited the nest. By playing back begging sounds consistently at either male or female visits, a sex difference in provisioning rate that lasted for the major part of the nestling period was induced. If each parent independently adjusts its effort to the begging intensity of nestlings, begging may also be the proximate control mechanism for the sexual division of labour. Received: 24 January 1997 / Accepted after revision: 30 August 1997     

Food supply differentially affects sibling negotiation and competition in the barn owl (Tyto alba)

In contrast to most birds, nestling barn owls (Tyto alba) vocalise not only when parents are at the nest but also in their absence. Calls produced in their absence have been shown to facilitate sibling negotiation over the impending food resource. Since nestlings vocalise more vigorously in the presence of parents, they may be calling not to negotiate resources but to compete amongst each other over parental food distribution. A critical issue is to determine whether offspring need differentially affects sibling negotiation and sibling competition, that is vocalisation in the absence and presence of parents. To answer this question, I manipulated the food supply of 26 broods by adding or removing prey items. In the absence of parents, food-added broods vocalised at a significantly lower level than food-removed ones. In contrast, once a parent arrived at the nest, the vocalisation level was not significantly related to the manipulation of brood food supply. This suggests that in the absence of parents, it is more important for food-removed nestlings to vocalise intensely, and that in their presence, the relationship between begging and offspring need tends to vanish. In other words, brood food supply may affect sibling negotiation to a larger extent than sibling competition.     

Need and nestmates affect begging in tree swallows

We conducted an experiment on nestling tree swallows (Tachycineta bicolor) to examine predictions from signalling models for the evolution of conspicuous begging behaviour. Specifically, we examined the relationship between (1) nestling begging intensity and hunger, (2) begging intensity and parental provisioning and (3) begging intensity and nestmate condition. Forty broods of 9-day-old nestlings were removed from their nests for 1 h and assigned to one of the following three treatments: (1) all nestlings in the brood deprived of food (n = 13), (2) all nestlings in the brood fed (n = 11) or (3) half the nestlings in the brood deprived and half fed (n = 16). Videotapes before and after the treatments showed that begging intensity increased in broods in which all of the nestlings had been deprived and decreased in broods in which all of the nestlings had been fed. Deprived nestlings in the half-and-half treatment did not change their begging intensity in response to treatment, while fed nestlings in this treatment group showed a decrease in begging intensity. Parent tree swallows increased their feeding rate to deprived broods and decreased their rate to fed broods. Within broods, parents decreased their feeding rate to fed nestlings, but showed no significant change in feeding to deprived nestlings. Our results suggest that begging intensity is influenced by hunger and that parents appear to respond to variation in begging intensity. The begging of nestmates also appears to influence begging independently of need. These results are consistent with predictions derived from signalling models of begging. Received: 20 June 1997 / Accepted after revision: 19 January 1998     

Resource allocation varies with parental sex and brood size in the asynchronously hatching green-rumped parrotlet (<Emphasis Type="Italic">Forpus passerinus</Emphasis>)

When eggs hatch asynchronously, offspring arising from last-hatched eggs often exhibit a competitive disadvantage compared with their older, larger nestmates. Strong sibling competition might result in a pattern of resource allocation favoring larger nestlings, but active food allocation towards smaller offspring may compensate for the negative effects of asynchronous hatching. We examined patterns of resource allocation by green-rumped parrotlet parents to small and large broods under control and food-supplemented conditions. There was no difference between parents and among brood sizes in visit rate or number of feeds delivered, although females spent marginally more time in the nest than males. Both male and female parents preferentially fed offspring that had a higher begging effort than the remainder of the brood. Mean begging levels did not differ between small and large broods, but smaller offspring begged more than their older nestmates in large broods. Male parents fed small offspring less often in both brood sizes. Female parents fed offspring evenly in small broods, while in large broods they fed smaller offspring more frequently, with the exception of the very last hatched individual. These data suggest male parrotlets exhibit a feeding preference for larger offspring—possibly arising from the outcome of sibling competition—but that females practice active food allocation, particularly in larger brood sizes. These differential patterns of resource allocation between the sexes are consistent with other studies of parrots and may reflect some level of female compensation for the limitations imposed on smaller offspring by hatching asynchrony.     

Begging and provisioning in broods of asynchronously-hatched yellow-headed blackbird nestlings

Studies of begging have found a positive relationship between begging level and provisioning level. Studies of unequal nestlings, however, have found that small nestlings generally beg more but are fed less than their larger siblings. We manipulated the begging levels of yellow-headed blackbird (Xanthocephalus xanthocephalus) chicks to investigate how begging benefits individuals in broods of unequal siblings. Food-deprived chicks begged more and were fed more; satiated chicks begged less and were fed less. When we deprived each chick of a brood in turn, large and small chicks generally increased begging and received more provisioning. Small chicks, however, rarely received more food than their larger siblings even when they behged relatively more. Parent yellow-headed blackbirds increase provisioning to hungry begging chicks, but also allocate food based on relative offspring size.     

Patterns of brood division and an absence of behavioral plasticity in a neotropical passerine

Studies of parental behavior in various habitats provide an opportunity to gain insight into how different environments may mold strategies of parental care. Brood division by parents has been hypothesized to occur facultatively within and among species. Brood division occurs when each parent cares for specific offspring within a brood. We studied brood division in a neotropical passerine, the western slaty antshrike (Thamnophilus atrinucha). Our results present a unique picture of a highly specialized example of avian brood division. Division was a fixed behavioral pattern in the population studied: all broods divided by fledging and remained divided during the entire post-fledging period. Brood division before fledging, a previously unreported phenomenon, occurred in 40% of nests observed. Parents that preferentially fed a certain offspring (defined as their focal offspring) in the nest fed the same individual after fledging. Each parent fed only its focal offspring in broods of one and two. The male parent cared for the heavier offspring and the first offspring to leave the nest. Siblings were segregated spatially during the time of highest predation risk. These observations suggest that a consistently high risk of predation on offspring has favored initial spatial segregation and inflexibility of brood division behavior in this species. Factors other than predation risk alone may explain the observed patterns of long-term, perfect brood division. Because high predation is common and relatively predictable in the tropics, selection for fixed brood division may be stronger in tropical birds than in the temperate zone.     

Helpers-at-the-nest have the same provisioning rule as parents: experimental evidence from play-backs of chick begging

Despite the success of kin selection in explaining helping-at-the-nest among communally breeding birds, we know almost nothing about how helpers regulate their chick-feeding effort. This is especially interesting given how much we now know about parental provisioning `rules-of-thumb' and the evolution of chick begging as an honest signal of `need'. This study explores the provisioning rules of helpers and parents in Arabian babblers (Turdoides squamiceps), using tape play-backs to supplement chick-begging signals and increase apparent brood demand. In all eight groups tested, both helpers and parents fed older, noisier broods at higher rates. Total provisioning rates to nests increased during begging play-back days compared to control days. Absolute provisioning rates by helpers and the scale of their responses to play-backs were statistically indistinguishable from those of parents. In both helpers and parents, increases in nest visits during play-backs were associated with reductions in foraging distance from the nest and increases in size of prey delivered. Older birds of both sexes delivered slightly larger prey items, possibly reflecting differences in foraging ability due to experience. These results are consistent with the idea that, like the parents, helpers-at-the-nest in Arabian babblers provision nestlings as part of a strategy of investment, irrespective of helper age, dominance status or sex. In this species, high relatedness within groups may provide parents and helpers with similar kin-selected fitness benefits, although the mutualistic advantages to helpers from simply augmenting group sizes cannot be ruled out. Received: 17 June 1997 / Accepted after revision: 28 February 1998     

No cultural transmission of species recognition between parents and offspring in free-living great tits and blue tits

Imprinting plays a key role in the development of species recognition, with young imprinting upon the morphological characters of their parents. However, the potential role that cultural transmission might play in species recognition remains largely uninvestigated. Great tits (Parus major) and blue tits (Cyanistes caeruleus) do not normally perceive each other as sexual competitors or potential partners. However, after reciprocal interspecific cross-fostering, both species may perceive individuals of the foster species as potential rivals or mates. Although the experience of being raised by heterospecifics clearly has affected the species recognition of cross-fostered birds, some of them breed naturally with conspecifics. The offspring of such cross-fostered birds (OCF) are hence raised by parents that look like ordinary conspecifics but display deviant species recognition as compared to controls in terms of aggressive response towards rivals. Comparing the aggressive behavior of OCF, cross-fostered birds and controls towards territorial intruders may thus help tease apart the influence of morphological vs behavioral cues of parents in the development of offspring species recognition. To this end, we compared birds from all three treatments with respect to their aggressive response to territorial intruders of both species during the breeding season. OCF and controls did not differ in their pattern of response towards heterospecific and conspecific stimuli. Compared to cross-fostered birds, OCF and controls showed less aggression towards heterospecific intruders, while the response towards conspecific intruders did not differ between treatments. These results demonstrate that both tit species imprint on the morphological characters of their parents, but that parental behavior is not important for the development of species recognition in terms of aggressive response towards territorial intruders.     

Parents influence asymmetric sibling competition: experimental evidence with partially dependent young

Asymmetric sibling competition, which occurs when some siblings hatch as stronger competitors than others, is an important component of avian reproductive strategies. Here, we report two experiments on the burying beetle Nicrophorus vespilloides investigating how parents might influence the outcome of asymmetric sibling competition. In this species, as in altricial birds, different-aged offspring compete for resources provided by the parents. However, unlike altricial birds, offspring depend only partially on their parents for resources, and parents adjust the brood size directly through filial cannibalism. In the first experiment, we compared the growth and survivorship of different-aged offspring when parents could and could not influence asymmetric sibling competition. In the second experiment, we recorded behavioral interactions between different-aged offspring and parents. We found that senior offspring (early-hatched) grew faster than juniors (late-hatched) when parents were present and could influence the outcome of sibling competition, whereas seniors and juniors grew at similar rates when parents were removed. Thus, seniors benefited more than did juniors when the offspring could obtain resources by begging from the female parent. There was no difference in the survivorship of seniors and juniors. We also found that seniors and juniors spent a similar amount of time feeding from female parents, but juniors spent more time begging and were less effective at begging than seniors. Interestingly, juniors spent more time begging only as long as seniors also begged, suggesting that juniors adjusted their begging effort in response to direct competition against seniors for resources provided by parents. Our study provides novel insights into the ecological significance of asymmetric sibling competition by showing that asymmetric sibling competition took place when parents were present and offspring could obtain resources by begging. In contrast, we found no evidence of asymmetric sibling competition when parents were absent and offspring obtained resources solely by self-feeding.     

The relationship between maternal ornamentation and feeding rate is explained by intrinsic nestling quality

In altricial birds, parental feeding is essential, and its amount may depend on the quality of both parents. A relationship between parental quality and feeding rate is generally attributed to an active adjustment by parents in order to retain good quality mates or ensure high fitness through raising high-quality offspring. However, the behaviour and need of young may also change with parental quality, and this may affect parental behaviour. A further problem is that most studies have investigated post-hatching parental investment in relation to the secondary sexual signals of males, but not females. In a cross-fostering experiment, we examined the feeding rates of rearing parents in relation to the size and ornamentation of both original and rearing parents in collared flycatchers (Ficedula albicollis). Using this setup, we could examine whether the observed feeding patterns were the results of the decision of the parents based on their own and their partner’s traits or the constraints imposed by the behaviour or need of offspring. When correcting for clutch size and year, we found that feeding rate of both foster parents correlated with the wing patch size of the original female. This implies that original maternal quality had an offspring-mediated indirect effect on investment of foster parents, that is intrinsic nestling quality may constrain parental feeding decisions. This explanation should not be overlooked in future studies on preferential parental investment, and our results also point out that maternal ornaments deserve more attention in such studies.     

Solicitation displays reliably reflect oxidative damage in barn swallow nestlings

Reproduction entails parental decisions over allocation of limiting resources. ‘Begging’ solicitation displays by the offspring have been hypothesised to evolve as reliable indicators of quality, allowing parents to adopt optimal allocation strategies. To function as such, however, begging signals must covary with offspring traits that affect viability. Here we tested whether oxidative damage of nestling barn swallows predicts begging bout duration, call amplitude and intensity of postural displays both under normal food provisioning and under food shortage. Oxidative damage as determined by normal metabolism, pathological conditions and functioning of the immune system can serve as a comprehensive indicator of offspring condition because it can profoundly affect viability, senescence and reproduction. Begging bout duration was negatively predicted by oxidative damage but only after food deprivation. Postural begging negatively covaried with oxidative damage, at least when nestlings were confronted with related nest mates. Plasma antioxidant capacity did not predict begging behaviour. Thus, we show for the first time that behavioural begging covaries with a comprehensive index of chick condition, lending support to reliability of such begging traits also as signals of quality rather than need or hunger only. Future studies are candidate to decouple the effect of hunger state and individual condition on behavioural begging.     

Parental favouritism strategies in the asynchronously hatching European Roller (<Emphasis Type="BoldItalic">Coracias garrulus</Emphasis>)

In altricial birds, resource allocation during early developmental stages is the result of an interaction between parental feeding decisions and scramble competition between nestmates. Hatching asynchrony in birds leads to a pronounced age hierarchy among their offspring. Therefore, whenever parents exert control over resource allocation parents feeding asynchronous broods should simultaneously assess individual offspring internal condition and age. In this study, we first studied whether the highly ultraviolet (UV) reflective body skin of nestlings in the asynchronous European Roller (Coracias garrulus; roller hereafter) relates to nestling quality. In a second stage, we experimentally studied parental biases in food allocation towards senior and junior sibling rollers in relation to a manipulation of UV reflectance of the skin of their offspring. Heavier roller nestlings had less brilliant and less UV saturated skins than weaker nestlings. In our experiment, we found that parents with large broods preferentially fed nestlings presenting skin coloration revealing small body size (i.e. control nestlings) over nestlings presenting skin coloration revealing large body size (i.e. UV-blocked nestlings). Within the brood, we found that parental food allocation strategy depended on nestling age: parents preferentially fed senior nestlings signalling small body size, but did not show preference between control and UV-blocked junior nestlings. These results emphasise that parent rollers use UV cues of offspring quality while balancing the age of their offspring to adjust their feeding strategies, and suggest that parents may adopt finely tuned strategies of control over resource allocation in asynchronous broods.     

The influence of parental age and weather on testosterone concentration and offspring survival in broods of tawny owl Strix aluco

Previous research has suggested that parental condition may affect offspring mortality patterns by affecting offspring testosterone levels. Accordingly, we hypothesized that there is a relationship between offspring testosterone concentration and survival during the early nestling period, and that both are influenced by parent age/experience and by prey availability. We tested our hypothesis on tawny owls Strix aluco in their first and third known breeding seasons, when they bred either in adverse or mild weather conditions, in Duna-Ipoly National Park, Hungary. Plasma testosterone concentrations of the nestlings were analyzed and related to parental condition, hatching order and nestling mortality. Inexperienced parents breeding in all weather conditions and experienced parents breeding in adverse conditions were both in poor condition compared to experienced parents breeding in mild conditions. Parents in poor condition produced broods with large between-sibling differences in testosterone concentrations and their later-hatched nestlings (which had low testosterone levels) died during the early nestling period, whereas parents in good condition produced broods with lower variation in offspring testosterone concentrations and all offspring survived the early nestling period. We discuss environmental influences on the amount of testosterone deposited in eggs, and also how maternal testosterone might induce those mechanisms producing testosterone in the nestlings.Communicated by M. Webster, T. Czeschlik     

Experimental increase in food supply influences the outcome of within-family conflicts in Tengmalm’s owl

Within a family there are conflicts of interest between parents and offspring, and between male and female parents, over the supply of parental care. The observed pattern of parental care is the outcome of negotiations within the family, and may be influenced by environmental factors such as food abundance. We experimentally increased food supply to ten Tengmalm’s owl (Aegolius funereus) nests from hatching to fledging, mimicking natural cached prey. Ten un-supplemented nests served as controls. Parents and offspring were fitted with radio-tags. Food provisioning by parents was measured both in the (1) mid- and (2) late nestling stage and in the (3) early and (4) late post-fledging stage. In response to food supplementation, both males and females reduced food provisioning, but the effect was more pronounced in females. Females generally contributed much less to food provisioning than males, and food supplementation increased the difference between the sexes. Mass loss during the brooding stage was substantially lower for supplemented than for control females. Food supplementation did not improve offspring survival, and had no effect on body measurements of nestlings. In conclusion, parents of both sexes used the increased food supply to reduce the costs of caring for their current offspring, but females responded more strongly than males.