Prenatal environmental effects match offspring begging to parental provisioning

The solicitation behaviours performed by dependent young are under selection from the environment created by their parents, as well as wider ecological conditions. Here we show how mechanisms acting before hatching enable canary offspring to adapt their begging behaviour to a variable post-hatching world. Cross-fostering experiments revealed that canary nestling begging intensity is positively correlated with the provisioning level of their own parents (to foster chicks). When we experimentally increased food quality before and during egg laying, mothers showed higher faecal androgen levels and so did their nestlings, even when they were cross-fostered before hatching to be reared by foster mothers that had been exposed to a standard regime of food quality. Higher parental androgen levels were correlated with greater levels of post-hatching parental provisioning and (we have previously shown) increased faecal androgens in chicks were associated with greater begging intensity. We conclude that androgens mediate environmentally induced plasticity in the expression of both parental and offspring traits, which remain correlated as a result of prenatal effects, probably acting within the egg. Offspring can thus adapt their begging intensity to variable family and ecological environments.     

Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks

Avian eggs contain considerable amounts of maternal yolk androgens, which have been shown to beneficially influence the physiology and behaviour of the chick. As androgens may suppress immune functions, they may also entail costs for the chick. This is particularly relevant for colonial species, such as the black-headed gull (Larus ridibundus), in which the aggregation of large numbers of birds during the breeding season enhances the risk of infectious diseases for the hatching chick.To test the effect of maternal yolk androgens on the chick's immune function, we experimentally manipulated, in a field study, yolk androgen levels within the physiological range by in ovo injection of either androgens (testosterone and androstenedione) or sesame oil (control) into freshly laid eggs. We determined cell-mediated immunity (CMI) and humoral immunity of the chicks at the beginning of the nestling period to evaluate early modulatory effects of yolk androgens on immune function.Embryonic exposure to elevated levels of androgens negatively affected both CMI and humoral immunity in nestling gull chicks. Consequently, maternal yolk androgens not only entail benefits of enhanced competitiveness and growth as previously shown, but also costs in terms of immunosuppression. The outcome of embryonic yolk androgen exposure thus likely depends on the post-hatching circumstances for the developing offspring such as parasite exposure and degree of sibling competition.     

Feeding experience and relative size modify the begging strategies of nestlings

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

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

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

Maternal testosterone influences a begging component that makes fathers work harder in chick provisioning

In species with biparental care, parents disagree evolutionarily over the amount of care that each of them is willing to provide to offspring. It has recently been hypothesised that females may try to manipulate their mates by modifying offspring begging behaviour through yolk hormone deposition, shifting the division of labour in their own favour. To test this hypothesis we first investigated how yellow-legged gull (Larus michaellis) parents feed offspring in relation to each component of complex begging behaviour and if feeding behaviour varies between sexes. Then we investigated the effect of yolk testosterone on chicks' begging by experimentally increasing yolk testosterone levels. Our results revealed that yolk testosterone has a component-specific effect on chicks' begging, specifically increasing the number of chatter calls. Parental feeding effort was influenced by the number of chatter calls emitted by chicks, but most importantly, the influence was stronger in male than in female parents. Moreover, chick body mass increased with the number of paternal feeds. In conclusion, these results show that female gulls may use yolk testosterone deposition to exploit their partners as predicted by the ‘Manipulating Androgen Hypothesis (MAH)’.     

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

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

The hormonal control of begging and early aggressive behavior: experiments in black-headed gull chicks

The hormonal control of begging and sibling competition is largely unknown, but recent evidence suggests a role for steroid hormones. We tested the influence of the aromatizable androgen testosterone (T), the non-aromatizable androgen 5alpha-dihydrotestosterone (DHT), and 17beta-estradiol (E) on both begging behavior and aggressive behavior in black-headed gull chicks (Larus ridibundus). Chicks of this species have a conspicuous begging display, while their frequently performed early aggressive behavior is facilitated by testosterone and important for territorial defense. Hormone treatment was applied by implants between days 6 and 16 after hatching. Behavior was tested by means of standard stimulus tests. The results were validated in a second experiment under semi-natural conditions. Begging was suppressed by T and DHT and not affected by E. Aggressive Pecking was strongly facilitated by T. The erect threat posture, characteristic for older chicks, was facilitated by T, DHT, and E and the nest-oriented threat display, typical for young chicks, only by T and DHT. Growth was suppressed in the T group. The results indicate that androgen production, needed for territorial defense, has costs in terms of a suppression of begging and growth. It is discussed to what extent older chicks may avoid these costs by converting testosterone to estrogen and why pre-natal and post-natal exposure to androgens differ in their effect on begging behavior.     

Experimental evidence for offspring learning in parent-offspring communication

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

Parent-offspring conflict and the coordination of siblings in gulls

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

Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks

Eggs of vertebrates contain steroid hormones of maternal origin that may influence offspring performance. Recently, it has been shown that glucocorticoids, which are the main hormones mediating the stress response in vertebrates, are transmitted from the mother to the egg in birds. In addition, mothers with experimentally elevated corticosterone levels lay eggs with larger concentrations of the hormone, which produce slow growing offspring with high activity of the hypothalamo-adrenal axis under acute stress. However, the effects and function of transfer of maternal corticosterone to the eggs are largely unknown. In the present study, we injected corticosterone in freshly laid eggs of yellow-legged gulls (Larus michahellis), thus increasing the concentration of the hormone within its natural range of variation, and analyzed the effect of manipulation on behavioral, morphological, and immune traits of the offspring in the wild. Eggs injected with corticosterone had similar hatching success to controls, but hatched later. Mass loss during incubation was greater for corticosterone-treated eggs, except for the last laid ones. Corticosterone injection reduced rate and loudness of late embryonic vocalizations and the intensity of chick begging display. Tonic immobility response, reflecting innate fearfulness, was unaffected by hormone treatment. Elevated egg corticosterone concentrations depressed T-cell-mediated immunity but had no detectable effects on humoral immune response to a novel antigen, viability at day 10, or growth. Present results suggest that egg corticosterone can affect the behavior and immunity of offspring in birds and disclose a mechanism mediating early maternal effects whereby stress experienced by females may negatively translate to offspring phenotypic quality.     

The Function of Embryonic Vocalization in the Little Tern (Sterna albifrons)

Various functional explanations can be proposed for the evolution of bird embryonic vocalizations during the pre-hatching period, namely: 1. To elicit switching of parents from incubation to parental behaviour typical of the chick period; 2. To allow thermoregulation of embryos by soliciting parents to incubate; or 3. To establish parent—offspring individual recognition. In this paper, we present the results of field experiments designed to test hypotheses 1 and 3 in the colonial, ground-nesting little tern. Parents that had their hatching eggs cross-fostered with foreign eggs at the same hatching stage exhibited a parental behaviour similar to unmanipulated controls. Parents that incubated foreign eggs up to a stage in which embryos were not yet vocalizing, and were challenged with their own hatching eggs that had been incubated in foster nests, performed less efficient parental cares than unmanipulated control pairs and pairs that had cross-fostered hatching eggs. The results do not support the hypothesis of early individual recognition and suggest that embryonic vocalizations in little terns have the function of promoting switching of parents from incubation to accepting and feeding hatchlings. Similar to other tern and gull species, the duration of incubation period in the little tern varies markedly among pairs and years. In these species, embryonic vocalizations can be adaptive since they provide parents a cue to switch at a proper time from incubation to parental cares typical of the chick period.     

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.     

Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks

Maternal effects mediated by egg quality are important sources of offspring phenotypic variation and can influence the course of evolutionary processes. Mothers allocate to the eggs diverse antioxidants that protect the embryo from oxidative stress. In the yellow-legged gull (Larus michahellis), yolk antioxidant capacity varied markedly among clutches and declined considerably with egg laying date. Analysis of bioptic yolk samples from clutches that were subsequently partially cross-fostered revealed a positive effect of yolk antioxidant capacity on embryonic development and chick growth, but not on immunity and begging behaviour, while controlling for parentage and common environment effects. Chick plasma antioxidant capacity varied according to rearing environment, after statistically partitioning out maternal influences mediated by egg quality. Thus, the results of this study indicate that egg antioxidants are important mediators of maternal effects also in wild bird populations, especially during the critical early post-hatching phase.     

Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch

The transfer of non-genetic resources from mother to the offspring often has considerable consequences for offspring performance. In birds, maternally derived hormones are known to influence a variety of morphological, physiological and behavioural traits in the chick. So far, the range of these hormonal effects involves benefits in terms of enhanced growth and competitive ability as well as costs in terms of immunosuppression. However, since yolk hormones can enhance growth and begging activity, high levels of these hormones may also involve energetic costs. Here, we show experimentally that elevated levels of prenatal testosterone increase resting metabolic rate in nestling zebra finches (Taeniopygia guttata). Surprisingly, however, elevation of prenatal testosterone did not result in higher growth rates and, thus, differences in resting metabolism do not seem to be linked to nestling growth. We conclude that apart from immunosuppressive effects, high levels of egg steroids may also entail costs in terms of increased energy expenditure.     

Chick begging as a signal: are nestlings honest?

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

Penguin Chicks Benefit from Elevated Yolk Androgen Levels under Sibling Competition

Crested penguins (genus Eudyptes) have a peculiar hatching pattern, with the first-laid egg (A-egg) hatching after the second-laid egg (B-egg) and chicks from A-eggs typically having a much lower survival probability. Maternal yolk androgens have been suggested to contribute to the competitive superiority of the B-chick in southern rockhopper penguins Eudyptes chrysocome, given their important role in mediating sibling competition in other species. We therefore increased the yolk androgen levels in freshly-laid eggs and examined the consequences for sibling competition - via effects on embryonic developmental times, chick growth and early survival. We placed one androgen-treated egg and one control egg into each foster nest, matching them for mass, laying date and laying order. The androgen treatment did not significantly affect embryonic developmental times or chick measurements at hatching. However, elevated yolk androgen levels benefitted chick growth in interaction with the number of siblings in a brood. Chicks from androgen-treated eggs had faster growth in the presence of a sibling than chicks from control eggs. Under these circumstances they also had a higher survival probability. Thus maternal androgens appear to reinforce the observed hatching pattern, facilitating brood reduction. This contrasts to most previous studies in other species where yolk androgens have been shown to compensate for the negative consequences of delayed hatching within the brood hierarchy.     

Embryonic vocalizations mediate parental care in Masked Lapwings (Vanellus miles) but not Red-capped Plovers (Charadrius ruficapillus)

Embryonic vocalizations in birds may enable communication between embryos and incubating parents but responses of parents to embryonic vocalizations have not been measured experimentally. In two ground-nesting shorebirds, we compare parental care of eggs without embryonic vocalizations, those with natural embryonic vocalizations, and those in which we experimentally introduced embryonic vocalizations, while accounting for prevailing temperatures. We continuously recorded nests (one block of up to 24 h per nest) of two ground-nesting shorebirds, the Red-capped Plover Charadrius ruficapillus and Masked Lapwing Vanellus miles and quantified parental behaviours. We predict an increase in egg thermoregulation behaviours (time spent incubating or shading) and ‘fussing’ (a combination of rising and re-settling, shuffling, orientation change and egg turning) when vocalizations were naturally present or when they were experimentally introduced in comparison to when no vocalizations were present (control). In Lapwings, the rate of fussing increased at the nest only when natural vocalizations were present; however, preening increased when natural or introduced vocalizations were present. Additionally, the frequency of bill to egg touches (inspections) increased only in the presence of introduced vocalizations. For Plovers, treatment had no influence on parental behavioural; however, the frequency of fussing, bill to egg touches and shell tossing increased with air temperature. For both species, there was no influence of the presence of the embryo’s vocalizations (natural or introduced) on the parent’s egg thermoregulation behaviours. Our results highlight that acoustic communication across the eggshell may occur and can influence parental care in shorebirds, but this appears to be species-specific.     

Should a parasite expose itself? (some theoretical aspects of begging and vigilance behavior)

This paper examines the evolutionarily stable (ESS) solution of the begging conflict in cases involving nest parasitization. As expected, the presence in the nest of a parasite chick leads to a more intense begging conflict, with the parasite displaying a more selfish behavior than the host chicks. The model also predicts opposite responses by the host and the parasite to changes in the number of nestmates. While a larger number of nestmates entails a reduced ESS begging intensity for each of the host chicks, it entails an increased begging intensity for the parasite. Consequences of the parasite's ability to disguise itself are compared to analogous results for the vigilance game: whereas in the begging game a parasite should conceal itself, exposure can be selectively advantageous for a defector in the vigilance game.     

Embryonic development within carotenoid-enriched eggs influences the post-hatch carotenoid status of the chicken

Carotenoids in the diet of the laying hen are incorporated into the egg yolk and subsequently into the liver and other tissues of the chicken embryo. Since these pigments are known to provide a range of health benefits to a variety of animals, it is of interest to know whether the effects of maternally derived carotenoids are strictly limited to the embryonic period or if they persist in the progeny after hatching. The aim of this study is to compare the effectiveness of pre-hatch (from the hen's diet) with that of post-hatch (from the progeny's diet) supplementation with carotenoids on the carotenoid status of the chick during the first 4 weeks of post-hatch life. Hens were fed a control diet or a diet supplemented with a carotenoid-rich extract of alfalfa. Eggs from the supplemented hens contained up to 22 times more carotenoids than the controls. The concentration of carotenoids in the livers of chicks hatching from the enriched eggs was initially 29 times greater than in the control chicks. Hepatic carotenoid concentrations in chicks from enriched eggs maintained post-hatch on the control diet were sustained at higher values compared with chicks from control eggs that were fed post-hatch on the carotenoid-supplemented diet, for at least the first 7 days. However, by 14 days, the latter group had overtaken the former in terms of liver carotenoid levels. Thus, under these conditions, maternal effects predominate for at least the first week after hatching, whereas from 2 weeks onwards, the progeny's diet becomes the main determinant of its carotenoid status. Since the antioxidant and immunostimulatory roles of carotenoids are likely to be especially important during the immediate post-hatch period, maternal dietary intake of carotenoids may have important ramifications for the viability of the offspring.     

Trans-Generational Influence of Human Disturbances in Japanese Quail: Egg Quality Influences Male Social and Sexual Behaviour

In many bird species prenatal exposure to yolk androgens of maternal origin has been found to influence offspring behavioural phenotype. In contrast to altricial birds, far less is known about maternal effects in precocial birds. In a previous experiment we found that female quail ( Coturnix japonica ) that were not previously habituated to humans (NH) produced eggs with less androgens (testosterone, androstenedione) and more progesterone when exposed to human disturbances than females habituated to humans (H). Here, we analysed social motivation and sexual behaviour of the male offspring of NH and H females. Classical behavioural test procedures were applied including separation, runway, partner choice and female encounter tests. As chicks, offspring of the NH females spent more time far from conspecifics than offspring of the H females. As adults, the same NH males showed less crowing and courtship behaviour (ritual preening) in female encounter tests than H males. Thus, maternal environment and egg quality may be key factors in the emergence of individual variability of appetitive behaviour, such as social proximity and courtship behaviour. Human disturbance of the mother seems to have triggered trans-generational effects resulting in consistently reduced social and sexual motivation in offspring until adulthood.