Decoding colouration of begging traits by the experimental addition of the appetite enhancer cyproheptadine hydrochloride in magpie Pica pica nestlings

The colouration of some traits in nestlings of altricial birds may influence parental food allocation as it may reflect physical condition or hunger. There is increasing evidence of the relationship between colouration of begging traits and nestling performance. However, evidence of the influence of hunger level on nestling colouration is scarce, mainly because of difficulty of distinguishing between the effects of physical condition and hunger levels. Here, we used the appetite stimulant cyproheptadine hydrochloride to increase the sensation of hunger of magpie Pica pica nestlings for eight days and assessed the effect on the colouration of rictal flanges, mouth and body skin. We found that nestlings administered with cyproheptadine had flanges more conspicuous (chromatic visual contrast), more UV coloured and less yellow coloured than their control nestmates. Conversely, mouths of experimental nestlings were more yellow coloured and less UV coloured than controls. Our pharmacological experiment affected the strength of the relationship between body mass and some colour components of body skin (chromatic and achromatic visual contrasts, UV–chroma and yellow–chroma) and of rictal flanges (chromatic visual contrasts, UV–chroma and yellow–chroma), but not for mouth colouration. These results taken together suggest that the effect of the cyproheptadine on nestling colourations is probably mediated by an increase in hunger levels of nestlings for rictal flanges and body skin colourations, and by an increase in physical condition in the case of mouth coloration.     

Nestling detectability affects parental feeding preferences in a cavity-nesting bird

In many avian species, nestlings have evolved striking plumage, behaviours and mouth colours to obtain a greater share of parental investment. Studies revealing parental feeding preferences for nestlings with red gapes have proposed that red mouth colour in songbirds can act as a signal of nestling need or condition. Alternative hypotheses suggest that bright nestling mouths in cavity-nesting birds evolved to increase nestling detectability by the parents. We tested whether nestling mouth colour affects parental feeding preferences in great tits, Parus major L. In broods of six young, we experimentally painted mouth gapes and flanges either red or yellow and tested the effect of mouth colour on nestlings' mass gain under two lighting conditions. In nests with high luminosity, there was no significant effect of mouth colour on mass gain. In nests with low luminosity, nestlings with red gapes and flanges gained less mass than nestlings with red gapes and yellow flanges or both yellow gapes and flanges. Our results suggest that, in nests with low luminosity, red mouths decreased nestling detectability to the feeding parents and support the hypothesis that poor luminosity in nesting cavities can select for pale mouths. Overall, our results do not support the hypothesis that red mouth colour signals nestling need or condition to parent great tits.     

Mouth coloration of nestlings covaries with offspring quality and influences parental feeding behavior

Altricial nestlings compete with their nest mates for resourcesdelivered by parents. Parents may allocate food to nestlingsbased on reproductive value of offspring. To test the hypothesisthat mouth coloration acts as a signal of nestling conditionin the barn swallow Hirundo rustica, we investigated whethergape coloration is correlated with offspring quality and age.We also examined the role of ultraviolet (UV) flange colorationin parental allocation in a manipulative experiment. Mouth colorationchanged with age, probably due to accumulation of dietary carotenoidsin the tissue and an increase in the number of collagen layers.Highly UV and redder palates and brighter flanges were associatedwith longer tarsi and greater body mass at day 6 and with feathergrowth at day 12 posthatching. Although we did not find evidencethat UV coloration of flanges is associated with nestling quality,parents preferentially fed young whose flanges reflected higherUV light, compared with experimentally UV-filtered nestlings.These results support the hypothesis that mouth coloration isa reliable signal of nestling condition. In addition, they showthat UV flange coloration influences parental decisions regardingfood allocation.     

Nestling colouration is adjusted to parent visual performance in altricial birds

Hitherto, most of the investigation on the perceptual efficacy of begging signals has dwelled on how patterns of nestling colouration adjust to predominant nest luminosity. However, visual sensitivity of birds varies across species, which raises the question of whether colouration of traits involved in begging displays is adjusted to parent visual capacities. Here, by comparing nestling colouration and visual sensitivity across 22 altricial bird species, we provide a first test of this hypothesis. Firstly, we assessed differences in performance of typical UV‐tuned and violet‐tuned bird eyes when looking at the nestling traits under the light regimes prevailing at their nests. Secondly, while controlling for common ancestry in a comparative approach, we explored variation in colouration of nestlings in relation to parent visual system. The colour discrimination model indicated a general higher performance of the ultraviolet over the violet eye at detecting gape and body skin traits in either open‐ or hole‐nest light conditions. Gape colouration was associated with parental visual system as the nestlings of UVS species displayed more yellow and less pure ultraviolet mouths than the nestlings of VS species. Thus, our results agree with an adaptive parent–offspring communication scenario where the nestlings’ colours tuned the perception capacities of their parents.     

Nestling birds put their best flange forward

The offspring of caring parents may evolve specialized traits uniquely adaptive during their dependence on parental care. For example, the mouths of passerine nestlings are often bordered by enlarged and colorful rictal flanges expressed only during the nestling period. Although these traits are commonly hypothesized to act as visual signals during begging, non‐communication functions for the specialized mouth have been proposed as well. To test the hypothesis that nestling flange colors have evolved largely or exclusively as visual signals, I compared the reflectance of flange tissue that would be visible to parents during begging to that of flange tissue not exposed during begging in nestling house sparrows Passer domesticus and cliff swallows Petrochelidon pyrrhonota. Specifically, I tested the prediction that both condition‐dependent color parameters and those associated with visual conspicuousness would be expressed more intensely in tissue displayed during begging. Consistent with this prediction, flange tissue exposed during begging was brighter (reflected more total light), more UV‐rich, and had more intense carotenoid‐based coloration than hidden tissue. These differences do not exclude a non‐signaling function for flanges, but are consistent with the hypothesis that flange colors have evolved as visual signals.     

Intensity of mouth coloration in Blackcap Sylvia atricapilla nestlings affects food distribution among siblings but not provisioning of the whole brood

Among various begging stimuli, mouth coloration has received increasing attention in recent years, and previous research has demonstrated that mouths of nestling Canaries Serinus canaria get redder with the extent of food deprivation and that parents preferentially feed nestlings of redder gapes. This study assesses whether the intensity of red mouth colour in nestling Blackcaps Sylvia atricapilla is a signal in parent–offspring communication. This is one of the few species with a naturally red gape in which the function of mouth redness has been tested. Three predictions were experimentally tested: (1) reddening the gape of a single nestling within a brood increases its provisioning in relation to other siblings; (2) reddening the gapes of all nestlings within a brood increases parental feeding rate; and (3) food deprivation increases nestling mouth redness. The effect of nestling quality on mouth redness was also assessed. The intensity of gape coloration affected food distribution, but in a way opposite to that expected: an increase in mouth redness of the nestling caused reduced feeding by parents. However, reddening the gapes of all nestlings had no effect on provisioning of the whole brood, suggesting that Blackcap parents use different cues for provisioning particular nestlings and the whole brood. Intensity of mouth redness in Blackcap nestlings was not affected either by food deprivation or by nestling quality in terms of mass and rank in the nest.     

Detectability matters: conspicuous nestling mouth colours make prey transfer easier for parents in a cavity nesting bird

An often underappreciated function of signals is to notify receivers of the presence and position of senders. The colours that ornament the mouthparts of nestling birds, for example, have been hypothesized to evolve via selective pressure generated by parents'' inability to efficiently detect and feed nestlings without such visually conspicuous targets. This proposed mechanism has primarily been evaluated with comparative studies and experimental tests for parental allocation bias, leaving untested the central assumption of this detectability hypothesis, that provisioning offspring is a visually challenging task for avian parents and conspicuous mouths help. To test this assumption, I manipulated the mouths of nestling house sparrows to appear minimally and maximally conspicuous, and quantified prey transfer difficulty as the total duration of a feeding event and the number of transfer attempts required. Prey transfer to inconspicuous nestlings was, as predicted, more difficult. While this suggests that detectability constraints could shape nestling mouth colour evolution, even minimally conspicuous nestlings were not prohibitively difficult for parents to feed, indicating that a more nuanced explanation for interspecific diversity in this trait is needed.     

A comparative study of host selection in the European cuckoo Cuculus canorus

Certain kinds of hosts are commonly regarded as being more suitable than other for rearing European cuckoos (Cuculus canorus) – insectivores that lay small eggs and have open, shallow nests – although empirical tests of cuckoo host selection are lacking. We analysed host use by the European cuckoo in 72 British passerines that are potential hosts and for which there was information available on life-history variables and variables related to cuckoo-host coevolution, such as rate of parasitism, rejection rate of non-mimetic model eggs and degree of cuckoo-egg mimicry of host eggs. The relative population size of the host species affected parasitism rate most strongly, followed by relatively short duration of the nestling period, and the kind of nest, with cuckoos selecting open-nesting hosts. However, the effect of the nestling period could be related to host body size and the kind of nest used, because hole-nesting species normally have longer nestling periods than open-nesters. We re-analysed the data excluding hole nesters and corvid species (species with larger body mass), but the results remained identical. The European cuckoo may benefit from selecting hosts with short nestling periods because such hosts provide food for their nestlings at a very high rate. When only those species known as cuckoo hosts were analysed, the variable that best accounted for the parasitism rate was duration of the breeding season. Therefore, availability of potential hosts in both time and space is important for cuckoos in selecting hosts. Received: 16 July 1998 / Accepted: 27 October 1998     

Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds

The colors of fruits and flowers are traditionally viewed as an adaptation to increase the detectability of plant organs to animal vectors. The detectability of visual signals increases with increasing contrasts between target and background. Contrasts consist of a chromatic aspect (color) and an achromatic aspect (light intensity), which are perceived separately by animals. To evaluate the relative importance of fruits’ chromatic and achromatic contrasts for the detection by avian fruit consumers we conducted an experiment with artificial fruits of four different colors in a tropical forest. We displayed the fruits against two different backgrounds, an artificial background and a natural one, because they differed in achromatic properties. We found no effect of the type of background on fruit detection rates. Detection rates differed for the four fruit colors. The probability of detection was explained by the chromatic contrast between fruits and their background, not by the achromatic contrasts. We suggest that birds attend primarily to chromatic contrast probably because these are more reliably detected under variable light conditions. Consistent with this hypothesis, we found habitat-specific differences in the conspicuousness of natural fruit colors in the study area. Fruits of understory species that are subjected to the variable light conditions within a forest displayed higher chromatic contrasts than species growing in the open restinga forest with constant bright illumination. There was no such difference for achromatic contrasts. In sum, we suggest that fruit colors differ between habitats because fruit colors that have strong chromatic contrasts against background can increase plants’ reproductive success, particularly under variable light conditions.     

Parental preference for red mouth of chicks in a songbird

Parental preferences during feeding and care-giving may select for ornamental traits in young, such as bright coloration. For chicks of coots, there is experimental evidence for this idea. We examined the hypothesis that bright yellow, orange and red mouths of chicks of songbirds have been favoured by feeding preferences in parents. In a field experiment, the orange–yellow mouths of great tit nestlings were dyed brightly red, and the feeding response of parents recorded. In nest boxes with extra daylight through a window, experimental chicks were on average given twice as much food (biomass) as control chicks (sham dyed). In normal nest boxes, the tendency was similar, but not significant. Thus, at least in good light, great tit parents prefer to feed young with red mouths, a preference for colourfulness that helps explain the evolution of bright gapes in chicks of songbirds (passerine birds).     

Supplemental food increases ornamentation of male nestling Eastern Bluebirds

Although the condition‐dependence and signaling function of ornamental plumage coloration among adult males is well studied, less research has focused on the information content of ornamental coloration among juvenile birds. Eastern Bluebird (Sialia sialis) nestlings grow their nuptial plumage while in the nest and dependent on parents for food, making them an ideal species for studying the development and function of elaborate plumage. Previous research suggests that plumage brightness of Eastern Bluebirds functions, in the juvenile stage, in parent–offspring interactions as a sexually selected trait in adults. Using an experimental approach, we tested the effects of supplemental food on the structural plumage coloration (i.e., tips of primary feathers) of Eastern Bluebird nestlings in Watauga County, North Carolina, during the 2011 breeding season. We provided supplemental mealworms daily to breeding pairs from the onset of incubation through the nestling period, and measured plumage brightness, UV chroma, and mass of nestlings (N = 89 males and 71 females). Male nestlings of supplementally fed parents exhibited brighter plumage. The mass and UV chroma of young bluebirds were not significantly affected by food supplementation. However, the relationship between mass and brightness differed between male nestlings in the control and supplementally fed treatments. Males reared in food‐supplemented territories exhibited a positive relationship between color and mass. Nestlings in control territories, however, exhibited a negative relationship between size and brightness, suggesting that reduced food availability results in a tradeoff between allocating resources toward somatic growth and development of bright plumage. Our results suggest that UV‐blue structural plumage in male juvenile Eastern Bluebirds is at least partially condition‐dependent and may help to explain why plumage color can influence social interactions in Eastern Bluebirds.     

Mouth Color Signals Thermal State of Nestling Dark-Eyed Juncos (Junco hyemalis)

In many species of birds, nestlings have brightly colored mouths. Some studies have found that mouth color is related to hunger, and may serve to solicit feedings from parents. We devised two experiments to test the hypothesis that mouth color is an indicator of hunger in nestling dark‐eyed juncos (Junco hyemalis), and neither experiment produced results to support the hypothesis. We did find, however, that mouth redness saturation increased for the duration of our experiments (60 min). We devised a third experiment to investigate the effect of a different stressor, temperature. In the third experiment, mouth redness decreased in saturation when microenvironment temperature increased following a period of cooling. These findings suggest that mouth color indicates thermal state of nestling dark‐eyed juncos and may function as a signal to the female to brood them.     

Phenotypic variation in nestlings of a bird of prey under contrasting breeding and diet conditions

Environmental conditions often vary in space and time, and this may explain variation in the expression of phenotypic traits related to individual quality, such as ornamental coloration. Furthermore, the direction and strength of the relationship between coloured trait expression and individual quality might vary under contrasting conditions. These issues have been explored in adult birds but much less so in nestlings, which are more likely to experience different selective pressures and different physiological trade‐offs than adults. Here, we empirically investigated the effects of contrasting breeding and diet conditions on the expression of carotenoid‐based colour traits displayed by marsh harrier (Circus aeruginosus) nestlings. We studied the variation in coloration, body condition, and immune responsiveness of nestlings in four populations over a 5‐year period. We characterized spatiotemporal differences in rearing conditions experienced by C. aeruginosus nestlings in terms of breeding (laying date, clutch size, and number of nestlings hatched and fledged) and diet (percentage of mammal in diet and prey diversity) conditions. We found that breeding conditions influenced the co‐variation between coloration and immune responsiveness in female nestlings, and that diet conditions influenced the condition‐dependence of nestling coloration in later‐hatched nestlings. In addition, breeding conditions influenced nestling body condition and immune responsiveness, whereas diet conditions influenced nestling coloration and body condition. Our study highlights that nestling phenotype (levels of signalling, circulating carotenoids, and immunity) varies both spatially and temporally, and that some of this variation is related to differences in breeding and diet conditions. Moreover, under contrasting conditions, the direction of the relationships between nestling carotenoid‐based coloration and nestling quality may also vary. In order to fully understand the evolution and maintenance of colour traits in nestling birds, studies and experiments should ideally be replicated under contrasting rearing conditions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Condition-dependent effects of corticosterone on a carotenoid-based begging signal in house sparrows

Begging is a complex display involving a variety of different visual and auditory signals. Parents are thought to use these signals to adjust their investment in food provisioning. The mechanisms that ensure the honesty of begging displays as indicators of need have been recently investigated. It has been shown that levels of corticosterone (Cort), the hormone released during the stress response, increase during food shortage and are associated with an increased begging rate. In a recent study in house sparrows, although exogenous Cort increased begging rate, parents did not accordingly adjust their provisioning rate. Here, we tested the hypothesis that Cort might affect the expression of other components of begging displays, such as flange color (a carotenoid-based trait). We experimentally increased levels of circulating Cort and investigated the effects of the treatment on (1) the flange coloration of the nestlings, (2) the behavioral response and (3) the parental allocation of food and (4) nestling condition and cell-mediated immune response. We found that Cort affected flange coloration in a condition-dependent way. Cort-injected nestlings had less yellow flanges than controls only when in poor body condition. Parental feeding rate was also affected by the Cort treatment in interaction with flange color. Feeding rate of Cort-injected nestlings was negatively and significantly correlated with flange color (nestlings with yellower flanges receiving more food), whereas feeding rate and flange color were not correlated in control chicks. We also found that nestlings injected with Cort showed a weaker immune response than controls. These results suggest that, indeed, Cort has the potential to affect multiple components of the begging display. As Cort levels naturally raise during fasting, parents have to take into account these multiple components to take a decision as to optimally share their investment among competing nestlings.     

Carotenoids in nestling Montagu’s harriers: variations according to age, sex, body condition and evidence for diet-related limitations

Carotenoids are colored pigments forming the basis of many avian social traits. Before their utilization carotenoids must be acquired through diet and mobilized for specific uses. The relationships between carotenoid-based coloration, circulating carotenoids and body condition have been well studied in adult birds, but little is known in nestlings. Here, we investigated variations in carotenoid-based coloration in a raptor nestling, the Montagu’s harrier (Circus pygargus), both in captivity and in natural conditions, and within a vole (poor-carotenoid source and cyclic prey) specialist population. We studied these variations according to nestling age and sex, and possible limitations in carotenoid availability by comparing years of contrasted prey abundance and using carotenoid supplementation experiments. Captive nestlings, fed only with mice, were strongly carotenoid limited. Wild nestlings were also carotenoid limited, especially in a year of high vole abundance. Nestlings were in better condition but less colored during a peak vole abundance year than during a low vole abundance year, when harriers targeted more alternative preys (birds, insects). Thus, variation in vole abundance resulted in a de-coupling of body condition and carotenoid-based coloration in this population. This suggested that the positive relation between the body condition and carotenoid-based traits, typically found in adult birds, could be restricted to adults or nestlings of species that feed on carotenoid-rich food. Our results should stimulate more work on the functions and mechanisms of carotenoid-based traits in nestlings, which deserve more attention and most likely differ from those of adult birds.     

Factors Affecting the Duration of Nestling Period and Fledging Order in Tengmalm’s Owl (Aegolius funereus): Effect of Wing Length and Hatching Sequence

In altricial birds, the nestling period is an important part of the breeding phase because the juveniles may spend quite a long time in the nest, with associated high energy costs for the parents. The length of the nestling period can be variable and its duration may be influenced by both biotic and abiotic factors; however, studies of this have mostly been undertaken on passerine birds. We studied individual duration of nestling period of 98 Tengmalm’s owl chicks (Aegolius funereus) at 27 nests during five breeding seasons using a camera and chip system and radio-telemetry. We found the nestlings stayed in the nest box for 27 – 38 days from hatching (mean ± SD, 32.4 ± 2.2 days). The individual duration of nestling period was negatively related to wing length, but no formally significant effect was found for body weight, sex, prey availability and/or weather conditions. The fledging sequence of individual nestlings was primarily related to hatching order; no relationship with wing length and/or other factors was found in this case. We suggest the length of wing is the most important measure of body condition and individual quality in Tengmalm’s owl young determining the duration of the nestling period. Other differences from passerines (e.g., the lack of effect of weather or prey availability on nestling period) are considered likely to be due to different life-history traits, in particular different food habits and nesting sites and greater risk of nest predation among passerines.     

No evidence for survival selection on carotenoid-based nestling coloration in great tits (Parus major)

In several vertebrate species evidence supports the hypothesis that carotenoid-based coloration of adults has evolved due to sexual selection. However, in some birds already the nestlings display carotenoid-based coloration. Because the nestling's body plumage is typically moulted before the first reproductive event, sexual selection cannot explain the evolution of these carotenoid-based traits. This suggests that natural selection might be the reason for its evolution. Here we test whether the carotenoid-based nestling coloration of great tits (Parus major) predicts survival after fledging. Contrary to our expectation, the carotenoid-based plumage coloration was not related to short- nor to long-term survival in the studied population. Additionally, no prefledging selection was detectable in an earlier study. This indicates that the carotenoid-based coloration of nestling great tits is currently not under natural selection and it suggests that past selection pressures or selection acting on correlated traits may have led to its evolution.     

Effects of common origin and common environment on nestling plumage coloration in the great tit (Parus major)

Abstract.— Carotenoids cannot be synthesized by birds and thus have to be ingested with food, suggesting that ca-rotenoid-based plumage coloration is environmentally determined. However signaling functions ascribed to plumage imply that plumage coloration is the outcome of an evolutionary process based on genetic variation. By means of a cross-fostering design we show significant effects of both a common rearing environment and the brood from which a nestling originally came from (common origin) on the plumage coloration of nestling great tits ( Parus major ). This demonstration of origin-related variation in carotenoid-based plumage coloration suggests that the observed variation of the trait has a partial genetic basis. Consistent with environmental determination of this trait, we also found a significant positive correlation between the color saturation of nestlings and their foster-father's plumage. There was no significant correlation between nestling plumage coloration and the food quantity provided to the nestlings by the male, the female, or both parents. This suggests that the nestling-foster father correlation arises by the carotenoid quantity ingested rather than the food quantity per se. No significant nestling-true father correlation was found, which suggests that nestling plumage coloration did not indirectly evolve due to sexual selection. Consistent with this result there was no significant correlation between the nestling's plumage color and its coloration as a breeding adult the following year, suggesting that nestling plumage color is a different trait than the first year plumage.     

Carotenoid-based coloration, condition, and immune responsiveness in the nestlings of a sexually dimorphic bird of prey

In many birds, nestlings exhibit brightly colored traits that are pigmented by carotenoids. Carotenoids are diet limited and also serve important health-related physiological functions. The proximate mechanisms behind the expression of these carotenoid-pigmented traits are still poorly known, especially in nestlings with sexual size dimorphism. In these nestlings, intrabrood competition levels and growth strategies likely differ between sexes, and this may in turn influence carotenoid allocation rules. We used dietary carotenoid supplementation to test whether wild marsh harrier (Circus aeruginosus) nestlings were carotenoid limited and whether carotenoid allocation strategies varied between sexes, which differ in their size and growth strategies. When supplemented, nestlings used the supplemental carotenoids to increase their coloration independently of their sex. We showed that the condition dependence of the carotenoid level and the response to an immune challenge (phytohemagglutinin test) differed between sexes, possibly because sexual size dimorphism influences growth strategies and/or intrabrood competition levels and access to different types of food. In this species, which often feeds on mammals, a trade-off likely exists between food quantity (energy) and quality (carotenoid content). Finally, carotenoid-based coloration expressed in marsh harrier nestlings appeared to be indicative of immune responsiveness rather than condition, therefore potentially advertising to parents nestling quality or value rather than nutritional need.     

Cross‐fostering reveals that among‐brood differences in ornamental mouth coloration mostly reflect rearing conditions in nestling house sparrows

Dependent offspring use specialized traits to attract parental care. In birds, this includes morphological ornaments (e.g. colourful plumage or mouthparts) that are associated with nestling condition and shape the allocation of parental care. Ornament expression often differs among broods, even after differences in individual condition are accounted for statistically. Understanding how this variation arises is important for understanding the information content of these signals, their functional importance, and their evolution. The present study used a cross‐fostering experiment to assess the relative contributions of parental effects to among‐brood differences in the mouth coloration of nestling house sparrows, specifically the carotenoid‐richness, overall brightness, and ultraviolet (UV) coloration of rictal flanges. The expression of carotenoid‐based coloration was explained by synchronous breeding, nest‐of‐rearing and nest‐of‐origin. Brightness and relative UV intensity, however, were explained only by synchronous breeding, and there was substantial unexplained variation in all three colour parameters. Among‐brood variation in mouth coloration, then, may primarily contain information about the environment in which offspring are reared. At the individual level, ontogenetic changes in the carotenoid‐richness and brightness of flanges positively reflected mass gain (a proxy for food intake). Larger and yellower chicks gained more mass, consistent with parental preferences for these traits. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 169–179.