Cheek Patch Research Articles

Attractive and healthy-looking male faces do not show higher immunoreactivity

Previous research has indicated that facial attractiveness may provide cues to the functioning of the immune system. Mating with individuals who have a more effective immune system could lead to a higher reproductive success. Our main aim was to test a possible association between immunoreactivity (stimulated by vaccination) and perceived facial attractiveness and healthiness. We experimentally activated the immune system of healthy men using vaccination against hepatitis A/B and meningococcus and measured levels of specific antibodies (markers of immune system reactivity) before and 30 days after the vaccination. Further, 1 day before the vaccination, we collected their facial photographs that were judged by females for attractiveness, healthiness, and facial skin patches for healthiness. In view of its proposed connection with the functioning of the immune system, we also measured skin colouration (both from the facial photographs and in vivo using a spectrophotometer) and we assessed its role in attractiveness and healthiness judgements. Moreover, we measured the levels of steroid hormones (testosterone and cortisol) and the percentage of adipose tissue, because both are known to have immunomodulatory properties and are related to perceived facial attractiveness and healthiness. We found no significant associations between antibody levels induced by vaccination and perceived facial attractiveness, facial healthiness, or skin healthiness. We also found no significant connections between steroid hormone levels, the amount of adipose tissue, rated characteristics, and antibody levels, except for a small negative effect of cortisol levels on perceived facial healthiness. Higher forehead redness was perceived as less attractive and less healthy and higher cheek patch redness was perceived as less healthy, but no significant association was found between antibody levels and facial colouration. Overall, our results suggest that perceived facial attractiveness, healthiness, and skin patch healthiness provide limited cues to immunoreactivity, and perceived characteristics seem to be related only to cortisol levels and facial colouration.

Born without night: the consequence of the no-night environment on reproductive performance in diurnal zebra finches.

We investigated the consequence of no-night environment (constant light, LL) on reproductive performance in zebra finches in the parent (P) and subsequent (F1) generation. As a measure of the overall effects on metabolic reproductive health, we monitored daily activity behaviour, recorded song and cheek patch size in males, and measured body size and hormone levels. As compared with controls under 12 h light:12 h darkness (12h:12 h LD), both P and F1 pairs showed a compromised reproductive success, as evidenced by fewer fledglings and fewer viable offspring with longer fledging durations, and increased offspring mortality with three successive clutches under LL. The overall negative effect of the no-night environment was increased in the F1 generation. As compared with P pairs, F1 pairs had more failed nesting and breeding attempts, took longer to initiate reproduction, incubated fewer eggs, produced fewer viable offspring with longer fledging duration, and showed increased offspring mortality. Consistent with negative reproductive effects, P males showed significant changes in the motif duration and other spectral features of song, and both F1 and F2 males copied poorly the song of their parent under LL. Plasma corticosterone and sex hormone (testosterone in males and oestradiol in females) levels were significantly lower under LL. Daily plasma melatonin rhythm persisted but with a reduced amplitude under LL. These results demonstrate the importance of night in reproduction in a continuously breeding diurnal species, and give insight into the possible impact on physiology of animals whose surrounding environment is consistently losing the darkness of night.

Male zebra finches exposed to lead (Pb) during development have reduced volume of song nuclei, altered sexual traits, and received less attention from females as adults

Lead (Pb) is a pervasive global contaminant that interferes with sensitive windows for neurological development and causes oxidative damage to tissues. The effects of moderate and high exposure to Pb have been well-studied in birds, but whether low-level early-life exposure to Pb influences adult phenotype remains unclear. Female songbirds use a male's song and coloration to discriminate between high- and low-quality males. Therefore, if early-life exposure to Pb disrupts song learning ability or shifts the allocation of antioxidant pigments away from colorful secondary sexual traits, male birds exposed to Pb may be less attractive to females. We exposed developing zebra finches (Taeniopygia guttata) to Pb-contaminated drinking water (100 or 1000 parts per billion [ppb]) after hatching (days 0–100). Once male finches reached adulthood (120–150 days post hatch), we measured song learning ability, coloration of bill and cheek patches, and volume of song nuclei in the brain. We also measured female preference for Pb-exposed males relative to control males. Finally, we measured motoric and spatial cognitive performance in male and female finches to assess whether cognitive traits differed in their sensitivity to Pb exposure. Male zebra finches exposed to 1000 ppb Pb had impaired song learning ability, reduced volume of song nuclei, bills with less redness and received less attention from females. Additionally, Pb exposure impaired motoric performance in both male and female finches but did not affect performance in a spatial cognitive task. Adult finches exposed to Pb-contaminated water had higher blood-Pb levels, though in all cases blood-Pb levels were below 7.0 µg dL−1. This study suggests that low-level exposure to Pb contributes to cognitive deficits that persist into adulthood and may indirectly influence fitness by altering secondary sexual traits and reducing male attractiveness.

Developmental effects of daily food availability times on song behaviour and neuronal plasticity of song-control system in male zebra finches

Food availability is a major ecological factor and affects body condition and sexual traits. Here, we investigated whether males’ song behaviour, a trait for female mate choice, was sensitive to the food availability period and its timing in songbirds. We manipulated daily food availability to 4 h in the morning or evening, with controls on food ad libitum, and assessed its effects on song behaviour and forebrain song control system in male zebra finches that were held as adult (parent) or offspring (since birth) at 24 ± 2 °C under 12 h daily photoperiod. Food restriction significantly affected both temporal and spectral features of daily song in offspring, not the parent. In offspring, we found reduced mesor (mean 24-h levels), attenuated amplitude (daily maxima relative to mesor) and altered acrophase (estimated time of daily maxima) of 24-h rhythm, and reduced motif length (in morning-fed), per motif unique syllables and an enhanced song pitch (in evening-fed). There was also a positive correlation of motif length with cheek patch and plasma testosterone levels, and of per motif syllables with cheek patch and daily activity levels in offspring. Among main song controlling forebrain nuclei, LMAN and HVC were reduced in size, and Area X and HVC showed decreased neuronal recruitment in offspring on food restrictions. These results demonstrate the importance of daily food availability and its timing in determining males’ sexual signals, and support growing evidence that among vertebrates well-fed males contain reproductive traits that females use for its mate choice.

Female and male plumage colour signals aggression in a dichromatic tropical songbird

Animal signals of competitive ability allow contests for limited resources to be settled without costly physical fights. Traits indicating competitive ability are diverse and span visual, acoustic or chemical modalities. Although animal signalling has been intensively studied, research has focused mainly on male traits. Little is known about the extent and functionality of competitive signals in females and whether there are sex differences in signal function. We studied whether plumage colour signals competitive ability in female and male lovely fairy-wrens, Malurus amabilis. In this species, both sexes sport elaborate but sexually dichromatic ornamental plumage. Using a mirror image stimulation test, we first assessed the relationship between male and female colour and agonistic behaviour, controlling for other physical, social and ecological variables. We then tested whether colourful plumage influenced aggressive response in both sexes by experimentally manipulating plumage colour and measuring individual responses to their mirror image. Females and males were more aggressive towards naturally less colourful reflections of the cheek patch in the mirror. However, when we manipulated plumage colour, both females and males responded more aggressively to experimentally increased cheek colour reflection in the mirror. Our findings suggest that plumage colour signals competitive ability in an aggressive context in both sexes and raises the possibility that signal reliability may be maintained by social interactions where individuals police and punish dishonest signals.

Colour change in a structural ornament is related to individual quality, parasites and mating patterns in the blue tit.

Carry-over effects refer to processes that occur in one season and influence fitness in the following. In birds, two costly activities, namely reproduction and moult, are restricted to a small time window, and sometimes overlap. Thus, colour in newly moulted feathers is likely to be affected by the costs of reproduction. Using models of bird vision we investigated male colour change in a free-living population of blue tits (Cyanistes caeruleus) in three sampling occasions: spring 1, winter and spring 2. We related crown, tail, breast and cheek feather colouration after the moult (winter) to the intensity of infections by blood parasites during reproduction (spring 1). In the following spring (spring 2), we explored mating patterns with respect to changes in feather colour (springs 1 vs. 2). Males that were less intensely infected by the malaria parasite Plasmodium while breeding showed purer white cheek feathers in winter, which may indicate higher feather quality. Increased brightness in the white cheek was associated with better body condition during reproduction. In the following season, males with brighter cheeks paired with females that had noticeably brighter cheek patches compared to the male's previous mate. These results suggest that the conditions experienced during reproduction are likely to affect moult and thus feather colouration, at least in the white patch. High quality individuals may allocate resources efficiently during reproduction increasing future reproductive success through variation in mating patterns. Carry-over effects from reproduction might extend not only to the non-breeding phase, but also to the following breeding season.

Mate choice decision rules: Trait synergisms and preference shifts.

An important and understudied question in sexual selection is how females evaluate information from multiple secondary sexual traits (SSTs), particularly when expression of traits is phenotypically uncorrelated. We performed mate choice experiments on zebra finches (Taeniopygia guttata castanotis Gould) to evaluate two hypotheses: preference shifts (obstacles to choice using one trait increase chooser reliance on others) and trait synergisms (choice based on the sum/product of two or more independently varying traits). The first experiment, which employed males raised on diets that impact SST expression, supported the trait synergism hypothesis: overall, male pairing success was best predicted by synergisms involving beak color and cheek patch size. Results did not support the preference shift hypothesis. Results of a follow‐up experiment that included males reared on a single diet, and in which male beak color and cheek patch size were manipulated, were also consistent with the trait synergism hypothesis. Results have implications for understanding the long‐term persistence of multiple SSTs in populations and for the measurement of repeatability and heritability of mate preferences.

Zebra finch males compensate in plumage ornaments at sexual maturation for a bad start in life.

BackgroundAn individual's fitness in part depends on the characteristics of the mate so that sexually attractive ornaments, as signals of quality, are used in mate choice. Often such ornaments develop already early in life and thus are affected by nutritional conditions experienced then. Individuals thus should benefit by compensating as soon as possible for poor initial development of ornaments, to be attractive already at sexual maturity. Here, we tested whether early nutritional stress affects the cheek patch size of male Zebra finches (Taeniopygia guttata), which are important in mate choice, and whether a small cheek patch size early on is compensated at sexual maturation. Furthermore we tested whether exploration behaviour is affected by such a compensation, as shown for other compensatory growth trajectories.ResultsZebra finch males which were raised under poorer nutritional conditions initially expressed smaller cheek patches at day 50 post-hatching but then compensated in cheek patch size already at 65 days, i.e. when becoming sexually mature. Furthermore, compensatory growth in cheek patch during adolescence was negatively correlated with activity and exploration behaviour, measured in a novel environment.ConclusionThis compensation in cheek patch size benefits male attractiveness but also was related to less exploration behaviour, an established proxy for avian personality traits. We discuss the possibility that compensatory priorities exist so that not all deficits from a bad start are caught-up at the same time. Resource allocation to compensate for poorly expressed traits is likely to have evolved to optimise traits by the time they are most beneficial.

More ornamented females produce higher-quality offspring in a socially monogamous bird: an experimental study in the great tit (Parus major)

IntroductionAnimals are often conspicuously colored and explanations range from aposematism and mimicry to sexual selection. Although sexual selection explains vivid coloration in males, functional significance of vivid coloration in females of socially monogamous species remains unclear. The hypothesis of mutual mate choice predicts that more ornamented females produce offspring of higher quality. We tested this prediction in the great tit (Parus major), a small, insectivorous, socially monogamous passerine.ResultsIn both females and males we quantified three ornaments that have been hypothesized to have signaling role in this species (size of black breast stripe, carotenoid chroma of yellow breast feathers, immaculateness of the white cheek). We swapped broods between nests soon after hatching, thus separating genetic plus pre-hatching vs. post-hatching effects on offspring performance. Body mass of offspring at 14 days of age was positively related to the area of black breast stripe of genetic mothers. Immune response to a novel antigen (phytohaemagglutinin) at 14 days of age was positively related to the immaculateness of the white cheek patch of both genetic and foster mothers.ConclusionsWe showed that females with more elaborate ornaments produced higher-quality offspring and we discuss potential proximate mechanisms of these relationships. We conclude that as more elaborate ornaments were reliable signals of offspring quality, direct selection by male mate choice might have been responsible for the evolution and/or maintenance of these signaling traits in females.

Egg yolk antioxidant deposition as a function of parental ornamentation, age, and environment in great tits Parus major

Females can modify phenotype of their offspring through the deposition of biologically active compounds into eggs, including carotenoids, vitamins and other antioxidants. Understanding patterns of deposition is critical for better insight into the significance of maternal effects. Here we investigated how egg yolk antioxidants (lutein, zeaxanthin, β-carotene, vitamin A and E) related to environmental conditions and parental characteristics in great tits Parus major using data from three breeding seasons. Male and female traits included condition, age and multiple feather ornaments, both carotenoid- and melanin-based (carotenoid and UV chroma of yellow breast feathers, area of black breast band, white cheek immaculateness). Yolk mass increased with ambient temperature during laying, laying date, and the area of male black breast band. Lutein, zeaxanthin, and vitamin E increased with laying date. Total antioxidants increased with female age, immaculateness of female white cheek patch, and UV chroma of carotenoid-based yellow breast feathers of the social mate. These patterns were thus consistent with 1) environmental effects on yolk mass and composition, 2) higher quality females depositing more antioxidants, and 3) differential allocation of resources in females in relation to male ornamentation. Overall, environmental factors, female traits, and male traits all had an influence on egg yolk characteristics in this socially monogamous songbird.

A white feathered area on the forehead is more common in hybrids of Greylag Goose Anser anser and Greater Canada Goose Branta canadensis than in the parent species

This study evaluated prevalence and extent of white areas on heads of Greylag Goose × Greater Canada Goose hybrids. A white area which bordered the bill and then to various degrees extended over the forehead was found in 17 out of 20 hybrids. This was significantly more common in the hybrids than in the parent species. The white areas in the hybrids were also significantly larger than in those 82 out of 191 adult Greylag Geese which had some amount of white area. There were too few Greater Canada Geese with a white area outside the normal pale cheek patch to make a meaningful similar quantitative comparison also with them. No white area was seen in the three presumed 1st Calendar Year (CY) hybrids but when two of them were seen again in September of the 2nd CY there were some pale feathers that were interpreted as the beginning of white areas. The white areas in hybrids are therefore regarded to be adult features which like in several pure Anser species begin to develop during the 2nd CY.

Feather ornaments are dynamic traits in the Great Tit Parus major

In behavioural studies it has been common to quantify plumage colours or ornaments over a range of dates and link them to fitness characteristics without accounting for seasonal changes in these traits. Such changes are likely to be widespread among birds, yet we lack assessments of this variability within individuals. We studied both within‐ and between‐individual temporal changes in Great Tit Parus major ornaments, specifically the melanin‐based black breast stripe and the pigment‐free white cheek patch. During the non‐breeding season both ornaments varied. In juveniles and adult females, the area of the breast stripe first rose and then, from near the end of December, decreased. In adult males there was a linear decrease. In the cheek patch, the irregularity of the cheek borders showed either a linear (adults) or a non‐linear (juveniles) increase as the season progressed. In individuals repeatedly sampled during the same winter, the decrease in the size of the breast stripe was larger for males than females and there was an overall decrease in the regularity of the cheek borders. There was no relationship between the size of the breast stripe and the white cheek patch irregularities or the cheek patch area. These results imply that more attention should be paid to quantification, within individuals, of the components of expression of phenotypic traits. In addition, we suggest that further research should focus on explaining the causes and functions of ornament change.

Stressful Dieting: Nutritional Conditions but Not Compensatory Growth Elevate Corticosterone Levels in Zebra Finch Nestlings and Fledglings

Unfavourable conditions throughout the period of parental care can severely affect growth, reproductive performance, and survival. Yet, individuals may be affected differently, depending on the developmental period during which constraints are experienced. Here we tested whether the nestling phase compared to the fledgling phase is more susceptible to nutritional stress by considering biometry, physiology, sexually selected male ornaments and survival using zebra finches (Taeniopygia guttata) as a model species. As nestlings (day 0–17) or fledglings (day 17–35), subjects were raised either on low or high quality food. A low quality diet resulted in significantly elevated baseline corticosterone titres in both nestlings and fledglings. Subjects showed substantial compensatory growth after they had experienced low quality food as nestlings but catch-up growth did neither lead to elevated baseline corticosterone titres nor did we detect long term effects on biometry, male cheek patch, or survival. The compensation for temporally unfavourable environmental conditions reflects substantial phenotypic plasticity and the results show that costs of catch-up growth were not mediated via corticosterone as a physiological correlate of allostatic load. These findings provide new insights into the mechanisms and plasticity with which animals respond to periods of constraints during development as they may occur in a mistiming of breeding.

The cheek plumage patch is an amplifier of dominance in great tits

Amplifiers are signals that enhance the perception of other signals or cues, but no studies to date provide empirical evidence for the role of these signals in a reproductive context. Here we use the white cheek patch of great tits as a model for studying this issue. Aggressive interactions decrease patch immaculateness, so patch size may be an amplifier of dominance, that is, more clearly reveal status. If so, in high-quality individuals patch size should correlate positively with reproductive success (here estimated by laying date, assuming that the earlier the better), whereas low-quality individuals with a large patch should only more clearly reveal their low quality and thus suffer low reproductive success, which is exactly the pattern found in males. In contrast, the cheek patch does not seem to function as an amplifier in female great tits.

Living with the Past: Nutritional Stress in Juvenile Males Has Immediate Effects on their Plumage Ornaments and on Adult Attractiveness in Zebra Finches

The environmental conditions individuals experience during early development are well known to have fundamental effects on a variety of fitness-relevant traits. Although it is evident that the earliest developmental stages have large effects on fitness, other developmental stages, such as the period when secondary sexual characters develop, might also exert a profound effect on fitness components. Here we show experimentally in male zebra finches, Taeniopygia guttata, that nutritional conditions during this later period have immediate effects on male plumage ornaments and on their attractiveness as adults. Males that had received high quality food during the second month of life, a period when secondary sexual characteristics develop, were significantly more attractive as adults in mate choice tests than siblings supplied with standard food during this period. Preferred males that had experienced better nutritional conditions had larger orange cheek patches when nutritional treatments ended than did unpreferred males. Sexual plumage ornaments of young males thus are honest indicators of nutritional conditions during this period. The mate choice tests with adult birds indicate that nutritional conditions during the period of song learning, brain and gonad development, and moult into adult plumage have persisting effects on male attractiveness. This suggests that the developmental period following nutritional dependence from the parents is just as important in affecting adult attractiveness as are much earlier developmental periods. These findings thus contribute to understanding the origin and consequences of environmentally determined fitness components.

Mate choice in zebra finches: does corticosterone play a role?

The importance of stress as a factor in influencing life history strategies has received considerable attention in recent years, because it appears to have a substantial impact on an individual's behaviour and physiology. Birds respond to environmental and social stressors by the production of corticosterone, a glucocorticoid hormone released by the adrenal gland. In this experiment, we tested whether female zebra finches preferred males selected to produce low or high peak levels of circulating plasma corticosterone. Plasma corticosterone and testosterone levels of the males were recorded, as were morphometric measurements and perch activity. Spectrophotometric measurements were also taken from several putatively sexually selected regions of the males. The females preferred the males from the low corticosterone lines to the high corticosterone males. In addition to, and consistent with this effect, females preferred males with the lowest corticosterone titres. Male activity, testosterone level, body size and mass had no effect on female preference. Leg and beak brightness were important, however, as were the brightness and chromaticity of the male cheek patch. These results are discussed in relation to contemporary hypotheses in sexual selection, particularly in the context of stress-mediated signalling.

Sex and population variation in ultraviolet reflectance of colour patches in Gallotia galloti (Fam. Lacertidae) from Tenerife (Canary Islands)

AbstractSex and population differences in the ultraviolet (UV) reflectance patterns of two phenotypically divergent lacertids from Tenerife, Gallotia galloti eisentrauti and G. g. galloti, are described. Adults in both populations have rows of lateral and ventro‐lateral blue patches on either side of the trunk that show a single peak of reflectance in the near UV. The lateral patches of males are more intensely reflective than those of females, but females have more chromatic and UV‐shifted lateral patches than males. Most G. g. eisentrauti and some G. g. galloti also have blue cheek patches on either side of the gular area. Male cheek patches have reflectance peaks in the near UV, whereas those of females peak in the visible part of the spectrum. The lateral patches of males from the two populations differ in hue but not in intensity, those of G. g. galloti being more UV‐shifted than those of G. g. eisentrauti. Female G. g. galloti have more intensely reflective lateral patches than female G. g. eisentrauti. Interindividual variation in peak wavelength and/or UV chroma is present in both sexes and populations. This is the first demonstration of sexual dichromatism in the UV reflectance of colour patches in a lacertid.

Achromatic Plumage Reflectance, Social Dominance and Female Mate Preference in Black‐Capped Chickadees (Poecile atricapillus)

AbstractIndividual variation in achromatic plumage reflectance of male Black‐capped Chickadees (Poecile atricapillus) is correlated with social rank and reproductive success, suggesting it may play an important role in sexual signaling. We asked whether female chickadees could assess male quality based on plumage, in the absence of information about relative social dominance. Sexually mature but inexperienced females captured during the pair formation period in late fall and early winter were presented with a choice of two unfamiliar, sexually experienced males in separate compartments of an outdoor mate choice arena. Following each preference trial, we released the males into a single compartment and scored their pairwise dominance interactions. In 10 of 11 trials, females spent significantly more time with the male subsequently identified as dominant, despite not witnessing the males interact. Spectral analysis of male plumage reflectance revealed that UV‐chroma of dark body regions (bib, cap and mantle) was significantly greater in dominant, preferred males and that dominant, preferred males had significantly brighter white cheek patches. There were no differences in vocalization rates of preferred and non‐preferred males. These results show that female chickadees can rapidly assess unfamiliar males based on visual cues, and suggest that variation in achromatic plumage functions in sexual signaling.

Immaculate tits: head plumage pattern as an indicator of quality in birds

Great tits, Parus major, display their white cheek patches to one another during intraspecific encounters. We measured the size of these patches and the regularity of their borders (immaculateness) as part of an investigation into their function as signals. Patch size was not significantly related to any of our measures of fitness, but male great tits with more immaculate cheek patches had significantly greater access to a safer feeding site in winter and produced heavier chicks in small woods. Females with more immaculate patches bred significantly earlier in 2 of the 3 years of the study in both large and small woods. We decreased the immaculateness of both sexes with dye and found that competition with other tits significantly increased their exposure to danger when feeding. Factors resulting in reduced immaculateness included ectoparasites, fighting with conspecifics, faster feather wear in young birds and the timing of the autumn moult. Selection for immaculateness by conspecifics may be one mechanism responsible for the evolution of regular head and body patterns in several species of birds and in other animals.

MELANIN BASIS OF ORNAMENTAL FEATHER COLORS IN MALE ZEBRA FINCHES

Abstract The carotenoid-pigmented bill of Zebra Finches (Taeniopygia guttata) has received much recent attention as a sexually selected signal of quality, but these birds also display several sexually dichromatic plumage traits, including rust-colored cheek patches, a black breast band, and brown flanks. Black, brown, and earth-toned features in animals are thought to be produced by melanin pigments, but few studies have identified the melanin content of such colors in bird feathers. We used a series of biochemical techniques to investigate the pigmentary basis of these plumage colors in male Zebra Finches. All three feather traits contained melanin pigments, but varied in the amounts of the two basic forms of melanin (eumelanin and phaeomelanin). Black breast feathers contained predominantly eumelanin, whereas cheek and flank feathers contained extraordinarily high concentrations of phaeomelanin. Conventional methods of carotenoid analysis detected no carotenoids in either the cheek or flank feathers. Co...