Optical properties of the uropygial gland secretion: no evidence for UV cosmetics in birds

Ultraviolet (UV) reflectance of the plumage is common in birds and plays an important role in sexual signalling. Recently, it has been proposed that birds are able to modify plumage UV reflectance by the application of uropygial gland secretion. Based on a survey of the optical properties of this secretion from 51 species belonging to 12 avian orders, we show that two main types of uropygial secretions exist, one predominantly found in passerines and one in non-passerines, both reducing relative UV reflectance of a white background (Teflon™ tape). We quantified how each type of secretion (exemplified by blue tit and mallard) affected feather UV reflectance. Both secretions reduced overall brightness and relative UV reflectance of white mallard feathers but hardly affected the reflectance of UV/blue blue tit crown feathers. According to models of avian colour vision, changes in reflectance due to application of the secretion were at or below the discrimination threshold of most birds. We conclude that the uropygial secretion is unlikely to play a major role in modifying plumage UV reflectance. However, the optical properties of the uropygial secretion may have been selected to interfere as little as possible with visual signaling through plumage reflectance. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Parental conflict and blue egg coloration in a seabird

When both parents provide offspring care, equal sharing of costly parental duties may enhance reproductive success. This is crucial for longlived species, where increased parental effort in current reproduction profoundly affects future reproduction. Indication of reproductive value or willingness to invest in reproduction may promote matching responses by mates, thus reducing the conflict over care. In birds with biparental care, blue-green eggshell color may function as a signal of reproductive value that affects parental effort, as predicted by the signaling hypothesis of blue-green eggshell coloration. However, this hypothesis has not been explored during incubation, when the potential stimulus of egg color is present, and has been little studied in longlived birds. We experimentally studied if egg color affected incubation patterns in the blue-footed booby, a longlived species with biparental care and blue eggs. We exchanged fresh eggs between nests of the same laying date and recorded parental incubation effort on the following 4 days. Although egg color did not affect male effort, original eggshell color was correlated with pair matching in incubation. Exchanged eggshell color did not affect incubation patterns. This suggests that biliverdin-based egg coloration reflects female quality features that are associated with pair incubation effort or that blue-footed boobies mate assortatively high-quality pairs incubating more colorful clutches. An intriguing possibility is that egg coloration facilitates an equal sharing of incubation, the signal being functional only during a short period close to laying. Results also suggest that indication of reproductive value reduces the conflict over care.     

Experimental evidence that keeping eggs dry is a mechanism for the antimicrobial effects of avian incubation

Avian incubation dramatically reduces the abundance and diversity of microbial assemblages on eggshells, and this effect has been hypothesized as an adaptive explanation for partial incubation, the bouts of incubation that some birds perform during the egg-laying period. However, the mechanisms for these antimicrobial effects are largely unknown. In this study, we hypothesized that microbial inhibition is partly achieved through removal of liquid water, which generally enhances microbial growth, from eggshells, and experimentally tested this hypothesis in two ways. First, we placed the first- and second-laid eggs of tree swallow (Tachycineta bicolor) clutches in unincubated holding nests with either ambient or increased water on eggshells. Second, we added water to eggshells in naturally partially incubated nests. We compared microbial growth on shells during a 5-day experimental period and found that, as predicted, both unincubated groups had higher microbial growth than naturally partially incubated controls, and that only in the absence of incubation did wetted eggs have higher microbial growth than unwetted eggs. Thus, we have shown that water increases microbial growth on eggshells and that incubation nullifies these effects, suggesting that removal of water from egg surfaces is one proximate mechanism for the antimicrobial effects of incubation.     

Preen gland removal increases plumage bacterial load but not that of feather-degrading bacteria

The preen gland is a holocrine sebaceous gland of the avian integument which produces an oily secretion that is spread on the plumage during preening. It has been suggested that birds may defend themselves against feather-degrading bacteria (FDB) and other potential pathogens using preen gland secretions. However, besides some in vitro studies, the in vivo bacterial inhibitory effects of the preen oil on the abundance of feather-associated bacterial species has not yet been studied in passerines. Here we tested the effect of gland removal on the abundance of FDB and other-cultivable bacterial loads (OCB) of male house sparrows (Passer domesticus). Our results did not support earlier results on in vitro antibacterial activity of preen oil against FDB since the absence of the preen gland did not significantly affect their loads related to the control birds. In contrast, we found that preen gland removal led to higher loads of OCB. This result suggests that the antimicrobial spectrum of the preen oil is broader than previously thought and that, by reducing the overall feather bacterial loads, the preen gland could help birds to protect themselves against a variety of potentially harmful bacteria.     

Sexually dichromatic coloration reflects size and immunocompetence in female Spanish terrapins, Mauremys leprosa

Many studies have shown the importance of colorful ornamentation in mate choosiness or intrasexual conflict. However, research on color ornaments has focused mainly on birds, lizards or fish, but remains practically unknown in other animal groups such as turtles. In addition, female ornaments and their relation with sexual selection also remain almost unknown. Here, we measured the coloration of the shell and the limb stripes of male and female Spanish terrapins Mauremys leprosa and explored the existence of sexual dichromatism and the relation of color characteristics with body size and health state estimated from the immune response to the injection of an antigen (phytohaemagglutinin test). Our results showed that shell coloration, which could be constrained by natural selection to be cryptic, changed with body size, but did not differ between sexes. In contrast, females had brighter and less ultraviolet-saturated and more orange-saturated limb stripes than males. In females, interindividual variation in limb stripe coloration was related with body size and immune response suggesting that this coloration may inform honestly about multiple traits that could be important in sexual selection. In contrast, coloration of limb stripes of males was duller than in females, and was not related with any trait suggesting that coloration is not important in sexual selection for males.     

Moorhens have an internal representation of their own eggs

How do birds recognize their own eggs? Do they have a stored template for their own egg characteristics, or do they use another mechanism? Intraspecific brood parasitism is considered to be an additional reproductive tactic where females can increase their own reproductive success. Because of the costs involved in rearing young that are not their own, it will pay females to detect and reject the eggs of a parasite, although it is not known how they do this. Here, we show experimentally that moorhens will cease laying in a nest when their first egg is replaced with another hen’s egg but not when it is replaced with their own egg taken from an earlier clutch. This provides good evidence that birds have an internal representation of their own eggs and use this in decisions about whether to reject foreign eggs.     

Parasites and health affect multiple sexual signals in male common wall lizards, Podarcis muralis

Multiple advertising sexual traits may either advertise different characteristics of male condition or be redundant to reinforce reliability of signals. Research has focused on multiple visual traits. However, in animals that use different multiple additional sensory systems, such as chemoreception, different types of traits might have evolved to signal similar characteristics of a male quality using different sensory channels. We examined whether ventral coloration and chemicals in femoral gland secretions of male common wall lizards, Podarcis muralis, are affected by their health state (blood-parasite load and cell-mediated immune response). Our results indicated that less parasitized lizards had brighter and more yellowish ventral colorations and also femoral secretions with higher proportions of two esters of octadecenoic acid. In addition, lizards with a greater immune response had more saturated coloration and secretions with higher proportions of octadecenoic acid methyl ester. We suggest that these signals would be reliable because only healthier males seemed able to allocate more carotenoids to coloration and presumably costly chemicals to secretions. The use of multiple sensory channels may provide more opportunities to signal a male quality under different circumstances, but also may reinforce the reliability of the signal when both types of traits may be perceived simultaneously.     

Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch

The Hamilton-Zuk hypothesis proposes that the bright colours displayed by many species of birds serve as signals of individual resistance to parasites. Despite the popularity of this hypothesis, only one previous study has tested whether plumage coloration predicts how individuals respond to a disease challenge. We inoculated 24 male house finches (Carpodacus mexicanus) of variable plumage hue with a novel bacterial pathogen, Mycoplasma gallicepticum (MG). We found no relationship between plumage hue and time to first symptoms following inoculation, but we found a significant negative relationship between plumage hue and clearance of disease: males with redder plumage cleared MG infection significantly better than did males with yellower plumage. The hue of carotenoid-based plumage coloration has been shown to be a primary criterion in female mate choice in the house finch. These observations suggest that one benefit to females for choosing redder males is obtaining mates with better resistance to parasites.     

Carotenoid-dependent coloration of male American kestrels predicts ability to reduce parasitic infections

The signaling function of sexually selected traits, such as carotenoid-dependent avian plumage coloration, has received a great deal of recent attention especially with respect to parasitism and immunocompetence. We argue that parasite-mediated models of sexual selection may have an implicit temporal component that many researchers have ignored. For example, previous studies have demonstrated that carotenoid-dependent traits can signal past parasite exposure, current levels of parasitism, or the ability of individuals to manage parasitic infections in the future. We examined repeated measures of carotenoid-dependent skin color and blood parasitism in American kestrels (Falco sparverius) to distinguish whether coloration might signal current parasitism or the potential to deal with infections in the future. We found no evidence that coloration was related to current levels of parasitism in either sex. However, coloration of males significantly predicted their response to parasitism; males with bright orange coloration during prelaying, when mate choice is occurring, were more likely than dull yellow males to reduce their levels of infection by the time incubation began. Coloration during prelaying may advertise a male’s health later in the breeding season. For kestrels, the ability to predict future health would be highly beneficial given the male’s role in providing food to his mate and offspring. Coloration of females was not a significant predictor of parasitism in the future, and we provide several possible explanations for this result.     

Reassessing the role of the honeybee (Apis mellifera) Dufour's gland in egg marking

Dufour's gland secretion may allow worker honeybees to discriminate between queen-laid and worker-laid eggs. To investigate this, we combined the chemical analysis of individually treated eggs with an egg removal bioassay. We partitioned queen Dufour's gland into hydrocarbon and ester fractions. The bioassay showed that worker-laid eggs treated with either whole gland extract, ester fraction or synthetic gland esters were removed more slowly than untreated worker-laid eggs. However, the effect only lasted up to 20 h. Worker-laid eggs treated with the hydrocarbon fraction were removed at the same rate as untreated eggs. The amount of ester which reduced the egg removal rate was far higher than that naturally found on queen-laid or worker-laid eggs, and at natural ester levels no effect was found. Our results indicate that esters or hydrocarbons probably do not function as the signal by which eggs can be discriminated.     

Color polymorphism in a land snail Cepaea nemoralis (Pulmonata: Helicidae) as viewed by potential avian predators

Avian predation is one of the most probable factors maintaining polymorphism of shell coloration in Cepaea nemoralis. This assumption is justified by the fact that birds frequently forage on snails and their prey choice varies with morph coloration. However, in all preceding studies, the conspicuousness of morphs was determined only by using human vision which is significantly different from birds’ visual perception. In this study, we assessed how birds perceive colors of four Cepaea nemoralis morphs using physiological models of avian color vision. We calculated combined chromatic and achromatic contrast between shells and three habitat background types as a measure of shell conspicuousness. The degree of background color matching in Cepaea nemoralis depended on both shell morph and habitat type. On average, banded morphs were more conspicuous than unbanded morphs. Morphs were the most cryptic against dry vegetation and the most conspicuous on bare ground. We also found a significant interaction between habitat type and color morph. The relative conspicuousness of shell morphs depended on habitat and was the most variable against green vegetation. Our study provides the first insight into how potential avian predators view Cepaea nemoralis morphs. The results are discussed in light of multiple hypotheses explaining selective predation on Cepaea nemoralis morphs.     

Diverse migration strategies in hoopoes (<Emphasis Type="Italic">Upupa epops</Emphasis>) lead to weak spatial but strong temporal connectivity

The annual cycle of migrating birds is shaped by their seasonal movements between breeding and non-breeding sites. Studying how migratory populations are linked throughout the annual cycle—migratory connectivity, is crucial to understanding the population dynamics of migrating bird species. This requires the consideration not only of spatial scales as has been the main focus to date but also of temporal scales: only when both aspects are taken into account, the degree of migratory connectivity can be properly defined. We investigated the migration behaviour of hoopoes (Upupa epops) from four breeding populations across Europe and characterised migration routes to and from the breeding grounds, location of non-breeding sites and the timing of key migration events. Migration behaviour was found to vary both within and amongst populations, and even though the spatial migratory connectivity amongst the populations was weak, temporal connectivity was strong with differences in timing amongst populations, but consistent timing within populations. The combination of diverse migration routes within populations and co-occurrence on the non-breeding grounds between populations might promote exchange between breeding populations. As a result, it might make hoopoes and other migrating bird species with similar strategies more resilient to future habitat or climatic changes and stabilise population trends.     

Soil and preen waxes influence the expression of carotenoid-based plumage coloration

The signaling function of carotenoid-based plumage is mainly determined by the concentration of pigments in feathers. For this reason, most studies of the proximate control of coloration focus on processes during and preceding moult. In great tits Parus major, past research demonstrates that carotenoid-based plumage coloration honestly indicates male quality and, thus, may be a sexually selected signal. In this study, we investigate how dirt and preen oil influence the coloration of carotenoid-based feathers in the great tit. We collected six feathers from each individual bird; three feathers served as controls while the remaining three feathers were washed with a chloroform/methanol mixture to remove soil and preen waxes. We assessed plumage coloration using digital photography. This cleaning procedure slightly enhanced ornamentation; the experimentally cleaned feathers expressed hues shifted towards shorter wavelengths and expressed brighter overall coloration than control feathers. This is the first experimental study conducted on wild birds demonstrating that, in addition to pigment concentration, the presence of preen waxes and soils on feathers may contribute to variation in coloration.     

Do females pay attention to secondary sexual coloration in vervet monkeys (Chlorocebus aethiops)?

Several primate species show sexual dichromatism with males displaying conspicuous coloration of the pelage or skin. Studies of scrotal coloration in male vervet monkeys (Chlorocebus aethiops) suggest that it is an important intrasexual signal, with relatively dark, colourful males dominating paler males. To date, no studies have examined the influence of male colour on intersexual social interactions in vervet monkeys. The primary goal of the present study was to evaluate whether female vervet monkeys attend to male coloration. We experimentally introduced females, housed with either “pale” or “dark” males, to stimulus males whose scrota were pale, dark, or pale but painted to look dark. Overall, during introductions, females did not differ in time spent directing affiliative behaviour toward pale, dark, and painted males; however, females, permanently housed with dark males, spent significantly more time directing affiliative behaviour toward pale than painted males. When the stimulus male was pale, affiliative exchanges between males and females were longer than when the stimulus male was painted. Home male colour was not related to female-initiated aggression. Home male colour was also not related to male-initiated aggression, although painted stimulus males were more likely to initiate aggression than pale stimulus males. These findings lead us to conclude that females pay attention to male coloration, but do not bias their interactions toward males solely on the basis of natural male coloration.     

Effects of access to preen gland secretions on mallard plumage

Preen glands exist in almost every bird species and several non-exclusive functions have been proposed for this gland and the oils that it produces. One function generally admitted is that the oily secretions of the preen gland would provide a waterproofing layer when spread over feathers. Alternatively, several authors have proposed that plumage waterproofness is mostly due to the spatial micro-structure of feathers. The purpose of this study was to examine, by manipulating the access to the preen gland, the effect of the preen oil on the plumage waterproofness and condition. To explore this question, we carried out two independent experiments where we temporarily blocked access to the preen gland secretions with a removable mechanism in one group of captive mallards (Anas platyrhynchos), whilst a second group of birds had access to gland secretions. In a long-term experiment (3 months of treatment) and a short-term experiment (10 days), we measured plumage water retention and condition. After 3 months without access to preen glands, we found a significant decrease of plumage condition and an associated increase in plumage water retention. Moreover, we found a significant correlation between plumage condition and water retention ability. In contrast, after 10 days of treatment, no significant effect was found on plumage condition and water retention. Our study shows that preen oil acts to maintain plumage condition and suggests that feather microstructure is essential to maintain plumage waterproofness.     

Alarm communication: a new function for the scent-gland secretion in harvestmen (Arachnida: Opiliones)

Most harvestmen are nocturnal, nonacoustical, and nonvisual arthropods. They have a pair of exocrine glands on the cephalothorax that produce defensive volatile secretions. We investigated in the field the possible alarm effect of these secretions in the gregarious harvestman Goniosoma aff. proximum. A cotton swab soaked with the species' own exudate (treatment), or with water (control), was held 1-2 cm from the center of harvestmen aggregations. The results showed that the gland secretion elicits an alarm response in Goniosoma: whereas 73.3% of the aggregations dispersed after being stimulated with the gland exudate, only 3.3% responded to the water control. Respondent groups are larger than nonrespondent groups, and the time of reaction to the secretion was inversely related to group size. This is the first demonstration of a chemically-mediated alarm effect in harvestmen. The alarm response in gregarious harvestmen has possibly evolved as a by-product of a primarily defensive reaction in the context of predator avoidance. The discovery of this novel function of scent-gland secretion is meaningful in view of the widespread occurrence of gregarious habit among species of the order Opiliones.     

Multiple UV reflectance peaks in the iridescent neck feathers of pigeons

Recent studies of colorful plumage signals in birds have been aided by the finding that birds can see ultraviolet (UV) light and thus may communicate using colors invisible to humans. Some of the pioneering and more pivotal work on avian color vision was performed with domestic pigeons (Columba livia), yet surprisingly there have been few detailed reports of the UV-reflecting properties of pigeon feathers. Here, I use UV-VIS fiber-optic spectrometry to document the full-spectrum reflectance characteristics of iridescent purple and green neck plumage in pigeons. Neck feathers that appear purple to the human eye exhibit four reflectance peaks—two in the UV and one in the blue and red regions—and thus exhibit a UV-purple hue. Neck feathers that appear green to the human eye are characterized by five spectral peaks: two in the UV (UVA and UVB), a predominant green peak, and secondary violet and red peaks, conferring a UV-purple-green color. Such elaborate UV coloration suggests that birds may use an even more complex and hidden UV signaling system than previously thought.     

Melanin-based coloration covaries with ovary size in an age-specific manner in the barn owl

While the adaptive function of black eumelanin-based coloration is relatively well known, the function of reddish-brown pheomelanin-based coloration is still unclear. Only a few studies have shown or suggested that the degree of reddish-brownness is associated with predator–prey relationships, reproductive parameters, growth rate and immunity. To gain insight into the physiological correlates of melanin-based coloration, I collected barn owl (Tyto alba) cadavers and examined the covariation between this colour trait and ovary size, an organ that increases in size before reproduction. A relationship is expected because melanin-based coloration often covaries with sexual activity. The results showed that reddish-brown juveniles had larger ovaries than whiter juveniles particularly in individuals in poor condition and outside the breeding season, while in birds older than 2 years lightly coloured females had larger ovaries than reddish-brown conspecifics. As barn owls become less reddish-brown between the first and second year of age, the present study suggests that reddish-brown pheomelanic and whitish colorations are associated with juvenile- and adult-specific adaptations, respectively.     

Now you see me,now you don’t: iridescence increases the efficacy of lizard chromatic signals

The selective forces imposed by primary receivers and unintended eavesdroppers of animal signals often act in opposite directions, constraining the development of conspicuous coloration. Because iridescent colours change their chromatic properties with viewer angle, iridescence offers a potential mechanism to relax this trade-off when the relevant observers involved in the evolution of signal design adopt different viewer geometries. We used reflectance spectrophotometry and visual modelling to test if the striking blue head coloration of males of the lizard Lacerta schreibeiri (1) is iridescent and (2) is more conspicuous when viewed from the perspective of conspecifics than from that of the main predators of adult L. schreibeiri (raptors). We demonstrate that the blue heads of L. schreiberi show angle-dependent changes in their chromatic properties. This variation allows the blue heads to be relatively conspicuous to conspecific viewers located in the same horizontal plane as the sender, while simultaneously being relatively cryptic to birds that see it from above. This study is the first to suggest the use of angle-dependent chromatic signals in lizards, and provides the first evidence of the adaptive function of iridescent coloration based on its detectability to different observers.