Sandpipers (Scolopacidae) switch from monoester to diester preen waxes during courtship and incubation,but why?

Recently, a shift in preen wax composition, from lower molecular weight monoesters to higher molecular weight diesters, was described for individuals of a sandpiper species (red knot, Calidris canutus) that were about to leave for the tundra breeding grounds. The timing of the shift indicated that diester waxes served as a quality signal during mate choice. Here, this hypothesis is evaluated on the basis of a survey of preen wax composition in 19 sandpiper species. All of these species showed the same shift observed in the high-Arctic breeding red knots. As the shift also occurred in temperate breeding species, it is not specific to tundra-breeding sandpipers. Both sexes produced the diester waxes during the incubation period until hatching, in addition to the short period of courtship, indicating that diesters' functions extend beyond that of a sexually selected 'make-up'. The few non-incubating birds examined (males of curlew sandpipers (C. ferruginea) and ruffs (Philomachus pugnax)) had the lowest likelihood of secreting diesters, indicating a functional role for diester preen waxes during incubation. We propose that diester preen waxes enhance olfactory crypticism at the nest.     

An avian equivalent of make-up?

We report that a long-distance migrating shorebird, the red knot, makes a complete switch from commonly occurring monoester preen waxes to a much rarer class of higher-molecular-weight diester waxes at the time of take-off to the high arctic breeding grounds. The cold arctic climate would have required a lowering of wax-viscosity, and thus, a shift in the reverse direction. We propose that a sexually selected need for a brilliant plumage has lead to this conter-intuitive temporary shift from monoesters to diester waxes. The difficulty of application of the diester preen waxes under cold conditions would ensure the reliability of the quality-signalling function of this most probably sexually selected trait.     

Expression of annual cycles in preen wax composition in red knots: constraints on the changing phenotype

Birds living in seasonal environments change physiology and behavior in correspondence to temporally changing environmental supplies, demands and opportunities. We recently reported that the chemical composition of uropygial gland secretions of sandpipers (Scolopacidae, order Charadriformes) changes during the breeding season from mixtures of monoesters to diesters, which fulfill specific functions related to incubation. A proper temporal match between the expression of diester preen waxes and incubation requires a flexible organization of the trait. Here we analyze the possible degrees of flexibility with reference to the functionality of better-understood molt and body mass cycles of free-living and captive red knots (Calidris canutus). The relative flexibility of seasonal cycles in preen wax composition was examined by two experimental perturbations: (1) giving birds restricted access to food and (2) monitoring them long-term under a constant photoperiodic regime. We found that wax type cannot change instantaneously, but that changing the type of wax is under similar organizational time constraints as the replacement of feathers. Just as molt and mass cycles, the seasonal rhythm of diester secretion appeared to be under endogenous control: most birds placed in a constant photoperiod still maintained seasonally changing preen waxes. Diester preen wax secretion was synchronized with the peak in body mass in spring, but became less well expressed under constant photoperiodic conditions and when food availability was limited.     

Preen waxes do not protect carotenoid plumage from bleaching by sunlight

The plumage coloration of wild birds often changes during the breeding season. One of the possible reasons for this is that sunlight, and particularly ultraviolet (UV) wavelengths, degrades the pigments responsible for plumage coloration. It has been suggested that birds may apply preen wax to feathers to protect feathers from bleaching. This hypothesis is tested by exposing carotenoid-based breast feathers of Great Tits to ambient light, light filtered to exclude UV and darkness. Preen waxes were experimentally removed from feather samples and the effect of light on coloration of treatment and control feathers compared. Ambient light had an effect on feather colour but preen wax did not. Feathers exposed to sun gradually became less saturated and hues shifted towards shorter wavelengths. This was not apparent in control feathers kept in darkness. Feathers exposed to full-spectra sunlight faded more than those that were kept in light with UV wavelengths removed. There was a decrease in brightness of feathers in both experimental and control groups, which was assumed to be an effect of dirt accumulation. This experiment confirmed earlier suspicions regarding the detrimental effects of UV irradiation on carotenoid-based coloration of avian feathers but failed to show any protective function of preen waxes. The possible consequences of these mechanisms of colour change for birds with regard to mating strategies are discussed.     

Parental role division predicts avian preen wax cycles

Previous studies have shown that preen wax composition in some sandpipers shifts from the usual monoesters to diesters during the breeding season, possibly to reduce the ability of mammalian predators to find nests using olfactory cues. To investigate further the relationship between incubation and wax secretion, we examined seven sandpiper species with different incubation patterns (species in which both sexes incubate, in which only males incubate and in which only females incubate). During the breeding period, diester preen wax was secreted almost exclusively by the incubating sex in species with uniparental incubation, and by both sexes in species with biparental incubation. These findings suggest that diester preen waxes have a function that is directly related to incubation. Unexpectedly, in female-incubating Curlew Sandpiper Calidris ferruginea and Buff-breasted Sandpiper Tryngites subruficollis , some males also secreted diester preen waxes during the breeding period. This suggests that some males may in fact incubate, that these waxes may be a remnant from their evolutionary past when both sexes incubated, or that males need to be olfactorally cryptic because they are involved in the making of nest scrapes. The seasonal pattern of preen wax composition was also studied in captive male, female and female-mimicking male ('faeder') Ruff Philomachus pugnax . Captive female Ruff changed preen wax composition from monoesters to diesters in the spring despite the fact that no incubation took place. This suggests that circannual rhythms rather than actual incubation behaviour may trigger the shift to diester waxes. All captive male Ruff, including the faeders, continued to secrete monoesters, supporting the hypothesis that only the incubating sex secretes diesters.     

Preen oil and bird fitness: a critical review of the evidence

The uropygial gland is a holocrine complex exclusive to birds that produces an oleaginous secretion (preen oil) whose function is still debated. Herein, I examine critically the evidence for the many hypotheses of potential functions of this gland. The main conclusion is that our understanding of this gland is still in its infancy. Even for functions that are considered valid by most researchers, real evidence is scarce. Although it seems clear that preen oil contributes to plumage maintenance, we do not know whether this is due to a role in reducing mechanical abrasion or in reducing feather degradation by keratinophilic organisms. Evidence for a function against pathogenic bacteria is mixed, as preen oil has been demonstrated to act against bacteria in vitro, but not in vivo. Nor is it clear whether preen oil can combat pathogenic bacteria on eggshells to improve hatching success. Studies on the effect of preen oil against dermatophytes are very scarce and there is no evidence of a function against chewing lice. It seems clear, however, that preen oil improves waterproofing, but it is unclear whether this acts by creating a hydrophobic layer or simply by improving plumage structure. Several hypotheses proposed for the function of preen oil have been poorly studied, such as reduction of drag in flight. Similarly, we do not know whether preen oil functions as repellent against predators or parasites, makes birds unpalatable, or functions to camouflage birds with ambient odours. On the other hand, a growing body of work shows the important implications of volatiles in preen oil with regard to social communication in birds. Moreover, preen oil clearly alters plumage colouration. Finally, studies examining the impact of preen oil on fitness are lacking, and the costs or limitations of preen‐oil production also remain poorly known. The uropygial gland appears to have several non‐mutually exclusive functions in birds, and thus is likely to be subject to several selective pressures. Therefore, future studies should consider how the inevitable trade‐offs among different functions drive the evolution of uropygial gland secretions.     

Effectiveness of a commonly-used technique for experimentally reducing plumage UV reflectance

Ultraviolet (UV) plumage is thought to be sexually selected through intra-sexual competition, female choice and differential allocation. Experimental manipulations of plumage UV reflectance are essential to demonstrate that mate choice or intra-sexual competition are causally related to UV coloration. The most widely-used technique for manipulating UV reflectance in wild birds is the application of a mixture of UV-absorbing chemicals and preen gland fat. However, although this UV reduction technique is commonly used, little is known about the persistence of the treatment and the temporal variation in UV reflectance that it causes. We manipulated the UV crown plumage of wild and captive blue tits Parus caeruleus , and took repeated photospectrometric measurements of both UV-reduced and control-treated individuals. Our results show that the UV reduction lasts for at least five days and that the treatment has no negative effects on the survival of wild birds.     

Novel chromatic and structural biomarkers of diet in carotenoid-bearing plumage

Previous attempts to establish a link between carotenoid-based plumage reflectance and diet have focused on spectral features within the human visible range (400-700 nm), particularly on the longer wavelengths (550-700 nm) that make these plumages appear yellow, orange or red. However, carotenoid reflectance spectra are intrinsically bimodal, with a less prominent but highly variable secondary reflectance peak at near-ultraviolet (UV; 320-400 nm) wavelengths visible to most birds but not to normal humans. Analysis of physical reflectance spectra of carotenoid-bearing plumages among trophically diverse tanagers (Thraupini, Emberizinae, Passeriformes) indicated that both the absolute and relative (to long visible wavelengths) amounts of short waveband (including UV) reflectance were lower in more frugivorous species. Striking modifications to the branched structure of feathers increased with frugivory. These associations were independent of phylogenetic relatedness, or other physical (specimen age, number of carotenoid-bearing patches) or ecological (body size, elevation) variables. By comparison, reflectance at longer visible wavelengths ('redness') was not consistently associated with diet. The reflectance patterns that distinguished frugivores should be more apparent to UV-sensitive birds than to UV-blind humans, but humans can perceive the higher plumage gloss produced by modified gross feather structure. Basic aspects of carotenoid chemistry suggest that increases in pigment concentration and feather dimensions reduce short waveband reflectance by the plumages of frugivores.     

Variation in ultraviolet reflectance by carotenoid-bearing feathers of tanagers (Thraupini: Emberizinae: Passeriformes)

Avian visual sensitivity encompasses both the human visible range (400–700 nm) and also near‐ultraviolet (UV) wavelengths (320–400 nm) invisible to normal humans. I used reflectance spectrophotometry to assess variation in UV reflectance for yellow, orange and red plumage in 67 species of tanager (Passeriformes). Previous chemical studies, and my analysis of reflectance minima, suggest that carotenoids are the dominant pigments in yellow, orange and red tanager plumage. Spectra recorded over the range of wavelengths to which birds are sensitive (320–700 nm) were invariably bimodal, with both a plateau of high reflectance at longer (> 500 nm) wavelengths and a distinct secondary peak at UV (< 400 nm) wavelengths. Within this overall framework, variation in UV reflectance was expressed within well‐defined quantitative limits: (1) peak reflectance was always lower than the corresponding plateau of reflectance at longer visible wavelengths; (2) the intensity of peak reflectance declined steadily below 350 nm; (3) wavelengths of peak reflectance clustered between 350 and 370 nm. Significant correlations were detected between various measures of total reflectance in the UV and visible wavebands, but not between various measures of spectral location of UV and visible reflectance. I propose that the strong absorption band at short visible wavelengths (～ 380–550 nm) responsible for bimodal spectra of carotenoids in vitro is also responsible for bimodal reflectance by carotenoid‐based plumage colours. The construction of the UV and visible reflectance bands from different sides of this same absorbance band provides a mechanism for the observed covariation between UV and visible wavelengths. Lack of an association between the spectral locations of the UV and visible reflectance bands may result from the limited variation in spectral location of the UV band. These patterns suggest that plumage colours are subject to constraints, just as are more traditional morphological characters. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84 , 243–257.     

Plumage maintenance affects ultraviolet colour and female preference in the budgerigar

Elaborate or colourful feathers are important traits in female-mate choice in birds but little attention has been given to the potential costs of maintaining these traits in good condition via preening behaviour. While preening is known to be an important component of plumage maintenance, it has received little attention with respect to colouration. We investigated whether preening can influence plumage reflectance and whether females show a preference for plumage cleanliness in captive-bred, wild-type budgerigars, Melopsittacus undulatus. To do this, we compared the spectral colour of birds that were allowed to preen their plumage and individuals that were prevented from preening. The plumage of birds that were prevented from preening showed a significant lower reflectance in the UV range (300-400 nm). Subsequently, we measured females’ preferences for preened and unpreened males using a two-choice test. In a second experiment we allowed females to choose between an unpreened male and a male smeared with UV-absorbing chemicals (UV-blocked male). The proportion of time that females stayed near preened males was statistically higher than for unpreened males, but females spent similar amounts of time with unpreened males and UV-blocked males. These results are consistent with the idea that female budgerigars are able to discriminate between preened and unpreened males, and that UV colours, mediated by preening, can convey information about a bird's current condition.     

Astaxanthin is responsible for the pink plumage flush in Franklin's and Ring-billed gulls

ABSTRACT.   Carotenoid pigments produce the red, orange, and yellow plumage of many birds. Carotenoid-containing feathers are typically rich in color and displayed by all adult members of the species. In many gulls and terns, however, an unusual light pink coloring (or flush) to the normally white plumage can be found in highly variable proportions within and across populations. The carotenoid basis of plumage flush was determined in an Elegant Tern ( Sterna elegans ; Hudon and Brush 1990 ), but it is not clear if all larids use this same mechanism for pink plumage coloration. We examined the carotenoid content of pink feathers in Franklin's ( Larus pipixcan ) and Ring-billed ( Larus delawarensis ) gulls and found that a single carotenoid—astaxanthin—was present. Astaxanthin was primarily responsible for the flush in Elegant Terns as well, but was accompanied by other carotenoids (e.g., canthaxanthin and zeaxanthin), as is typical of most astaxanthin-containing bird feathers. In both gull and tern species, carotenoids were contained within feathers and did not occur on the plumage surface in preen oil, as some have previously speculated. We hypothesize that some gulls turn pink because they acquire unusually high amounts of astaxanthin in their diets at the time of feather growth. It is tempting to link the increase in sightings of pink Ring-billed Gulls since the late 1990s with the introduction of pure, synthetic astaxanthin to the diets of hatchery-raised salmon.     

Experimental study of the effect of preen oil against feather bacteria in passerine birds

Avian plumage harbors various pathogens such as feather-degrading bacteria, which have the potential to reduce host fitness. A growing body of evidence suggests that the secretion of the uropygial gland of birds—preen oil—acts as one of the first lines of defence against harmful bacteria. However, previous studies on the antimicrobial impact of preen oil have yielded controversial results. The impact of preen oil on bacterial densities of feathers was experimentally investigated in two passerine species: great tits Parus major and pied flycatchers Ficedula hypoleuca. More specifically, we tested whether the antibacterial effect of the preen oil secreted by the same individual differs from that of the preen oil originating from the gland of other species. In the laboratory, ventral feathers were treated with preen oil from (1) an individual’s own gland, (2) from the gland of another passerine species, or (3) from the gland of a phylogenetically distant bird species. We detected a significant antibacterial effect of preen oil on bacteria that were attached to feathers, though the effect did not depend on whether the oil originated from the individual’s own gland or from the gland of another bird species. However, treatment with preen oil suppressed the density of bacteria more in the pied flycatcher than in the great tit. This is the first study providing experimental evidence that preen oil represents an important antimicrobial mechanism against those plumage bacteria that are attached to feathers.     

Ultraviolet reflectance of plumage for parent-offspring communication in the great tit (Parus major)

Ultraviolet (UV) reflectance has been implicated in mate selection.Yet, in some bird species the plumage of young varies in UVreflectance already in the nest and long before mate choiceand sexual selection come into play. Most birds molt the juvenilebody plumage before reaching sexual maturity, and thus, someconspicuous traits of the juvenile body plumage may rather haveevolved by natural selection, possibly via predation or parentalpreference. This second hypothesis is largely untested and predictsa differential allocation of food between fledging and totalindependence, which is a time period of 2–3 weeks whereoffspring mortality is also highest. Here, we test the predictionthat parents use the individual variation in UV reflectanceamong fledglings for differential food allocation. We manipulatedUV reflectance of the plumage of fledgling great tits Parusmajor by treating chest and cheek feathers with a lotion thateither did or did not contain UV blockers and then recordedfood allocation by parents in an outdoor design simulating postfledgingconditions. The visible spectrum was minimally affected by thistreatment. Females were found to feed UV-reflecting offspringpreferentially, whereas males had no preference. It is the firstevidence showing that the UV reflectance of the feathers ofyoung birds has a signaling function in parent–offspringcommunication and suggests that the UV traits evolved via parentalpreference.     

The ubiquity of avian ultraviolet plumage reflectance

Although several bird species have been shown to reflect ultraviolet (UV) light from their plumages, the incidence of UV reflectance, and therefore the potential for UV or UV-enhanced signals, across the avian tree of life is not known. In this study, we collected reflectance data from the plumages of 312 bird species representing 142 families. Our results demonstrate that all avian families possess plumages that reflect significant amounts of UV light. The ubiquity of UV reflectance indicates that all studies of avian behaviour, ecology and evolution involving plumage coloration would benefit from consideration of plumage reflectance in the UV portion of the electromagnetic spectrum. Additionally, we demonstrate the existence of cryptic UV plumage patches and cryptic dimorphism among birds.     

Sex differences in the chemical composition of uropygial gland waxes in domestic ducks

Sexual differences in the chemical composition of the uropygial gland waxes in domestic ducks have been detected before the nesting period. 3-Hydroxy fatty acids containing diester waxes and significant differences in the composition of the fatty acid and alcohol moieties of the monoester waxes occur during February–June only in the female preen wax. Males as well as ducklings, however, show constant wax patterns. Moreover, no significant influence on wax composition of testosterone or estradiol, respectively in male or female ducklings could be verified.     

Physical Alignments Between Plumage Carotenoid Spectra and Cone Sensitivities in Ultraviolet-Sensitive (UVS) Birds (Passerida: Passeriformes)

Among birds, single cone sensitivities responsible for color vision appear surprisingly conserved even though chromatic signals vary greatly. Thus it is widely held that avian visual signal and receptor characteristics are rarely aligned. Analysis of a diverse passerine clade (Passerida) with characteristically ultraviolet-sensitive (UVS) vision revealed that plumage carotenoid reflectance spectra matched cone maximal sensitivities at several levels: (1) plumage carotenoid reflectance minima and maxima in aggregate aligned with the four UVS single cones; (2) the corresponding reflectance features of yellow (hydroxy- and ε-keto) and red (3- and 4-β-keto) carotenoid classes aligned with different combinations of cones; (3) pairs of reflectance features (e.g. one minimum and one maximum) of each carotenoid class aligned with pairs of (opponent) cones that evoke chromatic perception; (4) passerid plumage carotenoids aligned more closely to their own (UVS) visual system than to the distinctive homologous cone classes of the violet-sensitive system found in other birds. The ubiquitous occurrence of plumage carotenoids ipso facto demonstrates that alignments of avian visual signals and receptors are widespread, and provides novel evidence that carotenoids are important to avian communication. Moreover, alignment of different physical spectra to different cone combinations in a fixed receptor array provides a straightforward mechanism that accommodates signal diversity within the context of a relatively conserved visual system. The distinct patterns of variation and alignment observed for yellow versus red carotenoids further suggest that these pigment classes convey different physical aspects of content, which may foster carotenoid-based plumage diversity through signal design trade-offs.     

Color expression in experimentally regrown feathers of an overwintering migratory bird: implications for signaling and seasonal interactions

Plumage coloration in birds plays a critical role in communication and can be under selection throughout the annual cycle as a sexual and social signal. However, for migratory birds, little is known about the acquisition and maintenance of colorful plumage during the nonbreeding period. Winter habitat could influence the quality of colorful plumage, ultimately carrying over to influence sexual selection and social interactions during the breeding period. In addition to the annual growth of colorful feathers, feather loss from agonistic interactions or predator avoidance could require birds to replace colorful feathers in winter or experience plumage degradation. We hypothesized that conditions on the wintering grounds of migratory birds influence the quality of colorful plumage. We predicted that the quality of American redstart (Setophaga ruticilla) tail feathers regrown after experimental removal in Jamaica, West Indies, would be positively associated with habitat quality, body condition, and testosterone. Both yearling (SY) and adult (ASY) males regrew feathers with lower red chroma, suggesting reduced carotenoid content. While we did not observe a change in hue in ASY males, SY males shifted from yellow to orange plumage resembling experimentally regrown ASY feathers. We did not observe any effects of habitat, testosterone, or mass change. Our results demonstrate that redstarts are limited in their ability to adequately replace colorful plumage, regardless of habitat, in winter. Thus, feather loss on the nonbreeding grounds can affect social signals, potentially negatively carrying over to the breeding period.     

Does sunlight enhance the effectiveness of avian preening for ectoparasite control?

Preening is a bird's first line of defense against harmful ectoparasites. Ectoparasites, in turn, have evolved adaptations for avoiding preening such as hardened exoskeletons and escape behavior. Earlier work suggests that some groups of ectoparasites, such as feather lice, leave hiding places in feathers that are exposed to direct sunlight, making them more vulnerable to preening. It is, therefore, conceivable that birds may choose to preen in direct sunlight, assuming it improves the effectiveness of preening. Using mourning doves and their feather lice, we tested 2 related hypotheses; (1) that birds with access to direct sunlight preen more often than birds in shade, and (2) that birds with access to direct sunlight are more effective at controlling their ectoparasites than birds in shade. To test these hypotheses, we conducted an experiment in which we manipulated both sunlight and preening ability. Our results provided no support for either hypothesis, i.e., birds given the opportunity to preen in direct sunlight did not preen significantly more often, or more effectively, than did birds in shade. Thus, the efficiency of preening for ectoparasite control appears to be independent of light intensity, at least in the case of mourning doves and their feather lice.     

Sexually selected male plumage color is testosterone dependent in a tropical passerine bird, the red-backed fairy-wren (Malurus melanocephalus)

Background

Sexual signals, such as bright plumage coloration in passerine birds, reflect individual quality, and testosterone (T) may play a critical role in maintaining signal honesty. Manipulations of T during molt have yielded mixed effects on passerine plumage color, in most cases delaying molt or leading to production of drab plumage. However, the majority of these studies have been conducted on species that undergo a post-nuptial molt when T is low; the role of T in species that acquire breeding plumage during a pre-nuptial molt remains largely unexplored.

Methodology/Principal Findings

We experimentally tested the effects of increased T on plumage color in second-year male red-backed fairy-wrens (Malurus melanocephalus), a species in which after-second-year males undergo a pre-nuptial molt into red/black (carotenoid and melanin-based) plumage and second-year males either assume red/black or brown breeding plumage. T treatment stimulated a rapid and early onset pre-nuptial molt and resulted in red/black plumage acquisition, bill darkening, and growth of the sperm storage organ, but had no effect on body condition or corticosterone concentrations. Control males molted later and assumed brown plumage. T treated males produced feathers with similar but not identical reflectance parameters to those of unmanipulated after-second-year red/black males; while reflectance spectra of red back and black crown feathers were similar, black breast feathers differed in UV chroma, hue and brightness, indicating a potentially age and plumage patch-dependent response to T for melanin- vs. carotenoid-pigmentation.

Conclusions/Significance

We show that testosterone is the primary mechanism functioning during the pre-nuptial molt to regulate intrasexually variable plumage color and breeding phenotype in male red-backed fairy-wrens. Our results suggest that the effects of T on plumage coloration may vary with timing of molt (pre- vs. post-nuptial), and that the role of T in mediating plumage signal production may differ across age classes, plumage patches, and between pigment-types.