Cosmetic enhancement of signal coloration ...

Behavioral Ecology Advance Access published May 10, 2010 Behavioral Ecology doi:10.1093/beheco/arq053

Cosmetic enhancement of signal coloration: experimental evidence in the house finch

Plumage coloration plays an important role in visual communication by signaling aspects of individual quality. It has been proposed that the need for preserving plumage condition and hence signaling content may have promoted a novel signaling mechanism: cosmetic coloration. Here, we investigated whether preen waxes may act as cosmetics by affecting feathers’ ornamental coloration in male house finches (Carpodacus mexicanus). We (1) blocked the access to uropygial gland of a group of males and compared their coloration with a control group and (2) applied preen wax extracted from live individuals to museum skins and measured color before and after wax application. We found that red feathers of control males were more colorful than those of experimental males and that applying waxes to museum skins’ red feathers increased their color saturation. Our results provide evidence that preen waxes act as cosmetics by enhancing plumage ornamentation, thus revealing the existence of novel mechanisms operating in signaling coloration. Although preen waxes per se would not constitute a signal, selection for signal efficacy might favor individuals that are able to increase signal intensity beyond the optimum necessary for plumage maintenance. Our results support the hypothesis that preen waxes reinforce the honesty of signals, which may be particularly useful in a social context where interactions between individuals are mediated by the intensity of the signals. Key words: cosmetic coloration, plumage coloration, plumage maintenance, preen waxes, uropygial gland. [Behav Ecol]

nimals often use conspicuous signals to advertise their quality and to attract mates (Darwin 1871). Plumage coloration is a widely investigated example of a secondary sexual trait in male birds, and it is known to play an important role in visual communication by signaling aspects of individual quality within both social and sexual selection contexts (reviewed Hill 2006; Senar 2006). The reliability of colorful plumage as a quality signal is related to the potential costs associated with the acquisition and maintenance of such ornamentation (Zahavi 1975, 1977). Theory predicts that high-quality males may assume these costs more easily, display more conspicuous plumage, and thus gain more resources (e.g., mates, food, and territories) than males of lower quality. Because condition-dependent expression of color has been demonstrated for most types of pigmentary and structural colors (e.g., Hill and Montgomerie 1994; McGraw et al. 2002; Jawor and Breitwisch 2003; Johnsen et al. 2003) and male social status has been shown to vary in relation to plumage coloration (reviewed Senar 2006), females are expected to choose to mate with the most colorful males in order to experience fitness benefits (Griffith and Pryke 2006). Feathers acquire their coloration during molt via either pigments (e.g., carotenoids and melanins) deposited into the keratin matrix or by the structural arrangement of feather tissues (Fox and Vevers 1960). Because birds grow feathers during periodic molts and retain them for extended periods of time, plumage color is traditionally regarded as a static signal that does not change over time. There is, however, increasing evidence that coloration does vary between molts ¨ rnborg et al. 2002; McGraw and Hill 2004; Figuerola and (O Senar 2005; Delhey et al. 2006) and that feathers become

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Address correspondence to I. Lo´pez-Rull. E-mail: isalorull@gmail .com. Received 11 November 2009; revised 12 March 2010; accepted 19 March 2010. The Author 2010. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: [email protected]

damaged through abrasion, dirt accumulation, exposure to UV light, and by ectoparasites’ and microbial activity (reviewed by Delhey et al. 2007). Because feather wear affects not only the primary functions of plumage but also secondary functions such as color signaling, feather maintenance mechanisms should reinforce the honesty of ornamental plumage as an indicator signal and may become the target of additional selective forces (Delhey et al. 2007). Therefore, whereas the mere presence of a colorful plumage indicates that its bearer was healthy and vigorous at the time the ornament was produced, the presence of a well-maintained plumage shows that its bearer is capable of the day-to-day investment required to maintain the ornament in good condition (Walther and Clayton 2004). Indeed, there is evidence that individuals with intact or not too worn-out plumage are in better condition, are dominant, have higher reproductive success, and are preferred by females over their counterparts (Fitzpatrick and Price 1997; Ferns and Lang 2003; Ferns and Hinsley 2004; Zampiga et al. 2004). One of the important functions of uropygial gland secretions (also called preen waxes) is feather maintenance. When preen glands have been removed, the feathers have become brittle and rough (Moyer et al. 2003). Although the exact biological function of preen wax is still highly debated, there is little doubt that it plays a key role in the preservation of feather structure by keeping the keratin flexible (Jacob and Ziswiler 1982). In addition, preen waxes have been shown to repel water (Jacob and Ziswiler 1982) and provide protection against pathogens such as feather degrading bacteria and ectoparasites (Jacob et al. 1997; Moyer et al. 2003; Shawkey et al. 2003; Haribal et al. 2005; Reneerkens et al. 2008). Preen waxes have also been proposed to act as cosmetics (Piersma et al. 1999; Piault et al. 2008). Cosmetics in birds are substances that convey a different color or texture to mature feathers and that are actively applied by the bird or secreted onto the feathers. Recently, it has been suggested that cosmetics might not only be useful in plumage maintenance but also in mate

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Isabel Lo´pez-Rull, Iluminada Pagań, and Constantino Macıás Garcia Departamento de Ecologıá Evolutiva, Instituto de Ecologıá, Universidad Nacional Autońoma de Me´xico, Apartado Postal 70-275, Me´xico DF 4510, Me´xico

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color of sexually dimorphic plumage. Male house finches that deposit more carotenoids into feathers to acquire redder plumage are in better condition, are more likely to acquire mates, begin breeding earlier, and fledge more offspring in a year (reviewed in Hill 2002). In the present study, we experimentally blocked the access to uropygial secretions of a group of male house finches and compared their plumage coloration with a control (nonblocked) group in order to analyze the extent to which plumage coloration changes within the treatment. In a second experiment, we manually applied preen wax extracted from the uropygial gland of live individuals to museum specimen skins of house finches and measured plumage color before and after treatment. In this second experiment, we also tested whether the effect of preen wax on feather color differ between sexes. For preen waxes to function as a cosmetic, feather coloration should be more colorful in control than in blocked males (experiment 1) and after manually applying preen wax to museum skins (experiment 2). In addition, if preen waxes increase signal intensity, we expect a greater effect of male secretions than of females secretions (experiment 2). MATERIAL AND METHODS We used adult house finches (C. mexicanus) collected at the State of San Luis Potosı´, Me´xico in February. Birds were kept at the Instituto de Ecologıá, Universidad Nacional Autońoma de Me´xico (UNAM) (Me´xico City) during February–April 2009. All individuals were marked with metallic rings and housed individually in steel cages (33 3 27 3 31 cm high) kept in an outdoor aviary at ambient temperature and under natural photoperiod. Birds were provided with seeds and water ad libitum, and experiments were performed after one month of acclimatization. On completion of the experiments, the birds were placed in large cages to regain flying condition before being freed by their capture place. Color measurements Color was measured using a MINOLTA handheld spectrophotometer (MINOLTA CR-200, Minolta Co. Ltd, Osaka, Japan) that measures the reflectance from 360 to 700 nm in intervals of 10 nm. Although it does not measure across the whole of the bird visible UV wavelengths (some birds are sensitive down to 320 nm), this limitation may not be a problem because the house finch has little plumage reflectance below 400 nm (Hill 2002). Reference calibrations against zero and a white standard tablet associated with the apparatus were performed according to the instructions provided by the maker. Reflectance spectra for each individual are automatically produced as means of 3 sequential measurements of each individual by changing its position with respect to the apparatus. The SPECTRAMAGIC software (Minolta Co. Ltd) was used to analyze spectra. Two values from the reflectance spectra were calculated: 1) brightness or total reflectance was obtained as the summed reflectance at each 10-nm interval from 360 to 700 nm. Brightness is a measure of the total amount of light reflected by the feathers (Endler 1990) thus as brightness increases, plumage tends to get lighter (Montgomerie 2006a). 2) Yellow–red chroma saturation (YRC) was calculated as the proportion of total reflectance that is in the yellow–red region (R560–700/ R360–700) of the spectrum. We used YRC to describe feather reflectance because this region corresponds to the color range that is subject to mate choice in this species (Hill 2002).


attraction by providing an honesty-reinforcing mechanism linking body condition and coloration (Negro et al. 1999; Piersma et al. 1999). In this line, a recent study in tawny owl nestlings found that a strong immune challenge impaired gland wax production, which presumably caused a change in bill coloration (Piault et al. 2008). Preen waxes have been proposed to function as a cosmetic in 2 ways: when these secretions are colored they could differentially absorb or reflect light of a certain wavelength range and thus stain the plumage; when transparent, preen waxes might cause a change in the appearance of feathers by affecting its achromatic brightness (Delhey et al. 2007). Although the use of colored uropygial gland secretion to change plumage color has been demonstrated for some species (reviewed by Montgomerie 2006b and Delhey et al. 2007), the use of transparent preen waxes to enhance plumage color has yet received no empirical support. Piersma et al. (1999) proposed that preen waxes colorless to our eyes may affect UV reflectance, which is often used in birds sexual signaling. However, this possibility was tested in the red knot (Calidris canutus) and no changes in plumage color due to the secretion were detected (Reneerkens and Korsten 2004) probably because the rusty–red breeding plumage of the red knot reflects little in the UV. Therefore, Delhey et al. (2008) aimed to test this hypothesis in other birds with UV-reflective plumage. By evaluating the optical properties of preen waxes from 51 species belonging to 12 avian orders, they found that 2 main types of uropygial secretions exist, one predominantly found in passerines and one in nonpasserines but both reducing relative UV reflectance of a white background (Teflon tape). In their study, Delhey et al. (2008) quantified how each type of secretion (exemplified by blue tit Cyanistes caeruleus and mallard Anas platyrhynchos) affected feather UV reflectance and found that both secretions reduced overall brightness and relative UV reflectance of white mallard feathers but had no effect on the reflectance of UV/blue blue tit crown feathers. These results imply that the magnitude of the effect may depend on the type of secretion and feather. However, the lack of an effect in the blue tit crown feathers may be a consequence of the small sample size used, which would have implied a reduced power to detect small differences in spectral reflectance. The chemical properties of preen waxes are likely to be the target of natural selection, which should mold them according not only to their consequences for different bird species in relation to specific ecological pressures (e.g., waterproofing, fending off parasites, and protection against abrasion) but also in response to their consequences in the specific signaling process of particular species. Thus, when plumage color influences mate choice, sexual selection should favor the evolution of preen waxes that, on top of fulfilling their physiological and other functions, may also increase signal intensity. Carotenoid-based coloration provides many examples of condition-dependent ornaments across taxa (Endler 1980; Hill 1990; Hill and Montgomerie 1994). These appear to serve as signals of male quality used by females in choosing mates (Endler 1983; Kodric-Brown 1985; Hill 1990). In birds, these ornaments have been deemed to indicate the condition of the male during the molt, which normally happens some time before females use color to assess male quality (Hill and Montgomerie 1994; Hill 2000; McGraw et al. 2005). We hypothesized that transparent preen waxes have the cosmetic role of enhancing the carotenoid-based ornamental plumage coloration, thus updating its value as a condition-dependent signal. To our knowledge, no study has experimentally tested this possibility. We addressed this hypothesis by manipulating preen wax deposition on the feathers of male house finches (Carpodacus mexicanus) and then assessing any effect on the

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Cosmetic enhancement of signal coloration in the house finch

Experimental design

Experiment 2 We assessed the effect of uropygial secretions on feather reflectance by comparing reflectance spectra before and after the application of the secretion to 20 house finch museum specimens. By gently squeezing the uropygial gland nipple with a sterilized forceps, we sampled preen waxes of live house finches (20 males and 10 females) and immediately applied them on different spots of the breast of each male skin. The breast of each male skin was divided in 2 zones ensuring the same distribution of plumage color among them (total reflectance: F1,38 ¼ 1.63, P ¼ 0.21; YRC: one-way analysis of variance (ANOVA): zone F1,38 ¼ 1.60, P ¼ 0.21). We randomly designated zones to be smeared with preen wax from one randomly chosen male or from one randomly chosen female. Color was measured before and after the application of uropygial secretion, using the same procedure as described above. Skins originated in the same house finch population and were collected at about the same time as the live finches used as preen wax donors. All birds used in our study were captured by a professional bird collector with license from the Mexican Ministry for the Environment (Secretarıá de Medio Ambiente

y Recursos Naturales) during a collection that yielded also birds for the Bird Collection of the Institute of Biology (UNAM). We used those museum birds for the second experiment reported here. Statistics Normality was tested using Shapiro–Wilk tests. Data were normally distributed (all P values .0.14), and thus parametric tests were used. For experiment 1, differences between treatments in plumage color were analyzed using repeated measurements ANOVAs. For experiment 2, differences in plumage color before and after the application of uropygial secretion were analyzed using repeated measurements ANOVAs including the donor sex as a fixed factor. In both experiments, probabilities from post hoc tests between and within subjects were calculated using Newman–Keuls test; only significant (P , 0.05) contrasts are reported. Statistical analyses were performed with STATISTICA software. RESULTS Experiment 1 Before the experimental manipulation, male breast color did not differ between experimental and control groups, indicating that plumage coloration was randomly distributed between treatments (brightness: F1,26 ¼ 0.003, P ¼ 0.958; YRC: one-way ANOVA: treatment F1,26 ¼ 2.166, P ¼ 0.153). The experimental manipulation resulted in differences in plumage coloration between groups (Figure 2a,b), both in brightness (repeated measurements ANOVA, treatment F1,26 ¼ 3.10, P ¼ 0.09; time F1,26 ¼ 0.14, P ¼ 0.71; time 3 treatment F1,26 ¼ 4.93, P ¼ 0.035; Figure 3a) and in YRC (F1,26 ¼ 8.57, P ¼ 0.007; time F1,26 ¼ 0.13, P ¼ 0.72; time 3 treatment F1,26 ¼ 2.25, P ¼ 0.14; Figure 3b). Males from the gland inaccessibility treatment showed higher brightness values (mean 6 standard deviation: 439.73 6 48.40; Newman–Keuls test P ¼ 0.037; Figure 3a) and lower YRC (0.75 6 0.03; Figure 3b) than males from the nonblocked group (brightness: 357.07 6 37.83; YRC: 0.79 6 0.03; Newman–Keuls test P ¼ 0.01). Experiment 2 Application of preen waxes changed spectral reflectance of male breast feathers (Figure 2c,d). When manually applied, preen waxes reduced the brightness (before application: 518.85 6 88.23; after application: 427.42 6 70.14; repeated measurements ANOVA, time F1,38 ¼ 203.3 P , 0.0001; Newman–Keuls test P , 0.0002; Figure 3c) and increased the YRC of breast feathers (before application: 0.72 6 0.05; after application: 0.75 6 0.05; F1,38 ¼ 162.3, P , 0.0001; Newman–Keuls test P , 0.0002; Figure 3d). The change in feather coloration after applying preen waxes was not different in relation to donor sex in brightness (D males: 98.93 6 42.02; D females: 99.27 6 45.84; sex F1,38 ¼ 2, P ¼ 0.17; time 3 sex F1,38 ¼ 0, P ¼ 0.98; Figure 3c) or in YRC (D males: 0.02 6 0.02; D females: 0.03 60.02; sex F1,38 ¼ 0.3, P ¼ 0.57; time 3 sex F1,38 ¼ 0.4, P ¼ 0.51; Figure 3d). DISCUSSION

Figure 1 Schematic representation of the uropygial gland showing how was it blocked in experimental males (a) and no blocked in control males (b). The silastic tube/ring is drawn in black.

Our results provide evidence that preen waxes act as cosmetics by enhancing plumage coloration. We found that males that were experimentally unable to smear their uropygial secretions into their plumage increased the overall brightness of their feathers and decreased the proportion of yellow–red


Experiment 1 Before the experimental manipulation, we measured the color of the red patch in the breast of each male and randomly assigned them to either a gland inaccessibility treatment (experimental males; N ¼ 15) or a control group (N ¼ 13). To block the application of uropygial secretion in the experimental group, we glued a silastic tube (1.95 mm outer diameter, 1.47 mm inner diameter; Dow Corning, Midland, USA) surrounding the nipple of the uropygial gland and sealed it at the base with surgical glue (tissue adhesive Vetbond; Henry Schein, USA). The length of the silastic tube created a gap between the base of the gland and the exterior, so the secretion was normally produced but the birds were not able to gather it in their beaks and smear it onto the plumage (Figure 1a). This method resembles the ‘‘avian condom’’ which was successfully used to prevent males from transferring sperm during copulations but still allowed them to ejaculate and defecate (Michl et al. 2002). Our manipulation did not damage any tissue, did not interfere with feeding, and had no measurable side effects on behavior (Lo´pez-Rull I, personal observations). The control group was equally manipulated but a ring of silastic, rather than a long tube, was glued surrounding the nipple, thus allowing control birds to smear the uropygial secretion into their feathers (Figure 1b). One week after, experimental manipulation color was measured again in both groups, and the silastic tube/ring was removed.

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reflectance. Similarly, when we manually applied preen waxes to museum specimens, we found that preen waxes significantly reduced brightness and increased YRC saturation. It has been proposed that the secretion of the uropygial gland could act as a cosmetic by increasing plumage brightness, and thus feathers coated more recently or with more preen wax would look brighter (Andersson and Amundsen 1996; Blanco et al. 1999; Delhey et al. 2007). Our results seem to contradict this prediction because we found that preen waxes decreased rather than increased brightness. The apparent discrepancy lies in the use of the term brightness, which causes some confusion as there is a generalized tendency to speak of colors that are more saturated as being brighter or more vivid even where there is no change in real brightness (Montgomerie 2006a). In fact, brightness is defined as a measure of the total amount of light reflected (i.e., by the feathers; Endler 1990), and thus colors that have higher brightness look washed out (Montgomerie 2006a). Therefore, assuming that as brightness increases plumage tends to get lighter, we would expect preen waxes to act as a cosmetic by decreasing plumage brightness, and thus increasing color hue and saturation. In agreement with our results, Piault et al. (2008) found that preen wax application reduced bill brightness in wild nestling tawny owls (Strix aluco) but did not differentially affect bill reflectance at different wavelength ranges. Similarly, Delhey et al. (2008) found that uropigyal secretions of blue tit (C. caeruleus) and mallard (A. platyrhynchos) reduced overall

brightness when manually applied to mallard feathers. Additionally, Surmacki and Nowakowski (2007) found that after removing soil and preen waxes from feathers of great tit (Parus major), the brightness increased. Unfortunately, these authors did not assess the relative contribution of those 2 agents (soil and wax) in influencing the change in color, and it is possible that there are differences in the effects of preen waxes and of soiling on the achromatic coloration. Altogether, these results may suggest that a decrease in brightness may be a general effect of preen gland secretion. In contrast with Piault et al. (2008) and 2 other studies in which no changes in plumage color due to the secretion were detected (Reneerkens and Korsten 2004; Delhey et al. 2008), here we show that the application of transparent preen waxes did affect feather reflectance at a particular color range. In both of our experiments, preen waxes enhanced relative reflectance at yellow–red wavelengths (560–700 nm), which is the color range that is subject to mate choice in house finches (Hill 2002). This result suggests that transparent preen waxes may play an important role in courtship and mate choice by making the ornament more conspicuous and thus updating its signal value. Because feather maintenance is unlikely to be cost free, a bird choosing a potential mate based on plumage appearance would select not only an individual that was in good condition during the molt to produce intensely colored feathers but also an individual of sufficiently high quality to devote enough time and energy to plumage maintenance


Figure 2 (a) The spectral reflectance of breast feathers after manipulation was higher in experimentally blocked males (i.e., without preen wax) than in control (nonblocked, i.e., waxed) males. (b) The change in spectral reflectance (mean reflectanceafter manipulation 2 mean reflectancebefore manipulation) of experimentally blocked males was higher (i.e., became brighter) across the spectrum, particularly in the yellow–red region, whereas the inverse was true for control (nonblocked) males. (c) In the second experiment, intact (nonwaxed) feathers were brighter than after smearing them with preen wax. (d) As in (b), feathers became less bright across the spectrum when preen wax was applied to them, especially in the yellow–red region.

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secretions and activities (Walther and Clayton 2005). Hence, changes in plumage coloration due to the application of preen waxes might be more accurate signals of current health and condition than either feather pigments or structural colors that are acquire by molting, usually long before they are used in displays (Montgomerie 2006a). Although preen waxes per se would not constitute a signal, selection for signal efficacy (Andersson 2000) might then favor those individuals that are able to increase signal intensity beyond what would result from merely preserving normal plumage condition. When feather-dressing substances have additional effects on plumage appearance, for example, making feathers appear more colorful, this could then provide the basis for further signal exaggeration (Delhey et al. 2007). Thus, individuals that are able to maintain their plumage in better condition are expected to be favored by sexual selection because they would display well-preserved feathers and more intense colors. Indeed, there is evidence that individuals with less worn-out plumage are in better condition, are dominant, have higher reproductive success, and are preferred by females over their less well-feathered counterparts (Fitzpatrick and Price 1997; Ferns and Lang 2003; Ferns and Hinsley 2004; Zampiga et al. 2004). In the present study, we did not measure female preferences in relation to cosmetic coloration, however, there is plenty of evidence that male house finches with

more colorful plumage pair more quickly and more often than less colorful males (Hill 2002). It seems likely that females would accrue the benefits of adaptive mate choice by preferentially mating with males whose signals provide an updated index of the males’ condition. Nevertheless, mate choice studies that experimentally manipulate the amount and quality of preen waxes smeared into feathers are required to assess how uropygial secretions have evolved their cosmetic functions. In a recent study, McGraw and Hill (2004) investigated the propensity for carotenoid-based color of feather patches in male house finches to change during the breeding period. They found that plumage coloration faded significantly over the season, probably due to feather degradation, plumage soiling, and pigment degradation. The likelihood of plumage fading over the course of the breeding season may serve as an important selective pressure for the evolution of feather morphology and also of seasonal mating behavior in house finches (McGraw and Hill 2004). Given the fitness benefits of displaying vividly colored plumage, males can be expected to evolve strategies to minimize color change. One such strategy in house finches appears to be the use of preen waxes because their application may not only prevent feather degradation but also enhance the ornamental value of plumage traits. If the different rates of color change between molts are


Figure 3 (a) Feather brightness (mean 6 standard deviation) of experimentally blocked males (open symbols) was higher than that of control (nonblocked) males (solid symbols) after (circles; time 2) but not before (squares; time 1) experimental manipulation (post hoc Newman–Keuls test s . d P ¼ 0.03). (b) Conversely, the feather YRC of control males after treatment was higher than that of experimentally blocked males (post hoc Newman–Keuls test d . s P ¼ 0.01, d . h P ¼ 0.03). (c) Similarly, feather brightness of museum skins was higher before (squares) than after (circles) manually applying preen waxes from living males (solid symbols) or females (open symbols; post hoc Newman–Keuls test n . d P ¼ 0.0001, n . s P ¼ 0.025, h . s P ¼ 0.0001, h . d P ¼ 0.0002). (d) As in experiment 1, feather YRC increased after manually applying preen waxes (post hoc Newman–Keuls test d . n P ¼ 0.0001, s . h P ¼ 0.0001, s . n P ¼ 0.05).

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be particularly useful in a social context where interactions between individuals are mediated by signal intensity. FUNDING Postdoctoral fellowship from the Consejo Superior de Investigaciones Cientı´ficas (Spain) to I.L.R. We thank P. Escalante and M. Gurrola from the bird collection of the Instituto de Biologıá, UNAM (Me´xico) for facilities with the museum skins and J.C. Morales from Facultad de Medicina Veterinaria y Zootecnia, UNAM (Me´xico) who helped to ensure the well-being of captive birds. We are grateful to R. Torres A. Velando, E. Avila, and J.A. Fargallo for their logistic help and suggestions. The authorization for working on animals was granted by Secretarıá del Medio Ambiente y Recursos Naturales (SEMARNAT).

REFERENCES Alonso-Alvarez C, Doutrelant C, Sorci G. 2004. Ultraviolet reflectance affects male–male interactions in the blue tit (Parus caeruleus ultramarinus). Behav Ecol. 15:805–809. Andersson S. 2000. Efficacy and content in avian colour signals. In: Espmark Y, Amundsen T, Rosenqvist G, editors. Animal signals: signalling and signalling design in animal communication. Trondheim (Norway): Tapir Academic. p. 47–60. Andersson S, Amundsen T. 1996. Ultraviolet colour vision and ornamentation in bluethroats. Proc R Soc Lond B Biol Sci. 264: 1587–1591. Blanco G, Seonae J, de la Puente J. 1999. Showiness, nonparasitic symbionts, and nutritional condition in a passerine bird. Ann Zool Fenn. 36:83–91. Darwin C. 1871. The descent of man, and selection in relation to sex. London: J. Murray. Delhey K, Peters A, Biederman P, Kempenaers B. 2008. Optical properties of the uropygial gland secretion: no evidence for UV cosmetics in birds. Naturwissenschaften. 95:939–946. Delhey K, Peters A, Johnsen A, Kempenaers B. 2006. Seasonal changes in blue tit colour: do they signal individual quality? Behav Ecol. 17:790–798. Delhey K, Peters A, Kempenaers B. 2007. Cosmetic coloration in birds: occurrence, function, and evolution. Am Nat. 169:145–158. Endler JA. 1980. Natural selection on color patterns in Poecilia reticulate. Evolution. 34:76–91. Endler JA. 1983. Natural and sexual selection on colour patterns in poeciliid fishes. Environ Biol Fishes. 9:173–190. Endler JA. 1990. On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc. 41:315–352. Ferns PN, Hinsley SA. 2004. Immaculate tits: head plumage pattern as an indicator of quality in birds. Anim Behav. 67:261–272. Ferns PN, Lang A. 2003. The value of immaculate mates: relationships between plumage quality and breeding success in shelducks. Ethology. 109:521–532. Figuerola J, Senar JC. 2005. Seasonal changes in carotenoid- and melanin based plumage coloration in great tit Parus major. Ibis. 147:797–802. Fitzpatrick S, Price P. 1997. Magpies’ tails: damage as indicator of quality. Behav Ecol. Sociobiol. 40:209–212. Fox HM, Vevers G. 1960. The nature of animal colors. New York: Macmillan. Ghosh A, Bhattacharyya SP. 1996. Endocrine factors in the regulation of the activity of the uropygial gland of avian skin. Proc Natl Acad Sci India. 66:227–236. Griffith SC, Pryke SR. 2006. Benefits to females of assessing colour displays. In: Hill EG, McGraw KJ, editors. Bird colouration. II. Function and evolution. Cambridge (MA): Harvard University Press. p. 233–279. Hasson O. 1991. Sexual displays as amplifiers: practical examples with an emphasis on feather decorations. Behav Ecol. 2:189–197. Haribal M, Dhondt AA, Rosane D, Rodriguez E. 2005. Chemistry of preen gland secretions of passerines: different pathways to same goal? Why? Chem Ecol. 15:251–260. Hill GE. 1990. Female house finches prefer colorful males: sexual selection for a condition-dependent trait. Anim Behav. 40:563–570.


related to individual capacity for preserving plumage, then the use of preen waxes could function as signal amplifier in birds because signal amplifiers increase the perceptibility of quality (Hasson 1991). In this context, preen waxes may amplify previously observed differences in male feather coloration on which female choice is based. Therefore, if female choice is initially based on color differences between males, then an amplifying signal may increase mating success of the more colorful male and further decrease mating success of the less colorful males. Conspicuous coloration may not only affect mate choice but also function as a status signal indicating the resource-holding potential (fighting ability) of the individual. Although melanin-based coloration is by far the best example of status signal ornamentation in birds (reviewed in Senar 2006), the expression of carotenoid-based plumage and structural color-based sexual ornaments have also been shown to predict success in dominance interactions between males (Pryke et al. 2002; Pryke and Andersson 2003; Alonso-Alvarez et al. 2004; Siefferman and Hill 2005). Because the expression of colorful ornaments may allow visual assessment of the rivals’ quality and thus prevent costly fighting, we propose that cosmetic coloration may also play a role in maintaining the honesty of dominant status signals. Indeed, the house finch plumage coloration is a condition-dependent trait and only males with access to large quantities of carotenoids, which avoid disease and are in good nutritional condition, can produce the reddest and more saturated plumage coloration (Hill 2002). However, although status and dominance are often correlated with condition (Griffith and Pryke 2006), no study has yet found that dimorphic color intensity correlates with dominance in this species (Hill 2002), thus the potential role of preen waxes on dominance via color enhancement will have to be assessed experimentally. Because the secretory activity of the uropygial gland is stimulated by high levels of circulating testosterone (Ghosh and Bhattacharyya 1996) and this and other hormones may mediate changes in the chemical composition of the secretion (Delhey et al. 2007), sex differences in chemical composition of preen waxes should be expected. Because the functions of preen waxes depend on their chemical composition (Patel et al. 2001), we predicted that preen waxes from males would increase more the signal intensity than those from females. When we manually applied preen waxes to museum skins, we found no differences in color change between feathers smeared with male secretion and feathers smeared with female secretion. This lack of relationship between plumage color change and sex may be explained in at least 4 ways: 1) We may have incurred in Type II error because of lack of power of our test (a ¼ 0.086), 2) natural selection has not decoupled the chemical nature of male and female preen waxes, 3) preen wax composition in females is also selected to enhance plumage coloration (female ornamentation), and 4) preen wax composition actually differs between sexes, yet their optical properties are similar in both sexes. Proper chemical analyses of preen wax composition at a speciesspecific level taking into consideration, sex may result in more testable hypotheses about functional aspects of preen wax variation within species. In conclusion, our results show that transparent preen waxes act as cosmetics by updating the signal content of feather ornamental traits. This finding implies that plumage color expression may function as a dynamic trait by accurately reflecting the current individual quality or condition, thereby increasing its signaling value. We suggest that sexual selection through mate choice or intrasexual competition has played a role in the evolution of preen wax composition and that cosmetic coloration reinforces the honesty of signals, which may

Lo´pez-Rull et al. • Cosmetic enhancement of signal coloration in the house finch

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