Behavioral Ecology Vol. 13 No. 6: 737–741
Individual color variation and male quality in pied flycatchers (Ficedula hypoleuca): a role of ultraviolet reflectance Heli Siitari and Esa Huhta Department of Biological and Environmental Science, Konnevesi Research Station, University of Jyva¨skyla¨, PO Box 35, FIN-40351 Jyva¨skyla¨, Finland Bright coloration of males in many animal species has inspired researchers for more than a century. In this field study, we investigated whether color variation between individuals is related to individual quality in pied flycatcher (Ficedula hypoleuca) males in terms of arrival time at the breeding sites. In addition to traditional visual color scoring, plumage color was measured using spectroradiometric measurements between 320 and 700 nm. This range includes the near-ultraviolet waveband from 320 to 400 nm. Males that arrived earlier at breeding sites had higher proportional UV reflectance in the crown and mantle. The proportional UV reflectance in the crown and mantle was not related to traditionally scored general brownness in males. However, adult males had a higher proportion of ultraviolet in the plumage than yearling males or females. These results suggest that in pied flycatcher males, the UV reflectance of plumage may be positively correlated with individual quality. Key words: breeding arrival, color variation, Ficedula hypoleuca, male quality, pied flycatchers, ultraviolet reflectance. [Behav Ecol 13:737– 741 (2002)]
I
n many animal species males advertise their quality with secondary sexual characteristics. One example is the bright plumage coloration of male birds in sexually dichromatic species; there is strong evidence that melanin- and carotenoid-based plumage colors operate in sexual selection (Andersson, 1994). Avian color vision differs from human vision; birds are sensitive to near-ultraviolet wavelengths (UV-A; 320–400 nm). Many bird species have UV-reflecting characters in the plumage (e.g., Andersson and Amundsen, 1997; Andersson et al., 1998; Bennett and Cuthill, 1994; Burkhardt, 1989; Finger and Burkhardt, 1994; Hunt et al., 1998), suggesting that UV reflectance might have a role in intra- and interspecific signaling. Recently, it has been shown that some structural colors (e.g., UV and blue) might be condition dependent (Keyser and Hill, 1999, 2000) and probably indicate male viability (Sheldon et al., 1999). The pied flycatcher (Ficedula hypoleuca) is a small, migratory, passerine bird (Lundberg and Alatalo, 1992) that is sexually dimorphic in color during the breeding season. However, the hue of males’ breeding plumage is highly variable, varying from conspicuous black and white to a femalelike dull brown. The color also varies between populations and depends on age: older birds are darker than young ones (Lundberg and Alatalo, 1992). Both intra- and interspecific signaling hypotheses have been used to explain male color variation in the pied flycatcher. The female mimicry hypothesis predicts that duller young males would benefit by obtaining a territory near the highquality territories of adult males (Rohwer et al., 1980). The status-signaling hypothesis (Slagsvold and Lifjeld, 1988) suggests that plumage coloration signals male quality to females and probably also functions in male–male interactions (e.g.,
Address correspondence to H. Siitari. E-mail:
[email protected]. E. Huhta is now at the Section of Ecology, Department of Biology, University of Turku, FIN-20014 Turku, Finland. Received 7 August 2001; revised 18 January 2002; accepted 18 January 2002. 2002 International Society for Behavioral Ecology
Kodric-Brown and Brown, 1984). Slagsvold and Lifjeld (1988) suggested that a conspicuous black-and-white plumage signals a bird’s presence to intruders and thus reduces the costs of holding a territory (the signaling of presence hypothesis). However, the results concerning the effects of male coloration in male–male interactions (Huhta and Alatalo, 1993; Saetre and Slagsvold, 1991) and in female mate choice (Alatalo et al., 1986, 1990; Saetre and Slagsvold, 1994; Saetre et al., 1995) are controversial. Interspecific competition may have affected male coloration. Evidence exists that plumage characteristics may prevent species hybridization when pied flycatchers are living in sympatric populations with collared flycatchers (Ficedula albicollis) (Saetre et al., 1997). Dark pied flycatcher males strongly resemble collared flycatcher males, but males of collared flycatchers are slightly larger and more dominant to pied flycatcher males (e.g., Alatalo et al., 1982). However, both the pied and collared flycatcher females are dull brown. The brown coloration of some male pied flycatchers may benefit them in interspecies competition over nest sites; compared to black pied flycatcher males, brown males can establish a territory closer to more dominant collared flycatchers’ high-quality territories (Alatalo et al., 1994). In general, studies concerning possible effects of individual quality on color variation and especially on UV color variation are scarce (see Keyser and Hill, 1999, 2000; Sheldon et al., 1999). It is known that pied flycatchers do not have reflectance peaks in the UV area of light spectrum (Go¨tmark and Hohlfa¨lt, 1995), in contrast to blue tits, for example (Hunt et al., 1998). However, this does not exclude the possibility that UV reflectance can affect visual signaling between individuals (Bennett et al., 1996, 1997; Cuthill et al., 1999, 2000). In addition, excluding the UV spectrum when measuring variation in plumage color is likely to bias the determination of total plumage brightness. In migratory birds, arrival time has direct effects on individual fitness. First-arriving males gain the best territories, and, in pied flycatchers, territory quality is an important cue in female mate choice (Alatalo et al., 1986). Moreover, in polyterritorial and polygynous species, early arrival improves the
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male’s possibilities of gaining a secondary territory and improves his chances of mating polygynously (Alatalo et al., 1984, 1990). This increases the male’s reproductive success (Lundberg and Alatalo, 1992; Stenberg, 1989). These effects of early arrival on male reproductive success have been observed in many other species (e.g., Hasselquist, 1998; Langefors et al., 1998; Lozano et al., 1996; Møller, 1994a,b). In collared flycatchers date of arrival is negatively correlated with a measure of male condition (% glycosylated hemoglobin; Andersson and Gustafsson, 1995), and in barn swallows a measure of condition (hematocrit) is related to both arrival date and the size of male’s sexual ornament (Saino et al., 1997a,b). In addition to the benefits gained, early arrival is also supposed to be costly (Kokko, 1999). This is because the earlyarriving males often suffer from unfavorable weather conditions and lack of suitable food (Alatalo et al., 1984). Only males in good condition will be able to tolerate the costs associated with early arrival (Møller, 1994b). In this field study, we investigated the individual color variation of pied flycatchers in a natural population. The development of tools to investigate color offered us a novel way to measure natural variation in color among individuals. We measured the color between 320 and 700 nm and examined whether the color correlates with male quality in terms of order of male arrival to the breeding sites. In addition, we investigated age and sex differences in UV coloration, which are invisible to human eye. METHODS The study was conducted at the Konnevesi Research Station in Central Finland (63⬚37⬘ N, 26⬚21⬘ E) in 1995 and 1999. Birds arrive in the study area mainly in May, and the last individuals arrive in the beginning of June. We observed arrival order of the birds by visiting nest-boxes daily in three separate study areas (total of 120 nest-boxes). We caught each male using nest-box traps on the day after arrival. A total of 66 males were captured; 32 males in May 1995 and 34 in May 1999. An additional 14 males were captured in June 1995, when they were feeding nestlings. These males were used only in color analysis when comparing plumage characteristics and were excluded from the analysis when testing the effect of arrival date on male plumage characteristics, as their arrival date was unknown. Birds were aged as yearlings or older on the basis of the cover and shape of the outer wing coverts (see Lundberg and Alatalo, 1992). Plumage color at the arrival date was measured using a spectroradiometer. In addition, we scored male plumage brownness of the dorsal side from 0 to 100% (100% means femalelike dull brown, 0% means totally black male in dorsal side; scoring was based on human vision in 5% increments; Lundberg and Alatalo, 1992). After that we ringed the birds and released them back to their territories. Females (n ⫽ 19) were caught from nest-boxes during incubation for color measurements and ringing using the same procedure as for males. Spectroradiometric measurements We measured plumage color with a spectroradiometer (EG and G Gamma Scientific GS 3100). The measurement procedure changed between 1995 and 1999 for the improvement of the equipment. In 1995 the illumination was provided with one Osram Eversun L 40W/79K solarium tube (emitting mainly between 300–400 nm) and 60 W visible light tube. In 1999 we used a standard light source (EG and G RS-22 UV xenon fibre optic light source) connected with a probe to an adjustable mounting stand (Gamma Scientific, 191C-02). The plumage was illuminated at 45⬚ to the measuring surface by a
xenon light source. Reflected light was collected with the fiber optic probe at 90⬚ (45⬚ to illumination) connected to a mounting stand at the fixed distance of 17 mm using the same spectroradiometer as in 1995. Spectra were recorded at 5-nm intervals between 320 and 700 nm and measured as a proportion of the light reflected from a calibrated reflectance standard (LabSphere, 98%). The step was adjusted at 5-nm intervals to speed up the procedure. Adjustment did not affect the shape of the spectrum measured. The shape of the spectrum determines the color of the spot measured. Humans perceive and classify color using two properties: hue and chroma (Endler, 1990). Hue is the sensation of the color, correlating with the wavelength of the maximum of the slope. Chroma is the measure of purity or saturation. The brightness of a color spot may be defined as the total intensity of the light spectrum (total reflectance, Rtot; Endler, 1990). However, the variation in hue and brightness in pied flycatchers is high due to the hue variation from almost completely black to dull-brown birds. To concentrate on the ultraviolet part of the spectrum, we calculated the proportion of the ultraviolet in each plumage spectrum measured (relative UV reflectance or UV chroma; R320–400nm/R320–700nm; see also Andersson et al., 1998; Sheldon et al., 1999). We measured the reflectance of the crown, mantle, and breast from both males and females. The area measured was 1 ⫻ 1.5 mm2. As the recording of one spectrum took about 2 min and the objects measured were live birds, we took only one measurement per plumage region. However, in the analysis we combined the proportional UV reflectance of crown and mantle to a single variable (dorsal side) by calculating the mean between their relative UV reflectance values. To control for any unwanted time effects on color determination, we remeasured the color of 21 birds in 1999. After the first measurement the birds were kept in captivity and measured again after about 6 days. The relative UV reflectance values did not change during the time, and the repeatability (R; Lessells and Boag, 1987) of relative UV reflectance measurements was high (R ⫽ 0.73; F21,20 ⫽ 6.475, p ⬍ .001). Because measurement equipment changed between 1995 and 1999, we obtained higher reflectance values in 1995 compared to 1999. The difference was due to differences in light sources and distance between plumage and measuring probe. The mean difference in total reflectance between the years (mean % ⫾ SE) was 1.25 ⫾ 0.51 for the dorsal side and 2.96 ⫾ 0.57 for the breast. We corrected this bias by removing the mean difference of the measurements between 1995 and 1999 from the original values of 1995. Corrected values are shown in Table 1. Analysis of data The relative UV reflectance and brownness values were arcsine square-root transformed to meet the assumptions of normality. We used univariate and multivariate ANOVAs in the analyses. All probabilities are two tailed. We carried out the statistics with version 10.0 of SPSS for Windows package. RESULTS UV reflectance in relation to male characteristics and arrival time The median arrival date in 1995 was 21 May, and in 1999 the median was 22 May. Arrival dates are presented as days of May, and they did not differ between the 2 years (Mann-Whitney U32,34 ⫽ 522.0, p ⫽ 0.777). Thus, we do not have to correct for dates in separate years. Age had an effect on male brown-
Siitari and Huhta • UV reflectance and male quality
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Table 1 Mean values of the relative UV reflectance (UV chroma) and brownness of adult and yearling males and females in years 1995 and 1999 Adult male
Yearling male
Female
Character
n
Mean
SD
n
Mean
SD
n
Mean
SD
1995 UV chroma of mantle UV chroma of breast Brownness
33 28 33
14.2 14.2 39.9
3.0 2.2 31.1
13 13 13
12.8 12.3 75.0
1.6 1.4 20.54
9 11 13
13.2 11.9 100.0
0.7 0.9 0
1999 UV chroma of mantle UV chroma of breast Brownness
19 20 21
15.4 14.8 32.4
2.4 2.7 33.6
13 13 13
13.4 12.3 62.5
2.5 2.5 35.7
10 10 10
10.7 11.2 100.0
2.8 2.2 0
ness and on relative UV reflectance of breast and dorsal side (Tables 1 and 2), and thus age was used as a factor in the analysis. However, after Bonferroni correction, the effect of age on UV reflectance of dorsal side relative was only marginal (Table 2). Male age was not related to male arrival time (age: F1,64 ⫽ 1.642, p ⫽ .205). Examples of the mean reflectance spectrum of human-visible black and human-visible brown male pied flycatchers are in Figure 1. The figure represents the typical human-visible black and brown males; the reflectance spectra of the rest of the males greatly varied between the two types represented here. The males with a darker dorsal side had a brighter breast. Age was also related to male brownness (Table 2, Figure 2a). Old males often had dark dorsal sides and bright breasts, whereas young males had duller breasts. Males with higher relative UV reflectance in their dorsal side, independently of male brownness (Table 2), arrived earlier to the breeding sites (Table 2, Figure 2b). First-arriving males had twice the relative UV reflectance of males arriving at the end of May (Figure 2b). In contrast, male arrival time was related to neither male browness nor to the relative UV reflectance of the breast (Table 2). UV reflectance in relation to sex As described in the previous section, age had an effect on male relative UV reflectance and brownness. Hence, when comparing sexes, age was taken into account and birds were divided into three groups: adult males, yearling males, and females. Again, years were pooled in the analysis. The relative UV reflectance of the breast and dorsal side differed between the three groups (dorsal side: F2,88 ⫽ 8.670, p ⬍ .001; breast: F2,88 ⫽ 16.106, p ⬍ .001). In pairwise comparisons the relative UV reflectance of the breast was higher in adult males compared to females and yearling males (probabilities corrected for multiple comparisons with sequential Bonferroni correc-
tions; Rice, 1989): p ⬍ .001 for differences between adult males and females (mean difference [MD] ⫽ 0.043) and adult males and yearlings (MD ⫽ 0.032). But the relative UV reflectance of the breast did not differ between yearlings and females (MD ⫽ 0.011, p ⫽ .784). The relative UV reflectance of the dorsal side differed only between adult males and females (MD ⫽ 0.041, p ⬍ .001; between adult males and yearlings, MD ⫽ 0.020, p ⫽ .152; between yearlings and females, MD ⫽ 0.021, p ⫽ .215). DISCUSSION Males with higher relative UV reflectance in their dorsal side, independent of their dorsal side brownness, arrived earlier to breeding sites (Figure 2b). This suggests that the relative UV reflectance of the dorsal side might reflect male quality in this species. Arrival time was not related to male age in this study, but in general, old males were darker and had higher relative UV reflectance values than yearling males. Early arrival is essential for pied flycatcher males, and according to earlier studies in other species, arrival time reflects male quality (e.g., Andersson and Gustafsson, 1995; Kokko, 1999; Møller, 1994a,b). Pied flycatcher males that arrive early have fewer blood parasites (Trypanosoma spp.) than males arriving later (Ra¨tti et al., 1993). Early breeders produce ⬎ 50% more offspring compared to males that arrive later (Stenberg, 1989). This is because clutch size decreases with the progress of breeding season (Lundberg and Alatalo, 1992), and late males will often have only one female and remain monogamous or unpaired (Alatalo et al., 1984, 1990). Thus, males arriving later suffer from reduced fitness (Lundberg and Alatalo, 1992). Recent studies have indicated condition-dependent variation in structural-based UV coloration in blue tits (Parus caeruleus; Sheldon et al., 1999) and in blue grosbeaks (Guiraca caerulea; Keyser and Hill, 1999). Blue tit males that survived
Table 2 Effects of age and year (factors) and arrival time (covariate) on male relative UV reflectance (UV chroma) of dorsal side and breast, and their effect on male brownness Breast
Age Year Arrival time
Dorsal side
df
F
p
df
1,55 1,55 1,55
15.741 0.550 0.011
⬍.001 .462 .916
1,55 1,55 1,55
F 4.900 1.898 15.000
Brownness p .062 .174 ⬍.001
df
F
p
1,55 1,55 1,55
13.343 0.742 0.043
.003 .393 .837
Sequential Bonferroni corrections (Rice, 1989) have been conducted for the p values.
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Behavioral Ecology Vol. 13 No. 6
Figure 1 Mean reflectance spectra of five black (thin line) and brown (thick line) pied flycatcher males. The range of human visual sensitivity is 400–700 nm. The near UV waveband is 320–400 nm.
the winter had higher relative UV reflectances (UV chromas) than males that were not recaptured (Sheldon et al., 1999). Moreover, manipulation of the crown UV color influenced brood sex ratios; males with greater crown UV chromas had proportionally more sons in their broods than males with experimentally reduced UV chromas (Sheldon et al., 1999). In blue grosbeaks the expression of blueness in plumage is positively correlated with increased tail feather growth (Keyser and Hill, 1999). In addition, intensity and size of the structural-based blue breast ornament is positively correlated with male body size, territory size, and prey abundance, suggesting that UV coloration functions as an honest, intraspecific signal of quality (Keyser and Hill, 2000). In contrast to the above species, the color of the pied flycatcher is melanin based (Lundberg and Alatalo, 1992). Melanin- and carotenoid-based colors are the two classes of pigment colors. Although pigment colors are not expected to reflect UV (Burkhardt, 1989), some variation in UV reflectance has been found also in these colors (e.g., Finger and Burkhardt, 1994; Hunt et al., 1998). In addition, many structural colors are produced by melanin in layers. For example, the structural color of the starling (Sturnus vulgaris) is melanin based and strongly reflects UV (Bennett et al., 1997). According to this study, old males usually have a darker dorsal side with relatively high proportional UV reflectance and a whiter breast (Figure 1). This color combination may signal male presence to potential mates and intruders in a territory early in the spring (Slagsvold and Lifjeld, 1988). Females may use plumage color as an indirect cue of male age and benefit directly from higher performance of parental care by older and high-quality males (Saetre et al., 1995). The similar relationship between age and UV coloration has been found in bluethroats (Luscinia s. svecica; Andersson and Amundsen, 1997) and in blue grosbeaks (Keyser and Hill, 1999). However, in pied flycatchers, male arrival date affects male mating success more than age (Alatalo et al., 1984). The effect of human-visible color (brownness) on male quality in pied flycatchers has been debated. In sympatric populations with collared flycatchers, the dorsal-side brownness may be important in species recognition, as hybrids with collared flycatchers suffer from reduced breeding success (Alatalo et al., 1994; Saetre et al., 1997). An experimental study by Alatalo et al. (1994) indicated that pied flycatcher males with femalelike brown plumage could establish a territory close to more dominant collared flycatcher males compared with dark pied flycatcher males. Moreover, male dorsal-side color (brownness) is highly heritable (Alatalo et al., 1994),
Figure 2 (a) The relationship between relative UV reflectance of breast and male brownness (years 1995 and 1999 pooled). (b) The relationship between relative UV reflectance of dorsal side and male arrival time. Only males that arrived in May are included in the analysis. For both panels, filled circles represent adult males, and open circles represent yearling males. For statistics, see Table 2.
and there are indications of only small effects of environmental conditions on male brownness (Alatalo et al., 1994; Slagsvold and Lifjeld, 1992). However, in contrast to brownness, the proportional UV reflectance of the male dorsal side could be a cue to quality for both potential mates and intruders because relative UV reflectance in the dorsal side was generally independent of male brownness. Finally, together with some recent studies (Keyser and Hill, 1999, 2000; Sheldon et al., 1999), this study suggests that UV reflectance of male plumage could be positively related to individual quality. In this study, however, the color is based on melanin in layers instead of basic structural coloration. Furthermore, this study indicates that UV reflectance might play an important role in intra- and intersexual signaling among pied flycatchers. Experiments manipulating short wavelength reflectance in the field and laboratory are the best way to investigate these further possibilities (Cuthill et al., 2000). We thank Mark Einbork, Petri Suorsa, and Rauno Alatalo for the help in the field. Birds were captured and kept in the captivity with the
Siitari and Huhta • UV reflectance and male quality
permission of Central Finland Environmental Centre (permission nr 0999LO253/254). We are grateful especially to Innes Cuthill, Rauno Alatalo, Ma˚ns Andersson, Johanna Honkavaara, Janne Kotiaho, Laura Vertainen, and the people in the roundtable discussion for valuable comments on the earlier versions of this manuscript. The Academy of Finland, Emil Aaltonen Foundation, and Ella and Georg Ehrnrooth’s Foundation supported the study.
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