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Proc Natl Acad Sci U S A. Aug 5, 1997; 94(16): 8618–8621.
PMCID: PMC23047
Ecology

Ultraviolet plumage colors predict mate preferences in starlings

Abstract

Avian plumage has long been used to test theories of sexual selection, with humans assessing the colors. However, many birds see in the ultraviolet (<400 nm), to which humans are blind. Consequently, it is important to know whether natural variation in UV reflectance from plumage functions in sexual signaling. We show that female starlings rank males differently when UV wavelengths are present or absent. Principal component analysis of ≈1300 reflectance spectra (300–700 nm) taken from sexually dimorphic plumage regions of males predicted preference under the UV+ treatment. Under UV− conditions, females ranked males in a different and nonrandom order, but plumage reflectance in the human visible spectrum did not predict choice. Natural variation in UV reflectance is thus important in avian mate assessment, and the prevailing light environment can have profound effects on observed mating preferences.

Ever since the work of Darwin (1), avian plumage coloration has been a major focus for studies of sexual selection (2). Almost without exception, these colors have been assessed, quantified, or manipulated according to human standards (3) even though humans are not the receivers for which the signals evolved. Avian color vision differs from our own in several key ways: most birds see in the UV (to which humans are blind), have at least four spectrally distinct classes of retinal cone cells (compared with only three in humans), and have oil droplets that filter the light reaching the cone photopigments (4, 5). Recent experiments (6) show that female zebra finches (Taeniopygia guttata) avoid males whose plumage lacks UV reflectance and that their preference for symmetry in artificial ornaments (7) extends to leg bands arrangements that are discriminable only in the UV (6). A crucial question remains: Is naturally occurring individual variation in UV reflectance used in mate choice decisions, or is it redundant in information terms and thus ignored, being correlated with reflectance variation in the human visible waveband? We tested these possibilities by forcing female starlings (Sturnus vulgaris) to choose between the same males under conditions in which their natural UV reflectance was either present or absent.

METHODS

The experiment was conducted on 48 wild-caught adult starlings that were in breeding plumage during spring (8, 9). Male plumage at this time exhibits extensive areas of iridescence, especially on the throat and coverts (8). These regions show variation in reflectance at short wavelengths (Fig. (Fig.1),1), so potential UV cues exist. Mate choice preferences were investigated in an apparatus we have described (6, 7) that is similar to that used in numerous avian mate choice experiments. In brief, a single female visually assesses four males, with her preference indicated by the number of hops (or time) in front of each male (6, 7). By means of transparent filters mounted vertically between the female and each stimulus male, wavelengths available for mate choice decisions were manipulated such that UV wavelengths were available in some trials (UV+) but not others (UV−) (Fig. (Fig.1).1). We used eight pairs of females (n = 16) and eight quartets of males (n = 32), with each female of a pair viewing the same quartet of males in separate trials. All females viewed males under both UV+ and UV− treatments (Fig. (Fig.1),1), so each quartet of males was assessed four times (two females × two treatments). By comparing the preferences of females (within a pair) within filter treatments and across filter treatments, we could determine (i) if the females’ rankings of males were consistent within each filter treatment and (ii) whether they differed when UV wavelengths were removed.

Figure 1
Left axis and solid lines, transmission spectra of the two filter types (UV+, UV−) used in the experiment. Spectra are the mean of five randomly located measurements on each filter taken with a Unicam Prism spectrophotometer. The two filter ...

To investigate the choice criteria used by females, we measured a variety of traits on males at the end of the mate choice experiment. Nine morphometric variables that we thought might be reliable indicators of size or body condition were measured: mass, fat score [a 6-point subjective scale (11)], length of tarsis (means of three measurements each on left and right leg), length of 8th primary feathers (mean of three measurements each on left and right wing), asymmetry of tarsi, asymmetry of 8th primary feathers, percentage of throat feathers with white spots, and percentage of covert feathers with white spots (methods as in ref. 12). Starling beaks change from black to yellow during the breeding season (8, 9), so the percentage of upper and lower mandible that was black was scored subjectively to the nearest 10%. The “color” of male plumage was assessed using ≈1300 reflectance spectra (300–700 nm) obtained from a sample of feathers which were removed at the completion of the experiment (details in legend to Fig. Fig.3).3). The analysis of reflectance spectra has major advantages over traditional methods used for assessing avian coloration (3, 13). Reflectance spectra are the inherent properties of feathers that, with the ambient illumination, determine the raw signal perceived by the avian eye (13); reflectance spectra are not biased by human trichromacy nor humans’ narrow spectral range (3). Second, subtle variation in reflectance spectra can be detected statistically via principal component analysis (13), as used here. Feathers were selected randomly from the throat and wing coverts because both of these regions are revealed during male displays (8, 14) and throat feathers are sexually dimorphic (8).

Figure 3
Reflectance spectra of the iridescent throat feathers of the most preferred and least preferred males under (a) UV+ conditions and (b) UV− conditions. Each spectrum is the mean of the bird means for the eight respective males, calculated ...

RESULTS AND DISCUSSION

In both UV+ and UV− treatments, the preferences for particular males were highly correlated between females within a pair (Fig. (Fig.2).2). In contrast, the preferences across the two treatments were not significantly correlated. From these effects we can draw the important conclusion that different females rank males in the same way within any one illumination condition but that females rank males differently under UV+ and UV− conditions. The fact that females show consistent preferences under UV− conditions implies that removing UV wavelengths does not totally abolish species or sex recognition, or have a nonspecific stress effect. If removal of UV made the stimulus birds unrecognizable as male starlings or was stressful through creation of “unnatural” or novel viewing conditions, we would expect UV− preferences to tend toward random. Instead, removing the UV did not abolish preference but changed the criteria for choice.

Figure 2
The similarity of preference of each pair of females for each of the four males within a quartet was assessed by Pearson correlation on the numbers of hops facing each male (actual durations show the same pattern). Whether any one pair of females shows ...

None of the morphological variables independently predicted which males were preferred under either UV+ or UV− conditions (Table (Table1).1). By contrast, the spectrophotometric variables did predict female preferences although only under UV+ conditions (Table (Table1).1). In that treatment, the shape of spectral reflections of both the iridescent region of throat feathers and the throat feather tips was correlated with male attractiveness. Of course, under UV− conditions, some other variable that we did not measure (such as display rate) may predict female choice; the crucial result is that spectral reflectance within the human visible waveband did not. Inspection of the principal components revealed which features of spectra predicted UV+ attractiveness (Table (Table1;1; Fig. Fig.3).3). It is intriguing that the throat “color” predictors of preference have human visible correlates (preferred males should have more purple, and less greenish, throats), yet removal of UV changes the “normal” ranking. This suggests that, although, in information terms, one could consider the UV signal as being somewhat redundant (being correlated with human visible variation), it is nevertheless a component of the birds’ mating decisions. This may arise because the UV waveband is “hard-wired” to contribute to hue perception, irrespective of any value of the waveband in information terms. Alternatively, as variation in the UV is not perfectly correlated with variation in the human visible waveband, the UV may still provide useful (nonredundant) information. Precisely what information the UV waveband is signaling remains to be determined. Nevertheless, our results suggests that even though variation in the UV waveband is correlated with variation in the human visible waveband, the UV variation plays an important role in mate choice decisions.

Table 1
Characteristics of males that predicted their rankings by females under UV+ and UV− conditions, shown separately for morphometric variables and plumage reflectance spectra

Hamilton (16), in relation to the parasite theory of sexual selection (17), suggested that it might be worthwhile paying attention to UV reflectances from birds such as starlings, which had high parasite loads but appeared dull to humans. Although our results might at first sight seem to support Hamilton’s proposition and so add to the tentative support for the hypothesis from a comparative study (18), our results in fact showed that preferred males had relatively less UV reflectance than nonpreferred males (Fig. (Fig.3).3). Moreover, it is probably unwise to think of particular wavebands as being particularly “colorful” or “conspicuous”; colors are the perceptual representation of particular comparisons of reflectance at certain wavelengths (3, 13). Our results strongly suggest that (relative) UV reflectance of starling plumage affects male attractiveness but that it is low UV and green reflectance, in combination with high violet and red wavelengths, that females prefer (Fig. (Fig.3).3). How preference translates to starling colors, as opposed to human colors, will only be clear when a fuller understanding of starling color cognition is available (3).

The fact that removal of the UV cues did not abolish preferences of females (i.e., to random levels) suggests that UV plumage cues are not used exclusively for species recognition. This conclusion is also supported by our finding that intraspecific variation (including the UV waveband) predicted female choice. We make no claims that UV cues are not used in avian species recognition, simply that our evidence points to finer-tuned discrimination. These results, and those from zebra finches (6), do not support the hypothesis (19) that UV will tend to be used in mate choice decisions when plumage reflects “purely” in the UV; in neither species are reflectances purely (or even predominantly) in the UV, yet in both species UV plays a clear role in conspecific ranking.

Our study also demonstrates how behavioral experiments conducted under UV-deficient conditions can produce statistically robust conclusions that are, nevertheless, spurious in a natural context. Further experiments will be required to determine if the UV is in any way a “special” waveband for avian sexual signaling (4, 19) or is predisposed for signaling condition-dependent rather than aesthetic traits (2). Clearly, though, one should be very cautious about ignoring the UV waveband when considering avian mate choice experiments (see also ref. 20), plumage coloration, or display behavior in natural environments. Like fish (2123), and consistent with recent studies on other avian species (6, 20, 24), birds are sensitive to the light conditions under which they choose mates.

Acknowledgments

We are very grateful to D. Burkhardt and R. H. Douglas for loans of equipment and to D. Burkhardt, R. H. Douglas, J. A. Endler, E. Finger, A. R. Goldsmith, W. D. Hamilton, E. Maier, N. J. Marshall, D. Osorio, A. Pomiankowski, J. Radwan, and an anonymous referee for stimulating discussions and helpful suggestions. This research was funded by the Biotechnology and Biological Sciences Research Council and the Nuffield Foundation.

References

1. Darwin C. The Descent of Man and Selection in Relation to Sex. London: Murray; 1871.
2. Andersson M. Sexual Selection. Princeton, NJ: Princeton Univ. Press; 1996.
3. Bennett A T D, Cuthill I C, Norris K J. Am Nat. 1994;144:848–860.
4. Bennett A T D, Cuthill I C. Vision Res. 1994;34:1471–1478. [PubMed]
5. Partridge J C. J Comp Physiol A. 1989;165:415–426.
6. Bennett A T D, Cuthill I C, Partridge J C, Maier E J. Nature (London) 1996;380:433–435.
7. Swaddle J P, Cuthill I C. Nature (London) 1994;367:165–166.
8. Feare C. The Starling. Oxford: Oxford Univ. Press; 1984.
9. Nicholls T J, Goldsmith A R, Dawson A. Physiol Rev. 1988;68:133–176. [PubMed]
10. Winer B J, Brown D J, Michels K M. Statistical Principles in Experimental Design. 3rd Ed. New York: McGraw–Hill; 1991.
11. Helms C W, Drury W H. Bird Band. 1960;31:1–40.
12. Swaddle J P, Witter M S. Proc R Soc London Ser B. 1994;255:147–152.
13. Endler J A. Biol J Linn Soc Lond. 1990;41:315–352.
14. Eens M, Pinxten R, Verheyen R F. Behavior. 1991;116:210–238.
15. Seigel S, Castellan N J. Nonparametric Statistics for the Behavioral Sciences. 2nd Ed. New York: McGraw–Hill; 1988.
16. Hamilton W D. Am Zool. 1990;30:341–352.
17. Hamilton W D, Zuk M. Science. 1982;218:384–387. [PubMed]
18. Radwan J. Acta Ornith. 1993;27:125–130.
19. Andersson S. Proc R Soc London Ser B. 1996;263:843–848.
20. Hunt, S., Cuthill, I. C., Swaddle, J. P. & Bennett, A. T. D. (1997) Anim. Behav., in press.
21. Endler J A. Anim Behav. 1987;35:1376–1385.
22. Milinski M, Bakker T C M. Nature (London) 1990;344:330–333.
23. Endler J A. Vision Res. 1991;31:587–608. [PubMed]
24. Endler J A, Thery M. Am Nat. 1996;148:421–452.

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