cryptic dichromatism and seasonal color variation in the diademed

The Condor 107:648–656 q The Cooper Ornithological Society 2005

CRYPTIC DICHROMATISM AND SEASONAL COLOR VARIATION IN THE DIADEMED TANAGER PABLO L. TUBARO1,3, DARIO A. LIJTMAER1,

AND

STEPHEN C. LOUGHEED2

1

Divisioń de Ornitologıá. Museo Argentino de Ciencias Naturales ‘‘Bernardino Rivadavia’’, Buenos Aires, Argentina 2Department of Biology, Queen’s University, Kingston, Ontario, K7L 3N6, Canada

Abstract. We studied the patterns of sexual dichromatism and seasonal variation in plumage color in the Diademed Tanager (Stephanophorus diadematus), a species previously considered devoid of variation in adult plumage. The general coloration of this species is dark blue-violet, with a white-blue and red crown. Plumage reflectance of seven body regions from 33 study skins belonging to adults of both sexes was measured. Reflectance values were used in a principal components analysis (PCA) and hue, short-wave chroma, and UV chroma were also measured directly on the spectra. Both PCA factor scores and these latter variables were subjected to twoway ANCOVAs with sex and season as main factors and the year of capture as a covariate. We found that crowns of males were significantly brighter than those of females. In addition, the nape, chest, and belly showed significant differences in spectral shape, with relatively greater short-wave reflectance and less long-wave reflectance in males than in females. Although sexes were alike in hue, they differed in chroma in almost all body regions. Brightness also differed between seasons, and contrary to our expectation nonbreeding birds were brighter than breeding ones. This result may be a consequence of the particular molt program of tanagers that includes only a complete post-reproductive molt. Despite finding seasonal differences in spectral shape in various body regions, no significant changes in hue, short-wave chroma, or UV chroma were evident. To our knowledge, this is the first report of variation in adult plumage color for the Diademed Tanager, and we suggest that dichromatism in tanagers may be even more pervasive than is currently recognized. Key words: plumage, sexual dimorphism, Stephanophorus diadematus, Thraupidae, UV, vision.

Dicromatismo Crı´ptico y Variacioń Estacional de Color en Stephanophorus diadematus Resumen. Estudiamos los patrones de dicromatismo sexual y variacioń estacional en la coloracioń del plumaje de Stephanophorus diadematus, una especie previamente considerada carente de variacioń en la coloracioń del plumaje adulto. La coloracioń general de esta especie es azul violaćeo oscuro, con una corona blanca azulada y roja. Se midio´ la reflectancia de siete regiones corporales en 33 pieles de estudio pertenecientes a adultos de ambos sexos. Los valores de reflectancia se utilizaron en un ana´lisis de componentes principales, y adema´s se midieron el tono (hue), la intensidad del color de onda corta y la intensidad del color de UV directamente sobre los espectros. Tanto los factores del ana´lisis de componentes principales como las variables mencionadas fueron sujetos a ANCOVAs de dos factores, considerando el sexo y la estacioń como factores principales, y el anõ de captura como covariable. Estos ana´lisis mostraron que la corona de los machos es significativamente ma´s brillante que la de las hembras. Adema´s, la nuca, el pecho y el vientre mostraron diferencias significativas en la forma espectral, presentando los machos mayor reflectancia en la zona de onda corta y menor en la zona de onda larga que las hembras. Si bien el tono no difirio´ entre sexos, la intensidad del color difirio´ en la mayorıá de las regiones corporales entre machos y hembras. El brillo tambień difirio´ entre temporadas y, contrariamente a nuestra expectativa, los individuos capturados en la temporada no reproductiva fueron ma´s brillantes que aquellos capturados en la temporada reproductiva. Este resultado podrıá deberse al programa de muda particular presente en Thraupidae, que incluye una uńica muda post-reproductiva completa. Si bien encontramos diferencias entre estaciones en la forma espectral en varias regiones corporales, no se detectaron diferencias en el tono, la intensidad del color de onda corta ni la intensidad del color de UV. Este es, de acuerdo a nuestro conocimiento, el primer estudio que muestra variacioń en la coloracioń del plumaje adulto de S. diadematus. Sugerimos que el dicromatismo en Thraupidae podrıá ser ma´s comuń de lo que actualmente se piensa. Manuscript received 11 July 2004; accepted 29 March 2005. 3 E-mail: [email protected] [648]

CRYPTIC COLOR VARIATION IN THE DIADEMED TANAGER

INTRODUCTION The tanagers (family Thraupidae) are among the most colorful birds of the New World, with about half of the species showing marked sexual dimorphism in plumage (Burns 1998, Isler and Isler 1999). In the case of the Diademed Tanager (Stephanophorus diadematus), both sexes are alike and thus, this species has always been considered monochromatic (Ridgely and Tudor 1989, Isler and Isler 1999). The adult plumage is blue-violet suffused black, with a white-blue crown, and a small patch of red feathers on top. The wings and the tail are predominantly black, feathers edged with blue, although marginal wing coverts, nape, rump, and edges of crown patch are bluer than the rest of the plumage. Forecrown, lores, and chin are black. The suggested monochromatism of the Diademed Tanager is based on human perception of color, which differs from that of birds (Bowmaker et al. 1997); humans cannot see UV wavelengths that are visible to birds (Bennett and Cuthill 1994, Cuthill et al. 2000a, 2000b). Moreover, birds have four types of single cones in the retina (instead of the three present in humans) and oil droplets that reduce both the waveband to which each cone is sensitive and the overlap among their spectral sensitivities. Thus, descriptions of plumage color made by humans are inadequate for the study of many biologically relevant questions (Cuthill et al. 2000a, 2000b). To overcome this problem, most recent studies of plumage color have employed reflectance spetrophotometry to quantify objectively the light reflected by feathers (Burkhardt 1989, Andersson et al. 1998, Cuthill et al. 1999, Sheldon et al. 1999, Hausmann et al. 2003). This, together with information about natural light sources, background reflectance, and sensitivity curves of bird photoreceptors, has markedly improved our understanding of visual signal ecology and evolution (Endler 1990, Endler and The´ry 1996, Andersson et al. 1998, McNaught and Owens 2002). We studied the reflectance spectrophotometry of museum specimens of the Diademed Tanager. This species is distributed from southern Brazil to northeastern Argentina and east of Paraguay and Uruguay. It is locally common in forest borders and woodlands, where it can be found in pairs or small groups, foraging at all vegetation

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levels on a mix of fruits, flowers, buds, and insects (Isler and Isler 1989, Ridgely and Tudor 1989). Here we describe for the first time, the presence of a cryptic dichromatism in adult Diademed Tanager plumage and document differences between breeding and nonbreeding plumages. METHODS DATA COLLECTION

This study was based on study skins deposited at the Museo Argentino de Ciencias Naturales ‘‘Bernardino Rivadavia’’. Only specimens in perfect condition (without evidence of degradation due to poor storage conditions or defects in preparation) and with complete information on sex, locality, and date of collection were included, totaling 33 adult individuals. Each specimen’s body was divided into seven regions: crown (excluding the small tuft of red feathers in the center), nape, back, rump, ‘‘blue’’ wing coverts (hereafter referred to as coverts), chest, and belly. These regions were chosen for two reasons: a) they appear homogeneously colored, and b) their size allowed us to take at least one reflectance measure. Dorsal regions were measured along the midline of the body; only once for crown and nape, twice for the rump (upper and lower), and three times for the back (upper, middle, and lower). Ventral measures were taken three times in breast and belly along their center and at both sides of the midline. Coverts of both wings were measured only once. REFLECTANCE SPECTROPHOTOMETRY

Plumage reflectance was measured using an Ocean Optics 2000 spectrophotometer with a PX-2 pulsed xenon light source (effective range of emission from 220 to 750 nm) calibrated against a white standard of barium sulphate following Osorio and Ham (2002). Before the measurement of each individual, a new calibration was done to correct for possible shifts in the performance of the equipment. Plumage was illuminated and reflected light collected at 458 to the surface and from the proximal end of the feather. This procedure was adopted to avoid the effect of specular reflectance that could result when the feather is illuminated and reflected light is collected perpendicular to its surface (Andersson 1996). The probe was mounted in a prismatic probe holder that was held (not

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pressed) over the selected region of the study skin. The diameter of the circular region illuminated and measured was 6 mm, and the distance between the probe and the plumage was 23 mm. The spectrophotometer resolution was 0.35 nm. Each spectrum was the average of three readings with an integer time of 100 msec. No boxcar smoothing was performed. Measurements were done blind to the sex, season, and year of capture of the specimens. STATISTICAL ANALYSES

In our analyses we included spectral data between 350 and 650 nm because wavelengths outside this range showed considerable noise. A principal components analysis (PCA) was performed on spectral data from each body region. Original variables were the reflectance values measured for each individual at intervals of 5 nm for the entire 350–650 nm range. If the same body region was measured more than once, individual means were calculated and employed in subsequent analyses. PCA reduces large sets of variables into a small number of mutually independent, orthogonal factors, a subset of which can account for most of the variation included in the original dataset. For such analyses, the first factor typically accounts for differences in brightness (total reflectance for the entire wavelength range), and additional factors relate to spectral shape and thus are measures of both hue (spectral location) and chroma (spectral purity; Endler 1990, Cuthill et al. 1999). We used factor scores from the first two PCA axes in separate two-way ANCOVAs with sex and season (breeding versus nonbreeding) as main factors, and included year of capture as a covariate to control for possible effects of plumage fading with age (Endler and The´ry 1996, McNaught and Owens 2002, Mahler and Kempenaers 2002, Hausmann et al. 2003). In addition, and because PCA factors capture variation in spectral shape but do not specifically describe hue and chroma, we quantified these latter variables and used them to perform ANCOVAs again to test for differences between sexes and seasons. Hue was calculated as the wavelength of maximum reflectance (l[Rmax]). Chroma was estimated as the reflectance of short wavelengths (between 350–450 nm) divided by total reflectance (R350–450 R350–65021). We centered our measurement of chroma at 400 nm because this is approximately the wavelength of maxi-

mum reflectance (see Results), and we hereafter call this the ‘‘short-wave chroma’’. Because of the importance of UV in visual perception in birds, we also calculated a ‘‘UV chroma’’ as the relative reflectance of UV wavelengths from 350 to 400 nm (R350–400 R350–65021). RESULTS The PCA produced two factors that accounted for more than 78% of the variation of the original dataset for all body regions. Factor 1 varied positively with brightness and factor 2 represented spectral shape (higher relative short-wave reflectance compared with long-wave reflectance). Two-way ANCOVAs performed on factor scores and spectral variables separately, using year of capture as a covariate (test of parallelism, Fs3,25 # 2.3, P . 0.1), showed significant effects of sex and season, but no interaction between them. Sexes differed in brightness of crown with males 40% brighter (Fs1,28 5 6.9, P 5 0.01, Table 1), and they differed in spectral shape of the nape, chest, and belly (Fs1,28 $ 4.5, P , 0.05, Table 1) with males having more short-wave reflectance and comparatively less long-wave reflectance than females in these regions (Fig. 1). However, the difference in spectral shape between sexes was not related to differences in hue (range 5 395–415 nm, Table 2), which did not differ between sexes (Fs1,28 # 2.3, P . 0.1, Table 2, Fig. 1). As shown in Figure 1, spectral shape differences between sexes were attributable to differences in chroma. In fact, shortwave chroma differed between sexes for almost all body regions with only the rump and coverts as exceptions (Fs1,28 $ 4.3, P , 0.05, Table 3). Because of the higher reflectance of male crowns across the spectrum, its short-wave chroma was significantly lower than that of females. In contrast, the nape, back, chest, and belly showed higher average short-wave chroma in males relative to females, not only because of the higher and steeper violet peak of reflectance but also because of the faster decrease in longwave reflectance. Consistent with the spectral location of hue, between 12% and 33% of the total reflected light across the spectrum was reflected in the near-UV band (350–400 nm). In addition, the proportion of UV reflectance differed between males and females in some body regions with UV chroma variation, in part, responsible for the spectral shape differences between sexes.


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TABLE 1. Results of the ANCOVAs (sex and season as main factors, year of capture as covariate) performed on the PCA factors of each body region. Factor 1 varies positively with brightness and factor 2 represents spectral shape (high values of this factor indicate higher relative short-wave reflectance compared with longwave reflectance). Sex

Season

Body region

Percent of variance explained by PC 1

Percent of variance explained by PC 2

F

P

F

P

F

P

F

P

Crown Nape Back Rump Coverts Chest Belly

83 55 62 75 62 70 58

2 27 19 6 20 11 21

6.9 0.1 1.9 0.0 2.0 0.0 0.5

0.01 0.82 0.18 0.98 0.17 0.85 0.47

1.4 7.7 4.0 0.8 0.1 4.5 8.9

0.25 0.01 0.05 0.38 0.79 0.04 0.01

5.2 0.0 0.8 0.5 0.6 2.7 1.9

0.03 0.98 0.37 0.50 0.43 0.11 0.18

0.0 4.1 1.0 9.6 0.2 11.3 2.0

0.98 0.05 0.33 0.01 0.64 0.01 0.17

PC 1

PC2

Specifically, the nape and back of males had higher average UV chroma than these same regions in females (Fs1,28 $ 4.8, P , 0.05, Table 4). Breeding and nonbreeding plumages differed in their crown brightness (F1,28 5 5.2, P 5 0.03) but, contrary to our expectations, nonbreeding birds were 25% brighter than breeding ones (Table 1 and Fig. 2). In addition, ANCOVAs performed on factor 2 indicated that the spectral shape of the rump, chest, and nape differed between seasons (Fs1,28 $ 4.1, P # 0.05). However, this result could not be explained by differences in short-wave or UV chroma (Fs1,28 # 3.9, P $ 0.05). Finally, there were no differences in hue between seasons (Fs1,28 # 1.8, P $ 0.2). DISCUSSION We showed that significant differences exist in plumage color between sexes and seasons in a species previously considered to be both sexually monochromatic and without differences between breeding and nonbreeding plumages (Ridgely and Tudor 1989, Isler and Isler 1999). These differences included variation in reflectance (male crowns brighter than female ones) and in spectral shape. Our analyses demonstrated that males have higher chroma values in several body regions but that chroma values for the white-blue crown of males are lower. These differences prove the existence of a cryptic dichromatism in the Diademed Tanager, and suggest that the presence of dichromatism in the tanagers might be even more prevalent than suggested by previous studies based on human vision (Burns 1998, Isler and Isler 1999).

PC1

PC2

A recent study showed differences in reflectance between sibling species belonging to the thraupine genus Anisognathus (Bleiweiss 2004a), while another reported differences between frugivorous and insectivorous species of tanagers (Bleiweiss 2004b). These studies, together with our study on the Diademed Tanager, show the potential of reflectance spectrophotometry to reveal unknown and unexpected phenomena in this diverse and colorful group of birds. Moreover, the existence of cryptic dichromatism and a previously unrecognized seasonal variation in plumage brightness in the Diademed Tanager demonstrates how important it is to understand intraspecific variation prior to pursuing studies at interspecific level, which generally compare many different species based on limited data for each (Bleiweiss 2004b). Noniridescent UV-blue reflectance is suggested to be a result of coherent scattering or constructive interference produced by the highly ordered structure of the spongy medullary keratin of feather barbs (Prum et al. 1998, Andersson 1999, Prum 1999). This model predicts that hue is determined by the size and spatial distribution of keratin rods and air vacuoles in the medullary layer (Prum et al. 1999, 2003). This prediction has been confirmed in several interspecific comparisons (Dyck 1971, 1976, Finger et al. 1992, Finger 1995), but not in intraspecific ones (Shawkey et al. 2003). There is also evidence indicating that the homogeneity in the diameter of circular keratin rods positively correlates with chroma and that the number of these structures positively correlates with UV chroma (Andersson 1999, Shawkey et al. 2003). In turn, features

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FIGURE 1. Reflectance spectra of the Diademed’s Tanager body regions according to sex. Each spectrum represents mean reflectance (6 SE) of males (n 5 19) and females (n 5 14) for each body region.

TABLE 2. Sex differences in hue (l[Rmax]; expressed in nm) of different body regions. Values are presented as means 6 SD. Statistics correspond to two-way ANCOVAs (sex and season as main factors, year of capture as covariate). Body region


Male (n 5 19)

416.05 402.63 397.37 406.84 412.89 403.42 408.42

6 6 6 6 6 6 6

10.61 12.06 12.84 7.68 11.34 10.15 12.48

Female (n 5 14)

df

F

P

6 6 6 6 6 6 6

1,28 1,28 1,28 1,28 1,28 1,28 1,28

0.4 0.4 1.8 2.1 0.1 0.8 2.3

0.55 0.55 0.19 0.16 0.80 0.38 0.14

414.29 404.29 401.79 403.57 413.21 405.71 413.93

9.78 7.56 13.53 6.91 11.03 8.52 9.84


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TABLE 3. Sex differences in chroma (R350–450 R350–65021) of different body regions. Values are presented as means 6 SD. Statistics correspond to two-way ANCOVAs (sex and season as main factors, year of capture as covariate). Body region


Male (n 5 19)

0.45 0.65 0.68 0.66 0.62 0.63 0.55

6 6 6 6 6 6 6

0.06 0.06 0.07 0.05 0.08 0.05 0.09

Female (n 5 14)

df

F

P

6 6 6 6 6 6 6

1,28 1,28 1,28 1,28 1,28 1,28 1,28

4.5 6.4 9.5 1.3 0.1 4.3 6.5

0.04 0.02 0.01 0.26 0.84 0.05 0.02

0.48 0.59 0.60 0.65 0.62 0.61 0.49

0.05 0.11 0.09 0.03 0.03 0.05 0.07

of the medullary layer in combination with other factors that are external to this matrix are believed to determine total reflection (Andersson 1999, Shawkey et al. 2003). Because Diademed Tanager males are brighter and have higher short-wave and UV chromas than females, we suggest that males should have a higher number of keratin bars and air vacuoles in the spongy medullary parts of their feathers and that these bars and vacuoles should be more homogeneous than in females. Male crowns should also have a higher number of reflecting units because they are brighter than those of females; however, their lower chroma does not necessarily imply more dissimilar reflecting units because their spectra are simply shifted upwards compared to that of females. We also found that the plumage brightness differed between breeding and nonbreeding seasons. Contrary to our expectations, nonbreeding birds were brighter than breeding ones. This finding may be explained by the observation that tanagers have only one annual molt after breeding (Snow and Snow 1964, Isler and Isler 1999). Thus, birds have the newest plumage during fall and winter and a worn plumage while breeding ¨ rnborg et (September to January). In contrast, O

al. (2002) found an increase in brightness of male Blue Tits (Parus caeruleus) throughout the breeding season. This was tentatively attributed to feather-wear that results in the exposure of more reflective surfaces (such as rachices and barbules) as the breeding season progresses. Although we do not have information about the annual patterns of change in microstructure in Diademed Tanager feathers, the mechanism proposed for Blue Tits cannot explain our result because we recorded a decrease rather than an in¨ rnborg et al. crease in reflectance. Moreover, O (2002) also found changes in chroma and UV chroma throughout the breeding season, but we did not see significant differences in hue, shortwave, or UV chroma between the breeding and nonbreeding seasons. Finally, it is important to ask what the ecological and behavioral consequences of such sexual and seasonal patterns of plumage differences might be. Given the importance of UV reflectance in mediating sexual preferences (Bennett et al. 1996, 1997, Andersson et al. 1998, Hunt et al. 1999, Johnsen et al. 1998, Pearn et al. 2001), we speculate that the cryptic dichromatism of the Diademed Tanager may function as a sexual selected character for mate

TABLE 4. Sex differences in UV chroma (R350–450 R350–65021) of different body regions. Values are presented as means 6 SD. Statistics correspond to two-way ANCOVAs (sex and season as main factors, year of capture as covariate). Body region


Male (n 5 19)

0.12 0.31 0.33 0.32 0.29 0.28 0.21

6 6 6 6 6 6 6

0.02 0.07 0.08 0.05 0.06 0.07 0.09

Female (n 5 14)

df

F

P

6 6 6 6 6 6 6

1,28 1,28 1,28 1,28 1,28 1,28 1,28

1.5 4.8 9.4 1.0 0.5 1.8 3.5

0.23 0.04 0.01 0.32 0.50 0.19 0.07

0.21 0.27 0.25 0.31 0.29 0.26 0.17

0.03 0.07 0.07 0.03 0.03 0.05 0.06

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FIGURE 2. Reflectance spectra of the Diademed’s Tanager body regions according to season. Each spectrum represents mean reflectance (6 SE) of birds captured in the summer (breeding season, n 5 14) and winter (nonbreeding season, n 5 19) for each body region.

choice. At first glance, this conclusion might seem counter to our finding that nonbreeding birds are brighter than breeding ones even for wavelengths in the UV spectrum. However, we do not know at what time of the year pairs are formed and it may indeed be the case that mate selection occurs prior to the breeding season. Alternatively, the patterns of plumage variation found in this study may be related to intrasexual functions such as male-male competition. A recent study in Blue Tits showed experimentally

that UV signals may play a role in male contests, with UV reduced models eliciting less aggression from nest defending males (Alonso-Alvarez et al. 2004). Because the Diademed Tanager is a common species that can be adapted to laboratory conditions and even bred in captivity, experimental tests to evaluate whether birds can detect the differences we have documented, and to examine the effects of plumage on sexual preferences or intrasexual interactions would be worth undertaking.


ACKNOWLEDGMENTS We thank B. Mahler for her comments and suggestions in the different stages of the study and two anonymous reviewers for their valuable comments on the manuscript. We also thank Gabriela Ibarguchi for bringing the spectrophotometer from Canada to Argentina, and R. Bleiweiss for providing a copy of one of his most recent papers. This work was supported by the Consejo Nacional de Investigaciones Cientı´ficas y Tećnicas, Argentina (PEI 6001 to PLT), and a Natural Sciences and Engineering Research Council of Canada Discovery Grant and a Canada Foundation for Innovation New Opportunities grant (SCL).

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