Colorful Tropical Birds are More Colorful at Higher Elevations: A Role
for Predation?
Laura Natalia Céspedes Arias
Advisors:
Oscar Laverde Rodríguez Daniel Cadena Ordoñez
Universidad de los Andes Departamento de Ciencias Biológicas
2014
TABLE OF CONTENTS
1.
Introduction……… 3
2.
Methods……… 5
Species and Study Sites Reflectance Measurements Colorimetric Data Analysis Phylogenetic Comparative methods
3.
Results……… 9
Plumage patterns: color volume, color span and hue disparity Contrast with the background
4.
Discussion……… 11
5.
Acknowledgments………. 15
6.
References………. 16
7.
Tables………. 21
8.
Figures……… 23
9.
Supplementary Information………. 29
Introduction
The evolution of communication signals in animals is thought to be shaped by the interaction of natural and sexual selection (Ryan et al, 1982; Endler, 1984; Stuart-‐Fox & Ord, 2004), especially in the case of bird coloration (Olsen et al, 2009). On one hand, natural selection via predation selects for dull or cryptic colors because conspicuous coloration increases the risk of being detected by predators (Slagsvold et al, 1995; Götmark , & Hohlfält , 1995; Stuart -‐Fox, 2003; Godin & McDonough , 2000; Ruiz-‐
Rodríguez et al, 2013). On the other hand, sexual selection often promotes the evolution of conspicuous and colorful patterns, especially in males (Lande, 1980; Hill, 1990).
Elevational gradients may offer ideal natural experiments for examining the interaction between natural and sexual selection in signal evolution. Predation rates on avian nests in tropical mountains decline with elevation (Boyle, 2008; Jankowski et al, 2013; Londoño, 2011). The diversity and abundance of diurnal raptors that prey upon small adult birds also decline with elevation (Thiollay, 1996) and because predator diversity correlates with the number of potential predators of a particular species (Valcu et al, 2014), predation pressure on adults likely decreases with elevation as well. However, studies of variation in avian coloration along elevational gradients have focused mainly on sexual dichromatism (Badyaev, 1997) and intraspecific variation (Rising et al, 2009), with no special attention to the effect of the variation in predation pressure.
Tanagers (Thraupidae) are a highly diverse Neotropical family of passerine birds that occupies a broad elevational range; species in this family display a wide range of plumage colors and patterns, foraging behaviors and vocalizations (Burns et al, 2014). Although some studies have examined color evolution in tanagers with a focus on sexual
dimorphism and on the effect of light environment on plumage coloration (Burns & Shultz, 2012; Shultz & Burns, 2013), there are no previous studies on how varying levels of
predation pressure along elevation gradients may have shaped interspecific variation in coloration in the Thraupidae. Understanding the evolution of plumage patterns in one of the most diverse and colorful families of the Neotropics would allow for considerable progress in teasing apart the relative influence of natural and sexual selection in the evolution of visual signaling.
In this study I explored whether interspecific differences in plumage conspicuousness and color heterogeneity among 48 Thraupidae species vary with elevation and can be
attributable to changes in predation pressure along an elevational gradient focusing on three localities at different elevations in the Colombian Andes. Specifically, I studied how color heterogeneity within the color pattern (colorfulness) and the contrast with the background (conspicuousness) vary with elevation gradient in both males and females. The hypothesis that plumage coloration evolves in response to predation risk allows one to make predictions about variation in colorfulness and conspicuousness in relation to elevation, assuming predation pressure on diurnal birds is stronger in the lowlands than in the highlands. First, I predict a positive relation between elevation and both colorfulness and conspicuousness: relaxed natural selection associated with predation would allow for greater elaboration in visual signals. I also predict different patterns of variation in females and males due to the different selective pressures that members of each sex likely
experience (Burns, 1998, Martin & Badyaev, 1996). In most Thraupidae, females -‐but not males-‐ play a predominant role in parental care during nesting (Isler & Isler, 1978); thus, natural selection against conspicuous patterns is likely stronger on females than in males. Additionally, male coloration is also under the action sexual selection, which likely favors colorful and conspicuous patterns. For these reasons, I expect that the relationship
between elevation and colorfulness and conspicuousness to be stronger in females than in males.
Methods
Species and Study sites
I studied coloration in 48 tanager species present in three sites at different elevations in Colombia (Table 1) to investigate the relationship between elevation and coloration.The high-‐elevation study site (2600-‐2900 m) was Reserva Forestal La Bolsa, an Andean cloud forest located in Junin (Cundinamarca) in the Colombian Cordillera Oriental. The mid-‐ elevation study site (1200 m) was an Andean montane forest named La Almenara in Santa María (Boyacá), located in the eastern slope of the Cordillera Oriental. Remedios
(Antioquia) was the low elevation site at 500 m. This site is located in the Magdalena River Valley, and consists on fragmented humid forest with patches of secondary growth in a pasture matrix. Tanager species composition at each locality was described based on previously existing lists and field observations. I gathered information on the elevational distribution and habitat use of each species from the literature (Hilty & Brown 1986, Stotz
et al, 1996), and augmented it with personal observations at the study sites (Table 1). For
the purposes of quantifying plumage contrast with respect to the environmental background (Gómez & Thery 2008, see below), I classified species in three categories of habitat use and foraging strata: open areas (O), canopy (C), and understory (U), as in a previous study of coloration in Thraupidae (Shultz & Burns, 2013).
Reflectance Measurements
Museum specimens
I quantified tanager plumage coloration using reflectance spectrophotometry. For each species, I measured coloration on four female and four males specimens with no apparent damage at the Instituto de Ciencias Naturales (ICN) and Museo de Historia Natural de la Universidad de los Andes (ANDES), Colombia. I only measured specimens collected after 1935 (Supplementary Table 2) to minimize effects of color degradation (McNet &
Marchetti, 2005; Armenta et al, 2008; Doucet & Hill, 2009). Almost all specimens were collected in Colombia and correspond to the subspecies found at my study sites
montana, Conirostrum albifrons and Hemispingus melanotis were collected in Peru and Bolivia, and were measured at the Louisiana State University Museum of Natural Science (LSUMZ).
On each specimen I measured five body parts: crown, rump, back, throat and belly. I also measured color patches additional to those mentioned above having a different
coloration to the human eye (as in Stoddard & Prum, 2008), but these measurements were not included in all of the analyses. Each color patch was measured twice and measures were averaged. Reflectance measurements were taken using an Ocean Optics USB4000 Spectrometer and a DH-‐2000 deuterium halogen light source coupled with an optic fiber QP400-‐2-‐UV-‐VIS with a 400 um diameter. Light was reflected on the surfaces with a standardized angle. The spectrometer was calibrated using a white standard before measuring each specimen.
Background Color
Characterizing the background habitat where birds live is necessary to determine the conspicuousness of color patterns (Gomez & Théry, 2007). To characterize the background colors at each locality, I collected samples of green leaves (from the understory and
canopy), tree trunks, and leaf litter along 100-‐m linear transects (Gomez & Thery 2007). I also collected leaves along a 100-‐m transect in a shrubby open area in the low-‐elevation site because this was the only locality with species occupying this habitat type (e.g.,
Sporophila minuta, Volatinia jacarina). At each site, I collected 40 samples of leaves from
the canopy, 40 samples of leaves from the understory, and 50 samples of litter and tree bark. I measured the reflectance spectra of these materials using the same equipment and protocol used to measure museum skins. Each element was measured twice and then these measurements were averaged. I averaged all the canopy leaves to obtain a mean canopy background reflectance spectrum (as in Gomez & Thery, 2007). To obtain the mean background spectrum for the understory I averaged all the leaves and the litter
separately for each locality, and then I contrasted bird color patches with both leaves and litter (see below).
Plumage patterns: color volume, color span and hue disparity
I calculated variables describing overall plumage coloration for each species using the Tetrahedral Color Space Model (Endler & Mielke, 2005; Stoddard & Prum, 2008). This model incorporates information on sensitivity spectra of cones and irradiance spectra (i.e luminance conditions) to transform the reflectance spectra of plumage patches into points located in a tetrahedral color space where each corner represents the maximum
stimulation for each of the four cone types existing in the retina of birds (Endler & Mielke 2005). I made all the calculations using generalized models of cone sensitivity spectra corresponding to the UV-‐sensitive (UVS) and V-‐sensitive (VS) types to account for the two main types of color vision in diurnal birds (Ödeen & Håstad, 2013). The UVS vision is characteristic of most passerine birds and Psittaciformes (Hastad et al, 2005) while the VS vision type is characteristic of other birds such as raptors (i.e., important avian predators) and the passerine clade Corvida (Hastad et al, 2005).
Color volume is the space encompassed by all points corresponding to the reflectance spectra of the five color patches measured. I obtained the color volume for each sex and species as implemented in the package pavo (Maia et al, 2013) for R (R Core Team, 2013). I also obtained values of mean color span, defined as the mean distance between pairs of points within the TCS, which provides a general idea of overall color dissimilarity within a plumage pattern (Stoddard & Prum, 2008). Additionally, I calculated hue disparity, which is the magnitude of the angle between two color vectors within the TCS (Stoddard & Prum, 2008). This is a measure of differentiation within a color pattern, which is independent of saturation. Color volume, mean color span and hue disparity can all be interpreted as estimates of color heterogeneity (Galván et al., 2013).
In addition to describing color diversity, I sought to estimate the conspicuousness of plumage patterns by measuring the contrast of color patches against species-‐ and site-‐ specific background color based on information from habitat and locality. I used the Receptor Noise model (Vorobyeb, 1998) to quantify chromatic (dS) contrast between plumage patches (crown, back, etc.) and the background, and then I averaged the dS values to obtain a single value describing the chromatic contrast of a given specimen with respect to the habitat occupied. Chromatic contrast is given in terms of Just-‐Noticeable-‐ Differences (JNDs). A value of one JND means that, even taking into account the receptor noise, two colors are distinguishable by the receptor, so it is positively correlated with the degree of differentiation between such colors. This is an intuitive measure of contrast that has been used in other studies as an approximation to conspicuousness (Stuart-‐Fox et al, 2004; Stobbe & Shaefer, 2008). In this analysis I excluded species found in more than one locality.
Phylogenetic Comparative methods
To examine whether color heterogeneity and conspicuousness (mean contrast with the background) vary with elevation I employed two approaches. First, I correlated the colorimetric variables with the midpoint of the elevational distribution of each species obtained from the literature (Hilty & Brown, 1986). Second, I tested for the relationship between elevational distribution and colorimetric variables, treating my three study sites categorically (low, intermediate, high elevation).
To account for the non-‐independence of species I used phylogenetic independent contrasts (Felsestein, 1985; Pagel, 1992) to obtain corrected p-‐ and R-‐values for linear regressions using the package Ape for R (Paradis et al., 2004). I also used phylogenetic generalized least-‐squares (PGLS) to examine relationships between elevational
in variables related to color pattern and contrast with the background among localities, I used PGLS with the locality as a factor. This approach is comparable to a generalized phylogenetic ANOVA for data not meeting assumptions for parametric tests, which assumes residuals evolve under Brownian motion (L. Revell, pers. com). In this analysis, I excluded species found in more than one locality to avoid lack of independence between localities (e.g. Thraupis episcopus, Thraupis palmarum, Sicalis flaveola). As a basis for phylogenetic analyses I used a comprehensive molecular phylogeny of the family based on sequences of multiple loci (Burns et al., 2014).
Results
Plumage patterns: color volume, color span and hue disparity
Color volume, mean color span and hue disparity were strongly correlated in both males and females (Fig. 1). Thus, for further analyses I only considered hue disparity, which is an intuitive measure of chromatic diversity.
Despite the high variation in plumage patterns (Fig. 2) existing even within localities, I found that the color heterogeneity of female plumage increases with elevation. As
predicted, the mean hue disparity of females was positively related to the midpoint of the elevation range of species (Fig. 3) after phylogenetic correction using independent
contrasts (p=0.00636 and R=0.1352 for UVS; p=0.00239 and R=0.169 for VS) and PGLS (p=0.0285 for UVS and p=0.013 for VS). The highest values of mean hue disparity were observed in species occurring at high-‐elevation sites: Iridosornis rufivertex and
Anisognathus igniventris (Fig. 2).
However, in the categorical analysis comparing my three localities, there were no significant differences in mean hue disparity in female plumage (Fig. 4; p>0.05 for both color-‐vision types). It is notable, however, that the variance in mean hue disparity was
higher in the mid and high-‐elevation localities relative to the lowland site (Fig. 4). At higher elevations species may exhibit either high or low values of hue disparity, but at low elevations there is less variation among species, with most tending to show low hue disparity (Fig. 4). For males, I did not find a significant relationship between mean hue disparity and the midpoint of the elevation range of species using independent contrasts (Fig. 3; p=0.4773 for UVS, p=0.384 for VS). There were no significant differences in mean hue disparity among localities for males (Fig. 4; p>0.05 for both color-‐vision types)
Conspicuousness
As predicted by the hypothesis that differential predation pressure along elevational gradients has shaped interspecific patterns of variation in coloration, I found that mean chromatic contrast (dS) between body patches and background (i.e. conspicuousness) shows a positive relationship with elevation in females (Fig. 5). This pattern was consistent under both visual types when phylogeny was controlled for using independent contrasts (p < 0.0001, and R = 0.5316 for UVS; p < 0.0001and R = 0.3664 for VS). In males, I found a significant relationship only using values of mean chromatic contrast calculated with the UVS vision type model (Fig. 5, p=0.03), but the relationship was weak (R=0.09). For both males and females, results using independent contrasts were consistent with those obtained using PGLS (for females both p<0.001; for males p=0.0282 for UVS and p=0.4043 for VS).
Differences in mean chromatic contrast with the background between localities at different elevations in mean chromatic contrast were significant for females under both UVS (p<0.001) and VS (p=0.0015) types of color vision (Fig. 6). In males, significant
differences exist only for mean chromatic contrast calculated under the UVS visual model (p=0.0109). It is notable that only in the low-‐elevation locality was mean chromatic contrast markedly different between sexes, with males having higher values of chromatic contrast with the background (Fig. 6). Differences in mean chromatic contrast between
females and males in this locality were significant for both generalized visual-‐types according to Mann-‐Whitney U Tests (p=0.0014 for UVS, p= 0.0016 for V).
Discussion
I evaluated whether interspecific variation in coloration in 48 species of tanagers is explained by the elevational distributional of species, possibly as a result of varying levels of predation pressure along an elevational gradient. My results generally support this hypothesis because I found that mean hue disparity (i.e., color heterogeneity or
colorfulness) and mean chromatic contrast with the background (i.e., conspicuousness) are positively related to the midpoint of the elevational range of species, at least for females. At higher elevations, where predation pressure is generally lower, species of tanagers tend to exhibit more colorful and conspicuous plumages. Mean hue disparity did not differ significantly among localities at three different elevations, but there was a trend indicating greater disparity at the high-‐elevation site. In any case, considering the
relatively low values of corrected R-‐values in linear regressions, the relationship between color heterogeneity and elevation in females does not appear to be strong.
Although my results fit predictions of the hypothesis that plumage coloration has evolved in response to varying predation pressures with elevation, the observed pattern may also reflect the influence of the light environment (Marchetti, 1993; McNaught & Owens, 2002; Gomez & Thery, 2004). At the low-‐elevation site, a considerable proportion of species (6 of 19) inhabit open areas, where uniform color patterns tend to be more
common (Shultz & Burns, 2013). In contrast, at the high elevation site, none of the species studied inhabits open areas. Thus, more work is necessary to understand the role of predation vs. light environments in driving the evolution of greater hue disparity at higher elevations.
Mean contrast with the background (i.e. conspicuousness) showed a strong relationship with elevation in females, and a weaker (or non existent) relationship in males. The results for females are consistent with my predictions and provide evidence for the idea that interspecific variation in conspicuousness may be shaped by differential predation
pressures along elevational gradients. Background matching (Cuthill et al, 2005; Gomez & Thery, 2007), which is likely negatively correlated to mean chromatic contrast, appears to be higher in females of species of the lowlands, were nest predation rates are higher (Boyle, 2008; Jankowski et al, 2013; Londoño, 2011) and so is the diversity of diurnal raptors (Thiollay, 1996). In contrast, at higher elevations, were natural selection via predation pressure is likely relaxed, conspicuous color patterns are more common in females.
The positive relationship between overall chromatic contrast and elevation requires deeper exploration. Future research should focus on quantifying plumage
conspicuousness more precisely by incorporating data on the irradiance spectra of different light environments at study sites (see Uy & Endler, 2004; Gomez & Thery, 2007) and on the spectral sensitivities of the usual predators of small birds, such as raptors (Trail, 1987) and reptiles (Londoño, 2011). Also, more research on elevational variation in predation pressure in adults is required (Badyaev, 1997) to fully understand the influence of predation pressure on variation in coloration along elevation gradients.
As expected given the relative sex roles of tanagers, my data suggest important
differences in patterns of variation between sexes. As in many other passerines, female tanagers provide greater parental care than males at the nest (Isler & Isler, 1987). Thus, it is likely that predation pressure, at least on nests, may have a stronger effect on the evolution of coloration in females (i.e., favoring cryptic plumage where predation pressure is high; see also Martin & Badyaev 1996). This is especially clear given the significant differences between mean chromatic contrast with the background between females and males occurring at the low-‐elevation site. In spite of the variation in coloration patterns in
this locality, males consistently exhibit higher values of mean chromatic contrast with the background than females.
Another plausible, but not exclusive, explanation for the weaker or inexistent relationship between mean chromatic contrast with the background and elevational distribution in males is related to sexual selection. It is possible that even in sites with high predation pressure, such as the lowlands, sexual selection still favors conspicuous patterns in males (Lande, 1980; Hill, 1990). Thus, even if natural selection favoring cryptic plumage is stronger in the lowlands, sexual selection may be overriding this effect.
Differentiation in color patterns –hue disparity and mean chromatic contrast– between sexes appears to vary with elevation (Fig. 4, Fig. 6, Supplementary Figure 3). At higher elevations females and males tends to be more similar in both variables. This is consistent with a relationship between sexual dichromatism and elevation reported for other groups of birds, such as Cardueline finches (Badyaev, 1997), which was attributed to stronger sexual selection at lower elevations. The fact that sexual dichromatism decreases with elevation and that mainly female plumage traits appear to vary with elevation supports previous ideas regarding the role of changes in female plumage in the evolution of dichromatism. Burns (1998) proposed that the frequent evolutionary changes in traits of female plumage in Thraupidae, which has also been reported for other bird groups (Price
et al, 2014), might have been the result of natural selection via predation pressure.
Therefore, evolutionary changes in sexual dichromatism within Thraupidae may have been driven by changes in female plumage coloration related to natural selection, rather than by changes in male plumage due to sexual selection (Wallace, 1889; Skutch, 1957). Patterns consistent with this idea have been found for other organisms such as Papilio butterflies (Kunte, 2008), dragon lizards (Ord & Stuart-‐Fox, 2006) and fairy-‐wrens (Johnson et al, 2013).
In conclusion, the evolution of coloration patterns in Thraupidae, as suggested by my findings for a set of species occurring at three sites in Colombia, likely reflects that visual communication signals are shaped by the interaction between natural and sexual
selection. The interspecific patterns of variation in mean hue disparity and especially so in mean chromatic contrast with the background suggest that contrasting selective pressures along elevational gradients have likely shaped elements of plumage coloration. On one hand, it is likely that different levels of predation pressure along elevational gradients have shaped the evolution of coloration, especially in females. On the other hand, sexual selection may have acted opposite to natural selection, promoting the evolution of colorful and conspicuous patterns in males even at sites with high predation pressure. Future studies should explore whether differences in coloration across all of the
Thraupidae are related to spatial variation in predation pressure (e.g., variation in relation to latitude; see Badyaev & Hill, 2003; Valcu et al, 2014). This would allow for a more comprehensive assessment of why are colorful tropical birds are more colorful in some areas (e.g., higher elevations), disentangling the role of predation and other factors such as the light environment.
Acknowledgements
I am grateful to my advisors, Oscar Laverde and Daniel Cadena for their invaluable support and guidance during the development of this project. I am also grateful to Oscar Ramos for his advice on the use of the spectrophotometer and data analysis, and to Iván Beltrán for his help with equipment-‐related logistics. I thank the Instituto de Ciencias Naturales (ICN) and Museo ANDES for allowing me to study their specimens. I am especially grateful to Angela Delgado, Edna Beltrán, Andrea Borbón and Ángela Matiz for their assistance in the field. I thank Natalia Gutiérrez and Elkin Tenorio for their helping in the construction of graphs. Kevin Burns provided the phylogeny of Thraupidae and Rafael Maia the script to calculate hue disparity. I am deeply thankful to all the members of the Laboratorio de Biología Evolutiva de Vertebrados (EVOLVERT) for their enormous support and valuable comments during the development of this project, especially Simón, David, Valentina and Paulo. Finally, I want to thank my parents, brothers and friends for their companionship and support.
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Table 1. Information of the 48 species of tanagers included in analyses of variation in coloration with elevation. Locality, maximum, minimum and midpoint of the elevational range, and habitat category are given for each species. Asterisks indicate cases which habitat category was modified from Stotz et al. (1996) based on personal observations.
Especie Locality Max Min Midpoint Category Habitat
Anisognathus igniventris La Bolsa 2400 3400 2900 C*
Buthraupis montana La Bolsa 2200 3300 2750 C
Chlorophanes spiza La Almenara 0 2300 1150 C
Chlorornis riefferii La Bolsa 1700 3300 2500 C
Cnemoscopus rubrirostris La Bolsa 2000 3300 2650 C
Coereba flaveola Remedios & La Almenara 0 2000 1000 O
Conirostrum albifrons La Bolsa 1800 3000 2400 C
Conirostrum rufum La Bolsa 2650 3300 2975 C*
Conirostrum sitticolor La Bolsa 2600 3700 3150 C
Cyanerpes caeruleus Remedios & La Almenara 0 1400 700 C
Cyanerpes cyaneus Remedios 0 1100 550 C
Dacnis cayana Remedios 0 1000 500 C
Diglossa albilatera La Bolsa 1600 3100 2350 U*
Diglossa caerulescens La Almenara & La Bolsa 1700 3100 2400 C
Diglossa cyanea La Bolsa 1800 3600 2700 C
Diglossa humeralis La Bolsa 2200 3400 2800 C*
Diglossa lafresnayii La Bolsa 2000 3700 2850 C*
Dubusia taeniata La Bolsa 2400 3600 3000 C*
Eucometis penicillata Remedios 0 1700 850 U*
Hemispingus atropileus La Bolsa 1800 3600 2700 U*
Hemispingus melanotis La Bolsa 1700 2900 2300 U
Hemispingus superciliaris La Bolsa 2100 3300 2700 C
Hemispingus verticalis La Bolsa 3000 3600 3300 C
Iridosornis rufivertex La Bolsa 2300 3800 3050 C*
Pipraeidea melanonota La Bolsa 0 1600 800 C*
Ramphocelus dimidiatus Remedios 0 1000 500 U*
Saltator maximus Remedios & La Almenara 0 1600 800 C*
Sericossypha albocristata La Bolsa 1400 3000 2200 C
Sicalis flaveola Remedios 0 1500 750 O
Sporohila funerea Remedios 0 1700 850 O
Sporophila crassirostris Remedios 0 1000 500 O
Sporophila minuta Remedios 0 1000 500 O
Sporophila nigricollis Remedios 0 2300 1150 O
Tachyphonus delatrii Remedios 0 1500 750 U*
Tachyphonus luctuosus La Almenara 0 2200 1100 C*
Tangara cyanicollis La Almenara 900 2400 1650 C
Tangara guttata La Almenara 1000 1800 1400 C
Tangara gyrola La Almenara 0 2100 1050 C
Tangara inornata Remedios 0 1200 600 C
Tangara larvata Remedios 0 1800 900 C
Tangara nigroviridis La Almenara & La Bolsa 900 3000 1950 C
Tangara vassorii La Bolsa 1900 3400 2650 C
Tersina viridis Remedios 50 1600 825 C
Thraupis cyanocephala La Bolsa 1400 3000 2200 C
Thraupis episcopus Remedios & La Almenara 0 2600 1300 C
Thraupis palmarum Remedios & La Almenara 0 2100 1050 C
Volatinia jacarina Remedios 0 2200 1100 O
Fig. 1: Strong correlation between variables describing color heterogeneity. Plots show raw values, but Spearman's r are all significant even using phylogenetic independent contrasts (all p>0.05). Dots are colored by visual model: light gray for VS-‐type and dark gray for UVS-‐type.
0.00 0.05 0.10 0.15 0.20 0.25 0.30
0.0
0.5
1.0
1.5
Females
Mean color span
Me an H ue D isp ari ty
0.00 0.05 0.10 0.15 0.20 0.25 0.30
0.0
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Males
Mean color span
Me an H ue D isp ari ty
0.05 0.10 0.15 0.20 0.25
0e +0 0 2e -0 4 4e -0 4 6e -0 4
Mean color span
C ol or Vo lu me
0.00 0.05 0.10 0.15 0.20 0.25 0.30
0e +0 0 4e -0 4 8e -0 4
Mean color span
C ol or Vo lu me
Fig. 2: Examples of the wide diversity of coloration patterns existing among species of Thraupidae included in the analyses. Species in the left column show high values for color volume, mean color span and mean hue disparity: Iridosornis rufivertex, Anisognathus
igniventris and Tangara cyanicollis. Species in the right show low values for these
variables: female Sporophila angolensis, Diglossa caerulescens and female Sporophila
funerea. (Photos by David Ocampo and Natalia Gutiérrez).
Fig. 3: Positive relationship between midpoint of the elevation range of tanager species and their plumage hue disparity for females but not males. For females, the corrected R values are significant (p<0.05) for both the VS (0.169) and UVS vision types (0.1352). Corrected R values for males are not significant (p>0.05). Dots are colored by visual model: light gray for VS-‐type and dark gray for UV-‐type.
500 1000 1500 2000 2500 3000
0.0 0.5 1.0 1.5 2.0 Females
Midpoint of the elevation range
Me an H ue D isp ari ty
500 1000 1500 2000 2500 3000
0.0
0.5
1.0
1.5
2.0
500 1000 1500 2000 2500 3000
0.0 0.5 1.0 1.5 2.0 Males
Midpoint of the elevation range 500 1000 1500 2000 2500 3000
0.0
0.5
1.0
1.5
Fig. 4: Boxplots showing there are no differences among localities in mean hue disparity, (using PGLS, all p> 0.05) in individuals of either sex and regardless of whether hue disparity is calculated UV (left) or V (right) vision-‐type models. Localities are ordered by elevation from low to high. Females are indicated by light green and males by dark green. Despite lack of significance, note there is a trend for greater hue disparity at higher elevations. Also, interspecific variation in hue disparity is greater at higher elevations
Fig. 5: Positive relationship between midpoint of the elevation range of tanager species and their mean chromatic contrast with the background (i.e conspicousness). For females, corrected R values are significant (p<0.05) for both VS (0.36) and and UV (0.53) type. For males, R is only significant for the UV model values (p=0.03) but with a low R value (0.09). Dots are colored by visual model: light gray for VS-‐type and dark gray for UV-‐type.
500 1000 1500 2000 2500 3000
5 10 15 20 25 30 Females
Midpoint of the elevation range
Me an C hro ma tic C on tra st (d S)
500 1000 1500 2000 2500 3000
5 10 15 20 25 30
500 1000 1500 2000 2500 3000
5 10 15 20 25 30 Males
Midpoint of the elevation range 500 1000 1500 2000 2500 3000
5 10 15 20 25 30
Fig 6. Tanager species are more conspicuous at higher elevations. Chromatic contrast with the background (i.e conspicousness) is significantly different among localities for females (p<0.0001 for UVS; p=0.0015 for VS). In males, differences among localities are significant only under the UV visual model (p=0.0109). Localities are ordered by elevation from low to high. Females are indicated by light green and males by dark green.
0
5
10
15
20
25
30
35
Remedios La Almenara La Bolsa UV
Locality
Mean chromatic contrast (JNDs)
0
5
10
15
20
25
30
35
Remedios La Almenara La Bolsa V
Locality
Supplementary Information
Supplementary Figure 1: Phylogenetic tree showing relationships among study species. Nomenclature follows Burns et al (2014), but in the text I adopt recent changes by the South American Classification Committee (e.g., Oryzoborus is now considered part of Sporophila; Remsen et al, 2014).
Anisognathus igniventris Buthraupis montana Chlorornis riefferii Chlorophanes spiza Cnemoscopus rubrirostris Coereba flaveola Conirostrum albifrons Conirostrum rufum Conirostrum sitticolor Cyanerpes caeruleus Cyanerpes cyaneus Dacnis cayana Diglossa albilatera Diglossa caerulescens Diglossa cyanea Diglossa humeralis Diglossa lafresnayii Dubusia taeniata Eucometis penicillata Hemispingus atropileus Hemispingus melanotis Hemispingus superciliaris Hemispingus verticalis Iridosornis rufivertex Oryzoborus angolensis Oryzoborus crassirostris Oryzoborus funereus Pipraeidea melanonota Ramphocelus dimidiatus Saltator maximus Sericossypha albocristata Sicalis flaveola Sporophila minuta Sporophila nigricollis Tachyphonus delatrii Tachyphonus luctuosus Tangara cyanicollis Tangara guttata Tangara gyrola Tangara inornata Tangara larvata Tangara nigroviridis Tangara vassorii Tersina viridis Thraupis cyanocephala Thraupis episcopus Thraupis palmarum Volatinia jacarina 1 0.33 0.67 0.65 0.77 0.98 1 1 1 0.85 1 0.37 1 0.74 0.51 1 0.82 0.22 1 0.39 0.97 0.98 1 0.87 1 1 1 1 0.74 1 0.79 1 0.99 1 1 0.99 1 1 0.95 1 1 1 1 1 1 0.43 0.14
Supplementary Figure 2: High overlap in color spaces among species occurring at our study sites. Dots are colored according to locality: gray (La Bolsa), blue (La Almenara) and red (Remedios).
Supplementary Figure 3: Negative relationship between the degree of sexual
dichromatism and midpoint of the elevational distribution of the study species. Values of sexual dichromatism are taken from Burns & Shultz (2008). These values correspond to the maximum value of chromatic contrast (dS) between a body patch of females and males.
500 1000 1500 2000 2500 3000
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14
Midpoint of the elevation range
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