Ostrich 2006, 77(3&4): 164–169 Copyright © NISC Pty Ltd Printed in South Africa — All rights reserved OSTRICH EISSN 1727–947X

Carotenoid-based breast plumage colour, body condition and clutch size in red fodies (Foudia madagascariensis)

Laura K Estep1*, Matthew D Shawkey2 and Geoffrey E Hill Department of Biological Sciences, 331 Funchess Hall, Auburn University, Alabama 36849, USA 1 Current address: Department of Epidemiology and Public Health, Yale School of Medicine, 60 College Street, PO Box 208034, New Haven, CT 06520–8034, Connecticut, USA 2 Current address: Department of Environmental Science, Policy and Management, 137 Mulford Hall #3114, University of California, Berkeley, CA 94720-3114, USA * Corresponding author, e-mail: [email protected]

Carotenoid-based feather colouration is a classic example of a condition-dependent ornamental trait. In some of , red, orange and yellow feather colouration reflects male quality and advertises the carotenoid concentration of feathers. Such colouration is an important aspect of mate selection by females. The red (Foudia madagascariensis) is a highly sexually dimorphic species of the family , in which males exhibit extensive carotenoid-based plumage. We investigated asso- ciations between body condition, clutch size, first egg date and carotenoid-based red plumage colour of male red fodies. Breast plumage brightness was positively associated with male body condition, suggesting that this component of colour is condition-dependent. Brighter-red males did not breed earlier but were mated to females that laid larger clutches compared to females mated to duller-coloured males. These data suggest that red colour in red fodies has the potential to function as an honest signal of male quality.

Introduction

One explanation for the existence of ornamental traits in Paridae). It is primarily from these studies that the is that such traits evolved as reliable signals of indi- above generalities are drawn (e.g. Hill and Montgomerie vidual quality (Zahavi 1975, Kodric-Brown and Brown 1984, 1994, Thompson et al. 1997, Lindström and Lundström Grafen 1990). Carotenoid-based colour displays in the 2000, Hõrak et al. 2001, Tschirren et al. 2003). Studies of skins of fish and the feathers of birds have played a central carotenoid-based plumage colour in weaver finches (family role in testing honest-signalling theory (Andersson 1994, Ploceidae) show that carotenoid colouration can also serve Hill 2002). This theory relies upon the precept that orna- functions other than mate attraction. The carotenoid-based ments used in honest signalling must be costly to produce plumage ornaments of both Red-collared ( or maintain (Andersson 1994). Carotenoid-based orna- ardens) and Red-shouldered Widowbirds (Euplectes axillar- ments are likely to be honest signals of quality, because of ies) are important for signalling status and resource-holding the cost associated with the acquisition and utilisation of the potential. In Cardueline finches, the quality of colour display pigments needed for maximum colour display (reviewed in is condition-dependent and the object of sexual selection, Hill 2002, 2006a). but in weaver finches, it is generally the size of the orna- Numerous studies on fish and birds have shown that ment rather than colour quality that is condition-dependent carotenoid-based colouration can serve as an honest signal and functions in sexual signalling (Pryke et al. 2001, Pryke of quality (reviewed in Houde 1997, Hill 2002). In general, and Andersson 2003a, 2003b). In the Red-billed these studies have shown that males with access to more (Quelea quelea), another weaver finch, carotenoid-based pigment resources, who are in better nutritional condition, or plumage ornamentation is not condition-dependent and who have lower parasite loads during moult, grow feathers does not function in sexual signalling (Dale 2000), but or scales with more saturated or longer-wavelength coloura- rather appears to be important in individual recognition tion. Furthermore, many studies have shown that females (Dale et al. 2001). prefer to mate with males who have more saturated or In a model, Dale et al. (2001) proposed a number of redder ornaments (Houde 1997, Hill 2006b) and a few stud- features that distinguish plumage colour that functions in ies have shown that females mated to redder males experi- individual recognition from plumage colour that functions in ence material benefits in the form of greater paternal provi- sexual signalling (Dale 2006). For example, a bimodal sioning and higher reproductive success (Hill 1991, McGraw distribution of colour suggests that it functions in individual et al. 2001). recognition, while a unimodal distribution suggests that it Within birds, the vast majority of studies of carotenoid functions in sexual signalling. In contrast to the continuous colouration have been conducted on Cardueline finches distribution of colour in Cardueline finches, colour patches (family Fringillidae, sub-family Carduelinae) and tits (family in are distributed bimodally as discrete red and Ostrich 2006, 77(3&4): 164–169 165 orange morphs, suggesting that they function in individual the date of his first breeding attempt of the season. We recognition. By identifying the features of plumage colour in recorded the number of eggs or nestlings at each visit. On a species and interpreting them in terms of this model, we some breeding territories, we captured the male of the pair may thereby gain some understanding of its function. with mist-nets set up in the breeding territory at least 10m We applied the concepts of Dale et al.’s (2001) model to from the nest location. Males were highly territorial, chasing the plumage colour of red fodies (Foudia other males and singing from regularly-used perches (LK madagascariensis), a little-studied weaver finch. Red fodies Estep, pers. obs.); thus, we were certain that the captured are highly sexually dichromatic during breeding; females male was the social mate. Males captured on the territories are olive and drab brown, while males vary continuously were processed following the same procedure used for from bright red to drab yellow over their entire bodies, males captured on the rice paddy. Because of high depreda- excluding the tail and wings (Langrand 1990). This sexual tion rates and flooding of nests containing nestlings (57.1%), dichromatism suggests that bright plumage colours in this we used final clutch size as our measure of reproductive species may have evolved through sexual selection success (Badyaev et al. 2000, Doucet et al. 2004). (reviewed in Badyaev and Hill 2003). Furthermore, the low variation in patch size (Langrand 1990 — in contrast to that Colour analyses of widowbirds) and continuous unimodal distribution of We stacked and taped five feathers from each male to colour (this study, in contrast to that of queleas) suggests gloss-free black construction paper and recorded spectral that the colour could function as an honest signal of quality. data from them using an Ocean Optics S2000 Spectrometer The signal content of colour in this species is, to our knowl- (range of 250–880nm, Dunedin, FL, USA) and a UV edge, entirely unstudied. By examining associations (deuterium bulb) and visible (tungsten-halogen bulb) light between plumage colour and measures of male body source. We used a bifurcated fibre-optic measuring probe condition and reproductive success, we tested the hypothe- (Ocean Optics, Dunedin, FL, USA), which provided illumina- sis that the red colouration in this species could serve as a tion from the lamp and transferred light reflected from the signal of individual quality. feather sample back to the spectrometer. This probe was held at a 90° angle to the feather surface. Ambient light was Procedures excluded with a block sheath that held the tip at a fixed distance of 5mm from the feather surface, providing a read- Data collection ing area of 2mm. All reflectance data were generated rela- We studied red fodies from January–April 2004 on their tive to a white standard (WS-1, Ocean Optics, Dunedin, FL, breeding and foraging ground in Ranomafana National Park, USA). The probe was lifted and replaced, and a new meas- along the eastern escarpment of Madagascar. We centred urement taken, five times on each feather sample. Each of our study site on the rice paddy that is directly adjacent to these five measurements was an average of 20 sequential the village of Vohiparara, which is used by flocks of red spectra generated by 00Ibase software, a spectra acquisi- fodies for foraging (21°14’S, 47°23’E). tion software package (Ocean Optics, Dunedin, FL). We We captured males in mist-nets set up along the perime- then averaged these five measurements for each feather ters of rice paddies from 07:00 to 11:00 and from 14:00 to sample. 18:00. Upon capture, we banded males with unique combi- We calculated standard indices for three different nations of one numbered aluminum band (Band and Tag elements of colour from these reflectance spectra (Hailman Corporation) and three coloured plastic leg bands. We 1977, Norris et al. 2004). These indices were restricted to recorded standard morphological measurements (wing wavelengths between 300nm and 700nm, as evidence chord, tail length, tarsus length, bill length and mass) for all suggests that this is the range of sensitivity for the avian individuals. We pulled breast feathers from approximately visual system (Jacobs 1981, Cuthill et al. 2000). Red the same area on each male and stored them in envelopes chroma, or spectral purity in the red region, is the proportion for future colour analyses. We did not measure breast patch of light reflected in the range from 575–700nm, and UV size because the red colouration of all males used in this chroma is the proportion of light reflected in the range from study extended from under the bill to the tip of the undertail 300–400nm (Norris et al. 2004). Brightness is the summed coverts (Langrand 1990). reflectance from 300–700nm (Endler 1990). Repeatability of Data concerning the dates of the onset of breeding for this measurements from the same individual male was 0.67 for species in the Ranomafana region were not available prior brightness (F = 11.33, df = 81,328, p < .0001), 0.73 for UV to our study, and full details of our data on the basic breed- chroma (F = 14.95, df = 81,328, p < .0001) and 0.75 for red ing biology of this species will be published separately else- chroma (F = 15.95, df = 81,328, p < .0001) (Lessells and where. Briefly, we intensively searched for nests in the area Boag 1987). We chose these variables based on the shape surrounding the central rice paddy complex and checked of the reflectance curve (see Figure 1), which exhibited a nests every three days. We began our surveys for nests in peak in the UV and a long plateau at longer wavelengths. mid-December, but did not discover nests until mid-January, Furthermore, red chroma has been found to accurately indi- suggesting that this was the beginning of the breeding cate the amount of carotenoids present in feathers (Inouye season. Mated pairs were never observed utilising the same et al. 2001, Saks et al. 2003a). To determine whether colour nest for multiple clutches, suggesting that fodies change variables were unimodally or bimodally distributed, we visu- location with each new breeding attempt. Thus, we took the ally examined histograms of UV chroma, red chroma and date at which a male was first associated with a nest to be brightness for modality patterns. 166 Estep, Shawkey and Hill

20 50 15 40

30 10 20

FREQUENCY 5 10

300 400 500 600 700 10 11 12 13 14 15 16 17 18 1920 21 PERCENT REFLECTANCE (%) REFLECTANCE PERCENT WAVELENGTH (nm) BRIGHTNESS (%) 40 Figure 1: Representative spectrometric curve of red breast feath- ers of a male Madagascar 35 30 Verification of the presence of carotenoids 25 We used an acidified pyridine extraction method (McGraw 20 et al. 2005) to verify the presence of carotenoids in feath- 15 ers. The acidified pyridine was coloured bright red following FREQUENCY 10 incubation, and the feathers from which pigments were extracted were white. These results suggest that 5 carotenoids are primarily responsible for the red colour of this plumage (McGraw et al. 2005). <70 70 75 80 85 90 95 RED CHROMA (%)

Statistical analyses 16 We used linear regression to compare first egg date and 14 male body condition to the three measured colour variables. We used the residuals of mass on tarsus length as our 12 measure of body condition, as is common for studies of live 10 birds (for review, see Blem 1990, Brown 1996). Although this 8 approach to measuring body condition has attracted some 6 criticism (Green 2001), recent research suggests that such FREQUENCY 4 criticism may be unwarranted (Schulte-Hostedde et al. 2005). Both response variables of first egg data and male 2 body condition were normally distributed (n = 12, D = 0.224, p = 0.094 and n = 13, D = 0.068, p > 0.150, respectively, 0246810121416 UV CHROMA (%) Kolmogorov-Smirnov test). We used backwards elimination to remove variables, until arriving at a final model (alpha-to- drop = 0.05). Because the response variable of final clutch Figure 2: Histograms for the colour variables UV chroma, red size was not normally distributed (n = 13, D = 0.394, p < chroma and overall brightness for the red breast feathers of .010, Kolmogorov-Smirnov test), we used non-parametric Madagascar red fodies (n = 82) correlations with a Bonferroni correction to compare the number of eggs to the three colour variables. to body condition. The final linear regression model arrived Results at for male body condition included only feather brightness (Figure 3, linear regression, n = 82, r2 = .084, β = 0.290, F = We captured and processed 82 males in and around the 7.371, p = 0.008). UV chroma dropped out of the model at rice paddy. The reflectance spectra of the red feathers was the first step in the selection process (β = 6.19, t = 1.12, p = similar to that of the feathers of other species with 0.266), and red chroma dropped out in the second step (β = carotenoid-based red colouration (Eaton and Lanyon 2003), 2.57, t = 1.29, p = 0.201). with a small peak in the UV wavelengths and a long plateau As an indirect test of female mate preference and male in the red wavelengths (Figure 1). plumage colouration, we compared nest initiation date to Histograms indicated that all three colour variables were male colouration. We monitored the nests of 13 males for unimodally distributed (Figure 2). Bins for the histograms which we had plumage colour data. Data for exact nest initia- were evenly distributed across the range of values for each tion date were unavailable for one nest. Neither red nor UV variable (Figure 2). chroma nor brightness of breast feather colouration predicted To test the hypothesis that plumage colouration is related nest initiation date. Feather brightness was dropped from the to body condition, we compared saturation and brightness model first (β = 3.53, t = 0.54, p = 0.602), followed by UV Ostrich 2006, 77(3&4): 164–169 167

2.0 Spearman Rank Correlation N = 13 5 rs = 0.797 1.0 p = 0.001

4 0.0

–1.0 Linear regression 3 n = 82, r2 = 0.84 ß = 0.290

–2.0 F = 7.371, p = 0.008 CLUTCH SIZE FINAL

RESIDUALS OF MASS/TARSUS 2 10 12.5 15 17.5 20 22.5 25 MALE BREAST BRIGHTNESS (%) 13.75 15.00 16.25 17.50 MALE BREAST BRIGHTNESS (%) Figure 3: Scatterplot of male body condition (residuals of mass/tarsus) and male breast brightness for male red fodies Figure 4: Scatterplot of number of eggs for the first nest of the captured on the rice paddy and on breeding territories breeding season and the brightness of male breast colouration chroma (β = 1 739.48, t = 1.61, p = 0.141), then red chroma be needed to test this hypothesis. However, a recent exper- (β = 35.72, t = 0.39, p = 0.7013). However, there was a imental study demonstrated that carotenoid deposition, but significant positive relationship between male colouration and not white structural colour, was dependent on condition during final clutch size (Figure 4, Spearman rank correlation, N = 13, molt in American Goldfinches Carduelis tristis (Shawkey et rs = 0.797, p = 0.001) and this pattern remained significant al., in press). after Bonferroni correction (adjusted alpha = 0.017). Clutch Our examination of male plumage colouration in relation size was not correlated with UV chroma or red chroma to fitness measures produced mixed results. Brighter

(Spearman Rank Correlation, N = 13, rs = 0.491, p = 0.089; N males did not breed earlier than duller males, but females

= 13, rs = –0.343, p = 0.251, respectively). mated to males with brighter plumage colouration laid more eggs. Breeding early may not confer the same advan- Discussion tages to tropical species such as fodies as it does to temperate species (Stutchbury and Morton 2001), so nest Brightness of breast plumage colour was positively asso- initiation date may not be a relevant gauge of male success ciated with male body condition and clutch size, but not first in tropical environments. The larger clutch size in the nests egg date for male fodies. Only one other study (Saks et al. of brighter males suggests that females may produce larger 2003b) has shown a significant correlation between overall clutches when mated to brighter males or that brighter brightness of carotenoid-based ornamental colouration and males may be mated to higher-quality females, suggesting male quality. These first two patterns are thus not consistent that colour may function as a sexual signal in fodies in the with most studies of plumage colouration in Cardueline same manner as in Cardueline finches (Hill 2002). Alter- finches and members of the family Paridae, in which hue and natively, brighter males may acquire higher-quality terri- saturation tend to be correlated with male quality (reviewed in tories, and it is the resources held by a male rather than his Hill 2002). Hue and saturation reflect the composition and colouration per se that determines the number of eggs a concentration of carotenoid pigments, respectively (Inouye et female lays. It should be noted that this specific result al. 2001, Saks et al. 2003a), while brightness has no clear applies to the entire male fody population we studied, relationship to the carotenoid content of feathers (Saks et contingent upon the assumption that events such as flood- al. 2003b). Of the three colour variables, brightness is most ing and depredation that resulted in clutch loss were sto- likely to be affected by the underlying white structural colour chastic, with respect to male quality. Otherwise, our results as well as carotenoid content (Shawkey and Hill 2005). In apply specifically to the subset of the males who were less both experimental and field correlational studies, carotenoid likely to lose clutches during such events. pigmentation of feathers has been clearly shown to be The nature of fody plumage colour suggests that it condition-dependent (reviewed in Hill 2002, 2006a). The serves as an indicator of individual quality. Dale et al. hypothesis that structural colouration is condition-dependent (2001) propose that such indicators should be relatively is not as strongly supported (Prum 2006), but some studies less variable, condition-dependent, unimodally distributed, have shown a relationship between structural colour vari- positively correlated with fitness measures, and have posi- ables and condition (Doucet 2002, Doucet and Montgo- tively correlated component characters. While we cannot merie 2003, Hill et al. 2005). Thus, both deposition of address the final condition of the model, the remainder of carotenoids and formation of the underlying white structural the conditions fit the case of the fody well. Carotenoid tissue may be condition-dependent in fodies. Experimental colouration in fodies is largely restricted to a UV-red colour, tests of the effects of condition on these two processes will appears to be condition-dependent, is unimodally distrib- 168 Estep, Shawkey and Hill uted and is positively correlated with some, but not all, Series B: Biological Sciences 267: 2143–2149 fitness measures. By contrast, the colour of the quelea, Dale J 2006. Intraspecific variation in bird colors. In: Hill GE and which has been argued to function in individual recogni- McGraw KJ (eds) Bird Coloration, Vol. 2: Function and Evolution. tion, is highly variable and bimodally distributed into two pp 36–86. Harvard University Press, Cambridge discrete colour morphs, and is not correlated with fitness Dale J, Lank DB and Reeve HK 2001. Signaling individual identity versus quality: a model and case studies with ruffs, queleas, and measures. Thus, by the terms of this model, the red colour house finches. American Naturalist 158: 75–86 of the fody likely functions as an indicator of individual Doucet SM 2002. Structural plumage coloration, male body size, quality. Why the colour of the widowbirds does not clearly and condition in the Blue-black Grassquit. Condor 104: 30–38 fit either set of conditions is not clear, although it appears Doucet SM and Montgomerie R 2003. Multiple sexual ornaments that the size, rather than the colour, of the ornament may in Satin Bowerbirds: ultraviolet plumage and bowers signal differ- function as an indicator of quality (Pryke and Andersson ent aspects of male quality. Behavioral Ecology 14: 503–509 2003a, 2003b). Doucet SM, Mennill DJ, Montgomerie R, Boag PT and Ratcliffe LM 2004. Achromatic plumage reflectance predicts reproductive Conclusions success in male Black-capped Chickadees. Behavioral Ecology 16: 218–222 Eaton MD and Lanyon SM 2003. The ubiquity of avian ultraviolet We showed that red colour in fodies reflects body condition plumage reflectance. Proceedings of the Royal Society of and a measure of reproductive success and thus could London Series B: Biological Sciences 270: 1721–1726 potentially be used as a sexual signal. Whether red colour Endler JA 1990. On the measurement and classification of color in functions in female choice or male-male competition could studies of color patterns. Biological Journal of the not be determined in this study; however, the fit of this Linnean Society 41: 315–352 species’ plumage characteristics to the model in Dale et al. Grafen A 1990. Biological signals as handicaps. Journal of (2001) suggests that carotenoid colouration in fodies could Theoretical Biology 144: 517–546 function as an indicator of individual quality. Future studies Green AJ 2001. Mass/length residuals: measures of body condi- should explicitly examine whether females assess this tion or generators of spurious results? Ecology 82: 1473–1483 colour when making mate-choice decisions, or if males use Hailman JP 1977. Optical Signals: Animal Communication and Light. Indiana University Press, Bloomington, USA it in competition with one another. Hill GE 1991. Plumage coloration is a sexually-selected indicator of male quality. Nature 350: 337–339 Acknowledgements — We are grateful to Solohery Rasamison Hill GE 2002. A Red Bird in a Brown Bag: the Function and for field assistance and to MICET/ICTE Madagascar and Aristide Evolution of Ornamental Plumage Coloration in the House Finch. Andrianarimisa at the Peregrine Fund Madagascar for assis- Oxford University Press, New York tance in Madagascar. We thank ANGAP, the Ranomafana Hill GE 2006a. Environmental regulation of ornamental coloration. National Park Service, the Centre Valbio, and local officials in In: Hill GE and McGraw KJ (eds) Bird Coloration, Vol. 1: the village of Vohiparara for helping us with the logistics of Mechanisms and Measurements. pp 507–560. Harvard establishing our field site. Herman L Mays Jr and Lynn University Press, Cambridge Siefferman provided helpful comments and insight during revi- Hill GE 2006b. Female mate choice for ornamental coloration in sion of this manuscript. This study was done under the Auburn birds. In: Hill GE and McGraw KJ (eds) Bird Coloration, Vol. 2: University IACUC (Permit # PRN 2003-0615) and was financially Function and Evolution. pp 137–200. Harvard University Press, supported by an Alabama Space Grant Consortium Fellowship to Cambridge LKE and National Science Foundation grants (IBN 0235778 and Hill GE and Montgomerie R 1994. Plumage colour signals nutri- DEB 0077804) to GEH. tional condition in the House Finch. 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Received January 2006, accepted June 2006 Editor: WRJ Dean