Food Color Preferences of Molting House Finches (Carpodacus mexicanus) in Relation to Sex and Plumage Coloration

Food color can be indicative of specific nutrients, and thus discrimination based on color can be a valuable foraging behavior. Several bird and fish species with carotenoid-based body ornamentation show color preferences for presumably carotenoid-rich red and orange foods. However, little is known within species about whether or not individuals with (or growing) more colorful ornaments show stronger food-color preferences than those with drabber coloration. Here, we examine food color preferences in house finches ( Carpodacus mexicanus ) – a species with sexually dichromatic and selected carotenoid coloration – as a function of sex and plumage coloration during molt. We captured wild, molting juvenile house finches over 4 wk in late summer/early fall, quantified the color and size of plumage ornaments being developed in males, and determined food color preference in captivity by presenting individuals with dyed sunflower chips (red, orange, yellow, and green). On average, finches showed an aversion to yellow-dyed chips and a preference for red- and green-colored chips. We found no significant difference between male and female preferences for specific food colors, and food color preference was not significantly related to male plumage ornamentation. However, we did find that redder birds demonstrated a higher degree of food selectivity, measured as the proportion of their preferred food color consumed. These results suggest that food color is not a major factor determining food choice in molting house finches, but that there still may be aspects of foraging behavior that are linked to the development of colorful plumage.     

Carotenoid-based ornamentation and status signaling in the house finch

The status signaling hypothesis (SSH) was devised primarilyto explain the adaptive significance of avian ornamental colorationduring the nonbreeding season. It proposes that conspicuousmale plumage serves as an honest signal of social status withina population of birds. However, to date this hypothesis hasbeen well tested and supported for only one type of plumage coloration, melanin-based coloration. Carotenoid-based pigmentationis known to positively reveal male health and condition duringmolt in a variety of species, but it is poorly understood whetherthis ornament type can also function as a status signal duringthe winter. We tested the SSH in male house finches (Carpodacusmexicanus) by manipulating the carotenoid-based plumage brightnessof first-year males and then pairing unfamiliar birds of differingcoloration in a series of dominance trials in captivity. Manipulated plumage color was unrelated to win/loss outcome in these trials.Similarly, the natural pigmentation of males was a poor predictorof winter dominance; as in other studies with this species,we found only a weak tendency for naturally drab males to dominatenaturally bright males. These results suggest that carotenoid-basedcoloration is not a reliable indicator of social status inmale house finches during the nonbreeding season. In fact, carotenoid-based coloration may function only in mate choice in this species,and it may be retained throughout the year either because timeconstraints preclude a second plumage molt or because it aidsin pair formation that begins in late winter.     

Dietary carotenoids predict plumage coloration in wild house finches

Carotenoid pigments are a widespread source of ornamental coloration in vertebrates and expression of carotenoid-based colour displays has been shown to serve as an important criterion in female mate choice in birds and fishes. Unlike other integumentary pigments, carotenoids cannot be synthesized; they must be ingested. Carotenoid-based coloration is condition-dependent and has been shown to be affected by both parasites and nutritional condition. A controversial hypothesis is that the expression of carotenoid-based coloration in wild vertebrates is also affected by the amount and types of carotenoid pigments that are ingested. We tested this carotenoid-limitation hypothesis by sampling the gut contents of moulting house finches and comparing the concentration of carotenoid pigments in their gut contents with the colour of growing feathers. We found a positive association: males that ingested food with a higher concentration of carotenoid pigments grew brighter ornamental plumage. We also compared the concentration of carotenoids in the gut contents of males from two subspecies of house finches with small and large patches of carotenoid-based coloration. Consistent with the hypothesis that carotenoid access drives the evolution of carotenoid-based colour displays, males from the population with limited ornamentation had much lower concentrations of carotenoids in their gut contents than males from the population with extensive ornamentation. These observations support the idea that carotenoid intake plays a part in determining the plumage brightness of male house finches.     

Melanin-based plumage coloration in the house finch is unaffected by coccidial infection

For most species of birds, ornamental plumage coloration may result from two types of pigments: carotenoids and melanins. Despite the fact that melanin pigments can be synthesized by birds from basic, amino acid precursors, while carotenoids cannot be synthesized by birds and must be ingested, melanin-based plumage coloration and carotenoid-based plumage coloration have often been treated as a single trait in investigations of the function and evolution of plumage coloration. Expression of carotenoid-based coloration is known to be dependent on condition, while the effects of individual condition have not been well-tested for expression of melanin-based coloration. In this study, we experimentally tested the effect of coccidial infection of the intestinal tract of male house finches during moult on expression of melanin-based plumage coloration. Coccidial infection had a significant negative effect on carotenoid-based coloration, but it had no significant effect on melanin-based feather coloration. Unlike carotenoid-based coloration, melanin-based coloration may be cheap to produce, and honesty of melanin-based coloration my require social mediation.     

Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration

In birds, carotenoid-based plumage coloration is more dependent on physical condition and foraging abilities and less constrained developmentally than is melanin-based coloration. Thus, female mate choice for honest signals should result in more intense sexual selection on carotenoid- than on melanin-based plumage coloration. Using variation in sexual dimorphism as an indirect measure of the intensity of sexual selection, we tested the prediction mat variation in sexual dimorphism is driven more by change in carotenoid-based coloration between males and females dian by change in melanin-based coloration. Examination of historical changes in carotenoid- versus melanin-based pigmentation in 126 extant species of Cardueline finches supported this prediction. We found that carotenoid-derived coloration changed more frequendy among congeners dian melanin-based coloration. In both sexes, increase in carotenoid-based coloration score, but not in melanin-based coloration score, was strongly associated with increase in sexual dichromatism. In addition, sexual dimorphism in carotenoid-based coloration contributed more to overall dichromatism than dimorphism in melanin-based plumage. Our results supported die hypothesis that melanin-based and carotenoid-based coloration have fundamentally different signal content and suggest that combining melanin-based and carotenoid-based coloration in comparative analyses is not appropriate.     

MALE MATE CHOICE AND THE EVOLUTION OF FEMALE PLUMAGE COLORATION IN THE HOUSE FINCH

The house finch (Carpodacus mexicanus) is a sexually dichromatic passerine in which males display colorful plumage and females are generally drab brown. Some females, however, have a subdued version of the same pattern of ornamental coloration seen in males. In previous research, I found that female house finches use male coloration as an important criterion when choosing mates and that the plumage brightness of males is a reliable indicator of male nest attentiveness. Male house finches invest substantially in the care of young and, like females, stand to gain by choosing high-quality mates. I therefore hypothesized that a female's plumage brightness might be correlated with her quality and be the basis for male mate choice. In laboratory mate choice experiments, male house finches showed a significant preference for the most brightly plumaged females presented. Observations of a wild population of house finches, however, suggest that female age is the primary criterion in male choice and that female plumage coloration is a secondary criterion. In addition, yearling females tended to have more brightly colored plumage than older females, and there was no relationship between female plumage coloration and overwinter survival, reproductive success, or condition. These observations fail to support the idea that female plumage coloration is an indicator of individual quality. Male mate choice for brightly plumaged females may have evolved as a correlated response to selection on females to choose brightly colored males.     

The carotenoid-based plumage coloration of adult Blue Tits Cyanistes caeruleus correlates with the health status of their brood

The Blue Tit Cyanistes caeruleus is a passerine bird in which both sexes provide substantial care to the offspring and display conspicuous carotenoid-based plumage coloration. It has been shown that carotenoid-based coloration in birds reflects both individual quality and foraging ability. Because the body condition of nestlings usually depends on the capacity of their parents to feed them, I predicted that, independent of sex, those individuals with the most exaggerated carotenoid-based plumage coloration should raise offspring in better health. I found that although, in my study population, the smallest females were paired with the largest males, the brightest females were paired with the brightest and most intensely coloured males. I used body condition and T-cell-mediated immune response of nestlings as measures of their health status. Generalized mixed models showed that brighter and more-yellow adults reared offspring in better than average condition and immune response. Older males and smaller females were also able to raise offspring with better immune response. All these results suggest that the carotenoid-based plumage coloration of parents is somehow linked with individual quality, as it presents a significant and positive correlation with the health status of their growing chicks. Thus, the brightest and more intensely coloured individuals raised the healthiest offspring.     

Condition-dependent sexual traits and social dominance in the house finch

Elaboration of costly sexual traits can reduce investment inother aspects of reproduction, such as parental care or intrasexualcompetition, which may lead to the evolution of alternativemating tactics. In house finches (Carpodacus mexicanus), lesselaborately ornamented (dull) males tend to dominate more elaborated(redder) males, but redder males pair earlier and invest morein parental care. This suggests that males may pursue alternativeparental or competitive tactics, depending on the elaborationof their sexual trait. Elevation of testosterone, a hormonethat is closely associated with condition in male house finches,influences dominance and sexual behaviors but is antagonisticto parental behaviors. We tested the hypothesis that the higherdominance status of dull males reflects an alternative testosterone-dependentmating tactic. First, we experimentally manipulated the testosteronelevels of captive males and measured the effect on dominancerank, and second, we measured the association of testosteroneelevation and plumage hue in free-living males. We found that,as predicted, testosterone elevation increased dominance rankin captive males. However, in free-living males, testosteronelevels were higher in redder males, suggesting that testosteroneis dissociated from dominance status under natural circumstances.This may be because the context of social interactions and thehigher motivation of dull males to access food resources havea stronger influence on the outcome of dominance interactionsthan does the physiological effects of testosterone elevation.In turn, the strong positive correlation between testosteronelevels and plumage elaboration likely reflects the common conditiondependence of these traits.     

Energetic constraints on expression of carotenoid-based plumage coloration

Carotenoid pigments are used by many bird species as feather colorants, creating brilliant yellow, orange, and red plumage displays. Such carotenoid-based plumage coloration has been shown to function as an honest signal that is used in female mate choice. Despite recent interest in carotenoid-based ornamental traits, the basis for individual variation in expression of carotenoid-based plumage coloration remains incompletely understood. I tested the hypothesis that, independent of carotenoid access, food stress during molt would cause reduced expression of carotenoid pigmentation. I fed molting male House Finches Carpodacus mexicanus seed diets supplemented with either the red carotenoid pigment canthaxanthin or the yellow/orange carotenoid pigment β-cryptoxanthin (in the form of tangerine juice). Within each diet treatment, one group of males was given restricted food access and the other group was given unrestricted food access. Carotenoid supplements were placed in water so carotenoid access was controlled independent of food access. The results indicated a strong effect of both carotenoid access and food access on color display. Some males in the β-cryptoxanthin-supplemented group grew red plumage, suggesting that they can metabolically modify yellow pigments into red pigments, but no bird supplemented with β-cryptoxanthin grew plumage as red as birds supplemented with canthaxanthin. Males in the unrestricted food groups grew redder and more intensely pigmented plumage than males in the restricted food groups. These observations provide the best evidence to date of an energetic cost of carotenoid utilization in the generation of colorful plumage.     

Paternal care as a conditional strategy: distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch

When individuals in a population differ in physiological conditionand residual reproductive value, selection should favor phenotypicplasticity in reproductive investment such that individualsare able to adopt the reproductive tactic that results in thehighest fitness under given conditions. Here we examined reproductivetactics in relation to the elaboration of condition-dependentsexual ornamentation (carotenoid breast coloration) in a Montanapopulation of the house finches (Carpodacus mexicanus). Malesused distinct reproductive tactics depending on elaborationof their sexual ornamentation. Males with red pigmentation (maximum ornament elaboration) paired with females that nestedearlier, but these males did little provisioning of incubatingfemales and nestlings. In contrast, males with yellow colorationpaired with females that nested later, but these males fedfemale and nestlings more. Consequently, for red males offspringrecruitment was primarily affected by earlier nest initiation, whereas in yellow males it was affected most by male provisioning.In males with intermediate plumage coloration, all measuredcomponents, nest initiation, provisioning of incubating female,and nestling feeding, strongly contributed to offspring recruitment.The fitness consequences of alternative reproductive tacticsof males were influenced by breeding experience and fidelityof their mates. Among first-time breeders, red males achievedthe highest fecundity because of the advantage gained throughearly nesting and pairing with more experienced females andbecause of compensation by their mates for low male provisioningof nestlings. Among experienced breeders, males with intermediateplumage coloration achieved the highest fecundity because ofthe combined benefits of relatively early pairing and high parental care. High variation in sexual ornamentation in a Montana populationof house finches may favor distinct associations of sexualdisplays with a particular set of reproductive behaviors.     

Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration

Carotenoid pigments can directly enhance the immune responsesof vertebrates, and they are used by many animals to createornamental color displays. It has been hypothesized that thesetwo functions of carotenoid pigments are linked: animals musttrade off use of carotenoid pigments for immune function versusornamental display. We tested two key predictions of this hypothesiswith captive American goldfinches, Carduelis tristis, a specieswith extensive carotenoid-based plumage coloration. First, wetested whether the immune systems of male goldfinches are carotenoidlimited during molt by supplying treatment groups with low,approximately normal, or high dietary access to lutein and zeaxanthin.Dietary treatment had a significant effect on plumage and billcolor but not on immunocompetence. We compared the cell-mediatedand humoral immune responses and the course of disease afterinfection for males in the different treatments. We observedno significant effect of the carotenoid content of diet on immuneresponse or disease resistance. Second, we tested whether therewas a positive relationship between immune function and expressionof ornamental coloration by comparing both the pre- and posttreatmentplumage coloration of males to their immune responses. We failedto find the predicted trade-off between ornament display andimmune function. These findings do not support the hypothesisthat songbirds with extensive carotenoid-based plumage displaystrade off the use of carotenoids for ornamentation versus immunefunction.     

Plumage color as a composite trait: developmental and functional integration of sexual ornamentation

Most studies of condition-dependent sexual ornaments have treated such ornaments as single traits. However, sexual ornaments are often composites of several components, each produced by partially independent developmental pathways. Depending on environmental and individual condition, components of these ornaments may reflect different behavioral or physiological properties of an individual. One of the best-known, condition-dependent ornaments is carotenoid-based plumage coloration, which has at least four distinct components: pigment elaboration, patch area, pigment symmetry, and patch area symmetry. Here we examined fitness consequences of variation in individual components of carotenoid ornamentation in male house finches (Carpodacus mexicanus). Over 5 yr and several selection episodes, we studied variation in the plumage components in a large sample (n = 498) of males from a Montana population. The ornament components were partially independent of each other and had distinct fitness consequences. Selection for higher fecundity favored an increase in redness of coloration and a decrease in pigment asymmetry and patch area asymmetry but did not act on patch area itself. In contrast, viability selection favored larger and more symmetrical ornamental patches but did not act on pigment elaboration. Developmental and functional interrelationships among individual components of ornamentation strongly differed between house finch populations. Distinct patterns of selection on individual components of condition-dependent ornaments, combined with partially independent development of components, should favor the evolution of composite sexual traits whose components reliably reflect condition across a wide array of environments.     

Dietary mineral content influences the expression of melanin-based ornamental coloration

Many animals develop bold patches of black or brown colorationthat are derived from melanin pigments and serve as sexual orsocial signals. At present, there is much debate among behavioralecologists over whether melanin-based color signals are costlyto produce. Studies that have manipulated crude aspects of nutrition(i.e., total food intake) or health have generally found melanin-basedplumage ornaments to be less responsive to such factors thanother types of extravagant color (e.g., carotenoid or structuralbased). However, a recently advanced hypothesis argues thatlimited minerals in the diet, such as calcium (Ca), zinc (Zn),and iron (Fe), may serve to increase melanin pigment productionand maintain signal honesty. Here, I experimentally tested whethervariation in the calcium content of the diet affects the colorand extent of melanin-based plumage in male zebra finches (Taeniopygiaguttata). Calcium supplementation increased the size, but notdarkness, of the black breast plumage patch in fledgling andadult males; however, sexually selected, carotenoid-based redbeak coloration was not affected by the diet manipulation. Theseresults are the first to support the idea that acquisition ofminerals from the diet is a unique, limiting factor for theexpression of ornamental melanin coloration in animals.     

Sex,size, and plumage redness predict house finch survival in an epidemic

Mycoplasma gallisepticum is a well-known disease of poultry but until 1994 had not been observed in passerine birds. From 1994 to 1996, tens of millions of house finches (Carpodacus mexicanus) are believed to have died in an epidemic of mycoplasmal conjunctivitis, similar to ''pinkeye'' in humans. The outbreak of Mycoplasma gallisepticum affected finches of both sexes but disproportionately killed males, shifting the sex ratio from male-biased to female-biased. This differential male mortality is consistent with a cost of testosterone, which is a key prediction of the immunocompetence handicap hypothesis. Males and females that survived the epidemic weighed significantly less and had significantly shorter wing chords, tarsi, and bills than did individuals before the epidemic. Male survivors also had significantly redder plumage than males that did not survive, supporting the idea that plumage brightness serves as an indicator of condition, as proposed by the honest advertisement model of sexual selection.     

Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny

Birds show striking interspecific variation in their use of carotenoid-based coloration. Theory predicts that the use of carotenoids for coloration is closely associated with the availability of carotenoids in the diet but, although this prediction has been supported in single-species studies and those using small numbers of closely related species, there have been no broad-scale quantitative tests of the link between carotenoid coloration and diet. Here we test for such a link using modern comparative methods, a database on 140 families of birds and two alternative avian phylogenies. We show that carotenoid pigmentation is more common in the bare parts (legs, bill and skin) than in plumage, and that yellow coloration is more common than red. We also show that there is no simple, general association between the availability of carotenoids in the diet and the overall use of carotenoid-based coloration. However, when we look at plumage coloration separately from bare part coloration, we find there is a robust and significant association between diet and plumage coloration, but not between diet and bare part coloration. Similarly, when we look at yellow and red plumage colours separately, we find that the association between diet and coloration is typically stronger for red coloration than it is for yellow coloration. Finally, when we build multivariate models to explain variation in each type of carotenoid-based coloration we find that a variety of life history and ecological factors are associated with different aspects of coloration, with dietary carotenoids only being a consistent significant factor in the case of variation in plumage. All of these results remain qualitatively unchanged irrespective of the phylogeny used in the analyses, although in some cases the precise life history and ecological variables included in the multivariate models do vary. Taken together, these results indicate that the predicted link between carotenoid coloration and diet is idiosyncratic rather than general, being strongest with respect to plumage colours and weakest for bare part coloration. We therefore suggest that, although the carotenoid-based bird plumage may a good model for diet-mediated signalling, the use of carotenoids in bare part pigmentation may have a very different functional basis and may be more strongly influenced by genetic and physiological mechanisms, which currently remain relatively understudied.     

Species divergence in sexually selected traits: increase in song elaboration is related to decrease in plumage ornamentation in finches

Elaborate plumage and complex songs of male birds are two of the best-known examples of sexually selected traits, yet the interaction between these traits is poorly understood. Theory suggests that among a suite of potential displays, animals will emphasize traits that are most conspicuous, least costly, or best signal condition and reduce display of other traits. Here we examined the relationship between song and plumage elaborations in cardueline finches, songbirds that are highly variable in plumage displays and songs, but that share a similar mating system. We statistically controlled for body mass, habitat characteristics, and phylogenetic relationships and found that across species song complexity was strongly negatively related to elaboration of plumage ornamentation. When plumage coloration was partitioned into carotenoid-based and melanin-based components, song complexity was negatively related to elaboration of male carotenoid-based coloration but unrelated to elaboration of melanin-based coloration. These observations support the idea that, for condition-dependent traits, animal species trade off trait expression in response to changes in the costs or the information content of these traits. We discuss several alternative explanations for the observed pattern.     

No evidence for survival selection on carotenoid-based nestling coloration in great tits (Parus major)

In several vertebrate species evidence supports the hypothesis that carotenoid-based coloration of adults has evolved due to sexual selection. However, in some birds already the nestlings display carotenoid-based coloration. Because the nestling's body plumage is typically moulted before the first reproductive event, sexual selection cannot explain the evolution of these carotenoid-based traits. This suggests that natural selection might be the reason for its evolution. Here we test whether the carotenoid-based nestling coloration of great tits (Parus major) predicts survival after fledging. Contrary to our expectation, the carotenoid-based plumage coloration was not related to short- nor to long-term survival in the studied population. Additionally, no prefledging selection was detectable in an earlier study. This indicates that the carotenoid-based coloration of nestling great tits is currently not under natural selection and it suggests that past selection pressures or selection acting on correlated traits may have led to its evolution.     

Structural coloration and sexual selection in the barn swallow Hirundo rustica

Structural coloration has been hypothesized to play a role insexual selection, and we tested whether this was the case ina field study of the barn swallow Hirundo rustica. The dorsaliridescent plumage of barn swallows has a strong reflectancein the ultraviolet (UV) region, with adult males on averagereflecting 8-9% more than adult females, as revealed by a 2-yearstudy in southwestern Spain. The correlation between structural coloration (described by the reflectance in the UV part of thespectrum, UV chroma and blue chroma) and three other secondarysexual characters significantly associated with male matingsuccess (tail length, tail asymmetry, and red facial coloration)was weak and generally nonsignificant. Nor was there a significantrelationship between color parameters and body condition. Wetested for an association between structural coloration of the dorsal plumage and sexual selection in a number of independenttests. Arrival date of males was not significantly relatedto color; there was no significant relationship between colorationand probability of survival or age; mated males did not havestronger reflectance than unmated males; and the duration ofthe premating period was not significantly related to color.Reproductive success was not significantly correlated withplumage coloration in males, nor was the feeding rate of offspringby brightly colored males higher than that of males with lessbright plumage. Given that sample sizes were large, and the power of statistical tests high, we conclude that current sexualselection on the coloration of the dorsal plumage in the barnswallow is, at best, weak.     

Structural and melanin coloration indicate parental effort and reproductive success in male eastern bluebirds

Male eastern bluebirds (Sialia sialis) have two types of ornamentalplumage coloration: a brilliant blue-ultraviolet head, back,and wings, and a patch of chestnut breast feathers. The blue-UVcoloration is produced from feather microstructure, whereasthe chestnut coloration is produced by a combination of pheaomelaninand eumelanin pigments deposited in feathers. We tested thehypothesis that plumage coloration reflects male quality ineastern bluebirds, a socially monogamous, sexually dichromaticbird. We investigated whether male ornamentation correlateswith mate quality and parental effort. We quantified three aspectsof male ornament coloration: (1) size of the patch of chestnutbreast feathers, (2) reflectance properties of the chestnutplumage coloration, and (3) reflectance properties of the blue-ultravioletplumage coloration. We found that males with larger breast patchesand brighter plumage provisioned nestlings more often, fledgedheavier offspring, and paired with females that nested earlier.Males with plumage coloration that exhibit more ultraviolethues fledged more offspring. These results suggest that plumagecoloration is a reliable indicator of male mate quality andreproductive success. Both melanin-based and structural-basedplumages appear to be honest signals of male quality and parentalcare that can be assessed by competitors or by potential mates.     

The effects of elevated testosterone on plumage hue in male House Finches

The majority of studies examining the role of hormones in the proximate mechanisms of plumage coloration in birds have focused on intersexual differences (plumage dichromatism) and on structural- or melanin-based plumage coloration. The relationship between hormones and carotenoid-based plumage color, and in particular intrasexual plumage color variation, has received little attention. We manipulated testosterone levels of both captive and wild male House Finches to determine whether testosterone influences the expression of male plumage color in this species. We found that in captive male House Finches elevated testosterone delayed molt and resulted in drabber, less red plumage, even when birds were supplemented with dietary carotenoids. Elevated testosterone also resulted in drab plumage color in wild males, and appeared to delay molt in wild birds as well. Wild males implanted with testosterone showed wide variation in expression of plumage coloration. Those implanted early in the year molted plumage similar in color to their pre-treatment plumage, but those implanted later molted substantially duller plumage, possibly because delayed molt resulting from elevated testosterone caused these males to molt when carotenoid pigments were not available in sufficient amounts. These observations have the potential to explain previously reported relationships between plumage color and behavior in male House Finches, and highlight the importance of considering the proximate mechanisms of plumage coloration in avian sexual selection.