Habitat structure is associated with the expression of carotenoid-based coloration in nestling blue tits Parus caeruleus

We investigated how the expression of carotenoid-based plumage coloration (lightness and chroma) in nestling blue tits Parus caeruleus is associated with forest structure in oak forests of central Spain. We found evidence of a reduced expression of carotenoid-based coloration in nestlings growing up in successionally young and structurally simple forest territories. Our results suggest that breast feather coloration can be used as an indicator of nestling quality because nestlings with more intense yellow plumage coloration had larger body size and stronger immune responses to the injection of phytohemagglutinin (PHA). Given the association of forest structural complexity with carotenoid-based plumage coloration, our findings suggest that variation in habitat structure may have a significant impact on forest birds in their first stages of life which has implications for forest management practices.     

Soil and preen waxes influence the expression of carotenoid-based plumage coloration

The signaling function of carotenoid-based plumage is mainly determined by the concentration of pigments in feathers. For this reason, most studies of the proximate control of coloration focus on processes during and preceding moult. In great tits Parus major, past research demonstrates that carotenoid-based plumage coloration honestly indicates male quality and, thus, may be a sexually selected signal. In this study, we investigate how dirt and preen oil influence the coloration of carotenoid-based feathers in the great tit. We collected six feathers from each individual bird; three feathers served as controls while the remaining three feathers were washed with a chloroform/methanol mixture to remove soil and preen waxes. We assessed plumage coloration using digital photography. This cleaning procedure slightly enhanced ornamentation; the experimentally cleaned feathers expressed hues shifted towards shorter wavelengths and expressed brighter overall coloration than control feathers. This is the first experimental study conducted on wild birds demonstrating that, in addition to pigment concentration, the presence of preen waxes and soils on feathers may contribute to variation in coloration.     

Integument coloration signals reproductive success,heterozygosity, and antioxidant levels in chick-rearing black-legged kittiwakes

Carotenoid pigments are important for immunity and as antioxidants, and carotenoid-based colors are believed to provide honest signals of individual quality. Other colorless but more efficient antioxidants such as vitamins A and E may protect carotenoids from bleaching. Carotenoid-based colors have thus recently been suggested to reflect the concentration of such colorless antioxidants, but this has rarely been tested. Furthermore, although evidence is accruing for multiple genetic criteria for mate choice, carotenoid-based colors have rarely been shown to reflect both phenotypic and genetic quality. In this study, we investigated whether gape, tongue, eye-ring, and bill coloration of chick-rearing black-legged kittiwakes Rissa tridactyla reflected circulating levels of carotenoids and vitamins A and E. We further investigated whether integument coloration reflected phenotypic (body condition and fledging success) and genetic quality (heterozygosity). We found that the coloration of fleshy integuments was correlated with carotenoid and vitamin A levels and fledging success but only in males. Furthermore, the coloration of tongue and eye-ring was correlated with heterozygosity in both males and females. Integument colors might therefore be reliable signals of individual quality used by birds to adjust their parental care during the chick-rearing period.     

Melanin- and carotenoid-dependent signals of great tits (<Emphasis Type="Italic">Parus major</Emphasis>) relate differently to metal pollution

Due to their high phenotypic plasticity, the expression of secondary sexual characteristics is particularly sensitive to stress. Here, we investigated the expression of two conspicuous visual signals in great tits (Parus major) in a metal pollution gradient. In three study sites with marked differences in metal contamination (mainly lead, cadmium, copper and zinc), we compared melanin and carotenoid colouration of great tits. While carotenoid colouration (yellow breast) was negatively related to metal pollution, the size of a melanin trait (breast stripe) was larger in the most polluted sites. Environmental pollutants not only affect the expression of conspicuous signals but may even enhance, directly or indirectly, a signal of male quality such as breast stripe. Our results also support the multiple messages hypothesis predicting that different signals highlight different aspects of geno- and phenotypic condition of the bearer.     

Assortative mating by carotenoid-based plumage colour: a quality indicator in American goldfinches,<Emphasis Type="Italic"> Carduelis tristis</Emphasis>

We investigated the mating patterns in 22 breeding pairs of wild American goldfinches (Carduelis tristis) with respect to their body size, condition, and carotenoid-based, yellow plumage colour. Using reflectance spectrometry, we objectively quantified plumage colours across the bird-visible wavelengths, revealing a unexpected UV peak in the reflectance spectrum from yellow feathers. We summarized our colour measurements using a principal components analysis to create a single variable, carotenoid PC1, that represents the intensity of this carotenoid-based yellow colour, a measure of phenotypic quality in this species. We found no evidence of assortative mating with respect to measures of body size or condition but there was positive assortative mating by carotenoid PC1, such that the yellow plumage colours of males and females were significantly correlated within pairs. We argue that the yellow carotenoid coloration of goldfinches may be important in mutual mate choice and, thus, that sexual selection in this species may act upon female ornamentation, as well as the more obvious plumage signals of males. Because assortative mating results in an increase in genetic variance, we suggest that this might be a mechanism that maintains variance in ornamental traits in spite of the variance-eroding effects of sexual selection.     

Carotenoid coloration is related to fat digestion efficiency in a wild bird

Some of the most spectacular visual signals found in the animal kingdom are based on dietarily derived carotenoid pigments (which cannot be produced de novo), with a general assumption that carotenoids are limited resources for wild organisms, causing trade-offs in allocation of carotenoids to different physiological functions and ornamentation. This resource trade-off view has been recently questioned, since the efficiency of carotenoid processing may relax the trade-off between allocation toward condition or ornamentation. This hypothesis has so far received little exploratory support, since studies of digestive efficiency of wild animals are limited due to methodological difficulties. Recently, a method for quantifying the percentage of fat in fecal samples to measure digestive efficiency has been developed in birds. Here, we use this method to test if the intensity of the carotenoid-based coloration predicts digestive efficiency in a wild bird, the house finch (Haemorhous mexicanus). The redness of carotenoid feather coloration (hue) positively predicted digestion efficiency, with redder birds being more efficient at absorbing fats from seeds. We show for the first time in a wild species that digestive efficiency predicts ornamental coloration. Though not conclusive due to the correlative nature of our study, these results strongly suggest that fat extraction might be a crucial but overlooked process behind many ornamental traits.     

Nuptial coloration of red shiners (<Emphasis Type="Italic">Cyprinella lutrensis</Emphasis>) is more intense in turbid habitats

Communication is shaped and constrained by the signaling environment. In aquatic habitats, turbidity can reduce both the quantity and quality of ambient light and has been implicated in the breakdown of visual signaling. Here, we examined the relationship between turbidity (quantified with long-term data) and the expression of carotenoid-based nuptial coloration in the red shiner (Cyprinella lutrensis), a small-bodied cyprinid. Males in more turbid habitats displayed redder fins, and an experimental manipulation of adult diet suggested that carotenoid intake alone did not explain among-population color differences. These results run counter to similar studies where signal expression decreased in turbid conditions, and may be explained by the non-territorial red shiner mating system, interactions between the mechanism of coloration and the signaling environment, or reduced cost of color expression in turbid habitats (e.g., reduced predation risk). Our results highlight how the behavioral and ecological contexts in which signals function can shape evolutionary responses to the environment.     

Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (<Emphasis Type="Italic">Alectoris rufa</Emphasis>)

Carotenoid pigments cannot be synthesized by vertebrates but must be ingested through the diet. As they seem to be a limited resource, carotenoid-based ornaments are particularly interesting as possible honest signals of individual quality, in particular of foraging efficiency and nutritional status. Some studies have demonstrated the condition dependence of carotenoid-based plumage in birds. However, many other carotenoid-pigmented bare parts (i.e. skin, caruncles, bills, cere, and tarsi) are present in birds but, in comparison with plumage, little is known about these traits as indicators of individual quality. Here, we show that the eye ring pigmentation and bill redness of the red-legged partridge (Alectoris rufa) are positively associated to body condition and recent changes in body mass. Also, we found a negative relationship between these two traits and heterophil-to-lymphocyte ratio, an indicator of physiological stress (the relationship with bill redness being significant only for males). In an experiment, we found that after a period of reduction in food intake (with the consequent loss of body mass), food-restricted birds showed lower eye ring pigmentation than ad-libitum-fed birds. Therefore, different ornaments seem to reflect changes in body condition but at different speeds or intensities (eye ring, a fleshy ornament, appears to respond more rapidly to changes in the nutritional status than a keratinized structure as the bill). These results indicate that carotenoid-based ornaments are condition-dependent traits in the red-legged partridge, being therefore susceptible to be employed as honest signals of quality in sexual selection.     

Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird

In egg-laying animals, mothers can influence the development of their offspring via the suite of biochemicals they incorporate into the nourishing yolk (e.g. lipids, hormones). However, the long-lasting fitness consequences of this early nutritional environment have often proved elusive. Here, we show that the colorful carotenoid pigments that female zebra finches (Taeniopygia guttata) deposit into egg yolks influence embryonic and nestling survival, the sex ratio of fledged offspring, and the eventual ornamental coloration displayed by their offspring as adults. Mothers experimentally supplemented with dietary carotenoids prior to egg-laying incorporated more carotenoids into eggs, which, due to the antioxidant activity of carotenoids, rendered their embryos less susceptible to free-radical attack during development. These eggs were subsequently more likely to hatch, fledge offspring, produce more sons than daughters, and produce sons who exhibited more brightly colored carotenoid-based beak pigmentation. Provisioned mothers also acquired more colorful beaks, which directly predicted levels of carotenoids found in eggs, thus indicating that these pigments may function not only as physiological ‘damage-protectants’ in adults and offspring but also as morphological signals of maternal reproductive capabilities.     

Melanin pattern morphs do not differ in metabolic rate: implications for the evolutionary maintenance of a melanophore polymorphism in the green swordtail, <Emphasis Type="Italic">Xiphophorus helleri</Emphasis>

Variation in melanin patterns among individuals, populations, and species is common in fishes of the genus Xiphophorus. In the variable platyfish, Xiphophorus variatus, variation in metabolic rate is associated with melanin coloration and the color morphs appear to be physiological specialists adapted to particular environmental conditions. This study investigates whether a melanin polymorphism in the green swordtail, Xiphophorus helleri, is likewise associated with variation in metabolic rate. We measured metabolic rate as oxygen consumption rate of both adult male and juvenile X. helleri in static respirometers. The oxygen consumption rate does not differ significantly between the spotted and nonspotted morphs in either group, suggesting that-unlike in X. variatus-selection on metabolic rate is not involved in maintaining the polymorphism in X. helleri. We suggest that explanations need to be sought for the evolution of melanophore diversity in Xiphophorus that are pertinent to each melanin pattern polymorphism or groups of similar polymorphisms.     

Multimodal sexual signals in male ocellated lizards Lacerta lepida: vitamin E in scent and green coloration may signal male quality in different sensory channels

The mechanisms that confer honesty to multiple sexual signals of vertebrates remain less known. We suggest that vitamin E in the scent (femoral secretions) and carotenoids in coloration of Lacerta lepida lizards might advertise quality because they are relevant in metabolism as major antioxidants and have a dietary origin. Results showed that there may be similar trade-offs between immunity and both chemical and visual signaling, as males with more vitamin E in secretions and those with more greenish, darker, and saturated carotenoid-dependent colorations had a higher immune response. This suggests that only high-quality males can divert from metabolism and allocate enough vitamin E to secretions and enough carotenoids to coloration. Therefore, information provided by visual and chemical signals is congruent. The use of multiple sensory channels may allow signaling a male quality under different circumstances or reinforce the reliability of the signal when both signals are perceived simultaneously. However, we also found that characteristics of carotenoid-dependent coloration mirror the amounts of vitamin E in secretions. This might support that carotenoids, which are not true antioxidants in the organism, would just reflect and “inform” on the actual contents of metabolic antioxidant vitamin E, which is part of the true system that prevent oxidation. We suggest that the metabolic roles of vitamins might be the actual basis of honesty of many sexual displays, and that carotenoid-based signals might be just the visible part of the whole system.     

The use of olfaction in the foraging behaviour of the golden-mantled flying fox,<Emphasis Type="Italic"> Pteropus pumilus</Emphasis>, and the greater musky fruit bat,<Emphasis Type="Italic"> Ptenochirus jagori</Emphasis> (Megachiroptera: Pteropodidae)

Double-choice experiments with three adult males of the little golden-mantled flying fox, Pteropus pumilus, and ten adult greater musky fruit bats, Ptenochirus jagori (both Megachiroptera: Pteropodidae), demonstrate that they are able to discriminate accurately between an empty dish and a dish containing fruits of one of several species by odour alone. Tests were run using fruits of six fruit species for Pteropus pumilus and five fruit species for Ptenochirus jagori. The fruit species used are known to be consumed in the wild by Ptenochirus jagori and are, with two exceptions, species of the natural rain-forest habitat. This is the first study to show that fruit bats are also able to assess the ripeness of a fruit exclusively by its odour. The bats preferred ripe over unripe fruits of the same species. Thus, both Pteropus pumilus and Ptenochirus jagori can not only locate fruits by their odour but can also discriminate between ripe and unripe fruits of the same species by olfaction. The results confirm and expand earlier findings on the role of olfactory cues in the orientation of foraging pteropodids.     

Sexually dichromatic coloration reflects size and immunocompetence in female Spanish terrapins, Mauremys leprosa

Many studies have shown the importance of colorful ornamentation in mate choosiness or intrasexual conflict. However, research on color ornaments has focused mainly on birds, lizards or fish, but remains practically unknown in other animal groups such as turtles. In addition, female ornaments and their relation with sexual selection also remain almost unknown. Here, we measured the coloration of the shell and the limb stripes of male and female Spanish terrapins Mauremys leprosa and explored the existence of sexual dichromatism and the relation of color characteristics with body size and health state estimated from the immune response to the injection of an antigen (phytohaemagglutinin test). Our results showed that shell coloration, which could be constrained by natural selection to be cryptic, changed with body size, but did not differ between sexes. In contrast, females had brighter and less ultraviolet-saturated and more orange-saturated limb stripes than males. In females, interindividual variation in limb stripe coloration was related with body size and immune response suggesting that this coloration may inform honestly about multiple traits that could be important in sexual selection. In contrast, coloration of limb stripes of males was duller than in females, and was not related with any trait suggesting that coloration is not important in sexual selection for males.     

A link between eumelanism and calcium physiology in the barn owl

In many animals, melanin-based coloration is strongly heritable and is largely insensitive to the environment and body condition. According to the handicap principle, such a trait may not reveal individual quality because the production of different melanin-based colorations often entails similar costs. However, a recent study showed that the production of eumelanin pigments requires relatively large amounts of calcium, potentially implying that melanin-based coloration is associated with physiological processes requiring calcium. If this is the case, eumelanism may be traded-off against other metabolic processes that require the same elements. We used a correlative approach to examine, for the first time, this proposition in the barn owl, a species in which individuals vary in the amount, size, and blackness of eumelanic spots. For this purpose, we measured calcium concentration in the left humerus of 85 dead owls. Results showed that the humeri of heavily spotted individuals had a higher concentration of calcium. This suggests either that plumage spottiness signals the ability to absorb calcium from the diet for both eumelanin production and storage in bones, or that lightly spotted individuals use more calcium for metabolic processes at the expense of calcium storage in bones. Our study supports the idea that eumelanin-based coloration is associated with a number of physiological processes requiring calcium.     

Immune challenges and visual signalling in tree frogs

In animals, mate-choice is often based on sexual signals that carry information and help the receiver make the best choice to improve the receiver’s fitness. Orange visual sexual signals have been hypothesised to carry immune information because they are often due to carotenoid pigments which are also involved in immunity response. Although many studies have focused on the direct relationships between coloration and immunocompetence, few studies have simultaneously studied immunocompetent response and coloration variation after an immune challenge. We tested this hypothesis on starved and ad libitum-fed males of the European tree frog Hyla arborea. Our results show that male coloration is not a reliable indicator of its immune response capacity in this species. However, after an immune challenge induced by a PHA (Phaseolus vulgaris phytohaemagglutinin) injection, starved males presented a significant coloration loss and this alteration was related to the immune response intensity. Taken together, these results suggest that the brighter (lighter) coloration may be used as a cue by female to exclude males with a recent immune challenge, due to diseases or parasites for example.     

A novel function for the pineal organ in the control of swim depth in the Atlantic halibut larva

The pineal organ of vertebrates is a photo-sensitive structure that conveys photoperiod information to the brain. This information influences circadian rhythm and related metabolic processes such as thermoregulation, hatching time, body growth, and the timing of reproduction. This study demonstrates extra-ocular light responses that control swim depth in the larva of the Atlantic halibut, Hyppoglosus hyppoglosus. Young larvae without a functional eye (<29 days) swim upwards after an average delay of 5 s following the onset of a downwelling light stimulus, but sink downwards a few seconds later. Older larvae (₉ days), which possess a functional eye, swim immediately downwards (microsecond delay) following the onset of the light stimulus, but proceed to swim upwards several seconds later. These two response patterns are thus opposite in polarity and have different time kinetics. Because the pineal organ of the Atlantic halibut develops during the embryonic stage, and because it is the only centre in the brain that expresses functional visual pigments (opsins) at early larval stages, it is the only photosensory organ capable of generating the extra-ocular responses observed.     

Are queen Bombus terrestris giant workers or are workers dwarf queens? Solving the 'chicken and egg' problem in a bumblebee species

In the social bee, Bombus terrestris, the two castes differ in size and physiology, but not in any other morphological and anatomical aspects. The size differences between the castes are the result of longer instar duration in prospective queen larvae. It appears that queen larvae are programmed to have a higher molting weight at the end of the 2nd, 3rd and 4th instars. Calculation of the growth ratio, the ratio between the logarithm of molting weight at two successive instars, revealed that queen larvae have a linear growth ratio over the entire larval development as predicted by Dyar's rule. In the worker larvae, in contrast, linearity of the growth ratio breaks after the second instar, resulting in larval molting at lower weights than expected by Dyar's rule. We therefore suggest that workers' development is abnormally shortened, either by parental manipulation or by adopting a different growth plan in response to the queen's signal.     

A novel sex-specific and inducible monoterpene synthase activity associated with a pine bark beetle,the pine engraver,<Emphasis Type="Italic"> Ips pini</Emphasis>

Ecological interactions of conifers and coniferophagous bark beetles are determined in part by terpenoids (isoprenoids), which are major defense metabolites of conifer oleoresin. Curiously, similar compounds are important aggregation pheromones of conifer-attacking bark beetles. Terpene synthases are responsible for generating the enormous variety of terpenoid carbon skeletons found in nature. These catalysts convert short-chain prenyl diphosphates to a diverse assortment of hemiterpene, monoterpene, sesquiterpene, and diterpene natural products. While terpene synthases have frequently been characterized from plant and microbial sources, they have not yet been described in animals. Here we report the discovery of a monoterpene synthase activity in an insect, the pine engraver, Ips pini (Say) (Coleoptera: Scolytidae). Cell-free assays of I. pini revealed that geranyl diphosphate (GDP) is converted to the acyclic monoterpene myrcene in whole-body extracts from males, but not females. Furthermore, the monoterpene synthase activity in males can be induced by prior treatment with juvenile hormone III (JH III) or by feeding on phloem from the host trees, Jeffrey pine (Pinus jeffreyi Grev. &; Balf.) or red pine (Pinus resinosa Ait.). The sex-specificity and endocrine induction of this activity argue for its involvement in the biosynthesis of monoterpenoid pheromones mediated by enzymes from insect tissue. This discovery is the first example of a monoterpene synthase in the Metazoa and evokes exciting new questions about the origin, evolution, and occurrence of terpene synthases.     

Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch

The Hamilton-Zuk hypothesis proposes that the bright colours displayed by many species of birds serve as signals of individual resistance to parasites. Despite the popularity of this hypothesis, only one previous study has tested whether plumage coloration predicts how individuals respond to a disease challenge. We inoculated 24 male house finches (Carpodacus mexicanus) of variable plumage hue with a novel bacterial pathogen, Mycoplasma gallicepticum (MG). We found no relationship between plumage hue and time to first symptoms following inoculation, but we found a significant negative relationship between plumage hue and clearance of disease: males with redder plumage cleared MG infection significantly better than did males with yellower plumage. The hue of carotenoid-based plumage coloration has been shown to be a primary criterion in female mate choice in the house finch. These observations suggest that one benefit to females for choosing redder males is obtaining mates with better resistance to parasites.     

Ancient specimens and DNA contamination: a case study from the 12S rRNA gene sequence of the "Linh Duong" bovid (Pseudonovibos spiralis)

In 1993, several unusual horn sheaths, collected in the South of Vietnam, were regarded as evidence for a new mammal species, Pseudonovibos spiralis. However, the taxonomic status of P. spiralis remains a highly controversial subject: firstly, it has been related to three different groups of the family Bovidae: Antilopini (gazelles), Bovini (oxen, bisons, and buffaloes), and Caprini sensu lato (goats, sheep and allies). Secondly, certain horns have been shown to be faked. Most recently, it has been suggested, on the basis of 12S rRNA gene sequences, that P. spiralis was a new species of buffalo. I demonstrate here that this conclusion was inaccurate, and base this on the grounds that: (1) the putative sequence of P. spiralis is shown to be a chimera obtained from three different species: Bos taurus, Bubalus bubalis and Saiga tatarica, and (2) several factors indicate that the specimen used was not authentic. This new study confirms earlier suggestions that the horns used to formally describe P. spiralis were bogus and were in fact derived from the horns of domesticated cattle (Bos taurus). The data suggest that P. spiralis never existed.