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Ketocarotenoid circulation, but not retinal carotenoid accumulation, is linked to eye disease status in a wild songbird
... We measured the area under the curve twice for every component and used averaged (mean) values for analysis; the measurer was blind to all data except the sample ID at the time of data collection. We calculated the concentration (in lmol/L) of each component following McGraw et al. (2013). We estimated the repeatability of plasma carotenoid and vitamin concentrations by adjusting linear models between both measurements to check for measurement consistency, using the lme4 package (Bates et al. 2015) in R. All linear models were positive and statistically significant, and the intrasample repeatability (between AUC measurements) estimates were as follows (r 2 in parentheses): alpha-tocopherol (99%), retinol (98%), lutein isomers (97%), lutein (99%), zeaxanthin (99%), beta-cryptoxanthin (18%), beta-carotene (16%), astaxanthin (46%), canthaxanthin (19%), 3 0hydroxy-echinenone (98%), and 3 0 -hydroxy-echinenone esters (75%). ...
... Only models with delta values that were lower than 4 are displayed. Colnago et al. 1984;da Silva et al. 2011;Cowieson et al. 2020) and with mycoplasmal conjunctivitis (McGraw et al. 2013) and poxvirus in House Finches (McGraw et al. 2020). Finches in our study might have had a mild or chronic infection, which might explain the lack of association between co-infection status and most of our physiological metrics. ...
Pathogens have traditionally been studied in isolation within host systems; yet in natural settings they frequently coexist. This raises questions about the dynamics of co-infections and how host life-history traits might predict co-infection versus single infection. To address these questions, we investigated the presence of two parasites, a gut parasite (Isospora coccidians) and a blood parasite (Plasmodium spp.), in House Finches (Haemorhous mexicanus), a common passerine bird in North America. We then correlated these parasitic infections with various health and condition metrics, including hematological parameters, plasma carotenoids, lipid-soluble vitamins, blood glucose concentration, body condition, and prior disease history. Our study, based on 48 birds captured in Tempe, Arizona, US, in October 2021, revealed that co-infected birds exhibited elevated circulating lutein levels and a higher heterophil:lymphocyte ratio (H/L ratio) compared to those solely infected with coccidia Isospora spp. This suggests that co-infected birds experience heightened stress and may use lutein to bolster immunity against both pathogens, and that there are potentially toxic effects of lutein in co-infected birds compared to those infected solely with coccidia Isospora sp. Our findings underscore the synergistic impact of coparasitism, emphasizing the need for more co-infection studies to enhance our understanding of disease dynamics in nature, as well as its implications for wildlife health and conservation efforts.
... Measurement of plasma carotenoids, vitamins, and oxidative stress We followed prior methods for carotenoid extraction and analysis via high-performance liquid chromatography (HPLC) ( McGraw et al. 2013), which included (unlike in our other prior study of finch plasma carotenoids; McGraw et al. 2006a) the additional acid pre-treatment of our HPLC column (Toomey and McGraw 2007) that permitted us to recover ketocarotenoids if present. Among the 338 total plasma samples (winter 2011: n ¼ 115; spring 2011: n ¼ 118; summer/fall 2011: n ¼ 105), we detected vitamin A (retinol; Navarro et al. 2010), vitamin E (alpha-tocopherol; Giraudeau et al. 2013), and seven different types of carotenoids: lutein, zeaxanthin,-cryptoxanthin,-carotene, dehydrolutein, 3hydroxy-echinenone (3HE), and an esterified form of 3HE (Fig. 1). ...
... However, these carotenoids may be physiologically depleted from the body due to oxidative challenges during breeding and molt (i.e., if serving as antioxidants; Krinsky 1989;Lozano 1994;von Schantz et al. 1999), and specific to molt can be deposited into plumage (Inouye et al. 2001) or serve as precursors for other metabolically produced carotenoids ( McGraw et al. 2006a). In contrast, the one ketocarotenoid we detected in circulation3HE-was present in circulation only during late summer/early fall, and this signifies the seasonally timed, specialized process of manufacturing red pigments only when new ornamental plumage is being grown ( McGraw et al. 2013). ...
Rapid worldwide urbanization is creating novel environments to which animals must adapt, a topic of growing interest for biologists. Studies of how organisms are affected by cities historically centered on large-scale censusing of populations, but recent investigations have considered finer-scaled, urban-rural differences among individuals and species in their behavior, morphology, and physiology, specifically as they relate to urban stress. A number of factors (e.g., corticosterone (CORT)-related stress response) may contribute to the degree of stress experienced by animals living under urban versus natural conditions, but several physiological variables have yet to be considered together in a large-scale assessment. Here, in a widespread species of desert passerine (the house finch, Haemorhous mexicanus), we quantified variation in plasma oxidative stress, plasma concentrations of vitamins and carotenoids, and body-mass of males in three successive seasons (winter, spring, and late summer/early fall) along an urban-rural gradient in Phoenix, Arizona, USA. We found that degree of urbanization was: (1) negatively related to circulating vitamin A concentrations in winter, (2) positively correlated with body-mass during spring, and (3) negatively associated with plasma concentrations of two carotenoids: zeaxanthin (during breeding) and 3-hydroxy-echinenone (3HE) (during molting). The striking link between 3HE levels and urbanization is consistent with previous research showing that urban songbirds have lower carotenoid levels and faded plumage; our finding is the first to implicate specific effects on a metabolically derived carotenoid for coloration. The fact that we observed only season-specific links between urbanization and indicators of quality in finches suggests that (at least for these metrics) there are no strong, lasting urban pressures imposed on finch physiology over the year. Interestingly, we found that a metric of plasma oxidative stress (lipid peroxidation) was positively correlated with levels of two carotenoids (lutein during breeding and 3HE during molting), which is consistent with a prior study of ours showing that finches with redder plumage deposit higher levels of CORT in their feathers; taken together, our studies suggest complex associations between carotenoids and stress.
... Yet, it is not clear how well these laboratory results generalize to infections in natural populations. Wild house finches infected with Mycoplasma gallisepticum, which causes inflammation of the eye conjunctiva, show no significant differences in retina carotenoid accumulation compared with healthy birds of the same population (McGraw et al., 2013). ...
Carotenoids color many of the red, orange and yellow ornaments of birds and also shape avian vision. The carotenoid-pigmented oil droplets in cone photoreceptors filter incoming light and are predicted to aid in color discrimination. Carotenoid use in both avian coloration and color vision raises an intriguing question: is the evolution of visual signals and signal perception linked through these pigments? Here, we explore the genetic, physiological and functional connections between these traits. Carotenoid color and droplet pigmentation share common mechanisms of metabolic conversion and are both affected by diet and immune system challenges. Yet, the time scale and magnitude of these effects differ greatly between plumage and the visual system. Recent observations suggest a link between retinal carotenoid levels and color discrimination performance, but the mechanisms underlying these associations remain unclear. Therefore, we performed a modeling exercise to ask whether and how changes in droplet carotenoid content could alter the perception of carotenoid-based plumage. This exercise revealed that changing oil droplet carotenoid concentration does not substantially affect the discrimination of carotenoid-based colors, but might change how reliably a receiver can predict the carotenoid content of an ornament. These findings suggest that, if present, a carotenoid link between signal and perception is subtle. Deconstructing this relationship will require a deeper understanding of avian visual perception and the mechanisms of color production. We highlight several areas where we see opportunities to gain new insights, including comparative genomic studies of shared mechanisms of carotenoid processing and alternative approaches to investigating color vision.
... Given that radiation sources are external (i.e. surrounding contaminated environment, such as water and soil) and internal (ingestion or dermal absorption), the intensity of this deposit is a function of radiation energy, as well as of the organisms' shape, composition and lifestyle 52 . ...
The nuclear accident in the Fukushima prefecture released a large amount of artificial radionuclides that might have short- and long-term biological effects on wildlife. Ionizing radiation can be a harmful source of reactive oxygen species, and previous studies have already shown reduced fitness effects in exposed animals in Chernobyl. Due to their potential health benefits, carotenoid pigments might be used by animals to limit detrimental effects of ionizing radiation exposure. Here, we examined concentrations of carotenoids in blood (i.e. a snapshot of levels in circulation), liver (endogenous carotenoid reserves), and the vocal sac skin (sexual signal) in relation to the total radiation dose rates absorbed by individual (TDR from 0.2 to 34 µGy/h) Japanese tree frogs (Hyla japonica). We found high within-site variability of TDRs, but no significant effects of the TDR on tissue carotenoid levels, suggesting that carotenoid distribution in amphibians might be less sensitive to ionizing radiation exposure than in other organisms or that the potential deleterious effects of radiation exposure might be less significant or more difficult to detect in Fukushima than in Chernobyl due to, among other things, differences in the abundance and mixture of each radionuclide.
The carotenoid-based colors of birds are a celebrated example of biological diversity and an important system for the study of evolution. Recently, a two-step mechanism, with the enzymes cytochrome P450 2J19 (CYP2J19) and 3-hydroxybutyrate dehydrogenase 1-like (BDH1L), was described for the biosynthesis of red ketocarotenoids from yellow dietary carotenoids in the retina and plumage of birds. A common assumption has been that all birds with ketocarotenoid-based plumage coloration used this CYP2J19/BDH1L mechanism to produce red feathers. We tested this assumption in house finches ( Haemorhous mexicanus ) by examining the catalytic function of the house finch homologs of these enzymes and tracking their expression in molting birds. We found that CYP2J19 and BDH1L did not catalyze the production of 3-hydroxy-echinenone (3-OH-echinenone), the primary red plumage pigment of house finches, when provided with common dietary carotenoid substrates. Moreover, gene expression analyses revealed little to no expression of CYP2J19 in liver tissue or growing feather follicles, the putative sites of pigment metabolism in molting house finches. Finally, although the hepatic mitochondria of house finches have high concentrations of 3-OH-echinenone, observations using fluorescent markers suggest that both CYP2J19 and BDH1L localize to the endomembrane system rather than the mitochondria. We propose that house finches and other birds that deposit 3-OH-echinenone as their primary red plumage pigment use an alternative enzymatic pathway to produce their characteristic red ketocarotenoid-based coloration.
Animals use diverse signal types (e.g. visual, auditory) to honestly advertise their genotypic and/or phenotypic quality to prospective mates or rivals. Behavioural displays and other dynamically updateable signals (e.g. songs, vibrations) can reliably reveal an individual’s quality in real-time, but it is unclear whether more fixed traits like feather colouration, which is often developed months before breeding, still reveal an individual’s quality at the time of signal use. To address this gap, we investigated if various indices of health and condition—including body condition (residual body mass), poxvirus infection, degree of habitat urbanization, and circulating levels of ketones, glucose, vitamins, and carotenoids—were related to the expression of male plumage colouration at the start of the spring breeding season in wild male House Finches (Haemorhous mexicanus), a species in which many studies have demonstrated a link between plumage redness and the health and condition of individuals at the time the feathers are grown in late summer and autumn. We found that, at the time of pair formation, plumage hue was correlated with body condition, such that redder males were in better condition (i.e. higher residual mass). Also, as in previous studies, we found that rural males had redder plumage; however, urban males had more saturated plumage. In sum, these results reveal that feather colouration developed long before breeding still can be indicative to choosy mates of a male’s current condition and suggest that females who prefer to mate with redder males may also gain proximate material benefits (e.g. better incubation provisioning) by mating with these individuals in good current condition.
As a major physiological mechanism involved in cellular renewal and repair, immune function is vital to the body's capacity to support tissue maintenance and organismal survival. Because immune defenses can be energetically expensive, the activities of metabolically active organs, such as the liver, are predicted to increase during infection by most pathogens. However, some pathogens are immunosuppressive, which might reduce the metabolic capacities of select organs to suppress immune response. Mycoplasma gallisepticum (MG) is a well-known immunosuppressive bacterium that infects domestic chickens and turkeys as well as songbirds. In the house finch (Haemorhous mexicanus), which is the primary host for MG among songbird species, MG infects both the respiratory system and the conjunctiva of the eye, causing conspicuous swelling. To study the effect of a systemic bacterial infection on cellular respiration and oxidative damage in the house finch, we measured mitochondrial respiration, mitochondrial membrane potential, reactive oxygen species production, and oxidative damage in the livers of house finches that were wild caught and either infected with MG, as indicated by genetic screening for the pathogen, or free of MG infection. We observed that MG-infected house finches showed significantly lower oxidative lipid and protein damage in liver tissue compared with their uninfected counterparts. Moreover, using complex II substrates, we documented a nonsignificant trend for lower state 3 respiration of liver mitochondria in MG-infected house finches compared with uninfected house finches (
P
=
0.07
). These results are consistent with the hypothesis that MG suppresses organ function in susceptible hosts.
Carotenoid pigments produce the ornamental red, orange, and yellow integumentary coloration of many species of animals. Among individuals of a population, the hue and saturation of carotenoid-based ornaments can be extremely variable, and studies of fish and birds have shown that females generally prefer males that display the most saturated and reddest coloration. Consequently, there has been a great deal of interest in determining the proximate factors that affect individual expression of carotenoid-based pigmentation. Parasites might affect production of ornamental coloration, and the Hamilton-Zuk hypothesis proposes that parasitized males will show decreased expression of the secondary sexual traits preferred by females. We found that captive male House Finches (Carpodacus mexicanus) experimentally infected with Isospora spp. (coccidians) and/or Mycoplasma gallisepticum produced carotenoid-based plumage coloration that was significantly less red and less saturated than that of noninfected males. These observations validate a necessary condition of the Hamilton-Zuk hypothesis, but heritable resistance to the pathogens we examined remains to be demonstrated.
Parasites are widely assumed to cause reduced expression of ornamental plumage coloration, but few experimental studies have tested this hypothesis. We captured young male house finches Carpodacus mexicanus in Alabama before fall molt and randomly divided them into two groups. One group was infected with the bacterial pathogen Mycoplasma gallicepticum (MG) and the other group was maintained free of MG infection. All birds were maintained through molt on a diet of seeds with tangerine juice added to their water as a source of β-cryptoxanthin, the natural precursor to the primary red carotenoid pigment in house finch plumage. All males grew drab plumage, but males with MG infection grew feathers that were significantly less red (more yellow), less saturated, and less bright than males that were not infected. MG targets upper respiratory and ocular tissue. Our observations show that a pathogen that does not directly disrupt carotenoid absorption or transportation can still have a significant effect on carotenoid utilization.
Individual variation in parasite exposure is often overlooked in studies of the role of parasites in the evolution of mate choice. Here we outline how androgen and carotenoid dependent red breeding coloration might broadcast reliable information about parasite exposure and genetic resistance to common parasites in a population of male three-spined sticklebacks (Gasterosteus aculeatus). Copepods, which are important prey for sticklebacks contain carotenoids essential for development of breeding coloration, but are also intermediate hosts for common parasites of sticklebacks. Of the five parasite species found in 46 males, only those three transmitted through copepods show associations with intensity of red breeding coloration. Two of these (Diphyllobothrium spp.) show a positive relationship with intensity of red coloration, whereas the apparently more pathogenic Schistocephalus solidus is negatively associated with intensity of red breeding coloration. The signal broadcasted by bright red males may thus be operating both as a sexually selected handicap, and as a reliable signal about degree of parasite exposure.
—Like males of many bird species, male House Finches (Carpodacus mexicanus) have patches of feathers with ornamental,coloration that are due to carotenoid,pigments. With- in populations, male House Finches vary in expression of ornamental coloration from pale yel- low to bright red, which previous research suggested was the result of variation in types and amounts,of carotenoid,pigments,deposited,in feathers. Here we used improved,analytical tech- niques to describe types and amounts,of carotenoid,pigments,present in that plumage. We then used,those data to make,comparisons,of carotenoid,composition,of feathers of male,House Finches at three levels: among individual males with different plumage hue and saturation, between age groups of males from the same population, and between males from two sub- species that differ in extent of ventral carotenoid,pigmentation,(patch size): large-patched,C. m. frontalis from coastal California and small-patched C. m. griscomi from Guerrero, Mexico. In all age groups and populations, the ornamental plumage coloration of male House Finches resulted from the same 13 carotenoid pigments, with 3-hydroxy echinenone and lutein being the most,abundant,carotenoid,pigments. The composition,of carotenoids,in feathers suggested that House Finches are capable,of metabolic,transformation,of dietary forms of carotenoids. The hue of male plumage depended on component carotenoids, their relative concentrations, and total concentration,of all carotenoids. Most 4-keto (red) carotenoids,were,positively cor- related with plumage redness, and most yellow carotenoid pigments were negatively associ- ated with plumage redness, although the strength of the relationship for specific carotenoid pigments,varied among,age groups,and,subspecies. Using age and subspecies,as factors and concentration of each component carotenoid as dependent variables in a MANOVA, we found a distinctive pigment profile for each age group within each subspecies. Among frontalis males, hatch-year birds did not differ from adults in mean plumage hue, but they had a significantly lower proportion of red pigments in their plumage, and significantly lower levels of the red
Independent of age or geographic variation, males of many species of birds exhibit dramatic variation in the expression of elaborate secondary sexual characters. ''Good genes'' models of sexual selection propose that males with relatively low resistance to parasites suffer high parasite loads that inhibit their ability to express these characters fully. In turn, variation in such characters may reliably indicate male quality and may be used by females to choose males. This is the first study to monitor (via mark-recapture) the long-term effects of parasites on color and growth of plumage in individual birds. Specifically, we used house finches, Carpodacus mexicanus, a sexually dimorphic species in which females are known to prefer more brightly plumaged males for mating, to test the hypothesis that high parasite load in males is correlated with poor physiological condition and reduced development of male secondary sex characters. Our results clearly demonstrate that both ectoparasitic feather mite (Proctophyllodes sp.) infestations and endoparasitic avian pox viral infections during molt are correlated with poor physiological condition and reduced development of bright male plumage during the same molt period, thus supporting good genes models.
Understanding the relative costs of different forms of ornamental displays is fundamental to research on the evolution of such traits. For traits such as elongated tails, assessing the degree of exaggeration is straight-forward: bigger is more exaggerated and more costly. In contrast, assignment of such a hierarchical ranking of costliness and exaggeration to color displays has not been possible. In this paper, I consider whether red carotenoid displays represent a more energetically costly form of ornamentation than yellow or orange carotenoid displays. Several lines of evidence support the idea that red carotenoid pigmentation is particularly costly. Red carotenoid pigments are less abundant than yellow pigments in the diet of virtually all vertebrates. Although many vertebrates can convert some yellow carotenes and xanthophylls to red pigments, all species appear to be restricted in the types of metabolic conversions of which they are capable as well as by the costs of such conversions. In virtually all avian taxa with carotenoid-based coloration, when females and juvenile males show plumage hue that is different than that of adult males, their plumage is less red (more orange or yellow). Finally, in a comparative study of cardueline finches, there was a significant positive relationship between the degree of sexual dichromatism and the redness of male plumage, suggesting that red is a particularly costly color display. The finding that red is a more costly color display than yellow or orange has important implications for comparative studies of the evolution of ornamental plumage.
Male House Finches (Carpodacus mexicanus) in southern California show a large range of plumage variation, with individuals varying along a continuum from yellow to orange to red. This extreme variation is largely unrelated to age and is likely to have fitness consequences (e.g. Hill 1990, 1991; Belthoff 1994; Thompson et al. 1997). New analyses based on museum specimens, a literature review, and recently captured individuals indicate that the high level of variation is a new phenomenon because most males were red prior to the 1950s, whereas half or more are currently orange or yellow. The change toward orange and yellow plumage may be related to a high incidence of avian pox that was first noted in the early 1970s but probably began earlier. In addition to a temporal link between pox and plum- age variation in California, there is also a geographic link. Pox is very common in Hawaii, where most males are orange or yellow, but rare or absent on San Nicolas Island off the coast of southern California and in eastern North America. At least 90% of the males are red in each of these two latter areas. The link between pox and plumage color may occur as an effect of physiological condition, patbogen virulence, or host resistance among populations, or from a combination of these factors. Received 17 July 1997, accepted 29 April 1998.
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Abstract Trade-offs in resource allocation have been widely stated as the means by which the honesty of ornamental traits is maintained, but an alternative to this resource trade-off hypothesis is that production of ornamentation is linked to the biochemical efficiency of vital cellular processes. Carotenoids are antioxidants, potentially tying carotenoid-based coloration to the oxidative state of an organism, and some carotenoids are also precursors for vitamin A, which regulates numerous cellular processes. We present a biochemical model for regulation of ornamental coloration based on interdependencies of carotenoid and retinoid biochemistry. We propose that vitamin A regulatory mechanisms, redox systems, and carotenoid pigmentation pathways link carotenoid coloration to oxidative state and to a host of important aspects of performance, such as immune function. The activity of β-carotene ketolase, which catalyzes the oxidation of yellow carotenoids into red carotenoids, is responsive to the states of vitamin A pools and redox systems such that coloration is a direct reflection of the physiological state of an animal. According to the vitamin A-redox hypothesis, feather coloration is associated with a range of performance measures because performance emerges from functionality of the same basic cellular processes that regulate pigmentation. We present the vitamin A-redox hypothesis as a testable alternative hypothesis to the resource trade-off hypothesis for the maintenance of honesty of carotenoid pigmentation.
Carotenoids are a large group of more than 600 different biochemicals synthesized by bacteria, fungi, algae and plants. Higher animals obtain these biologically active pigments in the diet, and they are subsequently used in diverse bodily functions. They are disproportionately common components of the color of animal signals such as those used in sexual communication, signaling between offspring and their parents and in warning colors. Carotenoids also play important roles in various aspects of immune function and detoxification, and a trade-off between signaling and these physiological functions has been hypothesized. They may either signal foraging efficiency, immunocompetence or anti-oxidative potential of signalers. Carotenoids are usually limiting the maximum possible expression of a signal since supplementation experiments have commonly produced more exaggerated signals. There is considerable evidence supporting the prediction that parasites reduce the expression of carotenoid-based signals, and that such signals reliably reflect the ability of the signaler to produce a strong immune response. There is also some evidence consistent with the hypothesis that signals may reflect the anti-oxidant potential of signalers. If carotenoids commonly have important physiological functions among captive and free-living organisms, we hypothesize several ways in which this should affect the design of animal breeding programs and conservation programs involving captive breeding.
Carotenoid pigments produce the ornamental red, orange, and yellow integ~ umentary coloration of many species of animals. Among individuals of a population, the hue and saturation of carotenoid-based ornaments can be extremely variable, and studies of fish and birds have shown that females generally prefer males that display the most saturated and reddest coloration. Consequently, there has been a great deal of interest in determining the proximate factors that affect individual expression of carotenoid-based pigmentation. Parasites might affect production of ornamental coloration, and the Hamilton-Zuk hypoth-esis proposes that parasitized males will show decreased expression of the secondary sexual traits preferred by females. We found that captive male House Finches (Carpodacus mexicanus) experimentally infected with Isospora spp. (coccidians) and / or Mycoplasma gallisepticum pro-duced carotenoid-based plumage coloration that was significantly less red and less saturated than that of noninfected males. These observations validate a necessary condition of the Hamilton-Zuk hypothesis, but heritable resistance to the pathogens we examined remains to be demonstrated. HAMILTON AND ZUK (1982) proposed that secondary sexual characteristics evolved be-cause they serve as reliable indicators of heri-table resistance to parasites and disease. Ac-cording to their hypothesis, only resistant males with low parasite loads can produce the most exaggerated and costly sexual ornamen-tation. Males with high parasite loads show re-duced expression of their sexual ornaments. Consequently, by choosing to mate with a high-ly ornamented male, a female receives benefits for her offspring in the form of genes for par-asite resistance.
Interest in animal carotenoids, especially in birds, has exploded in recent years, and so too have the methods employed to
investigate the nature and function of these pigments. Perhaps the most easily and commonly performed procedure in this work
has been the determination of carotenoid concentration from avian plasma. Over the past 20years of research on avian carotenoids,
numerous methods have been used to extract carotenoids from bird plasma, all of which have differed in several important parameters
(e.g., number and types of solvents used, degree of mixing/centrifugation). However, to date, no study has systematically
compared these methods to determine if any of them are more effective than others for recovering any or all types of carotenoids
present. We undertook such an investigation on plasma samples from two bird species (house finch, Carpodacus mexicanus, and mallard, Anas platyrhynchos) using five of the most commonly employed methods for extracting carotenoids from avian plasma: (1) acetone-only, (2) methanol-only,
(3) ethanol-only, (4) ethanol + hexane, and (5) ethanol + tert butyl methyl ether. We also manipulated the amount of time that extracts were centrifuged, which has varied tremendously
in previous studies, to evaluate its importance on carotenoid recovery. We found that all methods equally recovered the polar
xanthophylls (lutein and zeaxanthin), but that the methanol-only procedure poorly recovered non-polar carotenoids (less β-carotene
in both species and less β-cryptoxanthin in house finches) compared to the other methods. These results suggest that the data
accumulated to date on xanthophyll plasma carotenoids in birds should be comparable across studies and species despite the
different chemical extraction methods used. However, care should be taken to use relatively strong organic solvents for fully
recovering non-polar carotenoids. We also found no effect of centrifugation duration (1 vs. 10min at 10,000rpm) on carotenoid
recoveries, demonstrating that researchers can save considerable time by centrifuging for a much shorter time period than
is typically used.
A direct negative link between human health and urban pollution levels generated by increased internal levels of oxyradicals is well established. The impact of urban environment on the physiology of wild birds is however, poorly investigated. Here we compare oxidative damage (i.e., lipid peroxidation, measured as TBARS) and different antioxidant enzymes (glutathione reductase (GR), glutathione-S-transferase (GST), and catalase (CAT)) in lungs of urban and rural great tits, Parus major. In addition, we investigated enzymatic (i.e., CAT) and non-enzymatic (i.e., carotenoids) antioxidant levels in liver tissue. There was no significant difference in lipid peroxidation in lungs between the environments. Among the antioxidant enzymes measured in lungs, only CAT showed a tendency towards increased activity in the urban environment. In contrast, CAT in livers was highly non-significant. However, there was a significantly higher concentration of dietary carotenoids (i.e., lutein (Lut) and zeaxanthin (Zx)) in urban males, along with a sex-specific difference in composition (Lut:Zx ratio) between the environments. Taken together, these results suggest that great tit lungs and livers do not seem to be negatively affected, regarding oxidative stress, by living in an urban environment.
Many sexually selected traits are thought to be costly to produce, which ensures that they communicate information honestly to conspecifics. Carotenoid pigmentation is classically considered as a costly sexual signal in many fish and birds. It is often argued that carotenoid colours are ‘condition dependent’, with an individual's nutritional or health state directly determining trait expression. However, few studies have investigated precisely how a compromised nutritional state affects an animal's capacity to develop these sexually attractive colours. Here, we studied the effect of food restriction on the ability of male American goldfinches to physiologically process carotenoids during the period of feather growth. We used high-performance liquid-chromatography to determine the types and amounts of carotenoids circulating in blood during moult as well as in newly grown colourful feathers. We show that nutritional deprivation affects the degree to which male goldfinches transport carotenoids through the bloodstream. Food-restricted males circulated significantly less blood carotenoids than controls. They also incorporated less carotenoids into feathers and grew less colourful plumage, but the decrease in plumage carotenoids did not significantly exceed the depressed amounts already present in blood. These results suggest that the means by which these yellow-coloured passerines either extract carotenoids from food (e.g. via lipoidal micelles) or transport them through blood (e.g. via lipoproteins) are more sensitive to changes in nutritional/energy state than are the mechanisms for metabolizing dietary pigments or depositing metabolites into feathers.
The extent to which pathogens maintain the extraordinary polymorphism at vertebrate Major Histocompatibility Complex (MHC) genes via balancing selection has intrigued evolutionary biologists for over half a century, but direct tests remain challenging. Here we examine whether a well-characterized epidemic of Mycoplasmal conjunctivitis resulted in balancing selection on class II MHC in a wild songbird host, the house finch (Carpodacus mexicanus). First, we confirmed the potential for pathogen-mediated balancing selection by experimentally demonstrating that house finches with intermediate to high multi-locus MHC diversity are more resistant to challenge with Mycoplasma gallisepticum. Second, we documented sequence and diversity-based signatures of pathogen-mediated balancing selection at class II MHC in exposed host populations that were absent in unexposed, control populations across an equivalent time period. Multi-locus MHC diversity significantly increased in exposed host populations following the epidemic despite initial compromised diversity levels from a recent introduction bottleneck in the exposed host range. We did not observe equivalent changes in allelic diversity or heterozygosity across eight neutral microsatellite loci, suggesting that the observations reflect selection rather than neutral demographic processes. Our results indicate that a virulent pathogen can exert sufficient balancing selection on class II MHC to rescue compromised levels of genetic variation for host resistance in a recently bottlenecked population. These results provide evidence for Haldane's long-standing hypothesis that pathogens directly contribute to the maintenance of the tremendous levels of genetic variation detected in natural populations of vertebrates.
For many bird species, vision is the primary sensory modality used to locate and assess food items. The health and spectral sensitivities of the avian visual system are influenced by diet-derived carotenoid pigments that accumulate in the retina. Among wild House Finches (Carpodacus mexicanus), we have found that retinal carotenoid accumulation varies significantly among individuals and is related to dietary carotenoid intake. If diet-induced changes in retinal carotenoid accumulation alter spectral sensitivity, then they have the potential to affect visually mediated foraging performance.
In two experiments, we measured foraging performance of house finches with dietarily manipulated retinal carotenoid levels. We tested each bird's ability to extract visually contrasting food items from a matrix of inedible distracters under high-contrast (full) and dimmer low-contrast (red-filtered) lighting conditions. In experiment one, zeaxanthin-supplemented birds had significantly increased retinal carotenoid levels, but declined in foraging performance in the high-contrast condition relative to astaxanthin-supplemented birds that showed no change in retinal carotenoid accumulation. In experiments one and two combined, we found that retinal carotenoid concentrations predicted relative foraging performance in the low- vs. high-contrast light conditions in a curvilinear pattern. Performance was positively correlated with retinal carotenoid accumulation among birds with low to medium levels of accumulation (∼0.5-1.5 µg/retina), but declined among birds with very high levels (>2.0 µg/retina).
Our results suggest that carotenoid-mediated spectral filtering enhances color discrimination, but that this improvement is traded off against a reduction in sensitivity that can compromise visual discrimination. Thus, retinal carotenoid levels may be optimized to meet the visual demands of specific behavioral tasks and light environments.
The grey partridge is an important game bird in Europe that has declined considerably over the last decades. The production and release of farm-bred birds can be threatened by infectious agents. The objective of this study was to describe the outbreak, pathology, and blood and tissue biochemical responses in a flock of grey partridges naturally infected with Mycoplasma gallisepticum.
Morbidity and mortality rates were 100% and 60%, respectively. Necropsy revealed an accumulation of caseous exudate within the infraorbital sinuses, tracheitis, pneumonia and airsacculitis. There were significant increases in activities of lactate dehydrogenase, creatine kinase and amylase, and levels of total protein and glucose in Mycoplasma-infected birds when compared to control. Catalase showed significantly lower activity in the heart, lungs, liver and gonads of Mycoplasma-infected birds. Glutathione-S-transferase activity was elevated in the eye and the associated infraorbital sinus and kidneys, and decreased in the liver. Decreased levels of reduced glutathione were found in the heart, kidneys, liver and gonads. The activity of glutathione reductase was lower only in the lungs. Compared to healthy birds, mycoplasmosis in the grey partridge caused significant differences in the level of lipid peroxidation in lungs and plasma (p < 0.05), while the ferric reducing antioxidant power was lower in the heart and kidneys (p < 0.01). Significant correlations among responses of the antioxidant parameters were found namely in the heart, lungs, spleen, liver and plasma. There were also numerous significant inter-tissue correlations of all the studied antioxidant parameters.
The present study demonstrates the high susceptibility of grey partridges to natural infection by M. gallisepticum, the severity of the disease based on histopathology, and the modulation of blood chemical profiles and oxidative stress-associated parameters in the avian hosts, thus enhancing the understanding of the pathogenesis of mycoplasmosis in birds. Moreover, the reported reference values can be useful for the evaluation of the state of health in grey partridges.
Wild organisms are under increasing pressure to adapt rapidly to environmental changes. Predicting the impact of these changes on natural populations requires an understanding of the speed with which adaptive phenotypes can arise and spread, as well as of the underlying mechanisms. However, our understanding of these parameters is poor in natural populations. Here we use experimental and molecular approaches to investigate the recent emergence of resistance in eastern populations of North American house finches (Carpodacus mexicanus) to Mycoplasma galliseptum (MG), a severe conjunctivitis-causing bacterium. Two weeks following an experimental infection that took place in 2007, finches from eastern US populations with a 12-y history of exposure to MG harbored 33% lower MG loads in their conjunctivae than finches from western US populations with no prior exposure to MG. Using a cDNA microarray, we show that this phenotypic difference in resistance was associated with differences in splenic gene expression, with finches from the exposed populations up-regulating immune genes postinfection and those from the unexposed populations generally down-regulating them. The expression response of western US birds to experimental infection in 2007 was more similar to that of the eastern US birds studied in 2000, 7 y earlier in the epizootic, than to that of eastern birds in 2007. These results support the hypothesis that resistance has evolved by natural selection in the exposed populations over the 12 y of the epizootic. We hypothesize that host resistance arose and spread from standing genetic variation in the eastern US and highlight that natural selection can lead to rapid phenotypic evolution in populations when acting on such variation.
Carotenoid pigments can directly enhance the immune responses of vertebrates, and they are used by many animals to create ornamental color displays. It has been hypothesized that these two functions of carotenoid pigments are linked: animals must trade off use of carotenoid pigments for immune function versus ornamental display. We tested two key predictions of this hypothesis with captive American goldfinches, Carduelis tristis, a species with extensive carotenoid-based plumage coloration. First, we tested whether the immune systems of male goldfinches are carotenoid limited 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 bill color but not on immunocompetence. We compared the cell-mediated and humoral immune responses and the course of disease after infection for males in the different treatments. We observed no significant effect of the carotenoid content of diet on immune response or disease resistance. Second, we tested whether there was a positive relationship between immune function and expression of ornamental coloration by comparing both the pre- and posttreatment plumage coloration of males to their immune responses. We failed to find the predicted trade-off between ornament display and immune function. These findings do not support the hypothesis that songbirds with extensive carotenoid-based plumage displays trade off the use of carotenoids for ornamentation versus immune function. Copyright 2003.
Carotenoid and melanin pigments in the plumage of birds are hypothesized to be sensitive to oxidative stress. We manipulated oxidative status of captive greenfinches (Carduelis chloris L.) by the administration of buthionine sulfoximine (BSO), a selective inhibitor of the synthesis of glutathione (GSH), an intracellular antioxidant. Half of the birds in the treated group, as well as in the control group, also received dietary carotenoid (lutein) supplementation. BSO treatment reduced erythrocyte GSH levels and caused oxidative damage as indicated by the increased concentration of plasma malondialdehyde (MDA), an end product of lipid peroxidation. BSO treatment also reduced the brightness (i.e. increased blackness) of the tips of tail feathers grown during the experiment. These results show that a low systemic GSH level is required for development of eumelanin plumage coloration and that such a low GSH level is also potentially dangerous for the organism. Carotenoid supplementation increased plasma carotenoid levels and chroma of the yellow parts of the feathers grown during the experiment. However, carotenoid supplementation did not reduce plasma MDA levels. Manipulation of GSH did not affect plasma carotenoids or carotenoid-based plumage coloration. These findings argue against the antioxidant function of lutein in vivo and carotenoid signaling of antioxidant status.
Carotenoid pigments produce yellow, orange, and red integumentary color displays that can serve as reliable signals of health and condition. In many birds and fish, individuals gain competitive or mating advantages by ingesting and utilizing large quantities of carotenoid pigments. Carotenoid pigments serve as antioxidants, performing important functions as free-radical scavengers. The beneficial effects of carotenoid pigments are well documented, but rarely have researchers considered potential detrimental effects of high-level accumulation of carotenoids. We maintained American goldfinches (Carduelis tristis) on high- or low-carotenoid diets through molt and tested for damage to the liver and skeletal muscle. High intake of carotenoids had no measurable effect on liver enzymes but caused an increase in creatine kinase, an indicator of skeletal muscle breakdown, and a reduction in vertical flight performance, a measure of skeletal muscle integrity. The detrimental effects of high-level carotenoid accumulation were approximately equivalent to the negative effects of removing carotenoids from the diet. The adverse effects observed in this study have important implications for theories of the function and evolution of colorful plumage.
The costs of developing, maintaining, and activating the immune system have been cited as an important force shaping life-history evolution in animals. Immunological defenses require energy, nutrients and time that might otherwise be devoted to other life-history traits like sexual displays or reproduction. Carotenoid pigments in animals provide a unique opportunity to track the costs of immune activation, because they are diet-derived, modulate the immune system, and are used to develop colorful signals of quality. Carotenoids also accumulate in the retinas of birds, where they tune spectral sensitivity and provide photoprotection. If carotenoid accumulation in the retina follows the patterns of other tissues, then immune activation may deplete retinal carotenoid levels and impact visual health and function. To test this hypothesis, we challenged molting wild-caught captive house finches (Carpodacus mexicanus) with weekly injections of lipopolysaccharide (LPS) and phytohaemagglutinin (PHA) over the course of 8 weeks. Immunostimulated adult males and females produced significant antibody responses and molted more slowly than uninjected control birds. After 8 weeks, immune-challenged birds had significantly lower levels of specific retinal carotenoid types (galloxanthin and zeaxanthin), but there were no significant differences in the plasma, liver or feather carotenoid levels between the treatment groups. These results indicate that immune-system activation can specifically deplete retinal carotenoids, which may compromise visual health and performance and represent an additional somatic and behavioral cost of immunity.
Oxidative stress, the physiological condition whereby the production of reactive oxygen and nitrogen species overwhelms the capacity of antioxidant defences, causes damage to key bio-molecules. It has been implicated in many diseases, and is proposed as a reliable currency in the trade-off between individual health and ornamentation. Whether oxidative stress mediates the expression of carotenoid-based signals, which are among the commonest signals of many birds, fish and reptiles, remains controversial. In the present study, we explored interactions between parasites, oxidative stress and the carotenoid-based ornamentation of red grouse Lagopus lagopus scoticus. We tested whether removing nematode parasites influenced both oxidative balance (levels of oxidative damage and circulating antioxidant defences) and carotenoid-based ornamentation. At the treatment group level, parasite purging enhanced the size and colouration of ornaments but did not significantly affect circulating carotenoids, antioxidant defences or oxidative damage. However, relative changes in these traits among individuals indicated that males with a greater number of parasites prior to treatment (parasite purging) showed a greater increase in the levels of circulating carotenoids and antioxidants, and a greater decrease in oxidative damage, than those with initially fewer parasites. At the individual level, a greater increase in carotenoid pigmentation was associated with a greater reduction in oxidative damage. Therefore, an individual's ability to express a carotenoid-based ornament appeared to be linked to its current oxidative balance and susceptibility to oxidative stress. Our experimental results suggest that oxidative stress can mediate the impact of parasites on carotenoid-based signals, and we discuss possible mechanisms linking carotenoid-based ornaments to oxidative stress.
Avian vision is highly developed, with bird retinas containing rod and double-cone photoreceptors, plus four classes of single cones subserving tetrachromatic colour vision. Cones contain an oil droplet, rich in carotenoid pigments (except VS/ultraviolet-sensitive cones), that acts as a filter, substantially modifying light detected by the photoreceptor. Using dietary manipulations, we tested the effects of carotenoid availability on oil droplet absorbance properties in two species: Platycercus elegans and Taeniopygia guttata. Using microspectrophotometry, we determined whether manipulations affected oil droplet carotenoid concentration and whether changes would alter colour discrimination ability. In both species, increases in carotenoid concentration were found in carotenoid-supplemented birds, but only in the double cones. Magnitudes of effects of manipulations were often dependent on retinal location. The study provides, to our knowledge, the first experimental evidence of dietary intake over a short time period affecting carotenoid concentration of retinal oil droplets. Moreover, the allocation of carotenoids to the retina by both species is such that the change potentially preserves the spectral tuning of colour vision. Our study generates new insights into retinal regulation of carotenoid concentration of oil droplets, an area about which very little is known, with implications for our understanding of trade-offs in carotenoid allocation in birds.
Like males of many bird species, male House Finches (Carpodacus mexicanus) have patches of feathers with ornamental coloration that are due to carotenoid pigments. Within populations, male House Finches vary in expression of ornamental coloration from pale yellow to bright red, which previous research suggested was the result of variation in types and amounts of carotenoid pigments deposited in feathers. Here we used improved analytical techniques to describe types and amounts of carotenoid pigments present in that plumage. We then used those data to make comparisons of carotenoid composition of feathers of male House Finches at three levels: among individual males with different plumage hue and saturation, between age groups of males from the same population, and between males from two subspecies that differ in extent of ventral carotenoid pigmentation (patch size): large-patched C. m. frontalis from coastal California and small-patched C. m. griscomi from Guerrero, Mexico. In all age groups and populations, the ornamental plumage coloration of male House Finches resulted from the same 13 carotenoid pigments, with 3-hydroxy echinenone and lutein being the most abundant carotenoid pigments. The composition of carotenoids in feathers suggested that House Finches are capable of metabolic transformation of dietary forms of carotenoids. The hue of male plumage depended on component carotenoids, their relative concentrations, and total concentration of all carotenoids. Most 4-keto (red) carotenoids were positively correlated with plumage redness, and most yellow carotenoid pigments were negatively associated with plumage redness, although the strength of the relationship for specific carotenoid pigments varied among age groups and subspecies. Using age and subspecies as factors and concentration of each component carotenoid as dependent variables in a MANOVA, we found a distinctive pigment profile for each age group within each subspecies. Among frontalis males, hatch-year birds did not differ from adults in mean plumage hue, but they had a significantly lower proportion of red pigments in their plumage, and significantly lower levels of the red piments adonirubin and astaxanthin, but significantly higher levels of the yellow pigment zeaxanthin, than adult males. Among griscomi males, hatch-year birds differed from adults in plumage hue but not significantly in pigment composition, though in general their feathers had lower concentrations of red pigments and higher concentrations of yellow pigments than adult males. Both adult and hatch-year frontalis males differed from griscomi males in having significantly higher levels of most yellow carotenoid pigments and significantly lower levels of most red carotenoid pigments. Variation in pigment profiles of subspecies and age classes may reflect differences among the groups in carotenoid metabolism, in dietary access to carotenoids, or in exposure to environmental factors, such as parasites, that may affect pigmentation.
There is widespread interest in the roles that carotenoids play as yolk and shank pigments, antioxidants, and immune-system regulators in chickens, but nothing is known of such functions in the wild ancestors of chickens—the Red Junglefowl (Gallus gallus). We manipulated carotenoid access in the diet of captive male and female Red Junglefowl to investigate its effects on the coloration of the red comb and buff-brown legs and beak as well as on several indices of immunocompetence. Comb, leg, and beak did not differ in coloration between control and carotenoid-supplemented groups; in fact, biochemical analyses showed that, unlike in chickens, leg and beak tissue contained no carotenoids. Carotenoids showed variable effects on immunological performance, boosting the potency of whole blood in males to kill bacterial colonies, while inhibiting the ability of macrophages to phagocytize bacterial cells and having no significant effect on the accumulation of haptoglobin—an acute-phase protein whose production was induced by a simulated infectious challenge with lipopolysaccharide. These results bring into question interpretations of the evolutionary significance of carotenoid-based and sexually dichromatic shank coloration in domestic chickens, which was apparently derived through artificial selection, and suggest that carotenoids can exert different, mechanism-specific actions on the many lines of immune defense in birds.
Carotenoides, Inmunidad y Coloración Integumentaria en Gallus gallus
I studied female mate preference in relation to male plumage coloration in the House Finch (Carpodacus mexicanus). Males from an introduced eastern U.S. population averaged significantly brighter in plumage coloration, and males from an introduced Hawaiian population significantly drabber, than males from the parent population in California. Males from Guerrero, Mexico displayed a mean coloration similar to that of males from the eastern U.S., but with a much reduced color-patch size. In controlled feeding experiments, I found that male house finches from all populations possess the same potential to display bright or drab plumage and that variation in plumage coloration (but not patch size) reflects the type and quantity of carotenoid pigments ingested by individuals during molt. In the wild, male plumage coloration was correlated with parental investment and viability. In laboratory and field experiments, females from all populations chose the most brightly colored, largest patched males available, regardless of the appearance of males in their population. A phylogenetic analysis indicated that the small patch size displayed by Mexican House Finches is derived from a larger patch size, and indirect evidence suggests that small-patched males may have access to smaller quantities of carotenoids than large-patched males. These results support the hypothesis that plumage coloration evolved via intersexual selection as an indicator of male quality. In addition, the lack of conformity between male appearance and female preference among populations provides evidence against species isolation models and runaway sexual selection models for the evolution of male display traits.
There is widespread interest in the roles that carotenoids play as yolk and shank pigments, antioxidants, and immune-system regulators in chickens, but nothing is known of such functions in the wild ancestors of chickens-the Red Junglefowl (Gallus gallus). We manipulated carotenoid access in the diet of captive male and female Red Junglefowl to investigate its effects on the coloration of the red comb and buff-brown legs and beak as well as on several indices of immuno-competence. Comb, leg, and beak did not differ in coloration between control and carotenoid-supplemented groups; in fact, biochemical analyses showed that, unlike in chickens, leg and beak tissue contained no carotenoids. Carotenoids showed variable effects on immunological performance, boosting the potency of whole blood in males to kill bacterial colonies, while inhibiting the ability of macrophages to phagocytize bacterial cells and having no significant effect on the accumulation of haptoglobin-an acute-phase protein whose production was induced by a simulated infectious challenge with lipopolysaccharide. These results bring into question interpretations of the evolutionary significance of carotenoid-based and sexually dichromatic shank coloration in domestic chickens, which was apparently derived through artificial selection, and suggest that carotenoids can exert different, mechanism-specific actions on the many lines of immune defense in birds. /// Existe un amplio interés en el papel que tienen los carotenoides como pigmentos de la yema y parte inferior de las patas, así como también en antioxidantes y reguladores del sistema inmunológico en gallinas, pero nada se sabe sobre estas funciones en el ancestro silvestre de las gallinas, Gallus gallus. Manipulamos el acceso a carotenoides en la dieta de machos y hembras en cautiverio de G. gallus para investigar los effectos sobre la coloración roja de la cresta y coloración café de las patas y el pico, como así también en varios índices de inmuno-competencia. La cresta, las patas y el pico no difirieron en coloración entre el grupo control y el suplementado con carotenoides. De hecho, los análisis bioquímicos mostraron que, contrariamente a lo observado en las gallinas, los tejidos de las patas y el pico no contienen carotenoides. Los carotenoides mostraron efectos variados sobre el desempeño inmunológico. En los machos, impulsaron el potencial del tejido sanguíneo para matar colonias bacterianas, mientras que inhibieron la habilidad de los macrófagos de fagocitar células bacterianas y no tuvieron un efecto significativo sobre la acumulación de haptoglobina-una proteína de fase aguda cuya producción fue inducida por una infección simulada con lipo-polisacáridos. Estos resultados cuestionan las interpretaciones del significado evolutivo de la coloración con carotenoides y de la coloración di-cromática sexual de la parte inferior de las patas en gallinas domesticas, la cual aparentemente derivó a partir de selección artificial y sugiere que los carotenoides pueden ejercer acciones mecánicas específicas y diferentes sobre las variadas líneas de defensa inmunológica en aves.
We infected male guppies Poecilia reticulata with a naturally occurring monogenean parasite, Gyrodactylus turnbulli, in order to examine effects of parasitism on the expression of color patterns and on attractiveness to females. The color of carotenoid spots and ability to attract females were compared between experimentally infected fish and a control group of their fullsib brothers, which had identical color patterns and were treated identically except for actual exposure to parasites. The orange spots of males that had been infected for 9 days followed by treatment with medication to remove parasites became significandy paler and less saturated. Control males (also treated widi medication) showed no significant changes in their orange spots. Females in a divided aquarium choice-apparatus showed no preference between control and infection-treatment males initially, but showed significant discrimination after the infectiondisinfection treatment. Females spent less time near males that had been infected and responded to a smaller fraction of their courtship displays relative to control males. There were slight differences in courting rates of males between treatments. Parasitic infection appears to reduce the degree of expression of carotenoid colors in guppies, and females are able to discriminate against recently infected males, probably on the basis of the color change. By avoiding infected males, females may be able to avoid becoming infected themselves, or they may be able to identify mates based on "good genes" for parasite resistance diat can be passed on to their offspring.
Previous studies have shown that house finch field isolates of Mycoplasma gallisepticum (MG) vary in virulence and ability to induce an antibody response. After experimental inoculation, MG causes persistent, severe disease in a subset of individuals. In this study, we further characterized MG infection using five field isolates, with an emphasis on chronically diseased birds. After experimental inoculation of house finches, MG load was measured by quantitative PCR and anti-MG antibody responses were measured by ELISAs. Birds with chronic disease had significantly higher pathogen loads and antibody responses than did birds without chronic disease. Using a monoclonal antibody (MAb86) specific for a variant of the MG VlhA adhesin and immunodominant surface protein, we show that VlhA expression differs among MG isolates in this study, and that in vivo VlhA changes occur in house finches infected with MG. Overall, our results suggest that chronic MG disease has a strong pathogen-mediated component.
Existe un amplio interés en el papel que tienen los carotenoides como pigmentos de la yema y parte inferior de las patas, así como también en antioxidantes y reguladores del sistema inmunológico en gallinas, pero nada se sabe sobre estas funciones en el ancestro silvestre de las gallinas, Gallus gallus. Manipulamos el acceso a carotenoides en la dieta de machos y hembras en cautiverio de G. gallus para investigar los efectos sobre la coloración roja de la cresta y coloración café de las patas y el pico, como así también en varios índices de inmuno-competencia. La cresta, las patas y el pico no difirieron en coloración entre el grupo control y el suplementado con carotenoides. De hecho, los análisis bioquímicos mostraron que, contrariamente a lo observado en las gallinas, los tejidos de las patas y el pico no contienen carotenoides. Los carotenoides mostraron efectos variados sobre el desempeño inmunológico. En los machos, impulsaron el potencial del tejido sanguíneo para matar colonias bacterianas, mientras que inhibieron la habilidad de los macrófagos de fagocitar células bacterianas y no tuvieron un efecto significativo sobre la acumulación de haptoglobina—una proteína de fase aguda cuya producción fue inducida por una infección simulada con lipo-polisacáridos. Estos resultados cuestionan las interpretaciones del significado evolutivo de la coloración con carotenoides y de la coloración di-cromática sexual de la parte inferior de las patas en gallinas domesticas, la cual aparentemente derivó a partir de selección artificial y sugiere que los carotenoides pueden ejercer acciones mecánicas específicas y diferentes sobre las variadas líneas de defensa inmunológica en aves.
Male House Finches ( Carpodacus mexicanus ) colour their sexually selected plumage with carotenoid pigments, and there has been much interest in the factors that affect their ability to become bright red rather than drab yellow.
There is good support for the notions that health, nutritional condition and total carotenoid intake influence colour expression, but there are also suggestions that acquiring particular types of carotenoids from the diet may be important for developing red plumage.
We used high‐performance liquid chromatography (HPLC) to analyse the types and amounts of endogenous (in plasma and liver) and integumentary (in newly grown feathers) carotenoids in a wild, native population of moulting male and female House Finches from the south‐western United States to determine the carotenoid‐accumulation strategies for becoming optimally colourful.
Four plant carotenoids – lutein, zeaxanthin, β‐cryptoxanthin and β‐carotene – were detected in plasma and liver. However, as was found previously, 11 carotenoids were observed in colourful plumage, with xanthophylls (e.g. lutein, dehydrolutein) predominant in yellow feathers and ketocarotenoids (e.g. adonirubin, 3‐hydroxy‐echinenone) in red feathers. This indicates endogenous modification of ingested carotenoids.
Birds that accumulated more of one type of carotenoid in plasma and liver did not necessarily accumulate more of all other types, suggesting that individuals are not employing a simple ‘more is better’ strategy for coloration. Instead, when forward stepwise regression was used to examine the ability of individual types of carotenoids in plasma and liver to explain variation in red plumage pigments and plumage redness, we found that the lone variable remaining in all models was β‐cryptoxanthin concentration.
This supports the idea that, unlike some other songbirds (e.g. yellow Carduelis finches), there is a specialized biochemical strategy that male House Finches follow to become red and most sexually attractive – to accumulate as much β‐cryptoxanthin in the body as possible. β‐Cryptoxanthin is a less common dietary carotenoid than the typical xanthophylls and carotenes in grains and fruits and may be limited enough in the diet that, to become colourful, House Finches might adopt selective foraging strategies for the most β‐cryptoxanthin‐rich foods.
Summary 1. Studies of visual ecology generally focus on the tuning of the eye to the spectral environment. However, the environment may also shape vision if the availability of nutrients or other extrinsic stressors impact eye structure or function. 2. Carotenoids are diet-derived pigments that accumulate in the retinas of birds, where they provide photoprotection and tune colour vision. In domesticated species, carotenoid accumulation in retina is dependent on dietary intake, but little is known about the variability in or control of these pigments in the eyes of wild animals. 3. Carotenoids are also deposited in the integument of many animals, where they generate colourful sexually selected displays that communicate information about individual health and nutrition. We hypothesize that retinal carotenoid accumulation is subject to the same health and nutritional constraints as the use of carotenoids in colour signals. 4. As a first test of this hypothesis, we examined retinal carotenoid accumulation in relation to season, sex, body condition, circulating plasma carotenoid concentrations, and plumage colouration in a free ranging population of house finches ( Carpodacus mexicanus ) - a model species for studies of carotenoid ecology. 5. Retinal carotenoid accumulation varied considerably among individuals and differed significantly among seasons, with the highest levels observed in late fall and winter. Body condition and plasma zeaxanthin levels were significantly positively correlated with retinal carotenoid accumulation, but retinal carotenoid concentrations did not differ between the sexes. Plumage redness covaried positively with retinal carotenoid concentration as well, though this relationship was no longer significant when accounting for seasonal variation. 6. Our results, although correlational, do suggest that retinal carotenoid accumulation is a variable trait that may be influenced by environmental and physiological conditions, raising the intriguing possibility that plumage colouration and colour vision could be linked through a common biochemical mechanism.
For decades, carotenoids have attracted attention for their roles as vitamin-A precursors, antioxidants, and immunostimulants, but we still understand very little about the metabolic processes that accompany these compounds. Animals like birds use carotenoids to color their feathers and bare parts to become sexually attractive. They commonly metabolically derive their body colorants from dietary sources of carotenoids, but the sites of pigment metabolism remain unidentified. Here I test the hypothesis that songbirds manufacture their colorful feather and beak carotenoids directly at these tissues. I offer two lines of evidence to support this idea: (1) in a study of 11 colorful species from three passerine families, metabolically derived feather and beak carotenoids were found neither in the liver (a purported site of carotenoid metabolism), nor in the bloodstream (the means by which metabolites would be transported to colorful tissues from anywhere else in the body) at the time when pigments were being deposited into keratinized tissue, and (2) in a more detailed study of pigmentation in the American goldfinch Carduelis tristis, carotenoids sampled from the lipid fractions of maturing feather follicles yielded a mix of dietary and synthetic carotenoids, suggesting that this is the metabolically active site for feather-pigment production. This fresh perspective on carotenoid metabolism in animals should aid our efforts to characterize the responsible enzymes and to better understand the localized biological functions of these pigments.
Sexual ornaments might indicate better condition, fewer parasites or a greater immune responsiveness. Carotenoid-based ornaments are common sexual signals of birds and often influence mate choice. Skin or beaks pigmented by carotenoids can change colour rapidly, and could be particularly useful as honest indicators of an individual's current condition and/or health. This is because carotenoids must be acquired through diet and/or allocation for ornamental coloration might be to the detriment of self-maintenance needs. Here, we investigated whether the carotenoid-based coloration of eye rings and beak of male red-legged partridges Alectoris rufa predicted condition (mass corrected for size), parasite load (more specifically infection by coccidia, a main avian intestinal parasite) or a greater immune responsiveness (swelling response to a plant lectin, phytohaemagluttinin, or PHA). Redness of beak and eye rings positively correlated with plasma carotenoid levels. Also, males in better condition had fewer coccidia, more circulating carotenoids and a greater swelling response to PHA. Carotenoid-based ornamentation predicted coccidia abundance and immune responsiveness (redder males had fewer coccidia and greater swelling response to PHA), but was only weakly positively related to condition. Thus, the carotenoid pigmentation of beak and eye rings reflected the current health status of individuals. Our results are consistent with the hypothesis that allocation trade-offs (carotenoid use for ornamentation versus parasite defence needs) might ensure reliable carotenoid-based signalling.
1. Ecological immunology and disease ecology are two relatively young disciplines that apply ecological approaches and principles to traditionally non-ecological fields. In both cases, an ecological perspective has allowed new insights to emerge by focusing attention on variation over space and time, and by emphasizing the role of the environment in shaping individual responses and the outcome of host-pathogen interactions. Here we review the growing conceptual interface between these two rapidly evolving fields.
2. Areas of synergy between ecological immunology and disease ecology aim to translate variation in within-host processes (e.g. immunity) into between-host dynamics (e.g. parasite transmission). Emerging areas of synergy include potential immune mechanisms that underlie host heterogeneity in disease susceptibility, teasing apart the effects of environmental factors such as seasonality and climate on host susceptibility and pathogen dynamics, and predicting the outcome of co-infection by functionally distinct groups of parasites that elicit different immune responses.
3. In some cases, practical limitations have constrained the merging of ideas in ecological immunology and disease ecology. We discuss several logistical challenges, including dissecting the relative roles of host exposure and susceptibility, establishing links between measures of immunity and pathogen resistance in wild populations, and incorporating relevant immune variation into prevailing disease ecology modeling frameworks.
4. Future work at the interface of these two fields should advance understanding of life-history theory, host-pathogen dynamics, and physiological ecology, and will also contribute to targeted approaches for wildlife health and zoonotic disease prevention.
Conditional handicap models of sexual selection predict that ornamentation should be positively associated with an individual's ability to withstand challenges to their health.
We assessed whether levels of carotenoid ornamentation were related to the probability of adult male Common Redpolls, Carduelis flammea , dying in a salmonellosis epidemic by comparing the ornamentation of surviving adult male redpolls to those found dead. Hosts suffering from salmonellosis shed bacteria in faeces, and new individuals are typically infected when they ingest faeces‐contaminated food.
The proportion of adult males in the sample of dead birds was significantly higher than in the sample of living birds.
Among adult males, probability of survival was significantly predicted by the expression of their carotenoid signals: brightly ornamented adult males were more likely to die in the epidemic.
A probable hypothesis for these results is that if carotenoid ornamentation in redpolls functions as a status badge of dominance, bright males would have had priority access to highly preferred, and contaminated, food patches.
If kept in a cage, the Redpoll (Carduelis flammea) replaces all the red feathers of its plumage by yellowish ones in the next moult. A number of male Redpolls were caught in winter and released into three open-air aviaries of different size, the largest measuring 21.5 × 17 m, the smallest 11.5 × 5.6 m. All Redpolls kept in the largest aviary moulted from red to red, but in the smallest one from red to yellowish. The other conditions (food, light, temperature, humidity) being equal in the three cases, it is concluded that the essential difference consists in the degree of movement-freedom. During the weeks of courtship-performance the flock of males kept in the large aviary made long circling flights, while in the smaller aviaries there was no space available for such an exercise.
Carotenoid-based sexual coloration has been hypothesised to be prevalent across many vertebrate taxa because it reliably reflects individual phenotypic quality in terms of foraging efficiency or health status due to the trade-off between signal colour and use of carotenoids for immune function and detoxification. We investigated the ventral, yellow coloration of breeding adult great tits (Parus major L.) in relation to sex, age, breeding habitat, local survival and infection status with respect to Haemoproteus blood parasites. The extent of plumage coloration (estimated as hue and lutein absorbance) was generally higher in rural than in urban birds. Males had higher values of hue than females. In both male and female yearlings, the plumage of unparasitised individuals had a greater hue of yellow than parasitised ones, while older males revealed the opposite pattern. The survival of infected yearlings was worse than that of uninfected yearlings, while the opposite was true for old breeders. Survivors had generally higher values of hue than non-survivors. These results are consistent with predictions of functional hypotheses, suggesting that carotenoid-based plumage coloration serves as a signal reflecting individual quality in terms of health status and local survival.
1.1. A study was made of the lipoprotein composition of blood plasma from the scarlet ibis (Eudocimus ruber), white ibis and a pink hybrid. Donor animals were obtained either from the delta of the Amazon River or from the National Zoo, Washington, D.C.2.2. It was found that the carotenoid composition of the plasma of the captive scarlet ibis differed from that of the wild bird.3.3. The carotenoid pigments which are characteristic for scarlet ibis were principally associated with the high-density lipoprotein fractions. Pigment half-life was of the order of 80–100 hr and consistent with the metabolism of high-density lipoproteins (HDL).4.4. Further fractionation of the HDL by disc electrophoresis indicated the presence of a component which appears to be a carotenoid carrier protein. Substantial amounts of this protein were present in the scarlet ibis whereas only traces could be detected in the white ibis.
Theories of animal signalling emphasize the importance of costliness—to be effective, signals must be dependable; to be dependable, signals must carry costs—and carotenoid-based signals are a favoured example. The traditional view that carotenoids are costly because they are scarce still carries weight. However, biomedical research has led to alternative views on costliness, mainly related to beneficial, but also to detrimental, effects of carotenoids. Recent improvements in our understanding of carotenoids suggest that the relative importance of these mechanisms will soon be determined, leading to a fresh outlook on cost-based signalling.
Carotenoid pigments accumulate in the retinas of many animals, including humans, where they play an important role in visual health and performance. Recently, birds have emerged as a model system for studying the mechanisms and functions of carotenoid accumulation in the retina. However, these studies have been limited to a small number of domesticated species, and the effects of dietary carotenoid access on retinal carotenoid accumulation have not been investigated in any wild animal species. The purpose of our studies was to examine how variation in dietary carotenoid types and levels affect retinal accumulation in house finches (Carpodacus mexicanus), a common and colorful North American songbird. We carried out three 8-week studies with wild-caught captive birds: (1) we tracked the rate of retinal carotenoid depletion, compared to other body tissues, on a very low-carotenoid diet, (2) we supplemented birds with two common dietary carotenoids (lutein + zeaxanthin) and measured the effect on retinal accumulation, and (3) we separately supplemented birds with high levels of zeaxanthin--an important dietary precursor for retinal carotenoids--or astaxanthin--a dominant retinal carotenoid not commonly found in the diet (i.e. a metabolic derivative). We found that carotenoids depleted slowly from the retina compared to other tissues, with a significant (~50%) decline observed only after 8 weeks on a very low-carotenoid diet. Supplementation with lutein + zeaxanthin or zeaxanthin alone significantly increased only retinal galloxanthin and ε-carotene levels, while other carotenoid types in the retina remained unaffected. Concentrations of retinal astaxanthin were unaffected by direct dietary supplementation with astaxanthin. These results suggest highly specific mechanisms of retinal carotenoid metabolism and accumulation, as well as differential rates of turnover among retinal carotenoid types, all of which have important implications for visual health maintenance and interventions.