Melanin coloration in New World orioles II: ancestral state reconstruction reveals lability in the use of carotenoids and phaeomelanins

Although many animals use carotenoids to produce bright yellow, orange, and red colors, an increasing number of studies have found that other pigments, such as melanins, may also be used to produce bright colors. Yet, almost nothing is known about the evolutionary history of this colorful melanin use. We used reflectance spectrometry to determine whether colors in New World orioles were predominantly due to carotenoids, colorful melanins, or a mixture of both. We then used ancestral state reconstruction to infer the directionality of any pigment changes and to test for phylogenetic signal. We found that three oriole taxa likely switched from carotenoid- to melanin-based colors. Several other oriole taxa apparently gained localized melanin coloration, or had coloration that seemed to be produced by a mixture of carotenoids and melanins. We also found little phylogenetic signal on the use of carotenoids or melanins to produce color. However, all pigment changes occurred within one of three major clades of the oriole genus, suggesting there may be signal at deeper phylogenetic levels. These repeated independent switches between carotenoid and melanin colors are surprising in light of the important signaling role that color pigments (especially carotenoids) are thought to play across a wide range of taxa.     

The influence of carotenoid acquisition and utilization on the maintenance of species-typical plumage pigmentation in male American goldfinches (Carduelis tristis) and northern cardinals (Cardinalis cardinalis).

Birds display a tremendous variety of carotenoid-based colors in their plumage, but the mechanisms underlying interspecific variability in carotenoid pigmentation remain poorly understood. Because vertebrates cannot synthesize carotenoids de novo, access to pigments in the diet is one proximate factor that may shape species differences in carotenoid-based plumage coloration. However, some birds metabolize ingested carotenoids and deposit pigments that differ in color from their dietary precursors, indicating that metabolic capabilities may also contribute to the diversity of plumage colors we see in nature. In this study, we investigated how the acquisition and utilization of carotenoids influence the maintenance of species-typical plumage pigmentation in male American goldfinches (Carduelis tristis) and northern cardinals (Cardinalis cardinalis). We supplemented the diet of captive goldfinches with red carotenoids to determine whether males, which are typically yellow in color, were capable of growing red plumage. We also deprived cardinals of red dietary pigments to determine whether they could manufacture red carotenoids from yellow precursors to grow species-typical red plumage. We found that American goldfinches were able to deposit novel pigments in their plumage and develop a striking orange appearance. Thus, dietary access to pigments plays a role in determining the degree to which goldfinches express carotenoid-based plumage coloration. We also found that northern cardinals grew pale red feathers in the absence of red dietary pigments, indicating that their ability to metabolize yellow carotenoids in the diet contributes to the bright red plumage that they display.     

Influence of Social Factors on Seasonal Variations in Plasma Testosterone Levels of Microcebus murinus

Blue tail coloration in hatchling skinks (Eumeces fasciatus and E. laticeps) appears to be an antipredatory adaptation that distracts attention away from the body to the tail. The tail itself serves as a decoy that may be autotomized as a final defense against capture. The effectiveness of intact tails in deflecting attacks from the body was 50% against scarlet kingsnakes in the experimental conditions used. Brightness rather than hue presumably accounts for the higher attack frequency on blue than black tails in this study, but the blue color may have evolved in response to avian predation. Repeated predation without ill effects by several predators allows rejection of the hypothesis that the blue tail is aposematic for the predators tested. The hypothesis that blue tails provide stimuli inhibiting aggression or predation by adult male conspecifics is untenable for E. laticeps because adult males readily eat intact hatchlings. Although this study provides no statistical evidence that blue tail coloration inhibits attack by female E. laticeps on hatchlings, the trend of predation rates on blue- and black-tailed hatchlings is in the direction predicted for inhibition.     

Basking Activity is Modulated by Health State but is Constrained by Conspicuousness to Predators in Male Spanish Terrapins

Aerial basking may have several benefits for freshwater turtles in addition to thermoregulation such as removing parasites from the skin, which would improve health state. However, basking outside of water may be risky because it may expose freshwater turtles to terrestrial predators. Here, we monitored the basking activity of male Spanish terrapins (Mauremys leprosa) in a wild population of the south‐western of the Iberian Peninsula. We also measured body size, health state parameters, parasite prevalence, and limb coloration of these individuals. We aimed to examine whether basking may improve health state of turtles. The results showed that male turtles with higher basking activity were those parasitized by Hepatozoon and that had lower total white blood cell (WBC). This might indicate that turtles in worse health condition increase their time spent basking to improve their immune system. In addition, because basking might be risky, we also expected that turtles with more conspicuous coloration should reduce their basking activity to avoid being detected by potential predators. We found that infected turtles, but not uninfected ones, that spent more time basking also had less bright coloration in limb stripes. Our study provides evidence that basking activity may improve health state of terrapins, but that color conspicuity may increase costs of basking, especially for parasitized individuals. Understanding the balance between the benefits and the costs of basking might be essential for the conservation of freshwater turtle populations.     

COARSE DARK PATTERNING FUNCTIONALLY CONSTRAINS ADAPTIVE SHIFTS FROM APOSEMATISM TO CRYPSIS IN STRAWBERRY POISON FROGS

Ecological specialization often requires tight coevolution of several traits, which may constrain future evolutionary pathways and make species more prone to extinction. Aposematism and crypsis represent two specialized adaptations to avoid predation. We tested whether the combined effects of color and pattern on prey conspicuousness functionally constrain or facilitate shifts between these two adaptations. We combined data from 17 natural populations of strawberry poison frogs, Oophaga pumilio with an experimental approach using digitalized images of frogs and chickens as predators. We show that bright coloration often co‐occurs with coarse patterning among the natural populations. Dull green frogs with coarse patterning are rare in nature but in the experiment they were as easily detected as bright red frogs suggesting that this trait combination represents a transient evolutionary state toward aposematism. Hence, a gain of either bright color or coarse patterning leads to conspicuousness, but a transition back to crypsis would be functionally constrained in populations with both bright color and coarse patterning by requiring simultaneous changes in two traits. Thus, populations (or species) signaling aposematism by conspicuous color should be less likely to face an evolutionary dead end and more likely to radiate than populations with both conspicuous color and coarse patterning.     

Contributions of pterin and carotenoid pigments to dewlap coloration in two anole species

Animals can acquire bright coloration using a variety of pigmentary and microstructural mechanisms. Reptiles and amphibians are known to use two types of pigments - pterins and carotenoids - to generate their spectrum of colorful red, orange, and yellow hues. Because both pigment classes can confer all of these hues, the relative importance of pterins versus carotenoids in creating these different colors is not always apparent. We studied the carotenoid and pterin content of red and yellow dewlap regions in two neotropical anole species - the brown anole (Norops sagrei) and the ground anole (N. humilis). Pterins (likely drosopterins) and carotenoids (likely xanthophylls) were present in all tissues from all individuals. Pterins were more enriched in the lateral (red) region, and carotenoids more enriched in the midline (yellow) region in N. humilis, but pterins and carotenoids were found in similar concentrations among lateral and midline regions in N. sagrei. These patterns indicate that both carotenoid and pterin pigments are responsible for producing color in the dichromatic dewlaps of these two species, and that in these two species the two pigments interact differently to produce the observed colors.     

Leaf‐footed bugs possess multiple hidden contrasting color signals,but only one is associated with increased body size

Antipredatory displays that incorporate hidden contrasting coloration are found in a variety of different animals. These displays are seen in organisms that have drab coloration at rest, but when disturbed reveal conspicuous coloration. Examples include the bright abdomens of mountain katydids and the colorful underwings of hawk moths. Such hidden displays can function as secondary defenses, enabling evasion of a pursuant predator. To begin to understand why some species have these displays while others do not, we conducted phylogenetic comparative analyses to investigate factors associated with the evolution of hidden contrasting coloration in leaf‐footed bugs. First, we investigated whether hidden contrasting coloration was associated with body size because these displays are considered to be more effective in larger organisms. We then investigated whether hidden contrasting coloration was associated with an alternative antipredatory defense, in this case rapid autotomy. We found that leaf‐footed bugs with hidden contrasting coloration tended to autotomize more slowly, but this result was not statistically significant. We also found that the presence of a body size association was dependent upon the form of the hidden color display. Leaf‐footed bugs that reveal red/orange coloration were the same size, on average, as species without a hidden color display. However, species that reveal white patches on a black background were significantly larger than species without a hidden color display. These results highlight the diversity of forms that hidden contrasting color signal can take, upon which selection may act differently.     

The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.     

The effects of background coloration and dark spots on the risk of predation in poison frog models

Protective coloration is a well-known predator avoidance strategy in prey species. Aposematic species often display a contrasting color pattern consisting of dark spots of different shapes and sizes on a bright background coloration. Both elements, background color and spots are expected to serve different purposes. While the ecological function of the bright coloration has been addressed in many studies, the question of whether the interaction with differently sized spots influences predator behavior has received less attention by researchers. In a lowland rain forest in Costa Rica we used 2700 clay models that imitated the polytypic strawberry poison frog (Oophaga pumilio) as a proxy for an aposematic prey species. We manipulated the dorsal color pattern by using a local and a non-local aposematic and a non-local cryptic background color and combined them with black spots increasing in size (none, small, medium, large). The major objective was to test if spot size alters the survival rate of differently colored models. Background coloration and spot size were significant predictors of being attacked. However, the interaction between both effects was not. During five trials predators avoided the non-local aposematic color morph and did not discriminate between local aposematic and non-local cryptic models. Spot size and attack rate were negatively linear correlated which suggests that predator selection promotes the evolution of dark spots. We further conclude that spot size matters in a contrasting color pattern and plays an important role in predator avoidance.     

Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test

Many male birds use carotenoid pigments to acquire brilliant colors that advertise their health and condition to prospective mates. The direct means by which the most colorful males achieve superior health has been debated, however. One hypothesis, based on studies of carotenoids as antioxidants in humans and other animals, is that carotenoids directly boost the immune system of colorful birds. We studied the relationship between carotenoid pigments, immune function, and sexual coloration in zebra finches (Taeniopygia guttata), a species in which males incorporate carotenoid pigments into their beak to attract mates. We tested the hypotheses that increased dietary carotenoid intake enhances immunocompetence in male zebra finches and that levels of carotenoids circulating in blood, which also determine beak coloration, directly predict the immune response of individuals. We experimentally supplemented captive finches with two common dietary carotenoid pigments (lutein and zeaxanthin) and measured cell-mediated and humoral immunity a month later. Supplemented males showed elevated blood-carotenoid levels, brighter beak coloration, and increased cell-mediated and humoral immune responses than did controls. Cell-mediated responses were predicted directly by changes in beak color and plasma carotenoid concentration of individual birds. These experimental findings suggest that carotenoid-based color signals in birds may directly signal male health via the immunostimulatory action of ingested and circulated carotenoid pigments.     

Aposematic coloration does not deter corallivory by fish on the coral <Emphasis Type="Italic">Montastraea cavernosa</Emphasis>

Predation on corals by visual predators is a significant source of partial or total mortality on coral reefs, and corals have evolved strategies, including chemical defenses, to deter predation. One mechanism that organisms use to communicate the presence of chemical defenses is aposematic coloration, or the display of bright coloration as a warning to visual predators such as fish. Corals exhibit multiple colors, and it has been hypothesized that one role for this variability in coloration is as an aposematic warning of adverse palatability. Here, we test green and orange color morphs of the Caribbean coral Montastraea cavernosa for the presence of chemical defenses and whether their differences in coloration elicited different feeding responses. While M. cavernosa is chemically defended, there is no difference in feeding deterrence between color morphs; thus, the different color morphs of this coral species do not appear to represent an example of aposematic coloration.     

No evidence for differential survival or predation between sympatric color morphs of an aposematic poison frog

Because variation in warning signals slows down the predator education process, aposematic theory predicts that animal warning signals should be monomorphic. Yet, warning color polytypisms are not uncommon in aposematic species. In cases where warning signal variants are separated geographically, adaptation to local predators could explain this variation. However, this cannot explain the persistence of sympatric polymorphisms in aposematic taxa. The strawberry poison frog (Oophaga pumilio) exhibits both allopatric and sympatric warning color variation in and around the Bocas del Toro archipelago of Panama. One explanation that has been proposed for the rapid diversification of O. pumilio coloration in this archipelago is low predation; if island populations have few predators, stabilizing selection would be relaxed opening the door for diversification via selection or genetic drift. Using a combination of mark-recapture and clay model studies, we tested for differences in survival and predation among sympatric red and yellow color morphs of O. pumilio from Bastimentos Island. We found no evidence for differential survival or predation in this population, despite the fact that one morph (red) is more common and widely distributed than the other (yellow). Even in an area of the island where the yellow morph is not found, predator attack rates were similar among morphs. Visual modeling suggests that yellow and red morphs are distinguishable and conspicuous against a variety of backgrounds and by viewers with different visual systems. Our results suggest that general avoidance by predators of red and yellow, both of which are typical warning colors used throughout the animal kingdom, may be contributing to the apparent stability of this polymorphism.     

Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey

Recently there has been debate over the importance of innateavoidance of aposematic prey by predators, particularly birds.There is evidence that the predators have innate or unlearned,thus, inherited avoidance against certain colors, but whetherthere is any innate avoidance against gregariousness or conspicuousnessis unclear. Previously predator behavior toward these charactersof aposematic prey have been tested in separate experiments.We designed an experiment to separate inheritance toward color,gregariousness, and conspiucuosness. We simultaneously offeredthe predators warningly colored and nonwarningly colored preyitems, both aggregated and solitary, on white (conspicuous)or brown (cryptic) backgrounds. The predators we used were naive (handraised), wild-caught yearling and adult great tits (Parus major L.).The results confirm previous results regarding the innate avoidanceof color. Naive predators seemed to have a genetically or culturallytransmitted avoidance of yellow and black prey compared to brownprey. Surprisingly, yearling wild-caught great tits were moreselective than adults, which did not show as strong avoidanceof yellow and black prey. More importantly, birds did not findgregarious prey more aversive than single prey, which indicatesthat grouping alone does not serve as an innate avoidance signal.Conspicuousness itself was not aversive to the predators. Ourresults suggest that the avoidance against a particular colorpattern probably has an inherited basis, whereas gregariousand conspicuous characters of prey presumably aid the avoidancelearning.     

Wing coloration and reflectance in Morpho butterflies as related to reproductive behavior and escape from avian predators

Summary Different species of large tropical butterflies belonging to the genus Morpho vary dramatically in both the amount of blue color on their wings and the associated irridescence (reflectance). This paper discusses how such a morphological properties may be related to both courtship behavior and effective means of reducing predation (especially by birds) in the low density adult populations. Essentially, the hypothesis is advanced that territorial species of Morpho can afford to possess very conspicuous wing coloration that may facilitate courtship interactions, in addition to spacing the territorial male population over the suitable habitat. While territoriality may be favored by natural selection, such behavior can only evolve if the species involved possess effective means of reducing predation, because territoriality in morphos is an extremely predictable form of behavior, toward which predators can easily orient. Two alternate hypotheses are advanced to account for low predation in a territorial morpho, Morpho amathonte, a species in which males are very bright and showy. The first hypothesis, which is more consistent with traditional ideas on the function of bright colors in morpho wings, maintains that predators learn quickly to avoid these butterflies as prey, since they are very difficult to catch. The second hypothesis, suggests that conspicuous territorial male morphos actually employ pursuit-stimuli to invite birds to attack and be subsequently unsuccessful.     

Interspecific variation in dietary carotenoid assimilation in birds: links to phylogeny and color ornamentation

Many birds use carotenoid pigments to acquire rich red, orange, and yellow coloration in feathers and bare parts that is used as a signal of mate quality. Because carotenoids are derived from foods, much attention has been paid to the role of diet in generating color variation both within and among avian species. Less consideration has been given to physiological underpinnings of color variability, especially among species. Here, I surveyed published literature (e.g. captive feeding studies) on carotenoid assimilation in six bird species and completed additional controlled carotenoid-supplementation experiments in two others to consider the ability of different taxa to extract carotenoids from the diet in relation to phylogeny and coloration. I found that, for a given level of carotenoids in the diet, passerine birds (zebra finch, Taeniopygia guttata; house finch, Carpodacus mexicanus; American goldfinch, Carduelis tristis; society finch, Lonchura domestica) exhibit higher levels of carotenoids in circulation than non-passerines like gamebirds (domestic chicken, Gallus domesticus; red junglefowl, Gallus gallus; Japanese quail, Coturnix coturnix; red-legged partridge, Alectoris rufa). This difference in carotenoid accumulation is likely due to interspecific variation in micelle, chylomicron, or lipoprotein concentrations or affinities for xanthophyll carotenoids. Passerine birds more commonly develop carotenoid-based colors than do birds from ancient avian lineages such as Galliformes, and the physiological differences I uncover may explain why songbirds especially capitalize on carotenoid pigments for color production. Ultimately, because we can deconstruct color traits into component biochemical, physical, and physiological parts, avian color signals may serve as a valuable model for illuminating the proximate mechanisms behind interspecific variation in signal use in animals.     

Ornamental non-carotenoid red feathers of wild burrowing parrots

Bird plumage colors have the potential to indicate individual quality, condition, health, immunocompetence, or the extend of parental care. Color intensity of feathers has been found to correlate with parameters of individual quality, condition, parental care and breeding success. Psittaciformes are well known for their colorful plumage but the significance of parrot coloration is still poorly understood. Red colors are very common in many parrot species. They are produced by at least four non-carotenoid-based pigments (linear polyenal structure). In the present study, we investigated a collection of red abdominal feathers of a marked population of wild Burrowing Parrots Cyanoliseus patagonus in Patagonia, Argentina. The aims of this study were to investigate the ecological significance of the recently described non-carotenoid-based red pigments of Psittaciformes, and the relationships between objectively assessed plumage color and body size, body condition, breeding success and nestling growth in wild Psittaciformes. We found that sexes differed in plumage coloration (sexual dichromatism), that plumage color was a good predictor of female body condition and male size, and we identified the red coloration of the abdominal patch as a signal of individual quality and parental investment.     

Inter‐individual Variation in Antipredator Hiding Behavior of Spanish Terrapins Depends on Sex,Size, and Coloration

Behavioral responses to predation risk are critical for survival but as antipredator behavior is costly, prey animals should flexibly modulate their optimum defensive responses by considering both costs and benefits, which are partly influenced by the individual characteristics of the prey. Turtles have the shell as a morphological structure that may provide partial protection against predators, but hiding into the shell may entail some high costs, and turtles should decide when to switch to an active escape strategy to safe refuges. Here, we examined how gender, body size, and sexual coloration influence inter‐individual variability of antipredatory hiding behavior into the shell of Spanish terrapins (Mauremys leprosa). We simulated predatory attacks under different conditions and measured the time that the turtles spent hidden entirely inside the shell (i.e., appearance times) and from then until the turtle started to flee actively (i.e., waiting times). Our results showed that when risk increased, appearance times increased but waiting times decreased. When turtles were in a prone position, their hiding behavior was related with their body weight with heavier turtles having longer appearance times. Also, the conspicuousness of limb coloration was important for the appearance times of males, but not for females. Thus, males with brighter coloration of the limb stripes had longer appearance times than duller ones. In addition, when turtles were overturned, males appeared out of the shell earlier than females and heavier turtles started to right sooner, but only when risk was low. However, when turtles were overturned and risk was high, they should assume that they have already been detected, making inter‐individual differences in size and coloration apparently unimportant for deciding hiding behavior.     

Benefit by contrast: an experiment with live aposematic prey

Aposematic prey often have a coloration that contrasts withthe background. One beneficial effect of such conspicuous colorationis that it produces faster and more durable avoidance by predators.Another suggested benefit is that prey that contrast with thebackground are more quickly discerned and recognized as unpalatableby experienced predators. To further investigate the effectsof prey contrast on predator behavior, I conducted an experimentwith young chicks (Gallus gallus domesticus) as predators onlive aposematic and nonaposematic prey. Birds with prior experienceof both prey types were allowed into an arena with both palatableprey and aposematic prey on backgrounds that either closelymatched or contrasted with the coloration of the aposematicprey. Also, the time a bird had available to decide to attacka prey was manipulated by including a competing chick or not.The experienced birds showed greater attack latencies for aposematicprey on more contrasting backgrounds, and aposematic prey werealso attacked to a greater extent when on a matching background.The presence of a competitor generated similar effects, wherebirds in high competition attacked more and faster comparedto birds subjected to lower degree of competition, but therewas no interaction between competition and contrast. Thus,the experiment provides evidence that prey contrast againstthe background may produce better recognition and avoidance,independently of predator viewing time.     

Melanin‐Based Coloration Covaries with Hiding and Exploratory Behavior in Male Spanish Terrapins

Melanin‐based coloration reflects mostly social status and dominance in males of several species. However, the relation of melanism with other suites of behavioral traits has received less attention. Here, we examined whether the melanic coloration of the shell of male Spanish terrapins Mauremys leprosa was related to several behavioral patterns. To test this, we simulated predatory attacks of different risk levels and measured the time that the turtles spent hiding entirely in their own shells (i.e. appearance times). We also measured the activity level of the turtles in a novel‐environment test. The results showed that melanin‐based coloration was related to antipredatory behavior. Male terrapins with a greater extent of black coloration in their shells demonstrated shorter appearance times after a predator attack. However, this pattern was significant only when turtles were subjected to a high risk. In addition, darker turtles had longer latency times in a novel environment. The results of the present study support the hypothesis that melanin‐based coloration may be associated with some behavioral functions. Our study provides a good framework for future studies concerning the effect of melanin‐coloration on multiple behavioral traits that could be applied to further research using other animal models.     

Honest signaling and the uses of prey coloration

Abstract Although signal reliability is of fundamental importance to the understanding of animal communication, the extent of signal honesty in relation to antipredator warning signals has received relatively little attention. A recent theoretical model that assumed a physiological linkage between pigmentation and toxicity suggested that (aposematic) warning signals may often be reliable, in the sense that brightness and toxicity are positively correlated within prey populations. Two shortcomings of the model were (1) the requirement among predators for an innate aversion to brightly colored prey and (2) the assumption that prey can generate only bright coloration and not cryptic coloration. We evaluated the generality of predictions of reliable signaling when these shortcomings were removed. Without innate avoidance of bright prey, we found a positive brightness-toxin correlation when conspicuous prey coloration provided an additional fitness benefit unrelated to predation. Initially, this correlation could evolve for reasons unrelated to prey signaling; hence, aposematism might represent a striking example of exaptation. Given a choice between using pigmentation for bright or for cryptic coloration, crypsis was favored only in conditions of very low or very high resource levels. In the latter case, toxicity correlated positively with degree of cryptic coloration. Predictions of toxin-signal correlation appear robust, but we can identify interesting conditions in which signal reliability is not predicted.