Autumn tree colours as a handicap signal.

Many species of deciduous trees display striking colour changes in autumn. Here, we present a functional hypothesis: bright autumn coloration serves as an honest signal of defensive commitment against autumn colonizing insect pests. According to this hypothesis, individuals within a signalling species show variation in the expression of autumn coloration, with defensively committed trees producing a more intense display. Insects are expected to be averse to the brightest tree individuals and, hence, preferentially colonize the least defensive hosts. We predicted that tree species suffering greater insect damage would, on average, invest more in autumn-colour signalling than less troubled species. Here, we show that autumn coloration is stronger in species facing a high diversity of damaging specialist aphids. Aphids are likely to be an important group of signal receivers because they are choosy, damaging and use colour cues in host selection. In the light of further aspects of insect and tree biology, these results support the notion that bright autumn colours are expensive handicap signals revealing the defensive commitment of individual trees to autumn colonizing insect pests.     

What do red and yellow autumn leaves signal?

The widespread phenomenon of red and yellow autumn leaves has recently attracted considerable scientific attention. The fact that this phenomenon is so prominent in the cooler, temperate regions and less common in warmer climates is a good indication of a climate-specific effect. In addition to the putative multifarious physiological benefits, such as protection from photoinhibition and photo-oxidation, several plant/animal interaction functions for such coloration have been proposed. These include (1) that the bright leaf colors may signal frugivores about ripe fruits (fruit flags) to enhance seed dispersal; (2) that they signal aphids that the trees are well defended (a case of Zahavi’s handicap principle operating in plants); (3) that the coloration undermines herbivore insect camouflage; (4) that they function according to the “defense indication hypothesis,” which states that red leaves are chemically defended because anthocyanins correlate with various defensive compounds; or (5) that because sexual reproduction advances the onset of leaf senescence, the pigments might indicate to sucking herbivores that the leaves have low amounts of resources. Although the authors of hypotheses 3, 4, and 5 did not say that bright autumn leaves are aposematic, since such leaves are chemically defended, unpalatable, or both, we suggest that they are indeed aposematic. We propose that in addition to the above-mentioned hypotheses, autumn colors signal to herbivorous insects about another defensive plant property: the reliable, honest, and critical information that the leaves are about to be shed and may thus cause their mortality. We emphasize that all types of defensive and physiological functions of autumn leaves may operate simultaneously.     

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.     

Bright autumn colours of deciduous trees attract aphids: nutrient retranslocation hypothesis

We propose an alternative hypothesis to the handicap-signalling hypothesis, to explain the high number of specialist aphids on tree species having bright autumn colour. Since birch aphids actively seek the first yellowing leaves for breeding in autumn, it is obvious that autumn colour of foliage does not repel migrating aphids. We suggest that aphids use bright colours as a cue to detect individual trees and leaves that are good sources of nitrogen in the form of amino acids in autumn. The active formation of bright-coloured pigments in leaves is needed to protect them from photo inhibition during energy consuming nutrient retranslocation under cold autumn conditions. During nutrient export from leaves, nitrogen is in the form of amino acids in the sieve elements and easily available for aphids. Therefore, bright colours may act as a signal of easily available high-quality food for viviparous aphid migrants that are selecting suitable trees for their sexual offspring reproduction. The females of sexual generation grown on the better quality food probably can oviposit the over-wintering eggs to the twigs in higher numbers, which may have an adaptive advantage in competition with conspecific females.     

Autumn colours and the nutrient retranslocation hypothesis: a theoretical assessment

The adaptive value of the bright colours of leaves in autumn is still debated. It is possible that autumn colours are an adaptation to protect the tree against photoinibition and photooxidation, which allows a more efficient recovery of nutrients. It has been proposed that the preference of aphids for trees that retranslocate nitrogen more efficiently can explain the high diversity of aphids on tree species with bright autumn colours. This scenario however does not take into account the impact of insects on the fitness of the trees and has not been analysed theoretically. Its assumptions and predictions, therefore, remain uncertain. I show with a model of insect-tree interaction that the system can actually evolve under particular conditions. I discuss the differences with the coevolution theory of autumn colours, available evidence and possible tests.     

植物警戒色的研究进展

植物为适应植食动物的取食压力而进化出物理、化学等多种防御机制,以把植食伤害降到最低程度,但动物不断的抽样尝试行为还是让有防御行为的植物受到伤害。因此,向潜在的植食动物传达自己的防御信号对植物是有益的。颜色作为一种稳定有效的视觉信号通常是花和果实的诱惑信号,某些情况下也是一种警戒防御信号,植食动物经过抽样学习后能识别这种防御信号并主动回避,从而形成了植物的警戒色。起源于猎物-捕食者关系的警戒色理论在动物界得到了充分研究,但植物警戒色却不为人所知,直到2001年Hamilton关于秋季树叶颜色的信号假说公开发表后,才引起人们对植物警戒色的初步研究。如今在早秋变色树种、幼叶、多剌植物、植物繁殖器官都发现了警戒色的一些例证,尽管有些还不太明确甚至存在争议,但至少为植物警戒色的进一步研究奠定了基础。植物营养体颜色在时空上的多态性变化值得人们更深入地研究,防御权衡假说也预示了防御有害植食动物的警戒作用存在于繁殖器官的可能性,研究它们生理和生态适应意义有利于人们更深程度地理解植物-动物之间的复杂关系。     

The coevolution theory of autumn colours

According to the coevolution theory of autumn colours, the bright colours of leaves in autumn are a warning signal to insects that lay their eggs on the trees in that season. If the colour is linked to the level of defensive commitment of the tree and the insects learn to avoid bright colours, this may lead to a coevolutionary process in which bright trees reduce their parasite load and choosy insects locate the most profitable hosts for the winter. We try to clarify what the theory actually says and to correct some misunderstandings that have been put forward. We also review current research on autumn colours and discuss what needs to be done to test the theory.     

Antagonistic effects of growing season and autumn temperatures on the timing of leaf coloration in winter deciduous trees

Autumn phenology remains a relatively neglected aspect in climate change research, which hinders an accurate assessment of the global carbon cycle and its sensitivity to climate change. Leaf coloration, a key indicator of the growing season end, is thought to be triggered mainly by high or low temperature and drought. However, how the control of leaf coloration is split between temperature and drought is not known for many species. Moreover, whether growing season and autumn temperatures interact in influencing the timing of leaf coloration is not clear. Here, we revealed major climate drivers of leaf coloration dates and their interactions using 154 phenological datasets for four winter deciduous tree species at 89 stations, and the corresponding daily mean/minimum air temperature and precipitation data across China's temperate zone from 1981 to 2012. Results show that temperature is more decisive than drought in causing leaf coloration, and the growing season mean temperature plays a more important role than the autumn mean minimum temperature. Higher growing season temperature and lower autumn minimum temperature would induce earlier leaf coloration date. Moreover, the mean temperature over the growing season correlates positively with the autumn minimum temperature. This implies that growing season mean temperature may offset the requirement of autumn minimum temperature in triggering leaf coloration. Our findings deepen the understanding of leaf coloration mechanisms in winter deciduous trees and suggest that leaf life‐span control depended on growing season mean temperature and autumn low temperature control and their interaction are major environmental cues. In the context of climate change, whether leaf coloration date advances or is delayed may depend on intensity of the offset effect of growing season temperature on autumn low temperature.     

Warning signal properties covary with toxicity but not testosterone or aggregate carotenoids in a poison frog

Aposematic (warning) coloration is a highly conspicuous trait that is found throughout the animal kingdom. In several aposematic species, warning signals have been co-opted for use in conspecific communication systems; for example, in the toxic and bright orange Solarte population of the strawberry poison frog (Oophaga [Dendrobates] pumilio), the brightness of male warning coloration serves as a sexual signal by both attracting females and repelling rivals. Here, we investigate correlations between bright male warning coloration and several physiological characteristics (e.g., circulating testosterone and carotenoids and noxious alkaloids in the skin), to gain insights into the mechanisms underlying the signal variation in this population and to inform hypotheses regarding the evolutionary stability of this trait. We find that although measures of male brightness (viewer-dependent or viewer-independent) do not correlate with two classic correlates of sexually selected traits (circulating testosterone and aggregate carotenoids in the skin), male reflectance does show a positive correlation with concentrations of two xanthophyll carotenoids. Total reflectance (a viewer-independent measure of male brightness) also shows a negative relationship with aggregate pumiliotoxin in the skin, which is considered one of the major classes of defensive alkaloids in this species. Because the alkaloids used in this species’ chemical defense are acquired from dietary sources, the magnitude of the reflectance intensity of a male’s warning signal can potentially provide viewers with reliable information regarding territory quality, health, and/or current condition.     

A test of the coevolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus

According to the coevolution theory of autumn colours, the bright colours of trees evolved as a warning signal towards parasites colonizing the plant in autumn. We monitored colonization of the aphid Rhopalosiphum padi on individual tress of Prunus padus in autumn and observed a strong preference of aphids for trees with green leaves. This is the first direct observation of a key assumption of the theory, that parasites avoid bright colours. Moreover our observations, compared with previous data gathered on the same species, suggest that aphids colonizing trees with green leaves develop better in spring than aphids colonizing trees with bright autumn colours, which is consistent with the second main assumption of the coevolution theory.     

Decoupling vigour and quality in the autumn colours game: Weak individuals can signal, cheating can pay

According to the coevolution theory, autumn colours are a warning signal to insects, signalling the level of chemical defences or availability of nutrients. Because in the original model tree vigour and defences were positively correlated, it is not clear whether signalling would still be stable when they are decoupled, and the fact that weak trees often display bright autumn colours is usually presented as evidence against the coevolution theory. I show that in a theoretical model of insect-tree coevolution, signalling is still stable when vigour and defences are decoupled. Weak trees can signal. Moreover, partial cheating is possible. The different equilibria depend on the importance of vigour and defences against insect attack, of vigour in the production of the signal, and of pleiotropic effects between colour and defences. These results provide precise predictions that can be used for planning future empirical test.     

Visual conditions and habitat shape the coloration of the Eurasian perch (Perca fluviatilis L.): a trade‐off between camouflage and communication?

In theory, selection for effective camouflage (i.e. dull coloration) in fish should be strongest when the conditions for visual predation are most favourable, such as in structurally simple pelagic habitats. By contrast, in more sheltered (e.g. littoral) habitats, selection may favour effective intra‐specific communication (i.e. bright coloration) (at the expense of crypsis). Poor transparency, as in highly humic waters, should constrain colour adaptations. We investigated phenotypic variation in body coloration of Eurasian perch (Perca fluviatilis L.) in littoral and pelagic habitats of four humic boreal lakes. Perch from the most transparent lake had the lightest and less coloured belly and perch were more colourful in the littoral habitats than in the pelagic areas, with the pattern being clearest in the most transparent lake. In addition, perch in the most transparent lake exhibited sexual dichromatism, with males having a more colourful belly than the females, whereas no indications of sexual dichromatism were found in more humic lakes. Moreover, in the most transparent lake, the condition of fish correlated with bright belly coloration in the littoral, but with dull belly coloration in the pelagic habitat. The results obtained in the present study suggest that selection on perch coloration may differ between lakes as a result of visual properties of the water, and within lakes as a result of divergent selection for camouflage and communication in pelagic and littoral habitats. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 47–59.     

Bluegill Coloration as a Sexual Ornament: Evidence From Ontogeny,Sexual Dichromatism,and Condition Dependence

In aquatic environments, visual communication is expected in animals that inhabit clear, shallow waters. Here, we investigate variation in the colorful traits of bluegills, Lepomis macrochirus, to elucidate their possible function. Bluegills use alternative mating tactics whereby males develop into one of two irreversible phenotypes termed parental and cuckolder. Parentals build and defend nests and care for offspring whereas cuckolders obtain matings by sneaking copulations. We hypothesized that bluegill coloration might function as a sexual ornament in parental males and that ornamental coloration might serve as an honest indicator of male quality. We predicted that coloration should be more pronounced in parental males than in females and immature males and should be more pronounced during the breeding season. We also predicted that males in better condition should be more intensely colored than fish in poor condition. To test our predictions, we sampled 510 bluegills during the breeding and post‐breeding seasons at nine lakes in southern Ontario, Canada, in 2007. We used reflectance spectrometry to quantify the coloration of five body regions, aged and sexed each fish, and calculated Fulton’s condition factor from morphological measurements. A separate experiment showed that color did not fade several minutes post capture, suggesting that coloration could be measured reliably and consistently. We found that color was influenced by maturity, sex, and season, in the predicted direction, for three body regions (breast, cheek, and opercular flap). We also found that color varied with the condition of males such that males in better condition were darker for the sexually dichromatic ventral and facial regions. Our findings therefore suggest that some colorful traits in bluegills may serve as condition‐dependent sexual signals during the breeding season. Our research contributes to a growing appreciation of the importance of visual signaling in aquatic environments.     

Importance of olfactory and visual signals of autumn leaves in the coevolution of aphids and trees

Deciduous trees remobilize the nitrogen in senescing leaves during the process of autumn colouration, which in many species is associated with increased concentrations of anthocyanins. Archetti and Hamilton and Brown observed that autumn colouration is stronger in tree species facing a high diversity of specialist aphids. They proposed a coevolution theory that the bright colours in autumn might provide an honest signal of defence commitment, thus deterring migrant aphids from settling on the leaves. So far, there have been very few experimental results to support the hypothesis, and tree commitment to phenolics-based defences has not shown direct protection against aphids. Predators and parasitoids have been found to be the major controllers of arboreal aphids. Indirect defences involve the emission of attractive volatile compounds that enhance the effectiveness of carnivorous enemies. The indirect defence hypothesis is presented to explain low aphid diversity on tree species that are green during autumn. The hypothesis suggests that green foliage can continue to produce herbivore-inducible plant volatiles and maintain volatile-based indirect plant defences against aphids until leaf abscission.     

Determinants of Dominance in the Tree Lizard Urosaurus ornatus: the Relative Importance of Mass,Previous Experience and Coloration

A determination of some of the factors that predict the outcome of contests between male tree lizards, Urosaurus ornatus, was made using logistic regression modelling on matched-pair data. Two-day-long encounters were staged between pairs of males differing in size (snout-vent length and mass), previous contest status (previous winners and previous losers), and coloration (dorsal coloration during their previous contest and throat coloration, a fixed trait). Mass proved to be the best single predictor of contest outcome, resulting in an 80% correct classification rate for predicting winners and losers, far better than the less than 57% correct classification rate for snout-vent length. Previous social status (winner or loser) also was a powerful single predictor of contest outcome with a 793% correct classification rate, as was previous dorsal coloration (76.7%). When combined, mass and previous status produced the strongest combination of predictors with a better than 86% correct classification rate. Contrary to several previous studies, which implicated throat coloration as an important status signal of dominance, our results failed to show that throat coloration is a strong predictor of contest outcome. Possible reasons for this discrepancy with earlier findings are discussed. The logistic regression models also allow prediction of the magnitude of difference in mass between two contestants for there to be an equal chance of winning, given a second asymmetry in contest predictors.     

Is Brightest Best? Testing the Hamilton-Zuk Hypothesis in Mandrills

Although many primates exhibit striking coloration, including brightly colored pelage and bare areas of skin, our understanding of the function and evolution of these traits pales in the face of knowledge about color in other taxa. However, recent years have seen an increase in the number of studies of individual variation in primate color and evidence is accumulating that these traits can act as important signals to conspecifics. Mandrills are arguably the most colorful of all primates. Here, we review what we have discovered about the signal function of coloration in male and female mandrills from our long-term studies of a semi-free-ranging colony in Franceville, Gabon and test the predictions of the Hamilton-Zuk hypothesis—that bright coloration is condition dependent, and that only individuals of superior quality will be able to express color fully—in this species. We compare measures of facial coloration in both sexes with parasite load (using fecal analysis over 1 annual cycle), immune status (hematological parameters), neutral genetic diversity (microsatellite heterozygosity), and major histocompatability (MHC) genotype to examine whether red coloration acts as an honest signal of individual quality in mandrills. We found that red coloration was unrelated to parasitism and hematological parameters. Red was also unrelated to genome-wide heterozygosity and MHC diversity, although specific MHC genotypes were significantly related to red. The healthy, provisioned nature of the colony and problems associated with observational, correlational studies restrict interpretation of our data, and it would be premature to draw conclusions as to whether color signals individual quality in mandrills. We conclude with some suggestions for future studies on the signal content of color in mandrills and other primates.     

A test of an antipredatory function of conspicuous plastron coloration in hatchling turtles

Bright colorations in animals are sometimes an antipredatory signal meant to startle, warn, or deter a predator from consuming a prey organism. Freshwater turtle hatchlings of many species have bright ventral coloration with high internal contrast that may have an antipredator function. We used visual modeling and field experiments to test whether the plastron coloration of Chrysemys picta hatchlings deters predators. We found that bird predators can easily distinguish hatchling turtles from their backgrounds and can easily see color contrast within the plastron. Raccoons cannot easily discriminate within-plastron color contrast but can see hatchlings against common backgrounds. Despite this, we found that brightly-colored, high contrast, replica turtles were not attacked less than low contrast replica turtles, suggesting that the bright coloration is not likely to serve an antipredatory function in this context. We discuss the apparent lack of innate avoidance of orange coloration in freshwater turtles by predators and suggest that preference and avoidance of colors are context-dependent. Since the bright colors are likely not a signal, we hypothesize that the colors may be caused by pigments deposited in tissue from maternal reserves during development. In most species, these pigments fade ontogenetically but they may have important physiological functions in species that maintain the bright coloration throughout adulthood.     

Aggressive Behavior and Courtship Rejection in Brightly and Plainly Colored Female Keeled Earless Lizards (Holbrookia propinqua)

Relationships between bright secondary sexual coloration and behavior were studied in female Holbrookia propinqua, which develop striking orange and yellow colors during the breeding season. In tethered introduction studies, brightly colored females performed aggressive courtship rejection behaviors toward conspecific males; plainly colored females were not aggressive toward males, but attempted to avoid them. Responses of females of the two color patterns toward conspecific females of both color phases were not detectably different. Experimental introductions of lizards with coloration modified by paint showed that females of both color patterns recognize any other lizard bearing the bright female colors as female, regardless of actual sex. Both the orange and yellow components were shown to contribute to sex recognition. The yellow component alone allowed accurate sex identification, but only half the females responded to males painted with only the orange female component as if they were females. Because females did not behave differently toward other females on the basis of coloration, the hypothesis that bright coloration evolved as an adaptive signal between females is rejected. The dark ventrolateral stripes of male and plainly colored females did not appear to affect intraspecific social responses by females.     

Habitat structure and prey composition generate contrasting effects on carotenoid‐based coloration of great tit Parus major nestlings

Carotenoid‐based coloration of nestling plumage is generally considered a reliable signal of quality and has consistently been related to habitat structure. The main hypothesis proposed to explain this correlation is that high quality habitats contain high quality food, which in return affects the expression of carotenoid‐based plumage. It therefore assumes that, at the population level, the link between habitat structure and food composition is consistent and more relevant than inter‐individual differences in foraging ability or parental investment. In addition, it is assumed by default that food and habitat produce concordant effects on nestling coloration. In this work we evaluated habitat structure and prey composition in addition to several measures of parental investment. We investigated their relative effect on carotenoid‐based plumage coloration (lightness, chroma and hue) of great tit Parus major nestlings. We found a low correlation between carotenoid‐based coloration of nestlings and that of their parents. Nestling coloration, especially lightness and chroma, increased with the intake of more spiders. The time of breeding was positively correlated with lightness and chroma and negatively correlated with hue. Finally, the maturity of oak trees surrounding nest‐boxes correlated negatively with lightness, and the size of all tree species surrounding nest‐boxes correlated positively with hue of chick plumage. Our findings support the view that habitat structure and prey composition may produce divergent effects on feather pigmentation, and that prey proportions and variables related to parental investment should be assessed when considering carotenoid‐based coloration of chicks. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 547–555.     

Melanin‐based coloration covaries with fluctuating asymmetry,nutritional state and physiological stress response in common snipe

Adaptative significance of melanin‐based coloration in birds remains poorly recognized. It has been suggested that genes responsible for melanin synthesis may have pleiotropic effect on several physiological and behavioural functions, including immune defence. For this reason, we could expect that the expression of melanin‐based plumage coloration should covary with different condition‐related phenotypic traits via regulation of pathogen/parasite resistance. The aim of this study was to test this hypothesis in common snipe Gallinago gallinago, a species that exhibits conspicuous variation in the black eumelanism of underwing plumage. The study was conducted in central Poland, where common snipe were captured during autumn migration. We found that after accounting for the effects of age, sex and date of capture, underwing coloration correlated with nutritional state of snipes, as more extensively melanised individuals had higher plasma concentrations of triglycerides, total protein and albumin. Dark underwing coloration was also associated with lower heterophil/lymphocyte (H/L) ratio, suggesting better resistance of eumelanic individuals to physiological stress. Finally, adult males with darker underwings had lower asymmetry in wing shape (wingtip convexity), which indicated their higher developmental stability. In conclusion, melanin‐based coloration may be considered an honest indicator of phenotypic quality in common snipe.