Autumn coloration as a signal of tree condition

Hamilton and Brown suggested that bright autumn coloration in trees is an energetically expensive and therefore honest (handicap) signal of defensive commitment against insects. If this is so, one should expect that the intensity of the proposed signal should depend strongly on tree health. However, to the best of our knowledge, the link between vigour and autumn colour has never been tested. We explored the relationship between autumn coloration and tree condition (i.e. leaf fluctuating asymmetry) in mountain birch (Betula pubescens). Our results indicate that bright autumn birches are in better condition and therefore consequently should be better at combating herbivores.     

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.     

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.     

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.     

Coevolution and the adaptive value of autumn tree colours: colour preference and growth rates of a southern beech aphid

The evolutionary explanation for the change in leaf colour during autumn is still debated. Autumn colours could be a signal of defensive commitment towards insects (coevolution) or an adaptation against physical damage because of light at low temperatures (photoprotection). These two hypotheses have different predictions: (1) under the coevolution hypothesis, insects should not prefer red leaves in autumn and grow better in spring on trees with green autumn leaves; and (2) under the photoprotection hypothesis, insects should prefer and grow better on trees with red leaves because they provide better nutrition. Studying colour preference in autumn and growth rates in spring of a southern beech aphid species (Neuquenaphis staryi) on Nothofagus alessandrii, we found preference for green leaves in autumn but no differential performance of aphids in spring. We suggest that aphid preference for green might have evolved to exploit better their host during the autumn rather than to improve their performance in spring.     

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.     

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.     

The adaptive significance of autumn leaf colours

Recently W.D. Hamilton and colleagues proposed a provocative new theory to explain the adaptive significance of autumnal leaf colours. They suggested that these colours were signals produced by the trees to warn potential insect herbivores of their defensive ability and tested this theory by an analysis of data on aphid species richness on different tree species. Here we argue that the principal assumptions of their theory do not match current knowledge of plant pigment biochemistry and aphid ecology. We therefore present further adaptive explanations for autumn leaf colours and suggest alternative reasons for the reported relationship between tree leaf colour and aphid species richness.     

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.     

Female butterflies prefer males bearing bright iridescent ornamentation

Butterflies are among nature's most colorful animals, and provide a living showcase for how extremely bright, chromatic and iridescent coloration can be generated by complex optical mechanisms. The gross characteristics of male butterfly colour patterns are understood to function for species and/or sex recognition, but it is not known whether female mate choice promotes visual exaggeration of this coloration. Here I show that females of the sexually dichromatic species Hypolimnas bolina prefer conspecific males that possess bright iridescent blue/ultraviolet dorsal ornamentation. In separate field and enclosure experiments, using both dramatic and graded wing colour manipulations, I demonstrate that a moderate qualitative reduction in signal brightness and chromaticity has the same consequences as removing the signal entirely. These findings validate a long-held hypothesis, and argue for the importance of intra- versus interspecific selection as the driving force behind the exaggeration of bright, iridescent butterfly colour patterns.     

Carotenoid‐based bill coloration functions as a social,not sexual,signal in songbirds (Aves: Passeriformes)

Many animals use coloration to communicate with other individuals. Although the signalling role of avian plumage colour is relatively well studied, there has been much less research on coloration in avian bare parts. However, bare parts could be highly informative signals as they can show rapid changes in coloration. We measured bill colour (a ubiquitous bare part) in over 1600 passerine species and tested whether interspecific variation in carotenoid‐based coloration is consistent with signalling to potential mates or signalling to potential rivals in a competitive context. Our results suggest that carotenoid bill coloration primarily evolved as a signal of dominance, as this type of coloration is more common in species that live in social groups in the nonbreeding season, and species that nest in colonies; two socio‐ecological conditions that promote frequent agonistic interactions with numerous and/or unfamiliar individuals. Additionally, our study suggests that carotenoid bill coloration is independent of the intensity of past sexual selection, as it is not related to either sexual dichromatism or sexual size dimorphism. These results pose a significant challenge to the conventional view that carotenoid‐based avian coloration has evolved as a developmentally costly, condition‐dependent sexual signal. We also suggest that bare part ornamentation may often signal different information than plumage ornaments.     

Flowers for bees,autumn colours for whom? An experimental test with autumn colouration in mountain birches (Betula pubescens ssp. czerepanovii) as a signal against the moth Epirrita autumnata

In 2001, Hamilton and Brown proposed a controversial hypothesis of handicap signalling to potential insect parasites as an adaptive explanation for autumn leaf colouration. In subsequent studies there has been little attention to the costs and benefits of early autumnal colour change. Yet, in an observational study by Hagen et al. (2003) it was demonstrated that birch trees [Betula pubescens ssp. czerepanovii Ehrhart (Betulaceae)] turning yellow early in autumn had less damage from insects chewing on leaves the subsequent summer. Here, two experiments are presented which test the mechanisms in this model. The first addresses the proposed defence of leaves of B. pubescens ssp. czerepanovii by letting caterpillars of Epirrita autumnata Borkhausen (Lepidoptera: Geometridae), the birches’ most common insect parasites, choose between leaves from trees that either turned yellow late or early the foregoing autumn. The second experiment addresses whether adult female E. autumnata choose between early or late senescent (i.e., yellow or green) ‘twigs’ when ovipositing in autumn. We could not find evidence of preferences in either larvae or females, suggesting that timing of colour change in B. pubescens ssp. czerepanovii is not a warning signal that elicits a response in E. autumnata.     

Size-dependent colouration balances conspicuous aposematism and camouflage

Colour is an important component of many different defensive strategies, but signal efficacy and detectability will also depend on the size of the coloured structures, and how pattern size interacts with the background. Consequently, size-dependent changes in colouration are common among many different species as juveniles and adults frequently use colour for different purposes in different environmental contexts. A widespread strategy in many species is switching from crypsis to conspicuous aposematic signalling as increasing body size can reduce the efficacy of camouflage, while other antipredator defences may strengthen. Curiously, despite being chemically defended, the gold-striped frog (Lithodytes lineatus, Leptodactylidae) appears to do the opposite, with bright yellow stripes found in smaller individuals, whereas larger frogs exhibit dull brown stripes. Here, we investigated whether size-dependent differences in colour support distinct defensive strategies. We first used visual modelling of potential predators to assess how colour contrast varied among frogs of different sizes. We found that contrast peaked in mid-sized individuals while the largest individuals had the least contrasting patterns. We then used two detection experiments with human participants to evaluate how colour and body size affected overall detectability. These experiments revealed that larger body sizes were easier to detect, but that the colours of smaller frogs were more detectable than those of larger frogs. Taken together our data support the hypothesis that the primary defensive strategy changes from conspicuous aposematism to camouflage with increasing size, implying size-dependent differences in the efficacy of defensive colouration. We discuss our data in relation to theories of size-dependent aposematism and evaluate the evidence for and against a possible size-dependent mimicry complex with sympatric poison frogs (Dendrobatidae).     

The origin of autumn colours by coevolution

We lack an adaptive explanation for a striking phenomenon, that of bright colours displayed in autumn by the leaves of many deciduous trees. The usual explanation is that it is simply a non-adaptive secondary effect of leaf senescence. A game-theoretic model of biological signalling provides an adaptive hypothesis for autumn colours showing that they can be the result of a process of coevolution between insects and trees: if leaf colour acts as a warning indicator of the tree's vigour to autumn parasite insects, trees can gain advantage from the reduction of parasite load and insects can gain advantage from location of the most profitable hosts to lay their eggs. The results of the model are consistent with Zahavi's handicap principle. Possible explanations for the origin of the system and evidence from natural history are discussed.     

Environmental-induced acquisition of nuptial plumage expression: a role of denaturation of feather carotenoproteins?

Several avian species show a bright carotenoid-based coloration during spring and following a period of duller coloration during the previous winter, despite carotenoids presumably being fully deposited in feathers during the autumn moult. Carotenoid-based breast feathers of male linnets (Carduelis cannabina) increased in hue (redness), saturation and brightness after exposing them to outdoor conditions from winter to spring. This represents the first experimental evidence showing that carotenoid-based plumage coloration may increase towards a colourful expression due to biotic or abiotic environmental factors acting directly on full-grown feathers when carotenoids may be fully functional. Sunlight ultraviolet (UV) irradiation was hypothesized to denature keratin and other proteins that might protect pigments from degradation by this and other environmental factors, suggesting that sunlight UV irradiation is a major factor in the colour increase from winter to spring. Feather proteins and other binding molecules, if existing in the follicles, may be linked to carotenoids since their deposition into feathers to protect colourful features of associated carotenoids during the non-breeding season when its main signalling function may be relaxed. Progress towards uncovering the significance of concealment and subsequent display of colour expression should consider the potential binding and protecting nature of feather proteins associated with carotenoids.     

Function of bright coloration in the wasp spider Argiope bruennichi (Araneae: Araneidae)

There are two major competing explanations for the counter-intuitive presence of bright coloration in certain orb-web spiders. Bright coloration could lure insect prey to the web vicinity, increasing the spider's foraging success. Alternatively, the markings could function as disruptive camouflage, making it difficult for the insect prey to distinguish spiders from background colour variation. We measured the prey capture rates of wasp spiders, Argiope bruennichi, that were blacked out, shielded from view using a leaf fragment, or left naturally coloured. Naturally coloured spiders caught over twice the number of prey as did either blacked-out or leaf-shielded spiders, and almost three times as many orthopteran prey. Spectrophotometer measurements suggest that the bright yellow bands on the spider's abdomen are visible to insect prey, but not the banding on the legs, which could disguise the spider's outline. Thus, our results provide strong support for the hypothesis that bright coloration in the wasp spider acts as a visual lure for insect prey and weak support for the hypothesis that the arrangement of the banding pattern across the spider's body disguises the presence of the spider on the web.     

Autumn leaves seen through herbivore eyes

Why leaves of some trees turn red in autumn has puzzled biologists for decades, as just before leaf fall the pigments causing red coloration are newly synthesized. One idea to explain this apparently untimely investment is that red colour signals the tree's quality to herbivorous insects, particularly aphids. However, it is unclear whether red leaves are indeed less attractive to aphids than green leaves. Because aphids lack a red photoreceptor, it was conjectured that red leaves could even be indiscernable from green ones for these insects. Here we show, however, that the colour of autumnal tree leaves that appear red to humans are on average much less attractive to aphids than green leaves, whereas yellow leaves are much more attractive. We conclude that, while active avoidance of red leaves by aphids is unlikely, red coloration in autumn could still be a signal of the tree's quality, or alternatively serve to mask the over-attractive yellow that is unveiled when the green chlorophyll is recovered from senescing leaves. Our study shows that in sensory ecology, receiver physiology alone is not sufficient to reveal the whole picture. Instead, the combined analysis of behaviour and a large set of natural stimuli unexpectedly shows that animals lacking a red photoreceptor may be able to differentiate between red and green leaves.     

Autumn colouration and herbivore resistance in mountain birch (Betula pubescens)

We explored Hamilton and Brown's autumn signalling hypothesis in mountain birch (Betula pubescens). As predicted by the hypothesis, early autumn colour change (i.e. high degree of autumn colouration in September) was negatively correlated with insect damage the following season. Furthermore, as expected, indices of physiological stress (i.e. leaf fluctuating asymmetry) and reproductive investment (i.e. catkin production) were positively correlated with insect damage the following season. Indirectly, we also found support for the idea that the proposed handicap signal (i.e. early autumn senescence) might be associated with an honesty ensuring cost in terms of lost primary production. Further work is, however, required to determine whether the link between autumn colours and insect damage observed in this study is causal.     

Do autumn leaf colours serve as a reproductive insurance against sucking herbivores?

Although autumn leaf colours of deciduous trees have been shown to protect against photo-oxidative damage, they are sometimes seen as signals to pests and predators. Here I modify the coevolution hypothesis of autumn leaf colours. I suggest that much of the within-population variation in autumn leaf colours can be explained by differences in the allocation of resources to sexual reproduction. According to the novel hypothesis, reproductively active woody plants produce early and intense autumn leaf colours in order to protect seeds and other reproductive tissues from pests that lay eggs in the autumn. If many seeds mature at times of leaf senescence or during the next summer, a woody plant will reallocate plenty of nitrogen to seeds. If sucking insects reproduce on such hosts, their flightless offspring will suffer poor-quality food after the ripening of seeds. Before this, however, insects will probably concentrate around the ripening seeds to forage on nitrogen-rich veins. This will decline the quality and quantity of developing seeds. If, on the other hand, insects are able to recognize reproductively active plants while laying eggs in the autumn, both the insects and the plants benefit. The flightless offspring of insects feeds on plants that supply sufficiently nitrogen for longer than reproducing plants do, while these optimise their reproduction by avoiding pests, which also contributes to the abundance of specialist pests. Hence, I suppose that while physiological factors are the origin of autumnal colour changes of deciduous leaves, the visible cue utilized by insects has evolved several times to an honest signal that reveals the unsuitability of the potential host in the near future. The reproductive insurance hypothesis may help us to understand why bright autumn leaf colours are rare among herbaceous plants, and why plants at high altitudes and latitudes are often brightly coloured in autumn.     

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。