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.     

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.     

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.     

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.     

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 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.     

Evidence from the domestication of apple for the maintenance of autumn colours by coevolution

The adaptive value of autumn colours is still a puzzle for evolutionary biology. It has been suggested that autumn colours are a warning signal to insects that use the trees as a host. I show that aphids (Dysaphis plantaginea) avoid apple trees (Malus pumila) with red leaves in autumn and that their fitness in spring is lower on these trees, which suggests that red leaves are an honest signal of the quality of the tree as a host. Autumn colours are common in wild populations but not among cultivated apple varieties, which are no longer under natural selection against insects. I show that autumn colours remain only in the varieties that are very susceptible to the effects of a common insect-borne disease, fire blight, and therefore are more in need of avoiding insects. Moreover, varieties with red leaves have smaller fruits, which shows that they have been under less effective artificial selection. This suggests a possible trade off between fruit size, leaf colour and resistance to parasites. These results are consistent with the hypothesis that autumn colours are a warning signal to insects, but not with other hypotheses.     

A field study with geometrid moths to test the coevolution hypothesis of red autumn colours in deciduous trees

Red autumn colouration of trees is the result of newly synthesized anthocyanin pigments in senescing autumn leaves. As anthocyanin accumulation is costly and the trait is not present in all species, anthocyanins must have an adaptive significance in autumn leaves. According to the coevolution hypothesis of autumn colours, red autumn leaves warn herbivorous insects – especially aphids that migrate to reproduce in trees in the autumn – that the tree will not be a suitable host for their offspring in spring due to a high level of chemical defence or lack of nutrients. The signalling allows trees to avoid herbivores and herbivores to choose better host trees. In this study the coevolution hypothesis was tested with four deciduous tree species that have red autumn leaf colouration – European aspen (Populus tremula L.) (Salicaceae), rowan (Sorbus aucuparia L.) (Rosaceae), mountain birch [Betula pubescens ssp. czerepanovii (NI Orlova) Hämet‐Ahti], and dwarf birch (Betula nana L.) (Betulaceae), and with two generalist herbivores, the autumnal moth [Epirrita autumnata (Borkhausen)] and the winter moth [Operophtera brumata (L.)] (both Lepidoptera: Geometridae). Anthocyanin concentrations of autumn leaves were determined from leaf samples and the growth performance parameters of the moth larvae on the study trees were measured in the spring. Trees with higher anthocyanin concentration in the autumn were predicted to be low‐quality food for the herbivores. Our results clearly showed that anthocyanin concentration was not correlated with the growth performance of the moths in any of the studied tree species. Thus, our study does not support the coevolution hypothesis of autumn colours.     

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.     

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.     

Catching a red herring: autumn colours and aphids

The purpose of this note is not to support any particular hypothesis explaining the evolution of red coloured autumn leaves, but to present evidence that shows existing knowledge does not support one such hypothesis – that red coloured leaves evolved as a signal to protect trees from aphids feeding and laying eggs on them in autumn. An alternative hypothesis is that autumn-feeding aphids are senescence-feeders, evolved to feed only on senescing leaves. These aphids are programmed to detect and feed on such leaves when they are still green and yellow and actively exporting their nutrients. Aphids reject or ignore red leaves because they are no longer good food, not because they are protecting the trees from the aphids.     

Red reveals branch die-back in Norway maple Acer platanoides

Background and Aims

Physiological data suggest that autumn leaf colours of deciduous trees are adaptations to environmental stress. Recently, the evolution of autumn colouration has been linked to tree condition and defence. Most current hypotheses presume that autumn colours vary between tree individuals. This study was designed to test if within-tree variation should be taken into account in experimental and theoretical research on autumn colouration.

Methods

Distribution of red autumn leaf colours was compared between partially dead and vigorous specimens of Norway maple (Acer platanoides) in a 3-year study. In August, the amount of reddish foliage was estimated in pairs of partially dead and control trees. Within-tree variation in the distribution of reddish leaves was evaluated. Leaf nitrogen and carbon concentrations were analysed.

Key Results

Reddish leaf colours were more frequent in partially dead trees than in control trees. Reddish leaves were evenly distributed in control trees, while patchiness of red leaf pigments was pronounced in partially dead trees. Large patches of red leaves were found beneath or next to dead tree parts. These patches reoccurred every year. Leaf nitrogen concentration was lower in reddish than in green leaves but the phenomenon seemed similar in both partially dead and control trees.

Conclusions

The results suggest that red leaf colouration and branch condition are interrelated in Norway maple. Early reddish colours may be used as an indication of leaf nitrogen and carbon levels but not as an indication of tree condition. Studies that concentrate on entire trees may not operate at an optimal level to detect the evolutionary mechanisms behind autumnal leaf colour variation.Key words: Acer platanoides, Norway maple, branch die-back, coevolution hypothesis, leaf senescence, patchy distribution, red leaf pigments, tree condition, within-tree variation     

Aphids do not attend to leaf colour as visual signal, but to the handicap of reproductive investment

The evolution of visual warning signals is well known in animals but has received scant attention in plants. The coevolutionary hypothesis is the most influential hypothesis on warning signals in plants proposing that red and yellow leaf colours in autumn signal defensive strength to herbivores. So far, evidence in support of the hypothesis, which assumes a coevolutionary origin of autumnal leaf colours, is correlative and open to alternative explanations. We therefore tested the coevolutionary hypothesis experimentally by colouring the leaves either red or green of same-aged mountain ash (Sorbus aucuparia) individuals. We monitored the response of winged aphids to leaf colour using insect glue on branches with natural and artificial leaf colours in each individual. In contrast to the prediction of the coevolutionary hypothesis, aphid numbers did not differ between the individuals with artificial green or artificial red leaves. Likewise, at the within-plant level, aphids did not colonize branches with natural green leaves preferentially. However, we suggest that plants emitted warning signals because aphids colonized the hosts non-randomly. We found a strong positive correlation between aphid numbers and fruit production, suggesting an allocation trade-off between investment in plant defence and reproduction. Our study demonstrates that aphids use warning signals or cues in host selection, probably volatiles, but that they did not use leaf colour.     

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.     

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.     

Classification of hypotheses on the evolution of autumn colours

I review the hypotheses that have been proposed to explain the adaptive value of autumn leaf colours. The available adaptive hypotheses can be reduced to the following. Photoprotection: pigments protect against photoinhibition or photooxidation allowing a more efficient recovery of nutrients. Drought resistance: pigments decrease osmotic potential allowing leaves to tolerate water stress. Leaf warming: pigments convert light into heat and warm leaves. Fruit flag: colour attracts animals that help disperse seeds. Coevolution: colour signals that the tree is not a suitable host for insects. Camouflage: colour makes leaves less detectable to herbivores. Anticamouflage: colour enhances conspicuousness of parasites dwelling on leaves to predators or parasitoids. Unpalatability: pigments act as direct anti-feedants against herbivores. Reduced nutrient loss: yellow leaves have less to lose against herbivory. Tritrophic mutualism: colour attracts aphids which attract ants that defend the trees from other insects. For each hypothesis I mention the original references, I define assumptions and predictions, and I discuss briefly conceptual problems and available evidence.     

Colors of young and old spring leaves as a potential signal for ant-tended hemipterans

A new hypothesis explaining the adaptive significance of bright autumn leaf colors argues that these colors signal tree quality to myrmecophilous specialist aphids. In turn, the aphids attract aphid-tending ants during the following spring, which defend the trees from other aphids and herbivores. In this context, other types of plant coloration, such as the color change observed in young and old spring leaves, may function as a signal of plant quality for aphids and other myrmecophilous hemipterans. If these plant colors are costly for plants, then vividly colorful plants would be required to invest more in growth than in defense; as a result, colorful plants may be more palatable for honeydew-producing hemipterans, such as aphids, scale insects and treehoppers, although the relative importance of hemipterans other than aphids may be relatively low. These hemipterans may be attracted to colorful plants, after which their attendant ants would protect the plants from herbivory. However, it is necessary to examine color vision in hemipterans to support this hypothesis.Key words: ant-Hemiptera interactions, indirect effects, myrmecophiles, plant-ant mutualism, plant coloration, tritrophic interactionsRecently, the adaptive significance of plant coloration has attracted scientific interest.¹ Various theories have been postulated to explain the adaptive value of autumn leaf colors (red and yellow).² The coevolution hypothesis, the most novel and challenging theory among those proposed, argues that bright leaf colors serve as a conspicuous defense signal against autumn-colonizing insect herbivores, particularly aphids.³ According to this hypothesis, the production of autumn color pigments is an indicator of a particularly vigorous tree. Aphids, which have color vision and have long been associated with trees, migrate to winter host trees in the autumn and cause substantial damage. Therefore, vivid leaf color in the autumn would encourage aphids to colonize other less vigorously defended trees.⁴ Hamilton and Brown³ and Holopainen and Peltonen⁵ detected a higher number of specialist aphids on tree species with more intense autumn colors.After Hamilton and Brown,³ several researchers have attempted to explain the relationship between aphids and autumn color.^2,6 However, they did not account for several possibilities.⁶ First, healthy, vigorous trees may not be well defended, because they invest more in growth than in defense. Second, some aphid species avoid colonizing trees with bright colors, whereas others are attracted to bright colors. Finally, there are numerous multispecific interactions between plants, herbivores, predators and parasitoids in tree crowns. Ants prey on various arthropods living in trees, and ant-aphid mutualism affects arboreal arthropod communities. I incorporated these factors and formed a hypothesis in which autumn leaf colors signal tree quality to myrmecophilous specialist aphids. These aphids, in turn, attract aphid-tending ants during the following spring, which then defend the trees from other aphids and herbivores. Thus, autumn colors may be adaptive, because they attract myrmecophilous specialist aphids and their attendant ants, thereby reducing herbivory and interspecific competition among aphids.⁶In this addendum, I extend my former hypothesis beyond the relationship between autumn leaf colors and aphids. First, myrmecophilous aphids are not the only arthropods that benefit trees. Styrsky and Eubanks⁷ recently reviewed the literature regarding the effects of interactions between ants and honeydew-producing hemipterans on plants, and found that plants actually benefited indirectly from these interactions in most cases. This finding supports a new hypothesis focused on plant-ant mutualism via aphids. In addition, the mutualism between ants and honeydew-producing hemipterans includes many other organisms in addition to aphids, such as scale insects and treehoppers. Scale insects, especially soft scales (Coccidae) and mealybugs (Pseudococcidae), comprise many species that are tended by honeydew-collecting ants,⁸ and ant-scale insect mutualism is often beneficial for host plants.⁷ Although the female adults of scale insects are usually immobile, first-instar nymphs (crawlers) disperse by wind and locate on host plants, usually trees.⁹ The nymphs, emerging at various times from spring to autumn,¹⁰ may use plant coloration to select a suitable host. However, because specialist coccids and mealybugs represent a minority among the speciose scale insects,10 coevolutionary relationships between plants and ants via specialist scale insects may be relatively rare. The treehoppers also comprise many myrmecophilous species,^8,11 but the diversity of this group is highest in tropical regions; only a relatively small number of membracid species are present in temperate regions.¹² Therefore, scale insects and treehoppers may be attracted to autumn colors, and their attendant ants may then defend trees against other herbivorous insects. To fully account for the adaptive value of autumn colors, one would expect the importance of these hemipterans to be less than that of aphids, based on their low host-plant specificity, restricted distribution and life cycles. However, hemipterans may be associated with plant coloration in other aspects than autumn leaf color.Second, the colors of young and old spring leaves may also signal plant quality to ant-tended honeydew-producing hemipterans. The young leaves of many plants are reddish or yellowish (Fig. 1A and B).¹³ In the spring and other seasons, the old leaves of some evergreen tree species turn red or yellow (Fig. 1B). Because changes in leaf color may occur from spring to autumn, various hemipteran species may play specific roles as the season progresses. Aphids migrate in the spring and in the autumn,¹⁴ although most host-alternating aphids migrate to trees in autumn and to herbs in the late spring in temperate regions.¹⁵ If plants pay some cost for these colors¹⁶ and vivid colors indicate high plant quality for hemipterans, then changing colors may attract myrmecophilous hemipterans including aphids, scale insects and treehoppers, which may then protect plants against herbivory by other insects.Open in a separate windowFigure 1(A) Red young leaves of the evergreen oak Quercus glauca. (B) Yellowish young and reddish old leaves of the camphor tree Cinnamomum camphora.However, color vision has not been examined in detail in most hemipteran insects.^17,18 Many insects are insensitive to red, although one species of flower-visiting thrip is specifically attracted to red flowers.¹⁹ Thus, studies on color vision in hemipteran insects are required to evaluate this new hypothesis, as well as the coevolution hypothesis.     

Phylogenetic analysis reveals a scattered distribution of autumn colours

Background and Aims

Leaf colour in autumn is rarely considered informative for taxonomy, but there is now growing interest in the evolution of autumn colours and different hypotheses are debated. Research efforts are hindered by the lack of basic information: the phylogenetic distribution of autumn colours. It is not known when and how autumn colours evolved.

Methods

Data are reported on the autumn colours of 2368 tree species belonging to 400 genera of the temperate regions of the world, and an analysis is made of their phylogenetic relationships in order to reconstruct the evolutionary origin of red and yellow in autumn leaves.

Key Results

Red autumn colours are present in at least 290 species (70 genera), and evolved independently at least 25 times. Yellow is present independently from red in at least 378 species (97 genera) and evolved at least 28 times.

Conclusions

The phylogenetic reconstruction suggests that autumn colours have been acquired and lost many times during evolution. This scattered distribution could be explained by hypotheses involving some kind of coevolutionary interaction or by hypotheses that rely on the need for photoprotection.Key words: Autumn colour, leaf colour, comparative analysis, coevolution, photoprotection, phylogenetic analysis     

Spring versus autumn leaf colours: Evidence for different selective agents and evolution in various species and floras

Red colouration is common in young and old leaves of broadleaf woody species. Assuming that leaf colours are adaptive, we examined, by comparing the colouration in young versus old leaves, the possibility that different selection agents may have operated on spring versus autumn leaf colouration. We observed spring versus autumn colouration in three very different woody floras (Finland, Japan and Israel) in order to allow for a broad ecological and evolutionary spectrum. The null hypothesis was that if the same selective agents operated in spring and autumn, it is expected that when spring leaves are red, they should always be red in autumn, and when spring leaves are green, they should be green or yellow in autumn. We found that green spring leaves are almost exclusively associated with yellow leaf colour at senescence in autumn. Species with red autumn leaves almost always have at least some red colouration in their spring leaves. However, about half of the species with red spring leaves have yellow autumn leaves. Brown autumn leaves were not common in the species we studied. As about half of the species with red spring leaves have yellow autumn leaves but not vice versa, we conclude that there are many cases in which the selecting agents for spring versus autumn leaf colour were not the same.     

Loss of autumn colors under domestication: A byproduct of selection for fruit flavor?

According to the coevolution hypothesis the red autumn leaves of certain tree species are a warning signal towards insects that lay their eggs on the trees. A recent study has shown that red leaves are common in wild varieties of apple (Malus pumila) but not in cultivated varieties. This suggests that autumn colors have been lost during domestication due to relaxed selection against insects. The few varieties with red leaves have small fruits, similar to their wild ancestors, which shows that they have been under less effective artificial selection. As expected by the coevolution hypothesis these red varieties are very susceptible to an insect-borne disease, fire blight. Here I report further data on the loss of autumn colors under domestication. Since red leaf color is correlated with red fruit flesh color, if red fruit flesh has more astringent taste it is possible that loss of autumn colors is not only due to relaxed selection against insect, but also to direct artificial selection against astringent taste. However even varieties with yellow flesh turn out to have astringent taste. Moreover, while red fruit flesh is common in cultivated varieties with red leaves, it is very rare in wild varieties. It is unclear, therefore, whether loss of autumn color under domestication was a byproduct of artificial selection against red fruit flesh.Key words: coevolution, autumn colors, signaling, apple, Malus pumila, domestication, artificial selection, germplasm