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.     

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.     

Do aphids paint the tree red (or yellow)—can herbivore resistance or photoprotection explain colourful leaves in autumn?

We explored two mutually nonexclusive hypotheses on autumnal leaf colouration. The co-evolutionary hypothesis states that autumnal leaf colouration functions as a handicap signal to herbivorous insects, whereas the photoprotection hypothesis posits that plant pigments primarily protect the plant against cold-induced photoinhibition and enhance nutrient transfer. To contrast both hypotheses, we compared yellow and red leaf colouration in three groups of mountain ash (Sorbus aucuparia L.). Two montane groups of different age were characterised by low aphid numbers and low temperature, and a lowland group by high aphid numbers and high temperature. There were no consistent altitudinal differences in leaf colouration. Compared to young trees, adult trees developed fewer red but more yellow leaves at high altitude. In the lowland population, the development of red leaf colour was related to decreasing daytime temperature, whereas the appearance of yellow leaf colouration corresponded to the decreasing photoperiod. This is consistent with the photoprotection hypothesis. Individual differences in red and yellow leaf colouration were inversely correlated to the number of fruits, which might be interpreted as a trade-off between reproductive and protective commitment. Temperature effects explained variation in aphid numbers over time and leaf colouration explained aphid distribution on a given day. As predicted by the co-evolutionary hypothesis, strongly coloured individuals harboured fewer aphids than green or dull-coloured ones. Since decreasing temperature reduced the number of migrating aphids but induced red leaf colouration, these processes are not mutually fine-tuned, which likely restricts the potential for co-evolution between mountain ash and aphids.     

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.     

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.     

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.     

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.     

Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds

Many plants respond to herbivory with an increased production of extrafloral nectar (EFN) and/or volatile organic compounds (VOCs) to attract predatory arthropods as an indirect defensive strategy. In this study, we tested whether these two indirect defences fit the optimal defence hypothesis (ODH), which predicts the within-plant allocation of anti-herbivore defences according to trade-offs between growth and defence. Using jasmonic acid-induced plants of Phaseolus lunatus and Ricinus communis, we tested whether the within-plant distribution pattern of these two indirect defences reflects the fitness value of the respective plant parts. Furthermore, we quantified photosynthetic rates and followed the within-plant transport of assimilates with (13)C labelling experiments. EFN secretion and VOC emission were highest in younger leaves. Moreover, the photosynthetic rate increased with leaf age, and pulse-labelling experiments suggested transport of carbon to younger leaves. Our results demonstrate that the ODH can explain the within-plant allocation pattern of both indirect defences studied.     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

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.     

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     

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.     

Plants on red alert: do insects pay attention?

Two recent hypotheses have proposed that non-green plant colouration evolved as a defence against herbivores, either as protective colouration promoting handicap signals indicating plant fitness or by undermining their crypsis. The handicap hypothesis posits a co-evolutionary process between plants and herbivores, whereas the anti-crypsis hypothesis suggests that an arms race between insects and plants is the evolutionary mechanism. Both explanations assume that insects are the evolutionary origin causing plants' colouration. Here, we propose a different hypothesis, termed the "Defence Indication hypothesis". This idea focuses on the multiple protective functions of anthocyanins and carotenoids as pigments, and suggests that plant colouration evolved primarily in response to various stressors. Because pigments and defensive compounds share a common biosynthesis, the production of pigments also provides elevated defensive strengths against herbivores, a process termed priming. In effect, the Defence Indication hypothesis predicts that pleiotropic effects of the pigments and, more generally, plants' shared defence responses, explain why insects might react to plant colouration.     

Ecological trade-offs between jasmonic acid-dependent direct and indirect plant defences in tritrophic interactions

Recent studies on plants genetically modified in jasmonic acid (JA) signalling support the hypothesis that the jasmonate family of oxylipins plays an important role in mediating direct and indirect plant defences. However, the interaction of two modes of defence in tritrophic systems is largely unknown. In this study, we examined the preference and performance of a herbivorous leafminer (Liriomyza huidobrensis) and its parasitic wasp (Opius dissitus) on three tomato genotypes: a wild-type (WT) plant, a JA biosynthesis (spr2) mutant, and a JA-overexpression 35S::prosys plant. Their proteinase inhibitor production and volatile emission were used as direct and indirect defence factors to evaluate the responses of leafminers and parasitoids. Here, we show that although spr2 mutant plants are compromised in direct defence against the larval leafminers and in attracting parasitoids, they are less attractive to adult flies compared with WT plants. Moreover, in comparison to other genotypes, the 35S::prosys plant displays greater direct and constitutive indirect defences, but reduced success of parasitism by parasitoids. Taken together, these results suggest that there are distinguished ecological trade-offs between JA-dependent direct and indirect defences in genetically modified plants whose fitness should be assessed in tritrophic systems and under natural conditions.     

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.     

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.     

Life-history strategies affect aphid preference for yellowing leaves

According to the nutrient-translocation hypothesis, yellowing tree leaves are colonized by aphids at the end of the growing season owing to improved availability of nutrients in the phloem sap after chlorophyll degradation. We measured aphid densities on potted Betula pendula seedlings in a field site where a small proportion of foliage rapidly turned yellow before normal autumn coloration as a consequence of root anoxia. The number of adults and nymphs of the birch-feeding specialist aphids Euceraphis betulae, Betulaphis brevipilosa and Callipterinella tuberculata were counted from leaves on each of the 222 plants. Aphids were detected on 19 per cent of green leaves and on 41 per cent of yellow leaves. There was no indication of aphid avoidance of yellow leaves, and the number of winged (alate) viviparous E. betulae adults and their nymphs were significantly higher on yellow leaves than on green leaves, while the numbers of apterous B. brevipilosa and C. tuberculata did not differ between the leaf colour types. Our result suggests that only aphid species with alate generation during colour change can take advantage of yellowing leaves. This may explain the exceptional abundance of E. betulae compared with other aphid species on birches.     

Strategies of chemical anti-predator defences in leaf beetles: is sequestration of plant toxins less costly than de novo synthesis?

The evolution of defensive traits is driven both by benefits gained from protection against enemies and by costs of defence production. We tested the hypothesis that specialisation of herbivores on toxic host plants, accompanied by the ability to acquire plant defensive compounds for herbivore defence, is favoured by the lower costs of sequestration compared to de novo synthesis of defensive compounds. We measured physiological costs of chemical defence as a reduction in larval performance in response to repeated removal of secretions (simulating predator attack) and compared these costs between five species synthesising defences de novo and three species sequestering salicylic glucosides (SGs) from their host plants. Experiments simulating low predator pressure revealed no physiological costs in terms of survival, weight and duration of development in any of study species. However, simulation of high predation caused reduction in relative growth rate in Chrysomela lapponica larvae producing autogenous defences more frequently, than in larvae sequestering SGs. Still meta-analysis of combined data showed no overall difference in costs of autogenous and sequestered defences. However, larvae synthesising their defences de novo demonstrated secretion-conserving behaviour, produced smaller amounts of secretions, replenished them at considerably lower rates and employed other types of defences (regurgitation, evasion) more frequently when compared to sequestering larvae. These latter results provide indirect evidence for biosynthetic constraints for amounts of defensive secretions produced de novo, resulting in low defence effectiveness. Lifting these constraints by sequestration may have driven some leaf beetle lineages toward sequestration of plant allelochemicals as the main defensive strategy.     

Plant genotype mediates the effects of nutrients on aphids

Soil nutrients, and factors which influence their concentrations and bioavailability, form a basic component of bottom–up control of ecosystem processes, including plant–herbivore interactions. Increased nutrient levels are linked, through plant defence theory, with increased levels of herbivore susceptibility. The focal point of many ecological experiments examining this link is at the species level, where the response of single species is the average of many different genotypes. Here, we focus on the genetic basis of indirect ecological interactions. We investigated the effects of nutrient concentration on the population growth of an aphid herbivore across multiple genotypes of barley in relation to plant growth rate. In general, both aphid population size and plant growth rate increased with nutrient concentration. However, they were both dependent on the interaction between nutrient concentration and barley genotype. Our data raise the testable possibility of differential defense responses between genotypes of barley, for example divergent, fixed and inducible defences against aphids. We provide evidence that the indirect effects of soil nutrients on aphid population size are mediated by the genetics of the host plant.