Visual ecology of aphids—a critical review on the role of colours in host finding

We review the rich literature on behavioural responses of aphids (Hemiptera: Aphididae) to stimuli of different colours. Only in one species there are adequate physiological data on spectral sensitivity to explain behaviour crisply in mechanistic terms. Because of the great interest in aphid responses to coloured targets from an evolutionary, ecological and applied perspective, there is a substantial need to expand these studies to more species of aphids, and to quantify spectral properties of stimuli rigorously. We show that aphid responses to colours, at least for some species, are likely based on a specific colour opponency mechanism, with positive input from the green domain of the spectrum and negative input from the blue and/or UV region. We further demonstrate that the usual yellow preference of aphids encountered in field experiments is not a true colour preference but involves additional brightness effects. We discuss the implications for agriculture and sensory ecology, with special respect to the recent debate on autumn leaf colouration. We illustrate that recent evolutionary theories concerning aphid–tree interactions imply far-reaching assumptions on aphid responses to colours that are not likely to hold. Finally we also discuss the implications for developing and optimising strategies of aphid control and monitoring.     

Genotypic variation in yellow autumn leaf colours explains aphid load in silver birch

? It has been suggested that autumn-migrating insects drive the evolution of autumn leaf colours. However, evidence of genetic variation in autumn leaf colours in natural tree populations and the link between the genetic variation and herbivore abundances has been lacking. ? Here, we measured the size of the whole aphid community and the development of green-yellow leaf colours in six replicate trees of 19 silver birch (Betula pendula) genotypes at the beginning, in the middle and at the end of autumn colouration. We also calculated the difference between green leaf and leaf litter nitrogen (N) and estimated the changes in phloem sap N loading. ? Autumn leaf colouration had significant genetic variation. During the last survey, genotypes that expressed the strongest leaf reflectance 2-4 wk earlier had an abundance of egg-laying Euceraphis betulae females. Surprisingly, the aphid community size during the first surveys explained N loss by the litter of different birch genotypes. ? Our results are the first evidence at the tree intrapopulation genotypic level that autumn-migrating pests have the potential to drive the evolution of autumn leaf colours. They also stress the importance of recognizing the role of late-season tree-insect interactions in the evolution of herbivory resistance.     

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.     

Herbivore and pathogen effects on tree growth are additive,but mediated by tree diversity and plant traits

Herbivores and fungal pathogens are key drivers of plant community composition and functioning. The effects of herbivores and pathogens are mediated by the diversity and functional characteristics of their host plants. However, the combined effects of herbivory and pathogen damage, and their consequences for plant performance, have not yet been addressed in the context of biodiversity–ecosystem functioning research. We analyzed the relationships between herbivory, fungal pathogen damage and their effects on tree growth in a large‐scale forest‐biodiversity experiment. Moreover, we tested whether variation in leaf trait and climatic niche characteristics among tree species influenced these relationships. We found significant positive effects of herbivory on pathogen damage, and vice versa. These effects were attenuated by tree species richness—because herbivory increased and pathogen damage decreased with increasing richness—and were most pronounced for species with soft leaves and narrow climatic niches. However, herbivory and pathogens had contrasting, independent effects on tree growth, with pathogens decreasing and herbivory increasing growth. The positive herbivory effects indicate that trees might be able to (over‐)compensate for local damage at the level of the whole tree. Nevertheless, we found a dependence of these effects on richness, leaf traits and climatic niche characteristics of the tree species. This could mean that the ability for compensation is influenced by both biodiversity loss and tree species identity—including effects of larger‐scale climatic adaptations that have been rarely considered in this context. Our results suggest that herbivory and pathogens have additive but contrasting effects on tree growth. Considering effects of both herbivory and pathogens may thus help to better understand the net effects of damage on tree performance in communities differing in diversity. Moreover, our study shows how species richness and species characteristics (leaf traits and climatic niches) can modify tree growth responses to leaf damage under real‐world conditions.     

Tree diversity promotes generalist herbivore community patterns in a young subtropical forest experiment

Stand diversification is considered a promising management approach to increasing the multifunctionality and ecological stability of forests. However, how tree diversity affects higher trophic levels and their role in regulating forest functioning is not well explored particularly for (sub)tropical regions. We analyzed the effects of tree species richness, community composition, and functional diversity on the abundance, species richness, and beta diversity of important functional groups of herbivores and predators in a large-scale forest biodiversity experiment in south-east China. Tree species richness promoted the abundance, but not the species richness, of the dominant, generalist herbivores (especially, adult leaf chewers), probably through diet mixing effects. In contrast, tree richness did not affect the abundance of more specialized herbivores (larval leaf chewers, sap suckers) or predators (web and hunting spiders), and only increased the species richness of larval chewers. Leaf chemical diversity was unrelated to the arthropod data, and leaf morphological diversity only positively affected oligophagous herbivore and hunting spider abundance. However, richness and abundance of all arthropods showed relationships with community-weighted leaf trait means (CWM). The effects of trait diversity and CWMs probably reflect specific nutritional or habitat requirements. This is supported by the strong effects of tree species composition and CWMs on herbivore and spider beta diversity. Although specialized herbivores are generally assumed to determine herbivore effects in species-rich forests, our study suggests that generalist herbivores can be crucial for trophic interactions. Our results indicate that promoting pest control through stand diversification might require a stronger focus on identifying the best-performing tree species mixtures.     

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.     

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.     

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.     

A trait‐based plant economic framework can help increase the value of reforestation for conservation

While reforestation is gaining momentum to moderate climate change via carbon sequestration, there is also an opportunity to use tree planting to confront declining global biodiversity. Where tree species vary in support of diversity, selecting appropriate species for planting could increase conservation effectiveness. We used a common garden experiment in Borneo using 24 native tree species to examine how variation among tree species in their support of beetle diversity is predicted by plant traits associated with “acquisitive” and “conservative” resource acquisition strategies. We evaluate three hypotheses: (1) beetle communities show fidelity to host identity as indicated by variation in abundance and diversity among tree species, (2) the leaf economic spectrum partially explains this variation as shown by beetle preferences for plant species that are predicted by plant traits, and (3) a small number of selected tree species can capture higher beetle species richness than a random tree species community. We found high variation among tree species in supporting three highly intercorrelated metrics of beetle communities: abundance, richness, and Shannon diversity. Variation in support of beetle communities was predicted by plant traits and varied by plant functional groups; within the dipterocarp family, high beetle diversity was predicted by conservative traits such as high wood density and slow growth, and in non‐dipterocarps by the acquisitive traits of high foliar K and rapid growth. Using species accumulation curves and extrapolation to twice the original sample size, we show that 48 tree species were not enough to reach asymptote levels of beetle richness. Nevertheless, species accumulation curves of the six tree species with the highest richness had steeper slopes and supported 33% higher richness than a random community of tree species. Reforestation projects concerned about conservation can benefit by identifying tree species with a disproportional capacity to support biodiversity based on plant traits.     

Intra-specific leaf trait responses to species richness at two different local scales

Plant functional traits, especially leaf traits, are accepted proxies for ecosystem properties. Typically, they are measured at the species level, neglecting within-species variation. While there is extensive knowledge about functional trait changes (both within and across species) along abiotic gradients, little is known about biotic influences, in particular at local scales. Here, we used a large biodiversity-ecosystem functioning experiment in subtropical China to investigate intra-specific trait changes of 16 tree species as a response to species richness of the local neighbourhood. We hypothesized that because of positive complementarity effects, species shift their leaf traits towards a more acquisitive growth strategy, when species richness of the local neighbourhood is higher. The trait shift should be most pronounced, when a focal tree's closest neighbour is from a different species, but should still be detectable as a response to species richness of the directly surrounding tree community. Consequently, we expected that trees with a con-specific closest neighbour have the strongest response to species richness of the surrounding tree community, i.e., the steepest increase of acquisitive traits. Our results indicate that species diversity promoted reduced competition and complementarity in resource use at both spatial scales considered. In addition, the closest neighbour had considerably stronger effects than the surrounding tree community. As expected, trees with a con-specific nearest neighbour showed the strongest trait shifts. However, the predicted positive effect of local hetero-specificity disappeared at the highest diversity levels of the surrounding tree community, potentially resulting from a higher probability to meet a strong competitor in a diverse environment. Our findings show that leaf traits within the same species vary not only in response to changing abiotic conditions, but also in response to local species richness. This highlights the benefit of including within-species trait variation when analysing relationships between plant functional traits and ecosystem functions.     

Shifts in trait means and variances in North American tree assemblages: species richness patterns are loosely related to the functional space

One of the key hypothesized drivers of gradients in species richness is environmental filtering, where environmental stress limits which species from a larger species pool gain membership in a local community owing to their traits. Whereas most studies focus on small‐scale variation in functional traits along environmental gradient, the effect of large‐scale environmental filtering is less well understood. Furthermore, it has been rarely tested whether the factors that constrain the niche space limit the total number of coexisting species. We assessed the role of environmental filtering in shaping tree assemblages across North America north of Mexico by testing the hypothesis that colder, drier, or seasonal environments (stressful conditions for most plants) constrain tree trait diversity and thereby limit species richness. We assessed geographic patterns in trait filtering and their relationships to species richness pattern using a comprehensive set of tree range maps. We focused on four key plant functional traits reflecting major life history axes (maximum height, specific leaf area, seed mass, and wood density) and four climatic variables (annual mean and seasonality of temperature and precipitation). We tested for significant spatial shifts in trait means and variances using a null model approach. While we found significant shifts in mean species’ trait values at most grid cells, trait variances at most grid cells did not deviate from the null expectation. Measures of environmental harshness (cold, dry, seasonal climates) and lower species richness were weakly associated with a reduction in variance of seed mass and specific leaf area. The pattern in variance of height and wood density was, however, opposite. These findings do not support the hypothesis that more stressful conditions universally limit species and trait diversity in North America. Environmental filtering does, however, structure assemblage composition, by selecting for certain optimum trait values under a given set of conditions.     

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.     

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.     

Effects of leaf litter species on macroinvertebrate community properties and mosquito yield in Neotropical tree hole microcosms

Detritus quality and quantity affect macroinvertebrate productivity and distribution in many freshwater ecosystems. This study experimentally investigated the effects of leaf litter from Ceiba pentandra, Dipteryx panamensis, Ficus yoponensis, and Platypodium elegans on macroinvertebrate species composition, richness, and abundance in artificial water-filled tree holes in a lowland moist forest of Panama. Species composition was similar among treatments, but species richness and longevity differed among litter types and were consistently highest with Platypodium litter. Similar patterns were observed in natural tree holes of the focal tree species. The mosquito Culex mollis was the most abundant species in the field experiment. Average conductivity and dissolved oxygen concentration differed among leaf species, but pH did not. Leaf toughness was positively correlated with mean macroinvertebrate abundance and cumulative species richness. A laboratory experiment measured C. mollis yield and pupation time in tree hole microcosms containing the four litter species. Cumulative mosquito mass and time to pupation differed among leaf litter species, with Platypodium litter supporting the greatest yield. Pupation was slowest on Ceiba litter. Grazing by mosquito larvae facilitated leaf decomposition in all treatments. Results suggest that differences in macroinvertebrate species richness and mosquito yield can be attributed to differences in nutritional quality among litter species. Received: 14 October 1998 / Accepted: 21 February 1999     

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.     

Predation, resource availability, and community structure in Neotropical water-filled tree holes

Predation and resource availability influence community structure in many aquatic ecosystems. Predators (odonates) and resources (leaf litter) were manipulated to determine their independent effects on macroorganism species richness, abundance, and composition in water-filled tree holes of Barro Colorado Island, Panama. Interactive effects of these factors were also investigated in artificial tree holes. Large odonates reduced species richness in natural tree holes, but did not significantly reduce macroorganism abundance. The presence of larvae of the mosquito Culex urichii and the ceratopogonid midge Bezzia snowi were negatively associated with the presence of large odonate larvae. In natural tree holes, leaf litter addition and removal respectively increased and decreased richness by c. 1 species relative to controls, and macroorganism abundance was greater in litter addition holes than in litter removal holes. Independent effects of predation showed similar patterns in artificial holes, but there was no predator2resource interaction, partly due to the short duration of the experiment. Predators grew faster when litter was abundant, and indirectly reduced litter degradation rates when resources were scarce in artificial holes. Both resource availability and predation influence species richness in water-filled tree holes, but act at different time scales; richness follows productivity (litter quantity) over a period of weeks, whereas effects of predation may span several months.     

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.     

Reprint of: Drivers of within-tree leaf trait variation in a tropical planted forest varying in tree species richness

In plant ecology, community-weighted trait means are often used as predictors for ecosystem functions. More recently, also within-species trait variation has been confirmed to contribute to ecosystem functioning. We here go even further and assess within-individual trait variation, assuming that every leaf in a plant individually adjusts to its micro-environment. Using forest plots varying in tree species richness (Sardinilla experiment, Panama), we analysed how leaf traits within individual trees vary along the vertical crown gradient. Furthermore, we tested whether niche partitioning in mixed stands results in a decrease of within-species leaf trait variation and whether niche partitioning can be also observed at the level of individual trees. We focused on leaf traits that describe the growth strategy along the conservative-acquisitive spectrum of growth. We found a decrease in within-species variation of specific leaf area (SLA) with increasing neighbourhood species richness. Both sampling height and local neighbourhood richness contributed to explaining within-species leaf trait variation, which however, varied in importance among different species and traits. With increasing sampling height, leaf dry matter content (LDMC), carbon to nitrogen ratio and lignin content increased, while leaf nitrogen concentration (leaf N), SLA, cellulose and hemicellulose decreased. Variation in leaf N decreased with increasing neighbourhood species richness, while the magnitude of within-individual variation of most traits was unaffected by neighbourhood species richness. Our results suggest an increased niche partitioning with increasing species richness both in a plant community and at the level of individual plants. Our findings highlight the importance of including within-individual trait variation to understand biodiversity-ecosystem functioning relationships.     

Drivers of within-tree leaf trait variation in a tropical planted forest varying in tree species richness

In plant ecology, community-weighted trait means are often used as predictors for ecosystem functions. More recently, also within-species trait variation has been confirmed to contribute to ecosystem functioning. We here go even further and assess within-individual trait variation, assuming that every leaf in a plant individually adjusts to its micro-environment. Using forest plots varying in tree species richness (Sardinilla experiment, Panama), we analysed how leaf traits within individual trees vary along the vertical crown gradient. Furthermore, we tested whether niche partitioning in mixed stands results in a decrease of within-species leaf trait variation and whether niche partitioning can be also observed at the level of individual trees. We focused on leaf traits that describe the growth strategy along the conservative-acquisitive spectrum of growth. We found a decrease in within-species variation of specific leaf area (SLA) with increasing neighbourhood species richness. Both sampling height and local neighbourhood richness contributed to explaining within-species leaf trait variation, which however, varied in importance among different species and traits. With increasing sampling height, leaf dry matter content (LDMC), carbon to nitrogen ratio and lignin content increased, while leaf nitrogen concentration (leaf N), SLA, cellulose and hemicellulose decreased. Variation in leaf N decreased with increasing neighbourhood species richness, while the magnitude of within-individual variation of most traits was unaffected by neighbourhood species richness. Our results suggest an increased niche partitioning with increasing species richness both in a plant community and at the level of individual plants. Our findings highlight the importance of including within-individual trait variation to understand biodiversity-ecosystem functioning relationships.     

The functional trait space of tree species is influenced by the species richness of the canopy and the type of forest

Analysing how species modify their trait expression along a diversity gradient brings insight about the role that intraspecific variability plays over species interactions, e.g. competition versus complementarity. Here, we evaluated the functional trait space of nine tree species dominant in three types of European forests (a continental‐Mediterranean, a mountainous mixed temperate and a boreal) growing in communities with different species richness in the canopy, including pure stands. We compiled whole‐plant and leaf traits in 1719 individuals, and used them to quantify species trait hypervolumes in communities with different tree species richness. We investigated changes along the species richness gradient to disentangle species responses to the neighbouring environment, in terms of hypervolume size (trait variance), shape (trait relative importance) and centroid translation (shifts of mean trait values) using null models. Our main results showed differences in trait variance and shifts of mean values along the tree diversity gradient, with shorter trees but with larger crowns in mixed stands. We found constrained functional spaces (trait convergence) in pure stands, suggesting an important intraspecific competition, and expanded functional spaces (trait divergence) in two‐species admixtures, suggesting competition release due to interspecific complementarity. Nevertheless, further responses to increasing species richness were different for each forest type, waning species complementarity in sites with limiting conditions for growth. Our results demonstrate that tree species phenotypes respond to the species richness in the canopy in European forests, boosting species complementarity at low level of canopy diversity and with a site‐specific pattern at greater level of species richness. These outcomes evidence the limitation of functional diversity measures based only on traits from pure stands or general trait database values.