Host phylogeny and nutrient content drive galler diversity and abundance on willows

1. Different groups of specialised herbivores often exhibit highly variable responses to host plant traits and phylogeny. Gall‐forming insects and mites on willows are highly adapted to their hosts and represent one of the richest communities of gallers associated with a single genus of host plants. 2. The present study evaluated the effects of host plant secondary metabolites (salicylates, flavonoids, condensed tannins), physical traits (trichome density), nutrient content (N:C) and phylogeny on the abundance and richness of gall‐forming arthropods associated with eight willow species and Populus tremula. 3. Galler abundance was affected by N:C rather than by willow defensive traits or phylogeny, suggesting that gallers respond differently to host plant traits than to less specialised guilds, such as leaf‐chewing insects. None of the studied defensive traits had a significant effect on gall abundance. Gall morphospecies richness was correlated with the host phylogeny, mainly with the nodes representing the inner division of the willow subgenus Vetrix. This suggests that the radiation of some willow taxa could have been important for the speciation of gallers associated with willows. 4. In conclusion, it is shown that whereas willow traits, such as nutrient content, appeared to affect abundances of gallers, it is probably willow radiation that drives galler speciation.     

Above‐ and belowground herbivory jointly impact defense and seed dispersal traits in Taraxacum officinale

Plants are able to cope with herbivores by inducing defensive traits or growth responses that allow them to reduce or avoid the impact of herbivores. Since above‐ and belowground herbivores differ substantially in life‐history traits, for example feeding types, and their spatial distribution, it is likely that they induce different responses in plants. Moreover, strong interactive effects on defense and plant growth are expected when above‐ and belowground herbivores are jointly present. The strengths and directions of these responses have been scarcely addressed in the literature. Using Taraxacum officinale, the root‐feeding nematode Meloidogyne hapla and the locust Schistocerca gregaria as a model species, we examined to what degree above‐ and belowground herbivory affect (1) plant growth responses, (2) the induction of plant defensive traits, that is, leaf trichomes, and (3) changes in dispersal‐related seed traits and seed germination. We compared the performance of plants originating from different populations to address whether plant responses are conserved across putative different genotypes. Overall, aboveground herbivory resulted in increased plant biomass. Root herbivory had no effect on plant growth. Plants exposed to the two herbivores showed fewer leaf trichomes than plants challenged only by one herbivore and consequently experienced greater aboveground herbivory. In addition, herbivory had effects that reached beyond the individual plant by modifying seed morphology, producing seeds with longer pappus, and germination success.     

Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on <Emphasis Type="Italic">Datura wrightii</Emphasis>

The costs and benefits of defensive traits in plants can have an ecological component that arises from the effect of defenses on the natural enemies of herbivores. We tested if glandular trichomes in Datura wrightii, a trait that confers resistance to several species of herbivorous insects, impose an ecological cost by decreasing rates of predation by the natural enemies of herbivores. For two common herbivores of D. wrightii, Lema daturaphila and Tupiocoris notatus, several generalized species of natural enemies exhibited lower rates of predation on glandular compared to non-glandular plants. Lower rates of predation were associated with reductions in the residence time and foraging efficiency of natural enemies on plants with glandular trichomes, but not with direct toxic effects of glandular exudate. Our results suggest that the benefit of resistance to herbivores conferred by glandular trichomes might be offset by the detrimental effect of this trait on the natural enemies of herbivores, and that the fitness consequences of this trichome defense might depend on the composition and abundance of the natural-enemy community.     

Global patterns of leaf defenses in oak species

Plant defensive traits drive patterns of herbivory and herbivore diversity among plant species. Over the past 30 years, several prominent hypotheses have predicted the association of plant defenses with particular abiotic environments or geographic regions. We used a strongly supported phylogeny of oaks to test whether defensive traits of 56 oak species are associated with particular components of their climatic niche. Climate predicted both the chemical leaf defenses and the physical leaf defenses of oaks, whether analyzed separately or in combination. Oak leaf defenses were higher at lower latitudes, and this latitudinal gradient could be explained entirely by climate. Using phylogenetic regression methods, we found that plant defenses tended to be greater in oak species that occur in regions with low temperature seasonality, mild winters, and low minimum precipitation, and that plant defenses may track the abiotic environment slowly over macroevolutionary time. The pattern of association we observed between oak leaf traits and abiotic environments was consistent with a combination of a seasonality gradient, which may relate to different herbivore pressures, and the resource availability hypothesis, which posits that herbivores exert greater selection on plants in resource-limited abiotic environments.     

Geographic association and temporal variation of chemical and physical defense and leaf damage in Datura stramonium

The evolution of plant defense traits has traditionally been explained trough the “coevolutionary arms race” between plants and herbivores. According to this, specialist herbivores have evolved to cope effectively with the defensive traits of their host plants and may even use them as a cue for host location. We analyzed the geographic association between leaf trichomes, two tropane alkaloids (putative resistance traits), and leaf damage by herbivores in 28 populations of Datura stramonium in central Mexico. Since the specialist leaf beetles Epitrix parvula and Lema trilineata are the main herbivores of D. stramonium in central Mexico, we predicted a positive association between plant defense and leaf damage across populations. Also, if physical environmental conditions (temperature or precipitation) constrain the expression of plant defense, then the geographic variation in leaf damage should be explained partially by the interaction between defensive traits and environmental factors. Furthermore, we studied the temporal and spatial variation in leaf trichome density and leaf damage in five selected populations of D. stramonium sampled in two periods (1997 vs. 2007). We found a positive association between leaf trichomes density and atropine concentration with leaf damage across populations. The interaction between defensive traits and water availability in each locality had a significant effect on the geographic variation in leaf damage. Differences among populations in leaf trichome density are maintained over time. Our results indicate that local plant–herbivore interaction plays an important role in shaping the geographic and temporal variation in plant defense in D. stramonium.     

Enemy release and plant invasion: patterns of defensive traits and leaf damage in Hawaii

Invasive species may be released from consumption by their native herbivores in novel habitats and thereby experience higher fitness relative to native species. However, few studies have examined release from herbivory as a mechanism of invasion in oceanic island systems, which have experienced particularly high loss of native species due to the invasion of non-native animal and plant species. We surveyed putative defensive traits and leaf damage rates in 19 pairs of taxonomically related invasive and native species in Hawaii, representing a broad taxonomic diversity. Leaf damage by insects and pathogens was monitored in both wet and dry seasons. We found that native species had higher leaf damage rates than invasive species, but only during the dry season. However, damage rates across native and invasive species averaged only 2% of leaf area. Native species generally displayed high levels of structural defense (leaf toughness and leaf thickness, but not leaf trichome density) while native and invasive species displayed similar levels of chemical defenses (total phenolics). A defense index, which integrated all putative defense traits, was significantly higher for native species, suggesting that native species may allocate fewer resources to growth and reproduction than do invasive species. Thus, our data support the idea that invasive species allocate fewer resources to defense traits, allowing them to outperform native species through increased growth and reproduction. While strong impacts of herbivores on invasion are not supported by the low damage rates we observed on mature plants, population-level studies that monitor how herbivores influence recruitment, mortality, and competitive outcomes are needed to accurately address how herbivores influence invasion in Hawaii.     

Plant defense and density dependence in the population growth of herbivores

Long-standing theory has predicted that plant defensive and nutritional traits contribute to the population dynamics of insect herbivores. To examine the role of plant variation in density dependence, I took a comparative approach by conducting density manipulation experiments with the specialist aphid, Aphis nerii, on 18 species of milkweed (Asclepias spp.). The strength of density dependence varied on the plant species. Variation in plant secondary compounds (cardenolides), trichomes, leaf carbon and nitrogen concentrations, and seed mass of the milkweed species predicted the R(max) of aphid populations, while specific leaf weight, carbon concentration, latex, water content, and trichome density were significant predictors of the strength of density dependence. Thus, plant traits that probably evolved for primary and defensive functions contribute to the ecological dynamics of herbivore populations.     

Family matters: effect of host plant variation in chemical and mechanical defenses on a sequestering specialist herbivore

Insect herbivores contend with various plant traits that are presumed to function as feeding deterrents. Paradoxically, some specialist insect herbivores might benefit from some of these plant traits, for example by sequestering plant chemical defenses that herbivores then use as their own defense against natural enemies. Larvae of the butterfly species Battus philenor (L.) (Papilionidae) sequester toxic alkaloids (aristolochic acids) from their Aristolochia host plants, rendering larvae and adults unpalatable to a broad range of predators. We studied the importance of two putative defensive traits in Aristolochia erecta: leaf toughness and aristolochic acid content, and we examined the effect of intra- and interplant chemical variation on the chemical phenotype of B. philenor larvae. It has been proposed that genetic variation for sequestration ability is ??invisible to natural selection?? because intra- and interindividual variation in host-plant chemistry will largely eliminate a role for herbivore genetic variation in determining an herbivore??s chemical phenotype. We found substantial intra- and interplant variation in leaf toughness and in the aristolochic acid chemistry in A. erecta. Based on field observations and laboratory experiments, we showed that first-instar larvae preferentially fed on less tough, younger leaves and avoided tougher, older leaves, and we found no evidence that aristolochic acid content influenced first-instar larval foraging. We found that the majority of variation in the amount of aristolochic acid sequestered by larvae was explained by larval family, not by host-plant aristolochic acid content. Heritable variation for sequestration is the predominant determinant of larval, and likely adult, chemical phenotype. This study shows that for these highly specialized herbivores that sequester chemical defenses, traits that offer mechanical resistance, such as leaf toughness, might be more important determinants of early-instar larval foraging behavior and development compared to plant chemical defenses.     

Correlations between leaf structural traits and the densities of herbivorous insect guilds

The functional composition of herbivorous insect assemblages was correlated with aspects of new and mature leaf surface features, anatomy and morphology across 18 co‐occurring plant species. Multivariate analyses of insects and leaf traits revealed that the functional composition of the herbivore assemblage was more strongly correlated with leaf structural traits than with leaf constituents. Leaf traits were more strongly correlated with the functional composition of the herbivore assemblage than with its taxonomic composition. Densities of sessile phloem feeders, ­rostrum chewers, and all herbivores were significantly negatively correlated with specific leaf weight, lamina and cuticle thickness, vascular tissue depth and stomate length, and were significantly positively correlated with stomate density. External chewer densities were significantly negatively correlated with percent lignified vein area, and significantly positively correlated with leaf surface area and the distance between lignified tissues. Spine‐like leaves were associated with significantly lower densities of sessile phloem feeders, external chewers and all herbivores compared to kite leaves (kite leaves are comprised of unfortified leaf tissue supported by a framework of vascular tissue). The presence of a thickened leaf hypodermis was associated with significantly lower densities of external chewers and rostrum chewers, while midrib protection was associated with significantly lower densities of external chewers. Leaf structural traits may not be the proximal factors influencing herbivorous insects, as leaf structural traits are correlated with many other plant traits such as photosynthetic rate, relative growth rate and leaf life‐span. Nonetheless, these results indicate that certain leaf structural traits may potentially be used to predict the functional structure of herbivorous insect assemblages. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77 , 43–65.     

Leaf mining in the Myrtaceae

Abstract 1. Leaf mining insects feed within plant tissue and thus have close physical associations with their host plants. Little is known about the evolution of relationships between leaf miners and their host species. 2. The prevalence of leaf mining was examined in relation to the phylogeny of a dominant family of Australian plants, the Myrtaceae. Sixty‐eight species from the 10 major phylogenetic groups within the family were sampled in south‐eastern Australia. 3. Fifty‐seven per cent of the plant species examined were found to be mined. Several leaf traits were compared between mined and unmined plant species to investigate the potential role of both physical and nutritional characteristics in determining host‐plant susceptibility to these herbivores. 4. The physical leaf traits measured were leaf area, specific leaf area (SLA), lamina thickness, toughness, and amount of fibre (percentage hemicellulose). The nutritional traits were water content, and concentrations of carbon, nitrogen, total phenols and condensed tannins. Principal component analysis showed mined plant species differed from unmined in terms of several leaf traits. 5. In a post hoc regression weighted for phylogeny, leaf miner presence was significantly positively correlated with plant species having thinner laminas and higher phenol concentrations, and was positively correlated with marginal significance to SLA and water content.     

Sucking herbivore assemblage composition on greenhouse <Emphasis Type="Italic">Ficus</Emphasis> correlates with host plant leaf architecture

Understanding arthropod herbivore selectivity trends towards host plant attributes is essential for predicting plant-associated herbivore assemblage structure. Little is known about such interactions between spontaneous herbivore species and cultivated plants under specific conditions of botanical garden greenhouses. In this study, the taxonomic and functional composition of sucking arthropod herbivore assemblages were correlated with leaf anatomical and surface features of 33 host species of Ficus L. (Moraceae) across four distantly located greenhouse complexes of botanical gardens. The analyses revealed that the species number and abundance of scale insects and their individual families, sessile phloem feeders, total phloem feeders and total herbivores were significantly positively correlated with the thickness of leaf lamina, epidermis and mesophyll, stomatal length and width, and the presence of abaxial multiple epidermis and weak ferruginous non-glandular trichomes. Significant negative correlations were revealed between the same herbivore parameters and the density of glandular trichomes. Heliomorphic leaves supported higher abundance and species richness of sessile phloem feeders compared to sciomorphic ones. The parameters of some phloem and mesophyll feeder taxa also correlated with non-glandular trichome length and density, type of trichomes and epicuticular wax layer, and the presence of calcium oxalate crystals in the epidermis. Results of the study suggest that the leaf architecture-related herbivory trends under greenhouse conditions are similar to those occurring in natural ecosystems when considering the functional significance of particular leaf traits, and remain relevant at the scale of particular plant taxa with disregard of spatial factor.     

THE EVOLUTION OF HOST-PLANT USE AND SEQUESTRATION IN THE LEAF BEETLE GENUS PHRATORA (COLEOPTERA: CHRYSOMELIDAE)

Leaf beetles in the genus Phratora differ in host plant use and in the chemical composition of their larval defensive secretion. Most species specialize on either poplars or willows (family Salicaceae), but two species feed on birch (family Betulaceae). Phratora vitellinae utilizes salicylates from the host plant to produce its larval secretion, which contains salicylaldehyde, while other Phratora species produce an autogenous secretion. To reconstruct the evolutionary history of host plant use and the larval secretion chemistry in this genus, we sequenced 1383 base pairs of the mt cytochrome oxidase I gene for six European and one North American Phratora species and three outgroup taxa. Bootstrap values of the complete nucleotide sequence were 99-100% for six of eight nodes in the maximum parsimony tree. They were 71% and 77% for the two other nodes. The maximum parsimony tree and the maximum likelihood tree based on nucleotide sequence showed the same relationships as a maximum parsimony tree based on the amino acid sequence. Beetle phylogeny overlapped broadly with host plant taxonomy and chemistry, and it revealed historical constraints influencing host plant use. However, there was one host shift from the willow family (Salicaceae) to the birch family (Betulaceae). The use of host plant phenol glycosides for the larval defensive secretion evolved along the lineage that led to P. vitellinae. Phratora vitellinae feeds on the taxonomically widest range of host plants, which are characterized by moderate to high levels of salicylates. The results support the hypothesis that the use of salicylates for the larval secretion evolved twice independently in chrysomeline leaf beetles.     

植食性昆虫适应植物防御反应的研究进展

在植物与植食性昆虫协同进化过程中,植物在不断完善其防御反应,同时植食性昆虫也在选择压下不断适应植物防御反应。植食性昆虫适应植物防御反应存在多样性。昆虫能够利用其唾液中的效应因子抑制或弱化植物防御反应,激活其肠道中的某些特异性蛋白阻断植物防御性次生代谢物的产生或者将其直接降解,以及通过其携带微生物间接抑制植物防御反应。此外,昆虫还能够通过产卵、虫害诱导植物挥发物、识别植物防御物质等方式适应植物的防御反应。本文综述了植食性昆虫如何利用各种效应因子适应寄主植物防御反应的研究进展。     

Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (Malvaceae)

Plant defense theories commonly predict negative correlations among anti-herbivore resistance traits. Although this prediction has been widely accepted, the majority of empirical studies have failed to account for similarities among species due to common ancestry, thus risking pseudoreplication. Wild cotton plants possess traits conferring both direct resistance (toxic leaf glands and trichomes) and indirect resistance (extrafloral nectaries that reward enemies of herbivores). The evidence for negative phenotypic correlations among these resistance traits was examined at two levels: within Gossypium thurberi (wild cotton) and across species in the cotton clade (Gossypieae). A phylogenetic analysis controlled for shared ancestry among species. Across the Gossypieae, a strong negative correlation emerged between the direct resistance traits, leaf gland and trichomes. This correlation may reflect costs of these traits, a negative genetic correlation, or redundancy in their actions against herbivores. In contrast, the direct resistance traits (glands and trichomes) were not correlated with the indirect resistance trait of extrafloral nectar, either within or across species. The robust lack of correlation suggests that these direct and indirect resistance mechanisms evolve independently over evolutionary time scales. This conclusion conflicts with both predictions of plant defense theory and the majority of prior comparisons of direct and indirect resistance traits and may reflect the facultative nature of indirect resistance in Gossypieae.     

Effector proteins that modulate plant--insect interactions

Insect herbivores have highly diverse life cycles and feeding behaviors. They establish close interactions with their plant hosts and suppress plant defenses. Chewing herbivores evoke characteristic defense responses distinguishable from general mechanical damage. In addition, piercing-sucking hemipteran insects display typical feeding behavior that suggests active suppression of plant defense responses. Effectors that modulate plant defenses have been identified in the saliva of these insects. Tools for high-throughput effector identification and functional characterization have been developed. In addition, in some insect species it is possible to silence gene expression by RNAi. Together, this technological progress has enabled the identification of insect herbivore effectors and their targets that will lead to the development of novel strategies for pest resistances in plants.     

Delayed induced responses of birch glandular trichomes and leaf surface lipophilic compounds to mechanical defoliation and simulated winter browsing

Changes in morphology and chemistry of leaf surface in response to herbivore damage may increase plant resistance to subsequent herbivore attack; however, there is lack of studies on induced responses of glandular trichomes and their exudates in woody plants and on effects of these changes on herbivores. We studied delayed induced responses in leaf surface traits of five clones of silver birch (Betula pendula Roth) subjected to various types of mechanical defoliation and simulated winter browsing. Glandular trichome density and concentrations of the majority of surface lipophilic compounds increased in trees defoliated during the previous summer. This induced response was systemic, since control branches in branch defoliated trees responded to the treatments similarly to defoliated branches, but differently from control trees. In contrast to defoliation treatments, simulated winter browsing reduced glandular trichome density on the following summer and had fewer effects on individual surface lipophilic compounds. Moreover, constitutive density of glandular trichomes was negatively correlated with induced total amount of lipophilic compounds per trichome, indicating a trade-off between constitutive and induced resistance in silver birch. Induced changes in leaf surface traits had no significant effect on leaf damage by chewers, miners and gall mites, but increased susceptibility of birch trees to aphids. However, leaf damage by chewers, miners and gall mites in defoliated (but not in control) trees was correlated with concentrations of some fatty acids and triterpenoids, although the direction of relationships varied among herbivore species. This indicates that induction of surface lipophilic compounds may influence birch resistance to herbivores. Our study thus demonstrated both specificity of elicitation of induced responses of birch leaf surface traits by different types of damage and specificity of the effects of these responses on different types of herbivores.Electronic Supplementary Material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots

Determining links between plant defence strategies is important to understand plant evolution and to optimize crop breeding strategies. Although several examples of synergies and trade-offs between defence traits are known for plants that are under attack by multiple organisms, few studies have attempted to measure correlations of defensive strategies using specific single attackers. Such links are hard to detect in natural populations because they are inherently confounded by the evolutionary history of different ecotypes. We therefore used a range of 20 maize inbred lines with considerable differences in resistance traits to determine if correlations exist between leaf and root resistance against pathogens and insects. Aboveground resistance against insects was positively correlated with the plant's capacity to produce volatiles in response to insect attack. Resistance to herbivores and resistance to a pathogen, on the other hand, were negatively correlated. Our results also give first insights into the intraspecific variability of root volatiles release in maize and its positive correlation with leaf volatile production. We show that the breeding history of the different genotypes (dent versus flint) has influenced several defensive parameters. Taken together, our study demonstrates the importance of genetically determined synergies and trade-offs for plant resistance against insects and pathogens.     

Difference in defense strategy in flower heads and leaves of Asteraceae: multiple-species approach

Although a vast number of studies have investigated defenses against herbivores in leaves, relatively little is known about defenses in flowers. Using wild individuals of 34 species of Asteraceae, we investigated differences in five traits that are thought to affect the intensity of herbivory (C, N, P, water, and total phenolic contents). Combinations of these traits between flower heads and leaves were studied as well. We also evaluated phylogenetic patterns of flower head and leaf traits. Flower heads had higher P and lower total phenolics than leaves. Water and C contents were negatively correlated both in the flower heads and leaves. N, P, and water contents were positively correlated in the flower heads, whereas this pattern was not found in the leaves. Thus, the traits we measured were more tightly inter-correlated in flower heads than in leaves. Because the flower heads had a lower total phenolic content, the relative allocation of defensive compounds could not be explained solely by fitness values of the organs. Perhaps plants employ an escape strategy rather than a defense strategy to cope with floral herbivores and higher allocation in P may enhance their escape from herbivores by improving the growth rate of flower heads, though our result might be affected in part by the plasticity of plants growing at different sites. Moreover, we found weak phylogenetic signals in the defensive traits. Because we found significant differences in the flower head traits, these weak signals may imply that the traits we measured evolved frequently.     

Chemical and Mechanical Defenses Vary among Maternal Lines and Leaf Ages in Verbascum thapsus L. (Scrophulariaceae) and Reduce Palatability to a Generalist Insect

Intra-specific variation in host-plant quality affects herbivore foraging decisions and, in turn, herbivore foraging decisions mediate plant fitness. In particular, variation in defenses against herbivores, both among and within plants, shapes herbivore behavior. If variation in defenses is genetically based, it can respond to natural selection by herbivores. We quantified intra-specific variation in iridoid glycosides, trichome length, and leaf strength in common mullein (Verbascum thapsus L, Scrophulariaceae) among maternal lines within a population and among leaves within plants, and related this variation to feeding preferences of a generalist herbivore, Trichopulsia ni Hübner. We found significant variation in all three defenses among maternal lines, with T. ni preferring plants with lower investment in chemical, but not mechanical, defense. Within plants, old leaves had lower levels of all defenses than young leaves, and were strongly preferred by T. ni. Caterpillars also preferred leaves with trichomes removed to leaves with trichomes intact. Differences among maternal lines indicate that phenotypic variation in defenses likely has a genetic basis. Furthermore, these results reveal that the feeding behaviors of T. ni map onto variation in plant defense in a predictable way. This work highlights the importance of variation in host-plant quality in driving interactions between plants and their herbivores.     

Solar UV‐B radiation and ethylene play a key role in modulating effective defenses against Anticarsia gemmatalis larvae in field‐grown soybean

Solar UV‐B radiation has been reported to enhance plant defenses against herbivore insects in many species. However, the mechanism and traits involved in the UV‐B mediated increment of plant resistance are unknown in crops species, such as soybean. Here, we studied defense‐related responses in undamaged and Anticarsia gemmatalis larvae‐damaged leaves of two soybean cultivars grown under attenuated or full solar UV‐B radiation. We determined changes in jasmonates, ethylene (ET), salicylic acid, trypsin protease inhibitor activity, flavonoids, and mRNA expression of genes related with defenses. ET emission induced by Anticarsia gemmatalis damage was synergistically increased in plants grown under solar UV‐B radiation and was positively correlated with malonyl genistin concentration, trypsin proteinase inhibitor activity and expression of IFS2, and the pathogenesis protein PR2, while was negatively correlated with leaf consumption. The precursor of ET, aminocyclopropane‐carboxylic acid, applied exogenously to soybean was sufficient to strongly induce leaf isoflavonoids. Our results showed that in field‐grown soybean isoflavonoids were regulated by both herbivory and solar UV‐B inducible ET, whereas flavonols were regulated by solar UV‐B radiation only and not by herbivory or ET. Our study suggests that, although ET can modulate UV‐B‐mediated priming of inducible plant defenses, some plant defenses, such as isoflavonoids, are regulated by ET alone.