Effects of trichomes on the behavior and distribution of Platyprepia virginalis caterpillars

Trichomes are an important physical resistance mechanism of plants, as they reduce insect herbivore movement, feeding, and digestion. However, we know little about how trichomes influence herbivore distributions and populations. We conducted laboratory and field experiments to evaluate the preferences of Platyprepia virginalis (Boisduval) (Lepidoptera: Arctiidae) caterpillars to natural and manipulated densities of trichomes on their primary food, Lupinus arboreus Sims (Fabaceae). We then conducted field surveys to determine whether variation in trichome density among lupine bushes affected caterpillar spatial distribution on the landscape. Platyprepia virginalis caterpillars preferred lupine leaves with fewer trichomes in choice and no‐choice experiments. In the field, caterpillar feeding damage was found more often on leaves with fewer trichomes. These preferences scaled up to the level of bushes in the landscape such that more caterpillars were found on bushes with lower trichome densities than on bushes with higher trichome densities. This is one of few studies to show the potential for trichome density to influence herbivore population size and distribution in a natural system at a landscape level. The results are consistent with trichomes functioning as a resistance mechanism with consequences for herbivore choice, performance, and distribution.     

Exploiting physical defence traits for crop protection: leaf trichomes of Rubus idaeus have deterrent effects on spider mites but not aphids

Plants possess anti‐herbivore defences that could be exploited for crop protection. The potential for deploying physical defence traits for more sustainable pest management (i.e. reduced pesticide application) has not been fully realised. Using a perennial crop (red raspberry, Rubus idaeus), we take the novel approach of quantifying within‐ and between‐genotype variation in a resistance trait, leaf trichome density, to determine precisely the effect of trichomes on host plant preference and suitability for two shoot‐feeding arthropods, the European large raspberry aphid (Amphorophora idaei) and two‐spotted spider mite (Tetranychus urticae). Additionally, we tested whether this trait influenced searching behaviour of a generalist herbivore predator (lacewing larvae, Chrysoperla carnea). Although there was no consistent genotypic variation in R. idaeus suitability for T. urticae, our hypothesis that T. urticae would avoid high leaf trichome density was supported on certain genotypes. The deterrent effect was mainly on egg deposition rather than leaf selection by adults, with up to sixfold differences in leaf preference depending on the genotypes offered. By contrast, there was significant genotypic variation in R. idaeus suitability for A. idaei (10‐fold variation in aphid abundance), but, contrary to our prediction, aphid preference and infestation levels were unrelated to leaf trichome density. Instead, A. idaei performed best on vigorous genotypes, indicating that plant tolerance traits contributed to R. idaeus suitability for aphids. Leaf trichomes had little effect on the behaviour of the beneficial control agent C. carnea larvae. We conclude that physical anti‐herbivore defences, specifically leaf trichomes, could be deployed to deter particular arthropod pests. However, the mechanistic approach adopted here is necessary to avoid antagonistic effects on other pests or on natural enemies.     

Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus

Mimulus guttatus (yellow monkeyflower) frequently produce glandular trichomes, a trait that may resist herbivory. Constitutive production of trichomes is variable both within and among populations of M. guttatus and most of this variation is genetic. This study demonstrates that damage on early leaves can induce increased trichome production on later leaves, a plastic response that is likely adaptive. Moreover, this study shows that this induction can be maternally transmitted, increasing trichome density in progeny before they experience herbivory. This transgenerational response must involve a yet undescribed epigenetic mechanism. These experiments also show genetic variation among plants in the capacity for both within and between plant generation induction. Despite the clear evolutionary importance of variation in constitutive and induced herbivory-resistance traits, few other studies have noted genetic variation in both within a plant species.     

Cost of trichome production and resistance to a specialist insect herbivore in <Emphasis Type="Italic">Arabidopsis lyrata</Emphasis>

Theory predicts that trade-offs between resistance to herbivory and other traits positively affecting fitness can maintain genetic variation in resistance within plant populations. In the perennial herb Arabidopsis lyrata, trichome production is a resistance trait that exhibits both qualitative and quantitative variation. Using a paternal half-sib design, we conducted two greenhouse experiments to ask whether trichomes confer resistance to oviposition and leaf herbivory by the specialist moth Plutella xylostella, and to examine potential genetic constraints on evolution of increased resistance and trichome density. In addition, we examined whether trichome production is induced by insect herbivory. We found strong positive genetic and phenotypic correlations between leaf trichome density and resistance to leaf herbivory, demonstrating that the production of leaf trichomes increases resistance to leaf damage by P. xylostella. Also resistance to oviposition tended to increase with increasing leaf trichome density, but genetic and phenotypic correlations were not statistically significant. Trichome density and resistance to leaf herbivory were negatively correlated genetically with plant size in the absence of herbivores, but not in the presence of herbivores. There was no evidence of increased trichome production after leaf damage by P. xylostella. The results suggest that trichome production and resistance to leaf herbivory are associated with a cost and that the direction of selection on resistance and trichome density depends on the intensity of herbivory.     

Environmental Heterogeneity and Population Differentiation in Plasticity to Drought in <Emphasis Type="Italic">Convolvulus Chilensis</Emphasis> (Convolvulaceae)

Plant populations may show differentiation in phenotypic plasticity, and theory predicts that greater levels of environmental heterogeneity should select for higher magnitudes of phenotypic plasticity. We evaluated phenotypic responses to reduced soil moisture in plants of Convolvulus chilensis grown in a greenhouse from seeds collected in three natural populations that differ in environmental heterogeneity (precipitation regime). Among several morphological and ecophysiological traits evaluated, only four traits showed differentiation among populations in plasticity to soil moisture: leaf area, leaf shape, leaf area ratio (LAR), and foliar trichome density. In all of these traits plasticity to drought was greatest in plants from the population with the highest interannual variation in precipitation. We further tested the adaptive nature of these plastic responses by evaluating the relationship between phenotypic traits and total biomass, as a proxy for plant fitness, in the low water environment. Foliar trichome density appears to be the only trait that shows adaptive patterns of plasticity to drought. Plants from populations showing plasticity had higher trichome density when growing in soils with reduced moisture, and foliar trichome density was positively associated with total biomass. Co-ordinating editor: F. Stuefer     

Antagonism between herbivore‐induced plant volatiles and trichomes affects tritrophic interactions

We used tomato genotypes deficient in the jasmonic acid (JA) pathway to study the interaction between the production of herbivore‐induced plant volatiles (HIPVs) that serve as information cues for herbivores as well as natural enemies of herbivores, and the production of foliar trichomes as defence barriers. We found that jasmonic acid‐insensitive1 (jai1) mutant plants with both reduced HIPVs and trichome production received higher oviposition of adult leafminers, which were more likely to be parasitized by the leafminer parasitoids than JA biosynthesis spr2 mutant plants deficient in HIPVs but not trichomes. We also showed that the preference and acceptance of leafminers and parasitoids to trichome‐removed plants from either spr2 or wild‐type (WT) genotypes over trichome‐intact genotypes can be ascribed to the reduced trichomes on treated plants, but not to altered direct and indirect defence traits such as JA, proteinase inhibitor (PI)‐II and HIPVs levels. Although the HIPVs of WT plants were more attractive to adult insects, the insects preferred trichome‐free jai1 plants for oviposition and also had greater reproductive success on these plants. Our results provide strong evidence that antagonism between HIPV emission and trichome production affects tritrophic interactions. The interactions among defence traits are discussed.     

Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium

This study assessed the role of leaf trichome density as a component of resistance to herbivores, in six populations of Datura stramonium. Phenotypic selection on plant resistance was estimated for each population. A common garden experiment was carried out to determine if population differences in leaf trichome density are genetically based. Among population differences in leaf trichome density, relative resistance and fitness were found. Leaf trichome density was strongly positively correlated to resistance across populations. In 5 out of 6 populations, trichome density was related to resistance, and positive directional selection on resistance to herbivores was detected in three populations. Differences among populations in mean leaf trichome density in the common garden suggest genetic differentiation for this character in Datura stramonium. The results are considered in the light of the adaptive role of leaf trichomes as a component of defence to herbivores, and variable selection among populations.     

Evolutionary changes in plant tolerance against herbivory through a resurrection experiment

Both theoretical and empirical works have highlighted the difference in the evolutionary implications of host resistance and tolerance against their enemies. However, it has been difficult to show evolutionary changes in host defences in natural populations; thus, evaluating theoretical predictions of simultaneous evolution of defences remains a challenge. We studied the evolutionary changes in traits related to resistance and tolerance against herbivory in a natural plant population using seeds from two collections made in a period of 20 years. In a common garden experiment, we compared defensive traits of ancestral (1987) and descendant (2007) subpopulations of the annual plant Datura stramonium that shows genetic variation for tolerance and to which the specialist herbivore Lema daturaphila is locally adapted. We also examined the effects of different plant genotypes on the herbivore for testing the plant genetic variation in resistance. Based on the response to the contemporary herbivore populations, results revealed a nonsignificant response in plant resistance traits (herbivore consumption, foliar trichomes and tropane alkaloids), but a significant one in tolerance. The survival of herbivores in laboratory experiments depended on the plant genotype, which suggests genetic variation in plant resistance. Although we cannot identify the selective agent for the change nor exclude genetic drift, the results are consistent with the expectation that when resistance fails to control herbivory, tolerance should play a more important role in the evolution of the interaction.     

Ontogenetics of QTL: the genetic architecture of trichome density over time in Arabidopsis thaliana

Although much is known about the molecular genetic basis of trichome development in Arabidopsis thaliana, less is known about the underlying genetic basis of continuous variation in a trait known to be of adaptive importance: trichome density. The density of leaf trichomes is known to be a major determinant of herbivore damage in natural populations of A. thaliana and herbivores are a significant selective force on genetic variation for trichome density. A number of developmental changes occur during ontogeny in A. thaliana, including changes in trichome density. I used multiple interval mapping (MIM) analysis to identify QTL responsible for trichome density on both juvenile leaves and adult leaves in replicate, independent trials and asked whether those QTL changed with ontogeny. In both juvenile and adult leaves, I detected a single major QTL on chromosome 2 that explained much of the genetic variance. Although additional QTL were detected, there were no consistent differences in the genetic architecture of trichome density measured on juvenile and adult leaves. The finding of a single QTL of major effect for a trait of known adaptive importance suggests that genes of major effect may play an important role in adaptation.     

Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana

Abstract.  1. The annual herb Arabidopsis thaliana is a prime model organism of plant molecular genetics, and is currently used to explore the molecular basis of resistance to herbivores. However, both the magnitude and the causes of variation in resistance among natural populations of A. thaliana are poorly known. The hypotheses (a) that resistance to a specialist herbivore, the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is positively related to the density of leaf trichomes, and (b) that oviposition preference by female moths is positively correlated to larval performance on different populations and maternal lines of the host plant were examined.
2. Variation in leaf trichome density and resistance to P. xylostella within and among six natural populations of A. thaliana in Sweden was quantified . Resistance was quantified by examining the number of eggs laid on plants exposed to ovipositing female moths and by monitoring larval development on plants of different origin.
3. Trichome density varied significantly among populations; for 4-week-old plants (exposed to ovipositing moths), it also varied significantly among maternal families within populations. The rate of oviposition varied significantly both among populations and among families within populations. This variation could partly be explained by a negative relationship between trichome density and egg number, and a positive relationship between plant size and egg number. Time to pupation, pupal mass, and time to adult eclosion did not vary among populations or maternal lines of the host plant, and offspring performance was not related to P. xylostella oviposition preference . The results indicate that A. thaliana populations may respond to selection for increased resistance to P. xylostella , and suggest that trichome production contributes to resistance against this specialist herbivore.     

EXPERIMENTAL MANIPULATION OF PUTATIVE SELECTIVE AGENTS PROVIDES EVIDENCE FOR THE ROLE OF NATURAL ENEMIES IN THE EVOLUTION OF PLANT DEFENSE

Although biologists have long assumed that plant resistance characters evolved under selection exerted by such natural enemies as herbivores and pathogens, experimental evidence for this assumption is sparse. We present evidence that natural enemies exert selection on particular plant resistance characters. Specifically, we demonstrate that elimination of natural enemies from an experimental field population of Arabidopsis thaliana alters the pattern of selection on genetic variation in two characters that have been shown to reduce herbivore damage in the field: total glucosinolate concentration and trichome density. The change in pattern of selection reveals that natural enemies imposed selection favoring increased glucosinolate concentration and increased trichome density, and thus, supports one of the major assumptions of the coevolution hypothesis. We also demonstrate that a pattern of stabilizing selection on glucosinolate concentration results from a balance between the costs and benefits associated with increasing levels of this resistance character. This result provides direct confirmation of the appropriateness of cost-benefit models for characterizing the evolution of plant defenses.     

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.     

Variable responses of tuber moth to the leaf trichomes of wild potatoes

This study examines the response of tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae), during the initial stages of attack, to variability in trichome density and composition on foliage of Solanum berthaultii (Hawkes) and Solanum tarijense (Hawkes) (Solanaceae). Solanum berthaultii bears two types of glandular trichome (type A and type B) that together reduced oviposition by the moth. Females were often completely deterred from ovipositing on foliage with >300 trichomes per cm². In contrast, neonate establishment on S. berthaultii was generally positively related to trichome densities, indicating that trichomes may be a poor defense against P. operculella when the moth oviposits in soil and neonate larvae select the host plant. Solanum tarijense has only one type of glandular trichome (type A) and eglandular hairs. Most eggs were deposited on the adaxial leaf surfaces that had lower trichome densities. Although the density of type A trichomes was negatively related to oviposition, high densities of hairs on the abaxial and adaxial leaf surfaces appeared to stimulate oviposition, leading to stronger positive relations between hair densities and oviposition. Larvae generally established on the abaxial surface where hair densities were greatest. Relationships between the abaxial densities of leaf hairs and neonate establishment on S. tarijense were positive. The results indicate that the responses by P. operculella to the types and density of trichomes are complex. Whereas type A and type B trichomes may act synergistically to reduce oviposition by the moth, leaf hairs do not defend against oviposition and neither leaf hairs nor type A and B trichomes reduce neonate establishment by this herbivore species.     

Trichome production and variation in young plant resistance to the specialist insect herbivore Plutella xylostella among natural populations of Arabidopsis lyrata

The strength of plant‐herbivore interactions varies spatially and through plant ontogeny, which may result in variable selection on plant defense, both among populations and life‐history stages. To test whether populations have diverged in herbivore resistance at an early plant stage, we quantified oviposition preference and larval feeding by Plutella xylostella (L.) (Lepidoptera: Plutellidae) on young (5–6 weeks old) Arabidopsis lyrata (L.) O'Kane & Al‐Shehbaz (Brassicaceae) plants, originating from 12 natural populations, six from Sweden and six from Norway. Arabidopsis lyrata can be trichome‐producing or glabrous, with glabrous plants usually receiving more damage from insect herbivores in natural populations. We used the six populations polymorphic for trichome production to test whether resistance against P. xylostella differs between the glabrous and the trichome‐producing morph among young plants. There was considerable variation among populations in the number of eggs received and the proportion of leaf area consumed by P. xylostella, but not between regions (Sweden vs. Norway) or trichome morphs. Rosette size explained a significant portion of the variation in oviposition and larval feeding. The results demonstrate that among‐population variation in resistance to insect herbivory can be detected among very young individuals of the perennial herb A. lyrata. They further suggest that trichome densities are too low at this plant developmental stage to contribute to resistance, and that the observed among‐population variation in resistance is related to differences in other plant traits.     

Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies

1 The cultivated tomato, Lycopersicon esculentum, is an economically important worldwide crop. Current pest management techniques rely heavily on pesticides but trichome‐based host‐plant resistance may reduce pesticide use. 2 A review of the literature is provided on trichomes of wild Lycopersicon species and the effects of trichome‐based host‐plant resistance on arthropods. Solvents have been used to remove glandular trichome exudates and the resulting dimminution of their effects quantified. Correlational approaches to assess the relationship between the different trichome types and effects on pests have also been used. 3 Most studies have focused on Lepidoptera and Hemiptera, although some work has included Coleoptera, Diptera and Acarina, and both antibiotic and antixenotic effects have been demonstrated. 4 Natural enemies are a cornerstone of international pest management and this review discusses how the compatibility of this approach with trichome‐based host‐plant resistance is uncertain because of the reported negative effects of trichomes on one dipteran, one hemipteran and several Hymenoptera. 5 For trichome‐based host‐plant resistance to be utilized as a pest management tool, trichomes of wild species need to be introgressed into the cultivated tomato. Hybrids between the cultivated tomato and the wild species Lycopersicon hirsutum f. glabratum, Lycopersicon pennellii and Lycopersicon cheesmanii f. minor have been produced and useful levels of resistance to Acarina, Diptera and Hemiptera pests have been exhibited, although these effects may be tempered by effects on natural enemies. 6 This review proposes that studies on genetic links between fruit quality and resistance, field studies to determine the compatibility of natural enemies and trichome‐based host‐plant resistance, and a strong focus on L. cheesmanii f. minor, are all priorities for further research that will help realize the potential of this natural defence mechanism in pest management.     

Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies

1 The cultivated tomato, Lycopersicon esculentum, is an economically important worldwide crop. Current pest management techniques rely heavily on pesticides but trichome‐based host‐plant resistance may reduce pesticide use. 2 A review of the literature is provided on trichomes of wild Lycopersicon species and the effects of trichome‐based host‐plant resistance on arthropods. Solvents have been used to remove glandular trichome exudates and the resulting dimminution of their effects quantified. Correlational approaches to assess the relationship between the different trichome types and effects on pests have also been used. 3 Most studies have focused on Lepidoptera and Hemiptera, although some work has included Coleoptera, Diptera and Acarina, and both antibiotic and antixenotic effects have been demonstrated. 4 Natural enemies are a cornerstone of international pest management and this review discusses how the compatibility of this approach with trichome‐based host‐plant resistance is uncertain because of the reported negative effects of trichomes on one dipteran, one hemipteran and several Hymenoptera. 5 For trichome‐based host‐plant resistance to be utilized as a pest management tool, trichomes of wild species need to be introgressed into the cultivated tomato. Hybrids between the cultivated tomato and the wild species Lycopersicon hirsutum f. glabratum, Lycopersicon pennellii and Lycopersicon cheesmanii f. minor have been produced and useful levels of resistance to Acarina, Diptera and Hemiptera pests have been exhibited, although these effects may be tempered by effects on natural enemies. 6 This review proposes that studies on genetic links between fruit quality and resistance, field studies to determine the compatibility of natural enemies and trichome‐based host‐plant resistance, and a strong focus on L. cheesmanii f. minor, are all priorities for further research that will help realize the potential of this natural defence mechanism in pest management.     

Oviposition,larval survival and leaf damage by the willow leaf blotch miner,Micrurapteryx salicifoliella,in relation to leaf trichomes across 10 Salix species

1. Foliar trichomes clearly reduce chewing damage and efficiency of movement by some insect herbivores, but the effect of trichomes on insect oviposition is less well characterised. Trichomes are likely to have particularly strong, negative effects on species that require secure attachment of the egg to the leaf epidermis for successful transition to the feeding stage – a group that includes many leaf mining insects. 2. One such species, Micrurapteryx salicifoliella, must initially enter leaf cells directly from an egg adhered to the cuticle, but later instars can move between leaves and initiate new mines from the leaf exterior. 3. Natural patterns of occurrence by M. salicifoliella were quantified on 10 sympatric Salix species varying in trichome expression to test whether trichomes were associated with reduced oviposition, larval survival and leaf damage. 4. Mean egg density and leaf mining damage were negatively related to mean trichome density across Salix species. Survival of M. salicifoliella from egg to pupa was positively related to trichome density, suggesting that initiation of new mines by late‐instar larvae was not adversely affected by trichomes. There was no evidence that trichomes benefited leaf miner larvae indirectly by decreasing density‐dependent mortality; rather, the positive relationship between trichome density and larval survival may reflect less effective chemical defence by Salix species expressing high trichome density. 5. The results suggest that foliar trichomes serve as an effective defence against M. salicifoliella by deterring oviposition, but do not reduce the survivorship of those individuals that successfully transition from egg to larva.     

Induced responses in Ipomoea hederacea: simulated mammalian herbivory induces resistance and susceptibility to insect herbivores

Multispecies interactions between plants and natural enemies are ubiquitous, and often lead to diffuse interactions between plants and their herbivores. Non-specific induced responses, where responses induced by one species affect other species, are one potential mechanism generating diffuse interactions. Using 57 inbred lines of the Ivyleaf morning glory, Ipomoea hederacea, in a greenhouse experiment, we examined whether simulated mammalian herbivory induced responses that could affect plant resistance to the generalist insect herbivore, Spodoptera exigua. Inbred lines were highly variable for induced responses, ranging from induced resistance to induced susceptibility, with the rank-order for resistance in inbred lines changing between clipping and control treatments. We failed to detect significant genetic correlations between induced responses and trichome density, or that clipping modified the negative relationship between trichome density and Spodoptera exigua consumption and biomass. Our results suggest that non-specific induced responses can mediate the diffuse evolutionary relationship between I. hederacea and its herbivores, and that genetic variation in induced responses are an important component of this interaction. Handling Error: Heikki Hokkanen