The evolution of glandularity as a defense against herbivores in the tarweed clade.

PREMISE: Glandular trichomes are implicated in direct and indirect defense of plants. However, the degree to which glandular and non-glandular trichomes have evolved as a consequence of herbivory remains unclear, because their heritability, their association with herbivore resistance, their trade-offs with one another, and their association with other functions are rarely quantified. METHODS: We conducted a phylogenetic comparison of trichomes and herbivore resistance against the generalist caterpillar, Heliothis virescens, among tarweed species (Asteraceae: Madiinae) and a genetic correlation study comparing those same traits among maternal half-sibs of three tarweed species. RESULTS: Within a tarweed species, we found no evidence that herbivore growth rate decreased on tarweed individuals or maternal sib groups with more glandularity or denser trichomes. However, tarweed species with more glandularity and fewer non-glandular trichomes resulted in slower-growing herbivores. Likewise, a trade-off between glandular and non-glandular trichomes was apparent among tarweed species, but not among individuals or sib groups within a species. CONCLUSIONS: Our results suggest that this key herbivore does not select for trichomes as a direct defense in tarweed species. However, trichomes differed substantially among species and likely affect herbivore pressure on those species. Our results demonstrate that trade-offs among plant traits, as well as inference on the function of those traits, can depend on scale.

Plants trap pollen to feed predatory arthropods as an indirect resistance against herbivory.

Plants commonly employ indirect resistance to reduce herbivory by provisioning predatory arthropod populations with additional resources. Numerous predatory arthropods consume pollen that is entrapped on dense, wooly trichomes of plants. Over two seasons, we supplemented pollen on the wooly leaves of turkey mullein, Croton setiger, in natural populations to determine if pollen entrapped on leaves supplements predatory arthropods and reduces herbivore populations and damage to the plant. Pollen supplementation increased the abundance of predatory spiders in both years and omnivorous Orius bugs in 1 yr but had no effect on predatory hemipterans. Pollen supplementation reduced the abundance of herbivorous fleahoppers. Pollen supplementation decreased the amount of leaf damage experienced by plants over the season, suggesting that pollen entrapment may act as an indirect resistance. While C. setiger plants have little control over the amount of pollen on their surfaces, pollen adds to the diet of predatory arthropods that reduce herbivory, thus attraction of predators may be an adaptive benefit of leaf structures such as wooly trichomes that entrap pollen.

Tolerance and phenological avoidance of herbivory in tarweed species.

Avoidance and tolerance of herbivory are important components of plant interactions with herbivores. Their relationship to each other and to plant defense is important in understanding how plants maximize fitness in the face of herbivore pressure. Various tarweed species have populations comprised of both early-season and late-season flowering individuals. Late-season flowering individuals employ a recently described indirect defense against herbivores in which the accumulation of dead insects on their sticky surfaces attracts predatory insects that eat herbivores. In two tarweed species (Hemizonia congesta and Madia elegans), we observed that key herbivores rarely interact with early-season individuals in the field, and early-season individuals did not invest in dense glandular trichomes that cause indirect defense. We conducted field and greenhouse bud-removal experiments to assess tolerance of M elegans to herbivore damage. We found that late-season individuals were more tolerant of simulated herbivory than early-season individuals in both the field and the greenhouse. Late-season individuals that were forced into an earlier phenology with a 24-h light cue lost their tolerance to simulated herbivory. One possible mechanism linking phenological avoidance of herbivores with decreased tolerance is that early-season individuals invested less in below-ground biomass than late-season individuals, which may accumulate belowground resources for regrowth at the expense of early flowering.

Mirid (Hemiptera: Heteroptera) specialists of sticky plants: adaptations, interactions, and ecological implications.

Sticky plants-those having glandular trichomes (hairs) that produce adhesive, viscous exudates-can impede the movement of, and entrap, generalist insects. Disparate arthropod groups have adapted to these widespread and taxonomically diverse plants, yet their interactions with glandular hosts rarely are incorporated into broad ecological theory. Ecologists and entomologists might be unaware of even well-documented examples of insects that are sticky-plant specialists. The hemipteran family Miridae (more specifically, the omnivorous Dicyphini: Dicyphina) is the best-known group of arthropods that specializes on sticky plants. In the first synthesis of relationships with glandular plants for any insect family, we review mirid interactions with sticky hosts, including their adaptations (behavioral, morphological, and physiological) and mutualisms with carnivorous plants, and the ecological and agricultural implications of mirid-sticky plant systems. We propose that mirid research applies generally to tritrophic interactions on trichome-defended plants, enhances an understanding of insect-plant interactions, and provides information useful in managing crop pests.