Effects of prey availability, facultative plant feeding, and plant defenses on a generalist insect predator

This study examined the effects of feeding interval, access to host plants (thus, a source of sap), and plant defenses on the predatory insect, Podisus maculiventris Say (Hemiptera: Pentatomidae). The experiment consisted of a 2 × 2 design with two feeding intervals (1 day or 5 days) and predators living on either tomato plants or plastic plants. Females fed every day had greater body weights and egg hatch rates than females fed every five days. Females on tomato plants lived longer than females on plastic plants. However, access to plants did not alleviate the effects of low prey level on predator weight or reproductive output. In a second experiment, third instar nymphs were placed on either tomato plants or plastic plants for four days to examine the effects of tomato trichome defenses on these predators. Nymphs on tomato plants experienced 50% mortality compared to 15% mortality for nymphs on plastic plants. Some nymphs living on tomato plants were trapped by the hairy trichomes of the plant; others had gummed up legs from the exudates of the plants’ glandular trichomes, which inhibited their movement and ability to feed on prey. Although predators appeared to benefit from feeding on tomato plants, their ability to live on the plants was negatively affected by the defensive features of the plants. The potential effects of trichome defenses on predator survival and population dynamics must be considered when evaluating the benefits of plants on insect predator life histories and efficacy as biological control agents.     

“HAIRY CANOLA” – Arabidopsis GL3 Induces a Dense Covering of Trichomes on Brassica napus Seedlings

Transformation with the Arabidopsis bHLH gene 35S:GLABRA3 (GL3) produced novel B. napus plants with an extremely dense coverage of trichomes on seedling tissues (stems and young leaves). In contrast, trichomes were strongly induced in seedling stems and moderately induced in leaves of a hairy, purple phenotype transformed with a 2.2 kb allele of the maize anthocyanin regulator LEAF COLOUR (Lc), but only weakly induced by BOOSTER (B-Peru), the maize Lc 2.4 kb allele, or the Arabidopsis trichome MYB gene GLABRA1 (GL1). B. napus plants containing only the GL3 transgene had a greater proportion of trichomes on the adaxial leaf surface, whereas all other plant types had a greater proportion on the abaxial surface. Progeny of crosses between GL3⁺ and GL1⁺ plants resulted in trichome densities intermediate between a single-insertion GL3⁺ plant and a double-insertion GL3⁺ plant. None of the transformations stimulated trichomes on Brassica cotyledons or on non-seedling tissues. A small portion of bHLH gene-induced trichomes had a swollen terminal structure. The results suggest that trichome development in B. napus may be regulated differently from Arabidopsis. They also imply that insertion of GL3 into Brassica species under a tissue-specific promoter has strong potential for developing insect-resistant crop plants. Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Accumulation and turnover of 2-tridecanone in Tetranychus urticae and its consequences for resistance of wild and cultivated tomatoes

In this study we assessed the dynamic changes of 2-tridecanone in a herbivorous mite (Tetranychus urticae) on tomato (Lycopersicon esculentum, cv. Moneymaker), a plant with methyl ketones in the tetracellular tips of the glandular trichomes (Type VI). We showed that spider mites accumulate 2-tridecanone when foraging on cultivated tomato. Thus, the rate of mite–trichome contact multiplied by the amount of toxin per trichome tip exceeded the relative rate of toxin turnover multiplied by the amount of toxin per mite. The relative rate of toxin turnover was estimated to be 1.1 per day on cucumber, a plant without this toxin. The amount per trichome tip varied from 0.33 ng for middle-leaf trichomes to 1.26 ng for main-stem trichomes. Hence, to achieve a static level of 2-tridecanone equal to 8–17 ng per mite – representing the level we found in mites on middle leaves – the rate of mite–trichome contact should be 26–57 per day. Because methyl ketone apparently accumulates in the spider mites on tomato, the rate of mite–trichome contact is probably higher than that. We expect the accumulation of ketones to occur especially on the stems of cultivated tomato, since this is the area most densely occupied with glandular hairs and because here the hairs have higher levels of the methyl ketones.Using dose–response relationships assessed earlier (Chatzivasileiadis and Sabelis, 1997, 1998), we estimated that the number of mite–trichome contacts causing 50% mortality per day is equal to 88 on a tomato stem, whereas it equals 70 for another strain of spider mites collected from cucumber. On wild tomato, L. hirsutum f. glabratum (PI 134417), just one to two contacts would suffice to cause 50% mortality per day. We suggest that methyl ketones from glandular hairs on tomato are an important mortality factor for spider mites on wild tomato and probably also on cultivated tomato.     

Tomato-aphid-hoverfly: a tritrophic interaction incompatible for pest management

Trichome-based tomato resistance offers the potential to reduce pesticide use, but its compatibility with biological control remains poorly understood. We evaluated Episyrphus balteatus De Geer (Diptera, Syrphidae), an efficient aphidophagous predator, as a potential biological control agent of Myzus persicae Sulzer (Hemiptera, Aphididae) on trichome-bearing tomato cultivars. Episyrphus balteatus’ foraging and oviposition behavior, as well as larval mobility and aphid accessibility, were compared between two tomato cultivars (Lycopersicon esculentum Mill. ‘Moneymaker’ and ‘Roma’) and two other crop plants; broad bean (Vicia faba L.) and potato (Solanum tuberosum L.). Hoverfly adults landed and laid more eggs on broad beans than on three species of Solanaceae. Hoverfly larval movement was drastically reduced on tomato, and a high proportion of hoverfly larvae fell from the plant before reaching aphid prey. After quantifying trichome abundance on each of these four plants, we suggest that proprieties of the plant surface, specifically trichomes, are a key factor contributing to reduced efficacy of E. balteatus as a biological agent for aphid control on tomatoes. Handling editor: Stanislaw Gorb     

Trichoderma species form endophytic associations within Theobroma cacao trichomes

Trichoderma species are usually considered soil organisms that colonize plant roots, sometimes forming a symbiotic relationship. Recent studies demonstrate that Trichoderma species are also capable of colonizing the above ground tissues of Theobroma cacao (cacao) in what has been characterized as an endophytic relationship. Trichoderma species can be re-isolated from surface sterilized cacao stem tissue, including the bark and xylem, the apical meristem, and to a lesser degree from leaves. SEM analysis of cacao stems colonized by strains of four Trichoderma species (Trichoderma ovalisporum-DIS 70a, Trichoderma hamatum-DIS 219b, Trichoderma koningiopsis-DIS 172ai, or Trichoderma harzianum-DIS 219f) showed a preference for surface colonization of glandular trichomes versus non-glandular trichomes. The Trichoderma strains colonized the glandular trichome tips and formed swellings resembling appresoria. Hyphae were observed emerging from the glandular trichomes on surface sterilized stems from cacao seedlings that had been inoculated with each of the four Trichoderma strains. Fungal hyphae were observed under the microscope emerging from the trichomes as soon as 6 h after their isolation from surface sterilized cacao seedling stems. Hyphae were also observed, in some cases, emerging from stalk cells opposite the trichome head. Repeated single trichome/hyphae isolations verified that the emerging hyphae were the Trichoderma strains with which the cacao seedlings had been inoculated. Strains of four Trichoderma species were able to enter glandular trichomes during the colonization of cacao stems where they survived surface sterilization and could be re-isolated. The penetration of cacao trichomes may provide the entry point for Trichoderma species into the cacao stem allowing systemic colonization of this tissue.     

Glandular Trichomes on Alfalfa Impede Searching Behavior of the Potato Leafhopper Parasitoid

New cultivars of alfalfa, Medicago sativa L., have been released with glandular trichomes for resistance to potato leafhopper, Empoasca fabae (Harris). Yet, the impact of the glandular trichomes on the primary natural enemy of the leafhopper, Anagrus nigriventris Girault, is unknown. We compared the host searching behavior of the egg parasitoid on four alfalfa clones varying in trichome characters. Female wasps were videotaped on Ranger, a susceptible clone with relatively sparse trichomes, B14, a resistant clone with dense but nonglandular trichomes, and FG12 and FG18, two resistant clones with glandular trichomes. Although the number of leafhopper eggs per stem exposed to wasps did not significantly differ among the four clones, the frequency of foraging and total foraging time were less on the two clones with glandular trichomes than on the two clones with nonglandular trichomes. In addition, an analysis of covariance demonstrated that, although the number of ovipositional probes increased with egg density on a stem, the number of probes on stems with glandular trichomes was significantly less than that on stems without glandular trichomes. The allocation of time by wasps among drumming, probing, and grooming behaviors was similar among the clones. Wasps tended to fly off of clones with glandular trichomes more often than off of clones with nonglandular trichomes. This study suggests that cultivars with glandular trichomes may interfere with host searching by A. nigriventris.     

Nonglandular leaf trichomes as short-term inducible defense of the grey alder,Alnus incana (L.), against the chrysomelid beetle,Agelastica alni L.

Summary The grey alder compensates leaf area losses due to insect grazing by continuously producing new leaves throughout the vegetative period. Different degrees of defoliation were attained experimentally by a controlled release of the oligophagous beetle Agelastica alni on arbitrarily selected trees from a homogenous population of young alders. The reduction in leaf area per tree significantly influenced the density of leaf trichomes, assessed 10–30 days later, on newly sprouting leaves only. Cross-correlations between leaf area reduction and trichome density were strongest for leaves which completed unfolding 14–21 days after damage. Dualchoice assays suggested a negative influence of trichomes on oviposition rate of A. alni. Removal of trichomes by shaving demonstrated the highly significant effect of trichomes on feeding behavior of adults and larvae in dual-choice assays. The role of the induced increase in trichome density as a possible short-term defense reaction against herbivorous insects is discussed.     

Incidence of the introduced parasitoids Cotesia kazak and Microplitis croceipes (Hymenoptera: Braconidae) from Helicoverpa armigera (Lepidoptera: Noctuidae) in tomatoes, sweet corn, and lucerne in New Zealand

Morphological defense traits of plants such as trichomes potentially compromise biological control in agroecosystems because they may hinder predation by natural enemies. To investigate whether plant trichomes hinder red imported fire ants, Solenopsis invicta Buren (Hymenoptera: Formicidae), as biological control agents in soybean, field and greenhouse experiments were conducted in which we manipulated fire ant density in plots of three soybean isolines varying in trichome density. Resulting treatment effects on the abundance of herbivores, other natural enemies, plant herbivory, and yield were assessed. Trichomes did not inhibit fire ants from foraging on plants in the field or in the greenhouse, and fire ant predation of herbivores in the field was actually greater on pubescent plants relative to glabrous plants. Consequently, fire ants more strongly reduced plant damage by herbivores on pubescent plants. This effect, however, did not translate into greater yield from pubescent plants at high fire ant densities. Intraguild predation by fire ants, in contrast, was weak, inconsistent, and did not vary with trichome density. Rather than hindering fire ant predation, therefore, soybean trichomes instead increased fire ant predation of herbivores resulting in enhanced tritrophic effects of fire ants on pubescent plants. This effect was likely the result of a functional response by fire ants to the greater abundance of caterpillar prey on pubescent plants. Given the ubiquity of lepidopteran herbivores and the functional response to prey shown by many generalist arthropod predators, a positive indirect effect of trichomes on predation by natural enemies might be more far more common than is currently appreciated.     

Foraging behavior of specialist and generalist caterpillars on plantain (Plantago lanceolata) altered by predatory stinkbugs

Summary To examine the effects of predators and plant genotype on the behavior, patterns of herbivory, growth and survivorship of caterpillars, we used an experimental garden in which we contrasted two hostplant genotypes of plantain (Plantago lanceolata), two kinds of herbivores (specialist Junonia coenia vs. generalist Pyrrharctia isabella) and two levels of caterpillar predation (with and without Podisus maculiventris stinkbugs). Each of the replicate plots per treatment contained two plants of the same genotype. The stinkbugs reduced the survivorship of the specialist caterpillars but not that of the generalists, which reflects the differences in predatoravoidance behaviors of these species. Nonetheless, the stinkbugs influenced the behavior of both caterpillar species. When stinkbugs were present, both specialist and generalist caterpillars were less likely to be found on the plant upon which they were initially placed (=initial plant), and they were more likely to be off both plants within the plot than larvae in the absence of predators. Consequently in the presence of the stinkbug predators, the proportion of the initial plants consumed was less than in the absence of the predators. Plant genotype influenced plant size and the proportion of individual plants eaten, but it did not affect larval location on the plots. Neither presence of predators nor plant genotype had an effect on relative growth rate of the caterpillars.     

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.     

No Experimental Evidence for Host Ant Related Oviposition in a Parasitic Butterfly

The ability of adult butterflies of the genus Maculinea to locate their host ants prior to oviposition has been the subject of much discussion. We studied the egg laying behavior of the dusky large blue Maculinea nausithous whose larvae parasitize colonies of the ant Myrmica rubra. Flowerheads of the initial food plant were sprinkled with soil from ant nests, which contain chemicals involved in the nest recognition behavior of ants. The experiment was conducted to determine whether ant-released chemicals may act as oviposition cues and whether intraspecific competition for suitable plants may force female butterflies to alternative decisions. Host plant choice was not influenced by the presence of nest-derived host-ant cues. Density dependent shifts to less suitable host plants could not be ascertained nor changes in egg laying behavior across the flight period. The observed egg distribution could be primarily explained by host plant characteristics and environmental variability among sites. The result confirms the theory that host ant dependent oviposition appears to be a disadvantageous strategy in the face of resource limitation within ant colonies and the immobility of caterpillars.     

Herbivory-associated degradation of tomato trichomes and its impact on biological control of Aculops lycopersici

Tomato plants have their leaves, petioles and stems covered with glandular trichomes that protect the plant against two-spotted spider mites and many other herbivorous arthropods, but also hinder searching by phytoseiid mites and other natural enemies of these herbivores. This trichome cover creates competitor-free and enemy-free space for the tomato russet mite (TRM) Aculops lycopersici (Acari: Eriophyidae), being so minute that it can seek refuge and feed inbetween the glandular trichomes on tomato cultivars currently used in practice. Indeed, several species of predatory mites tested for biological control of TRM have been reported to feed and reproduce when offered TRM as prey in laboratory experiments, yet in practice these predator species appeared to be unable to prevent TRM outbreaks. Using the phytoseiid mite, Amblydromalus limonicus, we found exactly the same, but also obtained evidence for successful establishment of a population of this predatory mite on whole plants that had been previously infested with TRM. This successful establishment may be explained by our observation that the defensive barrier of glandular plant trichomes is literally dropped some time after TRM infestation of the tomato plants: the glandular trichome heads first rapidly develop a brownish discoloration after which they dry out and fall over onto the plant surface. Wherever TRM triggered this response, predatory mites were able to successfully establish a population. Nevertheless, biological control was still unsuccessful because trichome deterioration in TRM-infested areas takes a couple of days to take effect and because it is not a systemic response in the plant, thereby enabling TRM to seek temporary refuge from predation in pest-free trichome-dense areas which continue to be formed while the plant grows. We formulate a hypothesis unifying these observations into one framework with an explicit set of assumptions and predictions to be tested in future experiments.     

Influence of Hairiness ofGerbera jamesoniiLeaves on the Searching Efficiency of the ParasitoidEncarsia formosa

To characterize the relationship between the leaf surface ofGerbera jamesoniiHooker cultivars and the searching behavior of the parasitoidEncarsia formosaGahan on a leaf, the trichome density and shape were described, and the walking behavior was quantified. Leaf hair density varied from 80 to more than 1000 trichomes/cm²and the hair shape varied from single erect trichomes to tapestries of entangled trichomes above the leaf surface. The walking activity, speed, and pattern of the parasitoid were tested on leaves with different hair density and shape. In spite of the large differences in leaf surface structure, the walking activity was similar and around 75% on most cultivars. The walking speed was between 0.2 and 0.3 mm/s on all cultivars and was not significantly different from the speed on tomato. On hairless sweet pepper leaves the walking speed is much higher (0.73 mm/s), so the hairs onGerberaleaves do hamper parasitoid females and result in a strong reduction of the walking speed, but the variation in hair density and shape onGerberadoes not lead to differences in walking activity, pattern, and speed. It appears that the hairs ofGerberaare less of an obstacle forE. formosathan the stiff, large hairs occurring in a high density on cucumber, where the walking speed of the parasitoid is less than 0.2 mm/s. A rise of temperature of 5°C gave a significantly higher walking speed (0.39 mm/s) ofE. formosafemales on all cultivars tested. The relative straightness of the walking track was high and the same on all cultivars. Consequences of the results of the searching behavior ofE. formosaonG. jamesoniicultivars are discussed with respect to other host plants. As parasitoid walking speeds are the same onGerberaand tomato, and whitefly reproduction is also similar on these two host plants, we conclude that biological control of whiteflies onGerberais a realistic option. This conclusion is confirmed by the strong increase of commercial biological control onGerberawhich occurred during the past 5 years.     

Trichomes: their Diversity,Distribution and Density in Acclimatization of Teak (Tectona grandis L.) Plants Grown in vitro

Diversity, distribution and density of trichomes were studied in relation to other morphological and physiological parameters of in vivo and in vitro teak (Tectona grandis L.) plants with the objective to understand their role in hardening and acclimatization of micropropagated plants. Less diversity and scanty distribution of trichomes of in vitro leaves in comparison to the in vivo ones were correlated with water loss of the former plants leading to low rate of survival after transplantation. The probable cause for absence of certain types of trichome in in vitro plants was also discussed.     

Pre- and post-landing response of the parasitoid Encarsia formosa to whitefly hosts on Gerbera jamesonii

One of the factors that may complicate biological control of the greenhouse whitefly on Gerbera jamesonii by Encarsia formosa is the rosette shape of this ornamental, which differs from the vertical shape of most vegetable plants (cucumber, egg plant, tomato, etc.). Therefore, host-habitat location and the behaviour prior to landing on uninfested and infested leaves was studied. Attraction of E. formosa from a short distance by infested leaves could not be detected: the parasitoid females landed at random on uninfested and infested leaves. After the first landing, a redistribution of the wasps occurred on the leaves. After 24 h three times as many wasps were found on the infested leaves than on uninfested ones. In a dispersal experiment with four plants, E. formosa appeared to have no preference for landing on leaves of the medium age class, which is the age class on which most of the whiteflies in a suitable stage for parasitism occur. Twenty percent of the parasitoids were found on the plants 20 min after releasing them. These results were independent of the plant cultivar and the host density on the plants. In the course of 8 h, the number of E. formosa females recovered from plants increased linearly, and this increase was greater on plants where hosts were present and also greater on the plant cultivar with the lowest trichome density. After 24 h, the percentage of females was highest (56%) on plants with the highest host density. E. formosa females were arrested on leaves where hosts were present. Contrary to our expectation, the results from the two G. jamesonii cultivars that differed strongly in leaf hairiness were not significantly different in most experiments. Only at the high host density was parasitism found to be lower on the cultivar with the higher hair density. Parasitoids may walk on top of the `hair coverlet' of cultivars with high trichome density and, therefore, be hampered less than expected.     

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.     

Host plant resistance among tomato accessions to the spider mite <Emphasis Type="Italic">Tetranychus evansi</Emphasis> in Kenya

The spider mite Tetranychus evansi has a broad range of host plants. Control of T. evansi has been a big challenge to tomato farmers due to its fast rate of reproduction, development of resistance to chemical pesticides and its ability to use weeds as alternative hosts when the tomato plants are not available. The aim of the current study was to determine the host plant acceptance and the relative contributions of trichomes in the control of the red spider mite by comparing the survival, development and oviposition rates of the red spider mite on eight tomato accessions. Leaflets from eight tomato varieties were assayed with the spider mites to determine the egg laying capacity and developmental time of the spider mites on the tomato accessions as well as the trichome densities. Densities of trichome types I, IV, V and VI varied among the tomato accessions. Variation in types I, IV and VI accounted for most of the variation in mite responses. The varieties with high densities of types IV and VI had the highest fecundity and mite development did not go beyond the larval stage. The developmental time varied significantly among the tomato accessions. The results indicated that the higher the density of trichome type I the lower the adult survival. The findings indicated possible resistance of some of the tested tomato accessions against T. evansi which is partially associated with trichomes types and density.     

Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction

We tested whether a plant's life time seed production is increased by parasitization of herbivores in a tritrophic system, Arabidopsis thaliana (Brassicaceae) plants, Pieris rapae (Lepidoptera: Pieridae) caterpillars and the solitary endoparasitoid Cotesia rubecula (Hymenoptera: Braconidae). We established seed production for intact A. thaliana plants, plants that were mechanically damaged, plants fed upon by parasitized caterpillars and plants fed upon by unparasitized caterpillars. In the first experiment, with ecotype Landsberg (erecta mutant), herbivory by unparasitized P. rapae caterpillars resulted in a strongly reduced seed production compared to undamaged plants. In contrast, damage by P. rapae caterpillars that had been parasitized by C. rubecula did not result in a significant reduction in seed production. For the second experiment with the ecotype Columbia, the results were identical. Plants damaged by unparasitized caterpillars only produced seeds on regrown shoots. Seed production of plants that had been mechanically damaged was statistically similar to that of undamaged plants. Production of the first ripe siliques by plants fed upon by unparasitized caterpillars was delayed by 18–22 days for Landsberg and 9–10 days for Columbia. We conclude that parasitization of P. rapae by C. rubecula potentially confers a considerable fitness benefit for A. thaliana plants when compared to plants exposed to feeding damage by unparasitized P. rapae larvae. Plants that attract parasitoids and parasitoids that respond to herbivore-induced plant volatiles will both experience selective advantage, justifying the use of the term mutualism for this parasitoid-plant interaction. This type of mutualism is undoubtedly very common in nature.