2001. Suitability of stressed and vigorous plants to various insect herbivores. -Oikos 94: 228 -235.We conducted a controlled experiment to test the plant vigor and the plant stress hypotheses. The two hypotheses associate plant physiological conditions to insect feeding mode and performance. We exposed tomato, Lycopersicon esculentum, to different types of growing conditions: optimal (vigorous plants), resource based stress (water and/or nutrient deficit), and physical stress (punched hole in terminal leaflets). Plant performance, foliar nutritional value for insects and chemical defenses were analyzed after 14 d. These plants were offered to insects belonging to distinct feeding guilds: the silverleaf whitefly, Bemisia argentifolii, a phloem feeder; the leafminer, Liriomyza trifolii; and the corn earworm, Heliothis zea, a leaf chewing caterpillar. The experimental conditions generated a gradient of plant growth in the following order: optimal (vigorous)\control = hole punched \no fertilizer \no water \ no water and no fertilizer. The last two treatments resulted in plants with poor nutritional value (based on %water, C/N, %N) and higher levels of defensive compounds (i.e., peroxidase and total phenolics) compared with control and the vigorous plants. Hole-punching neither affected plant growth nor any of the phytochemicals measured. In a choice experiment adult whitefly ovipositioning was not affected by either vigor or punching but was reduced on the other plants (PB 0.01). Leafminer feeding and oviposition and corn earworm larval growth rates were higher on the vigorous plants and lower on the punched, no fertilizer, no water, and no water and no fertilizer host plants (P B0.01). Regardless of insect species or bioassay method, the results in the tomato system support the plant vigor hypothesis that predicts positive association between insect performance and plant growth. The results contradict the plant stress hypothesis that rank stressed plants as better hosts for insects. The mechanisms involved are a combination of poor nutritional value and chemical defenses. We demonstrate a negative association between plant growth and chemical defense. However, induced response triggered by hole-punching was not cost effective to the plants.
Our laboratory found that silverleaf whitefly (SLW; Bemisia argentifolii Bellows & Perring) feeding alters host plant physiology and chemistry. The SLW induces a number of host plant defenses, including pathogenesis-related (PR) protein accumulation (e.g., chitinases, beta-1,3-glucanases, peroxidases, chitosanases, etc.). Induction of the PR proteins by SLW feeding occurs in various plant species and varieties. The extent and type of induction is dependent on a number of factors that include host plant growing conditions, the length of time the host plant is exposed to SLW feeding, the plant variety, and SLW population densities. The appearance of PR proteins correlates well with reduced infestations of conspecific insect herbivore competitors. Greenhouse and field experiments in which herbivore competitors (cabbage looper, Trichoplusia ni; leaf miner, Liromyza trifolii) were placed on plants previously exposed to SLW feeding demonstrated behavioral differences (oviposition, feeding preferences) and reduced survival rates and development times of these insects. The interaction was asymmetrical, i.e., SLW infestations of plants previously exposed to leaf miners had little or no effect on SLW behavior (oviposition). Induction of plant-defensive proteins by SLW feeding was both local (at the feeding site) and systemic (uninfested leaves distant to the feeding site). There are interactions between diseases such as tomato mottle virus (ToMoV; a geminivirus) and the host plant and SLW. PR proteins were induced in tomato plants infected with ToMoV much as they were via non-viruliferous SLW feeding. The presence of ToMoV in tomato plants significantly increased the number of eggs produced by SLW females. Experiments using tomato plants, powdery mildew (PM), and tobacco mosaic virus (TMV) show that whitefly infestations can affect plant pathogen relationships but the effects vary among pathogen types. Enzyme analyses prior to pathogen inoculation showed that whitefly treatment significantly increased the activities of foliar chitinase and peroxidase. Evaluation of pathogen growth 3 weeks after inoculation showed that whitefly feeding significantly reduced the incidence of PM. However, TMV levels evaluated by ELISA were not significantly affected by whitefly feeding. Six weeks after inoculation with pathogens, the chitinase and peroxidase activities were still elevated in plants initially fed on by whiteflies but continuing pathogen infection had no effect on these enzymes. The possibility that geminivirus infection and/or SLW infestations isolate the host plant for the selected reproduction of the virus and the insect is discussed. Multitrophic cascade effects may contribute to the successful eruptive appearance of SLW on various crops, ranking them as a major pest. They may explain the general observation that when SLW infest a host plant there are few if any competing insect herbivores and pathogens found in the host. However, the results indicate that certain SLW-virus relationships could be mutualistic.
The whitefly, Bemisia tabaci biotype B, has been shown to cause pathogenesis-related (PR) proteins to accumulate in plants as a result of direct feeding, but their specific role in plant defensive systems is unclear. Our objective was to compare accumulation of tomato PR proteins (beta-1,3-glucanase, chitinase, peroxidase, P2 and P4) in response to whitefly, with or without tomato mottle virus (ToMoV) infection. Tomato PR protein response was measured over time in plants divided into three treatments: uninfected controls (with or without whiteflies) and plants infested with viruliferous (ToMoV) whiteflies. Five- to six-leaf plants were infested with approximately 5 adult whitefly per leaf. Plants were sampled prior to whitefly infestation and at 14, 28, 42, and 56 days. By 56 days, plants infested with viruliferous whiteflies had significantly more eggs (2.5-fold) and nymphs (4.5-fold) than plants with nonviruliferous whiteflies. A significant increase in the enzymatic activity of all measured PR proteins, as compared to control plants, was only seen in viruliferous whitefly-infested plants. No significant difference was observed in enzyme activities between the uninfected control plants either with or without whiteflies. The greatest differences for all PR proteins assayed were observed 42 days after treatment initiation. Protein blot analyses showed that the differences in PR protein activities among the treatments were due to changes in specific enzyme levels within the plant and were associated with concomitant increases in levels of P2 and P4 PR proteins. Under our experimental conditions, it is clear that PR protein response is much more intense when it is attacked by whiteflies carrying ToMoV than by whitefly alone.
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