Ecophysiological importance of phototoxins in plant-insect relationships.

Abstract

The ecophysiological importance of phototoxins (PTs), a group of plant light-activated secondary compounds toxic to a wide range of organisms, was investigated in the context of plant-insect relationships. The efficiency of PTs in protecting plants against herbivores was investigated in the field by measuring the herbivory damage on a series of ten plant species having different levels of phototoxic activity. Regression analyses performed between the herbivory level and the phototoxic activity of plants indicated a lower number of herbivore attacks per leaf and a higher leaf area removed per attack on the most phototoxic plants. There was, however, no effect of the phototoxic activity of plant tissues on the total area per leaf removed by herbivores or the percent of leaf area consumed. Field observations also revealed that specialist insects typically occurred on highly phototoxic plants whereas generalist insects were predominantly restricted to the least phototoxic plants. Thus PTs do not reduce the total herbivory pressure experienced by plants, although they restrict the range of herbivores attacking plants to specialist herbivores, that is those that are likely to have evolved some adaptation. The purported adaptations of insects to PTs present in their host plants were investigated in a group of specialist and generalist herbivorous insects feeding on the phototoxic foliage of either Hypericum perforatum (Guttiferae) or Viguiera annua (Asteraceae). This comparative approach identified distinct behavioral and biochemical adaptations that are used by generalist and specialist phytophagous insects to circumvent phototoxicity. Generalist insects, three long-horned grasshoppers collected on H. perforatum in the southwest of France, were observed to selectively feed between the glands located on leaves of Hypericum perforatum that contain the PT hypericin. On the other hand, specialist insects, three leaf beetles and one noctuid, all relied on light-avoidance behavioral strategies to prevent photosensitization. Glands containing the PT hypericin were indeed acting as a feeding stimulant to larvae of Cloantha perspicillaris, a specialist noctuid on St John's-wort. Some differences between specialist and generalist insects were also observed in the activities of antioxidant enzymes which are a major biochemical adaptation for insects to tolerate the oxidative stress induced by PTs. Generalist insects relied on high constitutive activities of antioxidant enzymes (glutathione reductase and glutathione S-transferase) whereas insects specialized on phototoxic plants had lower, but PT-inducible activities of antioxidant enzymes. Some important ecophysiological constraints for plants relying on phototoxic defenses were also identified. It was furthermore confirmed that these environmentally-mediated variations in the production of defensive traits in plants affected the performance of herbivorous insects under both laboratory and field conditions. Inconsistencies between the results that were obtained in the present study and predictions based on the classical theory of coevolutionary interactions between host plants and their associated herbivorous insects, led me to propose a modified evolutionary scheme referred to as plant integrated chemical defenses (PICDs). It is suggested that PICDs may have evolved in phototoxic plants to specifically counter the ecophysiological drawbacks associated with phototoxic chemical defenses. (Abstract shortened by UMI.)