Experience-based behavioral and chemosensory changes in the generalist insect herbivore Helicoverpa armigera exposed to two deterrent plant chemicals

Behavioral and electrophysiological responses of larvae of the polyphagous moth species Helicoverpa armigera to two plant-derived allelochemicals were studied, both in larvae that had been reared on a diet devoid of these compounds and in larvae previously exposed to these compounds. In dual-choice cotton leaf disk and pepper fruit disk arena assays, caterpillars reared on a normal artificial diet were strongly deterred by strychnine and strophanthin-K. However, caterpillars reared on an artificial diet containing strychnine were insensitive to strychnine and strophanthin-K. Similarly, caterpillars reared on an artificial diet containing strophanthin-K were also desensitized to both deterrent chemicals. Electrophysiological tests revealed that the deterrent-sensitive neurons in taste sensilla on the maxillae of caterpillars reared on each deterrent-containing diet displayed reduced sensitivity to the two chemicals compared with the caterpillars reared on normal diets. We conclude that the experience-dependent behavioral plasticity was partly based on the reduced sensitivity of taste receptor neurons and that the desensitization of taste receptor neurons contributed to the cross-habituation to the two chemicals.     

The role of the antennae and maxillary palps in mediating food preference by larvae of the tobacco hornworm, Manduca sexta

The role of antennae and maxillary palps in mediating food preferences by Manduca sexta (Johan.) (Lepidoptera: Sphingidae) was examined. Fifth‐instar larvae, having different chemosensory organs remaining after microsurgery, were tested in two‐choice feeding assays using three solanaceous host species Lycopersicon esculentum (Mill.), Datura innoxia (Mill.), and Solanum pseudocapsicum (L.), an acceptable non‐host Raphanus sativus (L.) (Cruciferae), and an unacceptable non‐host Pelargonium hortorum (L.H. Bailey) (Geraniaceae). Larvae had a choice between leaf discs of two plant species or between one species and moist filter paper discs (water). The antennae are fully competent in mediating normal (unimpaired) food preferences for S. pseudocapsicum vs. water and P. hortorum vs. water. Thus, the antennae alone can mediate both acceptance and rejection behaviour. The latter is the first report of such a function in M. sexta. The antennae are partly competent (reduced preference) for S. pseudocapsicum vs. P. hortorum. No antennal competence could be demonstrated using the other plant species tested. The antennae alone are either partly needed (R. sativus vs. water) or not necessary to elicit normal food preferences for the plant species tested. The maxillary palps are fully competent in mediating normal food preference for S. pseudocapsicum vs. water, and D. innoxia vs. water. The palps are partly competent for S. pseudocapsicum vs. P. hortorum and incompetent for the other plant species tested. Thus, the maxillary palps alone could only mediate acceptance behaviour in this study. The need of the maxillary palps in normal food preferences could not be demonstrated. Interestingly, the maxillary palps alone can mediate food preferences for two normally rejected plants, R. sativus and P. hortorum. Similar results are reported for two other non‐host plant species, Vigna unguiculata (Walp.) (Leguminosae) and Vinca rosea (L.) (Apocynaceae). Perhaps, the maxillary palps inform M. sexta mostly about feeding stimulatory chemicals common to most plant species.     

Induced preference for host plant chemicals in the tobacco hornworm: contribution of olfaction and taste

Many herbivorous insects induce preferences for host plants. Recent work in Manduca sexta indicates that induced preferences are mediated by a “tuning” of the peripheral taste system to chemicals within host plant foliage. We tested this hypothesis by rearing caterpillars on artificial diet or potato foliage, and then examining olfactory- and taste-mediated responses to potato foliage extract. First, we confirmed earlier reports that consumption of potato foliage tunes the peripheral taste system by reducing responsiveness to glucose and increasing responsiveness to foliage extract. Second, we offered caterpillars a choice between disks treated with foliage extract (experimental) or solvent alone (control). The foliage-reared caterpillars approached and consumed the experimental disks disproportionately, whereas the diet-reared caterpillars approached and consumed both disks indiscriminately. This indicated that induced preferences involve olfaction and taste. Third, we ran choice tests with foliage-reared caterpillars deprived of either olfactory or gustatory input. Caterpillars lacking olfactory input approached both disks indiscriminately, but fed selectively on experimental disks. In contrast, caterpillars lacking gustatory input approached experimental disks selectively, but fed indiscriminately on both types of disk. We conclude that even though olfaction helps caterpillars locate potato foliage, it is the “tuned” gustatory response that ultimately mediates the induced preference.     

Specialist deterrent chemoreceptors enable Pieris caterpillars to discriminate between chemically different deterrents

Pieris butterflies (Lepidoptera: Pieridae) are specialist herbivores of cruciferous plants. They exploit glucosinolates, secondary plant metabolites chemotaxonomically characteristic for this plant family, as token stimuli. In addition to particular glucosinolates, some genera of the Cruciferae contain cardenolides, steroidal allelochemicals that act as potent feeding and oviposition deterrents to several Pieris species. We investigated the sensory mechanisms by which these compounds are perceived in larvae. Pieris caterpillars and many other lepidopterous species are endowed with so-called generalist deterrent receptors, that respond to a broad spectrum of secondary plant substances. In Pieris caterpillars we found a second type of deterrent chemoreceptor in maxillary styloconic taste sensilla. This neuron is very sensitive to cardenolides (threshold 0.1–0.3 M). The generalist deterrent receptor also responds to these substances but its threshold lies at 50–100× higher concentrations. In behavioural preference experiments Pieris brassicae L. caterpillars preferred cardenolide-treated cabbage leaf discs when confronted with a choice between them and a deterrent substance that does not occur in the Brassicaceae. The cardenolides acted as potent deterrents when offered against untreated cabbage leaf discs. This demonstrates that the balance of activity elicited in the two types of deterrent chemoreceptors determines the behavioural decision.     

Olfactory receptors on the maxillary palps of small ermine moth larvae: evolutionary history of benzaldehyde sensitivity

In lepidopterous larvae the maxillary palps contain a large portion of the sensory equipment of the insect. Yet, knowledge about the sensitivity of these cells is limited. In this paper a morphological, behavioral, and electrophysiological investigation of the maxillary palps of Yponomeuta cagnagellus (Lepidoptera: Yponomeutidae) is presented. In addition to thermoreceptors, CO₂ receptors, and gustatory receptors, evidence is reported for the existence of two groups of receptor cells sensitive to plant volatiles. Cells that are mainly sensitive to (E)-2-hexenal and hexanal or to (Z)-3-hexen-1-ol and 1-hexanol were found. Interestingly, a high sensitivity for benzaldehyde was also found. This compound is not known to be present in Euonymus europaeus, the host plant of the monophagous Yponomeuta cagnagellus, but it is a prominent compound in Rosaceae, the presumed hosts of the ancestors of Y. cagnagellus. To elucidate the evolutionary history of this sensitivity, and its possible role in host shifts, feeding responses of three Yponomeuta species to benzaldehyde were investigated. The results confirm the hypothesis that the sensitivity to benzaldehyde evolved during the ancestral shift from Celastraceae to Rosaceae and can be considered an evolutionary relict, retained in the recently backshifted Celastraceae-specialist Y. cagnagellus.     

Ultra morphology of sensilla on the head and mouth parts of the earwig Anisolabis martima (Bonelli) (Dermaptera: Carcinophoridae)

The earwig Anisolabis maritima is a cosmopolitan insect with a worldwide distribution, omnivorous in feeding, eating the eggs of different insects. Recently recorded in Saudi Arabia as a beneficial predator on eggs and newly hatched larvae of the red palm weevil Rhyncophrous ferrugineus, scanning electron microscopy (SEM) observations revealed the presence of different kinds of receptor sensillae occurring on the head and mouth parts of A. maritime. The sensillae are the same, but differ in numbers on both sexes. The head surface bears three subtypes of trichoid sensillae, one type of ceoloconica. Labrum, labium, labial palps and maxillary palps, possess different kinds of sensillae. Three subtypes of trichoid have been identified on the labrum. The labium contained one type of tricoid and basiconic sensillae. There are great numbers and numerous sensillae cheatica differing in length distributed on the maxillary and the labial palps on all segments between other stutter spines. The last terminal segment of maxillary or labial palps bears the greatest number of the sensillae cheatica. Adult A. maritima may be introduced in the future as a beneficial predator of eggs of R. ferrugineus as a tool for integrated pest management.     

Consumption of a toxic food by caterpillars increases with dietary exposure: support for a role of induced detoxification enzymes

We examined whether there is a link between feeding behavior and detoxification enzyme activity, which increases over time in proportion to the ingested dose of toxic allelochemicals. We hypothesized that, for insects consuming a toxic but nondeterrent food, consumption would initially decline but then increase after continuous exposure in conjunction with the induction of detoxification enzyme activity. We tested this hypothesis by observing the feeding behavior of fall armyworms (Spodoptera frugiperda) when offered diets containing indole 3-carbinol (I3C), a well-known inducer of detoxification enzymes in this species. The I3C concentrations used were toxic but nondeterrent, thereby avoiding any confounding influence of preingestive responses. The feeding pattern of caterpillars previously unexposed to dietary I3C (i.e. with basal detoxification enzyme activity) was substantially altered when offered I3C-containing diets. Compared with control caterpillars fed I3C-free diets, they exhibited fewer feeding bouts and had a greater proportion of long (> 60 min) non-feeding pauses between bouts. In contrast, the feeding pattern of caterpillars pre-exposed to an I3C diet (i.e. with induced detoxification enzyme activity) did not differ from that of control caterpillars. We conclude that there is a relationship between feeding behavior and detoxification activity in these caterpillars, and propose two postingestive mechanisms that could link these processes.     

Sensilla of the antennae and the labial and maxillary palps of Blattella germanica (L.) (Dictyoptera: Blattellidae): Their classification and distribution

The various sensilla on the antennae and on the labial and maxillary palps of Blattella germanica (L.) were studied. Thick-walled chemoreceptors with fluted shafts and articulated bases are located on the antennae and on the labial and maxillary palps. Thin-walled chemoreceptors, without fluted shafts or articulated bases, are restricted to the flagellar segments of the antennae and to the distal segments of the palps. Antennae of adult males have more thin-walled chemoreceptors than do those of females. Hair-plate sensilla are found at the scape-head and scape-pedicel joints, and at the joints of segments on the palps. Campaniform sensilla are concentrated as a ring around the distal margin of the pedicel, and are also scattered singly on the scape, pedicel, and flagellar segments of the antennae, and on the first segment of the maxillary palps. Occasionally, a few sensilla coeloconica and cold receptor sensilla are found on the antennal flagellum.     

Deterrence coding by a larval Manduca chemosensory neurone mediating rejection of a non-host plant, Canna generalis L.

Abstract. The physiological basis of phagodeterrence was studied electrophy-siologically and behaviourally in the phytophagous caterpillars Manduca sexta and Manduca quinquemaculata. The model unacceptable non-host plant was the canna lily, Canna generalis. A strongly deterrent extract was obtained from fresh leaves of canna by extraction with hot ethanol or ethyl acetate in a blender. Behavioural rejection of these extracts was similar to that of fresh leaves, although less intense. In contrast, blender extracts using other solvents, as well as leaf surface rinses, were phagostimulant or neutral. Chromatographic fractionation of the deterrent ethanolic extract showed the active principles to be moderately polar and separable into two fractions. Previous ablation experiments had shown that the medial maxillary styloconica and epipharyngeal sensilla are the two most important chemosensory organs in mediating behavioural rejection of canna leaves; if only one of these organs is spared, the animal completely rejects canna. We investigated the neural responses of the medial styloconica and their contribution to the sensory coding responsible for this phagodeterrence. The active fractions of the deterrent ethanolic extract elicited a vigorous response from one chemosensory neurone in the medial styloconica. This neurone is distinguishable from others in the medial styloconica by its unique temporal response parameters and the characteristic shape changes of its action potentials. The response frequency of this neurone correlates with the degree of phagodeterrence in a dose-dependent manner. Threshold deterrence occurs at a concentration of extract (1%) that elicits firing in this neurone at a rate of c. 50 spikes/s peak instantaneous frequency and 30 total spikes in the first Is. We conclude that this is a ’deterrent neurone’ in the sense that vigorous response from this neurone is a sufficient sensory code for behavioural rejection of canna. Thus input from a single sensory neurone is capable of blocking feeding, since only one (unilateral) medial styloconicum is needed to mediate this rejection.     

Allelopathic hormesis and potent allelochemicals from multipurpose tree Moringa oleifera leaf extract

Abstract

The secondary metabolites produced by higher plants may act as allelochemicals to stimulate or inhibit growth of other plant species. Moringa oleifera is a multipurpose tree which have been reported, in separate studies, to promote growth of other plant species at low concentrations and inhibit the growth at high concentrations. However, allelopathic hormesis and allelochemicals from Moringa oleifera has not been reported. The present studies were conducted to evaluate hormesis, allelopathic potential and allelochemicals from Moringa oleifera leaf extract using Lepidium sativum as a test species. The results revealed that aqueous leaf extract of Moringa oleifera promoted the shoot growth of Lepidium sativum by 41% at lowest tested concentration of 2.5%, while the highest tested concentration (10%) of leaf extract inhibited shoot length and root length of Lepidium sativum by 38% and 85%, respectively, showing allelopathic hormesis. Twelve allelochemicals (p-coumaric acid, salicylic acid, p-hydroxybenzoic acid, m-coumaric acid, protocatechuic acid, ferulic acid, p-hydroxysalicylic acid, syringic acid, vanillic acid, p-hydroxybenzaldehyde, m-hydroxybenzaldehyde and gallic acid) were identified from leaf extract of Moringa oleifera. The results suggest that Moringa oleifera exhibit allelopathic hormesis which may have critical impact on defence, survival and invasion of plants in natural as well as agroecosystems.