Food aversion learning in the polyphagous grasshopper Schistocerca americana

ABSTRACT. The ability of the acridid Schistocerca americana (Drury) (Orthoptera: Acrididae) to learn to avoid a food when it is associated with an artificial aversive stimulus was examined. The aversive stimulus used was an injection of nicotine hydrogen tartrate at a concentration which usually did not cause knockdown. Insects learned to avoid a food which already had limited sustained acceptability. The learning was not found when the aversive stimulus followed a meal on a fully acceptable food.     

Declining acceptability of a food plant for the polyphagous grasshopper Schistocerca americana: the role of food aversion learning

ABSTRACT Successive contacts with a food that was initially acceptable to the acridid Schistocerca americana (Drury) (Orthoptera: Acrididae) were monitored. It was found that acceptability, as measured by meal length, declined with experience until the food, spinach, was completely rejected. Reduced acceptability of spinach was maintained even after feeding for three meals on a fully acceptable and suitable food, a period of 2–3 h. Experiments with spinach-filled capsules placed in the gut suggested that the decline in acceptability was not due to direct feedback from the gut or haemolymph on the sensory or feeding control systems. Food aversion learning is indicated as the mechanism underlying the decline in acceptability.     

Phytosterol structure and its impact on feeding behaviour in the generalist grasshopper Schistocerca americana

Abstract.Sixth-stadium nymphs of the grasshopper Schistocerca americana (Drury) (Orthoptera: Acrididae) were observed in a series of experiments designed to measure feeding behaviour in response to suitable and unsuitable phytosterols. In the first experiment, grasshoppers were presented with artificial diet that contained either sitosterol, a suitable phytosterol, or a spinach lipid extract which contained only unsuitable sterols as well as other spinach lipids. The diet with the spinach lipid extract, but not the sitosterol diet, evoked a deterrent response. To determine if the spinach sterols were responsible for the deterrent response, a second experiment was performed where the spinach lipid extract was separated into three lipid classes, including desmethyl sterols, dimethyl sterols and the remaining spinach lipids. Grasshoppers presented with artificial diet containing the desmethyl sterols (the end-product sterols in spinach) exhibited deterrent responses. Finally, feeding behaviour to a suite of different sterols, including cholesterol (suitable), stigmasterol (unsuitable), and lathosterol (unsuitable), was observed; these sterols were selected because they show variation in the position of double bonds. Grasshoppers presented with diets containing unsuitable sterols again exhibited deterrent responses. Overall, the deterrent effect was strongest when sterols with a double bond at position 22 were in the diet.     

Rutin: a phagostimulant for the polyphagous acridid Schistocerca americana

Rutin was demonstrated to be a phagostimulant for the grasshopper Schistocerca americana across a very wide concentration range. The effect was not maintained over a period of days if the insects had already ingested a large amount, but when individuals were given different concentrations on disks as supplements to their lettuce diet, they tended to self select a moderate quantity on a daily basis. In long term experiments on food utilization and growth rates using artificial diet, no beneficial effects of rutin could be demonstrated. Ingested rutin was absorbed and some of it deposited in the cuticle. Most was excreted as the aglycone quercetin. The possible functional significance of the phagostimulatory effect is discussed.Dedicated to G.B. Marini-Bettolo     

Tarsal taste sensilla of the autumn gum moth, Mnesampela privata: morphology and electrophysiological activity

Mnesampela privata Guenée (Lepidoptera: Geometridae: Ennominae) is a native Australian geometrid that conducts considerable host assessment prior to ovipositing on its host plants, which belong to the genus Eucalyptus . The leaves of some of their hosts are covered with a particularly thick and waxy cuticle and we have shown that epicuticular waxes influence the oviposition preferences of females. This necessitates that M. privata has evolved specific chemosensory organs to assess the identity and perhaps even the quality of its hosts. In this work, we examined the morphology of tarsal taste sensilla and the sensitivity of their sensory neurones to a range of primary metabolites possibly influential on host assessment and oviposition. The ventral surface of the fifth tarsomere of females bear two parallel rows of up to eight sensilla, each loosely aligned with two parallel rows of five spines. Salts, sugars, and amino acids elicited phasi-tonic multicellular neuronal responses of variable magnitude and form. Two pairs of sensilla are closely apposed to the most distal spine in each row; the sensory neurones associated with these sensilla exhibited notably larger responses to alanine and serine compared with those of all other sensilla. The arrangement of the taste sensilla in close proximity to prominent tarsal spines is unique and could represent an adaptation that enables them to penetrate the wax layer and be brought into contact with primary metabolites present closer to the leaf surface.     

Phytosterol unsuitability as a factor mediating food aversion learning in the grasshopper Schistocerca americana

Abstract Sixth stadium nymphs of the grasshopper Schistocerca americana (Drury) (Orthoptera: Acrididae) were presented with spinach with or without added cholesterol or β-sitosterol, and the lengths of the first four meals were monitored. Spinach alone evoked a typical aversion learning pattern in which successive meals were of decreasing duration; however, when cholesterol or β-sitosterol was added the spinach remained acceptable. Nymphs fed spinach for 24h preferred glass-fibre discs with added cholesterol in a choice test, but nymphs fed wheat (an acceptable food) did not prefer cholesterol-treated or control discs. Nymphs pretreated with spinach did not distinguish between discs treated with stigmasterol (an unsuitable phytosterol for grasshoppers) and control discs. In no-choice tests, nymphs pretreated with spinach also fed significantly longer on discs with added 10% cholesterol or 1%β-sitosterol, compared to meals on discs with stigmasterol or sucrose controls. Detection of appropriate sterols is likely to involve a post-ingestive feedback mechanism, as significantly longer meals on discs treated with only sucrose resulted when spinach-fed nymphs, were force-fed gelatin capsules packed with β-sitosterol or cholesterol, compared with stigmasterol. Contact chemoreception is unlikely to play a role in this behaviour, as discs (lacking sucrose) treated with cholesterol, β-sitosterol, stigmasterol, or a chloroform control, all required similar numbers of contacts before feeding was initiated.     

Developmental specialization and geographic structure of host plant use in a polyphagous grasshopper, Schistocerca emarginata (=lineata) (Orthoptera: Acrididae)

Host plant use and availability were determined in early nymphal and adult-stage Schistocerca emarginata (=lineata) (Orthoptera: Acrididae) populations at six localities in Texas, USA. Early instar nymphal populations were feeding almost exclusively on either Ptelea trifoliata (Rutaceae) or Rubus trivialis (Rosaceae). This study represents the first demonstration of a geographic structure of host plant specificity in a polyphagous grasshopper. Recognizing this geographic structure required investigations of both developmental and geographical variation in host plant use. Nymphal diet breadths were significantly less than adult diet breadths at four of six localities and smaller overall when pooled nymphal and adult diet breadths were compared among sites. Neither restricted nymphal mobility nor host plant availability accounted for the observed differences in host plant use between developmental stages and among localities. Evidence suggests that the differences in host use among populations are due to host-plant-associated genetic differentiation. Received: 4 June 1998 / Accepted: 10 March 1999     

The relationship between plant acceptability and suitability for survival and development of the polyphagous grasshopper,Schistocerca americana (Orthoptera: Acrididae)

The feeding behavior of final-instar nymphs ofSchistocerca americana was observed when they first encountered plants that ranged in acceptability from being eaten in large amounts to not being eaten at all. Growth and survival on the same plants through the last stadium were also studied and the results combined as a suitability index to facilitate comparison with the behavior. Although the plants that were eaten most gave the highest suitability index and those that were not eaten permitted no survival, there was no simple relationship between the amounts eaten and the suitability for growth and survival. The possibility that the insects might become habituated to plants that were initially unacceptable was investigated, but no habituation was found over a 3-day period. It is suggested that food intake is largely determined by the presence of deterrent compounds in the less acceptable foods and that nutritional differences between the plants are likely to have been of minor importance. The behavior on some foods suggests that food aversion learning may be involved. It is concluded that the variability of the insects' behavior makes it impossible to predict the suitability of a plant from their immediate behavioral responses. In the field, insects may sometimes reject foods that would be suitable for survival and development, and feed on plants that are nutritionally deficient or even toxic.     

Presence of corazonin in three insect species, and isolation and identification of [His7]corazonin from Schistocerca americana.

An ELISA for corazonin, a cardioactive neuropeptide from the American cockroach, Periplaneta americana, was developed. It was used to isolate corazonin from the cockroach Nauphoeta cinerea, the locust Schistocerca americana, and the hawkmoth Manduca sexta. The peptides from Nauphoeta and Manduca had the same retention times as Periplaneta corazonin, and their amino acid compositions also suggested that these peptides are identical with corazonin. The corazonin-immunoreactive peptide from Schistocerca eluted slightly earlier on HPLC than corazonin, and its structure was determined to be [His⁷]corazonin, or pGlu-Thr-Phe-Gln-Tyr-Ser-His-Gly-Trp-Thr-Asn-amide. These results indicate that corazonin is generally present in insects and that its structure has been well conserved.     

The time-course of behavioural phase change in nymphs of the desert locust, Schistocerca gregaria

Abstract. The time-course of behavioural phase change was investigated in nymphs of Schistocerca gregaria , using logistic regression analysis of behaviour recorded in a standard assay. Gregarization occurred very rapidly. Solitary-reared nymphs became markedly gregarious in behaviour within 1-4h of being placed in a crowd. These insects re-solitarized equally quickly if removed from the crowd. Crowd-reared locusts also solitarized within l-4h, but this effect was not complete. Results indicate that, while behavioural gregarization is maximal within a few hours of crowding, solitarization is a two-stage process, changing rapidly at first, then more slowly as a function of the period of previous crowding.     

Interactions between two neurons in contact chemosensilla of the grasshopper,Schistocerca americana

Summary The tibial contact chemosensilla of Schistocerca americana contain several neurons, one of which responds to nicotine hydrogen tartrate and certain other compounds. The activity of this cell is sometimes briefly interrupted by the firing of a second cell in the same sensillum which usually only fires a few times in the first 500 ms of a stimulation. The evidence suggests that the nicotine-sensitive cell is directly inhibited by the activity of the second cell. Not all cells in the sensillum produce the same effect.     

Ontogeny of tracheal dimensions and gas exchange capacities in the grasshopper, Schistocerca americana

How does body size affect the structure and gas exchange capacities of insect tracheae? Do insects become more oxygen-limited as they grow? We addressed these questions by measuring the dimensions of two transverse tracheae within the abdomen of American locusts of different ages, and evaluating the potential for diffusion or convection to provide adequate gas exchange. The grasshopper abdomen has longitudinal tracheae that run along the midgut, heart, nerve cord, and lateral body wall. Transverse tracheae run from each spiracle to the longitudinal tracheae. Dorsal air sacs attach near each spiracle. In both transverse tracheae studied, diffusive capacities increased more slowly than metabolic rates with age, and calculated oxygen gradients necessary to supply oxygen by diffusion increased exponentially with age. However, surgical studies demonstrated that transport of gas through these transverse tracheae occurred by convection, at least in adults. Convective capacities paralleled metabolic rates with age, and the calculated pressure gradients required to sustain oxygen consumption rates by convection were independent of age. Thus, in growing grasshoppers, tracheal capacities matched tissue oxygen needs. Our morphological and physiological data together suggest that use of convection allows older grasshoppers to overcome potential limitations on size imposed by diffusion through tracheal systems.     

Morphological and behavioural characteristics of a gynandromorph of the desert locust, Schistocerca gregaria

Abstract.  Morphological and behavioural characteristics are investigated for a gynandromorph of the desert locust, Schistocerca gregaria , appearing under isolated rearing conditions in the laboratory. It has both male and female external reproductive organs bilaterally. The body size and dimensions are similar to a normal male. Morphometric traits (fore wing length/maximum head width ratio and fore wing length/hind femur length ratio) of the gynandromorph are typical for the values of solitarious locusts. When the gynandromorph is placed into an arena holding ten sexually mature gregarious females, it shows a distinct male behaviour: it jumps on a female and tries to mate with her. When kept together with males, males recognize this gynandromorph as a female because some of them try to mount, although no successful copulation is observed. The results suggest that the gynandromorph might have had a female-specific pheromone. Dissection reveals that the gynandromorph has no testis but abnormal ovaries containing vitellogenic oocytes. These observations indicate that the gynandromorph obtained has a mixture of male and female morphological characteristics and behaves like a male but is recognized as a female by conspecific males.     

Antennal sensilla of male and female of the nut weevil,Curculio nucum Linnaeus, 1758 (Coleoptera: Curculionidae)

The nut weevil, Curculio nucum (Linnaeus, 1758), is the main pest in hazelnut orchards (Corylus avellana L.). Semiochemicals are interesting bio control tools that could be used to manipulate the pest behaviour and to control pest populations. The study of the sensorial equipment of the insect antennae provides information on the importance of olfaction in the adult life for host plants and mate findings as well as on the putative other senses. Before electrophysiological investigation, the knowledge of antennae equipment is also necessary. The aim of this study is to determine the types, number and location of sensilla on the antennae of male and female adult C. nucum in order to determine their implication in seeking a sexual partner and a host plant. The 12-segmented antenna comprises a scape, a 7-segmented funicle and a 4-segmented club. Out of the nine sensillum types listed, three are present on the scape and the funicle and seven types on the club which gathers 71–73% of the total of sensilla. Tactile aporous sensilla chaetica C1, gustatory uniporous sensilla chaetica C2, olfactory multiporous sensilla basiconica B1 and B2 are found on both the dorsal and ventral surfaces of the club in both sexes. Thermo-hygroreceptive dome-shaped sensilla D, olfactory multiporous sensilla basiconica B3 and olfactory multiporous fluted sensilla basiconica F are found exclusively on the ventral surface of the club, suggesting that these sensilla are utilized in host plant acceptance during antennal tapping. The sexual dimorphism concerns only the numbers of sensilla chaetica C1 and sensilla basiconica B2.     

Development of phenotypic differences in sensillum populations on the antennae of a grasshopper,Schistocerca americana

The development of diet-induced phenotypic differences in numbers of sensilla on the antennae of the grasshopper Schistocerca americana was studied using the exuviae produced at each molt. This made it possible to follow changes within an individual insect. In the first instar, insects had similar numbers of four sensillum types: uniporous trichoid sensilla, coeloconic sensilla, and large and small multiporous basiconic sensilla. Rearing on lettuce resulted in sixth instars with greater numbers of three sensillum types than siblings reared on an artificial diet. The first statistically significant differences between treatments in numbers of trichoid sensilla and large basiconic sensilla occurred in the third and fourth instars, respectively. No major reductions in sensillum numbers occurred at any time and the phenotypic differences resulted from differences in the numbers added at each molt.     

Presence of a single abundant storage hexamerin in both larvae and adults of the grasshopper, Schistocerca americana

We identified a single hexameric storage protein in the grasshopper, Schistocerca americana, and monitored its abundance through the last larval instar and up until reproductive competence in adults of both sexes. This storage hexamerin, termed Schistocerca americana Persistent Storage Protein (saPSP) was the most abundant soluble protein in both larvae and adults. In both sexes, saPSP abundance started out low at the onset of the last larval instar and accumulated during feeding, peaking just prior to molting. Adults of both sexes contained significant amounts of saPSP after eclosion. In adult males, saPSP content dropped continuously after eclosion and was lowest once individuals reached reproductive maturity. In contrast, adult females depleted saPSP reserves during the first days of adulthood, but subsequently accumulated significant saPSP stores. In adult females, saPSP stores peaked just prior to the completion of egg provisioning. Given the overall patterns of abundance, saPSP has functions in both larvae and adults. In addition, the observed pattern of storage hexamerin accumulation differs from patterns of accumulation in the other known grasshoppers, Locusta migratoria and Romalea microptera, suggesting that significant functional diversity has evolved in storage hexamerins among the grasshoppers.     

Morphological and electrophysiological characteristics of the epipharyngeal sensilla of the silkworm, Bombyx mori

One pair of gustatory sensilla was found on the epipharynx ofBombyx mori larvae, and some morphological and electrophysiological characteristics of the epipharyngeal sensilla were investigated. They are sensilla coeloconica composed of a small papilla with a pore at the tip and a swelling of cuticle encircling the papilla. Three bipolar neurons innervate each sensillum. One neuron is an inositol receptor which responds to inositol only. Another cell responds with action potentials of relatively large amplitude to some feeding deterrent substances, such as strychnine nitrate. The thresholds of these cells for inositol and strychnine nitrate are approximately 10⁻⁴ M and 10⁻⁷ M, respectively. At least two kinds of spikes can be observed when these sensilla are stimulated with some salts and acids. Dose-response relationships and time courses of responses to inositol and strychnine nitrate were also examined in this study.     

Volumetric feedback and the control of meal size in Schistocerca gregaria

The role and nature of volumetric feedbacks in the regulation of meal size was investigated for Schistocerca gregaria. Feedback from the anterior region of the crop was found to be important and denervation led to hyperphagia. Additional feedbacks were found from more posterior gut regions. Cannulating agar or paraffin into the mid- and hindgut caused a decrease in the size of a following meal. This effect was removed by cutting the ventral nerve cord anterior to the terminal abdominal ganglion. Increasing the blood volume by injections of isotonic saline into the haemocoel was also found to decrease subsequent meal size. This effect was not mediated via the gut or body wall stretch receptors and possible mechanisms are discussed. The results for S. gregaria are compared with those obtained previously from Locusta migratoria.

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Résumé L'étude de la nature et du rôle des feed backs volumétriques dans la régulation de la taille du repas a été effectuée chez S. gregaria. Un feed back, originaire de la région antérieure du jabot, s'est révélé important et la dénervation a provoqué l'hyperphagie. Des feed backs supplémentaires ont été décelés dans des régions plus postérieures du jabot. De l'agar ou de la paraffine canulés dans la jabot moyen et postérieur ont provoqué une diminution de la taille du repas suivant. Ces effets sont supprimés avec la section de la corde nerveuse centrale avant le ganglion abdominal terminal. L'augmentation du volume sanguin par des injections de solution saline isotonique a aussi diminué la taille du repas suivant. Cet effet n'est pas transmis via des récepteurs de tension du jabot ou de la paroi du corps; des mécanismes envisageables sont discutés. Ces résultats avec S. gregaria sont comparés à ceux obtenus antérieurement avec Locusta migratoria.

     

Contact chemoreception related to host selection and oviposition behaviour in the monarch butterfly, Danaus plexippus

Abstract. Behavioural events during host selection by ovipositing monarch butterflies (Danaus plexippus (L.), Danainae, Nymphalidae) include tapping the leaf surface with fore-tarsi and touching this surface with mid-tarsi (‘drumming’) and antennae. Flavonoids identified from host plant extracts are known to stimulate oviposition. Scanning electron microscopy revealed the presence of contact-chemoreceptor sensilla on all appendages that contact the leaf surface. This electrophysiological study was conducted to identify the contact chemoreceptors that are sensitive to the known oviposition stimuli and are therefore probably involved in host recognition. Receptor cells of conspicuous sensilla grouped in clusters on fore-tarsi of females were sensitive to the behaviourally active butanol fraction of host plant (Asclepias curassavica) extract. However, these receptors generally had low sensitivity to three oviposition-stimulating flavonoids identified from this fraction, but they were also sensitive to the butanol fraction of a non-host (Brassica oleracea). Chemoreceptors in sensilla of the tarsomers 2–4 of the mid-legs also responded to the behaviourally active fraction of host plant extract and showed some sensitivity to two of the flavonoids that stimulate oviposition. Similar results were obtained from receptor cells in sensilla on the tip of the antennae. Most of these sensilla had cells responding to the butanol fraction of A. curassavica extract but only 25% of them were also sensitive to one of the behaviourally active flavonoids. These electrophysiological results, in combination with behavioural observations, suggest that host selection in monarch butterflies relies on a complex pattern of peripheral sensory information from several types of tarsal and antennal contact chemoreceptors.     

Larval nutrition affects lipid storage and growth, but not protein or carbohydrate storage in newly eclosed adults of the grasshopper Schistocerca americana

Nitrogen availability from dietary protein can have profound effects on the physiology and evolutionary ecology of insect herbivores. While many studies consider the effects of nutrition on consumption and gross body composition of protein and other important nutrients, few consider partitioning to storage for future use. I used chemically defined artificial diets to quantitatively manipulate the amount of dietary carbohydrates and proteins available to growing larvae of the grasshopper Schistocerca americana to determine how larval nutrient availability affects growth and all three classes of stored nutrients (proteins, lipids, and carbohydrates) carried over from larval feeding into adulthood. Larvae on poor diets increased consumption, but could not compensate for diet quality, eclosing small and containing no significant nutrient stores at adulthood. Individuals fed intermediate to high nutrient content diets as larvae were significantly larger and contained a significantly greater proportion of lipid stores at adult eclosion, but not protein or carbohydrate stores than individuals fed low nutrient content diets. This suggests that larvally derived lipid stores may be more important to adult fitness than carbohydrate or protein stores. This result is contrary to previous studies performed on the role of larval nutrition and allocation to protein stores, and this difference is likely due to variation in the relative availability of protein in adult diets across species.