Frank E. Hanson

Foodplant selection and induction of feeding preference among host and non-host plants in larvae of the tobacco hornworm Manduca sexta

Ten host plant (Solanaceae) and twelve non‐host plant species were tested as foodplants for first instar larvae of the tobacco hornworm, Manduca sexta. Only nine host and three non‐host plant species elicited feeding and supported growth up to fifth instar. The range of acceptability suggested that plants be divided into hosts, acceptable non‐hosts, and unacceptable non‐hosts. Using the two‐choice feeding preference test we found that the initial preference for hosts was preserved when larvae were reared on hosts, but was less strong or absent for larvae reared on acceptable non‐hosts. Thus oligophagy in the tobacco hornworm is not induced, but must be inherited.

Olfactory capabilities of the “gustatory” chemoreceptors of the tobacco hornworm larvae

SummaryGustatory chemoreceptors on the maxillae ofManduca sexta responded to natural stimuli from distances of up to 600 μm (average is 100 μm). In the lateral sensilla styloconica, at least three of the four known chemoreceptive cells responded, indicating that different compounds could be involved in the stimulus. The medial sensilla did not show a comparable olfactory capability. Thus, chemoreceptors classed as contact receptors on a morphological basis (thick walls, single apical pore) were responsive to vapors of normal food substances. Adaptation of the receptor was observed prior to contact with the stimulus. This has important implications for experiments on gustatory receptors.

Electrophysiological Recording and Analysis of Insect Chemosensory Responses

The elegant behavioral experiments of Dethier (1955) on the chemosensory control of feeding in the blow fly set the stage for the first recordings of individual cell responses by Hodgson et al. (1955). The animals clearly accepted some substances and rejected others, leading Dethier to infer that one chemosensory cell coded for acceptance and another for rejection. When electrophysiological techniques became available, the resulting data indicated that more than one sensory cell mediates each of these behaviors. Further electrophysiological experimentation led to the elucidation of how salt-, sugar-, and water-sensitive cells can interact to regulate feeding behavior (Dethier, 1976). Since then many investigators have incorporated electrophysiology as an invaluable tool in conjunction with behavioral experiments for elucidating the chemosensory basis of behavior.

Food discrimination and induction of preference for artificial diets in the tobacco hornworm, Manduca sexta.

ABSTRACT. Feeding discrimination of Manduca larvae reared on leaves and a variety of artificial media was tested against leaves, various media, solvent fractions of leaves and media, and media components, including pure chemicals. Field‐collected animals showed the same preferences as did animals cultured in the laboratory for many generations. Rearing larvae on a leaf species, an artificial diet, or homogenized leaves added to artificial diet induced a preference for that food in subsequent choice tests. Extracts of these foods using organic solvents (particularly hexane) elicited feeding choices resembling those evoked by the foods themselves: water extracts were effective as stimulants or deterrents, but responses to them differed considerably from responses to the foods. Animals raised on a defined artificial diet showed an increased preference (or decreased deterrence) for the lipid component (linolenic acid) of that diet in behavioural tests. Thus induction of preference was shown to be influenced by a specific nutrient compound. Fifteen artificial diets were tested; three were successful, including a completely defined medium. Various components of the diets were tested for feeding preferences, both as omissions from the main diet and as pure compounds. Some were stimulatory, most were neutral or slightly deterrent; a few were strongly deterrent. With the exception of linolenic acid, preferences for pure compounds were not significantly correlated with the food on which the animals were reared. The data suggest that food discrimination depends on the perception of a complex chemical message comprised of both polar and non‐polar compounds, with the latter being of somewhat greater importance. The results are consistent with the explanation of the induction of feeding preferences being due to a reduced responsiveness to deterrents, to an increased preference for feeding stimulants or to both.

Differentiation of roles of chemosensory organs in food discrimination among host and non‐host plants by larvae of the tobacco hornworm, Manduca sexta

ABSTRACT. The contributions of olfactory and gustatory organs in food plant discrimination were examined in larvae of Manduca sexta (Johan.) (Lepidoptera, Sphingidae). Larvae, from which various chemosensory organs had been removed surgically, were tested for feeding preferences for a host, tomato (Lycopersicon esculentum); a weakly acceptable non‐host, rape (Brassica napus); and an unacceptable non‐host canna (Canna generalis), using a two‐choice disc bioassay.

Feeding responses to solanaceous allelochemicals by larvae of the tobacco hornworm, Manduca sexta

Feeding responses of the oligophagous tobacco hornworm to allelochemicals prevalent in their host plants were determined in food choice‐tests using filter paper discs laced with a test solution or water (control). Six solanaceous alkaloids, tomatine, tomatidine, solanine, solanocapsine, atropine and nicotine, were tested and only tomatine and solanocapsine were found to influence preference behavior. Solanocapsine (5 mM) deters feeding whereas tomatine (1 mM) stimulates feeding slightly. No synergistic effect of either tomatine or tomatidine with sucrose was found.

THE ROLE OF SENSORY STRUCTURES AND PREOVIPOSITION BEHAVIOR IN OVIPOSITION BY THE PATCH BUTTERFLY, CHLOSYNE LACINIA

The role of antennae and foretarsi in oviposition and host discrimination was investigated in Chlosyne lacinia Geyer (Nymphalidae, Lepidoptera) a cluster laying nymphalid butterfly which exhibits drumming and antennal dipping behavior prior to oviposition. Ablation of the entire antennae drastically reduced oviposition, while fractional antennectomy reduced it in proportion to the number of antennal receptors removed. Host/non‐host ovipositional discrimination was not significantly affected by antennal ablations. Ablation of the foretarsi abolished discrimination in a controlled environment chamber, but did not affect it in outdoor cages or in a greenhouse. This difference was retrospectively associated with a diminished release of host volatiles due to cooler leaf surface temperatures in the environmental chamber or with continuous air turbulance caused by humidifier fans in the environmental chamber. Electrophysiological techniques were used to demonstrate chemosensory activity in setae located on the foretarsi. We conclude that foretarsal contact chemoreceptors employed during drumming are used for host verification in environmental conditions where olfaction is unreliable.

Deterrence of feeding and oviposition responses of adult Heliothis virescens by some compounds bitter-tasting to humans

Some compounds that are bitter‐tasting to humans, both alkaloidal (quinine, quinidine, atropine, caffeine) and non‐alkaloidal (denatonium benzoate, sucrose octaacetate, naringin), deterred feeding and oviposition by Heliothis virescens (F.) in laboratory and field cage experiments. Preliminary electrophysiological studies of gustatory sensilla on the ovipositor of H. virescens provided evidence of 3 neurons, one of which is responsive to sucrose. Preliminary indications are that responses of this neuron may be inhibited by quinine and denatonium benzoate.

Ion dependence of the tarsal sugar receptor of the blowfly Phormia regina

The activity of the tarsal sugar receptor is greatly reduced following prolonged water exposure. The animals behavior, which characteristically reflects receptor input, also shows decreased acceptance of sucrose solutions following prolonged tarsal immersion in deionized water. Long exposure of the tarsi to Bodensteins saline instead of water does not produce as large a decrement in the acceptance response as does water exposure. Recovery of the behavioral response occurs spontaneously after a few hours. The original response level can also be restored immediately if a moderate concentration (0.05 to 0.2 M) of KCl or NaCl is added to the sucrose stimulus. The effect of LiCl is ambiguous: it inhibits the normal sucrose response, thereby tending to mask any restorative effects. The electrophysiological data show that the cellular response level is also restored when Na+ or K+ ions are present in the stimulus. The above data are interpreted to mean that the effect of tarsal water exposure is to slowly leach out ions in the effective extracellular fluid surrounding the receptor membrane, thus lowering the membrane potential and deceasing the receptor potential upon stimulation. The fact that Na+ and K+ when supplied in the stimulating solution temporarily restore the original response level suggests that these extrinsically added ions can be used as current carrying ions to depolarize the cell. The data suggest that the sensillum contains three functional compartments interconnected by partial diffusion barriers: (1) a ‘receptor compartment’ (2) an axial cylinder which contains the dendrites and functions as the immediate extracellular ion source, and (3) a larger axial cylinder which serves as an ion reservoir. A method for statistically analyzing behavioral acceptance data is presented.

The role of leaf lipids in food selection by larvae of the tobacco hornworm,Manduca sexta.

The role of leaf lipids in food plant selection by larvae ofManduca sexta was investigated by measuring preference responses in a two-choice preference test using glass fiber filter paper disks laced with extract (test) or water (control). The larvae respond to the petroleum ether extract of whole leaves of the host-plantLycopersicon esculentum (tomato) extract in a concentration-dependent manner. At “natural concentration” it is the most strongly stimulating extract or compound yet tested using the disk test. This response is affected by food plant experience of the larvae, suggesting stimulation by plant-specific compounds in the extract. The extract contains volatile compounds that attract the larvae. In contrast, it does not promote continued feeding on an agar-cellulose diet that incorporates the extract. Also stimulating are the extracts of leaf surfaces of two hosts,L. esculentum andSolanum pseudocapsicum, and two acceptable nonhosts,Brassicae napus andVigna sinensis, indicating the presence of nonpolar feeding stimulants at the leaf surface. However, similar leaf-surface extracts of the unacceptable plantCanna generalis were inactive, although the surface extraction process renders this plant acceptable. Leaf-surface extracts ofL. esculentum, S. pseudocapsicum, andB. napus evoke feeding responses that are qualitatively comparable to those of their corresponding leaves. However, no such parallel is found for surface extracts ofV. sinensis andC. generalis. Thus, nonpolar compounds at the leaf surface of host and some acceptable non-host-plant species strongly stimulate feeding and hence must play an important role in food selection by the tobacco hornworm.