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First published online November 10, 2003

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Loss of gustatory responses to pyrrolizidine alkaloids after their extensive ingestion in the polyphagous caterpillar Estigmene acrea

E. A. Bernays^1,*, D. Rodrigues², R. F. Chapman^3,, M. S. Singer¹ and T. Hartmann⁴

¹ Department of Entomology, University of Arizona, PO Box 210088, Tucson, AZ 85721-0088, USA
² Universidade Federal do Rio Grande do Sul, IB, PPG, Biologia Animal, Departamento de Zoologia, Avenida Bento Gonçalves, 9.500, Bloco IV, Prédio 43435, Bairro Agronomia, CEP 91.501-970, Porto Alegre – RS, Brazil
³ Division of Neurobiology, University of Arizona, PO Box 210077, Tucson, AZ 85721-0077, USA
⁴ Institut für Pharmazeutische Biologie der Technischen Universität, Mendelssohnstrasse 1, D-38106, Braunschweig, Germany

View larger version (33K): [in a new window]   Fig. 1. Examples of recordings from the lateral galeal sensillum. (A) Three recordings illustrate the normal response of the pyrrolizidine alkaloid (PA) cell to 10-7 mol l-1 seneciphylline N-oxide. (B) Three recordings of normal responses to the electrolyte alone, showing principally the response of a salt cell. (C) Six recordings to show the lack of response to 10-7 mol l-1 seneciphylline N-oxide after recent feeding on Senecio longilobus. First 500 ms shown.

View larger version (12K): [in a new window]   Fig. 2. The response of the pyrrolizidine alkaloid (PA) cell to 10-7 mol l-1 seneciphylline N-oxide after recent feeding on Senecio longilobus: (A) control vs 6-h exposure, (B) control vs 24- or 48-h exposure. Numbers in parentheses indicate number of replicates in each treatment. Arrows indicate median values. Asterisks indicate significant difference from controls using Dunnett's test at P<0.05.

View larger version (12K): [in a new window]   Fig. 3. The response of the pyrrolizidine alkaloid (PA) cell to 10-7 mol l-1 seneciphylline N-oxide in relation to feeding parameters on Senecio longilobus. (A) Spearman's rank correlation (relating duration of actual ingestion and resultant sensory response) shown for different durations of exposure to S. longilobus. (B) Response of the PA cell to 10-7 mol l-1 seneciphylline N-oxide for control insects and individuals that had fed for shorter times (1–35 min) or longer times (>35 min) during the previous 2 h. (C) Response of the PA cell to 10-7 mol l-1 seneciphylline N-oxide in insects that had different final bout durations on S. longilobus. Numbers in parentheses indicate number of replicates in each treatment. Arrows indicate median values. Different letters indicate significant differences among groups using Tukey tests at P<0.05.

View larger version (12K): [in a new window]   Fig. 4. Response of pyrrolizidine alkaloid (PA) cells in the lateral galeal sensillum to 10-7 mol l-1 seneciphylline N-oxide after 24 h of exposure to synthetic diets in the laboratory. The foods were control diet, diet containing 1% or 2% dry mass monocrotaline or diet containing 1% dry mass retrorsine. Numbers in parentheses indicate number of replicates in each treatment. Arrows indicate median values. Asterisks indicate significant difference from controls using Dunnett's test at P<0.05.

View larger version (16K): [in a new window]   Fig. 5. Effects of rearing on diet containing low concentration of monocrotaline. (A) Response of pyrrolizidine alkaloid (PA) cells in the lateral galeal sensillum to 10-7 mol l-1 seneciphylline N-oxide after 24 h of exposure to synthetic diets containing different concentrations of monocrotaline. Only those individuals that responded in a typical manner are shown. (B) Percentage of insects in each category in which sensory shutoff of the PA cell was observed (% less than 10 spikes). (C) Numbers of fecal pellets produced in the 24-h test feeding period. Bars represent means, and vertical lines represent S.E.M.

View larger version (30K): [in a new window]   Fig. 6. Adaptation to sap from Senecio longilobus plants. (A) Examples of traces to show the initial response to the sap and the loss of response after two and three minutes of exposure to the sap. (B) Firing rate of the lateral galeal sensillum to 10-7 mol l-1 seneciphylline N-oxide throughout the second of exposure at the three different times. Values are means ± S.E.M. (N=6).

View larger version (12K): [in a new window]   Fig. 7. Disadaptation of the pyrrolizidine alkaloid (PA) cells in the lateral galeal sensillum to 10-7 mol l-1 seneciphylline N-oxide after adaptation using exposure of the sensillum for 10 min to sap of Senecio longilobus. Asterisks indicate a significant decrease from initial level of response (P<0.05). The black square at time zero is the initial firing rate normalized to one.

View larger version (27K): [in a new window]   Fig. 8. Effects of injection. Response of pyrrolizidine alkaloid (PA) cells in the lateral galeal sensillum to 10-7 mol l-1 seneciphylline N-oxide after injection of saline or 5 µl of 1% monocrotaline. Data for the saline-injected individuals (N=9) are shown as means ± S.E.M. (broken line). Data for injected insects (N=10) are shown as individual trajectories. The arrow indicates injection time (within 10 min of the initial recording).

View larger version (11K): [in a new window]   Fig. 9. Responses of cells other than the pyrrolizidine alkaloid (PA) cell in the lateral galeal sensillum in various insects with or without a sensory shutoff in the PA cell in the lateral galeal sensillum. Open symbols represent individuals with no PA response in the lateral sensillum; filled symbols represent individuals with a normal PA response in the lateral sensillum. Asterisks indicate a significant decrease in response by insects whose PA cell in the lateral galeal sensillum is non-responsive.