Alkaloidal Glycosidase Inhibitors and Digestive Glycosidase Inhibition in Specialist and Generalist Herbivores of Omphalea diandra

Abstract

Generalist herbivores of the neotropical liana Omphalea diandra (Euphorbiaceae) were compared to the specialist herbivore, larvae of the uraniid moth Urania fulgens, with respect to their ability to accumulate the alkaloidal glycosidase inhibitors (AGIs) produced by the plant and the resistance of their digestive glycosidases to inhibition by these AGIs. The generalist herbivores did not accumulate the AGI aglycones 2R,5R-dihydroxymethyl-3R,4R-dihydroxypyrrolidine (DMDP) and 2,6-dideoxy-2,6-imino-D-glycero-L-gulo-heptitol (HNJ) to the levels detected in larvae of U. fulgens, which contained 0.05–0.11% dry weight DMDP and 0.17–0.35% HNJ. Glucosides of DMDP and HNJ that were synthesized by O. diandra were either absent from both the generalist and the specialist herbivores or present at low levels (less than 0.01%), even though HNJ-glucoside was often the most abundant AGI in the foliage. Analyses of the herbivores' feces indicated that failure to accumulate AGIs was due to the compounds being metabolized rather than excreted. The digestive glycosidases of U. fulgens larvae were more resistant to inhibition by AGI aglycones than those of the generalist herbivores. Similarly, sucrose and maltose hydrolysis in two of the generalist lepidopteran herbivores, larvae of Panthiades ballus and Theope virgilius, was more resistant to inhibition by DMDP than in larvae of Spodoptera littoralis, a lepidopteran which does not encounter O. diandra in nature. There was little difference in the susceptibility to AGIs of glycosidases from the generalist coleopteran Rhabdopterus fulvipes, which naturally feeds on O. diandra, compared with the coleopteran Dermestes maculatus, which does not. The glucoside of HNJ was found to be a very potent inhibitor of trehalase activity in all the insects examined. AGIs are considered to reduce the nutritional value of O. diandra to nonadapted herbivores rather than be acutely toxic. Nevertheless, U. fulgens does appear to be unique among Omphalea-feeding insects in its ability to accumulate AGIs, suggesting that it gains some advantage from storing these compounds.