Differential effect of tannic acid on two tree-feeding Lepidoptera: implications for theories of plant anti-herbivore chemistry

Feeding efficiencies of ultimate instar larvae of two polyphagous tree-feeding Lepidoptera, Malacosoma disstria (Lasiocampidae) and Orgyia leucostigma (Liparidae), were measured on artificial diets containing from 0% to 8% tannic acid. Relative growth rate (RGR) of O. leucostigma was not affected by up to 8% tannic acid, suggesting that O. leucostigma has evolved an effective counteradaptation to hydrolyzable tannins. In contrast, as little as 0.5% tannic acid caused a significant reduction in RGR of M. disstria , due both to reduced efficiency of conversion of digested food (ECD) and reduced relative consumption rate (RCR), and caused a significant increase in mortality during the pupal stage. Moreover, when reared from hatching on tannin-containing diets, no M. disstria larvae survived past the fourth instar.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/47780/1/442_2004_Article_BF00380074.pd

Surfactants: their role in preventing the precipitation of proteins by tannins in insect guts

Much more tannic acid or pin oak tannin is required to precipitate the abundant leaf protein, ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPC), from Manduca sexta gut fluid adjusted to pH 6.5 than is required to precipitate this protein from an aqueous buffer at the same pH. This finding demonstrates that some characteristic of M. sexta gut fluid, in addition to its basicity, counteracts the potential of tannins to precipitate ingested proteins. Gut fluid of M. sexta has a surface tension of 36–39 dynes/cm, indicating the presence of surfactants. Lysolecithin and linoleoylglycine, surfactants known to be present in insect gut fluids, also interfere with the precipitation of RuBPC by tannins at pH 6.5. It is concluded that detergency is a widespread property of insect gut fluids that counteracts the potential of tannins to precipitate die ary proteins, and it is argued that there is no longer any justification for continuing to refer to tannins as digestibility-reducing-substances. Finding that there has been no formidable barrier to the evolution of mechanisms that counter a generalized antidigestive action by tannins is difficult to reconcile with the idea that reduced digestibility is an evolved anti-herbivore adaptation of apparent plants.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/47751/1/442_2004_Article_BF00379632.pd

Food Preferences of the Rubber Plantation Litter Beetle, Luprops tristis, a Nuisance Pest in Rubber Tree Plantations

Massive invasion of the litter dwelling beetle, Luprops tristis Fabricius (Coleoptera: Tenebrionidae), numbering about 0.5 to 4 million per residential building following summer showers, and their prolonged stay in a state of dormancy, make them an extreme nuisance in rubber tree plantation belts of the Western Ghats in south India. Food preference of post-dormancy adults, larvae and teneral adults stages towards tender, mature and senescent leaves were assessed in three choice and no choice leaf disc tests. All stages have strong preference towards fallen tender leaves and lowest preference towards senescent leaves indicating that leaf age is a major attribute determining food selection and food preference of L. tristis. Ready availability of the preferred, prematurely fallen, tender rubber tree leaves as a food resource is suggested as being responsible for the exceptionally high abundance of L. tristis in rubber tree plantation belts

The Tri-Trophic Interactions Hypothesis: Interactive Effects of Host Plant Quality, Diet Breadth and Natural Enemies on Herbivores

Several influential hypotheses in plant-herbivore and herbivore-predator interactions consider the interactive effects of plant quality, herbivore diet breadth, and predation on herbivore performance. Yet individually and collectively, these hypotheses fail to address the simultaneous influence of all three factors. Here we review existing hypotheses, and propose the tri-trophic interactions (TTI) hypothesis to consolidate and integrate their predictions. The TTI hypothesis predicts that dietary specialist herbivores (as compared to generalists) should escape predators and be competitively dominant due to faster growth rates, and that such differences should be greater on low quality (as compared to high quality) host plants. To provide a preliminary test of these predictions, we conducted an empirical study comparing the effects of plant (Baccharis salicifolia) quality and predators between a specialist (Uroleucon macolai) and a generalist (Aphis gossypii) aphid herbivore. Consistent with predictions, these three factors interactively determine herbivore performance in ways not addressed by existing hypotheses. Compared to the specialist, the generalist was less fecund, competitively inferior, and more sensitive to low plant quality. Correspondingly, predator effects were contingent upon plant quality only for the generalist. Contrary to predictions, predator effects were weaker for the generalist and on low-quality plants, likely due to density-dependent benefits provided to the generalist by mutualist ants. Because the TTI hypothesis predicts the superior performance of specialists, mutualist ants may be critical to A. gossypii persistence under competition from U. macolai. In summary, the integrative nature of the TTI hypothesis offers novel insight into the determinants of plant-herbivore and herbivore-predator interactions and the coexistence of specialist and generalist herbivores

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

Attract and deter: a dual role for pyrrolizidine alkaloids in plant–insect interactions

Pyrrolizidine alkaloids (PAs) are the major defense compounds of plants in the Senecio genus. Here I will review the effects of PAs in Senecio on the preference and performance of specialist and generalist insect herbivores. Specialist herbivores have evolved adaptation to PAs in their host plant. They can use the alkaloids as cue to find their host plant and often they sequester PAs for their own defense against predators. Generalists, on the other hand, can be deterred by PAs. PAs can also affect survival of generalist herbivores. Usually generalist insects avoid feeding on young Senecio leaves, which contain a high concentration of alkaloids. Structurally related PAs can differ in their effects on insect herbivores, some are more toxic than others. The differences in effects of PAs on specialist and generalists could lead to opposing selection on PAs, which may maintain the genetic diversity in PA concentration and composition in Senecio species

Independent Recruitment of a Flavin-Dependent Monooxygenase for Safe Accumulation of Sequestered Pyrrolizidine Alkaloids in Grasshoppers and Moths

Several insect lineages have developed diverse strategies to sequester toxic pyrrolizidine alkaloids from food-plants for their own defense. Here, we show that in two highly divergent insect taxa, the hemimetabolous grasshoppers and the holometabolous butterflies, an almost identical strategy evolved independently for safe accumulation of pyrrolizidine alkaloids. This strategy involves a pyrrolizidine alkaloid N-oxygenase that transfers the pyrrolizidine alkaloids to their respective N-oxide, enabling the insects to avoid high concentrations of toxic pyrrolizidine alkaloids in the hemolymph. We have identified a pyrrolizidine alkaloid N-oxygenase, which is a flavin-dependent monooxygenase, of the grasshopper Zonocerus variegatus. After heterologous expression in E. coli, this enzyme shows high specificity for pyrrolizidine alkaloids of various structural types and for the tropane alkaloid atropine as substrates, a property that has been described previously for a pyrrolizidine alkaloid N-oxygenase of the arctiid moth Grammia geneura. Phylogenetic analyses of insect flavin-dependent monooxygenase sequences suggest that independent gene duplication events preceded the establishment of this specific enzyme in the lineages of the grasshoppers and of arctiid moths. Two further flavin-dependent monooxygenase sequences have been identified from Z. variegatus sharing amino acid identities of approximately 78% to the pyrrolizidine alkaloid N-oxygenase. After heterologous expression, both enzymes are also able to catalyze the N-oxygenation of pyrrolizidine alkaloids, albeit with a 400-fold lower specific activity. With respect to the high sequence identity between the three Z. variegatus sequences this ability to N-oxygenize pyrrolizidine alkaloids is interpreted as a relict of a former bifunctional ancestor gene of which one of the gene copies optimized this activity for the specific adaptation to pyrrolizidine alkaloid containing food plants

A Specific Male Olfactory Sensillum Detects Behaviorally Antagonistic Hairpencil Odorants

Within insect species, olfactory signals play a vital role in communication, particularly in the context of mating. During courtship, males of many moth species release pheromones that function as aphrodisiacs for conspecific females, or repellants to competing conspecific males. The physiology and antennal lobe projections are described of olfactory receptor neurons within an antennal sensillum present on male Heliothis virescens F. (Lepidoptera: Noctuidae) moths sensitive to conspecific male H. virescens-produced pheromone components. Olfactory receptor neurons responded to hexadecanyl acetate and octadecanyl acetate hairpencil components, and Z11-hexadecenyl acetate, an odorant used by closely related heliothine species in their female produced pheromone, which is antagonistic to male H. virescens responses. This acetate-sensitive sensillum appears homologous to a sensillum type previously described in females of this species, sharing similar physiology and glomerular projection targets within the antennal lobe. Wind tunnel observations indicate that H. virescens hairpencil odors (hexadecanyl acetate, octadecanyl acetate) function to antagonize responses of conspecific males following a female sex pheromone plume. Thus, male-male flight antagonism in H. virescens appears to be mediated by this particular sensillum type

Self-Medication as Adaptive Plasticity: Increased Ingestion of Plant Toxins by Parasitized Caterpillars

Self-medication is a specific therapeutic behavioral change in response to disease or parasitism. The empirical literature on self-medication has so far focused entirely on identifying cases of self-medication in which particular behaviors are linked to therapeutic outcomes. In this study, we frame self-medication in the broader realm of adaptive plasticity, which provides several testable predictions for verifying self-medication and advancing its conceptual significance. First, self-medication behavior should improve the fitness of animals infected by parasites or pathogens. Second, self-medication behavior in the absence of infection should decrease fitness. Third, infection should induce self-medication behavior. The few rigorous studies of self-medication in non-human animals have not used this theoretical framework and thus have not tested fitness costs of self-medication in the absence of disease or parasitism. Here we use manipulative experiments to test these predictions with the foraging behavior of woolly bear caterpillars (Grammia incorrupta; Lepidoptera: Arctiidae) in response to their lethal endoparasites (tachinid flies). Our experiments show that the ingestion of plant toxins called pyrrolizidine alkaloids improves the survival of parasitized caterpillars by conferring resistance against tachinid flies. Consistent with theoretical prediction, excessive ingestion of these toxins reduces the survival of unparasitized caterpillars. Parasitized caterpillars are more likely than unparasitized caterpillars to specifically ingest large amounts of pyrrolizidine alkaloids. This case challenges the conventional view that self-medication behavior is restricted to animals with advanced cognitive abilities, such as primates, and empowers the science of self-medication by placing it in the domain of adaptive plasticity theory

Functional identity versus species richness: herbivory resistance in plant communities

The resistance of a plant community against herbivore attack may depend on plant species richness, with monocultures often much more severely affected than mixtures of plant species. Here, we used a plant–herbivore system to study the effects of selective herbivory on consumption resistance and recovery after herbivory in 81 experimental grassland plots. Communities were established from seed in 2002 and contained 1, 2, 4, 8, 16 or 60 plant species of 1, 2, 3 or 4 functional groups. In 2004, pairs of enclosure cages (1 m tall, 0.5 m diameter) were set up on all 81 plots. One randomly selected cage of each pair was stocked with 10 male and 10 female nymphs of the meadow grasshopper, Chorthippus parallelus. The grasshoppers fed for 2 months, and the vegetation was monitored over 1 year. Consumption resistance and recovery of vegetation were calculated as proportional changes in vegetation biomass. Overall, grasshopper herbivory averaged 6.8%. Herbivory resistance and recovery were influenced by plant functional group identity, but independent of plant species richness and number of functional groups. However, herbivory induced shifts in vegetation composition that depended on plant species richness. Grasshopper herbivory led to increases in herb cover at the expense of grasses. Herb cover increased more strongly in species-rich mixtures. We conclude that selective herbivory changes the functional composition of plant communities and that compositional changes due to selective herbivory depend on plant species richness