Biochemical crypsis in the avoidance of natural enemies by an insect herbivore

Abstract

Plant-herbivore interactions provide well studied examples of coevolution, but little is known about how such interactions are influenced by the third trophic level. Here we show that larvae of the specialized lepidopteran herbivore Heliothis subflexa reduce their vulnerability to natural enemies through adaptation to a remarkable and previously unknown feature of their host plant, Physalis angulata: The fruits of this plant lack linolenic acid (LA), which is required for the development of most insects. By overcoming this nutritional deficiency, H. subflexa larvae achieve numerous advantages. First, they gain near-exclusive access to a food resource: we demonstrate that closely related Heliothis virescens larvae cannot develop on P. angulata fruit unless the fruit are treated with LA. Second, they reduce their vulnerability to enemies: LA is a key component of volicitin, an elicitor of plant-volatilesignaling defenses. We demonstrate that volicitin is absent in the oral secretions of fruit-feeding caterpillars, that the volatile profiles of plants induced by fruit feeding differ from those induced by leaf feeding or by feeding on LA-treated fruit, and that the former are far less attractive to female Cardiochiles nigriceps parasitoids. Finally, they render themselves nutritionally unsuitable as hosts for enemies that require LA for their own development: we show that C. nigriceps larvae fail to develop within the bodies of fruit-feeding caterpillars but do develop in caterpillars feeding on LA-treated fruit. Thus, H. subflexa larvae not only overcome a serious dietary deficiency but also reduce their vulnerability to natural enemies through a form of ''biochemical crypsis.'' T he vulnerability of insect herbivores to attack by predators and parasitoids is often mediated by interactions with the host plant on which the herbivore feeds (1-3). Specialist herbivores that have overcome certain plant defenses may subsequently co-opt those defenses, for example, by sequestering chemical toxins produced by the plant within their bodies as a defense against their own enemies (2, 4-6). Plants, in turn, often respond to herbivory by releasing volatile chemical compounds that are attractive to predators and parasitoids that are natural enemies of the herbivores (7,8). Thus, the particular physical and physiological characteristics of the host plant are thought to be major features influencing the vulnerability of insect herbivores to attack by predators and parasitoids, and adaptation to those specific characteristics may be expected to play an important role in avoiding attack by natural enemies (9-11). Lill et al. (3) demonstrated a strong effect of host-plant identity on parasitism rates and suggested that these differences might be influenced by features of the host plant including plant-volatile-related differences in parasitoid attraction and retention but did not address the specific mechanisms that might underlie such differences.In this article we describe behavioral and physiological adaptations of the speciali...

Mouse alarm pheromone shares structural similarity with predator scents

“…Another form of antipredator adaptation also involves olfactory emissions (chemical crypsis) (3). We might here speculate that, in the presence of a predator, the production of alarm pheromones, such as SBT (63), not only signals danger to conspecifics but also induces freezing and might also modify the prey scent, which could fool the predator by mimicry of its own scent (2,3).…”

“…Multiple hiding strategies (crypsis) coexist and are best when combined. Indeed, crypsis can be morphological when the prey uses its body shape/color to blend into the background (camouflage), it can be behavioral when the prey uses immobility or subtle steady movements to decrease the chance of being detected (freezing); or it can be chemical when the prey releases odorant molecules to mask its own odor (2,3).…”

Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae

“…Numerous studies have shown that this ingenious plant defense system is triggered by substances in the regurgitants of the herbivores. The best known of these plant volatile elicitors are the fatty acid amino acid conjugates (FACs) that first were identified from beet armyworm, Spodoptera exigua, larvae (3) but later also found in several other lepidopteran species (4)(5)(6)(7)(8) and other insects (9,10). Of the FACs, volicitin [N-(17-hydroxylinolenoyl)-L-glutamine], is the most active elicitor for seedlings of most cultivars of Zea mays (3,11,12).…”

“…The ammonia assimilation into FACs was studied by liquid chromatography-mass spectrometry (LCMS) analysis of regurgitant obtained from S. litura larvae treated with artificial diets enriched with [ 15 N]NH 4 Cl and glutamic acid. The labeling ratios for FACs calculated from area values of extracted ion chromato- 18.1 Ϯ 0.3% for volicitin, and 16.7 Ϯ 0.4% for N-(17-hydroxylinoleoyl)-L-glutamine.…”

Biological insight into design against crime

“…Many investigations have been realised in order to understand the strength of interactions among species within natural communities [28]. Other organisms, such as herbivores reduce their vulnerability to natural enemies through adaptation to host plants [29].…”