Anti-aphrodisiac Compounds of Male Butterflies Increase the Risk of Egg Parasitoid Attack by Inducing Plant Synomone Production

During mating in many butterfly species, males transfer spermatophores that contain anti-aphrodisiacs to females that repel conspecific males. For example, males of the large cabbage white, Pieris brassicae (Lepidoptera: Pieridae), transfer the anti-aphrodisiac, benzyl cyanide (BC) to females. Accessory reproductive gland (ARG) secretion of a mated female P. brassicae that is deposited with an egg clutch contains traces of BC, inducing Brussels sprouts plants (Brassica oleracea var. gemmifera) to arrest certain Trichogramma egg parasitoids. Here, we assessed whether deposition of one egg at a time by the closely related small cabbage white, Pieris rapae, induced B. oleracea var. gemmifera to arrest Trichogramma wasps, and whether this plant synomone is triggered by substances originating from male P. rapae seminal fluid. We showed that plants induced by singly laid eggs of P. rapae arrest T. brassicae wasps three days after butterfly egg deposition. Elicitor activity was present in ARG secretion of mated female butterflies, whereas the secretion of virgin females was inactive. Pieris rapae used a mixture of methyl salicylate (MeSA) and indole as an anti-aphrodisiac. We detected traces of both anti-aphrodisiacal compounds in the ARG secretion of mated female P. rapae, whereas indole was lacking in the secretion of virgin female P. rapae. When applied onto the leaf, indole induced changes in the foliar chemistry that arrested T. brassicae wasps. This study shows that compounds of male seminal fluid incur possible fitness costs for Pieris butterflies by indirectly promoting egg parasitoid attack

Plant responses to butterfly oviposition partly explain preference–performance relationships on different brassicaceous species

The preference–performance hypothesis (PPH) states that herbivorous female insects prefer to oviposit on those host plants that are best for their offspring. Yet, past attempts to show the adaptiveness of host selection decisions by herbivores often failed. Here, we tested the PPH by including often neglected oviposition-induced plant responses, and how they may affect both egg survival and larval weight. We used seven Brassicaceae species of which most are common hosts of two cabbage white butterfly species, the solitary Pieris rapae and gregarious P. brassicae. Brassicaceous species can respond to Pieris eggs with leaf necrosis, which can lower egg survival. Moreover, plant-mediated responses to eggs can affect larval performance. We show a positive correlation between P. brassicae preference and performance only when including the egg phase: 7-day-old caterpillars gained higher weight on those plant species which had received most eggs. Pieris eggs frequently induced necrosis in the tested plant species. Survival of clustered P. brassicae eggs was unaffected by the necrosis in most tested species and no relationship between P. brassicae egg survival and oviposition preference was found. Pieris rapae preferred to oviposit on plant species most frequently expressing necrosis although egg survival was lower on those plants. In contrast to the lower egg survival on plants expressing necrosis, larval biomass on these plants was higher than on plants without a necrosis. We conclude that egg survival is not a crucial factor for oviposition choices but rather egg-mediated responses affecting larval performance explained the preference–performance relationship of the two butterfly species.</p

Plant volatiles induced by herbivore eggs prime defences and mediate shifts in the reproductive strategy of receiving plants

Plants can detect cues associated with the risk of future herbivory and modify defence phenotypes accordingly; however, our current understanding is limited both with respect to the range of early warning cues to which plants respond and the nature of the responses. Here we report that exposure to volatile emissions from plant tissues infested with herbivore eggs promotes stronger defence responses to subsequent herbivory in two Brassica species. Furthermore, exposure to these volatile cues elicited an apparent shift from growth to reproduction in Brassica nigra, with exposed plants exhibiting increased flower and seed production, but reduced leaf production, relative to unexposed controls. Our results thus document plant defence priming in response to a novel environmental cue, oviposition-induced plant volatiles, while also showing that plant responses to early warning cues can include changes in both defence and life-history traits.</p

Getting prepared for future attack : induction of plant defences by herbivore egg deposition and consequences for the insect community

Plants have evolved intriguing defences against insect herbivores. Compared to constitutive Plants have evolved intriguing defences against insect herbivores. Compared to constitutive defences that are always present, plants can respond with inducible defences when they are attacked. Insect herbivores can induce phenotypic changes in plants and consequently these changes may differentially affect subsequent attackers and their associated insect communities. Many studies consider herbivore-feeding damage as the first interaction between plants and insects. The originality of this study was to start with the first phase of herbivore attack, egg deposition, to understand the consequences of plant responses to eggs on subsequently feeding caterpillars and their natural enemies. The main plant species used for most of the experiments was Brassica nigra (black mustard), which occurs naturally in The Netherlands. The main herbivore used was the lepidopteran Pieris brassicae, which lays eggs in clusters and feeds on plants belonging to the Brassicaceae family. This study investigated plant-mediated responses to oviposition and their effects on different developmental stages of the herbivore, such as larvae and pupae. Furthermore, the effects of oviposition were extended to four more plant species of the same family, and to higher trophic levels including parasitoids and hyperparasitoids. The experiments were conducted under laboratory, semi-field and field conditions. This study shows that B. nigra plants recognize the eggs of P. brassicae and initiate resistance against subsequent developmental stages of the herbivore. Interestingly, plant responses to oviposition were found to be species specific. Plants did not respond to egg deposition by another herbivore species, the generalist moth Mamestra brassicae. Moreover, most of the Brassicaceae species tested were found to respond to P. brassicae eggs, which indicates that plant responses against oviposition are more common among the family of Brassicaceae. To assess effects on other members of the food chain, the effects of oviposition on plant volatile emission and the attraction of parasitic wasps, such as the larval parasitoid Cotesia glomerata, were tested. It was shown that the wasps were able to use the blend of plant volatiles, altered by their hosts’ oviposition, to locate young caterpillars just after hatching from eggs. The observed behaviour of the wasps was associated with higher parasitism success and higher fitness in young hosts. Similar results were obtained in a field experiment, where plants infested with eggs and caterpillars attracted more larval parasitoids and hyperparasitoids and eventually produced more seeds compared to plants infested with caterpillars only. This study shows that an annual weed like B. nigra uses egg deposition as reliable information for upcoming herbivory and responds accordingly with induced defences. Egg deposition could influence plant-associated community members at different levels in the food chain and benefit seed production. As the importance of oviposition on plant-herbivore interactions is only recently discovered, more research is needed to elucidate the mechanisms that underlie such plant responses and how these interactions affect the structure of insect communities in nature

Intrinsic compeition between two secondary hyperparasitoids results in temporal trophic switch

Interspecific competition amongst parasitoids is important in shaping the evolution of life-history strategies in these insects as well as community structure. Competition for hosts may occur between adult female parasitoids (‘extrinsic’ competition) or their progeny (‘intrinsic’ competition). Here, we examined intrinsic competition between two solitary secondary hyperparasitoids, Lysibia nana and Gelis agilis in cocoons of a primary parasitoid, Cotesia glomerata. Each species was allowed to sting hosts previously parasitized by the other at 24 h time intervals over the course of 144 h (6 days). When hosts were attacked simultaneously, neither species was dominant although the species to attack first won most encounters when it had a 24–48 h head start. However, after this time there was dramatic shift in the outcome with G. agilis dominating in all hosts > 72-h old, regardless of which species had parasitized C. glomerata first. G. agilis larvae, which initially had competed with L. nana for control of C. glomerata resources, began attacking the larvae of L. nana, whereas L. nana rejected hosts with older G. agilis larvae or pupae. Effects of multiparasitism also affected the development time and adult mass of the winning parasitoid. Our results reveal a shift in the trophic status of G. agilis from C. glomerata (in younger hosts) to L. nana (in older hosts), the first time such a phenomenon has been reported in parasitoids.