Chemical Ecology of Floral Resources in Conservation Biological Control

Conservation biological control aims to enhance populations of natural enemies of insect pests in crop habitats, typically by intentional provision of flowering plants as food resources. Ideally, these flowering plants should be inherently attractive to natural enemies to ensure that they are frequently visited. We review the chemical ecology of floral resources in a conservation biological control context, with a focus on insect parasitoids. We highlight the role of floral volatiles as semiochemicals that attract parasitoids to the food resources. The discovery that nectar-inhabiting microbes can be hidden players in mediating parasitoid responses to flowering plants has highlighted the complexity of the interactions between plants and parasitoids. Furthermore, because food webs in agroecosystems do not generally stop at the third trophic level, we also consider responses of hyperparasitoids to floral resources. We thus provide an overview of floral compounds as semiochemicals from a multitrophic perspective, and we focus on the remaining questions that need to be addressed to move the field forward

Effect of host kairomones and oviposition experience on the arrestment behavior of an egg parasitoid

Chemical residues left by walking adults of the southern green stink bug, Nezara viridula (L.) (Heteroptera: Pentatomidae) induce arrestment behavior in the egg parasitoid Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) leading to prolonged periods of walking on contaminated areas and to systematic return to the stimulus after encountering the treatment borders. In this study, we quantified how the hierarchical value of residues from host adults and oviposition experience can influence the arrestment behavior of T. basalis females. Our results showed that: (1) female wasps perceived host residues at different hierarchical levels depending on the host gender, with a clear preference for the chemical residues deposited by host females rather then host males; (2) wasps' arrestment response to chemical residues of host females became weaker when wasps were not rewarded by an oviposition experience, and stronger following successful oviposition; (3) repeated encounters with host male chemical residues, followed or not by oviposition experience, did not cause wasps to change their innate arrestment response; (4) in the unrewarded condition, arrestment responses of wasps varied according to the time elapsed between successive visits to areas contaminated by host females: responses were weak with a short interval (less than 24 h) and stronger with a long interval (more than 72 h), suggesting that this unrewarded experience, i.e. encounter with female traces not followed by host egg location, fade within a few hours. The potential significance of these results to the host location behavior of T. basalis in the field is discussed

Contrasting reproductive traits of competing parasitoids facilitate coexistence on a shared host pest in a biological control perspective

BACKGROUND: Interspecific competition in insect parasitoids is an important ecological phenomenon that has relevant implications for biological pest control. To date, interspecific intrinsic (=larval) competition has been intensively studied, while investigations on extrinsic (=adult) competition have often lagged behind. In this study we examined the role played by parasitoid reproductive traits and host clutch size on the outcome of extrinsic competition between Trissolcus basalis (Wollaston) and Ooencyrtus telenomicida (Vassiliev), two egg parasitoids of the pest Nezara viridula (L). Laboratory experiments were conducted by allowing both parasitoid species to exploit an egg mass made of 10, 20, 30, or 40 hosts through single or simultaneous releases. Furthermore, under field conditions, egg masses consisting of 10 or 40 hosts were exposed in a tomato crop in order to validate laboratory investigation. RESULTS: The results show that the egg mass size is an important predictor of extrinsic competition in our study system as a higher proportion of T. basalis emerged from large egg masses, while O. telenomicida dominated in small egg masses. Analysis of reproductive traits of parasitoid species indicates that T. basalis has superior abilities in host exploitation compared with O. telenomicida. CONCLUSIONS: We found that contrasting reproductive traits of two competing egg parasitoid species facilitate coexistence on a shared stink bug host. This work also highlights the importance to consider extrinsic competitive interactions between parasitoid species in a biological control perspective. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry

Intraguild interactions between two egg parasitoids of a true bug in semi-field and field conditions

Research on interspecific competitive interactions among insect parasitoids has often been characterized by laboratory studies in which host insects are exposed to female parasitoids of different species in various sequences and combinations. In the last years, an increasing number of studies have investigated interspecific interactions under field and semi-field conditions although just a few number of works focused on egg parasitoids. In this work, we undertook a two-year study to investigate interspecific interactions between Trissolcus basalis (Wollaston) (Hymenoptera: Platygastridae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae), two egg parasitoids of the pest Nezara viridula (L.) (Heteroptera: Pentatomidae) that co-occur in cultivated crops. Under semi-field (in out-door mesh cages) and field conditions, we investigated: 1) the seasonal occurrence of competing parasitoid species on sentinel egg masses; 2) the impact achieved by competing species on the shared host on naturally laid egg masses; 3) the outcome of intraguild interactions under controlled conditions. Results from sentinel egg masses showed that T. basalis occurs in May and successfully parasitizes hosts until the end of September/beginning of October, whereas O. telenomicida is mainly occurring in July-August. In both years, it was found that T. basalis is predominant. From naturally laid egg masses, results indicated that T. basalis achieves higher impact on the hosts, even in those egg masses which are parasitized by more than one female of different species ( = multiparasitism). Results from manipulating intraguild interactions showed that T. basalis achieves higher impact on N. viridula when released alone, but it suffers from competition with O. telenomicida. The ecological factors that play a role in intraguild interactions in the context of biological control perspective are discussed

Trichoderma harzianum Strain T22 Modulates Direct Defense of Tomato Plants in Response to Nezara viridula Feeding Activity

Plant growth-promoting fungi belonging to genus Trichoderma are known to help plants when dealing with biotic stressors by enhancing plant defenses. While beneficial effects of Trichoderma spp. against plant pathogens have long been documented, fewer studies have investigated their effect on insect pests. Here, we studied the impact of Trichoderma root colonization on the plant defense responses against stink bug feeding attack. For this purpose, a model system consisting of tomato plant, Solanum lycopersicum cv Dwarf San Marzano, Trichoderma harzianum strain T22 and the southern green stink bug, Nezara viridula, was used. We firstly determined stink bug performance in terms of relative growth rate and survival on tomato plants inoculated by T. harzianum T22. Then, we evaluated relative expression of plant defense-related genes on inoculated plants induced by stink bug feeding. We found evidence that T. harzianum T22 affects tomato defense responses against N. viridula nymphs leading to reduction of growth rate. Our results also showed that T. harzianum T22 enhances plant direct defenses by an early increase of transcript levels of jasmonic acid marker genes. Yet this effect was time-dependent and only detected 8 h after herbivore induction. Taken together, our findings provide better understanding on the mechanisms underlying tomato induced resistance against herbivorous stink bugs

Only Females Oviposit: Chemical Discrimination of Adult Stink Bug Sex by the Egg Parasitoid Trissolcus japonicus

Egg parasitoids foraging for suitable hosts scattered in the environment rely mainly on chemical cues. Elucidating the chemical ecology of natural enemies is important in the development of effective and successful strategies for conservation biological control. In this context, the host cuticular hydrocarbons, which are exploited by several species of egg parasitoids as contact kairomones, could be used to retain them by providing information about the presence and the sex of adults of the target species: sex is important because only females of the host species lay the eggs that can be subsequently utilized for parasitoid reproduction. However, the chemical basis of host sex discrimination in egg parasitoids is not well understood. We carried out behavioral and chemical bioassays to investigate the role played by contact chemical cues left by adults of the brown marmorated stink bug, Halyomorpha halys Stål, in host egg searching behavior and adult host sex discrimination by the egg parasitoid Trissolcus japonicus (Ashmead). A first set of bioassays showed that parasitoids spent more time exploring patches contaminated with chemicals associated with adult H. halys females compared with adult males. Similar responses were displayed by T. japonicus when hexane extracts of H. halys were tested suggesting that non-polar chemical compounds are involved in host sex discrimination. GC-MS analysis of hexane extracts revealed quantitative differences in the cuticular compounds of the two sexes, with 1-hexadecene (more abundant in males) being the most important component in determining these differences. Hexane extracts of H. halys females blended with synthetic 1-hexadecene significantly reduced the wasps’ arrestment responses compared to crude extracts

Environmental Noise and Nonlinear Relaxation in Biological Systems

We analyse the effects of environmental noise in three different biological systems: (i) mating behaviour of individuals of \emph{Nezara viridula} (L.) (Heteroptera Pentatomidae); (ii) polymer translocation in crowded solution; (iii) an ecosystem described by a Verhulst model with a multiplicative L\'{e}vy noise.Comment: 32 pages; In "Ecological Modeling" by Ed. Wen-Jun Zhang. ISBN: 978-1-61324-567-5. - Nova Science Publishers, New York, 201

Nectar-Inhabiting Bacteria Affect Olfactory Responses of an Insect Parasitoid by Altering Nectar Odors

Floral nectar is ubiquitously colonized by a variety of microorganisms among which yeasts and bacteria are the most common. Microorganisms inhabiting floral nectar can alter several nectar traits, including nectar odor by producing microbial volatile organic compounds (mVOCs). Evidence showing that mVOCs can affect the foraging behavior of insect pollinators is increasing in the literature, whereas the role of mVOCs in altering the foraging behavior of third-trophic level organisms such as insect parasitoids is largely overlooked. Parasitoids are frequent visitors of flowers and are well known to feed on nectar. In this study, we isolated bacteria inhabiting floral nectar of buckwheat, Fagopyrum esculentum (Polygonales: Polygonaceae), to test the hypothesis that nectar bacteria affect the foraging behavior of the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae) via changes in odors of nectar. In behavioral assays, we found that T. basalis wasps are attracted toward nectar fermented by 4 out of the 14 bacterial strains isolated, which belong to Staphylococcus epidermidis, Terrabacillus saccharophilus (both Firmicutes), Pantoea sp. (Proteobacteria), and Curtobacterium sp. (Actinobacteria). Results of chemical investigations revealed significant differences in the volatile blend composition of nectars fermented by the bacterial isolates. Our results indicate that nectar-inhabiting bacteria play an important role in the interactions between flowering plants and foraging parasitoids. These results are also relevant from an applied perspective as flowering resources, such as buckwheat, are largely used in agriculture to promote conservation biological control of insect pests

Egg parasitoid attraction toward induced plant volatiles is disrupted by a non-host herbivore attacking above or belowground plant organs

Plants respond to insect oviposition by emission of oviposition-induced plant volatiles (OIPVs) which can recruit egg parasitoids of the attacking herbivore. To date, studies demonstrating egg parasitoid attraction to OIPVs have been carried out in tritrophic systems consisting of one species each of plant, herbivore host, and the associated egg parasitoid. Less attention has been given to plants experiencing multiple attacks by host and non-host herbivores that potentially could interfere with the recruitment of egg parasitoids as a result of modifications to the OIPV blend. Egg parasitoid attraction could also be influenced by the temporal dynamics of multiple infestations, when the same non-host herbivore damages different organs of the same plant species. In this scenario we investigated the responses of egg parasitoids to feeding and oviposition damage using a model system consisting of Vicia faba, the above-ground insect herbivore Nezara viridula, the above- and below-ground insect herbivore Sitona lineatus, and Trissolcus basalis, a natural enemy of N. viridula. We demonstrated that the non-host S. lineatus disrupts wasp attraction toward plant volatiles induced by the host N. viridula. Interestingly, V. faba damage inflicted by either adults (i.e., leaf-feeding) or larvae (i.e., root-feeding) of S. lineatus, had a similar disruptive effect on T. basalis host location, suggesting that a common interference mechanism might be involved. Neither na\uefve wasps or wasps with previous oviposition experience were attracted to plant volatiles induced by N. viridula when V. faba plants were concurrently infested with S. lineatus adults or larvae. Analysis of the volatile blends among healthy plants and above-ground treatments show significant differences in terms of whole volatile emissions. Our results demonstrate that induced plant responses caused by a non-host herbivore can disrupt the attraction of an egg parasitoid to a plant that is also infested with its hosts

Mediterranean ants can increase nymph mortality in the stink bug Nezara viridula without interfering with its egg parasitoid Trissolcus basalis

Ants (Hymenoptera: Formicidae) play a relevant ecological role across terrestrial ecosystems. Recent studies suggest that the presence of ants in crops could lead to a decrease in the populations of insect pests, but how these actions can vary along the different trophic levels is not well known. The southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae), is a cosmopolitan agricultural pest which is regularly found on horticultural agroecosystems closely associated with its main egg parasitoid, Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae). We conducted laboratory experiments to test whether two Mediterranean ant species, the generalist predators Crematogaster scutellaris (Olivier) and Tapinoma magnum Mayr, attack N. viridula eggs or nymphs, and whether they interfere with the parasitization activity of T. basalis. The experiment showed that both ant species significantly increased the mortality of N. viridula nymphs, whereas they do not attack their eggs and do not interfere with the egg parasitoids. Our results suggest that ants and egg parasitoids may have an integrable role in biocontrol strategies against this pest