The Ecology of Plant Chemistry and Multi-Species Interactions in Diversified Agroecosystems.

Over the past few years, our knowledge of how ecological interactions shape the structure and dynamics of natural communities has rapidly advanced. Plant chemical traits play key roles in these processes because they mediate a diverse range of direct and indirect interactions in a community-wide context. Many chemically mediated interactions have been extensively studied in industrial cropping systems, and thus have focused on simplified, pairwise and linear interactions that rarely incorporate a community perspective. A contrasting approach considers the agroecosystem as a functioning whole, in which food production occurs. It offers an opportunity to better understand how plant chemical traits mediate complex interactions which can enhance or hinder ecosystem functions. In this paper, we argue that studying chemically mediated interactions in agroecosystems is essential to comprehend how agroecosystem services emerge and how they can be guaranteed through ecosystem management. First, we discuss how plant chemical traits affect and are affected by ecological interactions. We then explore research questions and future directions on how studying chemical mediation in complex agroecosystems can help us understand the emergence and management of ecosystem services, specifically biological control and pollination.

Eliciting maize defense pathways aboveground attracts belowground biocontrol agents.

Plant defense pathways mediate multitrophic interactions above and belowground. Understanding the effects of these pathways on pests and natural enemies above and belowground holds great potential for designing effective control strategies. Here we investigate the effects of aboveground stimulation of plant defense pathways on the interactions between corn, the aboveground herbivore adult Diabrotica speciosa, the belowground herbivore larval D. speciosa, and the subterranean ento-mopathogenic nematode natural enemy Heterorhabditis amazonensis. We show that adult D. speciosa recruit to aboveground herbivory and methyl salicylate treatment, that larval D. speciosa are relatively indiscriminate, and that H. amazonensis en-tomopathogenic nematodes recruit to corn fed upon by adult D. speciosa. These results suggest that entomopathogenicnematodes belowground can be highly attuned to changes in the aboveground parts of plants and that biological control can be enhanced with induced plant defense in this and similar systems.

Current knowledge and future research perspectives on cassava (Manihot esculenta Crantz) chemical defenses: An agroecological view.

Cassava (Manihot esculenta Crantz) is one of the most important staple crops worldwide. It constitutes the major source of carbohydrates for millions of low-income people living in rural areas, as well as a cash crop for smallholders in tropical and sub-tropical regions. The Food and Agriculture Organization of the United Nations predicts that cassava plantations will increase and production systems will intensify in the future, highlighting the need for developing strategies that improve the sustainability of production. Plant chemical defenses hold the potential for developing pest management strategies, as these plant traits can influence the behavior and performance of both pests and beneficial arthropods. Cassava plants are well-defended and produce a number of compounds involved in direct defense, such as cyanogenic glycosides, flavonoid glycosides, and hydroxycoumarins. In addition, volatile organic compounds induced upon herbivory and the secretion of extrafloral nectar act as indirect defense against herbivores by recruiting natural enemies. Here, cassava chemical defenses against pest arthropods are reviewed, with the aim of identifying gaps in our knowledge and areas of research that deserve further investigation for developing sound pest control strategies to improve sustainable production of this crop, and how these defenses can be used to benefit other crops. Cyanogenic content in cassava is also highly toxic to humans, and can cause irreversible health problems even at sub-lethal doses when consumed over prolonged periods. Therefore, the promotion of chemical defense in this crop should not aggravate these problems, and must be accompanied with the education on processing methods that reduce human exposure to cyanide.

Stimulation of the Salicylic Acid Pathway Aboveground Recruits Entomopathogenic Nematodes Belowground.

Plant defense pathways play a critical role in mediating tritrophic interactions between plants, herbivores, and natural enemies. While the impact of plant defense pathway stimulation on natural enemies has been extensively explored aboveground, belowground ramifications of plant defense pathway stimulation are equally important in regulating subterranean pests and still require more attention. Here we investigate the effect of aboveground stimulation of the salicylic acid pathway through foliar application of the elicitor methyl salicylate on belowground recruitment of the entomopathogenic nematode, Steinernema diaprepesi. Also, we implicate a specific root-derived volatile that attracts S. diaprepesi belowground following aboveground plant stimulation by an elicitor. In four-choice olfactometer assays, citrus plants treated with foliar applications of methyl salicylate recruited S. diaprepesi in the absence of weevil feeding as compared with negative controls. Additionally, analysis of root volatile profiles of citrus plants receiving foliar application of methyl salicylate revealed production of d-limonene, which was absent in negative controls. The entomopathogenic nematode S. diaprepesi was recruited to d-limonene in two-choice olfactometer trials. These results reinforce the critical role of plant defense pathways in mediating tritrophic interactions, suggest a broad role for plant defense pathway signaling belowground, and hint at sophisticated plant responses to pest complexes.

Herbivory by a Phloem-feeding insect inhibits floral volatile production.

There is extensive knowledge on the effects of insect herbivory on volatile emission from vegetative tissue, but little is known about its impact on floral volatiles. We show that herbivory by phloem-feeding aphids inhibits floral volatile emission in white mustard Sinapis alba measured by gas chromatographic analysis of headspace volatiles. The effect of the Brassica specialist aphid Lipaphis erysimi was stronger than the generalist aphid Myzus persicae and feeding by chewing larvae of the moth Plutella xylostella caused no reduction in floral volatile emission. Field observations showed no effect of L. erysimi-mediated floral volatile emission on the total number of flower visits by pollinators. Olfactory bioassays suggested that although two aphid natural enemies could detect aphid inhibition of floral volatiles, their olfactory orientation to infested plants was not disrupted. This is the first demonstration that phloem-feeding herbivory can affect floral volatile emission, and that the outcome of interaction between herbivory and floral chemistry may differ depending on the herbivore's feeding mode and degree of specialisation. The findings provide new insights into interactions between insect herbivores and plant chemistry.

Response of the egg parasitoids Trissolcus basalis and Telenomus podisi to compounds from defensive secretions of stink bugs.

We tested the hypotheses that host-searching behavior of the egg parasitoids Telenomus podisi and Trissolcus basalis may be differentially influenced by the different blends of volatiles released from the metathoracic glands of adult stink bug host species. We further studied whether such a differential response is due to different individual components of these glands and whether these responses reflect host preferences. Y-tube olfactometer bioassays were carried out with crude extracts of metathoracic glands of five different host species of neotropical stink bugs. Additionally, we tested the parasitoids' responses to synthetic standards of individual compounds identified in these stink bug glands. Results showed that females of T. basalis and T. podisi responded differentially to crude gland extracts of the different species of host stink bugs and to the compounds tested. The parasitoid T. basalis showed a positive taxic behavior to Nezara viridula methathoracxic gland extracts of a host species preferred in the field, i.e., N. viridula. Furthermore, T. basalis responded positively to 4-oxo-(E)-2-hexenal and (E)-2-decenal, two components of N. viridula glandular secretion. Higher residence time, reduced linear velocity, and higher tortuosity in the arm of the olfactometer supplied with 4-oxo-(E)-2-hexenal showed that this compound modifies the kinetics of some traits of T. basalis walking pattern and suggests that it might stimulate the searching behavior of this parasitoid. The parasitoid T. podisi was attracted to crude gland extracts of the preferred host (Euschistus heros) and also to 4-oxo-(E)-2-hexenal. Additionally, this parasitoid responded positively to (E)-2-hexenal and to the hydrocarbon tridecane, both of which are defensive compounds released from the metathoracic glands by several stink bugs. The results indicate some degree of specialization in the response of two generalist parasitoid species toward defensive secretions of stink bugs.

The chemical volatiles (semiochemicals) produced by neotropical stink bugs (Hemiptera: Pentatomidae).

In recent years the growing concern about environmental changes and how we are using the natural resources have triggered a search for natural products as alternatives to synthetic pesticides. The stink bugs produce a wide variety of chemical compounds (semiochemicals) that show potential to manage these insects. The stink bugs Chinavia impicticornis (Stål), C. ubica (Rolston), Dichelops melacanthus (Dallas), Euschistus heros (F.), Piezodorus guildinii (Westwood), Thyanta perditor (Westwood) and Tibraca limbativentris (Stål) had their blends of defensive compounds evaluated both qualitative and quantitatively. The main compounds identified on the glands of Brazilian stink bugs are: 2-alkenals, mainly the E isomer; saturated aliphatic hydrocarbons; and 4 oxo-(E)-2-alkenals. The first sex attractant determined from a stink bug was obtained from Nezara viridula L., and consists on a mix of two isomers cis - and trans bisabolene-epoxides. Later the soybean stink bug E. heros was also studied and its sex attractant was identified as three esters methyl: 2,6,10-trimethyldecanoate, methyl 2,6,10-trimethyldodecanoate, and methyl E2, Z4-decadienoate. Recently, three new Brazilian sting bugs were studied and had their sex attractant elucidated. Males of T. perditor produce the ester, methyl 2E,4Z,6Z-decatrienoate. Whereas, the stink bug, P. guildinii has as sexual pheromone, the sesquiterpene beta-sesquiphellandrene, and the stink bug T. limbativentris produces as sex attractant the zingiberenol. In this review we discuss the advances obtained on the behaviour and identification of sex and defensive compound of stink bugs from Brazilian crops and the application of this knowledge to manage the stink bugs.

The chemical volatiles (Semiochemicals) produced by neotropical stink bugs (Hemiptera: Pentatomidae) / Os voláteis químicos (Semioquímicos) produzidos pelos percevejos neotropicais Hemiptera: Pentatomidae)

Nos últimos anos tem sido crescente a preocupação com as mudanças climáticas e com a utilização auto-sustentável dos recursos naturais, estimulando cada vez mais os estudos para a prospecção de novos produtos naturais visando minimizar o uso de pesticidas. Os percevejos produzem uma variedade de compostos químicos com potencial para o seu manejo. A composição química dos compostos defensivos dos percevejos Chinavia impicticornis (Stål), C. ubica (Rolston), Dichelops melacanthus (Dallas), Euschistus heros (F.), Piezodorus guildinii (Westwod), Thyanta perditor (Westwood) e Tibraca limbativentris (Stål) foi avaliada. Os principais compostos nas glândulas dos percevejos foram: 2-alcenais, principalmente o isômero E, hidrocarbonetos alifáticos saturados; e 4 oxo-(E)-2-alcenal. O primeiro feromônio sexual de percevejo identificado no Brasil foi do Nezara viridula L., que consiste na mistura dos isômeros cis e trans epóxi-bisabolenos; na sequência, o percevejo praga da soja E.. heros também teve seu feromônio sexual identificado. Os machos desta espécie produzem três ésteres: 2,6,10-trimetildecanoato de metila, 2,6,10 trimetildodecanoato de metila e 2E,4Z decadienoato de metila. Recentemente, mais três espécies de percevejos neotropicais tiveram a composição da mistura feromonal elucidada. Machos de T. perditor produzem o éster, 2E,4Z,6Z-decatrienoato de metila. O percevejo P. guildinii tem como feromônio sexual o β-sesquifelandreno, e o percevejo praga do arroz T. limbativentris tem também como feromônio sexual um sesquiterpenóide, o zingiberenol. Nessa revisão serão abordados os avanços obtidos no estudo do comportamento e identificação de feromônios sexuais e de alarme de várias espécies do complexo de percevejos praga da agricultura brasileira. A aplicação desses conhecimentos é discutida.

In recent years the growing concern about environmental changes and how we are using the natural resources have triggered a search for natural products as alternatives to synthetic pesticides. The stink bugs produce a wide variety of chemical compounds (semiochemicals) that show potential to manage these insects. The stink bugs Chinavia impicticornis (Stål), C. ubica (Rolston), Dichelops melacanthus (Dallas), Euschistus heros (F.), Piezodorus guildinii (Westwood), Thyanta perditor (Westwood) and Tibraca limbativentris (Stål) had their blends of defensive compounds evaluated both qualitative and quantitatively. The main compounds identified on the glands of Brazilian stink bugs are: 2-alkenals, mainly the E isomer; saturated aliphatic hydrocarbons; and 4 oxo-(E)-2-alkenals. The first sex attractant determined from a stink bug was obtained from Nezara viridula L., and consists on a mix of two isomers cis - and trans bisabolene-epoxides. Later the soybean stink bug E. heros was also studied and its sex attractant was identified as three esters methyl: 2,6,10-trimethyldecanoate, methyl 2,6,10-trimethyldodecanoate, and methyl E2, Z4-decadienoate. Recently, three new Brazilian sting bugs were studied and had their sex attractant elucidated. Males of T. perditor produce the ester, methyl 2E,4Z,6Z-decatrienoate. Whereas, the stink bug, P. guildinii has as sexual pheromone, the sesquiterpene β-sesquiphellandrene, and the stink bug T. limbativentris produces as sex attractant the zingiberenol. In this review we discuss the advances obtained on the behaviour and identification of sex and defensive compound of stink bugs from Brazilian crops and the application of this knowledge to manage the stink bugs.

Inter- and intraspecific variation in defensive compounds produced by five neotropical stink bug species (Hemiptera: Pentatomidae).

The differences in composition of defensive secretions between nymphs, adult males and adult females of Chinavia impicticornis (=Acrosternum impicticorne), Chinavia ubica (=Acrosternum ubicum), Euschistus heros, Dichelops melacanthus and Piezodorus guildinii (Hemiptera, Pentatomidae) were analysed within and between species using compositional log-ratio statistics and canonical variates analysis. Differences in composition between nymphs, males and females were found for all species, as well as when all species were pooled. In particular, tetradecanal appears to be a predominantly nymphal compound in D. melacanthus, E. heros and P. guildinii. In the two Chinavia species 4-oxo-(E)-2-hexenal and an unknown compound were more dominant in nymphs. The interspecific analysis revealed a good separation of defensive compounds according to their taxonomic relationship. Thus, the two Chinavia species grouped together, with (E)-2-decenal and (E)-2-hexenyl acetate, contributing to this separation. The other three species also differed from each other, with (E)-2-octenal associated to D. melacanthus, (E)-2-hexenal to P. guildinii and (E,E)-2,4-decadienal and tetradecanal to E. heros. The pooled analysis of stage ignoring species revealed tetradecanal and 4-oxo-(E)-2-decenal (tentative identification) strongly associated to nymphs. Thus, there are predictable differences between stages, and many of the differences are conserved between species. Consideration of these differences could prove to be important in understanding stink bug-natural enemy interactions, and in optimising biocontrol efforts.

Response of the aphid parasitoid Aphidius funebris to volatiles from undamaged and aphid-infested Centaurea nigra.

Two issues have hindered the understanding of the ecology and evolution of volatile-mediated tritrophic interactions: few studies have addressed noncrop systems; and few statistical techniques have been applied that are suitable for the analysis of complex volatile blends. In this paper, we addressed both of these issues by studying the noncrop system involving the plant Centaurea nigra, the specialist aphid Uroleucon jaceae, and the parasitoid Aphidius funebris. In a Y-tube olfactometer, A. funebris was attracted to the odor from undamaged C. nigra, but preferred the plant-host complex (PHC) after 3 d of feeding by 200 U. jaceae over the undamaged plant, but not after three or 5 d of feeding by 50 U. jaceae. When aphids were removed, the initial preference for the damaged plant remained, but the final preference was not greater than for the undamaged plant. No qualitative differences were detected between the headspaces of C. nigra and the C. nigra-U. jaceae PHC. For quantitative analysis, we used a compositional approach, which treats each compound produced as part of a blend, and not as a compound released in isolation, thus allowing analysis of the relative contribution of each compound to the blend as a whole. With this approach, subtle increases and decreases of some green leaf volatiles and monoterpenoids on the third day of aphid infestation were detected. Mechanically damaged C. nigra had a volatile profile that differed from undamaged C. nigra and the PHC. One and 10 ng of (Z)-3-hexenyl acetate, and 10 or 100 ng of 6-methyl-5-hepten-2-one were attractive to the parasitoid when placed in solution on filter paper. A. funebris appears to be using a combination of chemical cues to locate host-infested plants.