Species- and density-dependent induction of volatile organic compounds by three mite species in cassava and their role in the attraction of a natural enemy

Abstract

Upon damage by herbivores, plants induce an array of volatile organic compounds (VOCs) that mediate ecological interactions involving communication with organisms of the second and third trophic levels. VOC-mediated tritrophic interactions have largely been studied in various systems, including cassava (Manihot esculenta), but little is known about the chemical nature of herbivore-induced VOCs in this crop and the response they evoke in natural enemies. Several tetranychid and predatory mites are associated with cassava. Here, VOC emissions from uninfested plants and plants infested with 200 or 400 Mononychellus tanajoa, a specialist herbivore on cassava, and the generalists Tetranychus urticae and T. gloveri were measured. Dual-choice experiments were also conducted to assess the preference of inexperienced (reared on prey-infested bean plants) and experienced (adapted on prey-infested cassava plants) predatory mites, Neoseiulus idaeus (Phytoseiidae), between odors of uninfested plants versus odors of plants infested with M. tanajoa, T. urticae or T. gloveri. Two hundred individuals significantly increased the emissions of (Z)-3-hexen-1-ol, (E)-β-ocimene, β-caryophyllene, alloaromadendrene and (E)-geranyl acetone in T. urticae-infested plants, and (E)-β-ocimene and methyl salicylate (MeSA) in T. gloveri-infested plants. Four hundred individuals significantly increased the emissions of (Z)-3-hexen-1-ol, MeSA, α-pinene and D-limonene in M. tanajoa-infested plants. In addition, T. urticae at this density induced (E)-β-ocimene, D-limonene, (E)-geranyl acetone and six compounds that were not detected in other treatments. Tetranychus gloveri-infested plants induced the emissions of (E)-2-hexenal and D-limonene. Regardless of the infesting species, inexperienced N. idaeus did not discriminate between uninfested or infested plants. Upon experience, they discriminated between the odors of uninfested and T. urticae-damaged plants. Our findings reveal that mite infestations in cassava result in density-dependent and species-specific emission of VOCs, and that N. idaeus relies on associative learning to forage for its prey.

Specificity of Herbivore Defense Responses in a Woody Plant, Black Poplar (Populus nigra)

“…Similar emission profiles of black poplar have been shown previously (Clavijo McCormick et al 2014a , 2014b ; Unsicker et al 2015 ), even though a different volatile collection method was used here. In herbaceous plants, the emission of specific volatile patterns by different herbivore species is known (Cai et al 2014 ; Danner et al 2018 ; Hare and Sun 2011 ; Pinto-Zevallos et al 2018 ; Turlings et al 1998 ) and the pattern of stronger volatile induction after beetle herbivory was also observed (Hare and Sun 2011 ). At least one other woody plant also showed stronger induction of terpene emission after attack by coleopteran compared to lepidopteran herbivores (Moreira et al 2013 ).…”

A novel study approach on Scutellaria altissima L. cultivated at the Ghirardi Botanic Garden (Lombardy, Italy)

“…Indeed, previous studies underlined that ( Z )‐3‐hexenol acetate ( 7 , 44.14%) is responsible for the antifeedant action towards insects of the genus Lygus, parasites of cotton and other crops in North America (Williams et al, 2008) and aphids (Hedge et al, 2011), as well as for tritrophic interactions – plants–herbivores–parasites (Stevens et al, 2017). ( E )‐Geranyl acetone ( 34 ) and ( Z )‐3‐hexenyl isovalerate ( 24 ) contribute to the protective role (Heil et al, 2008; Morawo et al, 2016; Pinto‐Zevallos et al, 2018). 1,8‐Cineole ( 10 ) showed acaricidal (Hu et al, 2015), fumigant and larvicidal effects (Lucia et al, 2012), reinforced by the deterrent action of linalool ( 14 ) (Lobo et al, 2019; Stevenson, 2019), for which also an attractive power is already recognized (Stevenson, 2019).…”

Amazonian biogenic volatile organic compounds under global change

“…BVOC sources create volatile blends that can serve to identify the species of a recipient (Piva et al., 2019), allowing us to understand the nature of such communication (e.g. the identity and density of an attacking herbivore; Pinto‐Zevallos, Bezerra, Souza, & Ambrogi, 2018), and can also direct the evolution of plant chemical diversity (Salazar et al., 2018).…”

“…BVOC sources create volatile blends that can serve to identify the species of a recipient(Piva et al, 2019), allowing us to understand the nature of such communication (e.g. the identity and density of an attacking herbivore;Pinto-Zevallos, Bezerra, Souza, & Ambrogi, 2018), and can also direct the evolution of plant chemical diversity(Salazar et al, 2018).Signalling within plants can be based on cascading signals of jasmonates, salicylates and ethylene, but also other types of BVOCs such as GLV, methanol or isoprenoids(Filella, Peñuelas, & Llusià, 2006;Matsui, 2016;Matsui, Sugimoto, Mano, Ozawa, & Takabayashi, 2012;Seco, Filella, Llusià, & Peñuelas, 2011). The function of their emission can be involved in: inducing the production of BVOCs that can downregulate floral volatiles to produce BVOCs associated with fruit ripening, inducing BVOC production for defensive purposes, or for individual plant coexistence(Kigathi, Weisser, Reichelt, Gershenzon, & Unsicker, 2019;Ninkovic, Rensing, Dahlin, & Markovic, 2019).…”