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1 June 2017 Behavioral Responses of Aphis citricola (Hemiptera: Aphididae) and Its Natural Enemy Harmonia axyridis (Coleoptera: Coccinellidae) to Non-Host Plant Volatiles
Beizhou Song, Yinping Liang, Sizhou Liu, Linfeng Zhang, Guangbo Tang, Teng Ma, Yuncong Yao
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Abstract

Plant volatiles can act as chemical signals that influence the behavior and distribution of insects. Although considerable information has been acquired on the effects of plant volatiles emitted from plants on herbivorous insects and their natural enemies, practical implementation of this knowledge is still lacking. We investigated 3 aromatic plant species, French marigold, Tagetes patula L. (Asteraceae), ageratum, Ageratum houstonianum Mill. (Asteraceae), and catnip, Nepeta cataria L. (Lamiaceae), to test their effectiveness in repelling or attracting spirea aphid, Aphis citricola van der Goot (Hemiptera: Aphididae), and its natural enemy, the multicolored Asian lady beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in the field and the laboratory. We found that intercropping apple trees Malus spp. (Rosaceae) with aromatic plants in an orchard significantly reduced the number of A. citricola aphids present, but had the opposite effect on H. axyridis. In addition, the association between H. axyridis and A. citricola numbers was strengthened when the intercropping included French marigold. Using an H-tube olfactometer, we found that A. citricola was repelled by French marigold and catnip, whereas H. axyridis was attracted most by French marigold. Volatile analysis revealed that the sesquiterpenes Dlimonene and terpinolene and the alcohol 2-ethyl-1-hexanol were the most abundant volatile compounds released by French marigold and catnip. Harmonia axyridis was significantly attracted by 12.5 µL/L D-limonene, 50 µL/L terpinolene, and 25 µL/L of a 1:1 mixture of the 2 compounds, but was repelled by higher concentrations of D-limonene. The results suggest that aromatic plants increase the resistance of apple trees to A. citricola both directly, by reducing the population of A. citricola through chemical repulsion, and indirectly, by increasing the H. axyridis population through chemical attraction.

Plant volatiles can function as important sources of information that mediate many interactions within a plant—arthropod community and can influence the behavior and distribution of insects (Dicke 2015). When plants are attacked by herbivores, they release complex mixtures of volatile compounds called herbivore-induced plant volatiles, which can trigger enhanced plant defenses that directly or indirectly protect the plant against herbivores (Lucas-Barbosa et al. 2011). Two types of plant defenses can be distinguished, the first of which involves volatiles that affect the performance or behavior of herbivores and that may have a direct repellent effect on herbivores (Lucas-Barbosa et al. 2011). Examples include induced volatiles from tobacco, Nicotiana tabacum L. (Solanaceae), that are highly repellent to female moths of Heliothis virescens (F.) (Lepidoptera: Noctuidae) (Moraes et al. 2001) and induced volatiles from aromatic plants that are highly repellent to the beetles Serica orientalis Motschulsky, Maladera verticalis (Fairmaire), and Anomala corpulenta Motschulsky (all Coleoptera: Scarabaeidae) (Tang et al. 2013).

The other type of plant defense based on plant volatiles involves indirect defenses wherein induced volatiles attract the predators of herbivores, thereby exerting a degree of biological control (McCormick et al. 2012; Schausberger et al. 2012). For example, egg parasitoids (Trichogramma bournieri Pintureau & Babault; Hymenoptera: Trichogrammatidae) and larval parasitoids (Cotesia sesamiae [Cameron]; Hymenoptera: Braconidae) are attracted by volatiles induced by the stalk borer Chilo partellus Swinhoe (Lepidoptera: Crambidae) on teosinte, Zea sp. (Poaceae), which thereby provides an indirect defense mechanisms against the stalk borers (Mutyambai et al. 2015). As another example, treatment of seeds with the phytohormone jasmonic acid has also been shown to make tomato, Solanum lycopersicum L. (Solanaceae), plants more attractive to predatory mites (Smart et al. 2013).

The use of herbivore-induced plant volatiles to attract the natural enemies of crop herbivores, thereby reestablishing predator—prey relationships and reducing the need for additional pest suppression in agricultural habitats, has risen substantially over the past 10 yr (Kaplan 2012). These volatiles attract both parasitic and predatory insects that are natural enemies of the herbivores, and they may induce defense responses in neighboring plants (Paré & Tumlins