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Artificially Applied Plant Volatile Organic Compounds Modify The J Pest Sci (2017) 90:611–621 DOI 10.1007/s10340-016-0792-1 ORIGINAL PAPER Artificially applied plant volatile organic compounds modify the behavior of a pest with no adverse effect on its natural enemies in the field Improving the push–pull strategy against a major Brassicaceae pest 1,2 1,2 1,2 1,2 Fabrice C. Lamy • Denis Poinsot • Anne-Marie Cortesero • Se´bastien Dugravot Received: 20 January 2016 / Revised: 15 June 2016 / Accepted: 21 June 2016 / Published online: 6 July 2016 Ó Springer-Verlag Berlin Heidelberg 2016 Abstract The use of volatile organic compounds (VOCs) Keywords Push–pull strategy Á Plant–insect interaction Á derived from plants to manipulate insect pest behavior can Volatile organic compounds Á Brassicaceae Á be applied in an integrated pest management strategy Delia radicum Á Natural enemies (IPM) using a combination of attractive and repulsive stimuli. The ‘‘push–pull’’ strategy was developed on this idea in order to disturb and modify the distribution and Key message abundance of pests to protect crops and reduce the use of agrochemicals. This field experiment investigates, in a • A push–pull strategy successfully protected Brassi- ‘‘push–pull’’ context using broccoli as a target crop and caceae crop against Delia radicum, a major agricultural Chinese cabbage as a pull component, the stimulo-deterrent pest, using plant volatile organic compounds (VOCs). effect of five synthetic VOCs (dimethyl disulfide, linalool, • Most of the VOCs significantly reduced pest oviposi- geraniol, eucalyptol and citronellol) on the oviposition of tion. Eucalyptol was the most promising VOCs as it the cabbage root fly Delia radicum. With the exception of reduced final infestation of Delia radicum without linalool, all compounds tested had a significant effect in the affecting in a negative way the biodiversity of pest field and eucalyptol showed the most promising results, natural enemies (predators and parasitoids). reducing oviposition on broccoli by 45 %. Moreover, eucalyptol was the only VOC able to reduce the final infestation of D. radicum, i.e., the number of pupae. The Introduction other VOCs reduced oviposition by 20–30 %. No adverse effect of the treatments was found on major parasitoids Plants emit in their environment a wide diversity of volatile (Trybliographa rapae and Aleochara bipustulata) and organic compounds (VOCs) (Knudsen et al. 2006), which potential predators of D. radicum. This study highlights the are involved in diverse beneficiary functions such as pol- potential of VOCs as deterrent stimuli against agricultural linator’s attraction (Ibanez et al. 2010; Reinhard et al. pests in the field. 2004), defense against pathogens and phytophagous insects (Huang et al. 2012; Pare and Tumlinson 1999), or herbi- vore’s natural enemies recruitment (Heil 2008; Turlings et al. 1990; Vet and Dicke 1992). Those VOCs play a major role in the location and recognition of the host plant Communicated by J. Gross. by herbivorous insects (Kuhnle and Muller 2011; Wynde and Port 2012). & Fabrice C. Lamy The idea to protect a crop by manipulating the resource- [email protected] selection behavior of its pests appeared at the end of the 1 Universite´ Rennes 1, UMR1349 IGEPP, 35000 Rennes, eighties and was called stimulo-deterrent diversionary France strategy or ‘‘push–pull’’ strategy (Miller and Cowles 1990; 2 Universite´ Europe´enne de Bretagne, Rennes, France Pyke et al. 1987; Smart et al. 1994). This strategy consists 123 612 J Pest Sci (2017) 90:611–621 in pushing the herbivorous insect outside the crop and release of VOCs with the pest infestation. Good candidate pulling it at the periphery of the crop where it can be VOCs must markedly reduce (push) or increase (pull) the controlled (Cook et al. 2007). So far, researches have been oviposition behavior of D. radicum in order to significantly developed on some crop models (Bennison et al. 2001; impact the damage to the crop which results in yield loss. Martel et al. 2005; Meats et al. 2012; Smart et al. 1994; They must also be as harmless as possible to the environ- Tyler-Julian et al. 2014; van Tol et al. 2007; Yan et al. ment, farmers and final consumers. Finally the effect on the 2015) and have been strengthened by the major applied third trophic level (in particular the natural enemies of success of this strategy: the protection of maize and sor- D. radicum, i.e., its predators and parasitoids) must also be ghum against stem borers in sub-Saharan Africa (Khan considered. Our experiment was conducted on the second et al. 2000, 2008). Despite these encouraging results, the D. radicum generation or ‘flight’ in Brittany (France, potential of the push–pull strategy to protect crops remains approximately 48°N, 1°W) where two or three flights are largely unexplored, especially in temperate agrosystems. commonly observed per year. DMDS was used as positive The cabbage root fly, Delia radicum L. (Diptera: control in comparison with literature. We tested three Anthomyiidae) can inflict major losses to Brassicaceae VOCs previously described in the literature as affecting crops (Coaker and Finch 1971; King and Forbes 1954). insect oviposition: eucalyptol, geraniol, citronellol with the Host recognition is governed by complex behavior pat- hypothesis that they had the potential to limit infestation of terns. Gravid mated females, responsive to host plant odor crop plants in an agronomical context. Eucalyptol has been (Finch 1978; Hawkes 1975) and spectrophotometric shown to reduce D. radicum oviposition by 75 % in the reflectance of the host (Prokopy et al. 1983), move from the laboratory (den Ouden et al. 1996), whereas geraniol and edge of the field into the host crop with a diurnal period- citronellol had never been tested before on D. radicum but icity (Hawkes 1972). After landing, females taste the plant have shown interesting oviposition reduction in other taxa using leaf surface compounds (Roessingh et al. 1997), (Klocke et al. 1987; Li et al. 2007; Saxena and Basit 1982). climb down along the stem, probe the soil and oviposit at We also tested linalool with the hypothesis that it had the the base of the stem (Zohren 1968). Some studies have potential to increase plant infestation levels, because of its shown that it was possible to manipulate female behavior predominance in the VOC mix of the Chinese cabbage, with plant compounds, either to increase (Baur et al. 1996; which is attractive to D. radicum (Kergunteuil et al. 2015). Hurter et al. 1999) or to decrease oviposition (den Ouden We evaluated effects of VOCs on D. radicum oviposition et al. 1993), including when using synthetic VOCs in the by counting eggs laid on broccoli. We also evaluated the field (Kergunteuil et al. 2012). Dimethyl disulfide (DMDS) impact on final infestation by counting D. radicum pupae in is a VOC known to deter D. radicum oviposition (Ferry the soil near plants, and we evaluated possible impacts on et al. 2009; Kergunteuil et al. 2012) and could in principle predators and parasitoids by direct (pitfall traps) and indi- be used as a ‘push’ component in a push–pull strategy rect measurements (parasitism rate). against the cabbage root fly. However, the expected cor- relation between the reduction in oviposition of D. radicum and the number of pupae found near the treated plants Materials and methods could not be demonstrated (Ferry et al. 2009). Another limitation of DMDS, currently used as a soil fumigant Volatiles tested (Cabrera et al. 2014), is its high toxicity to vertebrates (Dugravot et al. 2003). When it comes to the necessary We investigated in the field the influence on (1) D. radicum ‘pull’ component, D. radicum host preferences have been oviposition (using felt traps or direct counting of eggs on compared among cultivated Brassicaceae, and Chinese the plant) and (2) the activity of natural enemies of D. cabbage (Brassica rapa L. subsp. pekinensis) appears to be radicum, (using pitfall traps) of five VOCs supplied from highly attractive (Rousse et al. 2003), making it a good Sigma-AldrichÒ (Saint-Louis, USA): dimethyl disulfide potential candidate. (DMDS, C99.0 %), linalool (97 %), geraniol (C97 %), The main purpose of our field experiment was to select, citronellol (C95 %) and eucalyptol (99 %). in a push–pull context, VOCs which could be integrated in such a strategy against the cabbage root fly D. radicum. Field setup The choice to select repellent volatile chemicals instead of repellent non-host plants was made because of some Broccoli plants (Brassica oleracea L. var. Italica cv. obvious agronomic and implementing advantages. Any Marathon) grown in peat soil cylinders in a plastic tunnel ‘‘push’’ intercrop would compete with the crop and com- were provided by Thomas Plants (Ploubazlanec, France) at plicate weed management. Moreover, using VOC dis- the age of 6 weeks (4–5 true leaves stage). Chinese cab- pensers instead of plants allows to easily coordinate the bage seeds (Brassica rapa L. subsp. Pekinensis Lour. cv. 123 J Pest Sci (2017) 90:611–621 613 Michiili) were provided by La Bonne Graine (Tigne´, counted then destroyed once per week on the same day France). The experimental field was located in an experi- during 6 weeks. In order to evaluate the eggs laid in the Pull mental field station at Le Rheu, France, (48°603100N, strips, eggs were counted on Chinese cabbage too. However, 1°470100W). Chinese cabbage was sown on May 14, 2014 at because of the rosette architecture of Chinese cabbage, D. a density of 100 seeds per m2 and protected from flea radicum can lay not only at the base of the plant but also beetles and D. radicum with a P17 fleece during 6 weeks; inside the rosette. Accordingly, felt traps underestimate eggs after this time the mean density (±SE) of Chinese cabbage laid on this species.
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