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– 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 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 as a target crop and caceae crop against Delia radicum, a major agricultural Chinese 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 (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 ) 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 ( 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. Eggs were therefore monitored by har- was estimated as 52 ± 14 plant/m2 (n = 50). Broccoli was vesting randomly one Chinese cabbage from the first and transplanted the week they were delivered, on June 24, third ranks (in a 2-m-wide band at the center of the rank) 2014 at a density of 2.7 plants per m2, and the experiment once a week during the three first weeks and counting in the was monitored during the following 6 weeks. laboratory all the eggs laid on the plant, distinguishing full Before plantation, weeds were controlled by creating a and hatched ones. This counting was performed only during false seed bed, and then weeding was performed using the three first weeks: Later, due to the high infestation of D. conventional herbicides: Chinese were weeded radicum and proximity of plants, most of Chinese cabbages using ButisanÒ S: 1.1L (i.e., 550 g metazachlor) per ha shoots were rotten, making egg counting impossible. after seeding and one treatment was performed 3 weeks All statistical analyses were performed with R software after implantation on broccoli (LentagranÒ: 1.2 kg (i.e., (R_Core_Team 2013). The mean number of eggs laid per 540 g pyridate) per ha. felt trap on broccoli was calculated per plot and week and The experimental field was divided into four blocks of six analyzed using a Wald test on a linear mixed model fully randomized plots corresponding to the five VOCs tested (LMM) including treatment and week as fixed factors and and the control (Fig. 1). Plots were separated by 3 m of bare blocks as a random factor (function ‘lmer’, package ‘lme4’ soil. Each plot had a central area planted with (17 Bates et al. 2015). Pairwise comparisons of least squares rows of 19 plants, with 0.75 m between rows and 0.5 m means (LSM) between treatments per week (function between plants), and a VOC dispenser filled with pure vola- ‘lsmeans’ of package ‘lsmeans,’ Lenth 2014) were per- tiles (used as the push component) was placed beside the plant formed using the false discovery rate for correction of at the center of the plot (i.e., 1 dispenser for 108 m2 or 93 P values (Benjamini and Hochberg 1995). dispensers per ha). Dispensers were made of a wick of The total number of eggs laid on Chinese cabbage was pheromone dispenser (Zobele Group, Trento, Italy) mounted calculated per plot and week and analyzed using a likeli- on a small glass vial (8 ml) containing the VOC. The device hood ratio test on a generalized linear model (GLM) (dis- was protected from rain and wind by a plastic vial (60 ml) tribution: negative binomial, link function: log, function pierced of eight holes (Ø = 3mm)andplaced20cmabove ‘glm.nb’ of package ‘MASS’, Venables and Ripley 2002) the ground on the top of a stake. Dispensers were regularly including treatment and week as fixed factors. refilled and volatilities corresponding to the quantity of pro- duct volatilized per time unit were calculated by differential Pupae collection weighing. In increasing order, mean volatilities (mg/day) were: 16 ± 3 (citronellol), 21 ± 13 (geraniol), 45 ± 13 (li- D. radicum pupation takes place in the soil near the roots. nalool), 130 ± 23 (eucalyptol) and 331 ± 31 (DMDS). The Pupae were collected on September 11 and 12 using a cost associated to VOCs consumed during 6 weeks was 15-cm-diameter and 15-cm-deep cylindrical auger. Eight comprised between 100 and 150€ per ha. The peripheral area soil samples corresponding to eight broccoli plants not of each plot (used as the pull component) was sown with monitored with felt traps were collected crosswise in each Chinese cabbage (six rows with 0.5 m between rows and 50 plot (Fig. 1). The auger was centered on the stem in order seeds per linear meter). The pull component was about one to collect most pupae. Soil samples were sifted through third of the total surface of the plot and the ratio between the 1-mm mesh and pupae were counted (including empty or number of Chinese cabbage and broccoli was 17–1. damaged ones). Pupae were washed then identified to species under the binocular to calculate parasitism rate of Oviposition D. radicum pupae by Aleochara sp. and Trybliographa rapae L. Pupae parasited by T. rapae are smaller than The oviposition of D. radicum was monitored both on healthy pupae (Varis 1967) but to provide a reliable iden- broccoli and Chinese cabbage. Eggs laid on broccoli were tification, nymphs were observed by transparency by wet- recorded using felt traps (Bligaard et al. 1999) positioned on ting the puparium and identified. Results obtained with this the stem of the plant where the fly normally lays its eggs. identification method are not biased by the extra mortality Seventeen felt traps were arranged crosswise per plot generated by manipulation and storage in laboratory con- (Fig. 1). All the felt traps in a block were observed and eggs ditions compared to a post-emergence identification. 123 614 J Pest Sci (2017) 90:611–621

(a)

(a)

(b)

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Fig. 1 Schematic representation of the experimental field formed of four blocks themselves divided into six plots (a) and detail on a plot (b)

The mean number of pupae and of T. rapae per broccoli Chinese cabbage strip and another two in each broccoli plot plant, and the mean proportion of T. rapae were calculated (Fig. 1). Traps were opened during 24 h once per week per plot and analyzed by LMM using a Wald test with during six weeks and were counted then treatment as a fixed factor and blocks as a random factor released. They were sorted into four groups for analysis: (function ‘lmer’, package ‘lme4’ Bates et al. 2015). Pairwise (1) Carabidae from Metallina and Bembidion, (2) comparisons of least squares means between treatments were other Carabidae (the main genus identified were: Poecilus, performed when needed (function ‘lsmeans’ of package Pseudoophonus, Amara, Anchomenus, Pterostichus, Acu- ‘lsmeans’, Lenth 2014) using the false discovery rate for palpus and Harpalus), (3) Aleochara bipustulata L., a correction of P values (Benjamini and Hochberg 1995). staphylinid and one of the major parasitoids of D. radicum, and (4) all other Staphylinidae. The other arthropods, found Pitfall traps in small numbers, were not considered. The total number of arthropods of each group captured The activity and diversity of natural enemies was estimated by pitfall traps was calculated per crop (i.e., broccoli or using dry pitfall traps to minimize the impact on the local Chinese cabbage) per plot and per week. The impact of density of beneficial insects. Two traps were placed in each treatment, crop and week were included as fixed factors 123 J Pest Sci (2017) 90:611–621 615 and assessed by GLM (distribution: negative binomial, link respectively by 43, 35, 27 and 21 % compared to control. function: log) using a likelihood ratio test (function: Moreover, this week, oviposition was significantly lower ‘glm.nb’ of package ‘MASS’ (Venables and Ripley 2002). on plots treated with eucalyptol and citronellol compared to When needed, pairwise comparisons of least squares means the DMDS reference treatment. On the fifth week, ovipo- were performed using package ‘lsmeans’ (Lenth 2014) sition globally decreased in all plots, but only eucalyptol using the false discovery rate for correction of P values and citronellol significantly reduced the number of eggs (Benjamini and Hochberg 1995). compared to control, with eucalyptol still reducing ovipo- sition significantly more than DMDS (Table 1).

Results Pupae collection and parasitism rates

Oviposition Eucalyptol reduced by over 60 % the number of pupae per plant compared to control (Fig. 2). The reduction in the The experimental field was colonized by D. radicum during number of pupae found in the other treatments were not the first week after broccoli transplantation (1.0 ± 0.2 statistically significant. Out of 930 D. radicum pupae col- eggs/broccoli). Maximal egg numbers were observed dur- lected, only five were parasitized by Aleochara sp., while ing the fourth week and the threshold of seven eggs per felt 219 (23 %) were parasitized by T. rapae. However, even if trap per week used by farmers as a warning to start a Wald test applied on a LMM reveals a significant global spraying insecticides was exceeded in the control on heterogeneity between treatments for both number of T. broccoli during the fourth and fifth weeks (Table 1). Eggs rapae per plant (LMM: v2 = 15.10, df = 5, P = 0.010) could not be counted in Chinese cabbage after week 3 (see and proportion of T. rapae in pupae (LMM: v2 = 11.33, ‘‘Materials and methods’’). df = 5, P = 0.045), no difference of parasitism rate The number of unhatched eggs counted on Chinese reaches significance in pairwise comparisons least squares cabbage did not differ significantly between treatments and means, Fig. 2. control during the three first weeks (LMM: v2 = 8.55, df = 5, P = 0.128) and weeks did not differ significantly Pitfall traps (LMM: v2 = 5.26, df = 2, P = 0.072). The number of eggs laid on broccoli was significantly The abundance of D. radicum natural enemies did not differ different among treatments (LMM: v2 = 117.22, df = 5, significantly between treatments (GLM: Metallina sp. and P \ 0.001), and between weeks (LMM: v2 = 3946.75, Bembidion sp.: v2 = 3.01, df = 5, P = 0.698, other carabids: df = 5, P \ 0.001). Few eggs were laid during the two first v2 = 5.72, df = 5, P = 0.335, A. bipustulata: v2 = 6.07, and the last week of our study, and no differences were df = 5, P = 0.300, other rove beetles: v2 = 6.60, df = 5, observed between treatments at those periods (Table 1). P = 0.252). High community differences were However, during the oviposition peak (weeks three to five), found between crops (Table 2), and these communities significant differences gradually appeared. During the third changed significantly with time (GLM: Metallina sp. and week, eucalyptol reduced significantly D. radicum ovipo- Bembidion sp.: v2 = 75.37, df = 5, P \ 0.001, other cara- sition by 54 % compared to control (Table 1). On week bids: v2 = 127.67, df = 5, P \ 0.001, A. bipustulata: four, oviposition on plots treated with eucalyptol, v2 = 581.57, df = 5, P \ 0.001, other rove beetles: citronellol, geraniol and DMDS was significantly reduced v2 = 348.74, df = 5, P \ 0.001).

Table 1 Mean number (± SE) Week 1 Week 2 Week 3 Week 4 Week 5 Week 6 of D. radicum eggs per felt trap and per week depending on the Control 1.1 ± 0.1a 1.7 ± 0.2a 3.7 ± 0.6a 17.3 ± 1.1a 8.2 ± 0.8a 0.5 ± 0.1a treatment DMDS 1.0 ± 0.4a 1.2 ± 0.1a 2.8 ± 0.9ab 13.6 – 0.5b 7.2 ± 0.4ab 0.2 ± 0.1a Geraniol 1.1 ± 0.4a 1.6 ± 0.4a 2.5 ± 0.5ab 12.7 – 0.5bc 7.1 ± 0.7ab 0.2 ± 0.1a Linalool 1.2 ± 0.3a 1.2 ± 0.2a 2.5 ± 0.1ab 15.7 ± 0.9a 7.6 ± 0.6ab 0.4 ± 0.0a Citronellol 0.8 ± 0.3a 1.0 ± 0.3a 2.2 ± 0.4ab 11.2 – 0.3cd 6.1 ± 0.5bc 0.2 ± 0.0a Eucalyptol 0.7 ± 0.1a 0.9 ± 0.1a 1.7 ± 0.3b 10.0 – 0.6d 4.3 ± 0.5c 0.1 ± 0.0a Different letters indicate significant differences between treatments during a given week (LMM, least- squares means). Bold figures indicate significant differences (P \ 0.05) from the control. Underlined figures indicate a number of eggs laid superior to the agronomic ‘warning’ threshold of seven eggs per felt trap per week, above which a pesticide treatment is recommended

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Fig. 2 Mean numbers (±SE) of D. radicum pupae and T. rapae per broccoli and proportion of T. rapae per pupae, as a function of treatment. Different letters indicate significant differences between treatments (P \ 0.05) for D. radicum pupae per plant (GLM, least-squares means)

Table 2 Mean number (±SE) Chinese cabbage Broccoli Statistics of arthropods per groups and per plot depending on the crop v2 df P

(1) Metallina sp. and Bembidion sp. 4.4 ± 0.3a 12.8 ± 1.0b 68.14 1 \0.001 (2) Other Carabidae 3.9 ± 0.3b 2.4 ± 0.2a 27.71 1 \0.001 (3) A. bipustulata 3.5 ± 0.5b 0.6 ± 0.1a 151.66 1 \0.001 (4) Other Staphylinidae 2.8 ± 0.3b 0.5 ± 0.1a 185.62 1 \0.001 Different letters indicate significant differences (P \ 0.05) between crops (GLM, least-squares means)

Discussion was found on parasitoids and potential predators. This bicyclic monoterpene, commonly found in plants of the In the present study we investigated the possibility to Myrtacea family, plays a major role in plant–microorgan- design a push–pull strategy against the cabbage root fly in ism (Steeghs et al. 2004) and plant–insect interactions the field by measuring the effect of five synthetic VOCs. (Schiestl and Roubik 2003). It has been tested against They were separately tested in a broccoli crop with Chinese mosquitoes (Klocke et al. 1987) and on a great variety of cabbage strips as pull component. Four of them (i.e., insect pests for its toxicity, repellency or its effect on DMDS, geraniol, citronellol and eucalyptol) were tested as oviposition (Bekele and Hassanali 2001; Karemu et al. potential push factors, while linalool was tested for its 2013; Koul et al. 2013; Li et al. 2007; ObengOfori et al. potential pull effect. 1997; Saxena and Basit 1982), revealing highly contrasted Of these five compounds, eucalyptol yielded the most results depending on the biological model, but was iden- promising results: It reduced by 45 % on average the tified to reduce D. radicum oviposition by 75 % in labo- oviposition of D. radicum during the three consecutive ratory conditions (den Ouden et al. 1996). Raw products weeks corresponding to the oviposition peak. During this containing eucalyptol, such as essential oils or eucalyptus period, the alert threshold of 7 eggs/plant/week in euca- leaves, have also been studied for pest management (Batish lyptol-protected plots was reached during 1 week, while it et al. 2008; Santos 2006). Eucalyptol is synthesized by was largely passed for two consecutive weeks in control plants of the Brassicaceae family (Chen et al. 2004) and is plots. As a result, the global D. radicum herbivory pressure, present at low concentrations during different growing estimated by the number of pupae produced per plant, was stages of Brassica napus (McEwan and Macfarlane Smith significantly lower in eucalyptol-protected plots compared 1998). This compound seems to take part in plant defense to control. No adverse effect of the eucalyptol treatment mechanism since its emission increases in Brassica

123 J Pest Sci (2017) 90:611–621 617 oleracea after an attack by caterpillars of the phytophagous DMDS by using a much higher dose than the one we used moth Plutella xylostella (Vuorinen et al. 2004). Eucalyptol might not be feasible on safety grounds alone. has been shown to promote oviposition in a single case, the Citronellol and geraniol both showed interesting results: tuber moth Phthorimaea operculella (Ma and Xiao 2013). the former reduced D. radicum oviposition by 30 % during The present study is the first to demonstrate in the field the 2 weeks and the latter reduced oviposition by 25 % during strong deterrent effect of eucalyptol on oviposition by a the highest peak, and they did not reduce the activity of pest. predators and parasitoids. However, neither of them could DMDS also reduced D. radicum oviposition markedly reduce significantly the number of D. radicum pupae pro- (–20 % compared to control during the highest peak) duced. These compounds are common acyclic monoter- although its effect was not as drastic as that of eucalyptol penes playing roles in plant–insect interaction, and their (–45 % during the peak). Contrary to some previous work repellent effect on mosquitoes is well known (Kaufman showing an attractive effect of DMDS on ground-dwelling et al. 2010; Montefuscoli et al. 2014). Their potential effect predators (Ferry et al. 2007; 2009), we did not find any on agronomic insect pests remain, however, largely unex- significant effects of this compound on predators, nor on plored (Lee et al. 1997; Saxena and Basit 1982), but the parasitism rate of D. radicum by parasitoids. However, essential oils containing these compound show some effi- unlike eucalyptol, DMDS did not significantly reduce the ciency (Costa et al. 2015; Olivero-Verbel et al. 2010), and number of D. radicum pupae recovered per plant. The our results suggest they have potential also against D. present field experiment thus confirms earlier results where radicum in the field. DMDS significantly reduced D. radicum oviposition suf- Linalool is the only VOC which did not show any sig- ficiently to avoid reaching the agronomic warning thresh- nificant effect on D. radicum oviposition or other param- old of 7 eggs/plant/week, but without reducing the final eters recorded in our study. Although it is already known to number of pupae produced (Ferry et al. 2009). In a later deter oviposition in some insect pests (Furtado et al. 2014; study, oviposition by D. radicum was significantly reduced Mbata and Payton 2013; Murungi et al. 2013), it was also but not sufficiently to prevent the agronomic warning identified as the major compound in the Chinese cabbage threshold to be reached (Kergunteuil et al. 2012). The VOC blend (Kergunteuil et al. 2015) which is very insect repellent effect of DMDS has also been reported in attractive to D. radicum (Rousse et al. 2003). Accordingly, some Psylidae and Miridae bugs (Hemiptera) (Diaz-Mon- we had made the hypothesis that linalool could be used as a tano and Trumble 2013; Pan et al. 2013). This compound is ‘pull’ factor, i.e., we postulated that it would attract D. derived from the decomposition of Brassicaceae (Lewis radicum and induce more damage in linalool-treated plots. and Papavizas 1970), which can be inducted in particular This hypothesis must be rejected since linalool did neither following damage by D. radicum larvae (Crespo et al. stimulate nor diminish egg laying by D. radicum in field 2012; Samudrala et al. 2015). DMDS is therefore used as a conditions, at least at the concentration used in our trial. It cue by D. radicum females to assess the quality of the is therefore dubious that linalool is the main factor resource: A low DMDS concentration means that the host responsible for the high attractiveness of Chinese cabbage plant is healthy and could provide sufficient resource for for this pest, unless its efficiency as an attractor depends on larvae development, while a high DMDS concentration its interaction with the rest of the Chinese cabbage blend warns of a plant which quality is degraded because it has (Mukherjee et al. 2015). already been largely exploited by conspecifics (Ferry In our trial, the diffusion of all VOCs relied on the same 2007). Indeed, larvae develop better on healthy rutabagas passive device; however, considering their different than on decaying ones (Doane and Chapman 1964). DMDS physicochemical properties, the amounts released were diffusion per day was the most important among the five highly different. A factor of 20 appears between DMDS VOCs tested because of its high volatility, and because in (331 ± 31 mg/day) and citronellol (16 ± 3 mg/day) order to reduce D. radicum oviposition, DMDS concen- making it difficult to compare VOCs on a weight-for- tration has to be sufficiently high. One drawback is that weight basis, but our main objective was to reveal their higher quantities of DMDS probably increase the potential and the question of the optimal dose would detectability of the crop by D. radicum at a larger scale. require additional experimentations. In this perspective, Moreover, the high toxicity of DMDS toward vertebrates active devices could improve the system, with a quantita- (Dugravot et al. 2003; Essawy et al. 2015) must be taken in tive and temporal controlled release of the VOC synchro- consideration (the pungent odor of DMDS was readily nized with the fly’s behavior. Indeed D. radicum females detectable in our trial). These two aspects outline the have a diurnal periodicity where they feed on flower in the agronomical limits of this product to protect a crop against morning and move into the crop in the early afternoon D. radicum, and trying to improve the repellent effect of (Hawkes 1972).

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In the conditions tested here, eucalyptol appears the Therefore, it seems that VOCs released are not able to most promising and we intend to investigate its use with mask the specific VOCs blend of an infested host and are industry-grade controlled dispensers. Also, VOCs were probably perceived by T. rapae as an additional perturba- tested as ‘push’ components on a broccoli crop bordered tion in the complexity of VOCs present in the agrosystem’s with a Chinese cabbage ‘pull’ strip, so the effect we atmosphere. observed could result from a synergy between VOCs and In conclusion, eucalyptol provided a strong reduction of the Chinese cabbage border, and the attraction of this oviposition of D. radicum in the field, it also reduced the border was probably accentuated by the higher vegetative number of pests produced by the crop and presented no growth and density of Chinese cabbage compared with detectable adverse effect on its natural enemies, making it a broccoli. However, as stated in the Materials and methods promising candidate to develop a push–pull strategy section, after the third week and because of their high against a major pest of Brassicaceae. Citronellol and density, most of the Chinese cabbages started to rot. This geraniol also demonstrated potential, to a lesser extent. unwanted situation probably had an important impact on Finally, DMDS confirmed its capability to reduce D. the global VOC blend of the pull strip including a rise of radicum oviposition but its toxicity in particular makes it sulfur-derived compounds like DMDS known to reduce D. difficult to envision its use if important doses must be radicum oviposition (Ferry et al. 2009). applied. However, more investigations are needed both in Pests other than D. radicum were not specifically the laboratory to understand the mechanisms behind the monitored in this study but no outstanding effect was oviposition decrease in D. radicum, and in the field to noticed throughout the experiment and their numbers on validate the dose necessary to fully protect a crop against broccoli plants remained very low. Furthermore, none of this pest. The possibility to use small amounts of innocuous the VOCs tested modified the abundance or diversity of VOCs appears like a promising alternative for the protec- natural enemies captured in pitfall traps, and most inter- tion of brassicaceous crops against the cabbage root fly. estingly the compounds reducing egg-laying (possibly though a repellent effect on D. radicum) did not appear to repel natural enemies. Only differences between weeks and Author contribution statement between broccoli and Chinese cabbage populations were observed, probably explained by the plants architecture All authors conceived and designed research. FL conducted offering different ground covers. For example, Metallina experiments. FL and DP analyzed data. FL wrote the sp. and Bembidion sp. were more abundant in the broccoli manuscript. All authors commented and approved the crop (mostly bare ground) than in Chinese cabbage (im- manuscript. portant ground cover), which is in line with the ecological preferences of this species (Mitchell 1963). However, Acknowledgements We thank the staff of the ‘Domaine experi- predator efficiency was not tested and it cannot be excluded mental de la Motte’ (INRA Center, Le Rheu, France) and especially Gabriel Nedelec for his advice and help with the field experiment. that ‘push’ VOCs could affect it. Surprisingly, very few A. The authors acknowledge Charline Ridard and Eileen Gazengel for bipustulata were found emerging from D. radicum pupae the precious help provided during the monitoring of the experiment. although this species is one of its major parasitoids (Fournet et al. 2000). Nevertheless, this result is coherent Funding This work was financed by the project ‘‘PURE’’ and a grant of the French ministry for research (MESR) to FL. with the spatiotemporal abundance revealed with pitfall traps, where the largest quantity of Aleochara sp. were Compliance with Ethical Standards trapped during the two first weeks of the trial, when D. radicum pupae were not yet formed. During that early Conflict of interest Authors declare that they have no conflict of interest. period, the A. bipustulata present could only have eaten D. radicum eggs or attacked its young larvae, but could not Ethical approval All applicable international, national, and/or parasitize nonexistent pupae. On the contrary, with close to institutional guidelines for the care and use of were followed. one in four pupae parasitized, the average parasitism rate by T. rapae was relatively high, since it generally ranges between 1 and 35 % (Wilkes and Wishart 1953; Wishart References and Monteith 1954). Trybliographa rapae seems not to be affected in the search for its hosts by ‘push’ VOCs released Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear in the broccoli crop, which is especially interesting because mixed-effects models using lme4. J Stat Softw 67:1–48. doi:10. this species relies heavily on special VOCs emitted by 18637/jss.v067.i01 Batish DR, Singh HP, Kohli SK, Kaur S (2008) Eucalyptus essential plants in response to an attack by D. radicum to find the oil as a natural pesticide. Forest Ecol Manag 256:2166–2174. larvae of its host (Neveu et al. 2002; Nilsson et al. 2012). doi:10.1016/j.foreco.2008.08.008 123 J Pest Sci (2017) 90:611–621 619

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