Modification of Macrosiphum euphorbiae colonisation behaviour and reproduction on potato plants treated by mineral oil
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1 Modification of Macrosiphum euphorbiae colonisation behaviour and reproduction on potato plants treated by mineral oil A. Ameline*, A. Couty, M. Martoub, S. Sourice & P. Giordanengo Unité de Recherche EA3900 BioPI, Biologie des Plantes et contrôle des Insectes ravageurs, Laboratoire de Biologie des Entomophages, Université de Picardie Jules Verne, 33 rue St Leu, Amiens cedex, France Accepted: 6 January 2010 DOI: /j x Keys words: aphid, Hemiptera, Aphididae, Solanum tuberosum, olfactometer, electrical penetration graph, EPG, host plant selection, feeding behaviour, population parameter, probiotic Abstract Although mineral oil spray is one of the most effective ways to control the transmission of non-persistent aphid-borne viruses in the field, its mode of action is poorly understood. In this study, the effects of mineral oil treatment of potato plants on host selection behaviour, growth, and reproduction of potato aphids, Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae), were investigated. The effects were assessed 30 min, 1 day, and 7 days after treatment, (1) on aphid orientation behaviour by using a Y-tube olfactometer, and (2) on aphid feeding behaviour by using the electrical penetration graph (EPG) technique. Olfactory experiments showed that the oil had a repulsive effect only 30 min after spraying. EPG experiments showed a slight modification of the aphid feeding behaviour mainly 7 days after treatment. The number of both salivation and sap ingestion events during the phloem phases were increased 7 days after treatment. In addition, irrespective of the time after treatment, xylem ingestion time was increased. Clip cage experiments were set up to assess potential effects of the oil treatment on aphid survival and population parameters. Nymphal mortality was increased on treated plants, whereas fecundity of surviving insects was enhanced. The antagonistic effects of oil treatment on aphids are discussed in a plant protection context. Introduction Mineral oil application is one of the most effective ways to control the transmission of non-persistent viruses by aphids in the field (Bradley et al., 1962, 1966; Simons et al., 1977; Powell & Hardie, 1994; Hooks & Fereres, 2006). However, its mode of action is poorly understood. Plants may be actively protected because of the direct intoxication of aphids by oil (e.g., anoxia of sprayed insects; Taverner, 2001; Najar-Rodríguez et al., 2008), but indirect effects could also occur. Host plant colonisation by alate aphid morphs is achieved through several steps (Niemeyer, 1990; Pickett et al., 1992; Powell et al., 2006): (1) habitat and host location, which are governed by visual and olfactory cues, (2) host plant acceptance after perception of leaf surface chemistry, (3) assessment of epidermic and mesophyll cells *Correspondence: arnaud.ameline@u-picardie.fr by probing, (4) host acceptance indicated by sustained feeding on phloem sap depending on gustatory cues, and (5) after settling on a plant, production of apterous virginoparae that colonise the plant and neighbouring ones (Narayandas & Alyokin, 2006). Plant treatment with mineral oil may alter habitat and host plant location processes by affecting the perception of plant chemistry by the arthropod pest. Cen et al. (2002) showed that the odour of sweet oranges sprayed with mineral oil repelled the citrus red mite Panonychus citri (McGregor). Ameline et al. (2009) demonstrated that apterous Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae) orientation behaviour towards an oil-treated plant was modified by a masking effect. Several studies on Myzus persicae (Sulzer) revealed that mineral oil may alter the activities of the stylets as they penetrate the plant surface. Delay in the initiation of the first probing was reported by Simons et al. (1977). Reduction in the occurrence of stylet punctures of epidermal cell Ó 2010 The Authors Entomologia Experimentalis et Applicata 135: 77 84, 2010 Journal compilation Ó 2010 The Netherlands Entomological Society 77
2 78 Ameline et al. membranes was shown by Powell (1991, 1992). Ameline et al. (2009) showed that M. euphorbiae sustained feeding was delayed on treated plants, even 7 days after oil-treatment. The effects of mineral oil on aphid population parameters after settling on a treated plant have not yet been investigated. It has been observed that weekly oil treatments protect potato against non-persistent virus transmission by aphids in the field (X Riquiez, pers. comm.), as practised successfully by potato growers in Picardie (France). However, aphid population levels do not seem to be affected by these oil treatments. The exact mechanism underlying this preventive effect is not completely understood. Wang & Pirone (1996) suggested that the main mechanism through which mineral oil reduces virus transmission efficiency is its interference with the binding sites of the virions on the aphid stylets. Here we aim to investigate, through laboratory experiments, whether mineral oil plant applications could play a secondary role on the host plant selection behaviour and on the growth and reproduction of the potato aphid M. euphorbiae on its host plant Solanum tuberosum L. (Solanaceae). Materials and methods Plants and insects Potato plants, S. tuberosum cv. Désirée, were grown from tubers in 9-cm plastic pots in a growth chamber maintained at 20 ± 1 C, 60 ± 5% r.h., and L16:D8 photoperiod. In the experiments 4- to 6-week-old plants were used. The M. euphorbiae colony was initiated from a single apterous parthenogenetic female from the clone Me LB05 (INRA-INSA, Villeurbanne, France). The aphids were reared on potato plants enclosed in Plexiglas Ò cages in chambers at 20 ± 1 C and L16:D8 to induce parthenogenesis. The alate morph was chosen for the experiments as it is the most capable of dispersing to locate new hosts (Braendle et al., 2006; Powell et al., 2006). Individuals were collected on the inner wall of the rearing cages and standardised as described by Brunissen et al. (2009). Mineral oil plant treatments The highly refined mineral oil Finavestan EMA Ò (Total Fluides, Paris, France) is a mixture of nc15 to nc37 hydrocarbons (C15 C21 = 13.7%, C22 C27 = 66.4%, and C28 C37 = 19.8%). Its active constituent is 807 g l )1 paraffin oil, with a 99.8% unsulfonated residue. A mixture of ethoxylates of fatty alcohols and oleic acid was used as an emulsifier. After thorough mixing, it was sprayed as a 3% (vol vol) emulsion in water onto the upper surface of 4-week-old potato plants using a hand-held trigger spray (Pulsar 1L; Tecnoma, Epernay, France). Each plant was sprayed with 6 ml of the emulsion at 1 m above the plant to mimic application in the fields. The experiments were performed 30 min (OTP-0), 1 day (OTP-1), and 7 days (OTP-7) after plant treatment. Water-treated plants (WTP) were used as control. Y-tube olfactometer bioassay Experiments were carried out at 20 C in a glass Y-tube olfactometer as described by Sabelis & van de Baan (1983). The Y-tube olfactometer had an internal diameter of 2 cm and the angle between the two arms was 110. Toavoid any potential bias because of light attraction, it was placed on a luminous table providing homogeneous light (300 lux) in a dark room. An airflow of 300 ml min )1 was supplied by a vacuum pump attached to the base of the olfactometer and regulated by a flow meter. The 10-l glass chambers containing the odour sources were connected to the two arms of the olfactometer by a 25-cm long polyethylene tube. Activated charcoal filters were used to purify the air before passing through the odour sources. Alate female aphids were individually introduced with a small paintbrush into the Y-olfactometer at the base of the common stem (2 cm from the opening) and their behaviour was observed for 5 min. A choice was recorded when an aphid passed a line located 4 cm from the intersection of the Y-tube arms. Aphids that did not make a choice within 5 min were considered as non-responding. To control for possible bias, the device was reversed every five observations. The aphids were offered the following odour source combinations: blank (no source) vs. WTP, OTP-0 vs. WTP, OTP-0 vs. blank, OTP-1 vs. WTP, OTP-1 vs. blank, OTP-7 vs. WTP, and OTP-7 vs. blank. For each of the seven combinations, individuals were assayed. To avoid contaminations, the whole system was dismantled, thoroughly washed with ethanol, and rinsed with distilled water between combinations. Electrical recording The electrical penetration graph (EPG) DC-system (Tjallingii, 1988) was used to investigate aphid probing behaviour on oil-treated (OTP-0, OTP-1, and OTP-7) or WTP. To insert one aphid and one plant in an electrical circuit, a thin gold wire (20 lm diameter and 2 cm long) was stuck on the insect s dorsum by conductive silver glue (EPG systems, Wageningen, The Netherlands), the other electrode was inserted in the soil of the potted plant. All plants and insects were held inside a Faraday cage at an ambient temperature of 20 ± 1 C. For each treatment, individuals (= replicates) were used.
3 Effects of mineral oil on aphid behaviour and reproduction 79 Table 1 Probing behaviour (mean ± SEM) of Macrosiphum euphorbiae monitored on leaflets of water-treated (WTP) or mineral oil-treated (OTP-0, OTP-1, and OTP-7) potato plants WTP (n = 18) OTP-0 (n = 18) OTP-1 (n = 19) OTP-7 (n = 24) General probing behaviour (8 h recording) 1 Time to beginning of first probe (min) ± ± ± ± 3.42 Non-probing total duration (min) ± ± ± ± Pathway phase (C) total duration (min) ± ± ± ± No. phloem salivation (E1) 3.16 ± ± ± ± 1.07* Phloem salivation total duration (min) 8.99 ± ± ± ± 3.32 No. phloem sap ingestion (E2) 1.47 ± ± ± ± 0.84* Phloem sap ingestion total duration (min) ± ± ± ± No. xylem sap ingestion (G) 1.63 ± ± ± 0.27* 2.28 ± 0.26 Xylem sap ingestion total duration (min) ± ± 5.44* ± 6.46* ± 8.57* Intracellular probing behaviour (1 h recording) 2 No. potential drops (pd) ± ± ± ± 2.53 pd duration (s) 4.79 ± ± ± ± 0.20 II-1 pd subphase duration (s) 1.85 ± ± ± 0.03* 1.79 ± 0.08 II-2 pd subphase duration (s) 1.29 ± ± ± ± 0.06 II-3 pd subphase duration (s) 1.65 ± ± ± ± Occurrence and total duration of general probing parameters were calculated for the whole 8-h recording; 2 Occurrence and mean duration of intracellular probing parameters were calculated for the 1st hour from the beginning of the first C phase (intra-plant stylet activity). n, number of replicates; OTP-0, oil-treated plant tested 30 min after treatment; OTP-1, oil-treated plant tested 1 day after treatment; OTP-7, oil-treated plant tested 7 days after treatment; WTP: water-treated plant. *Means followed by an asterisk indicate a significant difference from control plants (Mann Whitney U-test: P < 0.05). The acquisition and analysis of the EPG waveforms were performed with PROBE 3.4 software (WF Tjallingii, Wageningen University, The Netherlands). The waveforms of 14 parameters associated to five EPG phases (C, E1, E2, G, and pd) (Tjallingii, 1988) were calculated using the EPG-Calc 4.8 software (Giordanengo, 2009a). C corresponds to pathway phase (extracellular movements of the mouthparts within the plant tissues), E1 to salivation in phloem elements, E2 to passive phloem sap ingestion, G to active xylem sap ingestion, and pd (potential drops) to intracellular probing behaviour, i.e., intracellular stylet punctures. The pd phase was divided into three sub-phases linked to non-persistent virus transmission: II-1, saliva injection (virus inoculation); II-2, transition; and II-3, ingestion of saliva cytosol mixture (virus acquisition). EPG data recording was performed for eight continuous hours. The nine parameters related to general probing behaviour (Table 1) were analysed for the whole 8-h recording period. The five parameters related to intracellular probing behaviour (Table 1) were analysed only during the 1st hour after the first probe. Survival and life history traits bioassays Cohorts of aphid nymphs (<24 h old) were obtained by isolating parthenogenetic females (apterous adults) on artificial diet 24 h before the experiment. The artificial diet was prepared according to Febvay et al. (1988) and slightly modified as described by Down et al. (1996). Five nymphs were transferred to a clip-cage installed on the abaxial face of the fourth fully expanded leaf from the apex of a potted potato plant. The biological performance of M. euphorbiae was assessed on control and oil-treated plants. Aphid nymphs placed on plants at day 0 (OTP-0) were approximately at the end of their pre-reproductive period at day 7 (OTP-7). For each treatment, 20 replicates were carried out (20 5 aphids per clip cage). Population parameters were evaluated every 3 days as described by Le Roux et al. (2004), until aphids died or for a duration equivalent to twice their pre-reproductive period (period from birth to the onset of reproduction). The Jackknife method (Meyer et al., 1986) was used to evaluate the variance of r m (intrinsic rate of natural increase) with the DEMP 1.2 software (Giordanengo, 2009b). The finite ratio of increase (k ¼ e rm ) and the population s doubling time (DT = ln2 r m )werealsocalculated. Statistical analysis Statistical analyses were performed using STATISTICA 5.5 software (StatSoft, Tulsa, OK, USA). A v 2 test was performed to evaluate the effects of plant treatment on the insect choice between the two arms of the olfactometer. EPG parameters of aphids feeding on treated (OTP-0, OTP-1, and OTP-7) plants were compared pair-wise with the control plant (WTP) by a non-parametric
4 80 Ameline et al. Mann Whitney U-test. The effects of oil treatment on nymph survival were analysed with Pearson s v 2 test. Oneway ANOVA was carried out to test the effects of oil treatment on population parameters. Before ANOVA, the data was normalised with the arcsine function according to Rao (1952). Significant effects detected by one-way ANOVA were further analysed with Fisher s least significant difference test. % nymphal survival WTP OTP Time (days) Results Orientation responses Alate M. euphorbiae showed a preference for the odour of control (WTP) when tested against a blank (v 2 =11.64, d.f. = 1, P<0.01; Figure 1). Aphids preferred WTP rather than OTP-0 (v 2 = 10.12, d.f. = 1, P<0.01) or OTP-1 (v 2 =5.00,d.f.=1,P<0.05).Macrosiphum euphorbiae did not show any significant preference when given the choice between WTP and OTP-7 (v 2 = 0.11, d.f. = 1, P = 0.73). OTP-0 was less attractive than the blank (v 2 =4.00, d.f. = 1, P<0.05) and OTP-7 was preferred to the blank (v 2 = 5.24, d.f. = 1, P = 0.02). However, no preference was observed between the blank and OTP-1 (v 2 =2.45, d.f. = 1, P = 0.12). Stylet activities Among the nine parameters associated with general probing behaviour, four were significant (Table 1). The numbers of phloem salivation and phloem ingestion phases were increased on OTP-7 plants (U = 146, P = and U = 142, P = 0.019, respectively). Xylem sap ingestion duration was increased on OTP-0 (U = 94, P = 0.019), OTP-1 (U = 58, P<0.001), and OTP-7 (U = 144.5, n = 33 (40) n = 31 (40) n = 31 (38) n = 36 (40) n = 45 (53) n = 34 (38) n = 31 (36) % alate aphids making a choice * ns ns * * ** * Blank WTP OTP-0 OTP-1 OTP-7 Figure 1 Orientation responses of Macrosiphum euphorbiae alates in Y-tube olfactometer tests; n = number of responding aphids (in parentheses the number of tested aphids). Hatching of the bars reflects the odour sources tested: Blank, empty chamber; WTP, water-treated plant; OTP-0, oil-treated plant tested 30 min after treatment; OTP-1, oil-treated plant tested 1 day after treatment; OTP-7, oil-treated plant tested 7 days after treatment. *P 0.05, **P 0.01, ns, not significant (v 2 test, a =0.05). Figure 2 Survival (%) of Macrosiphum euphorbiae nymphs reared on water-treated (WTP) or mineral oil-treated plants (OTP). P = 0.027). The number of xylem sap ingestions increased at OTP-1 (U = 92.5, P<0.01). With regards to aphid intracellular probing behaviour, parameters were not modified, except for the mean duration of subphase II-1, that increased 1 day after oil treatment (OTP-1: U = 98, P = 0.026). Nymph survival and life history traits Macrosiphum euphorbiae nymph survival (Figure 2) was reduced when the aphids were placed on OTPs (v 2 = 69.25, d.f. = 12, P<0.01). Adult longevity, reproductive period, and fecundity were significantly enhanced. The intrinsic rate of natural increase (r m ) was significantly increased and, consequently, the finite ratio of increase (k) was increased and the doubling time of the population was decreased (Table 2). Discussion Our study demonstrated that mineral oil treatment had several effects on M. euphorbiae colonisation process, as time elapsed after spraying. Some expected negative effects of the mineral oil were observed during the host plant location process and in early stages after aphid settling (nymph survival). Surprisingly, a probiotic effect of the mineral oil treatment was observed on surviving adults. Additionally, some parameters related to feeding behaviour were significantly modified. The olfactometry experiment showed that mineral oil treatment induced a repellent effect shortly after spraying (OTP-0). Contrary to essential oils which are well known for their repulsive effects against phytophagous insects (Hori, 1998; Landolt et al., 1999; Tripathi et al., 2000), this is the first time that such an effect is clearly observed for a mineral oil. However, this repulsive effect lasted for less than 1 day. Subsequently, a transitory effect of the oil treatment was observed (the treated plant was neither repulsive nor attractive). Seven days after treatment, no effect of oil treatment was observed and treated plants became attractive again. The differential effects of the oil
5 Effects of mineral oil on aphid behaviour and reproduction 81 Table 2 Mean (± SD) population parameter values of Macrosiphum euphorbiae reared on water-treated (WTP; n = 100 aphids tested) or mineral oil-treated (OTP; n = 100) potato plants, and outcome of one-way ANOVA Population parameter WTP OTP F P Pre-reproductive period (days) 8.35 ± 0.97a 8.73 ± 1.44a Longevity (days) 6.5 ± 2.42a 9.43 ± 5.37b Total fecundity (nymphs per female) 8.1 ± 6.61a ± 13.6b Daily fecundity (nymphs per female per day) 1.16 ± 0.87a 1.77 ± 0.68b Reproductive period (days) 6.25 ± 2.79a 9.3 ± 5.09b r m (female per female per day) 0.17 ± 0.07a 0.21 ± 0.04b k (female per female per day) 1.18 ± 0.08a 1.23 ± 0.05b Doubling time (days) 4.75 ± 1.79a 3.5 ± 0.75b Values in a row followed by different letters indicate a significant difference between mean values (Fisher s least significant difference, a =0.05). over time could be related to the composition of the mineral oil. It is likely that the more volatile components (<nc21), that made 13.7% of the hydrocarbon mixture, were responsible for the repellent effect observed shortly after treatment. Probing behaviour was not drastically modified on oiltreated plants. This is in accordance with previous work on the M. euphorbiae apterous morph (Ameline et al., 2009) and other aphid species (Powell, 1992). However, 7 days after treatment, the number of phloem sap salivations (E1) and ingestions (E2) increased, whereas their total duration did not, indicating a succession of shorter salivation and ingestion phases. Such shifts between salivation and ingestion during a phloem phase have been interpreted as a response of the aphid to alterations of phloem sap properties (Will et al., 2007), such as those occurring after plant defence activation. Interestingly, the duration of xylem sap ingestion was significantly enhanced in M. euphorbiae feeding on oiltreated plants. Xylem ingestion has been reported to increase in number and duration in various situations, i.e., after periods of starvation in apterous aphids (Spiller et al., 1990; Ramírez & Niemeyer, 2000), after the teneral period in alate aphids (Powell & Hardie, 2002), and as a response to parasitism (Ramírez et al., 2006). This xylem sap ingestion enhancement is generally associated to a mechanism of rehydration. Najar-Rodriguez et al. (2007a,b) distinguished between direct and indirect effects of mineral oil on Aphis gossypii (Glover) on cotton. In our experiment, nymph survival was significantly reduced on oil-treated plants, suggesting either a direct toxicity of the treated plant or an indirect effect. Najar-Rodriguez et al. (2007b) suggested that aphids may die from starvation due to feeding deterrence. An indirect effect due to anti-feedant property of mineral oil was also found in adult M. persicae as the first probe was significantly delayed (Powell et al., 1998). However, in our experiments the first probe was not delayed and phloem ingestion was not altered. Although nymph survival was negatively affected on treated plants, surviving adults showed higher reproductive success. A shorter pre-reproductive period, enhanced longevity, and enhanced fecundity led to a higher reproductive rate. These results could be linked to an increase in xylem sap feeding duration (almost doubled) added to an unchanged phloem sap feeding duration that was observed on oil-treated plants. Xylem sap, which contains nutrients such as amino acids, organic acids, and sugars, is the main food source for some Hemiptera such as cicadellids (Andersen et al., 1989). Then, increased xylem ingestion could enhance the total amount of nutrients ingested by aphids on oil-treated plants. Under our experimental conditions, the mineral oil treatment clearly induced both a toxic and a probiotic effect. These opposite physiological effects (higher mortality of the nymphs and better fitness of the adults) due to mineral oil treatment can be related to the hormesis concept defined by Cohen (2006). He used the term hormesis to describe a phenomenon where exposure to high levels of stressors (such as pesticides) is inhibitory, whereas low (mild, sublethal, and subtoxic) doses are stimulatory. Exposure to oil-treated plants shortly after treatment could be regarded as an exposure to a high dose of a toxic product (during the nymphal stage), whereas an exposure delayed in time (during the adult stage) could be regarded as an exposure to subtoxic doses. Tan et al. (2005) suggested that after spraying, mineral oil moves in various plant cells and tissues (including phloem and xylem), which probably induces a decrease of the local concentration of the oil at the surface of the plant. Furthermore, petroleum oil applications have been known for a long time to induce physiological changes in the plant, such as alteration of respiration and photosynthesis (Helson & Minshall, 1951; Wedding et al., 1952). Mineral oil spray
6 82 Ameline et al. has been shown to trigger the expression of genes involved in plant defence mechanisms, such as genes encoding thaumatin-like proteins, which are pathogenesis-related proteins (Lin et al., 1996). Oleic acid, which is present in the emulsifier of the Finavestan EMA Ò formulation, could be involved in the expression of genes regulating defence signalling pathways induced by stress. Indeed, studies on Arabidopsis thaliana (L.) Heynh. have demonstrated that oleic acid could play a determinant role in inducing salicylic acid- and jasmonic acid-mediated signalling pathways (Kachroo et al., 2001). Tan et al. (2005) also suggested that the accumulation of mineral oil within plant tissues may induce some phytotoxic effects (loss of vigour, leaf and fruit drop, and reduced flowering and fruit set) by blocking translocation of metabolites and nutrients. The observed modifications of aphid behaviour and demography may be linked to such plant physiological changes. It may be possible that oil changed the distribution of nutrients in favour of feeding aphids, explaining the probiotic effect observed in aphids. Moreover, oil takes time to enter phloem tissue and then remains long (Tan et al., 2005). This could explain the main effects observed 7 days post-treatment in our EPG experiment. In our demographic study, the probiotic effect was visible after the pre-reproductive period of aphids (8 9 days posttreatment). Under our experimental conditions, the antagonistic effect of oil plant treatment on aphid nymphal and adult stages could explain the unchanged aphid population densities in the fields. However, the variations in aphid behaviour and reproductive rate cannot explain the 7-days protection against virus transmission observed in the fields. Indeed, the repulsive effect due to oil treatment is only observed shortly after treatment, and the lethal effect is only observed during the early stages of aphid development, whereas surviving adults perform better. Moreover, there was no modification of the superficial brief probes (potential drops), of which the subphases are linked to non-persistent virus transmission (Martin et al., 1997). Other mechanisms, such as direct intoxication of aphids by oil treatment, could play a role in the reduction of virus transmission (Gibson & Cayley, 1984; Martin-Lopez et al., 2006; Najar-Rodríguez et al., 2008). These oils are also believed to alter the surface structure of aphid stylets and thus interfere with their ability to retain virus particles and hence reduce transmission efficiency (Wang & Pirone, 1996). Our study showed that mineral oil plant treatment could modify the major steps of the host colonisation process of an insect vector of a phytovirus. Work is underway to investigate whether mineral oil treatment also modulates the activation of defence signalling pathways in plants. Such information would be valuable for the general understanding of the impact of mineral oil application on the aphid plant virus system. Acknowledgements The work was supported by the Ministère Français de la Recherche and the Comité Nord Plants de Pommes de terre. We thank Y. Rahbé (INRA, Villeurbanne, France) for providing the Macrosiphum euphorbiae clone and the Comité Nord Plants de Pommes de terre for providing the potato tubers. We thank Sébastien Dugravot for his valuable comments on the research questions. Andrew Roots and Charles Vincent are thanked for critical reading of the manuscript especially concerning the English language. References Ameline A, Couty A, Martoub M & Giordanengo P (2009) Effects of mineral oil application on the orientation and feeding behaviour of Macrosiphum euphorbiae (Homoptera: Aphidae). 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8 84 Ameline et al. by fluorescence and confocal microscopy. Journal of Experimental Botany 56: Taverner P (2001) Drowning or just waving? A perspective on the ways petroleum-derived oils kill arthropods pests of plants. Spray Oils Beyond 2000 (ed. by GAC Beattie, DM Watson, ML Stevens, DJ Rae & RN Spooner-Hart), pp University of Western Sydney, NSW, Australia. Tjallingii WF (1988) Electrical recording of stylet penetration activities. Aphids, Their Biology, Natural Enemies and Control (ed. by AK Minks & P Harrewijn), pp Elsevier Science, Amsterdam, The Netherlands. Tripathi AK, Prajapati V, Aggarwal KK, Khanuja SPS & Kumar S (2000) Repellency and toxicity of oil from Artemisia annua to certain stored product beetles. Journal of Economical Entomology 93: Wang RY & Pirone TP (1996) Mineral oil interferes with retention of tobacco etch potyvirus in the stylets of Myzus persicae. Phytopathology 86: Wedding RT, Riehl LA & Rhoads WA (1952) Effect of petroleum oil spray on photosynthesis and respiration in citrus leaves. Plant Physiology 27: Will T, Tjallingii WF, Thönnessen A & van Bel AJE (2007) Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences of the USA 104:
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