Opposite effects of different mineral oil treatments on ... - Springer Link

J Pest Sci (2011) 84:229–233 DOI 10.1007/s10340-010-0344-z

ORIGINAL PAPER

Opposite effects of different mineral oil treatments on Macrosiphum euphorbiae survival and fecundity Maria Martoub • Aude Couty • Philippe Giordanengo Arnaud Ameline

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Received: 10 August 2010 / Accepted: 25 November 2010 / Published online: 9 December 2010 Ó Springer-Verlag 2010

Abstract Mineral oil has been considered for several decades as an effective mean to control aphids and reduce the spread of non-persistent viruses. Mineral oil seems to reduce virus transmission efficiency interfering with the binding of the virions in the aphid stylets. However, several studies have shown the possible disruption of host selection process by mineral oil and some works have demonstrated a direct effect on the aphid vector. In this study the insecticidal properties of mineral oil (Finavestan EMA) alone against Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae) were evaluated through the three main routes of exposure (topical contact, inhalation and ingestion). Results showed that no aphid survived after topical contact at oil concentrations ranging from 3 to 100% v/v. However, surprisingly, at a lower concentration (0.3%), survival was not affected but fecundity was enhanced. Moreover, exposure to oil volatiles enhanced aphid survival at the highest concentrations (30 and 100%) and daily fecundity at the lowest ones (0.3 and 3%). Delivered via artificial diet, mineral oil only affected aphid survival at the 0.3% concentration. This study demonstrates that mineral oil alone, regardless of a potential plant effect can induce either probiotic effects or toxic effects, depending on the mode of application and the concentration tested. These results can be of significance for the understanding of mineral oil properties in the fields.

Communicated by B. Freier. M. Martoub A. Couty P. Giordanengo A. Ameline (&) Unite´ de Recherche EA3900—BioPI, Biologie des Plantes et Controˆle des Insectes Ravageurs (UPRES EA 3900), Laboratoire de Biologie des Entomophages, Universite´ de Picardie Jules Verne, 33 rue Saint Leu, 80039 Amiens Cedex, France e-mail: [email protected]

Keywords Aphid Hemiptera Aphididae Probiotic Artificial diet

Introduction For several decades, application of mineral oil sprays to plants has been considered as the most effective method to control non-persistent viruses in the field (Bradley et al. 1962, 1966; Simons et al. 1977; Hooks and Fereres 2006). The exact mechanism underlying this preventive effect remains unclear but seems to result from an inhibition of the virus transmission by the aphid vector. Wang and Pirone (1996) suggested that the main mechanism through which mineral oil reduces virus transmission efficiency relies on the alteration of the binding of the virions in the aphid stylets. Several studies have also shown the possible disruption of the host selection process by mineral oil. Ameline et al. (2009, 2010) showed that Macrosiphum euphorbiae orientation behaviour towards an oil-treated plant was modified (by a repellent or a masking effect). Concerning the aphid host-acceptance step, several studies on Myzus persicae showed that mineral oil may alter the activities of the stylets as they penetrate the plant surface: delay in the initiation of a first probing was reported by Simons et al. (1977), reduction in the occurrence of stylet punctures of epidermal cells membranes was shown by Powell (1991, 1992) and Ameline et al. (2009, 2010) showed that M. euphorbiae increased its xylem sap consumption on treated plants. Thus, plants may be actively protected because of the indirect effect of oil treatment (1) by interfering with the binding of viral particles to the mouthparts of the aphid and (2) by modifying host-plant selection processes. However, direct effect on aphids could also occur after crop mineral

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oil sprays, regardless of potential interactions between the oil and the plant. The commonly acknowledged theory concerning the mode of action of mineral oil is that it primarily kills arthropods by suffocation (anoxia) (NajarRodrı´guez et al. 2008). In this paper a bioassay was performed on the mineral oil to determine its insecticidal properties against Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae), which is an important virus vector of potato plants Solanum tuberosum L. (Blackman and Eastop 2000), through the three main routes of exposure (inhalation, topical contact and ingestion).

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performed in ultrapure water for topical contact and inhalation bioassays and in artificial diet for the ingestion bioassay. Eight replicates were carried out for each treatment. Topical contact 0.1 ll of oil solution or ultrapure water as control was applied on the abdomen of aphids with an Ependorff micropipette (0.1–2.5 ll). Aphids were then immediately transferred to oil-free feeding chambers. Inhalation

Materials and methods Insects The Macrosiphum euphorbiae (Thomas) colony was initiated from a single apterous parthenogenetic female from the clone Me LB05 (INRA-INSA, Villeurbanne, France). Aphids were reared on potato plants Solanum tuberosum L. (cv De´sire´e) raised in a growth room maintained at 20 ± 1°C under a photoperiod of L16:D8. Young adults (\24 h) were used for experiments. They were obtained from fourth instar larvae raised for 2 days on standard artificial diet in feeding chambers. A standard artificial diet, diet sachets and feeding chambers were prepared as described by Febvay et al. (1988) and modified by Down et al. (1996). Diet sachets containing 100 ll of artificial diet were changed every 48 h. Mineral oil The highly refined mineral oil, Finavestan EMAÒ (Total Fluides, Paris, France), is a mixture of nC15 to nC37 hydrocarbons (C15–C21 = 13.7%; C22–C27 = 66.4%; C28–C37 = 19.8%). Its active constituent is 807 g/l paraffin oil, with a 99.8% unsulfonated residue. A mixture of ethoxylates of fatty alcohols and oleic acid was used as emulsifier. The recommended field concentration is 3% volume/volume (v/v) solution. Mineral oil application procedure Three modes of exposure were tested on aphids: topical exposure, inhalation and ingestion. Five aphids were isolated in each feeding chamber and survival and fecundity were recorded daily for 7 days. Different oil concentration ranges were tested according to the mode of exposure: 0.3, 3, 30% v/v and pure formulation (100%) for topical contact and inhalation bioassays; 0.3, 0.03 and 0.003% v/v for the ingestion bioassays. Dilutions were

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Filter paper discs (diameter: 3 cm) were soaked with 25 ll of oil solution or ultrapure water as control. They were then covered with nylon mesh to prevent aphid contact and placed below the oil-free feeding chambers. Ingestion Artificial diet (details given above) added with oil or oilfree as control was delivered to the aphids. The sachets were renewed every second day until aphid death. Statistical analysis The Pearson’s v2 test (Yate’s correction) was performed to analyze mineral oil effects on aphid survival. Daily fecundity of treated aphids was compared pair-wise with that of control aphids by a non-parametric Mann–Whitney U-test. Statistical analyses were performed using Statistica (V. 5.5; Statsoft, Tulsa, USA). Results are reported as mean ± standard error of the mean (SEM).

Results Topical application One day post-treatment, no aphid survived (Fig. 1a) and no nymphs were laid at the three highest mineral oil concentrations (3, 30 and 100%, Fig. 1b). At the lowest concentration (0.3%, Fig. 1a), M. euphorbiae survival was not affected (v2 = 0.02, d.f. = 7, P = 0.88) and its fecundity (Fig. 1b) was significantly enhanced in comparison to control (U = 29.5, P \ 0.05). Inhalation Aphid survival (Fig. 2a) was not altered at the 0.3 or 3% concentrations (v2 = 0.51, d.f. = 7, P = 0.48; v2 = 0.51, d.f. = 7, P = 0.48; respectively) and was significantly

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b

Adults survival (%)

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Means (±standard error of the mean) associated to an asterisk indicate a significant difference from control situation (P \ 0.05)

Daily fecundity (nymphs per female per day)

Fig. 1 Effect of topical application of mineral oil at different concentrations (0.3, 3, 30 and 100% v/v) on a the survival (%) of M. euphorbiae adults and on b the fecundity of surviving aphids.


a

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1,6

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Fig. 2 Effect of exposure by inhalation of mineral oil at different concentrations (0.3, 3, 30 and 100% v/v) on a the survival (%) of M. euphorbiae adults and on b the fecundity of surviving aphids.


enhanced at the two highest concentrations (30%: v2 = 7.9, d.f. = 7, P \ 0.05; 100%: v2 = 4.50, d.f. = 7, P \ 0.05) in comparison to control. Aphid fecundity (Fig. 2b) was significantly increased at the lowest concentrations (0.3%: U = 7, P \ 0.05; 3%: U = 9, P \ 0.05) in comparison to control but was not affected at the two highest ones (30%: U = 10, P = 0.064; 100%: U = 14.5, P = 0.201).

U = 28, P = 0.27; 0.03%: U = 35, P = 0.63; 0.3%: U = 39, P = 0.89).

Ingestion Aphid survival (Fig. 3a) was only affected at the highest concentration tested (0.3%: v2 = 7.36, d.f. = 7, P \ 0.05) and not modified at the two lowest concentrations (0.003%: v2 = 0.09, d.f. = 7, P = 0.77; 0.03%: v2 = 1.37, d.f. = 7, P = 0.24). Figure 3b shows that, whatever the concentration, mineral oil did not affect aphid fecundity (0.003%:

Discussion This work shows that depending on the mode of exposure and the concentration tested, mineral oil has different effects on aphids and interestingly some opposite effects were observed on aphid survival and fecundity. Mineral oil strongly altered aphid survival when delivered through topical contact since no aphid survived when exposed to a concentration equal to or higher than the one recommended for field application (i.e. 3% v/v). Such insecticidal properties of mineral oils via topical contact have been reported (Agnello 2001). Several hypotheses

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J Pest Sci (2011) 84:229–233

b

Adults survival (%)

100

80

Control

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0.003 % 0.03 % 0.3%

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40 1

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8


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1,6

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0.003%

0.03%

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Fig. 3 Effect of ingestion of mineral oil via artificial diet at different concentrations (0.003, 0.03, 0.3% v/v) on a the survival (%) of M. euphorbiae adults and on b the fecundity of surviving aphids.


have been put forward to explain oil toxicity, among which the obstruction of the spiracles, leading to death by suffocation, has long been considered as the main mechanism. However, the rapid knock-down effect coupled to severe dehydration symptoms observed following direct application of petroleum oil was not due to suffocation as anoxia may take hours to kill insects (Najar-Rodriguez et al. 2007a). Further investigations by Najar-Rodrı´guez et al. (2008) led to the conclusion that some petroleum mineral oils (nC24) induced death through cellular disruption in relation to their lipophilic properties. In our experiments, aphid death was observed within minutes after oil application, long before the first 24 h checkpoint. Moreover, the Finevastan formulation is mostly composed of nC22–C27 hydrocarbons, suggesting that Finavestan toxicity could be due to cellular disruption. Strikingly, exposure to Finevastan volatiles induced probiotic effects depending on the dose used. The highest concentrations (30% and pure oil) increased aphid survival and the lowest ones (0.3 and 3%) increased fecundity. In a previous study (Ameline et al. 2010) we showed that M. euphorbiae fed on plants sprayed with a 3% Finavestan solution showed increased fecundity. This probiotic effect was attributed to plant physiological changes induced by oil treatment. Oleic acid, a component of the emulsifier present in the Finavestan EMAÒ formulation, could have been involved in the expression of genes regulating defence signalling pathways induced by stress (Kachroo et al. 2001). However, in this study, aphids were fed an artificial diet and were not tested on whole plants. Therefore, the observed probiotic effect can only be triggered by volatiles emitted by the mineral oil. Previous studies have also shown that volatile semiochemicals involved in plant defence responses can modify

aphid physiology. Volatile compounds from young tomato leaves (mainly aliphatic aldehydes, hexanal and 3-hexanal) can reduce Myzus nicotaniae fecundity (Hildebrand et al. 1993). The works by Vancanneyt et al. (2001) suggest that the better performance of M. persicae observed on HPLdepleted transgenic potato plants (modified in their hydroperoxide lyase activity) resulted from a reduction in aldehyde levels present in these plants. Interestingly, a probiotic effect was also observed after topical application at the lowest concentration (0.3%) that led to enhanced aphid fecundity. Again, volatiles from the oil droplet deposited on the aphid abdomen could be partly responsible for such an effect. This is the first time vapours of mineral oil are reported to improve aphid fecundity (or reproduction). Mineral oil had a direct toxic effect on aphids via the ingestion route, even at concentrations ten and a hundred times lower than the recommended field dose. These concentrations were chosen to take into account the likely dilution phenomenon of the oil after plant spray in the field. Indeed Tan et al. (2005) showed that mineral oil could be detected in all parts of the plant, including phloem vessels, after mineral oil was sprayed on mature orange trees. Aphicidal properties of mineral oils have previously been shown on aphids feeding on treated plants (Ameline et al. 2010; Martin-Lopez et al. 2006; Najar-Rodriguez et al. 2007a, b). In this work, we demonstrate that this oral toxicity can be attributed to the effect of the oil alone regardless of a potential plant effect. In the field, sprayed mineral oils have been shown to efficiently control the spread of non-persistent viruses. This effectiveness could be due to a direct effect on the virus– aphid stylet interactions (Wang and Pirone 1996), an

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J Pest Sci (2011) 84:229–233

alteration of the aphid host-selection behaviour (Ameline et al. 2010), or to a direct intoxication of the aphid by the oil (Najar-Rodriguez et al. 2007a, b). Our study reveals unexpected probiotic effects following oil inhalation which may compensate for the aphicidal properties of the oil via ingestion or topical contact. This is in accordance with field observations where aphid population levels do not seem to be affected by the oil treatment (Riquiez, pers. comm.). The effectiveness of mineral oil in controlling non-persistent viruses spreading in the field cannot be explained by a regulation of the vector populations. This is why mineral oil may be of particular interest when used in combination with commonly used insecticides such as pyrethroids (Collar et al. 1997; Gibson and Rice 1986) or plant-derived antifeedants (Powell et al. 1998). Finding the best combination between mineral oil and other insecticides in the context of integrated pest management (IPM) opens a very interesting new field of investigation. Acknowledgments The work was supported by the Ministe`re Franc¸ais de la Recherche, the Comptoir Commercial des Lubrifiants and the Comite´ Nord Plants de Pommes de terre. We thank Y. Rahbe´ (INRA, Villeurbanne, France) for providing the M. euphorbiae clone and the Comite´ Nord Plants de Pommes de terre for providing the potato tubers. Andrew Roots is thanked for advice on the use of the English language in the paper.

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