Passive Adsorption of Volatile Monoterpene in Pest Control: Aided by

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Passive adsorption of volatile monoterpene in pest control: aided by proximity, disrupted by ozone Adedayo O. Mofikoya, Tae Ho Kim, Ahmed M. Abd El-Raheem, James D. Blande, Minna Kivimäenpää, and Jarmo K. Holopainen J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b03251 • Publication Date (Web): 09 Oct 2017 Downloaded from http://pubs.acs.org on October 11, 2017

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Journal of Agricultural and Food Chemistry

Passive adsorption of volatile monoterpene in pest control: aided by proximity, disrupted by ozone

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Adedayo O. Mofikoya1*, Tae Ho Kim1, Ahmed M. Abd El-Raheem1,2, James D. Blande1, Minna

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Kivimäenpää1, Jarmo K. Holopainen1.

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1672, 70211, Kuopio, Finland.

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University, Shebin EL-Kom, P. O. Box 32514, Egypt.

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*Corresponding author

Department of Environmental and Biological Sciences, University of Eastern Finland, P. O. Box

Department of Economic Entomology & Agricultural Zoology, Faculty of Agriculture, Menoufia

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Email: [email protected]

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Phone number: +358449884290

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Abstract

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Plant volatiles mediate a range of interactions across and within trophic levels, including plant-to-

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plant interactions. Volatiles emitted by a plant may trigger physiological responses in neighbouring

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plants or adhere to their surfaces, which may in turn affect the neighbouring plant’s responses to

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herbivory. These volatiles are subject to chemical reactions during transport in air currents,

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especially in a polluted atmosphere. We conducted a field experiment to test for the adsorption of

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dispenser-released myrcene on the surfaces of cabbage plants, and the effects of distance from the

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dispenser and elevated ozone levels (1.4 x ambient) on the process. We also tested the effects of the

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same treatments on oviposition on cabbage plants by naturally occurring Plutella xylostella. Under

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low ambient ozone conditions of central Finland, there was evidence for the adsorption and re-

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release of myrcene by cabbage plants growing at a distance of 50cm from myrcene dispensers. This

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effect was absent at elevated ozone levels. The number of eggs deposited by P. xylostella was

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generally lower in plots under elevated ozone compared to ambient control plots. Our results

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indicate that passive adsorption and re-release of a volatile monoterpene can occur in nature;

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however, this process is dependent on distance between emitter and receiver plants as well as the

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concentration of atmospheric pollutants in the air. We conclude that in the development of field

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scale use of plant volatiles in modern pest control, the effects of distances and air pollution be

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considered.

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Keywords: Brassica oleracea, Volatile organic compounds, ozone, Plutella xylostella, myrcene,

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plant-to-plant interactions, adsorption, pollution.

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1. Introduction

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Volatile organic compounds (VOCs) emitted by plants are involved in a number of ecological and

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atmospheric processes.1 The emission of these volatile compounds can be constitutive or induced by

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mechanical damage, herbivore feeding, oviposition and abiotic environmental stresses.2-6 Plants use

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VOCs in both direct and indirect defence against herbivores. Direct defence involves the deterrence

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of feeding or oviposition, whereas indirect defence involves the attraction of natural enemies of

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herbivores.7,8 VOCs are also mediators of plant-to-plant interactions and within plant signalling.9-11

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The mode of action of volatile mediated plant-to-plant interactions can be either active or passive.

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Active interactions require the VOCs released by an emitter plant to trigger a physiological

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response in the receiver plant, whereas passive interactions involve volatiles released by emitter

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plants adsorbing to the surfaces of neighbouring plants.1 Active and passive processes may structure

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interactions that result in significant ecological effects.12,13

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The roles of VOCs in pollination, herbivore foraging and plant-to-plant interactions is dependent

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upon transport in air currents.14-17 For example, induced resistance in tobacco mediated by volatiles

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from clipped sagebrush neighbours is restricted when there is no air contact between the two

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plants.9

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where they occur as intermittent odour strands of high volatile concentrations interspersed by

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volatile free pockets.18-20 The intermittency of a volatile signal is dependent on release rate, air

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turbulence and the distance between the volatile plume and the source.21 The presence of reactive

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compounds such as ozone in the atmosphere may also degrade or change the blend of volatile

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compounds and subsequently affect the ecological processes they mediate.13,22 VOCs have varying

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atmospheric lifetimes ranging from as low as half a minute to several days.23 These lifetimes are

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dependent on chemical properties such as the number of C=C double bonds in the compound as

Volatiles disperse from their point source by diffusion and turbulent motion in the air



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well as the concentration of oxidizing agents in the atmosphere.24,25,1 VOCs in the atmosphere can

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either be removed or transformed via wet and dry deposition, photolysis, or by reacting with

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hydroxyl (OH) or nitrate (NO3) radicals, and ozone (O3).26

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Tropospheric ozone degrades terpenes and green leaf volatiles (GLVs), which are key compounds

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in plant-to-plant and plant-insect interactions.27-29 The concentration of ozone in the troposphere

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varies based on region and is projected to increase in the coming decades due to climate change.30

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Increasing ozone levels reduced the effective distance of active plant-to-plant communication in

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lima bean.31 Ozone affects the ability of neighbouring plants to detect volatiles or degrades

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adsorbed volatile compounds on neighbouring plant surfaces in passive interactions.12

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degradation of volatiles by ozone disrupts host location in Plutella xylostella larvae and oviposition

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by their adults.32,12,13 Hence, volatile-based plant-to-plant interactions are dependent on the

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concentrations of ozone in the atmosphere both in natural and agricultural systems.

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Dispenser released volatiles are commonly used to manipulate arthropod behaviour in forest and

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agricultural systems.33,34 Controlled release of methyl salicylate from sticky cards and slow

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releasing dispensers have been used for pest control strategies in grape and hop yards.35,36 A

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mixture of monoterpenes released from a dispenser reduced carrot psyllid damage in carrot crops37

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and dispenser-released myrcene along with other pheromone components was also used for the

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attraction of western pine beetle in a forest ecosystem.38 In a Belgian wheat field, slow-release of a

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GLV, (Z)-3-hexenol was successfully used to attract aphids, while employment of the sesquiterpene

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(E)-β-farnesene reduced aphid numbers by recruitment of aphid natural enemies to the wheat

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plots.39

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Myrcene is emitted by a wide variety of plants, including brassicaceous species, and in relatively

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high quantities by Rhododendron tomentosum

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tomentosum adsorb to surfaces of neighbouring plants and makes them less susceptible to

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herbivory.41,

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The

; some semivolatile compounds from R.

Myrcene is one of the most reactive monoterpenes in the atmosphere due to its 4 ACS Paragon Plus Environment

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acyclic nature and presence of three double bonds

; its reactions with ozone and OH radicals

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produce secondary compounds and SOA particles.43 The atmospheric lifetime of myrcene can be

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significantly shortened in atmospheres with high ozone levels.44 Birch trees growing in close

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proximity with R. tomentosum in boreal and subarctic environments had higher emissions of

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myrcene compared to trees growing without R. tomentosum neighbours (private communication).

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This suggests that given the right conditions, there is the possibility of uptake or adsorption and re-

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emission of VOCs by neighbouring plants.

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In this study, we investigated the effects dispenser-released myrcene on the volatile profile of

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cabbage plants. We also tested the effect of distance between plants and dispenser and elevated

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ozone concentration on the re-emission of myrcene. The effects of myrcene and ozone treatment on

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natural oviposition by P. xylostella was also tested. This study centred around four main

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hypotheses: a) dispensed myrcene adsorbs to the surface and is rereleased by neighbouring cabbage

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plants, b) adsorption and re-emission is dependent on distance between emission source and

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receiver, c) ozone breaks down the process of myrcene adsorption d) myrcene and ozone treatment

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affects P. xylostella oviposition on cabbage plants.

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2. Materials and Methods

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2.1. Plant Material

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Brassica oleracea convar. capitata var. alba Jetma RZ (white cabbage) seeds were sown in 1-L

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pots in a substrate mixture of peat, sand and mull (3:1:1). Plants were watered daily and fertilized

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once a week with 100ml of 0.1% solution of nitrogen, phosphorus and potassium (19-4-20) (Taimi

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Superex, Kekkilä Oyj, Eurajoki, Finland). They were grown in plant growth chambers (75 cm W;

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128 cm L; 130 cm H) (Weiss Bio 1300; Weiss Umwelttechnik Gmbh, Reiskirchen-Lindenstruth,

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Germany) [Day 16 h (photosynthetically active radiation 300 µmol-2 s-1), 23 °C, 60% humidity:

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Night 8 h dark, 18 °C, 80% humidity] for 5 weeks prior to the start of field experiments. 5 ACS Paragon Plus Environment


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2.2. Experimental Plan

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A field experiment was conducted in the Ruohoniemi open-air ozone exposure field of the

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University of Eastern Finland, Kuopio campus (62° 53´ 42´´ N, 27° 37´ 30´´E) between 30th June

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and 15th July 2016. The first field exposure was between 30th June and 7th July 2016 and the

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experiment was repeated between the 8th and 15th July 2016. The exposure field consisted of eight

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circular plots (Ø 9 m); four had elevated ozone levels and the other four had ambient ozone levels

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(control). Both ambient and elevated ozone plots were divided into plots with and without myrcene

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treatment. The plot treatments were; ambient ozone (A), ambient ozone with myrcene treatment

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(AM), elevated ozone (O), and elevated ozone with myrcene treatment (OM) (n=2, for each

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treatment in both exposures). Myrcene treatments within ambient and elevated plots were

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interchanged for the second field exposure. There was a mean distance of 28m between the plots

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and the minimum distance between two plots was 18m, as described in Karnosky et al. (2007)45.

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Ozone was produced from pure oxygen by an ozone generator (Pacific G22, Pacific Ozone

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Technology Inc., Benicia, CA, USA), and released via computer-controlled valves (Hoke

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2315G4Y, Hoke Inc., Spartanburg, SC, USA) into the plots through vertical perforated pipes. Each

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plot was surrounded by 40 of these pipes in 8 units each having 5 pipes. Ozone was released from

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20 upwind side pipes at a time until the main wind direction changed. Then the next 20 pipes best

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fitting the main wind direction were selected for ozone release. Elevated ozone plots had an average

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ozone level of 42 ppb during the experiment; in ambient plots, the ozone concentration averaged 29

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ppb (Figure 1). The highest hourly ozone concentration measured during the course of the

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experiment in the elevated ozone plot was 116 ppb. Six 5-week old white cabbage plants were

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placed at three distances (0.5 m, 1.5 m and 3 m) to the east and the west of the centre of each plot

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(Figure 2a). Myrcene dispensers (Figure 2b) were placed at the centres of two of the ambient ozone

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plots and two of the elevated ozone plots, the remaining plots had no dispenser. Ozone exposure

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was from 8:00 to 22:00 daily, and exposure automatically stopped when ambient ozone levels were 6 ACS Paragon Plus Environment

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below 10ppb, during high or low wind speeds, and when it rained. Ozone analysers (Dasibi 1008-

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RS, AMKO Systems Inc., ON, Canada and Environnement S.A O342M, Environnement S.A,

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Poissy, France) connected to the centres of the plots by Teflon tubes were used to continually

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measure ozone levels at a height of 1.5m during the course of the experiments. Wind direction and

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speed during the experimental period was collected from the Finnish meteorological institute (FMI)

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station in Savilahti, Kuopio.

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2.3. Myrcene Dispenser

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Five ml of 90% myrcene (Sigma Aldrich, 3050 Spruce Street, Saint Louis, MO 63103, USA) was

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pipetted into a glass tube (10 ml, 52 mm long X 13 mm Inner Diameter). The opening of the tube

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was sealed with a Teflon cap and a Teflon capillary tube (70 mm long X 3.5mm ID) was inserted.

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The structure was placed in a 1L glass jar and a lid complete with inlet and outlet Teflon tubes

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attached. Filtered air was passed into the glass jar at a rate of 1.2 L min-1 and a T-tube was attached

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to the outlet tube directing the air flow towards the east and west positioned plants (Figure 2b).

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During the course of the experiment, samples were collected from the release point of the dispenser

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at a flow rate of about 200 ml min-1 for 5 minutes to measure the myrcene release rate (0.34 ± 0.002

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mg h-1, mean ± SE, n =8). Air samples were also collected at distances of 50 cm and 100 cm from

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the dispenser to measure the myrcene concentration in the air. All samples were collected in

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stainless steel tubes filled with 200 mg of Tenax-TA mesh 60/80 (Supelco, Bellefonte, PA, USA)

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adsorbent tubes.

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2.4. Volatile Sampling and Analysis

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After exposure in the field, plants were moved to the cold room (4 ˚C) to reduce re-emission of

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adsorbed compounds and then to the lab in batches of six for collection of volatiles and counting of

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P. xylostella eggs and neonate larvae. We collected volatiles using the dynamic headspace

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technique; each potted plant was covered with aluminium foil and enclosed in a PET (polyethylene 7 ACS Paragon Plus Environment


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terephthalate) cooking bag (35 x 43 cm), which had been pre-cleaned at 120 °C for a minimum of

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an hour. We made a hole at the top of the bag through which filtered air was passed via Teflon

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tubing at a flow rate of ≈ 350 ml min-1 for 10 minutes to clean the system. A Tenax tube was

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attached to a second hole in the bag and connected to a suction pump that pulled the plant

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headspace air through the tube at approx. 200 ml min-1 for 20 minutes. The inlet and suction air was

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calibrated with a mini-Buck calibrator (Model M-5, A.P.Buck Inc., Orlando, FL., USA). Tenax

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tubes were stored at 4 ˚C before analyses. Volatile analyses were conducted by GC-MS (Gas

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Chromatography-mass Spectrometry, MSD 5973, Hewlett Packard GC type 6890, Wilmington, DE,

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USA). The compounds were desorbed at 250 °C for 20 minutes, cryofocused at -30 °C by an

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ATD400 automatic thermal desorption system (Perkin-Elmer Ltd., Waltham, MA, USA) and

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injected into an HP-5 capillary column (50 m length × 200.0 µm diameter× 33.0 µm film thickness),

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72.4 kPa pressure, 7cm sec-1 average velocity, with helium as the carrier gas. The oven was

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programmed with an initial temperature of 40 °C for 1 minute. The temperature was raised to 210

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°C at a rate of 5 °C min-1 and reached 250 °C at a rate of 20 °C·min-1. The compounds (Terpenes

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and GLVs) were identified by comparing their mass spectra and retention time with those in the

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Wiley and NIST libraries and with pure standards. The emission rates were expressed in ng g-1 h-1.

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The cabbage plants were oven-dried at 60 °C for 72 h and weighed after inspection for oviposition

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by P. xylostella.

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2.5. Egg Counting

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After volatile collection, eggs and neonate larvae on the leaves were counted under a microscope

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(Nikon SMZ800 Zoom stereo, Nikon Corporation, Tokyo, Japan). The P. xylostella egg is oval

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shaped with a shiny yellow colour and a length of < 0.5 mm. We used the sum of eggs and neonate

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larvae on plant leaves to estimate the oviposition level. As egg development takes an average of 5 to

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6 days46 and our experiments lasted 7 days in the field, the neonate larvae observed were considered


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to have emerged from eggs laid early in the experiment and hatched before the counting was

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initiated.

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2.6. Statistical Analyses

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Data from both field experiments were pooled and a linear mixed model ANOVA was used to study

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the main and interactive (2 to 4 way) effects of myrcene exposure, ozone enrichment, distance from

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the myrcene dispenser and direction of the plants (east / west) on leaf myrcene emission and

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number of eggs and neonate larvae on the leaves. Myrcene exposure, ozone level, distance between

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plants and dispenser and orientation of the plants (east / west) were fixed factors while plot number

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and exposure number were set as random factors. Simple main effects (SME) with Bonferroni

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corrections were used to further study significant 2 to 4-way interactions. The significance level for

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interactions was set at P ≤ 0.1, as used for a similar open field exposure experiment.47

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SMEs, significance level was set at P = 0.05. The independent sample t-test was used to compare

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myrcene concentration in AM and OM plots.

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For the

3. Results

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Ozone, myrcene and distance had a statistically significant effect on myrcene emission rate from

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cabbage plants (Table 1). Plants closest to the dispenser (0.5 m) in AM plots had higher emission

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rates of myrcene than plants growing further away; 1.5 m and 3 m (Table 2 Figure 3). Plants at a

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distance of 0.5 m from myrcene dispensers in AM plots also had higher myrcene emission rates

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than plants at the same distance in A plots (Figure 3, Table 2). At 0.5m distance, plants in OM plots

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had lower myrcene emission rates than plants in AM plots (Figure 3, Table 2), but not in the 1.5 m

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and 3 m distances. Myrcene concentrations in the air in AM plots were significantly higher than the

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concentrations in OM plots at 0.5 m from the dispenser (Figure 4), but there was no detectable

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concentration of myrcene in the air at further distances (1.5 m and 3 m) and in A and O plots.



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Myrcene treatment, plant direction and distance from dispenser also had an interactive effect on

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myrcene emissions (Table 1). Myrcene treatment increased the emission of myrcene by plants at

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distances of 0.5m and 3 m from the myrcene dispenser in the western direction (Table 2). For plants

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in the eastern direction, myrcene treatment increased myrcene emission rate by plants at a distance

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of 0.5 m (Table 2). Wind direction during the field experiment was more frequently easterly in the

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course of our experiments; mean wind direction was 263˚ (Figure 5).

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Ozone, myrcene, direction and distance had an interactive effect on the number of eggs and neonate

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larvae on cabbage plants (Table 1). SME tests showed that the number of eggs and larvae was lower

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on plants at a distance of 3 m from the centre of elevated ozone plots than ambient ozone plots

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(Table 2).

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Discussion

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3.1. Myrcene Adsorption and Re-emission

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Adsorption and re-emission of volatiles from neighbouring plants has been reported both in field

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and laboratory studies with varying effects on herbivore responses.39,40,12 Volatiles in the air can be

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taken up by plants through the stomata or may be adsorbed to foliar surfaces and re-emitted upon

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heating.48,12 Volatile uptake and deposition from plant’s immediate surrounding is dependent on the

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concentration of the volatiles in the air as well as the volatile’s physicochemical properties.49,50

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Ambient and elevated ozone plots without dispensers had no detectable myrcene concentration in

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the air; however, the concentration in OM plots was 1.8 ng L-1 and in AM plots, 4.7 ng L-1 at a

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distance of 50cm from the dispenser. This difference in air concentrations could be due to

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ozonolysis of myrcene in OM plots as well as differences in wind speed and direction during

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collection.44 Our results show evidence of adsorption and re-emission of myrcene; plants that were

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closest to the myrcene dispenser in AM plots emitted the highest amount of myrcene. Although

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cabbage and a number of other brassicaceous plants synthesize and emit myrcene as part of their 10 ACS Paragon Plus Environment

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volatile bouquet13, the amount emitted by those closest to the dispenser in our experiment was

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higher than what has been reported in literature. Laboratory and modelling experiments have shown

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that monoterpene emitting and non-emitting species can adsorb monoterpenes such as limonene.50,51

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Hydrophobic terpenes like myrcene tend to adsorb to the cuticle layer and leaf surface wax

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from where they may diffuse into the cuticle or be re-emitted upon heating. Terpenes dominate the

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volatile constituents of wax extracts of many plant species, in pine needles, leaf waxes contained

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myrcene concentrations equivalent to 9 h emissions from intact shoots.53 Artificial leaves made of

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glass slides coated with leaf wax have also been shown to adsorb and re-emit volatile compounds.12

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Our results suggests that volatile terpenes released from a dispenser into ambient air may adhere to

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the surfaces of plants and are re-emitted during volatile sampling. This process is, however

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dependent on distance between the emitter and receiver as well as the concentration of oxidizing

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pollutants in the atmosphere.

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48,50,52

3.2. Distance Effects

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Myrcene emission rate was higher in plants at a distance of 50cm from the dispenser in ambient

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plots suggesting that adsorption of volatile monoterpenes by a plant depends on the distance

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between the emitter and receiver plants. The question of how far volatile signals can travel is

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difficult to answer, since the compounds diffuse through air and move by eddy current dispersal.54

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Abiotic factors such as wind speed and direction play important roles in the distance they travel.9

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The dominant wind direction in our experiment was from the west towards the east. In the westerly

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direction, plants at a distance of up to 3 m from dispensers had higher myrcene emission rates; this

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effect was only observed in plants at 50 cm in the easterly direction. This observation may be due to

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strong winds carrying the volatile plume beyond the plants at this distance in the easterly direction.

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Generally, good evidence for volatile-mediated plant-to-plant signalling becomes scarcer as the

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distances between plants increases.55 In European black alder trees (Alnus glutinosa), plant-to-plant

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signalling resulted in decreased herbivore damage on receiver plants, this effect was reduced in 11 ACS Paragon Plus Environment


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trees as distance between the defoliated emitter plant – which was 1m away from the closest

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receiver plant – increased.56 Plant-to-plant communication between sagebrush and wild tobacco

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plants was limited to a threshold of 15 cm and communication between sagebrush neighbours did

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not exceed 60 cm.9,57 Accumulation of non-reactive plant volatiles on the surface of neighbouring

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plants over distances of more than 5 m has been observed in nature, where species-specific

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compounds from R. tomentosum were recovered from the surfaces of neighbouring birch foliage.41

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In cases where the accumulating volatile compound is not specie-specific, i.e. both emitter and

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receiver are capable of synthesizing and releasing the same volatiles, measurement of accumulation

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and re-release of volatile compounds in nature can be ambiguous. Hence, plant volatiles measured

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in field settings may originate from neighbouring plants.

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3.3. Ozone Effects

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Increasing the background ozone level by 1.4 times resulted in a reduction in the recovery of

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adsorbed myrcene from the surfaces of cabbage plants. The elevated ozone level of 42 ppb in our

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experiment is similar to some present day average ozone concentrations in the mid-latitude of the

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Northern Hemisphere.58

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40ppb in most parts of the world and up to 70 ppb in some other regions.59 Plants growing in plots

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with elevated ozone emitted similar amounts of myrcene irrespective of myrcene treatment. This

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reduced recovery rate could have been for a number of reasons. First, the breakdown of the

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dispensed myrcene before adsorption to the nearest leaf surface. There was a significant reduction

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in myrcene concentration in the air in elevated ozone plots compared to ambient plots with a

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myrcene dispenser. This reduction may be largely due to ozonolysis in combination with other

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factors like wind speed and direction during sampling time. Myrcene also tends to have a shorter

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atmospheric lifetime under elevated ozone levels.44 Under elevated ozone levels, the concentration

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of floral monoterpenes was significantly reduced with increasing distance from the emission

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source.22 Based on our results, ozone could reduce the effective distances in passive plant-to-plant

Ozone levels are expected to hit mean monthly 24-h averages of over


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interactions, particularly in cases where the compound is highly reactive. Secondly, there is the

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possibility that some dispensed myrcene adsorbed to the surfaces of plants in the elevated ozone

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plots and were degraded within the leaf boundary layer. Volatiles synthesized by plants or

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originating from neighbouring plants may undergo degradation on plant surfaces upon exposure to

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ozone.12,60 The breakdown of these volatiles on the leaf surface may protect the plants from uptake

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of phytotoxic ozone through the stomata or lead to the formation of secondary compounds, which

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may be released into the atmosphere.60

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reaction products of myrcene from plants in the elevated ozone plots. Thirdly, ozone may affect the

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capacity of the receiver plants to adsorb myrcene by altering the cuticular wax layer of the

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plants.61,62 Taken together, our results suggest that a 40% increase in background ozone levels in

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Central Finland which represents ambient ozone levels in many regions of the world is sufficient to

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degrade myrcene in the atmosphere and/or on plant surfaces and subsequently alter the ecological

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processes they may mediate.

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In our experiment, however, we did not detect known

3.4. Effects on Oviposition

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We observed that ozone decreased the number of eggs and neonate larvae on cabbage plants in the

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eastern direction. The prevailing wind direction during the experiment was easterly, which means

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the ozone released from the perforated pipes in the plot was mostly carried in the eastern direction

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resulting in the effects of ozone being more pronounced in that area of the plot. Ozone plots also

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had 40 % less eggs and neonate larvae on cabbage plants compared to control plots irrespective of

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myrcene treatment. These observations suggest that ozone may play an important role in P.

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xylostella oviposition.13 Our work shows no strong evidence of the effectiveness of myrcene in

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herbivore control. Myrcene application in plant pest control is usually done as part of a chemical

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bouquet rather than an individual component.63-66 These results suggests that myrcene effectiveness

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in herbivore control may be more pronounced as part of a volatile bouquet rather than as a single

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compound application. 13 ACS Paragon Plus Environment


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4. Conclusion

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Here we have shown passive adsorption of a volatile monoterpene to the surfaces of plants in a field

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experiment and the effects of elevated ozone levels on the process. Furthermore, we have shown

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that distance between the emitter source and receiver plant is an important factor in the process of

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passive plant-to-plant interactions, and that ozone reduces the effective distance. Passive plant-to-

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plant interactions should be considered during field measurements of volatiles as compounds

319

measured in the field may originate from surrounding plants. The likelihood of passive plant-to-

320

plant communication in the field is dependent on the chemical characteristics of the compounds

321

involved, the distances between emitter and receiver plants and air pollution levels. Based on these

322

field experiment results, it is important that in the development of field scale use of plant volatiles

323

in modern pest control 67,37, the distance between plants and volatile sources as well as the effects of

324

air pollutants be considered.

325

Acknowledgement

326

This study was funded by the Academy of Finland (project no. 278424) and a scientific exchange

327

grant from the Egyptian Ministry of Higher Education, Culture Affairs & Missions Sector for Dr.

328

A.M. Abd El-Raheem.

329

References

330 331

1. Holopainen, J. K.; Blande, J. D. Where do herbivore-induced plant volatiles go? Frontiers in plant science 2013, 4.

332

2. Rose, U.; Manukian, A.; Heath, R. R.; Tumlinson, J. H. Volatile Semiochemicals Released

333

from Undamaged Cotton Leaves (A Systemic Response of Living Plants to Caterpillar

334

Damage). Plant Physiol. 1996, 111, 487-495.


Page 14 of 29

Page 15 of 29

335 336


3. Hatanaka, A.; Kajiwara, T.; Sekiya, J. Biosynthetic pathway for C 6-aldehydes formation from linolenic acid in green leaves. Chem. Phys. Lipids 1987, 44, 341-361.

337

4. Turlings, T. C.; Bernasconi, M.; Bertossa, R.; Bigler, F.; Caloz, G.; Dorn, S. The induction

338

of volatile emissions in maize by three herbivore species with different feeding habits:

339

possible consequences for their natural enemies. Biological Control 1998, 11, 122-129.

340

5. Colazza, S.; Fucarino, A.; Peri, E.; Salerno, G.; Conti, E.; Bin, F. Insect oviposition induces

341

volatile emission in herbaceous plants that attracts egg parasitoids. J. Exp. Biol. 2004, 207,

342

47-53.

343 344 345 346 347 348 349

6. Holopainen, J. K.; Gershenzon, J. Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 2010, 15, 176-184. 7. Turlings, T. C.; Tumlinson, J. H.; Lewis, W. J. In Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 1990, 250, 1251-1253. 8. Kessler, A.; Baldwin, I. T. Defensive function of herbivore-induced plant volatile emissions in nature. Science 2001, 291, 2141-2144. 9. Karban, R.; Shiojiri, K.; Huntzinger, M.; McCall, A. C. Damage‐induced resistance in

350

sagebrush: volatiles are key to intra‐and interplant communication. Ecology 2006, 87, 922-

351

930.

352

10. Heil, M.; Silva Bueno, J. C. Within-plant signaling by volatiles leads to induction and

353

priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. U. S. A. 2007, 104,

354

5467-5472.

355 356 357 358

11. Li, T.; Blande, J. D. Volatile-Mediated within-Plant Signaling in Hybrid Aspen: Required for Systemic Responses. J. Chem. Ecol. 2017, 43, 327-338. 12. Li, T.; Blande, J. D. Associational susceptibility in broccoli: mediated by plant volatiles, impeded by ozone. Global Change Biol. 2015, 21, 1993-2004.



359

13. Girón-Calva, P. S.; Li, T.; Blande, J. D. Plant-plant interactions affect the susceptibility of

360

plants to oviposition by pests but are disrupted by ozone pollution. Agric., Ecosyst. Environ.

361

2016, 233, 352-360.

362 363 364

14. Pichersky, E.; Gershenzon, J. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 2002, 5, 237-243. 15. Bengtsson, M.; Jaastad, G.; Knudsen, G.; Kobro, S.; Bäckman, A.; Pettersson, E.; Witzgall,

365

P. Plant volatiles mediate attraction to host and non‐host plant in apple fruit moth,

366

Argyresthia conjugella. Entomol. Exp. Appl. 2006, 118, 77-85.

367

16. Halitschke, R.; Stenberg, J. A.; Kessler, D.; Kessler, A.; Baldwin, I. T. Shared signals–

368

‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol.

369

Lett. 2008, 11, 24-34.

370

17. Magalhães, D.; Borges, M.; Laumann, R.; Sujii, E.; Mayon, P.; Caulfield, J.; Midega, C.;

371

Khan, Z.; Pickett, J.; Birkett, M. Semiochemicals from herbivory induced cotton plants

372

enhance the foraging behavior of the cotton boll weevil, Anthonomus grandis. J. Chem.

373

Ecol. 2012, 38, 1528-1538.

374 375 376

18. Atema, J. Eddy chemotaxis and odor landscapes: exploration of nature with animal sensors. Biol. Bull. 1996, 191, 129-138. 19. Mylne, K. R.; Davidson, M. J.; Thomson, D. J. Concentration fluctuation measurements in

377

tracer plumes using high and low frequency response detectors. Bound. -Layer Meteorol.

378

1996, 79, 225-242.

379 380 381 382

20. Murlis, J.; Willis, M. A.; Carde, R. T. Spatial and temporal structures of pheromone plumes in fields and forests. Physiol. Entomol. 2000, 25, 211-222. 21. Koehl, M. The fluid mechanics of arthropod sniffing in turbulent odor plumes. Chem. Senses 2005, 31, 93-105.


Page 16 of 29

Page 17 of 29

383


22. Farré‐Armengol, G.; Peñuelas, J.; Li, T.; Yli‐Pirilä, P.; Filella, I.; Llusia, J.; Blande, J. D.

384

Ozone degrades floral scent and reduces pollinator attraction to flowers. New Phytol. 2016,

385

209, 152-160.

386 387 388 389 390

23. Atkinson, R.; Arey, J. Gas-phase tropospheric chemistry of biogenic volatile organic compounds: a review. Atmos. Environ. 2003, 37, 197-219. 24. Atkinson, R. Gas-phase tropospheric chemistry of volatile organic compounds: 1. Alkanes and alkenes. Journal of Physical and Chemical Reference Data 1997, 26, 215-290. 25. Pinto, D. M.; Blande, J. D.; Souza, S. R.; Nerg, A.; Holopainen, J. K. Plant volatile organic

391

compounds (VOCs) in ozone (O3) polluted atmospheres: the ecological effects. J. Chem.

392

Ecol. 2010, 36, 22-34.

393 394 395

26. Atkinson, R. Atmospheric chemistry of VOCs and NO x. Atmos. Environ. 2000, 34, 20632101. 27. Pinto, D. M.; Blande, J. D.; Nykänen, R.; Dong, W.; Nerg, A.; Holopainen, J. K. Ozone

396

degrades common herbivore-induced plant volatiles: does this affect herbivore prey location

397

by predators and parasitoids? J. Chem. Ecol. 2007, 33, 683-694.

398

28. Pinto, D. M.; Tiiva, P.; Miettinen, P.; Joutsensaari, J.; Kokkola, H.; Nerg, A.; Laaksonen,

399

A.; Holopainen, J. K. The effects of increasing atmospheric ozone on biogenic monoterpene

400

profiles and the formation of secondary aerosols. Atmos. Environ. 2007, 41, 4877-4887.

401 402 403 404 405 406

29. Kost, C.; Heil, M. Herbivore‐induced plant volatiles induce an indirect defence in neighbouring plants. J. Ecol. 2006, 94, 619-628. 30. Wilkinson, S.; Mills, G.; Illidge, R.; Davies, W. J. How is ozone pollution reducing our food supply? J. Exp. Bot. 2012, 63, 527-536. 31. Blande, J. D.; Holopainen, J. K.; Li, T. Air pollution impedes plant‐to‐plant communication by volatiles. Ecol. Lett. 2010, 13, 1172-1181.



407 408

32. Li, T.; Blande, J. D.; Holopainen, J. K. Atmospheric transformation of plant volatiles disrupts host plant finding. Scientific Reports 2016, 6, 33851.

409

33. Delaney, K. J., Wawrzyniak, M., Lemańczyk, G., Wrzesińska, D., & Piesik, D. Synthetic

410

cis-jasmone exposure induces wheat and barley volatiles that repel the pest cereal leaf

411

beetle, Oulema melanopus L. Journal of chemical ecology 2013, 39, 620-629.

412

34. Piesik, Dariusz, Didier Rochat, K. J. Delaney, and Frederic Marion‐Poll. Orientation of

413

European corn borer first instar larvae to synthetic green leaf volatiles. Journal of applied

414

entomology 2013, 137, 234-240.

415 416 417

35. James, D. G.; Price, T. S. Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J. Chem. Ecol. 2004, 30, 1613-1628. 36. Woods, J.; James, D.; Lee, J.; Gent, D. Evaluation of airborne methyl salicylate for

418

improved conservation biological control of two-spotted spider mite and hop aphid in

419

Oregon hop yards. Experimental and applied acarology 2011, 55, 401.

420

37. Nehlin, G.; Valterová, I.; Borg-Karlson, A. Use of conifer volatiles to reduce injury caused

421

by carrot psyllid, Trioza apicalis, Förster (Homoptera, Psylloidea). J. Chem. Ecol. 1994, 20,

422

771-783.

423

38. Byers, J. A. Novel diffusion-dilution method for release of semiochemicals: Testing

424

pheromone component ratios on western pine beetle. J. Chem. Ecol. 1988, 14, 199-212.

425

39. Zhou, H.; Chen, L.; Liu, Y.; Chen, J.; Francis, F. Use of slow-release plant infochemicals to

426

control aphids: a first investigation in a Belgian wheat field. Sci. Rep. 2016, 6, 31552.

427

40. Dampc, A.; Luczkiewicz, M. Rhododendron tomentosum (Ledum palustre). A review of

428 429

traditional use based on current research. Fitoterapia 2013, 85, 130-143. 41. Himanen, S. J.; Blande, J. D.; Klemola, T.; Pulkkinen, J.; Heijari, J.; Holopainen, J. K. Birch

430

(Betula spp.) leaves adsorb and re‐release volatiles specific to neighbouring plants–a

431

mechanism for associational herbivore resistance? New Phytol. 2010, 186, 722-732.


Page 18 of 29

Page 19 of 29


432

42. Himanen, S. J.; Bui, T. N.; Maja, M. M.; Holopainen, J. K. Utilizing associational resistance

433

for biocontrol: impacted by temperature, supported by indirect defence. BMC Ecology 2015,

434

15, 16.

435

43. Böge, O.; Mutzel, A.; Iinuma, Y.; Yli-Pirilä, P.; Kahnt, A.; Joutsensaari, J.; Herrmann, H.

436

Gas-phase products and secondary organic aerosol formation from the ozonolysis and

437

photooxidation of myrcene. Atmos. Environ. 2013, 79, 553-560.

438

44. Kim, Daekyun, Philip S. Stevens, and Ronald A. Hites. Rate Constants for the Gas-Phase

439

Reactions of OH and O3 with β-Ocimene, β-Myrcene, and α-and β-Farnesene as a Function

440

of Temperature. The Journal of Physical Chemistry 2010, 115, 500-506.

441

45. Karnosky, D. F., H. Werner, T. Holopainen, K. Percy, T. Oksanen, E. Oksanen, C. Heerdt et

442

al. Free-air exposure systems to scale up ozone research to mature trees. Plant Biology 2007,

443

9, 181-190.

444 445 446

46. Talekar, N.; Shelton, A. Biology, ecology, and management of the diamondback moth. Annu. Rev. Entomol. 1993, 38, 275-301. 47. Kivimäenpää, M.; Sutinen, S.; Valolahti, H.; Häikiö, E.; Riikonen, J.; Kasurinen, A.;

447

Ghimire, R. P.; Holopainen, J. K.; Holopainen, T. Warming and elevated ozone differently

448

modify needle anatomy of Norway spruce (Picea abies) and Scots pine (Pinus sylvestris).

449

Canadian Journal of Forest Research 2017, 47, 488-499.

450

48. Niinemets, Ü; Fares, S.; Harley, P.; Jardine, K. J. Bidirectional exchange of biogenic

451

volatiles with vegetation: emission sources, reactions, breakdown and deposition. Plant,

452

Cell Environ. 2014, 37, 1790-1809.

453 454

49. Schmid, C.; Steinbrecher, R.; Ziegler, H. Partition coefficients of plant cuticles for monoterpenes. Trees 1992, 6, 32-36.



455

50. Noe, S. M.; Copolovici, L.; Niinemets, Ü; Vaino, E. Foliar limonene uptake scales

456

positively with leaf lipid content: “Non‐emitting” species absorb and release monoterpenes.

457

Plant Biology 2008, 10, 129-137.

458

51. Niinemets Ü, Reichstein M. A model analysis of the effects of nonspecific monoterpenoid

459

storage in leaf tissues on emission kinetics and composition in Mediterranean sclerophyllous

460

Quercus species. Global Biogeochemical Cycles. 2002, 1, 4.

461 462 463

52. Müller, C.; Riederer, M. Plant surface properties in chemical ecology. J. Chem. Ecol. 2005, 31, 2621-2651. 53. Joensuu, J.; Altimir, N.; Hakola, H.; Rostás, M.; Raivonen, M.; Vestenius, M.; Aaltonen, H.;

464

Riederer, M.; Bäck, J. Role of needle surface waxes in dynamic exchange of mono-and

465

sesquiterpenes. Atmospheric Chemistry and Physics 2016, 16, 7813-7823.

466 467

54. Heil, M.; Karban, R. Explaining evolution of plant communication by airborne signals. Trends in ecology & evolution 2010, 25, 137-144.

468

55. Farmer, E. E. Surface-to-air signals. Nature 2001, 411, 854-856.

469

56. Dolch, R.; Tscharntke, T. Defoliation of alders (Alnus glutinosa) affects herbivory by leaf

470 471

beetles on undamaged neighbours. Oecologia 2000, 125, 504-511. 57. Karban, R.; Maron, J.; Felton, G. W.; Ervin, G.; Eichenseer, H. Herbivore damage to

472

sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants.

473

Oikos 2003, 100, 325-332.

474

58. Monks, P. S.; Archibald, A.; Colette, A.; Cooper, O.; Coyle, M.; Derwent, R.; Fowler, D.;

475

Granier, C.; Law, K. S.; Mills, G. Tropospheric ozone and its precursors from the urban to

476

the global scale from air quality to short-lived climate forcer. Atmospheric Chemistry and

477

Physics 2015, 15, 8889-8973.

478 479

59. Sitch, S.; Cox, P.; Collins, W.; Huntingford, C. Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature 2007, 448, 791.


Page 20 of 29

Page 21 of 29

480


60. Jud, W.; Fischer, L.; Canaval, E.; Wohlfahrt, G.; Tissier, A.; Hansel, A. Plant surface

481

reactions: an opportunistic ozone defence mechanism impacting atmospheric chemistry.

482

Atmospheric Chemistry and Physics 2016, 16, 277-292.

483 484 485

61. Kerstiens, G.; Lendzian, K. J. Interactions between ozone and plant cuticles. New Phytol. 1989, 112, 21-27. 62. Barnes, J.; Brown, K. The influence of ozone and acid mist on the amount and wettability of

486

the surface waxes in Norway spruce [Picea abies (L.) Karst.]. New Phytol. 1990, 114, 531-

487

535.

488

63. Komatsu, H. Repellency of rosemary oil and its components against the onion aphid,

489

Neotoxoptera formosana (Takahashi)(Homoptera, Aphididae). Appl. Entomol. Zool. 1997,

490

32, 303-310.

491

64. Yoon, C.; Kang, S.; Jang, S.; Kim, Y.; Kim, G. Repellent efficacy of caraway and grapefruit

492

oils for Sitophilus oryzae (Coleoptera: Curculionidae). Journal of Asia-Pacific Entomology

493

2007, 10, 263-267

494

65. Kim, S.; Yoon, J.; Jung, J. W.; Hong, K.; Ahn, Y.; Kwon, H. W. Toxicity and repellency of

495

origanum essential oil and its components against Tribolium castaneum (Coleoptera:

496

Tenebrionidae) adults. Journal of Asia-Pacific Entomology 2010, 13, 369-373.

497

66. Caballero-Gallardo, K.; Olivero-Verbel, J.; Stashenko, E. E. Repellent activity of essential

498

oils and some of their individual constituents against Tribolium castaneum Herbst. J. Agric.

499

Food Chem. 2011, 59, 1690-1696.

500 501

67. Cook, S. M.; Khan, Z. R.; Pickett, J. A. The use of push-pull strategies in integrated pest management. Annu. Rev. Entomol. 2007, 52, 375-400.

502 503

504



505

506

507

508

509

510

511

512

513

514

515


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Figures and Tables

Ozone concentration (ppb)

Elevated ozone

Ambient ozone

100 80 60 40 20 0

Figure 1. Daily mean ozone volume mixing ratio (ppb) for daylight hours (8:00-22:00) for experimental periods (30.06 – 7.7.2016 and 8.7.-15.07.2016) Myrcene dispenser

Ambient

(b) 1 L glass jar Capillary tube 10 mL glass tube Air inlet -1 1200 ml min

Myrcene

Ozone

9m

(a) 0m 0.5m 1.5m 3.0m

Figure 2. (a) Schematic representation of the experimental set up. The red dot in the middle of each plot represents a myrcene dispenser. Each pair of plots represents a different treatment; ambient ozone (A), ambient ozone and myrcene (AM), elevated ozone (O) elevated ozone and myrcene (OM). (b) Diagrammatic representation of a myrcene dispenser (n = 2 for each treatment/exposure).

ACS Paragon Plus Environment


50 30 10 (10) (30) AW3 AW2 AW1 AE1

Myrcene Emission (ng g-1 h-1)

Myrcene

Eggs + Larvae

9 8 7 6 5 4 3 2 1 0

130 110 90 70 50 30 10 (10) (30)

No of Eggs + Larvae

70

Myrcene

130 110 90 70 50 30 10 (10) (30)

No of Eggs + Larvae

90


110

No of Eggs + Larvae

130

9 8 7 6 5 4 3 2 1 0

O

AM

Eggs + Larvae

AE2 AE3

OM

Eggs + Larvae

9 8 7 6 5 4 3 2 1 0

130 110 90 70 50 30 10 (10) (30)


Myrcene

No of Eggs + Larvae


A

Page 24 of 29

Myrcene 9 8 7 6 5 4 3 2 1 0

Eggs + Larvae

OW3 OW2 OW1 OE1 OE2 OE3

Figure 3. Myrcene emission rates (bars) and number of eggs and neonate larvae (line) from four treatments (A=Ambient, AM=Ambient+Myrcene, O=Ozone, OM=Ozone+Myrcene) of cabbage plants at three distances 1, 2, 3 (0.5m, 1.5m and 3m) and two directions (W; West, E; East) from the plot centre. Data points represent mean ± SE (n = 4). See Tables 1 and 2 for the significant effects.

Myrcene concentration (ng/L-1)

6 5

P 0.001

4 3 2 1 0 AM

OM

Figure 4. Myrcene air concentration at 50cm from dispenser (18cm above soil surface) in AM and OM plots. Bars represent mean ± SE (n = 8) P = significant value from student t-test.

Figure 5. Wind rose diagram showing dominant wind direction and speed during experimental period.

ACS Paragon Plus Environment

Page 25 of 29


Table 1. Main and interactive effects of ozone, myrcene, direction and distance on the emission of myrcene from receiver plants and the number of eggs on cabbage plants. Linear mixed model ANOVA, significant values set at P 0.1 and marked by *. Factor

Myrcene emission 0.001* Ozone 0.002* Myrcene 0.191 Direction 0.036* Distance 0.309 Ozone * Myrcene 0.777 Ozone * Direction 0.001* Ozone * Distance 0.030 Myrcene * Direction 0.006* Myrcene * Distance 0.188 Direction * Distance 0.196 Ozone * Myrcene * Direction 0.001* Ozone * Myrcene * Distance 0.204 Ozone * Direction * Distance 0.094* Myrcene * Direction * Distance Ozone * Myrcene * Direction * Distance 0.248

Egg & Larvae 0.114 0.362 0.425 0.139 0.498 0.877 0.177 0.352 0.926 0.914 0.085 0.963 0.623 0.746 0.094*

Table 2. SME-test (effect of factor within treatments) with significant P-values on myrcene emission and number of eggs from white cabbage plants. represents decreasing effect and represents increasing effect. A, ambient ozone, M, myrcene, O, elevated ozone, E, east, DIR, direction and D, distance; at 1,2,3, represents 0.5m, 1.5m and 3m respectively. Only significant SME results are presented. Dependent variable

Number of Eggs + Neonate Larvae

Interaction

Ozone x Myrcene x Direction x Distance

Treatment / group

Factor Ptested value

D2 vs D1 in AM Plots D3 vs D1 in AM Plots AM vs A at D1 OM vs AM at D1 E at D1 vs ME at D1 W at D1 vs MW at D1 W at D3 vs MW at D3 D2 vs D1 in MW D3 vs D1 in MW O vs A at D3 in E direction AW vs AMW at D2 in W direction

D D M O M M M D D O

Passive Adsorption of Volatile Monoterpene in Pest Control: Aided by

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