Date Published: March 1, 2019
Publisher: Public Library of Science
Author(s): Niall J. A. Conboy, Thomas McDaniel, Adam Ormerod, David George, Angharad M. R. Gatehouse, Ellie Wharton, Paul Donohoe, Rhiannon Curtis, Colin R. Tosh, Nicolas Desneux.
Horticulturalists and gardeners in temperate regions often claim that planting marigolds next to tomato plants protects the tomatoes from the glasshouse whitefly (Trialeurodes vaporariorum Westwood). If shown to hold true, this technique could be used in larger-scale tomato production, protecting the crop and helping to introduce greater plant diversity into these agro-ecosystems. Here we present two large-scale glasshouse trials corresponding to the two main ways growers are likely to use marigolds to control whiteflies. In the first, marigolds are grown next to tomato throughout the growing period and we quantify whitefly population growth from the seedling stage over a 48 day infestation period. Here we show that association with marigolds significantly slows whitefly population development. Introducing additional whitefly-attractive ‘pull’ plants around the perimeter of plots has little effect, but reducing the proportion of marigolds and introducing other non-hosts of whiteflies (basil, nasturtium and Chinese cabbage) also reduces whitefly populations on tomato. The second experiment assesses the efficacy of marigolds when used as an ‘emergency’ measure. Here we allow whitefly populations to build to a high density on unprotected tomatoes then introduce marigolds and assess whitefly population over a further period. Following laboratory work showing limonene to be a major chemical component of French marigolds and a negative behaviour response of whiteflies to this compound, limonene dispensers are added as an additional treatment to this experiment. “Emergency” marigold companion planting yielded minimal reductions in whitefly performance, but the use of limonene dispensers was more effective. Our work indicates that companion planting short vine tomatoes with French marigolds throughout the growing season will slow development of whitefly populations. Introducing marigolds to unprotected tomatoes after significant whitefly build-up will be less effective. The use of limonene dispensers placed near to tomato plants also shows promise. It is argued that this work supports the possibility of the development of a mixture of tomato companion plants that infer ‘associational resistance’ against many major invertebrate pests of tomato. Such a mixture, if comprising edible or ornamental plants, would be economically viable, would reduce the need for additional chemical and biological control, and, if used outdoors, would generate plant-diverse agro-ecosystems that are better able to harbour invertebrate wildlife.
Tomatoes (Solanum lycopersicum L.) are the second most important edible horticultural crop by production in developed nations . Under glass, pest infestations are dominated by the common glasshouse whitefly (Trialeurodes vaporariorum)  which is known to cause severe yield losses to an array of crops through transmission of a number of plant viruses [3, 4]. Direct feeding from both adults and larvae results in honeydew secretion which reduces the photosynthetic capacity of the plant and renders fruit unmarketable . Biocontrol is widely used to manage T. vaporariorum infestations but limitations such as delayed efficacy  and hyperparasitism  can lead to failure. Where biocontrol fails, there is still reliance on chemical control for tomato production and excessive use of chemical sprays has resulted in resistant T. vaporariorum genotypes, phytotoxicity and pesticide residue problems [8–10]. As with most contemporary cropping systems, tomatoes are typically produced in monoculture, thus rendering crop areas of limited value to wildlife and largely devoid of “ecosystem services” . Any alternative methods of whitefly control that can reduce pesticide use and introduce greater animal and plant diversity into agricultural and horticultural systems should therefore be welcomed. The insistence of temperate region gardeners that planting marigolds next to tomatoes protects the tomato crop from whiteflies therefore merits further investigation. Companion planting is a well-researched (and implemented) pest control strategy and is believed to be founded on ‘associational resistance’ [12, 13]. Both French (Tagetes patula L.) and English marigold (Calendula officinalis) have been used as effective companion plants in a number of other pest/crop scenarios. They have been shown to reduce pest populations either directly through repellent volatile chemistry  or indirectly through promoting beneficial arthropod populations [15–18]. Despite this, no research appears to be available that quantifies the potential for marigolds to control whiteflies on tomatoes.
The first large scale glasshouse study sought to establish a scientific basis for the propagation of French marigolds amongst tomato plants from the start of the growing season to protect tomatoes from whitefly infestation. This work aimed to identify whether this practice achieved significant control of the important glasshouse pest T. vaporariorum, and whether this control could be enhanced by other aversive, non-host plants. A second treatment also sought to quantify whether this ‘push’ effect could be combined with the ‘pull’ of attractive host plants to increase whitefly control. French marigold was found to be an effective companion plant and subsequent headspace analysis followed by laboratory bioassays confirmed the volatile limonene to be the probable mechanistic basis of the repellent properties this plant possesses. In a second glasshouse trial, the potential for marigold plants and limonene dispensers to control a heavy infestation of whiteflies on tomato was assessed.
The efficacy of a method popular amongst domestic gardeners, of intercropping tomato with French marigolds for pest control, appears to have been supported in the present study. Significant control of whitefly was achieved when marigolds were intercropped amongst tomatoes from the beginning of the growth period. However introducing marigolds as a replacement for chemical control methods after significant whitefly infestation produced minimal effects. In the “emergency” situation, the limonene dispensers were more effective at reducing whitefly performance than whole plants, and this method warrants further experiments for optimisation of its deployment. Future experiments should look to ascertain how repellent volatiles effect whitefly behaviour in a no-choice situation without control plots present, which could have acted as refuge areas for the whitefly. Despite this, we predict that repellent volatiles would still reduce whitefly performance by invoking restlessness and/or abnormal behaviour, as has been shown previously . Effects on natural enemies and other prominent pest species should be explored before implementing our methods in a commercial glasshouse setting. Nevertheless, the results obtained from this work are extremely promising for the application of repellent volatile chemistry for the protection of glasshouse grown tomatoes.