insects Review Context-Dependence and the Development of Push-Pull Approaches for Integrated Management of Drosophila suzukii 1 1, , 2, , Jeroen T. Alkema , Marcel Dicke * y and Bregje Wertheim * y 1 Laboratory of Entomology, Wageningen University, P.O. Box 16, 6700AA Wageningen, The Netherlands; [email protected] 2 Groningen Institute of Evolutionary Life Sciences, University of Groningen, P.O. Box 11103, 9700 CC Groningen, The Netherlands * Correspondence: [email protected] (M.D.); [email protected] (B.W.) Shared senior authors and corresponding authors. y Received: 13 November 2019; Accepted: 10 December 2019; Published: 15 December 2019 Abstract: Sustainable pest control requires a systems approach, based on a thorough ecological understanding of an agro-ecosystem. Such fundamental understanding provides a basis for developing strategies to manipulate the pest’s behaviour, distribution, and population dynamics, to be employed for crop protection. This review focuses on the fundamental knowledge required for the development of an effective push-pull approach. Push-pull is a strategy to repel a pest from a crop, while attracting it toward an external location. It often relies on infochemicals (e.g., pheromones or allelochemicals) that are relevant in the ecology of the pest insect and can be exploited as lure or repellent. Importantly, responsiveness of insects to infochemicals is dependent on both the insect’s internal physiological state and external environmental conditions. This context-dependency reflects the integration of cues from different sensory modalities, the effect of mating and/or feeding status, as well as diurnal or seasonal rhythms. Furthermore, when the costs of responding to an infochemical outweigh the benefits, resistance can rapidly evolve. Here, we argue that profound knowledge on context-dependence is important for the development and implementation of push-pull approaches. We illustrate this by discussing the relevant fundamental knowledge on the invasive pest species Drosophila suzukii as an example. Keywords: behaviour; repellent; attractant; invasive pest; evolution 1. Introduction The aim of integrated pest management (IPM) is to design a cropping system that manages pests below the economic damage threshold [1]. Main components of IPM are biological control, host plant resistance, cultural control, and the use of infochemicals such as pheromones and repellents (behavioural control). While approaches focusing merely on pesticides aim at eradicating pests, IPM seeks to manage pests below the economic injury threshold by promoting activities that support factors regulating the pest while mitigating factors that interfere with such regulating factors [1–3]. Developing effective and efficient IPM strategies requires a thorough ecological understanding of the crop system. This includes, but is not restricted to, an understanding of how the pest interacts with its resources such as the crop plants, non-crop plants surrounding the crop, as well as conspecifics, competitors, and natural enemies [1]. Successfully implemented IPM strategies have been shown to result in improved resilience of the crop system, and to be financially and environmentally more beneficial than pesticide use [4–6]. Insects 2019, 10, 454; doi:10.3390/insects10120454 www.mdpi.com/journal/insects Insects 2020, 11, x 2 of 19 Insects 2019, 10, 454 2 of 19 1.1. Push-Pull Approach as Part of Integrated Pest Management (IPM) 1.1.One Push-Pull tactic Approachwithin IPM as Part is the of Integratedpush-pull Pest approach Management, which (IPM) aims to manipulate the behaviour of pest insectsOne tactic using within a two-pronged IPM is the push-pull strategy: approach,to push the which target aims organism to manipulate away thefrom behaviour a crop while of pest pullinginsects it using toward a two-pronged a trapping strategy:system (Figure to push 1) the [6–8]. target Pushing organism and away pulling from is a cropachieved while by pulling using it repellenttoward a(push) trapping and system attractant (Figure 1)[(pull)6–8]. Pushingcues, usually and pulling volatiles is achieved including by using pheromones repellent (push)and allelochemicalsand attractant [7]. (pull) The cues, trap usuallyto which volatiles the insects including are guided pheromones can either and be a allelochemicals designed killing [7 trap]. The (e.g., trap a tocontainer which the or insectsadhesive are strip guided with can an either attractant) be a designedto capture, killing sequester, trap (e.g., and akill container the roaming or adhesive pest insects,strip with or a antrap attractant) plant as an to alternative capture, sequester, host plant and for killthe pest the roaming[6,7]. Candidate pest insects, trap plants or a trap are planthighly as attractivean alternative and include host plant sub-optimal for the pestor lethal [6,7]. hosts Candidate that hamper trap plants the development are highly attractive of the pest and insect, include or high-qualitysub-optimal plants or lethal that hosts are destroyed that hamper before the development the pest can disperse of the pest to insect,the crop or [7–9]. high-quality plants that are destroyed before the pest can disperse to the crop [7–9]. FigureFigure 1. 1. TheThe push-pull push-pull strategy strategy employs employs repellent repellent (push) (push) and and attractive attractive (pull) (pull) odours odours to to deal deal with with insectinsect pests. pests. Crops Crops to to be be protected protected from from a apest, pest, dr drosophilidosophilid flies flies in in this this ex example,ample, are are treated treated with with a a repellentrepellent (yellow (yellow cloudcloud on on the the left). left). This repellentThis repellent pushes thepushes pest awaythe pest from away the crop. from Simultaneously, the crop. Simultaneously,a trap containing a trap an attractive containing volatile an attractive compound volatile pulls compound the pest away pulls from the thepest crop away (blue from cloud the oncrop the (blueright). cloud on the right). TheThe push-pull push-pull approach approach can can form form an an integral integral part part of of a acrop crop management management system system that that prevents prevents outbreaks;outbreaks; it itis isnot not suited suited to to deal deal with with the the pest pest species species when when its its population population density density has has already already reachedreached high high levels. levels. The The push push system system is islikely likely to to be be less less effective effective at at high high pest pest densities densities when when there there is is strongstrong competition competition among among pest pest individuals, individuals, and and larg largee populations populations have have an an increased increased risk risk of of evolving evolving resistanceresistance to to either either the the push push or or the the pull pull comp componentonent [7,10]. [7,10]. Cook, Cook, Khan, Khan, and and Pickett Pickett [7] [7 ]therefore therefore proposedproposed to to apply apply the push-pull methodmethod before before the the pest pest species species has has been been detected, detected, e.g., e.g., at the at startthe start of the ofcrop the season.crop season. Thus, theThus, push-pull the push-pull approach approach should beshould a true be component a true component of the total of crop the management total crop managementsystem in place system [7]. Using in place lethal [7]. traps Using would lethal reduce traps the would spread reduce of organisms the spread that developof organisms resistance that to developeither the resistance push or to the either pull elementthe push [ 11or]. the Alternatively, pull element the [11]. population Alternatively, stress the on population the push-pull stress method on thecould push-pull be relieved method by reducingcould be relieved pest population by reducing size throughpest population natural size enemies through of the natural pest [ 7enemies]. of the pestAn [7]. example in which the push strategy has been very effective is the application of the host-marking pheromoneAn example of the in tephritidwhich the fruit push fly strategyRhagoletis has cerasi beenin very cherry effective orchards. is the Spraying application of crops of the with host- the markinghost-marking pheromone pheromone of the tephritid reduced tephritidfruit fly Rhagoletis infestations cerasi by 90%in cherry [10,12 orchards]. The oviposition-deterring. Spraying of crops withpheromone the host-marking underlying pheromone this behaviour reduced was tephritid isolated infestations and has been by 90% developed [10,12]. intoThe anoviposition- optimized deterringblend [10 pheromone,13]. However, underlying habituation this andbehaviour resistance was toisolated this pheromone and has been was observeddeveloped after into some an optimized blend [10,13]. However, habituation and resistance to this pheromone was observed after Insects 2019, 10, 454 3 of 19 time [10,14]. To avoid this, it is more effective to combine a push strategy with a pull strategy toward a lethal trap [7]. 1.2. Fundamental Ecological Knowledge Required to Design Effective Push-Pull Systems To design and implement a push-pull strategy effectively, fundamental knowledge is required [7]. This knowledge should go beyond an understanding of repellent or attractive properties. More detailed insight into the evolution of a cue, how it affects an organism, and why it is repellent or attractive will illuminate the degree to which it is susceptible to the pest evolving resistance.