Attracting Carnivorous Arthropods with Plant Volatiles: the Future of Biocontrol Or Playing with ﬁre? ⇑ Ian Kaplan

Biological Control 60 (2012) 77–89 Contents lists available at SciVerse ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Perspective Attracting carnivorous arthropods with plant volatiles: The future of biocontrol or playing with fire? ⇑ Ian Kaplan Department of Entomology, Purdue University, 901 W. State St., West Lafayette, IN 47907, USA highlights graphical abstract " Herbivore-induced plant volatiles are potent attractants for carnivorous arthropods. " Recent field studies have manipulated HIPVs for augmenting biocontrol impact. " Recent successes are reviewed and future challenges evaluated for this field. article info abstract Article history: Herbivore-induced plant volatiles (HIPVs) are potent attractants for entomophagous arthropods and Received 12 August 2011 researchers have long speculated that HIPVs can be used to lure natural enemies into crops, reestablish- Accepted 31 October 2011 ing predator–prey relationships that become decoupled in disturbed agricultural habitats. This specula- Available online 9 November 2011 tion has since become reality as the number of field trials investigating HIPV-mediated attraction and its consequences for pest suppression has risen dramatically over the past 10 years. Here, I provide an over- Keywords: view of recent field efforts to augment natural enemy populations using HIPVs, with emphasis on those Beneficial insects studies manipulating synthetic compounds in controlled-release dispensers, and outline a prospectus for HIPVs future research needs. Specifically, I review and discuss: (i) choice of compounds and release rates; (ii) Indirect plant defenses Methyl salicylate functional changes in predator and parasitoid communities; (iii) non-target effects; (iv) mechanisms of Pest management attraction and prey suppression; (v) spatial- and landscape-level considerations; (vi) context-dependent Tritrophic interactions responses; and (vii) temporal stability of attraction. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction why strong aggregative responses are thought to stabilize predator–prey interactions (Murdoch et al., 1985; Kareiva, 1987; Döbel Herbivorous insects are predicted to outbreak on plants grow- and Denno, 1994). Thus, the temporal sequence of colonization ing in ephemeral, early succession habitats in which frequent dis- across trophic levels is central to understanding when and where turbances decouple natural enemies from their prey (Southwood, natural enemies suppress their prey and, more importantly, when 1977). This implicitly assumes that herbivores colonize new habi- and where they fail to. tats in advance of their enemies, thereby receiving a head-start on Asynchronous crop colonization by pest and beneficial insects is feeding and reproduction during the time lag before predators and at the heart of why biocontrol is difficult to implement, especially parasitoids arrive. It also forms the theoretical basis underlying in annual cropping systems: enemies are always one-step behind the pest (Ehler and Miller, 1978; Wiedenmann and Smith, 1997; ⇑ Fax: +1 765 494 2152. Wissinger, 1997). When this asynchrony is experimentally cor- E-mail address: [email protected] rected by augmenting early-season predators, however, pest popu- 1049-9644/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2011.10.017 78 I. Kaplan / Biological Control 60 (2012) 77–89 lations are more stable and rarely erupt (e.g., Settle et al., 1996). A map for future research efforts in this field. By nature it is designed mathematical model testing the consequences of variation in nat- to raise far more questions than it answers. Although some of these ural enemy traits for pest abundance further supports this view issues have been addressed in previous reviews on the topic, sur- (Kean et al., 2003). Spatial attraction of enemies resulted in a near prisingly, most of them have either only been mentioned in passing linear decline in pest density and was concluded to be ‘‘the most or ignored altogether. To avoid recreating the wheel, I also draw useful mechanism for conservation biological control in ephemeral heavily on analogous reviews of kairomones in biological pest crops’’. The challenge then is to effectively manipulate predator management (e.g., Vinson, 1977; Gross, 1981; Nordlund et al., and parasitoid behavior in the field, luring them into crops earlier 1981; Powell, 1986; Lewis and Martin, 1990). In the same vein as and at higher densities than they might otherwise occur. earlier critiques (Hunter, 2002), my emphasis is entirely on field- While the behavioral manipulation of biocontrol agents is cer- based investigations rather than those conducted in the laboratory tainly not a new topic (Vinson, 1977; Gross, 1981; Nordlund or greenhouse. et al., 1981; Powell, 1986; Lewis and Martin, 1990), the concept Due to personal biases, this review is admittedly slanted to- has taken on renewed interest with the discovery of herbivore-in- wards synthetic compounds deployed as slow-release lures. Most duced plant volatiles (hereafter, HIPVs) as potent attractants for of the questions and concerns raised below, however, are equally entomophagous arthropods (Turlings and Wäckers, 2004; Mumm relevant to other techniques such as genetically engineered crops. and Dicke, 2010; Hare, 2011), and speculation has since run ram- Moreover, several comprehensive reviews exist on the prospects of pant that HIPVs can be deployed to enhance the control of agricul- using transgenic plants with augmented HIPV profiles (Degenhardt tural pests (Dicke et al., 1990; Bottrell et al., 1998; Sabelis et al., et al., 2003; Aharoni et al., 2005; Dudareva and Pichersky, 2008; 1999; Degenhardt et al., 2003; Pickett et al., 2006; Turlings and Kos et al., 2009), and there has also been a dramatic rise over the Ton, 2006; Khan et al., 2008; Åhman et al., 2010; Shrivastava past 10 years in the number of field trials testing synthetic com- et al., 2010). In other words, how can we make crops ‘smell’ more pounds. It is, therefore, an opportune time to reflect on the existing attractive to foraging carnivores? group of field experiments that have been conducted and evaluate This perspective represents a radical departure from the ratio- how to proceed from here. nale underpinning traditional efforts to increase natural enemy impact on pests, which have largely emphasized the provisioning of 2.1. Optimizing attraction – where to begin? habitat and supplemental foods (e.g., cover crops, floral borders – Pickett and Bugg (1998) and Gurr et al. (2004)), or what might The most fundamental, and some may argue most important, be called the field of dreams approach to biocontrol (i.e., if you question in this field is how to attract carnivores with HIPVs. As build it, they will come; sensu Palmer et al. (1997)). The latter strat- noted above, my focus will largely be on synthetic lures, but vola- egy is predicated on the idea that, if abundant in the local environ- tiles can also be manipulated via metabolic engineering (Kappers ment, enemies will naturally colonize pest-infested fields; yet this et al., 2005; Schnee et al., 2006; Degenhardt et al., 2009), phytohor- is not always the case (Heimpel and Jervis, 2005), or the response is monal elicitors (Thaler, 1999; Stout et al., 2002; Rohwer and Erwin, only detectable within several meters of the crop border, resulting 2008), or intercropping aromatic plants (Khan et al., 1997, 2008). in a distinct edge effect (Tylianakis et al., 2004). Using HIPVs as The ‘how’ question can be further dissected into two main com- lures to pull entomophagous arthropods into a patch of plants from ponents: (1) Which compound(s) should be targeted? and (2) How neighboring refuges builds on the framework of existing biocontrol much of that compound should be released? Each of these ques- theory, an opportunity noted in recent reviews (Khan et al., 2008; tions will be considered in turn: Gurr and Kvedaras, 2010). Even within fields, predation and para- sitism pressure may be weak if certain volatile signals were unin- 2.1.1. Compound(s) tentionally bred out of crops from wild progenitors (Bottrell et al., The choice of compound or compounds will affect which spe- 1998; Rasmann et al., 2005; Köllner et al., 2008; Rodriguez-Saona cies are attracted and the magnitude of their attraction, and thus et al., 2011a). is a crucial decision (Degenhardt et al., 2003; Turlings and Ton, Despite their promise, using HIPVs to enhance natural enemy 2006). Given that >1000 volatiles have been identified from plants recruitment, retention, and attack on pests remains a controver- (Pichersky et al., 2006), it is also a difficult decision. A common ap- sial topic. On one hand, dozens of laboratory olfactometer trials proach is to first test electroantennogram (EAG) and/or y-tube have illustrated the primacy of these cues compared with those behavioral responses of natural enemies to candidate HIPVs in emanating from an undamaged plant, the prey itself or its frass the lab; whichever compound(s) appear most promising based (Du et al., 1996; Turlings and Wäckers, 2004; Allison and Hare, on these preliminary data are then selected for subsequent field 2009). This alone makes them an alluring target. On the other trials (Zhu et al., 1999, 2005; Zhu and Park, 2005; Williams et al., hand, arthropod attraction and repulsion to chemical signals is 2008; Tóth et al., 2009; Yu et al., 2010). This approach, however, a complex process that is not fully understood, especially in real- is typically intended for use in a system where a focal predator istic field settings. Interfering could be counterproductive for a or parasitoid is known to be attracted to an herbivore-damaged number of reasons that are outlined below. In fact, most of the plant and the goal is to identify the source of attraction. For exam- currently published reviews aimed at application of volatiles in ple, lady beetles were observed aggregating in soybean fields in- pest management are replete with warnings of the potential fested with the soybean aphid, Aphis glycines Matsumura, and dangers of doing so. this response was thought to be mediated by aphid-induced volatiles (Zhu and Park, 2005).

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