Biological Control 60 (2012) 77–89

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Biological Control

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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 preda- tor–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 im- pact 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 vola- tiles (Zhu and Park, 2005). By comparing the VOC profiles of aphid- infested vs. aphid-free soybeans, followed by coupled GC-EAG 2. A prospectus for future research needs on plant volatiles in analyses for aphid-infested plants, the authors found that A. gly- biocontrol cines feeding induces the emission of methyl salicylate (hereafter, MeSA) and that MeSA also elicits a strong EAG response in lady This paper is not intended to be an exhaustive review of HIPV- beetles. A field experiment then confirmed that synthetic MeSA natural enemy interactions, nor is it meant to explore all possible is indeed attractive to lady beetles and likely underlies the orienta- avenues of semiochemical manipulation in agriculture. Rather, tion of aphidophagous predators toward soybean plants harboring my goal here is simply to highlight major gaps in our understand- aphids. While this approach follows a logical train of thought (i.e., ing of how to exploit HIPVs in biocontrol and thus serve as a road- field observation ? laboratory biochemical assay ? field experi- I. Kaplan / Biological Control 60 (2012) 77–89 79 ment) and thus is intuitively appealing, it is also a time-intensive parasitic Hymenoptera, predaceous Heteroptera, and lacewings process and relegates the investigation to the subset of HIPVs (Rodriguez-Saona et al., 2011b). emitted by that plant. Considering that important volatile attrac- tants are missing from some crop cultivars, as shown in corn 2.1.2. Release rate (Gouinguené et al., 2001; Rasmann et al., 2005; Köllner et al., The amount of HIPV released will affect its atmospheric concen- 2008), this may be problematic. tration and thus exposure to foraging arthropods. Two factors dic- Selecting HIPVs as attractants without a priori knowledge of a tate the release rate: first, how much compound is emitted per lure particular plant-insect system can nevertheless occur when ubiq- over time, and second, how many lures are exposed per unit area. uitous or commonly induced volatiles such as MeSA are systemat- Releasing too little compound per field may not exert a strong en- ically screened for arthropod community-level responses (Flint ough pull, but releasing too much can weaken attraction or even et al., 1979; James, 2003a,b, 2005; James and Price, 2004; James lead to repulsion. In a laboratory wind tunnel assay, for example, and Grasswitz, 2005; Yu et al., 2008; Alhmedi et al., 2010; Lee, Whitman and Eller (1992) created dose-response curves for braco- 2010; Jones et al., 2011; Rodriguez-Saona et al., 2011b). Among nid wasps orienting to green leaf volatiles (GLV) over a range of studies comparing multiple HIPVs in this manner, the maximum concentrations. For all eight GLVs tested, wasp attraction was high- number screened in a single field experiment was 15, due to logis- est at intermediate concentrations and declined with increasing tical constraints. Unfortunately, this is barely scratching the sur- concentration thereafter, resulting in distinctly hump-shaped face, especially given that most studies evaluate single curves. Therefore, studies are aiming for an optimum level or zone compounds rather than complex odor blends, which are likely to of HIPV release to maximize their impact. Deciding on release tar- be more effective but require far more treatments to mechanisti- gets is challenging because that optimal concentration is unknown cally tease apart (Tóth et al., 2009). Jones et al. (2011), for instance, for most arthropods and, more importantly, we have little to no tested the attraction of three lacewing species to synthetic HIPVs in knowledge on the diffusion of HIPVs and thus their spatial sphere apple orchards. Interestingly, they found that MeSA and iridodial (a of influence in the field (but see Hiltpold and Turlings, 2008). From male-produced aggregation pheromone) alone were weak attrac- a logistical standpoint this also becomes problematic when trying tants for lacewings, but the combination of MeSA + iridodial was to determine the distance between HIPV treated and untreated a strong attractant. In this example, the magnitude of attraction plots to avoid chemical interference. Studies have used a range of to the two-part blend was more than twice the sum of the two interplot spacings, from 15 to 150 m, but to my knowledge this compounds presented individually. There is good reason to suspect is a mere guessing game and not based on biologically-relevant that such non-additive effects may be prevalent and identifying information. these biochemical synergies should be a priority for future studies. Release rate from individual lures can be modified in a number It remains an open question whether odor blends are best evalu- of ways, most commonly by using serial dilutions of the focal com- ated by trial and error (i.e., randomly combining HIPVs into novel pound, polyethylene tubing that varies in length or thickness, and blends) or whether blends should mimic those naturally emitted vials with openings that vary in number or diameter. Several stud- from herbivore-damaged plants (i.e., synthetic lures whose release ies have assessed the consequences of variable release rate for profile matches the chromatogram of some focal plant). It is abun- point-source attraction of natural enemies in the field. Of these dantly clear though, that arthropods perceive HIPVs as greater than studies, most have documented that the magnitude of attraction the sum of their parts and lures need to better reflect this (van Wijk increases in proportion to release rate (Flint et al., 1979, 1981; et al., 2008, 2010). Murchie et al., 1997; James, 2006; Tóth et al., 2006; Jones et al., The decision of which compounds to release also depends in 2011). As the amount of synthetic caryophyllene oxide released part on the goals of the study. If the aim is to enhance the impact in cotton fields increased from 0 to 0.1 to 1 to 10 g, trap catch of of a single, highly effective natural enemy, this is likely to be more the predaceous beetle, Collops vittatus (Say), increased from 0 to straightforward than augmenting an entire guild. Turlings and col- 2.7 to 3.3 to 7.6, respectively (Flint et al., 1981). Similarly, abun- leagues sought to improve suppression of corn rootworm, Diabro- dance of green lacewings, Chrysopa oculata Say, more than doubled tica virgifera virgifera LeConte, by entomopathogenic nematodes on yellow sticky cards baited with 99% MeSA compared to those and were able to do so by amplifying the belowground expression with MeSA diluted in hexane to 10% or 1% concentrations (James, of a single chemical, (E)-b-caryophyllene, from corn roots 2006). In two studies (Ferry et al., 2007; Zhu and Park, 2005), pred- (Degenhardt et al., 2009; Rasmann et al., 2005). Other work, how- ator attraction declined at the highest release rate treatment, but ever, has searched for broad-spectrum carnivore attractants, which in most of these cases the decline was slight and attraction was may be more compatible with the goals of conservation biocontrol still maintained well-above that of the unbaited control. Given that seek to enhance the impact of a diverse species assemblage. In these outcomes, the risk of releasing too much compound from this sense, the vast majority of tests have focused on MeSA, a com- individual lures seems relatively low. pound that is emitted in response to sap-feeding (e.g., aphids, Interestingly, the limited data on lure density suggest the oppo- mites) and chewing (e.g., caterpillars, beetles) herbivores on a wide site. Across several field experiments, James and colleagues used range of plants from grasses to trees (Bolter et al., 1997; van den the same MeSA lures (i.e., constant release rate per lure of ca. Boom et al., 2004; Lou et al., 2005; Kigathi et al., 2009; Ament 40 mg/day) to elevate plot-level abundance of predaceous and par- et al., 2010; Staudt et al., 2010). It also constitutes the active ingre- asitic arthropods in commercial hop yards and grape vineyards but dient for PredaLure (AgBio, Inc., Westminster, CO, USA), a pur- varied lure density across farms. In James and Price (2004), 448 ported natural enemy attractant that was recently developed and lures were deployed per hectare in the hops experiment, whereas marketed for use in pest management. Although attraction to 2297 per hectare were used in the vineyard experiment, a >5-fold MeSA has been relatively weak in some studies (Zhang et al., difference. Although natural enemies occurred at higher densities 2006a,b; Jones et al., 2011), most have documented strong in MeSA-baited plots than MeSA-free plots in both experiments, attraction for at least certain taxa. Overall densities of predaceous the magnitude of this increase was considerably greater for the insects in hop yards were 4-times higher in MeSA-baited compared low lure density (448/ha). The same outcome was observed in a with control plots (James and Price, 2004). Notably, a recent companion trial where MeSA lures were applied at a range of den- meta-analysis reviewed evidence for MeSA as a broad-spectrum sities from 180 to 642 per hectare (James et al., 2005). Again, pre- attractant and found significant field responses for key beneficial dators were attracted regardless of density, but the low rate plot insect groups including Anthocoridae, Coccinellidae, Syrphidae, (180/ha) was considerably more attractive than the high rate ones 80 I. Kaplan / Biological Control 60 (2012) 77–89

(447–642/ha). These results should be interpreted with caution be- creased aphid parasitism from 8.5% to 22.5% (Titayavan and Altieri, cause the low and high rates were not replicated in either study 1990); (Z)-3-hexenyl acetate and a-farnesene caused a 2- to 3-fold and were confounded by crop-type differences, but the data are elevation in egg parasitism of Lygus lineolaris (Palisot de Beauvois) at least suggestive that less is more when it comes to lure density in a cotton field (Williams et al., 2008); and 3,7-dimethyl-1,3,6- and recruitment of beneficial arthropods. Additional studies are octatriene elicited a significant, albeit minor, rise in parasitism of clearly needed in this area; until that time, decisions on release tar- the lepidopteran cotton pest Helicoverpa armigera (Hübner) in field gets and lure densities will be speculative at best. cages (Yu et al., 2010). In the two studies that tested predation rates, Mallinger et al. (2011) compared caged vs. uncaged soybean 2.2. Moving beyond point-source attraction to field-scale plants in MeSA baited and unbaited plots to show that increased manipulation predation is the mechanism behind MeSA-induced declines in aphid populations; and Ferry et al. (2009) found that egg predation Field research on synthetic HIPVs has thus far been overwhelm- on the cabbage root fly Delia radicum (L. 1758) was the same or ingly biased towards point-source attraction, usually by affixing slightly lower in broccoli plots with dimethyl disulfide lures. the odor source to a sticky trap (Table 1). This approach is useful Although point-source studies still far outnumber those evalu- in addressing several of the issues highlighted above, namely for ating functional changes, most of the studies cited in this section evaluating which HIPV blends attract which natural enemies and have only emerged within the past several years. This appears to fine-tuning release rates. It is less useful, however, in understand- be a clear indication that investigations are shifting toward lar- ing the functional components of attraction, i.e., can we increase ger-scale tests that are ultimately needed to assess the utility of the density of carnivorous arthropods on plants? Can we elevate HIPVs in biocontrol and counter-balance those aimed at optimizing the frequency of predation or parasitism on pests? attraction. Several studies have documented an increase in the abundance of entomophagous arthropods in field plots baited with HIPVs 2.3. Non-target effects (James and Price, 2004; James and Grasswitz, 2005; Ferry et al., 2009; Lee, 2010; Mallinger et al., 2011; Simpson et al., 2011a,b). In a review of behavior-modifying strategies in arthropod pest Unfortunately, most of these studies used sticky card sampling management, Rodriguez-Saona and Stelinski (2009) compare and and it is therefore unknown whether the individuals are remaining contrast the application of host-plant volatiles vs. sex pheromones. in the baited area to forage for prey or simply passing through. James This is an intriguing comparison because the latter has been more and Price (2004) provide the most convincing on-plant data based intensively studied than the former and thus the field of HIPVs has on canopy shake samples in MeSA-baited and unbaited hop yards; much to gain by learning from the past successes and failures of compared with the unbaited plots, on-plant densities of Orius tristi- pheromone research. However, plant volatiles and sex pheromones color (White) and Stethorus punctum picipes (Casey) increased by > fundamentally differ in one crucial attribute – pheromones are 7-fold and >57-fold, respectively, in baited areas. Even more impres- highly specific to a single species, sex, and developmental stage sive is that these dramatic differences are calculated from the sea- of insect, whereas plant volatiles are quite the opposite, widely sonal means (May–September) of a weekly sampling regime and accessible to eavesdropping by a range of species and trophic lev- are not based on a single outlier date. Lee (2010) also found elevated els. This, unfortunately, makes plant volatile manipulations more on-plant natural enemy abundance in strawberry plots with MeSA susceptible to undesirable non-target effects. The adoption of HIP- lures, but only on a few dates over a 2-year period. Vs in agriculture in large part hinges on the severity of such non- Assuming carnivores can be attracted to a broad area, can we target effects and our ability to minimize them. then convince them to stay in this area? Ideally, this would be Pest responses to plant volatiles are variable. It is considered tested by tracking oviposition responses to determine whether adaptive for herbivorous insects to exploit constitutively emitted arthropods view it as a profitable patch. In a laboratory experi- volatiles in host-plant location and colonization (Szendrei and ment, Harmonia axyridis Pallas placed more than twice as many Rodriguez-Saona, 2010). Damage-induced volatiles, however, sig- eggs on bean plants exposed to a rubber septum infused with nify a poor quality or otherwise occupied host-plant and herbi- either limonene or b-caryophyllene (Alhmedi et al., 2010). Two vores should be repelled by these signals (except for cases when studies have tested for this HIPV-induced egg laying response in high herbivore pressure is required to overcome plant defenses, the field. Despite finding substantially higher numbers of natural e.g., Ips bark beetles attacking pine trees). Induced volatiles are in- enemies on sticky cards in soybean plots with MeSA lures, Mallinger deed repellant to quite a few herbivorous pests (Hardie et al., 1994; et al. (2011) found no corresponding difference in the per plant Bernasconi et al., 1998; De Moraes et al., 2001; Sanchez-Hernandez number of eggs or larvae of hoverflies, lacewings, or lady beetles. et al., 2006), but not universally so (Landolt et al., 1999; Halitschke Kunkel and Cottrell (2007), on the other hand, documented in- et al., 2008). Given that this topic has been extensively discussed in creased oviposition of the green lacewing Chrysoperla rufilabris previous reviews (Pickett et al., 2006; Cook et al., 2007; Khan et al., (Burmeister) on pecan branches treated with caryophyllene. 2008), I will not comment further here other than to note that most Last, and most importantly, if natural enemies are attracted and of the community-level field surveys cited in Table 1 included at convinced to stay in an area, will they stay and eat? Altieri et al. least some herbivores, the majority of which were not attracted (1981) originally tested this by spraying crude plant extracts of to the HIPV tested (but see Molleman et al., 1997; Orre et al., 2010). corn or Amaranthus onto a range of crops, which more than dou- Two non-target pathways have not received nearly the same le- bled the rate of Trichogramma parasitism on Heliothis zea (Boddie) vel of scrutiny as with herbivores. First, 4th trophic level consum- eggs. Of studies that have assessed synthetic HIPVs, several have ers may be attracted to HIPVs, which could disrupt the 3rd trophic inferred pest suppression due to correlative patterns of higher level, relaxing pest suppression. This was recently described for a predator densities and fewer herbivores in HIPV-treated plots study that caught higher numbers of lacewing parasitoids, Ana- (e.g., James and Price, 2004). While predation pressure may indeed charis zealandica Ashmead (Hymenoptera: Figitidae), in a turnip underlie this pattern, it cannot be causally demonstrated because field with MeSA lures (Orre et al., 2010). Second, it is rather sur- HIPVs also have direct effects on pest colonization and host-plant prising that pollinators have not been considered in the debate quality (see Section 2.3.). Three studies have directly tested the on this topic given the recent attention devoted to colony collapse manipulation of synthetic HIPVs to enhance pest parasitism in disorder and global declines in native bees (Potts et al., 2010; Cameron the field: application of allyl isothiocyanate to broccoli plants in- et al., 2011). Pollinators rely heavily on floral volatiles in their I. Kaplan / Biological Control 60 (2012) 77–89 81

Table 1 List and outcome of field studies using synthetic HIPVs as lures for predaceous and parasitic arthropods in agricultural crops. A species was considered to be ‘attracted’ if it occurred at significantly (P < 0.05) higher abundance on a trap or in a plot baited with the focal HIPV for at least one sampling date.

HIPVa Natural enemies attractedb,c Species not respondingb,c References Allyl isothiocyanates Diaeretiella rapae (Braconidae) Omphale clypealis (Eulophidae), Platygaster Murchie et al. (1997) and Titayavan and subuliformis (Platygastridae) Altieri (1990) Benzaldehyde Chrysoperla plorabunda (Chrysopidae), Anagrus daanei (Mymaridae), Braconidae, Chrysopa James (2005), Jones et al. (2011), Oakley Orius tristicolor (Anthocoridae), nigricornis (Chrysopidae), Chrysopa oculata and Smart (2002), and Zhang et al. Sarcophagidae, Stethorus punctum picipes (Chrysopidae), Dolichopodidae, Empididae, (2006b) (Coccinellidae), Tachinidae Frankliniella occidentalis (Thripidae), Geocoris pallens (Lygaeidae), Lygus hesperus (Miridae), Macroglenes penetrans (Pteromalidae), micro-Hymenoptera, O. tristicolor, Syrphidae, Therevidae b-Bisabolene – Chrysopa carnea (Chrysopidae), Collops vittatus Flint et al. (1979, 1981) (Melyridae) Caryophyllene C. carnea C. carnea, C. vittatus Dean and Satasook (1983) and Flint et al. (1979, 1981) b-Caryophyllene C. carnea C. carnea, C. vittatus, Coleomegilla maculata Flint et al. (1979), Oakley and Smart (Coccinellidae), M. penetrans (2002), Tóth et al. (2009), and Zhu et al. (1999, 2005) Caryophyllene C. vittatus – Flint et al. (1981) alcohol Caryophyllene oxide C. vittatus C. carnea, C. vittatus Flint et al. (1979, 1981) Decanal – Campoletis chlorideae (Ichneumonidae), Chrysopa Yu et al. (2008) sinica (Chrysopidae), Coccinella septempunctata (Coccinellidae), Deraeocoris punctulatus (Miridae), Epistrophe balteata (Syrphidae), Erigonidium graminicolum (Micryphantidae), Geocoris pallidipennis (Lygaeidae), Macrocentrus linearis (Braconidae), Orius similis (Anthocoridae), Paragus quadrifasciatus (Syrphidae), Propylaea japonica (Coccinellidae) Dimethyl disulfide Aleochara bilineata (Staphylinidae), – Ferry et al. (2007, 2009) Aleochara bipustulata (Staphylinidae), Bembidion sp. (Carabidae) 3,7-Dimethyl-1,3,6- M. linearis, O. similis, P. quadrifasciatus C. chlorideae, Coccinella septempunctata, C. sinica, D. Yu et al. (2008) octatriene punctulatus, E. balteata, E. graminicolum, G. pallidipennis, P. japonica (E)-4,8-Dimethyl- – Anagrus sp., C. nigricornis, Coccinellidae, Deraeocoris James (2003a,b) 1,3,7-nonatriene brevis (Miridae), G. pallens, Hymenoptera, L. hesperus, Leptothrips mali (Phlaeothripidae), Miridae, O. tristicolor, S. punctum, Syrphidae Farnesene A. daanei Braconidae, Dolichopodidae, F. occidentalis, L. James (2005) hesperus, O. tristicolor, S. punctum, Sarcophagidae, Tachinidae, Therevidae (E)-b-Farnesene – C. carnea, C. maculata Zhu et al. (1999, 2005) Geraniol Braconidae, Sarcophagidae A. daanei, Dolichopodidae, Empididae, F. occidentalis, James (2005) G. pallens, L. hesperus, micro-Hymenoptera, O. tristicolor, S. punctum, Syrphidae, Tachinidae, Therevidae 1-Hexanol – C. carnea, C. maculata Zhu et al. (1999, 2005) Trans-2-hexen-1-al G. pallens A. daanei, Braconidae, Dolichopodidae, Empididae, F. James (2005) occidentalis, L. hesperus, micro-Hymenoptera, O. tristicolor, S. punctum, Sarcophagidae, Syrphidae, Tachinidae, Therevidae (Z)-3-Hexen-1-ol A. daanei, Braconidae, M. linearis, micro- C. carnea, C. chlorideae, C. maculata, C. sinica, Coccinella James (2005), Yu et al. (2008), and Zhu Hymenoptera, O. tristicolor, S. punctum, septempunctata, D. punctulatus, Dolichopodidae, E. et al. (1999, 2005) Syrphidae balteata, E. graminicolum, Empididae, F. occidentalis, G. pallens, G. pallidipennis, L. hesperus, O. similis, O. tristicolor, P. japonica, P. quadrifasciatus, Sarcophagidae, Tachinidae, Therevidae (Z)-3-Hexenal – C. carnea, C. maculata Zhu et al. (1999, 2005) (Z)-3-Hexenyl Anagrus sp., Braconidae, C. nigricornis, A. daanei, Anagrus sp., C. chlorideae, C. nigricornis, C. James (2003a,b, 2005), James and acetate Coccinella septempunctata, D. brevis, E. oculata, C. sinica, Coccinellidae, D. punctulatus, Grasswitz (2005), Jones et al. (2011), Yu graminicolum, Metaphycus sp. Dolichopodidae, E. balteata, Empididae, F. occidentalis, et al. (2008), Zhang et al. (2006b), and (Encyrtidae), O. similis, O. tristicolor, S. G. pallens, G. pallidipennis, L. hesperus, L. mali, M. Zhu et al. (2005) punctum linearis, micro-Hymenoptera, Miridae, O. tristicolor, P. japonica, P. quadrifasciatus, S. punctum, Sarcophagidae, Syrphidae, Tachinidae, Therevidae Indole C. oculata, G. pallens, micro-Hymenoptera A. daanei, Braconidae, C. carnea, Dolichopodidae, James (2005) and Zhu et al. (2005) Empididae, F. occidentalis, L. hesperus, O. tristicolor, S. punctum, Sarcophagidae, Syrphidae, Tachinidae, Therevidae Isopropanol Chrysopa quadripunctata (Chrysopidae) – Pszczolkowski and Johnson (2011) Cis-jasmone Braconidae, Sarcophagidae A. daanei, Dolichopodidae, Empididae, G. pallens, James (2005) Syrphidae, O. tristicolor, micro-Hymenoptera, F. occidentalis, L. hesperus, Therevidae, S. punctum, Tachinidae

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Table 1 (continued)

HIPVa Natural enemies attractedb,c Species not respondingb,c References Limonene Harmonia axyridis (Coccinellidae) C. carnea, C. vittatus, Episyrphus balteatus (Syrphidae) Alhmedi et al. (2010), and Flint et al. (1979, 1981) Linalool – A. daanei, Braconidae, Dolichopodidae, Empididae, F. James (2005) occidentalis, G. pallens, L. hesperus, micro- Hymenoptera, O. tristicolor, S. punctum, Sarcophagidae, Syrphidae, Tachinidae, Therevidae Methyl anthranilate Braconidae A. daanei, C. carnea, Dolichopodidae, Empididae, F. James (2005), and Tóth et al. (2009) occidentalis, G. pallens, L. hesperus, micro- Hymenoptera, O. tristicolor, S. punctum, Sarcophagidae, Syrphidae, Tachinidae, Therevidae Methyl eugenol C. carnea, Chrysopa basalis (Chrysopidae), C. nigricornis James (2003b), Suda and Cunningham Chrysopa albolineata (Chrysopidae) (1970), Umeya and Hirao (1975), and Tóth et al. (2009) Methyl jasmonate Anagrus sp., Braconidae, Metaphycus sp. A. daanei, Dolichopodidae, Empididae, F. occidentalis, James (2005) and James and Grasswitz G. pallens, L. hesperus, micro-Hymenoptera, O. (2005) tristicolor, S. punctum, Sarcophagidae, Syrphidae, Tachinidae, Therevidae Methyl salicylate Aeolothrips sp., Anagrus sp., Araneae, A. daanei, Anagrus sp., Anthocoridae, Anthocoris sp. James (2003a,b, 2005, 2006), James and Braconidae, C. carnea, C. nigricornis, C. (Anthocoridae), Braconidae, C. carnea, C. chlorideae, C. Price (2004), James and Grasswitz (2005), oculata, C. plorabunda, Coccinella nigricornis, C. oculata, C. plorabunda, Coccinella Jones et al. (2011), Lee (2010), Mallinger septempunctata, Chalcidoidea, septempunctata, C. sinica, Chilopoda, Chloropidae, et al. (2011), Molleman et al. (1997), Orre Chrysopidae, Coccinellidae, D. brevis, Chrysopa septempunctata (Chrysopidae), et al. (2010), Rodriguez-Saona et al. Diadegma semiclausum (Ichneumonidae), Coccinellidae, D. brevis, D. punctulatus, (2011a,b), Tóth et al. (2009), Yu et al. E. graminicolum, Empididae, Episyrphus Dolichopodidae, E. balteata, E. balteatus, F. occidentalis, (2008), Zhang et al. (2004, 2006a,b), and auricollis (Syrphidae), G. pallens, G. pallidipennis, H. axyridis, Hemerobius sp., Zhu and Park (2005) Hemerobius sp. (Hemerobiidae), Hymenoptera, Ichneumonidae, L. hesperus, L. mali, M. Metaphycus sp., Metasyrphus luniger linearis, Metasyrphus corollae (Syrphidae), Miridae, (Syrphidae), micro-Hymenoptera, Orius Nebria brevicollis (Carabidae), Opiliones, O. insidiosus sp., O. similis, O. tristicolor, S. punctum, (Anthocoridae), P. japonica, P. quadrifasciatus, Panorpa Sarcophagidae, Syrphidae, Syrphus ribesii sp. (Panorpidae), Pterostichus melanarius (Carabidae), (Syrphidae), Tachinidae, Toxomerus Sarcophagidae, Staphylinidae, Stethorus sp., marginatus (Syrphidae) Tachinidae, Therevidae Nonanal E. graminicolum, O. similis, Sarcophagidae A. daanei, Braconidae, C. chlorideae, Coccinella James (2005), and Yu et al. (2008) septempunctata, C. sinica, D. punctulatus, Dolichopodidae, E. balteata, F. occidentalis, G. pallidipennis, L. hesperus, M. linearis,O.tristicolor, P. japonica, P. quadrifasciatus, S. punctum, Tachinidae, Therevidae Octanal D. punctulatus, P. quadrifasciatus C. chlorideae, Coccinella septempunctata, C. sinica, E. Oakley and Smart (2002) and Yu et al. balteata, E. graminicolum, G. pallidipennis, M. linearis, (2008) M. penetrans, O. similis, P. japonica 3-Octanone – A. daanei, Braconidae, Dolichopodidae, F. occidentalis, James (2005) L. hesperus, O. tristicolor, S. punctum, Sarcophagidae, Tachinidae, Therevidae 1-Octen-3-ol – C. carnea, C. maculata Zhu et al. (1999, 2005) Octyl aldehyde A. daanei, O. tristicolor Braconidae, Dolichopodidae, F. occidentalis, L. James (2005) hesperus, S. punctum, Sarcophagidae, Tachinidae, Therevidae Phenylacetaldehyde C. carnea M. penetrans Oakley and Smart (2002), and Tóth et al. (2006, 2009) 2-Phenylethanol C. maculata, C. carnea, H. axyridis, C. carnea, C. maculata, C. nigricornis, C. oculata, Sedlacek et al. (2009), Tóth et al. (2009), Syrphidae Coccinella septempunctata, H. axyridis Zhang et al. (2006b), Zhu et al. (1999, 2005), and Zhu and Park (2005) 2-Phenylethyl P. subuliformis O. clypealis Murchie et al. (1997) isothiocyanates a-Pinene – C. carnea, C. vittatus Flint et al. (1979, 1981) Squalene C. nigricornis – Jones et al. (2011) a-Terpineol C. maculata C. carnea Zhu et al. (1999, 2005)

a Only HIPVs tested as single compounds are reported, not blends of several compounds. b Reported to species-level if possible, otherwise recorded as the lowest possible taxonomic affiliation (i.e., family or order). c In certain cases, two or more studies reported conflicting results for attraction of the same natural enemy species to a particular HIPV; these species are included in both columns. foraging (Dudareva and Pichersky, 2006; Kessler et al., 2008; Raguso, from leaves are constitutively emitted from flowers (Brodmann 2008), and deploying HIPVs could have detrimental effects on the et al., 2008; Kessler and Halitschke, 2009). The active ingredients success or efficiency of crop pollination, offsetting any of the for two commercially available carnivore attractants, PredaLure benefits gained by pest control. Notably, synthetic HIPVs have been and Benallure (MSTRS Technologies, Ames, IA, USA) are MeSA tested for their biocontrol potential in several crops where pollin- and 2-phenylethanol, respectively; these two compounds are also ators are required such as apple (Jones et al., 2011), cherry (Tóth common components of odor blends released from flowers et al., 2009), and cranberry (Rodriguez-Saona et al., 2011b). While (Primante and Dotterl, 2010; Rodriguez-Saona et al., 2011b). the consequences of attracting predators and parasitoids for polli- It is not a foregone conclusion that HIPVs will necessarily deter nator behavior have yet to be evaluated in the field, the interaction pollinators. In theory, a predator foraging for prey is comparable to seems likely considering that many of the same HIPVs emitted a pollinator foraging for flowers. If volatiles pull in predators to in- I. Kaplan / Biological Control 60 (2012) 77–89 83 crease predation, would they not also pull in pollinators to increase cur on plants growing near the lures or is the entire field of plants pollination? The pollinator attractant, Bee-Scent (Scentry Biologi- affected? Keep in mind that the scenarios outlined above are not cals, Inc., Billings, MT, USA), was developed to manipulate pollina- mutually exclusive processes, but for simplicity’s sake they will tor behavior in the same sense as carnivore attractants, but has be treated as such below. thus far had limited success in improving crop yield (Waller, If natural enemies respond directly to the synthetic compound 1970; Schultheis et al., 1994). (i.e., assuming a scenario where plants do not play an active role Future HIPV field manipulations would benefit from a food web in attraction), then pest-induced signals from the crop may be ig- approach that quantifies the impact of the released compound on nored in favor of lures. This may nevertheless prove beneficial if predators, parasitoids, pests, and pollinators. This could be paired an increase in natural enemy abundance compensates for the de- with path analysis to estimate direct and indirect effects on crop cline in per-capita effects on prey. In other words, it might be bet- yield through various trophic pathways (e.g., Eubanks, 2001). It ter to have 10 lady beetles per plant, each of which consumes five would also be useful to selectively compare crops that differ in their aphids per day (50 total), than to have two lady beetles per plant, degree of pollinator reliance and/or behavior of their primary pests. each of which consumes 10 aphids per day (20 total). In the end, it For example, crops that produce tubers belowground such as potato comes down to a trade-off between population-level abundance vs. obviously do not require pollination and the likelihood for non-tar- individual foraging efficiency. Should efficient predators be sacri- get effects in these systems is minimized. But potato also has a spe- ficed for more predators? Of course, no study has yet demonstrated cialist pest, Colorado potato beetle Leptinotarsa decemlineata (Say), that efficiency decreases in HIPV-baited fields and this remains a that is attracted to damaged-induced volatiles and may preferen- major untested assumption (but see Ferry et al., 2009). Another tially colonize fields baited with synthetic HIPVs (Bolter et al., important consideration in evaluating this trade-off is temporal 1997; Landolt et al., 1999). Cucurbits, on the other hand, are highly scale. In the short-term low efficiency consumers may be accept- dependent on pollinators, but their major pests include aphids able, but in the long-term inefficient predators and parasitoids that are more likely to be repelled by HIPVs (Hardie et al., 1994; could have lower fecundity leading to a population decline (Powell, Bernasconi et al., 1998; Turlings and Wäckers, 2004). Because the 1986). From the opposing view, aggregating species into a single nature and relative importance of non-target effects change from field may also increase the likelihood of finding a mate, ultimately one crop to the next, the net impact of HIPVs on crop yield and thus resulting in higher fitness. their applied value will likely co-vary with these factors. If arthropods are responding to volatiles emitted from the crop, it is critical to differentiate between fully induced vs. primed 2.4. Mechanisms of attraction and prey suppression plants. If all plants are induced, this should decrease foraging effi- ciency, as described above, because of consumers following ‘false Despite a sharp rise in the number of field studies on attraction leads’ to prey-free patches (Vinson, 1977; Puente et al., 2008). If to plant volatiles, we still have little to no knowledge of what ento- plants are primed by synthetic compounds, however, this is pre- mophagous arthropods are actually responding to. Are the syn- dicted to elicit stronger and more rapid pest-induced responses thetic lures directly mediating attraction (Fig. 1, Scenario #1) or from the crop, resulting in more efficient prey location (Pickett indirectly via volatiles emitted from crops whose indirect defenses and Poppy, 2001; Turlings and Ton, 2006; Dudareva and Pichersky, were triggered by exposure to lures? If the latter, did synthetic 2008; Khan et al., 2008). HIPVs induce plants to indiscriminately release their full comple- Several recent studies provide some insight into the likelihood ment of damage-induced volatiles (Fig. 1, Scenario #2) or prime of synthetic lures indirectly attracting natural enemies via crop them to respond stronger when attacked by pests (Fig. 1, Scenario volatiles. First, two studies found attraction of carnivores to #3)? What is the spatial scale of this phenomenon? Does it only oc- vegetable crops treated with foliar sprays of synthetic HIPVs mixed

Natural enemy attraction?

Reduced foraging efficiency? 2 3 1 Habituation? Amplified HIPV Induction? Priming? response?

Synthetic MeSA

Fig. 1. Potential mechanisms underlying natural enemy attraction to fields baited with synthetic HIPVs, in this case using MeSA as an example. In Scenario 1, parasitoids are directly attracted to MeSA being emitted from slow-release dispensers embedded within the crop. In Scenario 2, parasitoids are responding to plant-derived HIPVs that were induced via exposure to synthetic lures. In these first two scenarios, natural enemy foraging efficiency is predicted to decrease because the signal is not associated with the presence of herbivores and thus wasps waste time searching prey-free plants. In Scenario 3, lures prime neighboring plants, which then amplifies the pest-induced volatile response that occurs when the crop is damaged. In all cases, habituation is a prime concern from over-exposing entomophagous arthropods to large quantities of the focal compound. 84 I. Kaplan / Biological Control 60 (2012) 77–89 in botanical oil (Simpson et al., 2011a,b). Because attraction was designed for pests (Cook et al., 2007), but with stimuli working in maintained for up to six days after application, the authors con- the opposite direction. cluded that sprays induced the crops to release endogenous vola- Another important spatial consideration is the scale of lure tiles. Second, Rodriguez-Saona et al. (2011b) placed cranberry attraction. Virtually all of the plot-level HIPV manipulations have vines near PredaLure sachets containing MeSA in a greenhouse been conducted within spatial blocks that co-occur in the same and found that exposed plants subsequently emitted far more field but are separated by 100 m or more. If higher densities are MeSA from their leaves. Interestingly, unexposed plants did not re- found in the HIPV-baited block, those individuals were likely lease detectable quantities of MeSA and the induced response may pulled from non-experimental sections of the same field rather therefore have been a passive process whereby the compound was than increasing immigration from outside of the field. Thus, adsorbed and re-released. Last, a field trial was reported in which a HIPV-mediated natural enemy augmentation is likely a conse- four-part blend of synthetic green leaf volatiles were emitted from quence of redistributing individuals within an area rather than controlled-release dispensers in corn plots; volatiles were then col- truly elevating the population in that field (Mallinger et al., lected from the head-space of adjacent corn plants and analyzed 2011). This could be exploited for spot-treating pests, which are of- for differences compared with unexposed plants (von Mérey ten patchily distributed, by herding beneficial insects from one et al., 2011). Similar to Rodriguez-Saona et al. (2011b), the lure ex- outbreak to the next. Biocontrol manipulations are frequently posed plants released more volatiles, in this case sesquiterpenes. couched in military terminology and predator herding would be As a whole, the above studies demonstrate that plants are likely equivalent to redeploying the troops. playing a key role in arthropod attraction to lures, but none of these experiments were designed to differentiate whether or not 2.6. Context-dependent responses priming occurred and this remains an important missing piece of the puzzle. For HIPVs to be useful as a pest management tool, their impact on beneficial arthropods must be predictable and reliable, but the 2.5. Spatial and landscape-level considerations published literature on natural enemy field attraction suggests otherwise. The same compound that elicits a positive response in Considering that attraction by nature is a spatial phenomenon, one study, sometimes has no effect on the same species in subse- it is surprising that few studies to date have integrated a spatial quent studies (e.g., Chrysoperla carnea Steph. attraction to caryo- component into their experiments (Lee, 2010; Mallinger et al., phyllene in Flint et al. (1979) vs. Dean and Satasook (1983)). 2011; Rodriguez-Saona et al., 2011b). This may be a function of Similarly, significant HIPV  time statistical interactions are com- scale – historically, plant volatiles have been studied in controlled monly reported from experiments (James, 2003a; James and Price, laboratory settings, which do not allow for a spatial context (Hun- 2004; James and Grasswitz, 2005; Ferry et al., 2009; Lee, 2010; ter, 2002). In an open field setting, however, a finite number of Mallinger et al., 2011; Rodriguez-Saona et al., 2011b), meaning that individuals exist in a population and pulling some of those individ- the magnitude of attraction is highly variable from one week to the uals into a concentrated area necessarily means removing them next. The mediating factors that drive this variation can be grouped from other areas (Gross, 1981). This was originally noted by Vinson into one of the following three categories: (i) taxonomic artifact, (1977) in his review on kairomone manipulations of wasp behav- (ii) exogenous factors, and (iii) endogenous factors. ior: ‘‘the constant attraction and retention of parasitoids in the tar- get area may result in the depletion of these insects from 2.6.1. Taxonomic artifact surrounding areas... The loss of parasitoids from untreated crops Many field studies evaluate attraction at the community-level, could result in aggravated pest problems in those areas ‘‘robbed’’ which is ideal for comparing responses across divergent arthropod of their normal parasitoid complement’’. Jones et al. (2011) voiced groups but virtually always entails sacrificing taxonomic resolu- similar concerns in their ‘‘robbing Peter to pay Paul’’ scenario de- tion. This is especially the case in speciose taxa such as wasps that scribed for lacewing attraction in orchards. are often broadly categorized as Hymenoptera or micro-Hymenop- Like most of the concerns surrounding HIPV application, there tera. Even family-level identification is problematic when that are virtually no field data to substantiate this worry. This is not family constitutes a complex of several or more species, which is to say that the concern is unfounded, but rather that future field likely the norm. Thus, seemingly context-dependent responses experiments need to be explicitly designed with spatial dynamics may simply be a taxonomic artifact whereby differences in attrac- in mind. The central question here is: Are predator and parasitoid tion can be explained by species-specific responses. This cannot populations source limited? This will likely depend on the size of explain all of the across- and within-study discrepancies observed the area targeted for natural enemy enhancement and the strength in the literature, but it almost certainly underlies some of it. of the pull exerted on them. It seems logical to predict that smaller One could easily imagine a scenario where a treatment  time acreage fruit and vegetable crops are less likely to deplete local interaction was detected for attraction of syrphid flies, for instance, sources than large acreage field crops. This will also hinge on to a trap baited with some HIPV, but the response is stronger late in how large the source population is and from where it originates the summer than it is early in the summer. What if syrphids (i.e., neighboring crops or uncultivated habitats). HIPV manipula- consisted of two species differing in their phenologies such that tions are predicted to be most effective in heterogeneous land- Species 1 emerges in May–June and Species 2 in July–August? If scapes consisting of a mosaic of crop fields and natural habitats, Species 2 is inherently attracted to the focal compound and Species with biocontrol agents taking refuge from disturbance (e.g., pesti- 1 is not, then the temporal variation observed is merely explained cides, tillage, cold winter temperatures) in non-crop areas which by species-level differences in attraction rather than context- later serve as a reservoir to re-colonize agricultural lands (Khan dependency. The more species that are lumped into a broad cate- et al., 2008; Mallinger et al., 2011). Although biological pest sup- gory such as family or order, the more likely that these taxonomic pression tends to be most effective in complex compared with sim- artifacts become. ple landscapes (Marino and Landis, 1996; Tscharntke et al., 2005; A good real-life example of this phenomenon can be observed Bianchi et al., 2006; Gardiner et al., 2009), we do not yet know if across experiments that have assessed the field attraction of lace- synthetic lures work best when sources and sinks are aligned such wings (Chrysopidae) to synthetic MeSA. Some studies have docu- that non-crop habitats ‘push’ and HIPVs ‘pull’ natural enemies into mented attraction (James, 2003b, 2006; Lee, 2010; Jones et al., agricultural fields. This would be analogous to a push–pull system 2011; Mallinger et al., 2011), while others have found no response I. Kaplan / Biological Control 60 (2012) 77–89 85

(Zhang et al., 2004, 2006a,b; Zhu and Park, 2005; Yu et al., 2008; are expected to be highly variable among carnivores in the field Tóth et al., 2009). Upon closer evaluation, four of the six studies and correlate strongly with chemotactic response to HIPVs. failing to find attraction worked with lacewing species that were Additional factors, such as population age-structure, undoubt- never tested in the studies documenting attraction: C. carnea edly play key roles in explaining context-dependency. Field studies (Zhu and Park, 2005; Tóth et al., 2009), Chrysopa septempunctata that seek to gain a mechanistic understanding of when, where, and Wesmael (Zhang et al., 2006a), and Chrysopa sinica Tjeder (Yu why arthropods respond to HIPVs would be extremely valuable. et al., 2008). James (2003b, 2006) speculated that interspecific dif- ferences in lacewing response to MeSA may be partially explained 2.7. Temporal stability of attraction by dietary variation in the adult stage. Because MeSA is a putative indication of prey availability, it should attract lacewing species Arthropod attraction to olfactory cues is a consequence of in- whose adults are carnivorous but not those that specialize on pol- nate and acquired odor preferences (Papaj and Lewis, 1992; Dukas, len and/or nectar. That being said, the remaining studies report 2008; Matthews and Matthews, 2010). In the case of natural en- inconsistent responses that cannot be explained by species-level emy orientation to plant volatiles, acquired preferences (i.e., asso- differences for Chrysopa nigricornis Burmeister, C. oculata Say, and ciative learning) are considered to be of paramount importance Chrysoperla plorabunda (Fitch). (Lewis and Tumlinson, 1988; Turlings et al., 1992; Drukker et al., 2000; De Boer and Dicke, 2004, 2006), particularly with regard to polyphagous consumers (Vet and Dicke, 1992; Steidle and van 2.6.2. Exogenous and endogenous factors Loon, 2003; Glinwood et al., 2011). Field-caught individuals of True context-dependent outcomes can be partitioned into those the anthocorid predator, Anthocoris nemoralis (Fabricius), for exam- driven by exogenous or endogenous factors (Yu et al., 2008). Exog- ple, were highly attracted to the scent of psyllid-infested pear enous factors are those external to the arthropod in question but leaves, but after one generation reared in the lab on flour moth inherent in the study system at large. Although this can encompass eggs this preference disintegrated (Drukker et al., 2000). When a large number of potential explanatory variables, perhaps the lab-reared individuals were subsequently offered prey in the pres- most important for biocontrol purposes is the plant matrix that ence of synthetic MeSA, their preference for this induced volatile synthetic lures are embedded in. Background odors are known to returned. In a similar study, the lady beetle Coccinella septempunc- have an overriding influence on olfactory detection (Dicke et al., tata L. learned to associate subtle shifts in the volatile profiles of 2003; Schröder and Hilker, 2008), and thus lures may differentially four barley cultivars with the presence of their aphid prey after pull depending on crop background. Flint et al. (1979) invoked 24 h of exposure (Glinwood et al., 2011). Notably, lady beetles only lure-crop competition as a factor explaining the seasonal variation retained this memory for a brief period of time; after four days in trap catch of lacewings, C. carnea, in response to synthetic caryo- without reinforcing the aphid-cultivar pairing, the beetles no long- phyllene deployed in cotton fields. Caryophyllene was highly er displayed a preference for the learned odor. If these species are attractive early in the growing season when cotton plants were representative of predators at large, it suggests that preference small, but as the crop matured response to the lures diminished. hierarchies are highly plastic and natural enemies are constantly Because cotton synthesizes and emits caryophyllene, Flint and col- fine-tuning their behaviors to track variable environments (i.e., leagues proposed that waning responses to lures in late-season good short-term but poor long-term memory). cotton were a consequence of duplicating the plant’s odor; how- Learned odor preferences represent a fundamental challenge, ever, this hypothesis was not explicitly tested. It would be instruc- and perhaps the biggest impediment, to the sustainable manipula- tive for future studies to quantify attraction to synthetic tion of HIPVs in biocontrol. The worry is that natural enemies will compounds in crops where the odor is shared vs. those where it rapidly adapt to constitutively emitted volatiles in pest-free crop is unique. Phytochemically ‘novel’ signals should be easier for fields where signals are decoupled from rewards, leading to a arthropods to detect and orient towards compared with those di- ‘boy who cried wolf’ scenario (Lewis and Martin, 1990; Degenhardt luted by the crop’s emissions. This was also predicted by Hilker et al., 2003; Turlings and Ton, 2006). As a result, individuals could and McNeil (2008) in their ‘olfactory contrast hypothesis’ which ultimately ignore or, worse yet, perceive HIPVs as repellents if de- states that background odors can either camouflage hosts or facil- ployed indiscriminately. This can further be partitioned into two itate their discovery by parasitoid wasps exploiting HIPVs. core issues that will be addressed below: (a) the likelihood for Endogenous factors include those that are inherently associated habituation; and (b) minimizing the risk of habituation by coupling with the focal arthropod. For example, males and females may re- signals with food rewards. spond differently to the same attractant, and these differences can further be accentuated by mating history (Zhu et al., 1999, 2005; 2.7.1. Will the magnitude attraction to constitutively-emitted HIPVs Chen and Fadamiro, 2007; Kugimiya et al., 2010; Orre et al., diminish over time? 2010; Jones et al., 2011). Orre et al. (2010) found a significant As described above, entomophagous arthropods clearly have HIPV Â sex interaction for attraction of the ichneumonid wasp the capacity for olfactory learning in controlled laboratory settings. Diadegma semiclausum Hellén to MeSA-baited fields with female This has led to widespread concern that behavioral adaptation in responses far more pronounced than males. Therefore, spatiotem- field populations will occur rapidly. I do not intend to belittle the poral heterogeneity in sex ratios and mating status of field popula- gravity of this concern; however, I will take the devil’s advocate tions will likely correlate with the strength of responses to lures. position here since habituation is not inevitable (also see Turlings Another endogenous factor that is expected to have an overrid- and Ton, 2006). The existing large-scale field studies that have in- ing influence on attraction is hunger. We assume that natural ene- fused plots with synthetic compounds show no evidence for re- mies respond to HIPVs because they signal the presence of food; sponse attenuation (James and Price, 2004; James and Grasswitz, thus, all else being equal, a hungry individual should be more at- 2005; Ferry et al., 2009; Lee, 2010; Mallinger et al., 2011; Simpson tracted than one who is satiated. Alternatively, consuming herbiv- et al., 2011a,b). This would be evident if abundance in the control orous prey on crop or non-crop plants might reinforce cue-reward and treatment plots were strongly separated from one another relationships that are necessary to maintain field attraction via early in the season, but gradually converged over time. That being associative learning, in which case attraction may be positively said, no field trials have been specifically designed to test for associated with prey abundance (James, 2005). Although the direc- behavioral or physiological adaptation; until that time, all is hear- tion of hunger-attraction linkages remains debatable, hunger levels say. Ideally, naturally-occurring individuals would be collected 86 I. Kaplan / Biological Control 60 (2012) 77–89 from field plots with and without HIPV augmentation, returned to items (e.g., those herbivores occurring on weeds or cover crops), the lab, and immediately evaluated for odor responsiveness most of the discussion has revolved around floral borders since through EAG and/or olfactometer trials. If responses progressively the majority of entomophagous species are omnivores that readily waned over time in the HIPV plot, this would suggest that habitu- consume pollen and/or nectar (Lundgren, 2009). Similar ideas have ation is occurring and that the value of the manipulation is been proposed for combining attractants with artificial food sprays diminishing. (Flint et al., 1979; Kunkel and Cottrell, 2007). However, the few In many ways the potential for habituation of beneficial arthro- studies to date that have assessed synergistic HIPV–reward inter- pods to HIPVs is analogous to pest adaptation to insecticides or actions do not provide strong support (Kunkel and Cottrell, 2007; resistant crops. In both cases, the speed of change should be di- Simpson et al., 2011b). Additional experiments that test this strat- rectly proportional to the extent of exposure; when exposure lev- egy are needed before we can evaluate its value. Moreover, we els are high, adaptation should occur rapidly. Indeed, this logic need to know far more about the consequences of ‘calling’ preda- underlies the theoretical basis for pest resistance management, tors into fields with prey-signals and offering them floral re- i.e., the use of refuge plantings in Bt crops. I argue that three factors sources. This would be tantamount to ordering a steak and being are likely to affect natural enemy exposure and thus risk of habit- served a salad. It also assumes that we understand the true inten- uation to HIPVs. tions of foraging arthropods. As noted earlier, many HIPVs are com- First, long-term exposure necessitates that the species in ques- ponents of floral odor blends and thus individuals may be tion remains in the treated area for a substantial period of time. responding to the manipulated compound in search of a nectar Admittedly, the term ‘substantial’ is rather vague and needs clari- or pollen meal rather than prey. fication. Would 2 days be considered a ‘substantial’ amount of A comparable approach would entail using the focal pest as the exposure time? One week? The answer is entirely unknown, but reward in a strategy that might be termed ‘attract and release’ this could be evaluated by caging predators or parasitoids in plots whereby HIPVs are used to pull natural enemies into fields only for varying time intervals. However, highly mobile species are un- after pest density reaches some critical threshold. Because pests likely to remain in one area long enough for over-exposure to occur are already present, synthetic lures could then be deployed for a and, consequently, life-history differences among beneficial brief period (i.e., two or three weeks) to enhance colonization arthropods might lead to differing rates of habituation. Despite a and subsequently removed with the hope that pest-induced crop broad array of hunting strategies, higher trophic level consumers volatiles would then retain the colonizers. Depending on the pest are fairly mobile, especially generalists that evolved to track patch- species targeted, this would work best if volatile releases were syn- ily distributed prey aggregations through space. Thus, I cautiously chronized with oviposition such that eggs are just beginning to speculate that natural enemies are often pre-adapted to avoid hatch as natural enemy populations are building (Vinson, 1977). habituation because of their tendency for dispersal. The main benefits here are that carnivores would be trained to Second, field size will almost certainly play a central role in associate the volatile with the pest of interest and it would also determining exposure level. Immigration and emigration rates, minimize the risk of over-exposure. This strategy will require reg- and thereby overall community turnover, are expected to be inver- ularly scouting crops and establishing pest thresholds that take sely related to field size (e.g., Kareiva, 1985). Smaller fields have into account the lag time associated with population build-up of higher perimeter to area ratios, more exposed edge habitat, and predators and parasitoids. The primary drawback of this approach therefore greater exchange of individuals. Again, ‘small’ is a rela- is that tracking pest outbreaks via routine scouting is a time inten- tive term that needs clarification; there may be a threshold field sive and thus expensive process due to labor costs. Future experi- size beyond which HIPV augmentation is ill-advised. This may ex- ments would benefit from incorporating an economic analysis in plain why habituation is not evident in existing field experiments their studies to compare the costs associated with scouting and that use fairly small plot designs. It remains to be seen whether deployment vs. the benefits of enhanced biocontrol services. The commercial-scale farms are beyond the size threshold within cost/benefit trade-off will undoubtedly vary widely across pest which HIPVs would be advocated. species, crops, and production systems (i.e., conventional, organic, Last, exposure persistence and intensity can be mitigated by low-input IPM). applying fewer lures per unit area. This would allow for signal patchiness within a field such that carnivores intermittently forage 3. Conclusions through sections of high and low HIPV zones (Carthey et al., 2011). Relaxed exposure in the low concentration zones would then Returning to the original question posed in the title, it is still too maintain attraction in the high zones. As noted earlier, the limited soon to say whether or not HIPVs will someday become a valued evidence to date suggests that fewer MeSA lures attract more ento- cog in the toolbox of biocontrol practitioners or whether their mophagous arthropods compared with high density plots and cue manipulation is bound to backfire. The topics outlined above are patchiness may be the mechanism driving this pattern. among the key unanswered questions that need to be addressed before we can make this evaluation. However, other opportunities 2.7.2. Can the stability of HIPV attraction be maintained by coupling abound for integrating plant volatiles into biocontrol research. For signals with rewards? example, virtually all of the emphasis thus far has been on conser- Because of the emphasis on associative learning, food rewards vation biocontrol; yet the major limitation of augmentation bio- have been the primary focus of existing efforts to extend the tem- control is natural enemy dispersal from the release site (Collier poral stability of field attraction (Khan et al., 2008; Simpson et al., and Van Steenwyk, 2004). Volatiles could ultimately prove to be 2011b). This strategy, termed ‘attract and reward’, argues that as or more valuable as arrestants in augmentation than they are attenuation of natural enemy responses is a direct result of disas- as attractants in conservation, but this has not been pursued (see sociating prey-location cues from the prey itself. Therefore, cou- also Heimpel and Asplen, 2011 for opportunities in classical bio- pling food rewards with volatile lures is thought to maintain the control). Similarly, a major limitation in biocontrol impact on pests learned response, akin to training naturally occurring carnivores. is intraguild predation (Rosenheim and Harmon, 2006). If different Moreover, stable food supplies should maximize performance (lon- volatiles or volatile blends attract specific natural enemy taxa, HIP- gevity, fecundity, flight propensity, etc.) and residency once at- Vs could be used to draw in predator assemblages that minimize tracted to the targeted area. While in theory this could be intraguild interference and maximize prey suppression. This would accomplished using any suitable food including non-pest prey be an outstanding opportunity to fuse our ever-growing knowl- I. Kaplan / Biological Control 60 (2012) 77–89 87 edge of chemical ecology with community ecology. These and Dicke, M., Sabelis, M.W., Takabayashi, J., Bruin, J., Posthumus, M.A., 1990. 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