J Chem Ecol (2017) 43:487–492 DOI 10.1007/s10886-017-0847-7

Caterpillar-Induced Plant Volatiles Attract Adult

D. M. Suckling1,2 & A. M. El-Sayed1

Received: 31 October 2016 /Revised: 9 April 2017 /Accepted: 13 April 2017 /Published online: 6 May 2017 # Springer Science+Business Media New York 2017

Abstract Binary and ternary combinations of volatile organic Keywords Kairomone . Tortricidae . phenylacetonitrile . compounds identified earlier from caterpillar-infested apple 2-phenylethanol . Benzyl alcohol . Acetic acid . Eye-spotted foliage caught more than one thousand individuals of both budmoth . ocellana . Oblique-banded leafroller . sexes of several adult tortricid leafroller species in several Choristoneura rosaceana . Three-lined leafroller . days of trials conducted in apple orchards in southern British Pandemis limitata Columbia. A series of combinations with phenylacetonitrile, benzyl alcohol, and/or 2-phenylethanol and acetic acid en- abled substantial catches of both sexes of eye-spotted Introduction budmoth, Spilonota ocellana, oblique-banded leafroller, Choristoneura rosaceana and three-lined leafroller, Herbivore-induced plant volatiles that arise after herbi- Pandemis limitata. These findings suggest that new monitor- vore attack on plants are used for host location by parasitoids ing aides can be developed to seasonally track populations, (Turlings et al. 1990). These volatiles have been well studied enabling practical applications in surveillance of female leaf- and reviewed because they have complex and sometimes un- roller populations for the first time. It may also be possible to predictable effects at more than one trophic level (Dicke and develop suppression tools based on combinations of kairo- Baldwin 2010; Poelman et al. 2012). However, the application mone compounds originally identified from leafroller larval- of synthetic volatiles to manage natural enemies has proven damaged apple trees, given the level of attraction. The discov- more complex than expected (Kaplan 2012). In addition, there ery of these adult tortricid attractants (aromatic compounds has been surprisingly little field investigation of the attraction plus acetic acid) raises new ecological questions about of herbivore pest , the group that is of most direct eco- evolved direct plant defences against herbivores. Larval nomic interest. The discovery of confamilial attraction (El- feeding-induced attraction of adult herbivores produces sig- Sayed et al. 2016) suggests an evolutionary advantage for nals that are potentially harmful to the plant by increasing the plant, although evidence for effects on plant fitness from herbivory in the same family and probably feeding guild, such signalling remains elusive. but evidence for effects on plant fitness is needed. In fact, whole groups of pest insects of many perennial crops have received comparatively little investigation thus far. A number of species of Tortricidae (leafrollers) are orchard pests, particularly favored by the habitat and conditions pro- duced in s deciduous tree fruit orchards (Beers et al. 2003). * D. M. Suckling Populations can occur with webbing of nests between leaves [email protected] and fruit, providing a risk of live larvae associated with exported fruit (Lo et al. 2000). Decades of insecticidal control 1 The New Zealand Institute for Plant & Food Research Limited, have led to selection for insecticide resistance (Lowery and Gerald Street, Lincoln 7608, New Zealand Smirle 2000), non-target impacts on beneficial insects mea- 2 School of Biological Sciences, University of Auckland, Tamaki surable as reduced biodiversity (Epstein et al. 2000), residues Campus, Building, Auckland 733, New Zealand on fruit unwanted by consumers, and consequent adoption of 488 J Chem Ecol (2017) 43:487–492 pheromones for reduced reliance on insecticides in some compounds emerging with behavioral activity share an aro- countries (Walker et al. 2017). matic ring. This led us to focus here on phenylacetonitrile, The development of trapping and direct control systems for benzyl alcohol and 2-phenylethylalcohol, together with acetic Tortricidae based on sex pheromones has included a wide acid. Having discovered the activity first on adult array of innovations including mating disruption (El-Sayed E. postvittana in New Zealand (El-Sayed et al. 2016), we set 2017). Some multi-species systems have been developed to out to explore the effect of combinations of these compounds target ecosystem level pest management in North America on economically-important North American leafroller species with a single pheromone release device (Judd and Gardiner the oblique-banded leafroller (OBLR), Choristoneura 2008). In New Zealand, the pheromone-based systems rosaceana (Harris), and eye-spotted bud (ESBM), target nil or low residues on fruit combined with no insects Spilonota ocellana (Denis and Schiffermüller), as well as oth- present, the stringent standard needed for market access er species present in lower density such as three-lined leafroll- (Walker et al. 2017). However, these literally disruptive tech- er, Pandemis limitata (Robinson)(TLLR), European leafroller nologies can make pest surveillance more difficult, by Archips rosana, (Linnaeus, 1758)(ELR) and fruit-tree leafroll- preventing the operation of sex pheromone traps baited with er, Archips argyrospila (Walker, 1863) (FTLR). the same compounds (Judd and Gardiner 2008). Several tortricid pests are undergoing geographic range expansion (Suckling et al. 2016). These include the Materials and Methods European grapevine moth, Lobesia botrana Denis & Schiffermüller, in the USA and Chile (Varela et al. 2010) Chemicals Chemical purities of compounds used in trapping and the light brown apple moth, Epiphyas postvittana experiments were as follows: glacial acetic acid (>99%), ben- (Walker), now established in Hawaii, California, Great zyl alcohol (>99%), phenylacetonitrile (>99%), and 2- Britain and several European countries (Suckling and phenylethanol (>99%) (Sigma Aldrich, St. Louis, MO, Brockerhoff 2010). Hence, there is a need to develop new USA). Glacial acetic acid was stored under ambient tempera- technologies for surveillance, and potentially new control ture while all other compounds were stored at −20 °C until tactics to support leafroller pest suppression in existing and used. Aromatic lures were prepared in sealed polyethylene new jurisdictions. sachets, with acetic acid in a Nalgene vial (Nalg-Nunc Like other plants (Schittko et al. 2001; Turlings et al. 1990) International, Rochester, NY, USA). Lures containing apple, Malus domestica Borkhausen, have apparently co- phenylacetonitrile, benzyl alcohol and 2-phenylethanol were evolved chemical communication with their insect herbivores. made as reported elsewhere (El-Sayed et al. 2016), by dis- Chemical attraction of herbivores to apple fruit involving vol- pensing each compound into a permeable polyethylene bag atile organic compounds (VOC) has long been recognised that was then heat-sealed. In the final experiment, (Sutherland 1972; Wearing and Hutchins 1973). Some fruit phenylacetonitrile was added directly to the 3 mL of acetic volatiles compounds have been successfully incorporated into acid in the vial, as well as being presented separately in a trapping systems for female codling (Landolt et al. sachet. A trap with a blank lure without chemical was used 2007; Light et al. 2001). The potential now exists to do this as negative control in all trials. for other tortricids. A particular chemical signalling pathway was identified to Field Experimental Protocol All field experiments were con- result from a fatty acid-amino acid conjugate elicitor released ducted in a mixed variety organic apple orchard (49° 13′N, during caterpillar feeding on foliage (Alborn et al. 1997). Fatty 119° 58′W) in Cawston, British Columbia, Canada during acid amino acid conjugates also occur in many families of 2015. Large white delta traps (Pherocon VI, Trécé Inc., , including leaf feeding Tortricidae (Yoshinaga Adair, OK) were used all trials. Traps baited with different et al. 2010). Volatiles induced from apple foliage from leaf- blends of host-induced plant volatile (HIPV) compounds were roller larval feeding were attractive to a braconid wasp haphazardly assigned to five rows as replicates, each contain- (Suckling et al. 2012), which appears to be a general phenom- ing treatments tested in a randomized complete block design. enon for other leafroller species on other hosts than apple, All trials had five replicates. Traps were positioned 1.7 m where the same wasp locates and parasitizes the larvae above the ground in each trap tree, and were spaced 20 m apart (Suckling et al. 2001). We recently reported attraction of in each row. The polyethylene sachets and vials containing host-induced plant volatiles which were discovered to be acetic acid were attached at the center and on the side, inner highly attractive for adult moths of several species of surface, of a delta trap using a 2.5-cm length of Velcro® in- Tortricidae (El-Sayed et al. 2016). This reinvestigation of dustrial sticky-back tape (Canadian Tire, Penticton, BC, leafroller-damaged apple foliage showed additional com- Canada). Counts were made of common tortricid moths, in- pounds not reported earlier, identified acetic acid and its role cluding S. ocellana, C. rosaceana and P. limitata,aswellas in odor combinations for attracting adult moths. The A. rosana, and A. argyrospila where abundant. J Chem Ecol (2017) 43:487–492 489

Ternary Blends of HIPV Compounds Three field trapping software. Moth total catches are presented for the main species experiments (each with 5 replicates) were conducted to inves- caught in each experiment, including where numbers were too tigate binary aromatic blend combinations loaded at five dif- low to analyse for significance of effects. ferent ratios loaded at 100 mg (100: 0, 75:25, 50:50, 25:75 and 0:100 mg) in combination with an acetic acid vial. Test 1 conducted from 4 to 6 July) evaluated phenylacetonitrile Results and benzyl alcohol, respectively (100: 0, 75:25, 50:50, 25:75 and 0:100 mg) in combination with an acetic acid co-lure Phenylacetonitrile, Benzyl Alcohol and Acetic Acid (3 mL), Test 2 (30 June - 2 July) evaluated phenylacetonitrile There was a significant effect of treatment on catch of and 2-phenylethanol, respectively (i. e. 100: 0, 75:25, S. ocellana over the blank lures, F1,5,5 (treatment) = 22.8; 50:50, 25:75 and 0:100 mg) with an acetic acid co- P < 0.001, but not sex (F1,5,5 (sex) = 0.13; P =0.72).Nomoths lure as before, and from 30 June - 2 July 2015, Test 3 were caught in blank traps, compared with 632 of both sexes evaluated 2-phenylethanol and benzyl alcohol (100: 0, caught to the treatments (Table 1). With the removal of blanks, 75:25, 50:50, 25:75 and 0:100 mg) with an acetic acid co- no significant treatment effect remained between the five lures lure as before. (F4,55 = 1.79; P = 0.15). Similar results were obtained for C. rosaceana, with a significant catch over blanks for the all

Synergism between Phenylacetonitrile and Acetic Acid lures (F1,5 (treatment) = 5.87; P < 0.001, but no effect of sex A combinatorial design experiment compared traps baited (F1,5 (sex) = 0.0; P = 0.95). There was no significant effect on with the following lures: 1) 100 mg phenylacetonitrile alone total catch between treatments after removal of the blanks in a sachet; 2) 3 mL acetic acid alone in a vial; and 3) 100 mg (F4,25 =0.53;P = 0.72). Fewer C. rosaceana than phenylacetonitrile in a sachet with 3 mL acetic acid in a vial S. ocellana were caught in this experiment (N = 140 males and 4) a blank negative control. This experiment was conduct- and females), Table 1. ed from 21 June to 2 July. The relative attractiveness of the following binary treat- Phenylacetonitrile, 2-Phenylethanol and Acetic Acid A ments was investigated with a second experiment using 1) two-way ANOVA produced a significant effect of treatment

100 mg phenylacetonitrile +3 mL acetic acid; 2) 1000 mg on catch of S. ocellana above the blanks (Table 2)(F1,5,5 phenylacetonitrile +3 mL acetic acid; and 3) 100 mg (treatment) = 100.35, P < 0.001), with no effect of sex (F1,5,5 phenylacetonitrile +3 mL acetic acid combined together in (sex) =0.00,P = 0.96). A one way ANOVAon lures that caught the same Nalgene vial, and 4) a blank negative control. insects had no significant treatment difference between the

Traps were operated from June 21 to 6 July. five binary or ternary treatments (F4,55 =1.79,P =0.15).In this trial, catches of S. ocellana, C. rosaceana and P. limitata Data Analyses The variance of mean captures obtained with to baited traps were 1117, 14 and 161, respectively. For each compound or blend was stabilized using log (x + 1) of P. l imi ta ta, the one way ANOVA without the blanks had no counts for tests of significance of treatments using a difference between treatments (F4,20 =2.06,P =0.12). randomised block two-way Analysis of Variance ANOVA (sex and treatment), followed by one way ANOVA, where Benzyl Alcohol, 2-Phenylethanol and Acetic Acid A two- appropriate to pool sexes. Significantly different treatment way ANOVA indicated that significant catches over the means were identified with Tukey’s HSD test with an blanks were made of both sexes of OBLR (99 caught) to all experiment-wise alpha level of 0.05, using Minitab 16 treatments with acetic acid and 2-phenylethanol above blanks

Table 1 Mean catch per trap of adult male and female Spilonota and benzyl alcohol plus acetic acid lures (3 mL) in apple orchards in ocellana and Choristoneura rosaceana from 4–6 July 2015, by lures British Columbia. Different letters indicate significant differences with ternary blends containing varying ratios of phenylacetonitrile between treatments by Tukey’s test. Unbaited blanks caught nothing

Compound and species Blend 1 Blend 2 Blend 3 Blend 4 Blend 5

Phenylacetonitrile (mg) 100 75 50 25 0 Benzyl alcohol (mg) 0 25 50 75 100 Acetic acid (mL) 3 3 3 3 3 S. ocellana mean catch 14.1a 10.6a 11.0a 22. 7a 9.5a Standard error 1.8 1.1 1.6 1.1 1.0 C. rosaceana mean catch 3.9a 2.0a 3.3a 4.6a 3.0a Standard error 0.9 1.2 1.6 0.9 1.3 490 J Chem Ecol (2017) 43:487–492

Table 2 Mean catch per trap of adult male and female Spilonota phenylethanol plus acetic acid (3 mL) in apple orchards in British ocellana and Pandemis limitata from 4–6 July 2015, by lures with Columbia. Different letters indicate significant differences between ternary blends containing varying ratios of phenylacetonitrile and 2- treatments by Tukey’s test. Unbaited blanks caught nothing

Compound and species Blend 1 Blend 2 Blend 3 Blend 4 Blend 5

Phenylacetonitrile (mg) 100 75 50 25 0 2-Phenylethanol (mg) 0 25 50 75 100 Acetic acid (mL) 3 3 3 3 3 S. ocellana mean catch 49.8a 53.4a 56.2a 42.6a 21.4a Standard error 5.7 6.2 9.2 5.0 5.7 P. limitata mean catch 3.6a 7.2a 8.2a 5.8a 7.4a Standard error 2.0 0.5 1.5 1.0 2.4

(F4,1,4 (treatment) =3.45,P = 0.016). Unusually, the numbers of P = 0.1)(109 caught). Catches of C. rosaceana to lures females caught here were significantly lower than males in the three treatments were lower overall (60).

(F4,1,4 (sex) =86.5,P = 0.001) Table 3.

2-Phenylacetonitrile with Acetic Acid A two-way ANOVA Discussion indicated a significant effect of treatment on S. ocellana (F3,1,3 (treatment) = 72.9, P < 0.001), but no effect of sex (F3,1,3 The co-presentation of acetic acid and aromatic volatiles (sex) =0.16,P = 0.695. After removal of the blanks and attracted male and female moths of several pest Tortricidae, pooling of the sexes, and ANOVA showed a significant treat- confirming earlier experiments (El-Sayed et al. 2016). Catches ment effect when the two components were presented together were made with the combination of acetic acid and all three

(F2,27 =65.6,P <0.001)(Table4)(catches of 291 S. ocellana). aromatic compounds, with a relatively evenly-balanced sex The improvement over acetic acid alone was 3.7- fold. ratio derived from hundreds of field-caught moths. These find- Numbers of Choristoneura rosaceana were too low for anal- ings have potential to solve the long-running surveillance ysis (132 caught), but means and standard errors have been problem experienced with the use of sex pheromone traps calculated. under mating disruption (Witzgall et al. 2010), as well as pro- For the test of phenylacetonitrile in sachets at two load- vide a cost-effective basis for mass-trapping or lure and kill ings with acetic acid, and with the combination of both sub- technologies of leafrollers for the first time (El-Sayed et al. stances in a single vial, a two-way ANOVA indicated a sig- 2006, 2009). The species attracted so far by various nificant effect of treatment (F3,1,3 (treatment) =16.5,P <0.001) blends of aromatic compounds and acetic acid include and sex (F4,1,4 (sex) =29.6,P < 0.001), as well as an interaction E. postvittana, S. ocellana, C. rosaceana, P. limitata, (F3,1,3 =4.5,P = 0.01) for S. ocellana. ANOVA was signifi- A. rosana, and A. argyrospila (the last two species were less cant for male catches with all three treatments overlapping abundant and were not studied quantitatively). Similarly, and above the blanks (F3,16 = 19.3, P < 0.001)(282 El-Sayed et al. (2016) reported the positive response of vari- caught). For females, there was no treatment effect prob- ous conspecific and heterospecific herbivores to HIPV com- ably due to some catch in blank traps (F3,16 =2.4, pounds which suggest that this phenomena is widespread

Table 3 Mean catch per trap of adult male and female Choristoneura (3 mL) in apple orchards in British Columbia. Different letters indicate rosaceana from 4–6 July 2015, by lures with ternary blends containing significant differences between treatments by Tukey’s test. Unbaited varying ratios of benzyl alcohol and 2-phenylethanol plus acetic acid blanks caught nothing

Compound Blend 1 Blend 2 Blend 3 Blend 4 Blend 5

Benzyl alcohol (mg) 100 75 50 25 0 2-Phenylethanol (mg) 0 25 50 75 100 Aceticacid(mL) 33333 Male C. rosaceana. mean catch 2.4a 4.4a 3.8a 4.4a 4.0a Standard error 1.1 0.2 0.4 0.6 0.8 Female C. rosaceana mean catch 1.0a 1.4a 1.2a 1.8a 1.6a Standard error 0.0 0.4 0.2 0.5 0.4 J Chem Ecol (2017) 43:487–492 491

Table 4 Mean catch per trap of adult male and female Spilonota acetic acid, and acetic acid lures (3 mL) alone in apple orchards in British ocellana (291 caught) and Choristoneura rosaceana (132 caught) from Columbia. Different letters indicate significant differences between 4–6 July 2015, by lures containing phenylacetonitrile with or without treatments by Tukey’stest

Compound Treatment 1 Treatment 2 Treatment 3 Blank

Phenylacetonitrile (mg) 100 100 - - Acetic acid (mL) - 3 3 - S. ocellana. mean catch 1.2c 44.6a 12.0b 0.0d Standard error 0.7 7.9 2.9 0.0 C. rosaceana mean catch 0.0b 14.7a 3.4a 0.7b Standard error 0.0 2.4 1.1 0.6

among leaf-feeding moths (El-Sayed et al. 2016). Another insects for which these compounds have apparent activity group of species is attracted to acetic acid and pear ester include leafrollers of widely different biogeographical ori- (E,Z)-ethyl 2,4-decadienoate) in field tests (Schmidt et al. gin, including Australia, North America and Eurasia. Pest 2007;Tóthetal.2012;Jósvaietal.2016). A similar test for managers will want answers to many questions, including attraction is warranted with other species of Tortricidae using trap efficiency, active space and other aspects. It seems aromatic compounds and acetic acid, based on our results. likely that these new tools will be amenable to refinement More than 40 species of Tortricidae have emerged as the for a number of pest Tortricidae, and that future pest man- target of pest management research using pheromones, and a agement solutions will be developed based on female leaf- number have also been targeted with official control or erad- roller attractants such as those reported here. ication programs (Suckling et al. 2016). We suggest that new More fundamentally, the discovery of adult tortricid opportunities may emerge for many of these targets. Low attractants raises new questions about plant defence catch of any one species in or sex in individual trials may be against herbivores, since attraction of adults is apparently due to patchy occurrence at certain sites or times. harmful to the plant. This work suggests that a Bdouble- Both aromatic and acetic acid elements are necessary and edged sword^ effect may be present, with both natural sufficient for significant attraction. Fortunately, the com- enemies and herbivores alerted to the location and quality pounds of interest are available. There is some evidence of of food sources. Further work on the fitness of plants with different preferences between species in this study and the and without signalling could be useful to elucidate a fuller previous study (El-Sayed et al. 2016), although more field picture of the ecology of the phenomenon. trials could reveal the magnitude of this difference. A number of applications can be envisaged for orchard pest Acknowledgements This work was supported by the New Zealand management, particularly for use with mating disruption prod- Institute for Plant & Food Research by Pipfruit Core Funding from the ucts. It is surprising that some of these compounds can substi- Ministry of Business Innovation and Employment and the Washington tute for each other as effectively as observed here. A choice of Tree Fruit Research Commission, Wenatchee, WA, USA. Ashraf M. El- Sayed gratefully acknowledges the receipt of a fellowship from the several aromatic compounds can provide activity in combina- OECD Co-operative Research Programme: Biological Resource tion with acetic acid. There appears to be considerable flexi- Management for Sustainable Agricultural Systems in 2015, hosted at bility in the composition of these lures, but the possibility of Agriculture and Agri-Food Canada Summerland, British Columbia. The negative interactions also needs to be considered. authors thank AL Knight and GJR Judd for comments on the manuscript. Furthermore, the possibility of more than one compound fir- ing the same olfactory receptor neuron could readily be ex- plored by single sensillum recording of responses to these References compounds, which could expedite the design of new lures by answering questions involving the structure-activity rela- Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet army- tionships of analogs (Suckling et al. 2013). Further development worm oral secretion. Science 276:945–949 of formulations will be needed before commercialisation. Beers EH, Suckling DM, Prokopy RJ, Avilla J (2003) Ecology and man- Combinations of pheromone and kairomone-based trap- agement of apple pests. In: Ferree DC, Warrington IJ (eds) ping could prove useful, although the relative attraction of Apples: botany, production and uses. CABI Publishing, Wallingford the new lures compared with the sex pheromone requires Dicke M, Baldwin IT (2010) The evolutionary context for herbivore- induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci investigation. If catch values can be maintained at the 15:167–175. doi:10.1016/j.tplants.2009.12.002 levels seen here for S. ocellana then the prospects look El-Sayed AM (2017) The Pherobase: Database of Pheromones and promising for control by female and male removal. The Semiochemicals www.pherobase.com. Accessed 1 February 2017. 492 J Chem Ecol (2017) 43:487–492

El-Sayed AM, Suckling DM, Wearing CH, Byers JA (2006) Potential of Schmidt S, Anfora G, Ioriatti C, Germinara GS, Rotundo G, De mass trapping for long-term pest management and eradication of Cristofaro A (2007) Biological activity of ethyl (e,z)-2,4- invasive species. J Econ Entomol 99:1550–1564. doi:10.1603/ decadienoate on different tortricid species: Electrophysiological re- 0022-0493-99.5.1550 sponses and field tests. Environ Entomol 36:1025–1031. doi:10. El-Sayed AM, Suckling DM, Byers JA, Jang EB, Wearing CH (2009) 1603/0046-225X(2007)36[1025:BAOEEO]2.0.CO;2 Potential of “lure and kill” in long-term pest management and erad- Suckling DM, Brockerhoff EG (2010) Invasion biology, ecology, and man- ication of invasive species. J Econ Entomol 102: 815-835. doi:10. agement of the light brown apple moth (Tortricidae). Annu Rev 1603/029.102.0301 Entomol 55:285–306. doi:10.1146/annurev-ento-112408-085311 El-Sayed AM, Knight AL, Byers JA, Judd GJR, Suckling DM (2016) Suckling DM, Burnip GM, Gibb AR, Daly JM, Armstrong KF (2001) Caterpillar-induced plant volatiles attract conspecific adults in na- Plant and host effects on the leafroller parasitoid Dolichogenidia ture. Sci Report 6:37555. http://www.nature.com/articles/srep37555 tasmanica. Entomologia Experimentalis et Applicata 100:253– http://www.nature.com/articles/srep37555#supplementary- 260. doi:10.1046/j.1570-7458.2001.00870.x information Suckling DM, Twidle AM, Gibb AR, Manning LAM, Mitchell VJ, Epstein DL, Zack RS, Brunner JF, Gut L, Brown JJ (2000) Effects of Sullivan TES, Wee SL, El-sayed AM (2012) Volatiles from apple broad-spectrum insecticides on epigeal arthropod biodiversity in trees infested with light brown apple moth larvae attract the parasit- Pacific northwest apple orchards. Environ Entomol 29:340–348 oid Dolichogenidia tasmanica.JAgricFoodChem60:9562–9566. Jósvai JK, Koczor S, Tóth M (2016) Traps baited with pear ester and doi:10.1021/jf302874g acetic acid attract both sexes of Hedya nubiferana (Lepidoptera: Suckling DM, Dymock JJ, Park, KC, Wakelin RH, Jamieson LE (2013) – Tortricidae). J Appl Entomol 140:81 90. doi:10.1111/jen.12216 Communication disruption of guava moth (Coscinoptycha Judd GJR, Gardiner MGT (2008) Efficacy of Isomate-CM/LR for man- improbana) using a pheromone analog based on chain length. J aging codling moth and leafrollers by mating disruption in organic Chem Ecol 39:1161–1168. doi:10.1007/s10886-013-0339-3 apple orchards in western Canada. J Entomol Soc Brit Columbia Suckling DM, Conlong DE, Carpenter JE, Bloem KA, Rendon P, – 105:45 60 Vreysen MJB (2016) Global range expansion of pest Lepidoptera Kaplan I (2012) Attracting carnivorous with plant volatiles: requires socially acceptable solutions. Biol Invasions:1–13. doi:10. – the future of biocontrol or playing with fire? Biol Control 60:77 89. 1007/s10530-016-1325-9 doi:10.1016/j.biocontrol.2011.10.017 Sutherland ORW (1972) The attraction of newly hatched codling moth Landolt PJ, Suckling DM, Judd GJR (2007) Positive interaction of a (Laspeyresia pomonella) larvae to apple. Entomol Exp Appl 15: feeding attractant and a host kairomone for trapping the codling 481–487 moth, Cydia pomonella (L.) J Chem Ecol 33:2236–2244. doi:10. Tóth M, Landolt P, Szarukán I, Szólláth I, Vitányi I, Pénzes B, Hári K, 1007/s10886-007-9391-1 Jósvai JK, Koczor S (2012) Female-targeted attractant containing Light DM, Knight AL, Henrick CA, Rajapaska D, Lingren B, Dickens pear ester for Synanthedon myopaeformis. Entomol Exp Appl 142: JC, Reynolds KM, Buttery RG, Merrill G, Roitman J, Campbell BC 27–35. doi:10.1111/j.1570-7458.2011.01198.x (2001) A pear-derived kairomone with pheromonal potency that attracts male and female codling moth, Cydia pomonella (L.) Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore- Naturwissenschaften 88:333–338 induced plant odors by host-seeking parasitic wasps. Science 250: – Lo PL, Suckling DM, Bradley SJ, Walker JTS, Shaw PW, Burnip GM 1251 1253 (2000) Factors affecting feeding site preferences of lightbrown apple Varela LG, Smith RJ, Cooper ML, Hoenisch RW (2010) European grape- moth, Epiphyas postvittana (Lepidoptera: Tortricidae), on apple vine moth, Lobesia botrana, in Napa Valley. Practical Vineyard and – trees in New Zealand. N Z J Crop Hortic Sci 28:235–243 Winery 30:1 5 Lowery DT, Smirle MJ (2000) Toxicity of insecticides to obliquebanded Walker JTS, Suckling DM, Wearing CH (2017) Past, present, and future leafroller, Choristoneura rosaceana, larvae and adults exposed pre- of integrated control of apple pests: the New Zealand experience. viously to neem seed oil. Entomol Exp Appl 95:201–207 Annu Rev Entomol. doi:10.1146/annurev-ento-031616-035626 Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE, Wearing CH, Hutchins RFN (1973) Alpha-Farnesene, a naturally occur- Jongema Y, van Loon JJA, Vet LEM, Harvey JA, Dicke M (2012) ring oviposition stimulant for the codling moth, Laspeyresia Hyperparasitoids use herbivore-induced plant volatiles to locate pomonella. J Insect Physiol 19:1251–1256 their parasitoid host. PLoS Biol 10:e1001435. doi:10.1371/journal. Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and their impact on pbio.1001435 pest management. J Chem Ecol 36:80–100. doi:10.1007/s10886- Schittko U, Hermsmeier D, Baldwin IT (2001) Molecular interactions 009-9737-y between the specialist herbivore Manduca sexta (Lepidoptera, Yoshinaga N, Alborn HT, Nakanishi T, Suckling DM, Nishida R, Sphingidae) and its natural host Nicotiana attenuata.II. Tumlinson JH, Mori N (2010) Fatty acid-amino acid conjugates Accumulation of plant mRNAs in response to insect-derived cues. diversification in lepidopteran caterpillars. J Chem Ecol 36:319– Plant Physiol 125:701–710 325. doi:10.1007/s10886-010-9764-8