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A meta-analytic investigation of the potential for plant volatiles and sex pheromones to enhance detection and management of Lepidopteran pests

Published online by Cambridge University Press:  19 October 2023

Tom Staton Open the ORCID record for Tom Staton [Opens in a new window]  and
David T. Williams
Tom Staton*
Affiliation:
Forest Research, Alice Holt Lodge, Farnham, UK
David T. Williams
Affiliation:
Forest Research, Alice Holt Lodge, Farnham, UK
*
Corresponding author: Tom Staton; Email: tom.staton@reading.ac.uk
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Abstract

Effective early detection, monitoring and management methods are critical for reducing the impacts of insect pests in agriculture and forestry. Combining host plant volatiles with sex pheromones could enhance trapping methodologies, whilst the use of non-host volatiles could improve the effectiveness of pest management through repellency effects. In this meta-analysis approach, we analysed 51 studies that used electroantennograms (EAG), wind tunnels and/or field traps to evaluate the antennal and behavioural responses of Lepidoptera to sex pheromones combined with attractant or repellent plant volatiles. Proposed attractant plant volatiles had a positive association with female Lepidoptera responses to sex pheromone, but effects on males were highly variable, with unexpected repellency reported in some studies. Proposed repellent plant volatiles were significantly or near-significantly negatively associated with male attraction to sex pheromones but were scarcely studied. Sub-group analysis identified that male responses to sex pheromone were reduced when the dose of attractant plant volatile relative to sex pheromone was increased. Green-leaf volatiles were associated with the strongest positive effects for males in field traps. Multiple-compound attractant plant volatile blends were less effective than single compounds in field studies. Our analysis demonstrates, (i) the potential value of combining host plant volatiles with sex pheromones to capture females rather than only males, (ii) the importance of identifying appropriate host plant volatiles and optimal relative doses, and (iii) the potential for non-host plant volatile use in pest management strategies.

Keywords

electroantennograminsectskairomonesemiochemicaltrappingwind tunnel
Type
Review Article
Information
Bulletin of Entomological Research , Volume 113 , Issue 6 , December 2023 , pp. 725 - 734
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Copyright
Copyright © Crown Copyright - Forest Research, 2023. Published by Cambridge University Press

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References

Barnes, MM, Millar, JG, Kirsch, PA and Hawks, DC (1992) Codling moth (Lepidoptera: Tortricidae) control by dissemination of synthetic female sex pheromone. Journal of Economic Entomology 85, 1274–1277.CrossRefGoogle Scholar
Barros-Parada, W, Ammagarahalli, B, Basoalto, E, Fuentes-Contreras, E and Gemeno, C (2018) Captures of oriental fruit moth, Grapholita molesta (Lepidoptera: Tortricidae), in traps baited with host-plant volatiles in Chile. Applied Entomology and Zoology 53, 193–204.CrossRefGoogle Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Borrero-Echeverry, F, Bengtsson, M, Nakamuta, K and Witzgall, P (2018) Plant odor and sex pheromone are integral elements of specific mate recognition in an insect herbivore. Evolution 72, 2225–2233.CrossRefGoogle Scholar
Bruce, TJA and Pickett, JA (2011) Perception of plant volatile blends by herbivorous insects – finding the right mix. Phytochemistry 72, 1605–1611.CrossRefGoogle ScholarPubMed
CABI (2022) Invasive Species Compendium. Available at https://www.cabi.org/isc/. Retrieved from https://www.cabi.org/isc/Google Scholar
Cai, X, Bian, L, Xu, X, Luo, Z, Li, Z and Chen, Z (2017) Field background odour should be taken into account when formulating a pest attractant based on plant volatiles. Scientific Reports 7, 1–10.Google ScholarPubMed
Cook, SM, Khan, ZR and Pickett, JA (2007) The use of push-pull strategies in integrated pest management. Annual Review of Entomology 52, 375–400.CrossRefGoogle ScholarPubMed
Culliney, TW (2014) Crop losses to arthropods. In Pimentel, D and Rajinder, P (eds), Integrated Pest Management: Pesticide Problems, vol. 3. Dordrecht: Springer, pp. 201–225.CrossRefGoogle Scholar
Deisig, N, Dupuy, F, Anton, S and Renou, M (2014) Responses to pheromones in a complex odor world: sensory processing and behavior. Insects 5, 399–422.CrossRefGoogle Scholar
Deng, JY, Wei, HY, Huang, YP and Du, JW (2004) Enhancement of attraction to sex pheromones of Spodoptera exigua by volatile compounds produced by host plants. Journal of Chemical Ecology 30, 2037–2045.CrossRefGoogle ScholarPubMed
Deutsch, CA, Tewksbury, JJ, Tigchelaar, M, Battisti, DS, Merrill, SC, Huey, RB and Naylor, RL (2018) Increase in crop losses to insect pests in a warming climate. Science 361, 916–919.CrossRefGoogle Scholar
Eigenbrode, SD, Birch, ANE, Lindzey, S, Meadow, R and Snyder, WE (2016) A mechanistic framework to improve understanding and applications of push-pull systems in pest management. Journal of Applied Ecology 53, 202–212.CrossRefGoogle Scholar
Elkinton, JS and Cardé, RT (1988) Effects of intertrap distance and wind direction on the interaction of gypsy moth (Lepidoptera: Lymantriidae) pheromone-baited traps. Environmental Entomology 17, 764–769.CrossRefGoogle Scholar
Fang, Y, Zeng, R, Lu, S, Dai, L and Wan, X (2018) The synergistic attractiveness effect of plant volatiles to sex pheromones in a moth. Journal of Asia-Pacific Entomology 21, 380–387.CrossRefGoogle Scholar
Fettig, CJ and Munson, AS (2020) Efficacy of verbenone and a blend of verbenone and nonhost volatiles for protecting lodgepole pine from mountain pine beetle (Coleoptera: Curculionidae). Agricultural and Forest Entomology 22, 373–378.CrossRefGoogle Scholar
Gregg, PC, Del Socorro, AP and Landolt, PJ (2018) Advances in attract-and-kill for agricultural pests: beyond pheromones. Annual Review of Entomology 63, 453–470.CrossRefGoogle ScholarPubMed
Guo, H and Wang, CZ (2019) The ethological significance and olfactory detection of herbivore-induced plant volatiles in interactions of plants, herbivorous insects, and parasitoids. Arthropod-Plant Interactions 13, 161–179.CrossRefGoogle Scholar
Hedges, LV (1981) Distribution theory for Glass's estimator of effect size and related estimators. Journal of Educational and Behavioral Statistics 6, 107–128.CrossRefGoogle Scholar
Hu, D, Feng, J, Wang, Z, Wu, H and Zhang, X (2013) Effect of nine plant volatiles in the field on the sex pheromones of Leguminivora glycinivorella. Natural Product Communications 8, 393–396.CrossRefGoogle ScholarPubMed
Jactel, H, Birgersson, G, Andersson, S and Schlyter, F (2011) Non-host volatiles mediate associational resistance to the pine processionary moth. Oecologia 166, 703–711.CrossRefGoogle Scholar
Jactel, H, Moreira, X and Castagneyrol, B (2021) Tree diversity and forest resistance to insect pests: patterns, mechanisms, and prospects. Annual Review of Entomology 66, 277–296.CrossRefGoogle ScholarPubMed
Jósvai, JK, Koczor, S and Tóth, M (2016) Traps baited with pear ester and acetic acid attract both sexes of Hedya nubiferana (Lepidoptera: Tortricidae). Journal of Applied Entomology 140, 81–90.CrossRefGoogle Scholar
Judd, GJR, Knight, AL and El-Sayed, AM (2017a) Development of kairomone-based lures and traps targeting Spilonota ocellana (Lepidoptera: Tortricidae) in apple orchards treated with sex pheromones. The Canadian Entomologist 149, 662–676.CrossRefGoogle Scholar
Judd, GJR, Knight, AL and El-Sayed, AM (2017b) Trapping Pandemis limitata (Lepidoptera: Tortricidae) moths with mixtures of acetic acid, caterpillar-induced apple-leaf volatiles, and sex pheromone. The Canadian Entomologist 149, 813–822.CrossRefGoogle Scholar
Knight, AL, Hilton, R and Light, DM (2005) Monitoring codling moth (Lepidoptera: Tortricidae) in apple with blends of ethyl (E, Z)-2,4-decadienoate and codlemone. Environmental Entomology 34, 598–603.CrossRefGoogle Scholar
Knight, A, Cichon, L, Lago, J, Fuentes-Contreras, E, Barros-Parada, W, Hull, L, Krawczyk, G, Zoller, B, Hansen, R, Hilton, R and Basoalto, E (2014) Monitoring oriental fruit moth and codling moth (Lepidoptera: Tortricidae) with combinations of pheromones and kairomones. Journal of Applied Entomology 138, 783–794.CrossRefGoogle Scholar
Knight, AL, El-Sayed, AM, Judd, GJR and Basoalto, E (2017) Development of 2-phenylethanol plus acetic acid lures to monitor obliquebanded leafroller (Lepidoptera: Tortricidae) under mating disruption. Journal of Applied Entomology 141, 729–739.CrossRefGoogle Scholar
Kong, WN, Wang, Y, Guo, YF, Chai, XH, Li, J and Ma, RY (2020) Behavioral effects of different attractants on adult male and female oriental fruit moths, Grapholita molesta. Pest Management Science 76, 3225–3235.CrossRefGoogle ScholarPubMed
Kvedaras, OL, Del Socorro, AP and Gregg, PC (2007) Effects of phenylacetaldehyde and (Z)-3-hexenyl acetate on male response to synthetic sex pheromone in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Australian Journal of Entomology 46, 224–230.CrossRefGoogle Scholar
Landolt, PJ and Phillips, TW (1997) Host plant influences on sex pheromone behavior of phytophagous insects. Annual Review of Entomology 42, 371–391.CrossRefGoogle ScholarPubMed
Larson, ER, Graham, BM, Achury, R, Coon, JJ, Daniels, MK, Gambrell, DK, Jonasen, KL, King, GD, LaRacuente, N, Perrin-Stowe, TIN, Reed, EM, Rice, CJ, Ruzi, SA, Thairu, MW, Wilson, JC and Suarez, AV (2020) From eDNA to citizen science: emerging tools for the early detection of invasive species. Frontiers in Ecology and the Environment 18, 194–202.CrossRefGoogle Scholar
Lehmann, P, Ammunét, T, Barton, M, Battisti, A, Eigenbrode, SD, Jepsen, JU, Kalinkat, G, Neuvonen, S, Niemelä, P, Terblanche, JS, Økland, B and Björkman, C (2020) Complex responses of global insect pests to climate warming. Frontiers in Ecology and the Environment 18, 141–150.CrossRefGoogle Scholar
Lenth, RV (2021) emmeans: Estimated marginal means, aka least-squares means. R package version 1.5.5–1. Available at https://CRAN.R-project.org/package=emmeansGoogle Scholar
Li, J, Valimaki, S, Shi, J, Zong, S, Luo, Y and Heliovaara, K (2012a) Attraction of the gypsy moth to volatile organic compounds (VOCs) of damaged Dahurian larch Zeitschrift Fur Naturforschung – Section C. Journal of Biosciences 67 C, 437–444.Google Scholar
Li, P, Zhu, J and Qin, Y (2012b) Enhanced attraction of Plutella xylostella (Lepidoptera: Plutellidae) to pheromone-baited traps with the addition of green leaf volatiles. Journal of Economic Entomology 105, 1149–1156.CrossRefGoogle ScholarPubMed
Li, X, Liu, Y, Duan, M, Yu, Z and Axmacher, JC (2018) Different response patterns of epigaeic spiders and carabid beetles to varying environmental conditions in fields and semi-natural habitats of an intensively cultivated agricultural landscape. Agriculture, Ecosystems and Environment 264, 54–62.CrossRefGoogle Scholar
Light, DM (2016) Control and monitoring of codling moth (Lepidoptera: Tortricidae) in walnut orchards treated with novel high-load, low-density ‘meso’ dispensers of sex pheromone and pear ester. Environmental Entomology 45, 700–707.CrossRefGoogle ScholarPubMed
Ma, M, Chang, MM, Lei, CL and Yang, FL (2016) A garlic substance disrupts odorant-binding protein recognition of insect pheromones released from adults of the angoumois grain moth, Sitotroga cerealella (Lepidoptera: Gelechiidae). Insect Molecular Biology 25, 530–540.CrossRefGoogle ScholarPubMed
Mafra-Neto, A, Wright, M, Fettig, C, Progar, R, Munson, S, Blackford, D, Moan, J, Graham, E, Foote, G, Borges, R, Silva, R, Lake, R, Bernardi, C, Saroli, J, Clarke, S, Meeker, J, Nowak, J, Agnello, A, Martini, X, Rivera, MJ and Stelinski, LL (2022) Repellent semiochemical solutions to mitigate the impacts of global climate change on arthropod pests. In Coats, J, Corona, C and Debboun, M (eds), Advances in Arthropod Repellents. London: Academic Press, pp. 279–322.CrossRefGoogle Scholar
McCormick, AC, Heyer, J, Sims, JW, Mescher, MC and De Moraes, CM (2017) Exploring the effects of plant odors, from tree species of differing host quality, on the response of Lymantria dispar males to female sex pheromones. Journal of Chemical Ecology 43, 243–253.CrossRefGoogle ScholarPubMed
McNair, C, Gries, G and Gries, R (2000) Cherry bark tortrix, Enarmonia formosana: olfactory recognition of and behavioral difference by nonhost angio- and gymnosperm volatiles. Journal of Chemical Ecology 26, 809–821.CrossRefGoogle Scholar
Meagher, J (2001) Trapping fall armyworm (Lepidoptera: Noctuidae) adults in traps baited with pheromone and a synthetic floral volatile compound. Florida Entomologist 84, 288–292.CrossRefGoogle Scholar
Miluch, CE, Dosdall, LM and Evenden, ML (2014) Factors influencing male Plutella xylostella (Lepidoptera: Plutellidae) capture rates in sex pheromone-baited traps on canola in western. Canada Journal of Economic Entomology 107, 2067–2076.CrossRefGoogle ScholarPubMed
Mitchell, VJ, Manning, L-A, Cole, L, Suckling, DM and El-Sayed, AM (2008) Efficacy of the pear ester as a monitoring tool for codling moth Cydia pomonella (Lepidoptera: Tortricidae) in New Zealand apple orchards. Pest Management Science 64, 209–214.CrossRefGoogle ScholarPubMed
Mujica, V, Preti, M, Basoalto, E, Cichon, L, Fuentes-Contreras, E, Barros-Parada, W, Krawczyk, G, Nunes, MZ, Walgenbach, JF, Hansen, R and Knight, AL (2018) Improved monitoring of oriental fruit moth (Lepidoptera: Tortricidae) with terpinyl acetate plus acetic acid membrane lures. Journal of Applied Entomology 142, 731–744.CrossRefGoogle Scholar
Nakagawa, S, Lagisz, M, Jennions, MD, Koricheva, J, Noble, DWA, Parker, TH, Sánchez-Tójar, A, Yang, Y and O'Dea, RE (2022) Methods for testing publication bias in ecological and evolutionary meta-analyses. Methods in Ecology and Evolution 13, 4–21.CrossRefGoogle Scholar
R Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Retrieved from https://www.r-project.org/Google Scholar
Reardon, BJ, Sumerford, DV and Sappington, TW (2006) Impact of trap design, windbreaks, and weather on captures of European corn borer (Lepidoptera: Crambidae) in pheromone-baited traps. Journal of Economic Entomology 99, 2002–2009.CrossRefGoogle ScholarPubMed
Reddy, GVP and Guerrero, A (2000) Behavioral responses of the diamondback moth, Plutella xylostella, to green leaf volatiles of Brassica oleracea subsp. capitata. Journal of Agricultural and Food Chemistry 48, 6025–6029.CrossRefGoogle ScholarPubMed
Reddy, GVP and Guerrero, A (2004) Interactions of insect pheromones and plant semiochemicals. Trends in Plant Science 9, 253–261.CrossRefGoogle ScholarPubMed
Rizvi, SAH, George, J, Reddy, GVP, Zeng, X and Guerrero, A (2021) Latest developments in insect sex pheromone research and its application in agricultural pest management. Insects 12, 1–26.CrossRefGoogle ScholarPubMed
Rohatgi, A (2021) WebPlotDigitizer. California, USA: Pacifica. Available at https://automeris.io/WebPlotDigitizerGoogle Scholar
Ryall, KL, Silk, PJ, Mayo, P, Crook, D, Khrimian, A, Coss, AA, Sweeney, J and Scarr, T (2012) Attraction of Agrilus planipennis (Coleoptera: Buprestidae) to a volatile pheromone: effects of release rate, host volatile, and trap placement. Environmental Entomology 41, 648–656.CrossRefGoogle ScholarPubMed
Sans, A, Morán, M, Riba, M, Guerrero, Á, Roig, J and Gemeno, C (2016) Plant volatiles challenge inhibition by structural analogs of the sex pheromone in Lobesia botrana (Lepidoptera: Tortricidae). European Journal of Entomology 113, 579–586.CrossRefGoogle Scholar
Schmidt-Büsser, D, Von Arx, M and Guerin, PM (2009) Host plant volatiles serve to increase the response of male European grape berry moths, Eupoecilia ambiguella, to their sex pheromone. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 195, 853–864.CrossRefGoogle ScholarPubMed
Schouest, LP Jr and Miller, TA (1994) Automated pheromone traps show male pink bollworm (Lepidoptera: Gelechiidae) mating response is dependent on weather conditions. Journal of Economic Entomology 87, 965–974.CrossRefGoogle Scholar
Szendrei, Z and Rodriguez-Saona, C (2010) A meta-analysis of insect pest behavioral manipulation with plant volatiles. Entomologia Experimentalis et Applicata 134, 201–210.CrossRefGoogle Scholar
Tang, R, Zhang, JP and Zhang, ZN (2012) Electrophysiological and behavioral responses of male fall webworm moths (Hyphantria cunea) to herbivory-induced mulberry (Morus alba) leaf volatiles. PLoS ONE 7, 1–7.CrossRefGoogle ScholarPubMed
van Lierop, P, Lindquist, E, Sathyapala, S and Franceschini, G (2015) Global forest area disturbance from fire, insect pests, diseases and severe weather events. Forest Ecology and Management 352, 78–88.CrossRefGoogle Scholar
Varela, N, Avilla, J, Anton, S and Gemeno, C (2011) Synergism of pheromone and host-plant volatile blends in the attraction of Grapholita molesta males. Entomologia Experimentalis et Applicata 141, 114–122.CrossRefGoogle Scholar
Viechtbauer, W (2010) Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36, 1–48.CrossRefGoogle Scholar
Wang, F, Deng, J, Schal, C, Lou, Y, Zhou, G, Ye, B, Yin, X, Xu, Z and Shen, L (2016) Non-host plant volatiles disrupt sex pheromone communication in a specialist herbivore. Scientific Reports 6, 1–8.Google Scholar
Weissling, TJ and Knight, AL (1996) Oviposition and calling behavior of codling moth (Lepidoptera: Tortricidae) in the presence of codlemone. Annals of the Entomological Society of America 89, 142–147.CrossRefGoogle Scholar
Williams, DT and Jonusas, G (2019) The influence of tree species and edge effects on pheromone trap catches of oak processionary moth Thaumetopoea processionea (L.) in the U.K. Agricultural and Forest Entomology 21, 28–37.CrossRefGoogle Scholar
Willis, KJ (ed.) (2017) State of the World's Plants 2017. Kew: Royal Botanic Gardens.Google Scholar
Wittman, JT, Silk, P, Parker, K and Aukema, BH (2021) Optimizing early detection strategies: defining the effective attraction radius of attractants for emerald ash borer Agrilus planipennis Fairmaire. Agricultural and Forest Entomology 23, 527–535.CrossRefGoogle Scholar
Witzgall, P, Kirsch, P and Cork, A (2010) Sex pheromones and their impact on pest management. Journal of Chemical Ecology 36, 80–100.CrossRefGoogle ScholarPubMed
Xiang, HM, Chen, Z, Li, XW, Guo, YQ, Li, XC and Ma, RY (2019) Two terpenoids activates close mating behavior and enhances trap efficiency of sex pheromone of Grapholita molesta. Journal of Asia-Pacific Entomology 22, 1109–1114.CrossRefGoogle Scholar
Xiao, C, Gregg, PC, Hu, W, Yang, Z and Zhang, Z (2002) Attraction of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), to volatiles from wilted leaves of a non-host plant, Pterocarya stenoptera. Applied Entomology and Zoology 37, 1–6.CrossRefGoogle Scholar
Xu, H and Turlings, TCJ (2018) Plant volatiles as mate-finding cues for insects. Trends in Plant Science 23, 100–111.CrossRefGoogle ScholarPubMed
Yang, Z, Bengtsson, M and Witzgall, P (2004) Host plant volatiles synergize response to sex pheromone in codling moth, Cydia pomonella. Journal of Chemical Ecology 30, 619–629.CrossRefGoogle ScholarPubMed
Yu, H, Feng, J, Zhang, Q and Xu, H (2015) (Z)-3-hexenyl acetate and 1-undecanol increase male attraction to sex pheromone trap in Grapholita molesta (Busck) (Lepidoptera: Tortricidae). International Journal of Pest Management 61, 30–35.CrossRefGoogle Scholar
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