Abstract
Within the framework of finding new fumigants, less toxic and environmentally friendly, in comparison with conventional fumigants, natural products and essential oils are considered to be alternative sources of potentially active compounds. In this context, the aim of the present study was the chemical analysis and the evaluation of fumigant toxicity against the adults of rice weevil Sitophylus oryzae of sixteen essential oils obtained from fourteen plant species. The essential oils of the species Apium nodiflorum, Bupleurum fruticosum, Crithmum maritimum, Liquidambar orientalis and Laurus azorica consisted mainly of monoterpene hydrocarbons. Oxygenated monoterpenes were the prevailing group of compounds in the essential oils of Laurus nobilis, Myrtus communis, Salvia fruticosa S. pomifera subsp. calycina, S. officinalis and Thymbra capitata. The essential oils of Cotinus coggygria, S. microphylla and Teucrium capitatum were rich in sesquiterpenes. The most active essential oils were those of T. capitata (LC50 = 3.4 μL/L air) and S. pomifera subsp. calycina (LC50 = 4.4 μL/L air) against S. oryzae adults. The essential oils of S. fruticosa, L. nobilis and S. officinalis were also found to be highly toxic (LC50 = 7.4–15.5 μL/L air). Most of the other essential oils tested exhibited moderate to low toxicities (LC50 = 17.7–37.9 μL/L air), while those of C. coggygria and S. microphylla did not exhibit any noticeable activity. Our results indicate that some essential oils, and in particular those of T. capitata and S. pomifera subsp. calycina might be promising fumigants for the control of important pests of stored grain such as the rice weevil S. oryzae.
Similar content being viewed by others
References
Abdelgaleil SA, Mohamed MI, Shawir MS, Abou-Taleb HK (2016) Chemical composition, insecticidal and biochemical effects of essential oils of different plant species from Northern Egypt on the rice weevil Sitophilus oryzae L. J Pest Sci 89(1):219–229. https://doi.org/10.1007/s10340-015-0665-z
Adams RP (2007) Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy, 4th edn. Allured Publishing Corporation, Carol Stream
Ahn YJ, Lee SB, Lee HS, Kim GH (1998) Insecticidal and acaricidal activity of carvacrol and β-thujaplicine derived from Thujopsis dolabrata var. hondai sawdust. J Chem Ecol 24(1):81–90. https://doi.org/10.1023/A:1022388829078
Andrade EHA, Alves CN, Guimarặes EF, Carreira LMM, Maia JGS (2011) Variability in essential oil composition of Piper dilatatum L. C. Rich. Biochem Syst Ecol 39:669–675. https://doi.org/10.1016/j.bse.2011.05.021
Antunes T, Sevinate-Pinto I, Barroso JG, Cavaleiro C, Salgueiro LR (2004) Micromorphology of trichomes and composition of essential oil of Teucrium capitatum. Flavour Fragr J 19:336–340. https://doi.org/10.1002/ffj.1310
Athanassiou CG, Buchelos CT (2001) Detection of stored-wheat beetle species and estimation of population density using unbaited probe traps and grain trier samples. Entomol Exp Appl 98:67–78. https://doi.org/10.1046/j.1570-7458.2001.00758.x
Attia S, Grissa KL, Ghrabi ZG, Mailleux AC, Lognay G, Hance T (2012) Acaricidal activity of 31 essential oils extracted from plants collected in Tunisia. J Essent Oil Res 24(3):279–288. https://doi.org/10.1080/10412905.2012.676777
Barbosa P, Lima AS, Vieira P, Dias LS, Tinoco MT, Barroso JG, Pedro LG, Figueiredo AC, Mota M (2010) Nematicidal activity of essential oils and volatiles derived from Portuguese aromatic flora against the pinewood nematode, Bursaphelenchus xylophilus. J Nematol 42(1):8–16
Benhalima H, Chaudhry MQ, Mills KA, Price NR (2004) Phosphine resistance in stored-product insects collected from various grain storage facilities in Morocco. J Stored Prod Res 40:241–249. https://doi.org/10.1016/S0022-474X(03)00012-2
Blumenthal M (2000) Sage leaf in herbal medicine expanded: commission E monographs. American Botanical Council, Newton
Bouajaj S, Benyamna A, Bouamama H, Romane A, Falconieri D, Piras A, Marongiu B (2013) Antibacterial, allelopathic and antioxidant activities of essential oil of Salvia officinalis L. growing wild in the Atlas Mountains of Morocco. Nat Prod Res 27:1673–1676. https://doi.org/10.1080/14786419.2012.751600
Boyer S, Zhangand H, Lempérière G (2012) A review of control methods and resistance mechanisms in stored-product insects. Bull Entomol Res 102(2):213–229. https://doi.org/10.1017/S0007485311000654
Božović M, Garzoli S, Sabatino M, Pepi F, Baldisserotto A, Andreotti E, Romagnoli C, Mai A, Manfredini S, Ragno R (2017) Essential oil extraction, chemical analysis and anti-Candida activity of Calamintha nepeta (L.) Savi subsp. glandulosa (Req.) Ball—new approaches. Molecules 22(2):203. https://doi.org/10.3390/molecules22020203
Bradesi P, Tomi F, Casanova J, Costa J, Bernardini AF (1997) Chemical composition of Myrtle leaf essential oil from Corsica (France). J Essent Oil Res 9:283–288. https://doi.org/10.1080/10412905.1997.10554245
Cardiet G, Fuzeau B, Barreau C, Fleurat-Lessard F (2012) Contact and fumigant toxicity of some essential oil constituents against a grain insect pest Sitophilus oryzae and two fungi, Aspergillus westerdijkiae and Fusarium graminearum. J Pest Sci 85(3):351–358. https://doi.org/10.1007/s10340-011-0400-3
Chialva F, Monguzzi F, Manitto P (1992) Composition of the essential oils of five Salvia species. J Essent Oil Res 4:447–455. https://doi.org/10.1080/10412905.1992.9698108
de Araújo AMN, Faroni LRDA, de Oliveira JV, Navarro DMDAF, Barbosa DRES, Breda MO, de França SM (2017) Lethal and sublethal responses of Sitophilus zeamais populations to essential oils. J Pest Sci 90(2):589–600. https://doi.org/10.1007/s10340-016-0822-z
Duru ME, Cakir A, Harmandar M (2002) Composition of the volatile oils isolated from the leaves of Liquidambar orientalis Mill. var. orientalis and L. orientalis var. integriloba from Turkey. Flavour Fragr J 17:95–98. https://doi.org/10.1002/ffj.1050
El Hadj Ali IB, Guetat A, Boussaid M (2012) Variation of volatiles in Tunisian populations of Thymbra capitata (L.) Cav. (Lamiaceae). Chem Biodivers 9:1272–1285. https://doi.org/10.1002/cbdv.201100344
European Pharmacopoeia (2014) 8th edn. European directorate for the quality of medicines & healthCare (EDQM). Council of Europe, Strasbourg
Farhat MB, Jordán MJ, Chaouech-Hamada R, Landoulsi A, Sotomayor JA (2009) Variations in essential oil, phenolic compounds, and antioxidant activity of tunisian cultivated Salvia officinalis L. J Agric Food Chem 57:10349–10356. https://doi.org/10.1021/jf901877x
Faria JM, Barbosa P, Bennett RN, Mota M, Figueiredo AC (2013) Bioactivity against Bursaphelenchus xylophilus: nematotoxics from essential oils, essential oils fractions and decoction waters. Phytochemistry 94:220–228. https://doi.org/10.1016/j.phytochem.2013.06.005
Faria JMS, Sena I, Ribeiro B, Rodrigues AM, Maleita CMN, Abrantes I, Bennett R, Mota M, da Silva Figueiredo AC (2016) First report on Meloidogyne chitwoodi hatching inhibition activity of essential oils and essential oils fractions. J Pest Sci 89:207–217. https://doi.org/10.1007/s10340-015-0664-0
Fields PG, White ND (2002) Alternatives to methyl bromide treatments for stored-product and quarantine insects. Annu Rev Entomol 47(1):331–359. https://doi.org/10.1146/annurev.ento.47.091201.145217
Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, London
Garry VF, Griffith J, Danzl TJ, Nelson RL, Whorton EB, Krueger LA, Cervenka J (1989) Human genotoxicity: pesticide applicators and phosphine. Science 246:251–255. https://doi.org/10.1126/science.2799386
Ghrabi-Gammar Z, George DR, Daoud-Bouattour A, Jilani IBH, Saad-Limam SB, Sparagano OA (2009) Screening of essential oils from wild-growing plants in Tunisia for their yield and toxicity to the poultry red mite, Dermanyssus gallinae. Ind Crop Prod 30(3):441–443. https://doi.org/10.1016/j.indcrop.2009.07.001
Giatropoulos A, Papachristos DP, Kimbaris A, Koliopoulos G, Polissiou MG, Emmanouel N, Michaelakis A (2012) Evaluation of bioefficacy of three Citrus essential oils against the dengue vector Aedes albopictus (Diptera: Culicidae) in correlation to their components enantiomeric distribution. Parasitol Res 111(6):2253–2263. https://doi.org/10.1007/s00436-012-3074-8
Gross AD, Kimber MJ, Coats JR (2014a) G-protein-coupled receptors (GPCRs) as biopesticide targets: a focus on octopamine and tyramine receptors. In: Gross AD, Coats JR, Duke SO, Seiber JN (eds) Biopesticides: state of the art and future opportunities. American Chemical Society, Washington, pp 44–56
Gross AD, Kimber MJ, Day TA et al (2014b) Investigating the effect of plant essential oils against the American cockroach octopamine receptor (Pa oa1) expressed in yeast. In: Gross AD, Coats JR, Duke SO, Seiber JN (eds) Biopesticides: state of the art and future opportunities. American Chemical Society, Washington, pp 113–130
Herrera JM, Zunino MP, Massuh Y, Pizzollito RP, Dambolena JS, Gañan NA, Zygadlo JA (2014) Fumigant toxicity of five essential oils rich in ketones against Sitophilus zeamais (Motschulsky). Agriscientia 31:35–41
Hertlein MB, Thompson GD, Subramanyam B, Athanassiou CG (2011) Spinosad: a new natural product for stored grain protection. J Stored Prod Res 47(3):131–146. https://doi.org/10.1016/j.jspr.2011.01.004
Isman MB (2000) Plant essential oils for pest and disease management. Crop Prot 19(8):603–608. https://doi.org/10.1016/S0261-2194(00)00079-X
Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66. https://doi.org/10.1146/annurev.ento.51.110104.151146
Jallali I, Zaouali Y, Missaoui I, Smeoui A, Abdelly C, Ksouri R (2014) Variability of antioxidant and antibacterial effects of essential oils and acetonic extracts of two edible halophytes: Crithmum maritimum L. and Inula crithmoides L. Food Chem 145:1031–1038. https://doi.org/10.1016/j.foodchem.2013.09.034
Jemâa JMB, Tersim N, Toudert KT (2012) Insecticidal activities of essential oils from leaves of Laurus nobilis L. from Tunisia, Algeria and Morocco, and comparative chemical composition. J Stored Prod Res 48:97–104. https://doi.org/10.1016/j.jspr.2011.10.003
Kanda D, Kaur S, Koul O (2017) A comparative study of monoterpenoids and phenylpropanoids from essential oils against stored grain insects: acute toxins or feeding deterrents. J Pest Sci 90:531–545. https://doi.org/10.1007/s10340-016-0800-
Karousou R, Hanlidou E, Kokkini S (2000) The Sage plants of Greece: distribution and infraspecific variation. In: Kintzios S (ed) Sage, the genus Salvia. Harwood Academic Publishers, Amsterdam, pp 27–46
Kim SW, Kang J, Park IK (2013) Fumigant toxicity of Apiaceae essential oils and their constituents against Sitophilus oryzae and their acetylcholinesterase inhibitory activity. J Asia Pac Entomol 16(4):443–448. https://doi.org/10.1016/j.aspen.2013.07.002
Kim KH, Yi CG, Ahn YJ, Kim SI, Lee SG, Kim JR (2015) Fumigant toxicity of basil oil compounds and related compounds to Thrips palmi and Orius strigicollis. Pest Manag Sci 71(9):1292–1296. https://doi.org/10.1002/ps.3925
Koliopoulos G, Pitarokili D, Kioulos E, Michaelakis A, Tzakou O (2010) Chemical composition and larvicidal evaluation of Mentha, Salvia and Melissa essential oils against the West Nile virus mosquito Culex pipiens. Parasitol Res 107:327–335. https://doi.org/10.1007/s00436-010-1865-3
Kovacevic NN, Simic MD, Ristic MS (2007) Essential oil Laurus nobilis from Montenegro. Chem Nat Compd 43:408–411. https://doi.org/10.1007/s10600-007-0150-x
Kumar P, Mishra S, Malik A, Satya S (2011a) Insecticidal properties of Mentha species: a review. Ind Crops Prod 34(1):802–817. https://doi.org/10.1016/j.indcrop.2011.02.019
Kumar P, Mishra S, Malik A, Satya S (2011b) Repellent, larvicidal and pupicidal properties of essential oils and their formulations against the housefly, Musca domestica. Med Vet Entomol 25(3):302–310. https://doi.org/10.1111/j.1365-2915.2011.00945.x
Lamiri A, Lhaloui S, Benjilali B, Berrada M (2001) Insecticidal effects of essential oils against Hessian fly, Mayetiola destructor (Say). Field Crop Res 71:9–15. https://doi.org/10.1016/s0378-4290(01)00139-3
Lee S, Peterson CJ, Coats JR (2003) Fumigation toxicity of monoterpenoids to several stored product insects. J Stored Prod Res 39(1):77–85. https://doi.org/10.1016/S0022-474X(02)00020-6
Lima RK, Cardoso MG, Andrade MA, Guimaraes PL, Batista LR, Nelson DL (2012) Bactericidal and antioxidant activity of essential oils from Myristica fragrans Houtt and Salvia microphylla H.B.K. J Am Oil Chem Soc 89:523–528. https://doi.org/10.1007/s11746-011-1938-1
Liu K, Lota ML, Casanova J, Tomi F (2009) The essential oil of Bupleurum fruticosum L. from Corsica: a comprehensive study. Chem Biodivers 6:2244–2254. https://doi.org/10.1002/cbdv.200800310
Maceljski M (1999) Poljoprivredna entomologija. Zrinski, Ĉakovec
Margaris N, Koedam A, Vokou D (1982) Aromatic plants: basic and applied aspects. The Hague, London
Maxia A, Falconieri D, Piras A, Porcedda S, Marongiu B, Assunta Frau M, Gonçalves MJ, Cabral C, Cavaleiro C, Salgueiro L (2012) Chemical composition and antifungal activity of essential oils and supercritical CO2 extracts of Apium nodiflorum (L.) Lag. Mycopathologia 174:61–67. https://doi.org/10.1007/s11046-011-9519-2
Menghini L, Leporini L, Tirillini B, Epifano F, Genovese S (2010) Chemical composition and inhibitory activity against Helicobacter pylori of the essential oil of Apium nodiflorum (Apiaceae). J Med Food 13:228–230. https://doi.org/10.1089/jmf.2009.0010
Nenaah G (2014a) Chemical composition, insecticidal and repellence activities of essential oils of three Achillea species against the Khapra beetle (Coleoptera: Dermestidae). J Pest Sci 87(2):273–283. https://doi.org/10.1007/s10340-013-0547-1
Nenaah G (2014b) Chemical composition, toxicity and growth inhibitory activities of essential oils of three Achillea species and their nano-emulsions against Tribolium castaneum (Herbst). Ind Crops Prod 53:252–260. https://doi.org/10.1016/j.indcrop.2013.12.042
Nenaah G (2014c) Bioactivity of powders and essential oils of three Asteraceae plants as post-harvest grain protectants against three major coleopteran pests. J Asia Pac Entomol 17:701–709. https://doi.org/10.1016/j.aspen.2014.07
Nenaah G, Ibrahim S, Al-Assiuty B (2015) Chemical composition, insecticidal activity and persistence of three Asteraceae essential oils and their nanoemulsions against Callosobruchus maculatus (F.). J Stored Prod Res 61:9–16. https://doi.org/10.1016/j.jspr.2014.12.007
Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101(1):372–378. https://doi.org/10.1016/j.biortech.2009.07.048
Nguyen TT, Collins PJ, Duong TM, Schlipalius DI, Ebert PR (2016) Genetic conservation of phosphine resistance in the rice Weevil Sitophilus oryzae (L.). J Hered 107(3):228–237. https://doi.org/10.1093/jhered/esw001
Novaković M, Vučković I, Janaćković P, Soković M, Filipović A, Tešević V, Milosavljević S (2007) Chemical composition, antibacterial and antifungal activity of the essential oils of Cotinus coggygria from Serbia. J Serb Chem Soc 72:1045–1051. https://doi.org/10.2998/JSC0711045N
Panagiotopoulos E, Kapetanos C, Skapeti M, Cholevas C, Drossopoulos J, Loukas M, Kintzios SE (2000) The ecophysiology of Salvia: disorders and adaptation. In: Kintzios SE (ed) Sage. The genus Salvia, vol 14. Harwood Academic Publisher, Amsterdam, pp 125–133
Papachristos DP, Stamopoulos DC (2002) Repellent, toxic and reproduction inhibitory effects of essential oil vapours on Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae). J Stored Prod Res 38(2):117–128. https://doi.org/10.1016/S0022-474X(01)00007-8
Papachristos DP, Karamanoli KI, Stamopoulos DC, Menkissoglu-Spiroudi U (2004) The relationship between the chemical composition of three essential oils and their insecticidal activity against Acanthoscelides obtectus (Say). Pest Manag Sci 60(5):514–520. https://doi.org/10.1002/ps.798
Pavela R (2008) Insecticidal properties of several essential oils on the house fly (Musca domestica L.). Phytother Res 22(2):274–278. https://doi.org/10.1002/ptr.2300
Pedro LG, Santos PAG, da Silva JA, Figueiredo AC, Barroso JG, Deans SG, Looman A, Scheffer JJC (2001) Essential oil from Azorean Laurus azorica. Phytochemistry 57:245–250. https://doi.org/10.1016/S0031-9422(00)00497-0
Pitarokili D, Tzakou O, Loukis A, Harvala C (2003) Volatile metabolites from Salvia fruticosa as antifungal agents in soilborne pathogens. J Agric Food Chem 51:3294–3301. https://doi.org/10.1021/jf0211534
Rajendran S (2002) Postharvest pest losses. In: Pimentel D (ed) Encyclopedia of pest management. Marcel Dekker Inc., New York, pp 654–656
Rajendran S, Sriranjini V (2008) Plant products as fumigants for stored-product insect control. J Stored Prod Res 44(2):126–135. https://doi.org/10.1016/j.jspr.2007.08.003
Regnault-Roger C, Philogène BJ (2008) Past and current prospects for the use of botanicals and plant allelochemicals in integrated pest management. Pharm Biol 46(1–2):41–52. https://doi.org/10.1080/13880200701729794
Regnault-Roger C, Hamraoui A, Holeman M, Theron E, Pinel R (1993) Insecticidal effect of essential oils from Mediterranean plants upon Acanthoscelides obtectus Say (Coleoptera, Bruchidae), a pest of kidney bean (Phaseolus vulgaris L.). J Chem Ecol 19:1233–1244. https://doi.org/10.1007/BF00987383
Rojht H, Horvat A, Athanassiou CG, Vayias BJ, Tomanović Ž, Trdan S (2010) Impact of geochemical composition of diatomaceous earth on its insecticidal activity against adults of Sitophilus oryzae (L.) (Coleoptera: Curculionidae). J Pest Sci 83(4):429–436. https://doi.org/10.1007/s10340-010-0313-6
Rozman V, Kalinovic I, Korunic Z (2007) Toxicity of naturally occurring compounds of Lamiaceae and Lauraceae to three stored-product insects. J Stored Prod Res 43(4):349–355. https://doi.org/10.1016/j.jspr.2006.09.001
Salehi T, Karimi J, Hasanshahi G, Askarianzadeh A, Abbasipour H, Garjan AS (2014) The effect of essential oils from Laurus nobilis and Myrtus commonis on the adults of mediterranean flour moth, Ephestia kuehniella zeller (Lep.: Pyralidae). J Essent Oil Bear Plants 17(4):553–561. https://doi.org/10.1080/0972060X.2014.935059
Salgueiro LR, Pinto E, Gonçalves MJ, Pina-Vaz C, Cavaleiro C, Rodrigues AG, Palmeira A, Tavares C, Costa-de-Oliveira S, Martinez-de-Oliveira J (2004) Chemical composition and antifungal activity of the essential oil of Thymbra capitata. Planta Med 70:572–575. https://doi.org/10.1055/s-2004-827162
Saroukolai AT, Moharramipour S, Meshkatalsadat MH (2010) Insecticidal properties of Thymus persicus essential oil against Tribolium castaneum and Sitophilus oryzae. J Pest Sci 83(1):3–8. https://doi.org/10.1007/s10340-009-0261-1
Shaaya E, Ravid U, Paster N, Juven B, Zisman U, Pissarev V (1991) Fumigant toxicity of essential oils against four major stored product insects. J Chem Ecol 17:499–504. https://doi.org/10.1007/BF00982120
Shagun S, Sujata B, Manjul S (2016) Chemical profiling, antioxidant and antibacterial properties of Cotinus coggygria essential oil from Western Himalaya. Int J Pharmacogn Phytochem Res 8(7):1183–1186
SPSS (2004) SPSS 14 for Windows User’s Guide. Copyright 2004 by SPSS Inc., SPSS, Chicago
Stejskal V, Hubert J, Aulicky R, Kucerova Z (2015) Overview of present and past and pest-associated risks in stored food and feed products: European perspective. J Stored Prod Res 64:122–132. https://doi.org/10.1016/j.jspr.2014.12.006
Tsoukatou M, Tsitsimpikou C, Vagias K, Roussis V (2001) Chemical intra-mediterranean variation and insecticidal activity of Crithmum maritimum. Z Naturforsch C 56:211–215. https://doi.org/10.1515/znc-2001-3-407
Tzakou O, Bazos I, Yannitsaros A (2005) Essential oils of leaves, inflorescences and infructescences of spontaneous Cotinus coggygria Scop. from Greece. Flavour Fragr J 20:531–533. https://doi.org/10.1002/ffj.1456
Wang CF, Yang K, You CX, Zhang WJ, Guo SS, Geng ZF, Du SS, Wang YY (2015) Chemical composition and insecticidal activity of essential oils from Zanthoxylum dissitum leaves and roots against three species of storage pests. Molecules 20(5):7990–7999. https://doi.org/10.3390/molecules20057990
Yildirim E, Emsen B, Kordali S (2013) Insecticidal effects of monoterpenes on Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). J Appl Bot Food Qual 86:198–204. https://doi.org/10.5073/JABFQ.2013.086.027
Zhang Z, Yang T, Zhang Y, Wang L, Xie Y (2016) Fumigant toxicity of monoterpenes against fruitfly, Drosophila melanogaster. Ind Crop Prod 81:147–151. https://doi.org/10.1016/j.indcrop.2015.11.076
Acknowledgements
The authors would like to thank Prof. B. Galatis (J. & A. N. Diomedes Botanic Garden, University of Athens) for providing the plant material from Diomedes Botanical Garden and Dr I. Vallianatou (J. & A. N. Diomedes Botanic Garden, University of Athens) for the collection and plant identification of the cultivated plant material. Additionally the authors wish to thank Assoc. Prof. T. Constandinidis and Dr I. Bazos (Institute of Systematic Botany, Department of Biology, University of Athens) for the identification of the plant material collected from natural populations.
Author information
Authors and Affiliations
Contributions
DPP and OT designed research. AK, VA, AV, SA and DPP conducted experiments; DPP analyzed data; AK, VA, AV, SA, AM, DPP and OT wrote the manuscript; All authors have read and approved the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals (vertebrates) performed by any of the authors.
Additional information
Communicated by M. B. Isman.
Rights and permissions
About this article
Cite this article
Koutsaviti, A., Antonopoulou, V., Vlassi, A. et al. Chemical composition and fumigant activity of essential oils from six plant families against Sitophilus oryzae (Col: Curculionidae). J Pest Sci 91, 873–886 (2018). https://doi.org/10.1007/s10340-017-0934-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-017-0934-0