Application of sulfur-based products reduces Halyomorpha halys infestation and damage in pome fruit orchards.
brown marmorated stink bug
fruit damage
integrated pest management
phytotoxicity
repellence
wettable sulfur
Journal
Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744
Informations de publication
Date de publication:
06 Aug 2024
06 Aug 2024
Historique:
revised:
03
04
2024
received:
06
02
2024
accepted:
19
07
2024
medline:
6
8
2024
pubmed:
6
8
2024
entrez:
6
8
2024
Statut:
aheadofprint
Résumé
The brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) is an invasive pest that causes economic damage on crops, decreasing fruit yield and quality. Conventional insecticides are frequently used to reduce infestations, but these are often with a limited residual effect, besides being costly and detrimental to nontarget organisms and the environment. In integrated pest management, novel strategies against H. halys are proposed, such as the use of alternative substances with an effect on insect behaviour and mobility. As one of the oldest multi-site fungicides applied against fungal pathogens and as an insecticide and acaricide to control scales and mites, sulfur is proposed here to reduce H. halys infestation in fruit orchards. Field experiments were performed to evaluate the effect of repeated wettable sulfur applications on H. halys in apple and pear orchards. Sulfur-induced plant phytotoxicity effects and quanti-qualitative parameters on apple fruits were also recorded. Halyomorpha halys infestation was significantly reduced in sulfur-treated compared to untreated pears and apples. Furthermore, sulfur sprays reduced fruit damage caused by H. halys. Besides, sulfur-mediated phytotoxicity such as symptoms on leaves and fruit drop were not observed. Fruit quality was not influenced by sulfur treatments. Wettable sulfur seems to be a promising formulation given the low phytotoxicity, considering the technical aspects for an effective use of sulfur-based products to counteract H. halys in pome fruit orchards. © 2024 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Sections du résumé
BACKGROUND
BACKGROUND
The brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) is an invasive pest that causes economic damage on crops, decreasing fruit yield and quality. Conventional insecticides are frequently used to reduce infestations, but these are often with a limited residual effect, besides being costly and detrimental to nontarget organisms and the environment. In integrated pest management, novel strategies against H. halys are proposed, such as the use of alternative substances with an effect on insect behaviour and mobility. As one of the oldest multi-site fungicides applied against fungal pathogens and as an insecticide and acaricide to control scales and mites, sulfur is proposed here to reduce H. halys infestation in fruit orchards.
RESULTS
RESULTS
Field experiments were performed to evaluate the effect of repeated wettable sulfur applications on H. halys in apple and pear orchards. Sulfur-induced plant phytotoxicity effects and quanti-qualitative parameters on apple fruits were also recorded. Halyomorpha halys infestation was significantly reduced in sulfur-treated compared to untreated pears and apples. Furthermore, sulfur sprays reduced fruit damage caused by H. halys. Besides, sulfur-mediated phytotoxicity such as symptoms on leaves and fruit drop were not observed. Fruit quality was not influenced by sulfur treatments.
CONCLUSIONS
CONCLUSIONS
Wettable sulfur seems to be a promising formulation given the low phytotoxicity, considering the technical aspects for an effective use of sulfur-based products to counteract H. halys in pome fruit orchards. © 2024 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : European Union Next-GenerationEU
Organisme : European Union nor the European Commission
Informations de copyright
© 2024 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Références
Lee DH, Short BD, Joseph SV, Bergh JC and Leskey TC, Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641 (2013).
Leskey TC and Nielsen AL, Impact of the invasive brown marmorated stink bug in North America and Europe: history, biology, ecology, and management. Annu Rev Entomol 63:599–618 (2018).
Bariselli M, Bugiani R and Maistrello L, Distribution and damage caused by Halyomorpha halys in Italy. EPPO Bull 46:332–334 (2016).
Maistrello L, Dioli P, Vaccari G, Nannini R, Bortolotti P, Caruso S et al., First record in Italy of the Asian stink bug Halyomorpha halys, a new threat for fruit crops. Atti Giornate Fitopatol 1:283–288 (2014).
Wermelinger B, Wyniger D and Forster B, First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees. Bull Société Entomol Suisse 81:1–8 (2008).
Hoebeke ER and Carter ME, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237 (2003).
Gariepy TD, Haye T, Fraser H and Zhang J, Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. J Pest Sci 87:17–28 (2014).
Cesari M, Maistrello L, Piemontese L, Bonini R, Dioli P, Lee W et al., Genetic diversity of the brown marmorated stink bug Halyomorpha halys in the invaded territories of Europe and its patterns of diffusion in Italy. Biol Invasions 20:1073–1092 (2018).
Martinez‐Sañudo I, Perotti MA, Scaccini D, Pozzebon A, Marri L and Mazzon L, Co‐haplotyping symbiont and host to unravel invasion pathways of the exotic pest Halyomorpha halys in Italy. Sci Rep 10:1–10 (2020).
Laterza I, Dioli P and Tamburini G, Semi‐natural habitats support populations of stink bug pests in agricultural landscapes. Agric Ecosyst Environ 342:108223 (2023).
Cianferoni F, Graziani F, Dioli P and Ceccolini F, Review of the occurrence of Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae) in Italy, with an update of its European and world distribution. Biol 73:599–607 (2018).
Cesari M, Maistrello L, Ganzerli F, Dioli P, Rebecchi L and Guidetti R, A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci 88:1–7 (2015).
Mele A, Scaccini D, Zanolli P and Pozzebon A, Semi‐natural habitats promote biological control of Halyomorpha halys (Stål) by the egg parasitoid Trissolcus mitsukurii (Ashmead). Biol Control 166:104833 (2022).
Tamburini G, Laterza I, Nardi D, Mele A, Mori N, Pasini M et al., Effect of landscape composition on the invasive pest Halyomorpha halys in fruit orchards. Agric Ecosyst Environ 353:108530 (2023).
Acebes‐Doria AL, Morrison WR, Short BD, Rice KB, Bush HG, Kuhar TP et al., Monitoring and biosurveillance tools for the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). Insects 9:1–17 (2018).
Moore L, Tirello P, Scaccini D, Toews MD, Duso C and Pozzebon A, Characterizing damage potential of the brown marmorated stink bug in cherry orchards in Italy. Entomol Gen 39:271–283 (2019).
Chen JH, Avila GA, Zhang F, Guo LF, Sandanayaka M, Mi QQ et al., Field cage assessment of feeding damage by Halyomorpha halys on kiwifruit orchards in China. J Pest Sci 93:953–963 (2020).
Francati S, Masetti A, Martinelli R, Mirandola D, Anteghini G, Busi R et al., Halyomorpha halys (Hemiptera: Pentatomidae) on kiwifruit in northern Italy: phenology, infestation, and natural enemies assessment. J Econ Entomol 114:1733–1742 (2021).
Hedstrom CS, Shearer PW, Miller JC and Walton VM, The effects of kernel feeding by Halyomorpha halys (Hemiptera: Pentatomidae) on commercial hazelnuts. J Econ Entomol 107:1858–1865 (2014).
Lara JR, Kamiyama MT, Hernandez G, Nay J and Hoddle MS, Assessment of feeding acceptance and injury of kerman pistachios, pistacia vera, by brown marmorated stink bug (Hemiptera: Pentatomidae). J Insect Sci 17:106 (2017).
Rijal J and Gyawaly S, Characterizing brown marmorated stink bug injury in almond, a new host crop in California. Insects 9:1–8 (2018).
Stahl JM, Scaccini D, Pozzebon A and Daane KM, Comparing the feeding damage of the invasive brown marmorated stink bug to a native stink bug and leaffooted bug on California pistachios. Insects 11:1–13 (2020).
Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G et al., Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5:1–13 (2014).
Martinson HM, Raupp MJ and Shrewsbury PM, Invasive stink bug wounds trees, liberates sugars, and facilitates native hymenoptera. Ann Entomol Soc Am 106:47–52 (2013).
Scaccini D and Pozzebon A, Invasive brown marmorated stink bug (Hemiptera: Pentatomidae) facilitates feeding of European wasps and ants (hymenoptera: Vespidae, Formicidae) on plant exudates. Eur J Entomol 118:24–30 (2021).
Nielsen AL and Hamilton GC, Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J Econ Entomol 102:1133–1140 (2009).
Acebes‐Doria AL, Leskey TC and Bergh JC, Injury to apples and peaches at harvest from feeding by Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) nymphs early and late in the season. Crop Prot 89:58–65 (2016).
Maistrello L, Dioli P, Bariselli M, Mazzoli GL and Giacalone‐Forini I, Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in southern Europe. Biol Invasions 18:3109–3116 (2016).
Peiffer M and Felton GW, Insights into the saliva of the brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae). PLoS One 9:e88483 (2014).
Leskey TC, Short BD and Lee DH, Efficacy of insecticide residues on adult Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) mortality and injury in apple and peach orchards. Pest Manag Sci 70:1097–1104 (2014).
Kuhar TP and Kamminga K, Review of the chemical control research on Halyomorpha halys in the USA. J Pest Sci 90:1021–1031 (2017).
Blaauw BR, Polk D and Nielsen AL, IPM‐CPR for peaches: incorporating behaviorally‐based methods to manage Halyomorpha halys and key pests in peach. Pest Manag Sci 71:1513–1522 (2015).
Salerno G, Rebora M, Piersanti S, Saitta V, Kovalev A and Gorb E, Reduction in insect attachment caused by different nanomaterials used as particle films (kaolin, zeolite, calcium carbonate). Sustainability 13:8250 (2021).
Mafra‐Neto A, Wright M, Fettig C, Progar R, Munson S, Blackford D et al., Repellent semiochemical solutions to mitigate the impacts of global climate change on arthropod pests, in Advances in Arthropod Repellents, ed. by Corona C, Debboun M and Coats J. Academic press, Elsevier Science Publishers, London, pp. 279–322 (2022).
Shepard H, The Chemistry and Action of Insecticides. McGraw‐Hill, New York, NY (1951).
Forsyth W, in Observations on the Diseases, Defects, and Injuries, in all Kinds of Fruit and Forest Trees, ed. by Longman TN and Rees O. London, Goldsmiths'‐Kress library of economic literature, UK (1802).
Robertson J, On the Mildew and some Other Diseases Incident to Fruit Trees. Horticultural Society of London Transactions, London, UK (1824).
Emmett B, Wicks T and Magarey P, Strategic use of sulphur in integrated pest and disease management (IPM) programs for grapevines. Grape Wine Res Dev Corp:220 (2003).
Katsoulas N, Løes AK, Andrivon D, Cirvilleri G, de Cara M, Kir A et al., Current use of copper, mineral oils and sulphur for plant protection in organic horticultural crops across 10 European countries. Org Agric 10:159–171 (2020).
Griffith CM, Woodrow JE and Seiber JN, Environmental behavior and analysis of agricultural sulfur. Pest Manag Sci 71:1486–1496 (2015).
Daniel C, Haeseli A and Weibel F, The side effects of lime sulphur on predaceous arthropods, i.e. Typhlodromus pyri, and other leaf occupying arthropods, Vol. 1. FiBL – Forschungsinstitut für biologischen Landbau, Frick, Switzerland, pp. 1–8 (2002).
Webber J and Chapman RB, Timing of sulphur spray application for control of hazelnut big bud mites (Phytoptus avellanae and Cecidophyopsis vermiformis). New Zeal Plant Prot 61:191–196 (2008).
Duso C, Castagnoli M, Simoni S and Angeli G, The impact of eriophyoids on crops: recent issues on Aculus schlechtendali, Calepitrimerus vitis and Aculops lycopersici. Exp Appl Acarol 51:151–168 (2010).
Zappalà L, Siscaro G, Biondi A, Mollá O, González‐Cabrera J and Urbaneja A, Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J Appl Entomol 136:401–409 (2012).
Pérez‐Guerrero S, Molina JM, Montiel C, Redondo‐Villa A and Avivar‐Lozano L, Laboratory evaluation of effects of powdered sulphur on the oviposition, fruit detection and behaviour of Drosophila suzukii (Diptera: Drosophilidae) on strawberry. Eur J Entomol 117:210–215 (2020).
Tacoli F, Cargnus E, Zandigiacomo P and Pavan F, Side effects of sulfur dust on the European grapevine moth Lobesia botrana and the predatory mite Kampimodromus aberrans in vineyards. Insects 11:1–13 (2020).
Falk KL, Tokuhisa JG and Gershenzon J, The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biol 9:573–581 (2007).
Capaldi FR, Gratão PL, Reis AR, Lima LW and Azevedo RA, Sulfur metabolism and stress defense responses in plants. Trop Plant Biol 8:60–73 (2015).
Holb IJ, De Jong PF and Heijne B, Efficacy and phytotoxicity of lime sulphur in organic apple production. Ann Appl Biol 142:225–233 (2003).
Cappellini M, Il gelo danneggia il 75% della produzione agricola del Centro Nord. Il Sole 24 ore Available: https://www.ilsole24ore.com/art/il‐gelo‐danneggia‐75percento‐produzione‐agricola‐centro‐nord‐ADI9RKWB?refresh_ce=1 [10 December 2023].
Fornasiero D, Scaccini D, Lombardo V, Galli G and Pozzebon A, Effect of exclusion net timing of deployment and color on Halyomorpha halys (Hemiptera: Pentatomidae) infestation in pear and apple orchards. Crop Prot 172:106331 (2023).
Edwards L, Organic Tree Fruit Management. Certified Organic Association of British Columbia, Canada (1998).
Fallahi E and Willemsen KM, Blossom thinning of pome and stone fruit. HortScience 37:474–477 (2002).
Stopar M, Thinning of flowers/fruitlets in organic apple production. J Fruit Ornam Plant Res 12:77–84 (2004).
Alrashedi MM, Blossom Thinning and Managing Bitter Pit, Storage Life and Fruit Quality in Organically Grown Apples. Curtin University in Perth, Australia (2015).
SAS Institute ed, PROC User's Manual, 6th edn. SAS Institute, Cary, NC, USA (2016).
Littell RCG, Milliken A, Stroup WW, Wolfinger RD and Schabenberger O, SAS for Mixed Models. SAS Institute, Cary, NC (1996).
Lee DH, Short BD, Nielsen AL and Leskey TC, Impact of organic insecticides on the survivorship and mobility of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in the laboratory. Fla Entomol 97:414–421 (2014).
Zhang QH, Schneidmiller RG, Hoover DR, Zhou G, Margaryan A and Bryant P, Essential oils as spatial repellents for the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). J Appl Entomol 138:490–499 (2014).
Bulgarini G, Bortolini S and Maistrello L, Repellent activity of essential oils on adults of Halyomorpha halys (Heteroptera: Pentatomidae) in different physiological‐behavioural phases. J Appl Entomol 145:575–586 (2021).
Kuhar TP, Morehead JA and Formella AJ, Applications of kaolin protect fruiting vegetables from brown marmorated stink bug (Hemiptera: Pentatomidae). J Entomol Sci 54:401–408 (2019).
Scaccini D, Mirandola E, Sirapu S, Simoni F, Fornasiero D, Duso C et al., Wettable sulphur application for Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) management: laboratory and semi‐field experiments. Pest Manag Sci 80:3620–3627 (2024). https://doi.org/10.1002/ps.8066.
Hartley T, Sulphur particle size composition, Vol. 393. Australian Grapegrower and Winemaker, Adelaide, Australia, p. 76 (1996).
IRAC, The IRAC mode of action classification online – The definitive, global scheme on the target sites of acaricides and insecticides Available: https://irac-online.org/mode-of-action/classification-online/ [21 March 2024].
Yarwood C, Effect of temperature on the fungicidal action of sulphur. Phytopathology 40:173–180 (1949).
Thomas CS, Gubler WD, Silacci MW and Miller R, Changes in elemental sulfur residues on pinot noir and cabernet sauvignon grape berries during the growing season. Am J Enol Vitic 44:205–210 (1993).
Drake CR, Efficacy of various fungicides and fungicide combinations for control of peach disease. Fungicide Nematicide Tests 39:40 (1984).
Scherm H and Savelle AT, Control of peach scab with reduced summer fungicide programmes. Plant Dis 85:706–712 (2001).
Lan Z, Scherm H and Horton DL, Reduced midseason pesticide program for control of scab and plum curculio in peach. Plant Dis 87:699–706 (2003).
Palmer JW, Davies SB, Shaw PW and Wünsche JN, Growth and fruit quality of “Braeburn” apple (Malus domestica) trees as influenced by fungicide programmes suitable for organic production. New Zeal J Crop Hortic Sci 31:169–177 (2003).
Basak A, Soczek Z, Cisek B and Karolczak W, Control of russeting of Golden delicious apples with Golclair. Fruits Sci Reports 10:67–72 (1983).
Sánchez E, Soto JM, Uvalle JX, Hernández AP, Ruiz JM and Romero L, Chemical treatments in “Golden delicious spur” fruits in relation to russeting and nutritional status. J Plant Nutr 24:191–202 (2001).
Steenkamp J, Van Zyl HJ and Westraad I, A preliminary evaluation of various chemical substances for the control of calyx‐end russeting in Golden delicious apples. J Hortic Sci 59:501–505 (1984).
Schnabel G and Layne DR, Comparison of reduced‐application and sulfur‐based fungicide programs on scab intensity, fruit quality, and cost of disease control on peach. Plant Dis 88:162–166 (2004).
Haye T, Abdallah S, Gariepy T and Wyniger D, Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci 87:407–418 (2014).
Scaccini D, Duso C and Pozzebon A, Lethal effects of high temperatures on brown marmorated stink bug adults before and after overwintering. Insects 10:355 (2019).
Khadka A, Hodges AC, Leppla NC and Tillman PG, The effects of relative humidity on Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) egg hatch, nymph survival, and adult reproduction. Fla Entomol 103:136–138 (2020).
Fisher JJ, Rijal JP and Zalom FG, Temperature and humidity interact to influence brown marmorated stink bug (Hemiptera: Pentatomidae), survival. Environ Entomol 50:390–398 (2021).
Stahl JM, Scaccini D and Daane KM, Field survival of the brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae) on california tree crops. Environ Entomol 50:1187–1193 (2021).
Candian V, Pansa MG, Briano R, Peano C, Tedeschi R and Tavella L, Exclusion nets: a promising tool to prevent Halyomorpha halys from damaging nectarines and apples in NW Italy. Bull Insectol 71:21–30 (2018).
Candian V, Pansa MG, Santoro K, Spadaro D, Briano R, Peano C et al., First multi‐target application of exclusion net in nectarine orchards: effectiveness against pests and impact on beneficial arthropods, postharvest rots and fruit quality. Insects 12:210 (2021).
Falagiarda M, Carnio V, Chiesa SG, Pignalosa A, Anfora G, Angeli G et al., Factors influencing short‐term parasitoid establishment and efficacy for the biological control of Halyomorpha halys with the samurai wasp Trissolcus japonicus. Pest Manag Sci 79:2397–2414 (2023).
Zapponi L, Tortorici F, Anfora G, Bardella S, Bariselli M, Benvenuto L et al., Assessing the distribution of exotic egg parasitoids of Halyomorpha halys in Europe with a large‐scale monitoring program. Insects 12:316 (2021).