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Impact of the invasive painted bug Bagrada hilaris on physiological traits of its host Brassica oleracea var botrytis

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Abstract

Bagrada hilaris is a herbivorous insect native of Asia and Africa, which has invaded southern Europe and North America where it causes major damage to cole crops. Laboratory experiments were conducted to assess how the infestation of this invasive species damages the host Brassica oleracea var botrytis, and to evaluate the interaction between plant emission of volatile organic compounds (VOC) and B. hilaris adults. Plant responses to insect feeding were evaluated through changes in photosynthesis, stomatal conductance, VOC emission, and visual damage on leaves. The impact of B. hilaris was compared with that of Nezara viridula, a polyphagous species distributed worldwide. Plant VOC role in host plant detection was tested with electroantennography bioassays on B. hilaris antenna. Photosynthesis and stomatal conductance were consistently reduced in plants infested with 40 B. hilaris adults for 24 h. The feeding activity of a single B. hilaris caused larger discolored spots on host leaves in comparison with N. viridula. VOC emitted by B. oleracea changed significantly in response to B. hilaris and N. viridula infestation. In particular, production of limonene was strongly reduced by the infestation of the two pentatomids, while an increase in the emission of acetic acid and 2-ethyl-1-hexanol was observed. EAG dose–response tests using the main plant VOC showed B. hilaris antennal responses to benzaldehyde, octanal, nonanal, and acetic acid, which indicates a role of these compounds in host location.

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References

  • Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500

    Article  Google Scholar 

  • Agrawal AA, Kurashige NS (2003) A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. J Chem Ecol 29:1403–1415

    Article  CAS  PubMed  Google Scholar 

  • Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302

    Article  CAS  PubMed  Google Scholar 

  • Barros AF, Campos VP, da Silva JCP, Pedroso MP, Medeiros FHV, Pozza EA, Reale AL (2014) Nematicidal activity of volatile organic compounds emitted byBrassica juncea, Azadirachta indica, Canavalia ensiformis, Mucuna pruriens and Cajanus cajan against Meloidogyne incognita. Appl Soil Ecol 80 :34–43

    Article  Google Scholar 

  • Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  CAS  PubMed  Google Scholar 

  • Bundy CS, Grasswitz TR, Sutherland C (2012) First report of the invasive stink bug Bagrada hilaris (Burmeister) (Heteroptera: Pentatomidae) from New Mexico, with notes on its biology. Southwest Entomol 37:411–412

    Article  Google Scholar 

  • CAB International (1981) Bagrada hilaris. Distribution map. Distribution Maps of Plant Pests. Map 417

  • Colazza S, Guarino S, Peri E (2004) Bagrada hilaris (Burmeister) (Heteroptera: Pentatomidae) fitofago dannoso al cappero nell’isola di Pantelleria. Inf Fitopatol 12:30–34

    Google Scholar 

  • Conti E, Zadra C, Salerno G, Leombruni B, Volpe D, Frati F, Marucchini C, Bin F (2008) Changes in the volatile profile of Brassica oleracea due to feeding and oviposition by Murgantia istrionica (Heteroptera: Pentatomidae). Eur J Entomol 105:839–847

    Article  CAS  Google Scholar 

  • Dicke M, Van Loon JJA (2000) Multitrophic effect of the herbivore-induced plant volatile in a evolutionary context. Ent Exp Appl 97:237–249

    Article  CAS  Google Scholar 

  • Du Y, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM (1998) Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355–1368

    Article  CAS  Google Scholar 

  • Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51

    Article  CAS  PubMed  Google Scholar 

  • Franke H, Fegan M, Hayward C, Leonard G, Stackebrandt C, Sly LI (1999) Description of Gluconacetobacter sacchari sp. nov., a new species of acetic acid bacterium isolated from the leaf sheath of sugar cane and from the pink sugar-cane mealy bug. Int J Syst Evol Microbiol 49:1681–1693

    CAS  Google Scholar 

  • Gershenzon J (1993) The cost of plant chemical defenses against herbivory: a biochemical perspective. In: Bernays EA (ed) Insect-plant interactions, vol 5. CRC Press, Boca Raton, pp 105–173

    Google Scholar 

  • Gershenzon J, Croteau R (1991) Terpenoids. In: Rosenthal GA, Berenbaum MR (eds) Herbivores, their interactions with secondary metabolites. Academic Press, New York, pp 169–219

    Google Scholar 

  • Guarino S, De Pasquale C, Peri E, Alonzo G, Colazza S (2008) Role of volatile and contact pheromones in the mating behaviour of Bagrada hilaris (Heteroptera: Pentatomidae). Eur J Entomol 105:613–617

    Article  CAS  Google Scholar 

  • Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333

    Article  CAS  PubMed  Google Scholar 

  • Hare JD, Elle E (2002) Variable impact of diverse insect herbivores on dimorphic Datura wrightii. Ecology 83:2711–2720

    Article  Google Scholar 

  • Hatanaka A (1993) The biogeneration of green odour by green leaves. Phytochemistry 34:1201–1218

    Article  CAS  Google Scholar 

  • Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184

    Article  CAS  PubMed  Google Scholar 

  • Hopkins RJ, van Dam NM, van Loon JJ (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83

    Article  CAS  PubMed  Google Scholar 

  • Hori K (2000) Possible causes of disease symptoms resulting from the feeding of phytophagous Heteroptera. Heteroptera of economic importance. CRC Press, Boca Raton, pp. 11–36

    Google Scholar 

  • Huang TI, Reed DA, Perring T, Palumbo JC (2014) Feeding damage by Bagrada hilaris (Hemiptera: Pentatomidae) and impact on growth and chlorophyll content of Brassicaceous plant species. Arthropod Plant Interact 8:89–100

    Article  Google Scholar 

  • Jardine K, Barron-Gafford GA, Norman JP, Abrell L, Monson RK, Meyers KT, Pavao-Zuckerman M, Dontsova K, Kleist E, Werner C, Huxman TE (2012) Green leaf volatiles and oxygenated metabolite emission bursts from mesquite branches following light-dark transitions. Photosynth Res 113:321–333

    Article  CAS  PubMed  Google Scholar 

  • Jenkins MA (2003) Impact of the balsam woolly adelgid (Adelges piceae Ratz.) on an Abies fraseri (Pursh) Poir. dominated stand near the summit of Mount LeConte, Tennessee. Castanea 68:109–111

    Google Scholar 

  • Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Péré C, Cock MJW, Settele J, Augustin S, Lopez-Vaamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45

    Article  Google Scholar 

  • Lewinsohn E, Gijzen M, Croteau R (1991) Defense mechanisms of conifers, differences in constitutive and wound-induced monoterpene biosynthesis among species. Plant Physiol 96:44–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Litvak ME, Monson RK (1998) Patterns of induced and constitutive monoterpene production in conifer needles in relation to insect herbivory. Oecologia 114:531–540

    Article  PubMed  Google Scholar 

  • Loreto F, Ciccioli P, Cecinato A, Brancaleoni E, Frattoni M, Tricoli D (1996) Influence of environmental factors and air composition on the emission of α-pinene from Quercus ilex leaves. Plant Physiol 110:267–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loreto F, Forster A, Durr M, Csiky O, Seufert G (1998) On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex fumigated with selected monoterpenes. Plant Cell Environ 21:101–107

    Article  CAS  Google Scholar 

  • Loreto F, Pinelli P, Manes F, Kollist H (2004) Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilexleaves. Tree Physiol 24:361–367

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Barta C, Brilli F, Nogues I (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant Cell Environ 29:1820–1828

    Article  CAS  PubMed  Google Scholar 

  • Ludwig SW, Kok LT (2001) Harlequin bug, Murgantia histrionica (Hahn) (Heteroptera: Pentatomidae) development on three crucifers and feeding damage on broccoli. Crop Prot 20:247–251

    Article  Google Scholar 

  • Mattiacci L, Dicke M, Posthumus MA (1994) Induction of parasitoid attracting synomone in Brussels sprouts plants by feeding of Pieris brassicae larvae: Role of mechanical damage and herbivore elicitor. J Chem Ecol 20:2229–2247

    Article  CAS  PubMed  Google Scholar 

  • Miles PW (1972) The saliva of Hemiptera. Adv Insect Physiol 9:183–255

    Article  CAS  Google Scholar 

  • Moujahed R, Frati F, Cusumano A, Salerno G, Conti E, Peri E, Colazza S (2014) Egg parasitoid attraction toward induced plant volatiles is disrupted by a non-host herbivore attacking above or belowground plant organs. Front Plant Sci. doi:10.3389/fpls.2014.00601

    PubMed  PubMed Central  Google Scholar 

  • Müller K, Pelzing M, Gnauk T, Kappea A, Teichmann U, Spindler S, Haferkorn S, Jahn Y Hartmut H (2002) Monoterpene emissions and carbonyl compound air concentrations during the blooming period of rape (Brassica napus). Chemosphere 49:1247–1256

    Article  PubMed  Google Scholar 

  • Müller C, van Loon J, Ruschioni S, De Nicola GR, Olsen CE, Iori R, Agerbirk N (2015) Taste detection of the non-volatile isothiocyanate moringin results in deterrence to glucosinolate-adapted insect larvae. Phytochemistry 118:139–148

    Article  PubMed  Google Scholar 

  • Palumbo JC, Natwick ET (2010) The Bagrada bug (Hemiptera: Pentatomidae): a new invasive pest of cole crops in Arizona and California. Plant Management Network, http://www.plantmanagementnetwork.org/pub/php/brief/2010/bagrada/. Accessed 30 August 2010

  • Palumbo JC, Perring TM, Millar JG, Reed DA (2016) Biology, ecology, and management of an invasive stink bug, Bagrada hilaris, in North America. Annu Rev Entomol 61:453–473

    Article  CAS  PubMed  Google Scholar 

  • Paré PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167

    Article  PubMed  PubMed Central  Google Scholar 

  • Paris C, Llusia J, Peñuelas J (2010) Changes in monoterpene emission rates of Quecus ilex infested by aphid tended by native or invasive Lasius ant species. J Chem Ecol 36:689–698

    Article  CAS  PubMed  Google Scholar 

  • Reed DA, Palumbo JC, Perring TM, May C (2013) Bagrada hilaris (Hemiptera: Pentatomidae), an invasive stink bug attacking cole crops in the southwestern United States. J Int Pest Man 4:1–7

    Google Scholar 

  • Romeo V, Ziino M, Giuffrida D, Condurso C, Verzera (2007) A Flavour profile of capers (Capparis spinosa L.) from the Eolian Archipelago by HS-SPME/GC–MS. Food Chem 101:1272–1278

    Article  CAS  Google Scholar 

  • Roques A, Rabitsch W, Rasplus JY, Lopez-Vaamonde C, Nentwig W, Kenis M (2009) Alien terrestrial invertebrates of Europe. In: Handbook of alien species in Europe. Springer, Netherlands, pp. 63–79

    Chapter  Google Scholar 

  • Ruther J, Reinecke A, Hilker M (2002) Plant volatiles in the sexual communication of Melolontha hippocastani: response towards time-dependent bouquets and novel function of (Z)-3-hexen-1-ol as a sexual kairomone. Ecol Entomol 27:76–83

    Article  Google Scholar 

  • Sánchez-Peña S (2014) First record in Mexico of the invasive stink bug Bagrada hilaris, on cultivated crucifers in Saltillo. Southwest Entomol 39:375–376

    Article  Google Scholar 

  • Schaefer CW, Panizzi AR (2000) Economic importance of Heteroptera: a general view. Heteroptera of economic importance. CRC Press, Boca Raton, pp. 3–8

    Book  Google Scholar 

  • Schroeder R, Hilker M (2008) The relevance of background odor in resource location by insects: a behavioral approach. Bioscience 58:308–316

    Article  Google Scholar 

  • Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits—possible consequences for their natural enemies. Biol Control 11:122–129

    Article  Google Scholar 

  • Van der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. In Proceedings of the 9th International Symposium on Insect-Plant Relationships, Springer, Netherlands, pp. 307–310

  • Velikova V, Salerno G, Frati F, Peri E, Conti E, Colazza S Loreto F (2010) Influence of feeding and oviposition by phytophagous pentatomids on photosynthesis of herbaceous plants. J Chem Ecol 36:629–641

    Article  CAS  PubMed  Google Scholar 

  • Welter SC (1989) Arthropod impact on plant gas exchange. In: Bernays EA (ed) Insect–Plant Interactions. CRC Press, Boca Raton, pp 135–151

    Google Scholar 

  • Williams III L, Rodriguez-Saona C, Paré PW, Crafts-Brandner SJ (2005) The piercing-sucking herbivores Lygus hesperus and Nezara viridula induce volatile emission in plants. Arch Insect Biochem 58:84–96

    Article  CAS  Google Scholar 

  • Wiman NG, Walton VM, Shearer PW, Rondon SI (2014) Electronically monitored labial dabbing and stylet ‘probing’behaviors of brown marmorated stink bug, Halyomorpha halys, in simulated environments. PLoS One 9(12):e113514

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao D, Thang J, Ding X (2007) Analysis of volatile components during potherb mustard (Brassica juncea Coss.) pickle fermentation using SPME–GC-MS. LWT-Food Sci Technol 40:439–447

    Article  CAS  Google Scholar 

  • Zvereva E, Lanta V, Kozlov M (2010) Effects of sap-feeding insect herbivores on growth and reproduction of woody plants: a meta-analysis of experimental studies. Oecologia 163:949–960

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to Dr. David Hall for reviewing an early draft of the manuscript and to Dr. Gabriele Cencetti for his helpful assistance during the GC–MS analysis. This work was supported by the Italian Ministry of Education, University and Research, within the Project “Assessing the impacts of invasive fungal pathogens and phytophagous insects on native plants, pathogens, phytophagous insects and symbionts” (FIRB 2012 - Programma “Futuro in Ricerca” 2012 - RBFR128ONN).

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Authors and Affiliations

  1. Dipartimento di Scienze Agrarie e Forestali, Università degli Studi di Palermo, Viale delle Science, Edificio 5, 90128, Palermo, Italy

    Salvatore Guarino, Ezio Peri & Stefano Colazza

  2. Istituto per la Protezione Sostenibile delle Piante, CNR, Via Madonna del Piano, 10, Sesto Fiorentino, 50019, Florence, Italy

    Salvatore Guarino & Nicola Luchi

  3. Istituto di Bioscienze e Biorisorse, CNR, Via Madonna del Piano, 10, Sesto Fiorentino, 50019, Florence, Italy

    Marco Michelozzi

  4. Dipartimento di Scienze Bio-agroalimentari, CNR, Piazzale Aldo Moro 7, 00185, Roma, Italy

    Francesco Loreto

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  1. Salvatore Guarino
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  2. Ezio Peri
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  3. Stefano Colazza
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  4. Nicola Luchi
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  6. Francesco Loreto
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Correspondence to Salvatore Guarino.

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Guarino, S., Peri, E., Colazza, S. et al. Impact of the invasive painted bug Bagrada hilaris on physiological traits of its host Brassica oleracea var botrytis. Arthropod-Plant Interactions 11, 649–658 (2017). https://doi.org/10.1007/s11829-017-9516-6

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  • DOI: https://doi.org/10.1007/s11829-017-9516-6

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