Eur. J. Entomol. 118: 200-209, 2021 | DOI: 10.14411/eje.2021.021
SOIL-INSECT toolbox: A new chamber for analysing the behaviour of herbivorous insects and tri-trophic interactions in soilOriginal article
- 1 Department of Plant Protection, The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland; e-mails: ewa.furmanczyk@inhort.pl, malgorzata.tartanus@inhort.pl, eligio.malusa@inhort.pl
- 2 Fruit and Vegetable Storage and Processing Department, The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland; e-mail: zbigniew.jozwiak@inhort.pl
A chamber, named SOIL-INSECT toolbox, was developed to analyse the effect of various factors on the behaviour of soil-dwelling insects. It is equipped with sensors that continuously monitor the concentration of CO2 in the different compartments of the chamber without disturbing the air balance in the soil. The chamber can be adapted to study different stimuli, including volatile compounds, both in the presence and absence of plants. The chamber was tested using the larvae of Melolontha spp., which confirmed its suitability for carrying out complex studies on insect-insect and insect-plant-microbiome interactions in a complex environment such as soil. The results of behavioural experiments using L3 larvae of Melolontha spp. in sterilized and natural soils revealed that the soil condition affected the behaviour of the larvae, likely due to its effect on the soil microbiome and physico-chemical characteristics.
Keywords: Subterranean insects, behaviour, herbivory, tri-trophic interactions, biotest arena, carbon dioxide, Melolontha spp., volatile compounds
Received: February 12, 2021; Revised: May 14, 2021; Accepted: May 14, 2021; Published online: July 7, 2021 Show citation
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References
- Arimura G.-I., Ozawa R. & Maffei M.E. 2011: Recent advances in plant early signaling in response to herbivory. - Int. J. Mol. Sci. 12: 3723-3739.
Go to original source... - Ariño A.H., Belascoáin C. & Jordana R. 2008: Optimal sampling for complexity in soil ecosystems. In Minai A.A. & Bar-Yam Y. (eds): Unifying Themes in Complex Systems IV. Springer, Berlin, Heidelberg, pp. 222-230.
Go to original source... - Badía D. & Martí C. 2003: Plant ash and heat intensity effects on chemicaland physical properties of two contrasting soils. - Arid Land Res. Manag. 17: 23-41.
Go to original source... - Bernklau E.J., Fromm E.A. & Bjostad L.B. 2004: Disruption of host location of western corn rootworm larvae (Coleoptera: Chrysomelidae) with carbon dioxide. - J. Econ. Entomol. 97: 330-339.
Go to original source... - Biasazin T.D., Chernet H.T., Herrera S.L., Bengtsson M., Karlsson M.F., Lemmen-Lechelt J.K. & Dekker T. 2018: Detection of volatile constituents from food lures by tephritid fruit flies. - Insects 9: 119, 14 pp.
Go to original source... - Biere A. & Bennett A.E. 2013: Three-way interactions between plants, microbes and insects. - Funct. Ecol. 27: 567-573.
Go to original source... - Bustos-Segura C. & Foley W.J. 2018: Foliar terpene chemotypes and herbivory determine variation in plant volatile emissions. - J. Chem. Ecol. 44: 51-61.
Go to original source... - Dolci P., Guglielmo F., Secchi F. & Ozino O.I. 2006: Persistence and efficacy of Beauveria brongniartii strains applied as biocontrol agents against Melolontha melolontha in the valley of Aosta (northwest Italy). - J. Appl. Microbiol. 100: 1063-1072.
Go to original source... - Erwin A.C., Geber M.A. & Agrawal A.A. 2013: Specific impacts of two root herbivores and soil nutrients on plant performance and insect-insect interactions. - Oikos 122: 1746-1756.
Go to original source... - Fang C. & Moncrieff J.B. 1999: A model for soil CO2 production and transport 1: Model development. - Agric. For. Meteorol. 95: 225-236.
Go to original source... - Fierer N., Strickland M.S., Liptzin D., Bradford M.A. & Cleveland C.C. 2009: Global patterns in belowground communities. - Ecol. Lett. 12: 1238-1249.
Go to original source... - G³owacka B. & Sierpiñska A. 2012: Control of adult cockchafers Melolontha spp. with Mospilan 20 SP. - Folia For. Pol. (A) 54: 109-115.
- Görres C.-M. & Chesmore D. 2019: Active sound production of scarab beetle larvae opens up new possibilities for species-specific pest monitoring in soils. - Sci. Rep. 9: 10115, 10 pp.
Go to original source... - Grunseich J.M., Thompson M.N., Aguirre N.M. & Helms A.M. 2020: The role of plant-associated microbes in mediating host-plant selection by insect herbivores. - Plants 9: 6, 23 pp.
Go to original source... - Hassani M.A., Durán P. & Hacquard S. 2018: Microbial interactions within the plant holobiont. - Microbiome 6: 58, 17 pp.
Go to original source... - Hinsinger P., Gobran G.R., Gregory P.J. & Wenzel W.W. 2005: Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. - New Phytol. 168: 293-303.
Go to original source... - Johnson S.N. & Gregory P.J. 2006: Chemically-mediated host-plant location and selection by root-feeding insects. - Physiol. Entomol. 31: 1-13.
Go to original source... - Kallenbach M., Veit D., Eilers E. & Schuman M. 2015: Application of silicone tubing for robust, simple, high-throughput, and time-resolved analysis of plant volatiles in field experiments. - BIO-Protoc. 5: e1391, 12 pp.
Go to original source... - Kanchiswamy C.N., Malnoy M. & Maffei M.E. 2015: Chemical diversity of microbial volatiles and their potential for plant growth and productivity. - Front. Plant Sci. 6: 151, 23 pp.
Go to original source... - Karpelson M., Wood R. & Wei G.-Y. 2008: A review of actuation and power electronics options for flapping-wing robotic insects. In: Proc. of the IEE International Conference on Robotics and Automation, Pasadena, CA, USA, May 19-23, 2008. Institute of Electrical and Electronics Engineers, pp. 779-786.
Go to original source... - Kojima W. 2015: Attraction to carbon dioxide from feeding resources and conspecific neighbours in larvae of the rhinoceros beetle Trypoxylus dichotomus. - PLoS ONE 10: e0141733, 11 p.
Go to original source... - Kuzyakov Y. & Larionova A.A. 2005: Root and rhizomicrobial respiration: A review of approaches to estimate respiration by autotrophic and heterotrophic organisms in soil. - J. Plant Nutr. Soil Sci. 168: 503-520.
Go to original source... - Loreto F. & Schnitzler J.-P. 2010: Abiotic stresses and induced BVOCs. - Spec. Issue Induc. Biog. Volatile Org. Compd. Plants 15: 154-166.
Go to original source... - Malusá E., Tartanus M., Furmanczyk E.M. & £abanowska B.H. 2020: Holistic approach to control Melolontha spp. in organic strawberry plantations. - Org. Agric. 10: 13-22.
Go to original source... - McAlary T., Groenevelt H., Nicholson P., Seethapathy S., Sacco P., Crump D., Tuday M., Hayes H., Schumacher B., Johnson P. et al. 2014a: Quantitative passive soil vapor sampling for VOCs- part 3: field experiments. - Environ. Sci. Process Impacts 16: 501-510.
Go to original source... - McAlary T., Wang X., Unger A., Groenevelt H. & Górecki T. 2014b: Quantitative passive soil vapor sampling for VOCs- part 1: theory. - Environ. Sci. Process Impacts 16: 482-490.
Go to original source... - Mercado-Blanco J., Abrantes I., Barra Caracciolo A., Bevivino A., Ciancio A., Grenni P., Hrynkiewicz K., Kredics L. & Proença D.N. 2018: Belowground Microbiota and the health of tree crops. - Front. Microbiol. 9: 1006, 27 pp.
Go to original source... - Moreau M., Arrufat P., Latil G. & Jeanson R. 2011: Use of radio-tagging to map spatial organization and social interactions in insects. - J. Exp. Biol. 214: 17-21.
Go to original source... - Murlis J., Elkinton J.S. & Cardé R.T. 1992: Odor plumes and how insects use them. - Annu. Rev. Entomol. 37: 505-532.
Go to original source... - Neumann G., George T.S. & Plassard C. 2009: Strategies and methods for studying the rhizosphere - the plant science toolbox. - Plant Soil 321: 431-456.
Go to original source... - Paudel S., Lin P.-A., Foolad M.R., Ali J.G., Rajotte E.G. & Felton G.W. 2019: Induced plant defenses against herbivory in cultivated and wild tomato. - J. Chem. Ecol. 45: 693-707.
Go to original source... - Pedrazzini C., Strasser H., Holderegger R., Widmer F. & Enkerli J. 2021: Development of a SNP-based tool for the identification and discrimination of Melolontha melolontha and Melolontha hippocastani. - Bull. Entomol. Res. [in press].
Go to original source... - R Core Team 2019: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
- Reinecke A., Müller F. & Hilker M. 2008: Attractiveness of CO2 released by root respiration fades on the background of root exudates. - Basic Appl. Ecol. 9: 568-576.
Go to original source... - Rolston D.E. 2005: Aeration. In Hillel D. (ed.): Encyclopedia of Soils in the Environment. Elsevier, Oxford, pp. 17-21.
Go to original source... - Sas Paszt L. & Zurawicz E. 2005: Studies of the rhizosphere of strawberry plants at the research institute of pomology and floriculture in Skierniewice, Poland. - Int. J. Fruit Sci. 5: 115-126.
Go to original source... - Schenkel D., Lemfack M.C., Piechulla B. & Splivallo R. 2015: A meta-analysis approach for assessing the diversity and specificity of belowground root and microbial volatiles. - Front. Plant Sci. 6: 107, 12 pp.
Go to original source... - Schmidt M. & Hurling R. 2014: A spatially-explicit count data regression for modeling the density of forest cockchafer (Melolontha hippocastani) larvae in the Hessian Ried (Germany). - For. Ecosyst. 1: 19, 16 pp.
Go to original source... - Shen R., Pennell K.G. & Suuberg E.M. 2013: Influence of soil moisture on soil gas vapor concentration for vapor intrusion. - Environ. Eng. Sci. 30: 628-637.
Go to original source... - Shikano I., Rosa C., Tan C.-W. & Felton G.W. 2017: Tritrophic interactions: Microbe-mediated plant effects on insect herbivores. - Annu. Rev. Phytopathol. 55: 313-331.
Go to original source... - Smith K.A., Ball T., Conen F., Dobbie K.E., Massheder J. & Rey A. 2018: Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. - Eur. J. Soil Sci. 69: 10-20.
Go to original source... - Stêpniewski W., Stêpniewska Z. & Ro¿ej A. 2011: Gas Exchange in Soils. Soil Management: Building a Stable Base for Agriculture. John Wiley & Sons, pp. 117-144.
Go to original source... - Thompson L.R., Sanders J.G., McDonald D., Amir A., Ladau J., Locey K.J., Prill R.J., Tripathi A., Gibbons S.M., Ackermann G. et al. 2017: A communal catalogue reveals Earth's multiscale microbial diversity. - Nature 551: 457-463.
Go to original source... - Turlings T.C.J., Davison A.C. & Tamò C. 2004: A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. - Physiol. Entomol. 29: 45-55.
Go to original source... - Vemmer M., Schumann M., Beitzen-Heineke W., French B.W., Vidal S. & Patel A.V. 2016: Development of a CO2-releasing coformulation based on starch, Saccharomyces cerevisiae and Beauveria bassiana attractive towards western corn rootworm larvae. - Pest Manag. Sci. 72: 2136-2145.
Go to original source... - Wagenhoff E., Blum R. & Delb H. 2014: Spring phenology of cockchafers, Melolontha spp. (Coleoptera: Scarabaeidae), in forests of south-western Germany: Results of a 3-year survey on adult emergence, swarming flights, and oogenesis from 2009 to 2011. - J. For. Sci. 60: 154-165.
Go to original source... - Zvereva E.L. & Kozlov M.V. 2012: Sources of variation in plant responses to belowground insect herbivory: a meta-analysis. - Oecologia 169: 441-452.
Go to original source...
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