Effects of host plants reared under elevated CO2 concentrations on the foraging behavior of different stages of corn leaf aphids rhopalosiphum maidis

Chen, Yu; Martin, Clément; Fingu Mabola, Junior Corneille; Verheggen, François; Wang, Zhenying; He, KangLai; Francis, Frédéric

doi:10.3390/insects10060182

Article (Scientific journals)

Effects of host plants reared under elevated CO2 concentrations on the foraging behavior of different stages of corn leaf aphids rhopalosiphum maidis

Chen, Yu; Martin, Clément; Fingu Mabola, Junior Corneille et al.

2019 • In Insects

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/242259

DOI
10.3390/insects10060182

PubMed
31234573

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Keywords :

climate change; corn leaf aphid; foraging behavior; volatile organic compounds (VOCs)

Abstract :

[en] Climate change is a major environmental concern and is directly related to the increasing concentrations of greenhouse gases. The increase in concentrations of atmospheric carbon dioxide (CO2), not only a ects plant growth and development, but also a ects the emission of plant organic volatile compounds (VOCs). Changes in the plant odor profile may a ect the plant-insect interactions, especially the behavior of herbivorous insects. In this study, we compared the foraging behavior of corn leaf aphid (Rhopalosiphum maidis) on barley (Hordeum vulgare L.) seedlings grown under contrasted CO2 concentrations. During the dual choice bioassays, the winged and wingless aphids were more attracted by the VOCs of barley seedlings cultivated under ambient CO2 concentrations (aCO2; 450 ppm) than barley seedlings cultivated under elevated CO2 concentrations (eCO2; 800 ppm), nymphs were not attracted by the VOCs of eCO2 barley seedlings. Then, volatile compositions from 14-d-old aCO2 and eCO2 barley seedlings were investigated by GC-MS. While 16 VOCs were identified from aCO2 barley seedlings, only 9 VOCs were found from eCO2 barley seedlings. At last, we discussed the potential role of these chemicals observed during choice bioassays. Our findings lay foundation for functional response of corn leaf aphid under climate change through host plant modifications.

Disciplines :

Agriculture & agronomy

Author, co-author :

Chen, Yu ; Université de Liège - ULiège > Stem Cells-Medical Chemistry

Martin, Clément ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Fingu Mabola, Junior Corneille ; Université de Liège - ULiège > Gembloux Agro-Bio Tech

Verheggen, François ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Wang, Zhenying

He, KangLai

Francis, Frédéric ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Language :

English

Title :

Effects of host plants reared under elevated CO2 concentrations on the foraging behavior of different stages of corn leaf aphids rhopalosiphum maidis

Publication date :

2019

Journal title :

Insects

eISSN :

2075-4450

Publisher :

Multidisciplinary Digital Publishing Institute (MDPI), Switzerland

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 14 December 2019

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Stocker, T.; Qin, D.; Plattner, G.; Tignor, M.; Allen, S.; Boschung, J.; Nauels, A.; Xia, Y.; Bex, V.; Midgley, P. IPCC, 2013: Climate Change 2013: The physical science basis. contributionof working group i to the fifth assessment report of the intergovernmental panel on climate change. Comput. Geom. 2013, 18, 95–123.
Hartley, S.E.; Jones, C.G.; Couper, G.C.; Jones, T.H. Biosynthesis of plant phenolic compounds in elevated atmospheric CO2. Glob. Chang. Biol. 2000, 6, 497–506. [CrossRef]
Bae, H.; Sicher, R. Changes of soluble protein expression and leaf metabolite levels in Arabidopsis thaliana grown in elevated atmospheric carbon dioxide. Field Crops Res. 2004, 90, 61–73. [CrossRef]
Seneweera, S.P.; Conroy, J.P. Enhanced leaf elongation rates of wheat at elevated CO2: Is it related to carbon and nitrogen dynamics within the growing leaf blade? Environ. Exp. Bot. 2005, 54, 174–181. [CrossRef]
Ainsworth, E.A.; Rogers, A. The response of photosynthesis and stomatal conductance to rising CO2: Mechanisms and environmental interactions. Plant Cell Environ. 2007, 30, 258–270. [CrossRef] [PubMed]
Johns, C.V.; Hughes, L. Interactive effects of elevated CO2 and temperature on the leaf-miner Dialectica scalariella Zeller (Lepidoptera: Gracillariidae) in Paterson’s Curse, Echium plantagineum (Boraginaceae). Glob. Chang. Biol. 2002, 8, 142–152. [CrossRef]
Chen, F.; Ge, F.; Parajulee, M.N. Impact of elevated CO2 on tri-trophic interaction of Gossypium hirsutum, Aphis gossypii, and Leis axyridis. Environ. Entomol. 2005, 34, 37–46. [CrossRef]
Sun, Y.; Guo, H.; Yuan, E.; Ge, F. Elevated CO2 increases R gene-dependent resistance of Medicago truncatula against the pea aphid by up-regulating a heat shock gene. New Phytol. 2018, 217, 1696–1711. [CrossRef]
Zhang, Y.; Dai, Y.; Wan, G.; Liu, B.; Xing, G.; Chen, F. Effects of elevated CO2 on plant chemistry, growth, yield of resistant soybean, and feeding of a target lepidoptera pest, Spodoptera litura (Lepidoptera: Noctuidae). Environ. Entomol. 2018, 47, 848–856.
Drake, B.G.; Azcon-Bieto, J.; Berry, J.; Bunce, J.; Dijkstra, P.; Farrar, J.; Gifford, R.; Gonzalez-meler, M.A.; Koch, G.; Lambers, H. Does elevated atmospheric CO2 concentration inhibit mitochondrial respiration in green plants? Plant Cell Environ. 1999, 22, 649–657. [CrossRef]
Ziska, L.H.; Namuco, O.; Moya, T.; Quilang, J. Growth and yield response of field-grown tropical rice to increasing carbon dioxide and air temperature. Agron. J. 1997, 89, 45–53. [CrossRef]
Kim, K.N.; Cheong, Y.H.; Grant, J.J.; Pandey, G.K.; Luan, S. CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 2003, 15, 411–423. [CrossRef]
Ainsworth, E.A.; Long, S.P. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol. 2005, 165, 351–372. [CrossRef] [PubMed]
Karowe, D.N.; Seimens, D.H.; Mitchell-Olds, T. Species-specific response of glucosinolate content to elevated atmospheric CO2. J. Chem. Ecol. 1997, 23, 2569–2582. [CrossRef]
Coviella, C.E.; Stipanovic, R.D.; Trumble, J.T. Plant allocation to defensive compounds: Interactions between elevated CO2 and nitrogen in transgenic cotton plants. J. Exp. Bot. 2002, 53, 323–331. [CrossRef]
Karowe, D.N.; Grubb, C. Elevated CO2 increases constitutive phenolics and trichomes, but decreases inducibility of phenolics in Brassica rapa (Brassicaceae). J. Chem. Ecol. 2011, 37, 1332–1340. [CrossRef]
Stiling, P.; Cornelissen, T. How does elevated carbon dioxide CO2 affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Glob. Chang. Biol. 2007, 13, 1823–1842. [CrossRef]
Robinson, M.T.; Weeks, A.R.; Hoffmann, A.A. Geographic patterns of clonal diversity in the earth mite species Penthaleus major with particular emphasis on species margins. Evolution 2002, 56, 1160–1167. [CrossRef] [PubMed]
Bidart-Bouzat, M.G.; Imeh-Nathaniel, A. Global change effects on plant chemical defenses against insect herbivores. J Integr. Plant Biol. 2008, 50, 1339–1354. [CrossRef] [PubMed]
Hansson, B.; Wicher, D. Chemical ecology in insects. In Chemosensory Transduction: The Detection of Odors, Tastes, and other Chemostimuli; Zufall, F., Munger, S.D., Eds.; Academic press: London, UK, 2006; pp. 29–45.
Qualley, A.V.; Dudareva, N. Metabolomics of plant volatiles. Methods Mol. Biol. 2009, 553, 329–343.
Knudsen, J.T.; Tollsten, L.; Bergström, L.G. Floral scents-a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 1993, 33, 253–280. [CrossRef]
Holopainen, J.K.; Heijari, J.; Oksanen, E.; Alessio, G.A. Leaf volatile emissions of Betula pendula during autumn coloration and leaf fall. J. Chem. Ecol. 2010, 36, 1068–1075. [CrossRef] [PubMed]
Jiménez-Martínez, E.; Bosque-Pérez, N.; Berger, P.; Zemetra, R. Life history of the bird cherry-oat aphid, Rhopalosiphum padi (Homoptera: Aphididae), on transgenic and untransformed wheat challenged with Barley yellow dwarf virus. J. Econ. Entomol. 2004, 97, 203–212. [CrossRef] [PubMed]
Maffei, M.E. Sites of synthesis, biochemistry and functional role of plant volatiles. S. Afr. J. Bot. 2010, 76, 612–631. [CrossRef]
Boullis, A.; Detrain, C.; Francis, F.; Verheggen, F.J. Will climate change affect insect pheromonal communication? Curr. Opin. Insect Sci. 2016, 17, 87–91. [CrossRef]
Harrewijn, P.; Minks, A.K. Aphids: Their Biology, Natural Enemies, and Control, Vol. A.; Elsevier: Amsterdam, The Netherlands, 1987.
Nault, L. Arthropod transmission of plant viruses: A new synthesis. Ann. Entomol. Soc. Am. 1997, 90, 521–541. [CrossRef]
Braendle, C.; Davis, G.K.; Brisson, J.A.; Stern, D.L. Wing dimorphism in aphids. Heredity 2006, 97, 192–199. [CrossRef] [PubMed]
Pickett, J.; Wadhams, L.; Woodcock, C.; Hardie, J. The chemical ecology of aphids. Annu. Rev. Entomol. 1992, 37, 67–90. [CrossRef]
Pettersson, J.; Ninkovic, V.; Glinwood, R.; Al Abassi, S.; Birkett, M.; Pickett, J.; Wadhams, L. Chemical stimuli supporting foraging behaviour of Coccinella septempunctata L. (Coleoptera: Coccinellidae): Volatiles and allelobiosis. Appl. Entomol. Zool. 2008, 43, 315–321. [CrossRef]
Webster, B. The role of olfaction in aphid host location. Physiol. Entomol. 2012, 37, 10–18. [CrossRef]
Quiroz, A.; Niemeyer, H. Olfactometer-assessed responses of aphid Rhopalosiphum padi to wheat and oat volatiles. J. Chem. Ecol. 1998, 24, 113–124. [CrossRef]
Boullis, A.; Francis, F.; Verheggen, F.J. Climate change and tritrophic interactions: Will modifications to greenhouse gas emissions increase the vulnerability of herbivorous insects to natural enemies? Environ. Entomol. 2015, 44, 277–286. [CrossRef] [PubMed]
Boullis, A.; Fassotte, B.; Sarles, L.; Lognay, G.; Heuskin, S.; Vanderplanck, M.; Bartram, S.; Haubruge, E.; Francis, F.; Verheggen, F.J. Elevated carbon dioxide concentration reduces alarm signaling in aphids. J. Chem. Ecol. 2017, 43, 164–171. [CrossRef] [PubMed]
Boullis, A.; Blanchard, S.; Francis, F.; Verheggen, F. Elevated CO2 concentrations impact the semiochemistry of aphid honeydew without having a cascade effect on an aphid predator. Insects 2018, 9, 47. [CrossRef] [PubMed]
Blanchard, S.; Lognay, G.; Verheggen, F.; Detrain, C. Today and tomorrow: Impact of climate change on aphid biology and potential consequences on their mutualism with ants. Physiol. Entomol. 2019, 44, 77–86. [CrossRef]
El-Ibrashy, M.T.; El-ziadys, S.; Riad, A.A. Laboratory studies on the biology of the corn leaf aphid, Rhopalosiphum maidis (Homoptera: Aphididae). Entomol. Exp. Appl. 1972, 15, 166–174. [CrossRef]
Everly, R.T. Loss in corn yield associated with the abundance of the corn leaf aphid, Rhopalosiphum maidis, in Indiana. J. Econ. Entomol. 1960, 53, 924–932. [CrossRef]
Foott, W.H.; Timmins, P.R. Effects of infestations by the corn leaf aphid, Rhopalosiphum maidis (Homoptera: Aphididae), on field corn in southwestern Ontario. Can. Entomol. 1973, 105, 449–458. [CrossRef]
Bing, J.W.; Guthrie, W.D.; Dicke, F.F.; Obrycki, J.J. Seedling stage feeding by corn leaf aphid (Homoptera: Aphididae): Influence on plant development in maize. J. Econ. Entomol. 1991, 84, 625–632. [CrossRef]
Tottman, D.; Makepeace, R.; Broad, H. An explanation of the decimal code for the growth stages of cereals, with illustrations. Ann. Appl. Biol. 1979, 93, 221–234. [CrossRef]
Powell, G.; Hardie, J.; Pickett, J. Behavioural evidence for detection of the repellent polygodial by aphid antennal tip sensilla. Physiol. Entomol. 1995, 20, 141–146. [CrossRef]
Pettersson, J.; Tjallingii, W.F.; Hardie, J. Host-Plant Selection and Feeding. In Aphids as Crop Pests; van Emden, H.F., Harrington, R., Eds.; CABI: Wallingford, UK, 2007; pp. 87–113.
Park, K.C.; Hardie, J. Electrophysiological characterisation of olfactory sensilla in the black bean aphid, Aphis fabae. J. Insect Physiol. 2004, 50, 647–655. [CrossRef] [PubMed]
Wohlers, P.; Tjallingii, W. Electroantennogram responses of aphids to the alarm pheromone (E)-β-farnesene. Entomol. Exp. Appl. 1983, 33, 79–82. [CrossRef]
Babikova, Z.; Gilbert, L.; Randall, K.C.; Bruce, T.J.; Pickett, J.A.; Johnson, D. Increasing phosphorus supply is not the mechanism by which arbuscular mycorrhiza increase attractiveness of bean (Vicia faba) to aphids. J. Exp. Bot. 2014, 65, 5231–5241. [CrossRef] [PubMed]
Harmel, N.; Almohamad, R.; Fauconnier, M.L.; Du Jardin, P.; Verheggen, F.; Marlier, M.; Haubruge, E.; Francis, F. Role of terpenes from aphid-infested potato on searching and oviposition behavior of Episyrphus balteatus. Insect Sci. 2007, 14, 57–63. [CrossRef]
Halbert, S.; Corsini, D.; Wiebe, M.; Vaughn, S. Plant-derived compounds and extracts with potential as aphid repellents. Ann. Appl. Biol. 2009, 154, 303–307. [CrossRef]
Bukovinszky, T.; Gols, R.; Posthumus, M.; Vet, L.; Van Lenteren, J. Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellen). J. Chem. Ecol. 2005, 31, 461–480. [CrossRef] [PubMed]
Wenda-Piesik, A.; Piesik, D.; Ligor, T.; Buszewski, B. Volatile organic compounds (VOCs) from cereal plants infested with crown rot: Their identity and their capacity for inducing production of VOCs in uninfested plants. Int. J. Pest Manag. 2010, 56, 377–383. [CrossRef]
Piesik, D.; Łyszczarz, A.; Tabaka, P.; Lamparski, R.; Bocianowski, J.; Delaney, K. Volatile induction of three cereals: Influence of mechanical injury and insect herbivory on injured plants and neighbouring uninjured plants. Ann. Appl. Biol. 2010, 157, 425–434. [CrossRef]
Visser, J.; Taanman, J. Odour-conditioned anemotaxis of apterous aphids (Cryptomyzus korschelti) in response to host plants. Physiol. Entomol. 1987, 12, 473–479. [CrossRef]
Nottingham, S.F.; Hardie, J.; Dawson, G.W.; Hick, A.J.; Pickett, J.A.; Wadhams, L.J.; Woodcock, C.M. Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. J. Chem. Ecol. 1991, 17, 1231–1242. [CrossRef] [PubMed]
Storer, J.R.; Young, S.; Hardie, J. Three-dimensional analysis of aphid landing behaviour in the laboratory and field. Physiol. Entomol. 1999, 24, 271–277. [CrossRef]
Vargas, R.R.; Troncoso, A.J.; Tapia, D.H.; Olivares-Donoso, R.; Niemeyer, H.M. Behavioural differences during host selection between alate virginoparae of generalist and tobacco-specialist Myzus persicae. Entomol. Exp. Appl. 2005, 116, 43–53. [CrossRef]
Goldansaz, S.H.; McNeil, J.N. Effect of wind speed on the pheromone-mediated behavior of sexual morphs of the potato aphid, Macrosiphum euphorbiae (Thomas) under laboratory and field conditions. J. Chem. Ecol. 2006, 32, 1719. [CrossRef] [PubMed]
Hardie, J.; Gao, N.; Timar, T.; Sebok, P.; Honda, K.I. Precocene derivatives and aphid morphogenesis. Arch. Insect Biochem. Physiol. 1996, 32, 493–501. [CrossRef]
Kennedy, J. Behavioural post-inhibitory rebound in aphids taking flight after exposure to wind. Anim. Behav. 1990, 39, 1078–1088. [CrossRef]
Sørensen, J.G.; Kristensen, T.N.; Loeschcke, V. The evolutionary and ecological role of heat shock proteins. Ecol. Lett. 2003, 6, 1025–1037. [CrossRef]
Gish, M.; Inbar, M. Host location by apterous aphids after escape dropping from the plant. J. Insect Behav. 2006, 19, 143. [CrossRef]
Zhang, W.; Chang, X.Q.; Hoffmann, A.A.; Zhang, S.; Ma, C.S. Impact of hot events at different developmental stages of a moth: The closer to adult stage, the less reproductive output. Sci. Rep. 2015, 5. [CrossRef]
Webster, B.; Bruce, T.; Pickett, J.; Hardie, J. Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim. Behav. 2010, 79, 451–457. [CrossRef]