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Wheat-pea intercropping for aphid control: from laboratory tritrophic approach to field application

Research Paper | September 1, 2016

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Thomas Lopes, Haibo Zhou, Julian Chen, Yong Liu, Bernard Bodson, Frédéric Francis

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Int. J. Agron. Agri. Res.9( 3), 20-33, September 2016


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Intercropping is an interesting practice to promote the sustainable control of insect pests such as aphids. In particular, volatile organic compounds emitted by aphid-infested intercropped plants may deter other aphid species from their host plants, while attracting natural enemies. In this study, olfactometer and net-cage behavioural assays were first conducted to determine the effect of wheat-pea mixtures combined with aphid infestations on odour preferences of the wheat aphid Sitobion avenae and two associated predator species, the ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus. Healthy wheat plants were preferred by S. avenae, while wheat-pea mixtures combined with aphid infestations were significantly less attractive. H. axyridis preferred odours from healthy wheat plants mixed with aphid-infested pea plants. As for E. balteatus, their searching and oviposition behaviours were stimulated by the different wheat/pea combinations associated with aphid infestations. A field trial was also carried to compare the effect of mix and strip cropping wheat with pea on aphids and their natural enemies with both monocultures. Wheat and pea aphid populations were significantly reduced by both types of intercropping when compared to monocultures. Moreover, higher abundances of hoverflies, lacewings and ladybirds were found in wheat mixed with pea field, followed by strip cropping and monocultures. These findings show that wheat-pea intercropping can be efficient to reduce aphid populations, namely by promoting their biological control.


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Wheat-pea intercropping for aphid control: from laboratory tritrophic approach to field application

Alhmedi A, Haubruge E, Francis F. 2010. Intraguild interactions and aphid predators: biological efficiency of Harmonia axyridis and Episyrphus balteatus. Journal of Applied Entomology 134, 34-44.

Almohamad R, Verheggen F, Francis F, Haubruge E. 2008. Impact of aphid colony size and associated induced plant volatiles on searching and oviposition behaviour of a predatory hoverfly. Belgian Journal of Entomology 10, 17-26.

Andow DA. 1991. Vegetational diversity and arthropod population response. Annual Review of Entomology 36, 561-586.

Andrews DJ, Kassam AH. 1976. The importance of multiple cropping in increasing world food supplies. In: Papendick RI, Sanchez PA, Triplett GB, Ed. Multiple Cropping. WI, USA: Madison, 1-10.

Anil L, Park J, Phipps RH, Miller FA. 1998. Temperate intercropping of cereals for forage. Grass and Forage Science 53, 301-317.

Barbosa PA, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z. 2009. Associational resistance and associational susceptibility: having right or wrong neighbors. Annual Review of Ecology, Evolution, and Systematics 40, 1-20.

Campbell CAM, Pettersson J, Pickett JA, Wadhams LJ, Woodcock CM. 1993. Spring migration of damson-hop aphid, Phorodon humuli (Homoptera, Aphididae), and summer host plant-derived semiochemicals released on feeding. Journal of Chemical Ecology 19(7), 1569-1576.

De Moraes CM, Mescher MC, Tumlinson JH. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410, 577-580.

Devine GJ, Furlong MJ. 2007. Insecticide use: contexts and ecological consequences. Agriculture and Human Values 24, 281-306.

Dicke M, Sabelis MW, Takabayashi J, Bruin J, Posthumus MA. 1990. Plant strategies of manipulating predatorprey interactions through allelochemicals: Prospects for application in pest control. Journal of Chemical Ecology 16, 3091-3118.

Döring TF. 2014. How aphids find their host plants, and how they don’t. Annals of Applied Biology 165, 3-26.

Glinwood R, Ahmed E, Qvarfordt E, Ninkovic V, Pettersson J. 2009. Airborne interactions between undamaged plants of different cultivars affect insect herbivores and natural enemies. Arthropod-Plant Interactions 3, 215-224.

Gray SM, Chapin JW, Smith DM, Banerjee N, Thomas JS. 1998. Barley yellow dwarf luteoviruses and their predominant aphid vectors in winter wheat grown in south Carolina. Plant Disease 82(12), 1328-1333.

Gurr GM, Wratten SD, Luna JM. 2003. Multi-function agricultural biodiversity: pest management and other benefits. Basic and Applied Ecology 4, 107-116.

Gurr GM, Wratten SD, Altieri A. 2004. Ecological engineering for pest management, advances in habitat manipulation for arthropods. Wallingford, UK: CAB International.

Han B-y, Chen Z-m. 2002. Composition of the volatiles from intact and tea aphid-damaged tea shoots and their allurement to several natural enemies of the tea aphid. Journal of Applied Entomology 126, 497-500.

Harmel N, Almohamad R, Fauconnier M-L, Du Jardin P, Verheggen F, Marlier M, Haubruge E, Francis F. 2007. Role of terpenes from aphid-infested potato on searching and oviposition behavior of Episyrphus balteatus. Insect Science 14, 57-63.

Hassanali A, Herren H, Khan ZR, Pickett JA, Woodcock CM. 2008. Integrated pest management: the push-pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philosophical Transactions of the Royal Society B 363, 611-621.

Hatano E, Kunert G, Michaud JP, Weisser WW. 2008. Chemical cues mediating aphid location by natural enemies. European Journal of Entomology 105, 797-806.

Konar A, Singh NJ, Paul R. 2010. Influence of intercropping on population dynamics of major insect pests and vectors of potato. Journal of Entomological Research 34, 151-154.

Landis DA, Marino PC. 1999. Landscape structure and extra-field processes: impact on management of pests and beneficials. In: Ruberson J, Ed. Handbook of Pest Management. New York, USA: Marcel Dekker, 79-104.

Landis DA, Wratten SD, Gurr GM. 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology 45, 175-201.

Laubertie EA, Wratten SD, Sedcole JR. 2006. The role of odour and visual cues in the pan-trap catching of hoverflies (Diptera: Syrphidae). Annals of Applied Biology 148, 173-178.

Lopes T, Bodson B, Francis F. 2015. Associations of wheat with pea can reduce aphid infestations. Neotropical Entomology 44, 286-293.

Ndzana RA, Magro A, Bedoussac L, Justes E, Journet EP, Hemptinne JL. 2014. Is there an associational resistance of winter pea–durum wheat intercrops towards Acyrthosiphon pisum Harris? Journal of Applied Entomology 138, 577-585.

Ninkovic V, Al Abassi S, Pettersson J. 2001. The Influence of Aphid-Induced Plant Volatiles on Ladybird Beetle Searching Behavior. Biological Control 21, 191-195.

Ninkovic V, Pettersson J. 2003. Searching behaviour of the sevenspotted ladybird, Coccinella septempunctata – effects of plant-plant odour interaction. Oikos 100, 65-70.

Ofori F, Stern WR. 1987. Cereal-legume intercropping systems. Advances in Agronomy 41, 41-90.

Oluwafemi S, Bruce T, Pickett J, Ton J, Birkett M. 2011. Behavioral Responses of the Leafhopper, Cicadulina storeyi China, a Major Vector of Maize Streak Virus, to Volatile Cues from Intact and Leafhopper-Damaged Maize. Journal of Chemical Ecology 37, 40-48.

Perrin RM, Phillips ML. 1978. Some effects of mixed cropping on the population dynamics of insect pests. Entomologia Experimentalis et Applicata 24, 385-393.

Pettersson J, Pickett JA, Pye BJ, Quiroz A, Smart LE, Wadhams LJ, Woodcock CM. 1994. Winter host component reduces colonization by bird-cherry-oat aphid, Rhopalosiphum padi (L.) (Homoptera, Aphididae), and other aphids in cereal fields. Journal of Chemical Ecology 20(10), 2565-2575.

Pettersson J, Ninkovic V, Glinwood R, Birkett MA, Pickett JA. 2005. Foraging in a complex environment – semiochemicals support searching behaviour of the seven spot ladybird. European Journal of Entomology 102, 365-370.

Poveda K, Gómez MI, Martínez E. 2008. Diversification practices: their effect on pest regulation and production. Revista Colombiana de Entomología 34, 131-144.

Rodriguez-Saona C, Kaplan I, Braasch J, Chinnasamy D, Williams L. 2011. Field responses of predaceous arthropods to methyl salicylate: A meta-analysis and case study in cranberries. Biological Control 59(2), 294-303.

Root R. 1973. Organization of a Plant-Arthropod Association in Simple and Diverse Habitats: The Fauna of Collards (Brassica Oleracea). Ecological Monographs 43, 95-124.

Roy HE, Brown PMJ, Comont RF, Poland RL, Sloggett JJ. 2013. Ladybirds (Naturalists’ Handbooks 10). Exeter, UK: Pelagic Publishing.

San Martin G. 2004. Clé de détermination des Chrysopidae de Belgique. Wavre, Belgium : Jeune et Nature asbl.

Sema Gencer N, Alper Kumral N, Sivritepe H, Seidi M, Susurluk H, Senturk B. 2009. Olfactory response of the ladybird beetle Stethorus gilvifrons to two preys and herbivore-induced plant volatiles. Phytoparasitica 37, 217-224.

Smith HA, McSorley R. 2000. Intercropping and Pest Management: A Review of Major Concepts. American Entomologist 46, 154-161.

Smith JG. 1969. Some effects of crop background on the populations of aphids and their natural enemies on Brussels sprouts. Annals of Applied Biology 63, 326-330.

Smith JG. 1976. Influence of crop backgrounds on aphids and other phytophagous insects on Brussels sprouts. Annals of Applied Biology 83, 1-13.

Suresh R, Sunder S, Pramod M. 2010. Effect of intercrops on the temporal parasitization of Helicoverpa armigera (Hub.) by larval parasitoid, Campoletis chlorideae Uchida in tomato. Environment and Ecology 28, 2485-2489.

Tahvanainen JO, Root RB. 1972. The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta crucifera (Coleoptera: Chrysomelidae). Oecologia 10, 321-346.

Taylor LR. 1981. Euraphid 1980: aphid forecasting and pathogens & a hanbook for aphid identification. Harpenden, UK: Rothamsted Experimental Station.

Vaiyapuri K, Amanullah MM, Rajendran K, Sathyamoorthi K. 2010. Intercropping Unconventional Green Manures in Cotton: An Organic Approach for Multiple Benefits: A Review. Asian Journal of Plant Sciences 9, 223-226.

Vandereycken A, Durieux D, Joie E, Francis F, Haubruge E, Verheggen F. 2015. Aphid species and associated natural enemies in field crops: what about the invasive ladybird Harmonia axyridis (Coleoptera: Coccinellidae)? Faunistic Entomology 68, 3-15.

van Veen MP. 2010. Hoverflies of Northwest Europe: Identification Keys to the Syrphidae. Zeist, Netherlands: KNNV Publishing.

Verheggen F, Arnaud L, Bartram S, Gohy M, Haubruge E. 2008. Aphid and Plant Volatiles Induce Oviposition in an Aphidophagous Hoverfly. Journal of Chemical Ecology 34, 301-307.

Vet LEM, Lenteren JCV, Heymans M, Meelis E. 1983. An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiological Entomology 8, 97-106.

WHO (World Health Organization). 1990. Public health impact of pesticides used in agriculture. Geneva, Switzerland: World Health Organization.

Xie HC, Chen JL, Cheng DF, Zhou HB, Sun JR, Liu Y, Francis F. 2012. Impact of wheat-mung bean intercropping on English grain aphid (Hemiptera: Aphididae) populations and its natural enemy. Journal of Economic Entomology 105(3), 854-859.

Zhou HB, Chen L, Chen JL, Liu Y, Cheng DF, Sun JR. 2009a. The effect of intercropping between wheat and pea on spatial distribution of Sitobion avenae based on GIS. Scientia Agricultura Sinica 42(11), 3904-3913.

Zhou HB, Chen JL, Cheng DF, Liu Y, Sun JR. 2009b. Effects of wheat-pea intercropping on Sitobion avenae and the functional groups of its main natural enemies. Acta Entomologica Sinica 52, 775-782.

Zhu J, Park KC. 2005. Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. Journal of Chemical Ecology 31(8), 1733-1746.