Neotrop Entomol DOI 10.1007/s13744-015-0282-9
PEST MANAGEMENT
Associations of Wheat with Pea Can Reduce Aphid Infestations T LOPES1, B BODSON2, F FRANCIS1 1
Dept of Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, Univ of Liège, Gembloux, Belgium Dept of Crop Production, Gembloux Agro-Bio Tech, Univ of Liège, Gembloux, Belgium
2
Keywords Crop associations, hoverflies, ladybirds, Pisum sativum, Triticum aestivum Correspondence T Lopes, Dept of Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, Univ of Liège, Passage des Déportés 2, 5030 Gembloux, Belgium;
[email protected] Edited by Wesley AC Godoy—ESALQ/USP Received 25 July 2014 and accepted 11 February 2015 * Sociedade Entomológica do Brasil 2015
Abstract Increasing plant diversity within crops can be beneficial for pest control. In this field study, the effects of two wheat and pea associations (mixed cropping and strip cropping) on aphid populations were compared with pure stands of both crops by observations on tillers and plants. Pea was more susceptible to infestations than wheat. As expected, the density of aphid colonies was significantly higher in pure stands during the main occurrence periods, compared with associations. Additionally, flying beneficials, such as not only aphidophagous adult ladybirds but also parasitoid, hoverfly and lacewing species that feed on aphids at the larval stage, were monitored using yellow pan traps. At specific times of the sampling season, ladybirds and hoverflies were significantly more abundant in the pure stand of pea and wheat, respectively, compared with associations. Few parasitoids and lacewings were trapped. This study showed that increasing plant diversity within crops by associating cultivated species can reduce aphid infestations, since host plants are more difficult to locate. However, additional methods are needed to attract more efficiently adult beneficials into wheat and pea associations.
Introduction Aphids are important pests of pea and wheat as they weaken plants by sucking their phloem sap, while some species are efficient vectors of phytoviruses (Williams & Dixon 2007). Moreover, aphids have developed resistance to many insecticides (Foster et al 2007), which have negative effects on the environment (Devine & Furlong 2007) and human health (WHO 1990). Therefore, alternative methods are needed to control these pests in an efficient and sustainable manner. Nowadays, these methods focus mainly on cultural practices and plant management systems (Deguine et al 2009). Among these, increasing plant diversity within crops can have several beneficial effects on pest control. In fact, most studies show that the density of pest populations is lower in polycultures compared with monocultures (Andow 1991, Muriel & Velez 2004, Letourneau et al 2011). To explain that, the resource concentration hypothesis states that specialist herbivores are more likely to find their host plants when these are concentrated in dense or pure stands (Root 1973). Their visual (Smith 1969, 1976) and olfactory
(Tahvanainen & Root 1972) location is expected to be easier if compared with diverse environments. Additionally, the enemy hypothesis (Root 1973) states that natural enemies (predators and parasitoids) are more abundant in complex environments, especially because they can benefit from alternative sources of prey, nectar and pollen, as well as shelter and moderate microclimate (reviewed by Landis et al 2000, Wratten et al 2007, Rodriguez-Saona et al 2012). However, if most studies showed that these two hypotheses are complementary, there are also evidences that they might be antagonistic (Andow 1991). In fact, although the effect of diversified cultivation systems seems clear on pests, natural enemies are not always more abundant in those habitats (Risch 1981, Risch et al 1983, Andow 1991, Rämert & Ekbom 1996, Björkman et al 2010). In these cases, it is assumed that the searching efficiency of predators and parasitoids may decrease when increasing the chemical and structural complexity of vegetation (Randlkofer et al 2010). In the recent years, it has been demonstrated that wheatpea mixtures are efficient to produce proteins with low external nitrogen inputs (Lithourgidis et al 2011, Pelzer et al
Lopes et al
2012), which makes this practice interesting for growers. However, their effect on insect populations received less attention. In the present study, we tried to determine the impact of two wheat-pea associations (mixed cropping and strip cropping) on aphid populations and compare it with pure stands of both crops. Based on the above cited theories, aphids were expected to be less abundant into associations, compared with pure stands. Additionally, we tried to determine whether associations were more attractive to flying beneficials, such as aphidophagous adult ladybirds, compared with pure stands. This was also assessed for parasitoid, hoverfly and lacewing species that feed on aphids at the larval stage.
Material and Methods Field layout This field study was conducted in 2012 at the experimental farm of Gembloux Agro-Bio Tech (University of Liege), Namur Province of Belgium (50°33′52″N, 4°42′44″E). Four treatments were tested: (1) pure stand of wheat, (2) pure stand of pea, (3) alternating strips of wheat and pea and (4) wheat mixed with pea with no specific row arrangement. These were established in a 4×4 Latin Square design (four replicates per treatment), with 100-m2 plots (10×10 m) (Fig 1). Strip cropping was composed by three strips of peas and two strips of wheat, each with 2 m wide. Winter pea (variety “James”) and winter wheat (variety “Sahara”) were both sowed on October 24, 2011. Pea was sowed before wheat, with 80 seeds/m2 in the pure stand and pea strips and 35 seeds/m2 in the mixing. As for wheat, the density of 350 seeds/m2 was used in the pure stand, the strips, the mixing and the space between plots (15 m). No insecticide and no herbicide were used in the whole experimental area. Meteorological data were provided by the permanent official station of Ernage-Gembloux, situated near the experimental site. Mean temperatures and rainfalls were lower in May (13.7°C/day and 1.7 mm/day) as compared to June (16.1°C/day and 3 mm/day) and July (16.7°C/day and 3.3 mm/day). Sampling of aphids and beneficials Aphids (winged females, wingless females and nymphs of various instars) were identified and counted directly on pea plants and wheat tillers every 7 days between May 23 and July 11, 2012 (total of eight observations). Depending on the crop, 20 plants or tillers were randomly selected in each pure stand plot. Regarding associations, 20 pea plants and 20 wheat tillers were observed in each plot. Predators (ladybird, hoverfly and lacewing larvae) and
Fig 1 Layout of treatments (mixing, strip cropping, pure stand of wheat and pure stand of pea) in a 4×4 Latin square design.
parasitized aphids were not considered in this study, since a higher number of plants should have been sampled to have exploitable results. After the observations on plants and tillers, not only aphidophagous adult ladybirds but also parasitoid, hoverfly and lacewing species that feed on aphids at the larval stage were collected in yellow pan traps (Flora®, 27-cm diameter and 10-cm depth). These are efficient to assess the diversity and abundance of beneficial species in their adult stage (Colignon et al 2002). Traps were attached to fibreglass sticks, positioned at crop height and filled with water and few drops of detergent (dish-washing liquid) to reduce the surface tension of water. A single trap was placed in the middle of each plot (total of 16 traps), to maximize the distance between them and the edges of plots. Traps were emptied and refilled every 7 days between May 16 and July 11, 2012 (total of eight collections). The trap content was decanted through a 0.5 mm mesh sieve and the insects transferred to plastic vials containing 70% ethanol. All individuals were identified in the laboratory down to the level of species, using specific identification keys. The number of each insect was also recorded. Figures showing the distribution of beneficial species according to aphid density on pea
Effects of Two Wheat-Pea Associations on Aphids and Beneficials Table 1
Diversity and abundance (total numbers) of aphids recorded on plants and tillers in the different treatments through 2012 growing season.
Species
Aphids (Aphididae) Acyrthosiphon pisum (Harris) Metopolophium dirhodum (Walker) Sitobion avenae (Fabricius) Proportion of total number of aphid species (%)
Treatments M
SC
PSW
PSP
%a
310 24 211 9.4
1882 24 82 34.3
0 54 280 5.8
2934 0 0 50.6
88.4 1.8 9.9
Observations
M mixing, SC strip cropping, PSW pure stand of wheat, PSP pure stand of pea. a
Proportional representation of each species.
plants and wheat tillers were made with Mathematica software.
Results Aphids observed on pea plants and wheat tillers
Statistical analysis Data from the observations and insect trapping were first analysed using the general linear model (GLM) procedure, taking into account the position of plots in the Latin square (lines and columns). As this factor had no significant influence on the population densities of aphids and beneficials, two-way analysis of variance (ANOVA) was used with treatments and sampling weeks as factors. Given that significant interactions were systematically found between these factors, the two-way ANOVA was decomposed into eight oneway ANOVA, including treatments factor as fixed effect. This allowed determining the effect of treatments for each sampling week. Data from the observations on pea plants and wheat tillers were treated separately since pea aphids are not found on wheat and vice versa for wheat aphids on pea. Prior to the analyses, a data log10 (n+1) transformation was applied to normalize distributions. All analyses were performed using MINITAB® 16 software.
Fig 2 Seasonal occurrence and abundance (mean number per week±SEM) of aphids observed in plots (*p<0.05; ***p<0.001) (M mixing, SC strip cropping, PSW pure stand of wheat, PSP pure stand of pea).
A total of 5801 aphids were recorded during the growing season (Table 1). Most of these were found on pea plants and belonged to the Acyrthosiphon pisum (Harris) species (88.4%). Their populations increased rapidly in the third week (Fig 2), where a significantly higher number of individuals were observed in the pure stand, compared with the mixing condition (F2,9 =14.69; p<0.001). When pea aphids reached their maximum density (in the fourth week for the pure stand and mixing conditions, and fifth week for strip cropping), a significantly higher number of plants were infested in the pure stand and strip cropping, compared with the mixing (F2,9 =7.58; p<0.01). During these 2 weeks, the number of aphids was also significantly higher in the pure stand and strip cropping conditions, compared with the mixing (fourth week, F2,9 =13.32; p<0.001; fifth week, F2,9 = 16.19; p<0.001). Populations decreased rapidly in the sixth week. Since then, no significant differences were observed between treatments until the end of the seventh week (sixth
Lopes et al
week, F2,9 =2.87; p=0.063; seventh week, F2,9 =0.67; p= 0.516). No aphids were found on pea plants in the last week. Fewer aphids were recorded on wheat tillers (11.6%). These were represented by two species: Sitobion avenae (Fabricius) and Metopolophium dirhodum (Walker), the first one being largely predominant (84.9%). Compared with pea aphids, individuals appeared later in the growing season. In fact, populations began to increase in the fifth week (Fig 2), with no significant differences between treatments (F2,9 = 2.80; p=0.067). When wheat aphids reached their maximum density (in the sixth week for the strip cropping and mixing conditions, and seventh week for the pure stand of wheat), a significantly higher number of tillers were infested in the pure stand, compared with mixing and strip cropping conditions (F2,9 =6.46; p<0.01). However, no significant difference on aphid numbers was observed between treatments in the sixth week (F2,9 =1.50; p=0.230). One week later, the pure stand had significantly higher number of aphids, compared with the strip cropping condition (F2,9 = 9.78; p<0.001). This treatment had significantly less aphids compared with the pure stand and mixing conditions (F2,9 = 4.92; p<0.05) in the last week. Beneficials trapped Beneficials were mainly represented by ladybirds (50.3%), followed by hoverflies (30.2%), braconid wasps (10.7%) and lacewings (8.7%) (Table 2). Most aphidophagous ladybirds were trapped in the first two sampling weeks (Fig 3). This period coincided with the appearance of Acyrthosiphon pisum on pea plants (Fig 2). During that time, significantly more ladybirds were trapped in the pure stand of pea compared with the pure stand of wheat and mixing conditions (first week, F3,12 =3.42; p<0.05; second week, F3,12 =5.11; p<0.01). Significantly more individuals were once again trapped in the pure stand of pea in the fifth week (which coincided with the pea aphid abundance period), compared with the other treatments (F3,12 =4.30; p<0.01). At the species level, the occurrence of the two main ladybird species (Coccinella septempunctata Linnaeus and Propylea quatuordecimpunctata (Linnaeus)) increased with the presence of Acyrthosiphon pisum on pea plants (Fig 4a). Concerning hoverflies (Fig 3), their occurrence in traps coincided with the appearance of Sitobion avenae and M. dirhodum on wheat tillers (Fig 2). In the sixth and seventh sampling weeks, significantly more individuals were trapped in the pure stand of wheat, compared with the pure stand of pea (sixth week, F3,12 =2.72; p<0.05; seventh week, F3,12 = 5.10; p<0.01). In the last week, significantly more hoverflies were trapped in the pure stand of wheat and mixing conditions, compared with the two other treatments (F3,12 =19.77; p<0.001). Similarly to ladybirds, the abundance of the two main species Sphaerophoria scripta (Linnaeus) and Eupeodes
corollae (Fabricius) in traps increased with the occurrence of Sitobion avenae and M. dirhodum on wheat tillers (Fig 4b). Braconid wasps were mainly represented by Aphidius rhopalosiphi De Stefani-Perez (68.8%), while Chrysoperla carnea (Stephens) is almost the only lacewing species (96.2%). No statistical analyses were made for these two families, since few individuals were trapped.
Discussion Results from the observations on plants and tillers support the resource concentration hypothesis. As expected, aphid populations were significantly denser in pure stands during the abundance periods as compared with associations. The mixing was particularly beneficial for the pea, since significantly fewer plants were infested during the pea aphid population peak when compared with the pure stand and strip cropping conditions. The lower density of pea plants in mixing plots may have favoured their physical obstruction (Perrin & Phillips 1978) and visual camouflage (Smith 1969, 1976) by wheat. The latter may also have contributed to mask pea plant odours (Tahvanainen & Root 1972). These factors could explain why fewer pea aphids found their host plants in the mixing condition, compared to the other treatments. Our results differ from those of Seidenglanz et al (2011), who found similar occurrences of Acyrthosiphon pisum in a pure stand of pea and in mixtures with wheat or barley. However, the proportions of pea plants were higher in their mixtures, which may have reduced the abovementioned beneficial effects. Concerning wheat, strip cropping was the most efficient to reduce aphid populations. In fact, fewer individuals found their host plants in this treatment during the infestation peak, compared with the pure stand and mixing. Similar beneficial effects were obtained in other field studies, where wheat-oilseed rape (Wanlei et al 2009) and wheat-mung bean (Xie et al 2012) intercropping reduced the incidence of Sitobion avenae. Xie et al (2012) also found in Y-tube olfactometer bioassays that alate aphids prefer host plant odours than odour blends of host plants intercropped with another species, which could explain our results. In fact, it is unlikely that host finding was disrupted by physical obstruction and visual camouflage of wheat by pea plants, since both crops were arranged in distinct strips. Regarding beneficials, their abundance in traps was similar between treatments if we consider the entire sampling season. However, significantly more ladybirds were trapped in the pure stand of pea in the first, second and fifth weeks if compared with the other treatments. The same happened with hoverflies in the pure stand of wheat in the last three sampling weeks. These results are somehow contrary to the enemy hypothesis, although it would have been interesting
Effects of Two Wheat-Pea Associations on Aphids and Beneficials Table 2 Code
Diversity and abundance (total numbers) of beneficials trapped in the different treatments through 2012 growing season. Species
Ladybirds (Coccinellidae) 1 Adalia decempunctata (Linnaeus) 2 Coccinella septempunctata Linnaeus 3 Harmonia axyridis (Pallas) 4 Propylea quatuordecimpunctata (Linnaeus) Hoverflies (Syrphidae) 5 Episyrphus balteatus (De Geer) 6 Eupeodes corollae (Fabricius) 7 Melanostoma mellinum (Linnaeus) 8 Melanostoma scalare (Fabricius) 9 Platycheirus manicatus (Meigen) 10 Platycheirus peltatus (Meigen) 11 Sphaerophoria scripta (Linnaeus) 12 Syrphus ribesii (Linnaeus) 13 Syrphus vitripennis Meigen Lacewings (Chrysopidae) 14 Chrysopa phyllochroma Wesmael 15 Chrysoperla carnea (Stephens) Braconid wasps (Braconidae) 16 Aphidius ervi Haliday 17 Aphidius matricariae Haliday 18 Aphidius picipes (Nees) 19 Aphidius rhopalosiphi De Stefani-Perez 20 Diaeretiella rapae (M’Intosh) 21 Praon volucre (Haliday) Total numbers of beneficial species Proportion of total numbers of beneficial species (%)
Treatments %a
M
SC
PSW
PSP
50.3%b 0
0
1
1
9
18
4
40
47.3
3 6
11 13
3 7
13 21
20.0 31.3
30.2%b 2 4 4
2 1 0
6 9 3
4 3 0
15.6 18.9 7.8
1
0
5
0
6.7
0
1
0
0
1.1
1 15
0 6
1 17
0 2
2.2 44.4
1 0 8.7%b 0
1 1
0 0
0 0
2.2 1.1
0
0
1
3.8
8 10.7%b 0 1 1 4
5
4
8
96.2
1 0 0 9
0 0 0 5
1 0 1 4
6.3 3.1 6.3 68.8
1 1 62 20.8
0 1 70 23.5
0 1 66 22.1
0 1 100 33.6
3.1 12.5
1.3
A code is given for each species to indicate their identity in Fig 4. M mixing, SC strip cropping, PSW pure stand of wheat, PSP pure stand of pea. a
Proportional representation of each species by family.
b
Relative occurrence of each family in the beneficial population.
to observe aphid natural enemies on plants to confirm such statement. Moreover, due to the small size of plots and short distance between them, adult beneficials could easily move from a plot to another, which makes the treatments effect difficult to analyse. In the case of ladybirds, their abundance period coincided with the presence of Acyrthosiphon pisum on pea plants. At that time, this species was the only food source, and no alternative preys were available on wheat tillers in the mixing and strip cropping conditions. The same
occurred during the hoverflies abundance period, since wheat aphids were the main food source and few pea aphids were present in both associations. Moreover, flying beneficials use herbivore-induced plant volatiles (HIPVs) to locate habitats where aphids might be present (reviewed by Hatano et al 2008). These chemical cues are emitted from infested plants to indicate the availability of prey for natural enemies and attract them to promote pest control (Dicke et al 1990, Turlings et al 1990, Han & Chen 2002). For example, Zhu &
Lopes et al
Fig 3 Seasonal occurrence and abundance (mean number per week±SEM) of some beneficials collected in the traps (*p<0.05; **p<0.01; ***p<0.001) (M mixing, SC strip cropping, PSW pure stand of wheat, PSP pure stand of pea).
Fig 4 Distribution of beneficial species according to aphid density on pea plants (a) and wheat tillers (b). In the top, black bars represent the abundance of ladybirds, hoverflies and lacewings, while white bars represent the abundance of parasitoids. The widths of bars are magnified relative to those of aphids according to a factor (×22 for a and ×3 for b). The species identities (numbers) are given in Table 2. In the bottom, black bars represent aphid abundance in the different treatments: M mixing, SC strip cropping, PSW pure stand of wheat, PSP pure stand of pea. Beneficial species and aphids are linked by triangular wedges. Their relative widths represent the abundance of beneficials according to aphid density in each treatment.
Effects of Two Wheat-Pea Associations on Aphids and Beneficials
Park (2005) showed that methyl salicylate emitted from infested soybean plants was attractive to Coccinella septempunctata. Other substances, such as aphid honeydew and (E)-β-farnesene, which is the main component of the aphid alarm pheromone (Francis et al 2005), are used by beneficials as short-range chemical cues to search for aphids on their host plants (reviewed by Hatano et al 2008). It is namely the case for the hoverfly species Episyrphus balteatus (De Geer), which oviposition is stimulated by the presence of honeydew (Budenberg & Powell 1992) and (E)-β-farnesene (Verheggen et al 2008). The latter substance also proved to be attractive to other aphid natural enemies, such as the ladybirds Coccinella septempunctata (Al Abassi et al 2000), Harmonia axyridis (Harmel et al 2007) and Adalia bipunctata (Linnaeus) (Francis et al 2004), and the parasitoids Aphidius uzbekistanicus Luzhetzki and Praon volucre (Micha & Wyss 1996). In general, it is possible that the concentrations of volatile compounds were higher in pure stand plots, since aphid populations were denser than in fields with associations. This factor could also explain our results. In conclusion, despite the fact that this study was conducted over one growing season, results clearly demonstrate that wheat-pea associations can reduce aphid infestations. The mixing condition was particularly beneficial for the pea aphid control. Even though wheat was less infested than pea, strip cropping also proved to be interesting. Therefore, these practices could be effective in keeping aphid populations below the economic threshold in years of high pest pressure, avoiding insecticide applications. Regarding adult beneficials, they did not benefit from wheat-pea associations. Therefore, additional methods are needed to attract them more efficiently. In this area, the use of semiochemicals, such as HIPVs, combined with crop associations seems promising (Wang et al 2011). Acknowledgments The authors thank the technicians from the Crop Management Unit of Gembloux Agro-Bio-Tech (University of Liège, Belgium) for the installation and management of experimental fields, Dr. Y. Brostaux for help with statistical analyses, Axel Vandereycken for help with graphics and the Belgian National Fund for Scientific Research (FNRS) for providing PhD fellowship.
References Al Abassi S, Birkett MA, Pettersson J, Pickett JA, Wadhams LJ, Woodcock CM (2000) Response of the seven-spot ladybird to an aphid alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells. J Chem Ecol 26:1765–1771 Andow DA (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36:561–586 Björkman M, Hambäck PA, Hopkins RJ, Rämert B (2010) Evaluating the enemies hypothesis in a clover-cabbage intercrop: effects of generalist and specialist natural enemies on the turnip root fly (Delia floralis). Agric For Entomol 12:123–132
Budenberg WJ, Powell W (1992) The role of honeydew as an ovipositional stimulant for two species of syrphids. Entomol Exp Appl 64:57–61 Colignon P, Gaspar C, Haubruge E, Francis F (2002) Impact of close habitat on the entomological diversity and abundance in carrot open fields. Meded Fac Landbouwkd Toegep Biol Wet 67(3):481–486 Deguine JP, Ferron P, Russell D (2009) Crop protection: from agrochemistry to agroecology. Science Publisher, Enfield, p 216 Devine GJ, Furlong MJ (2007) Insecticide use: contexts and ecological consequences. Agric Hum Values 24:281–306 Dicke M, Sabelis MW, Takabayashi J, Bruin J, Posthumus MA (1990) Plant strategies of manipulating predator–prey interactions through allelochemicals: prospects for application in pest control. J Chem Ecol 16:3091–3117 Foster SP, Devine G, Devonshire AL (2007) Insecticide Resistance. In: van Emden HF, Harrington R (eds) Aphids as crop pests. CAB International, Wallingford, pp 261–285 Francis F, Lognay G, Haubruge E (2004) Olfactory responses to aphid and host plant volatile releases: (E)-beta-farnesene an effective kairomone for the predator Adalia bipunctata. J Chem Ecol 30:741–755 Francis F, Vandermoten S, Verheggen F, Lognay G, Haubruge E (2005) Is the (E)-beta-farnesene only volatile terpenoid in aphids? J Appl Entomol 129:6–11 Han BY, Chen ZM (2002) Behavioral and electrophysiological responses of natural enemies to synomones from tea shoots and kairomones from tea aphids, Toxoptera aurantii. J Chem Ecol 28:2203–2219 Harmel N, Almohamad R, Fauconnier ML, 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 Sci 14:57–63 Hatano E, Kunert G, Michaud JP, Weisser WW (2008) Chemical cues mediating aphid location by natural enemies. Eur J Entomol 105:797–806 Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201 Letourneau DK, Armbrecht I, Rivera BS, Lerma JM, Carmona EJ, Daza MC, Escobar S, Galindo V, Gutiérrez C, López SD, Mejía JL, Rangel AMA, Rangel JH, Rivera L, Saavedra CA, Torres AM, Trujillo AR (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21 Lithourgidis AS, Vlachostergios DN, Dordas CA, Damalas CA (2011) Dry matter yield, nitrogen content, and competition in pea–cereal intercropping systems. Eur J Agron 34:287–294 Micha SG, Wyss U (1996) Aphid alarm pheromone (E)-β-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiinae). Chemoecology 7:132–139 Muriel SB, Velez LD (2004) Evaluando la diversidad de plantas en los agroecosistemas como estrategia para el control de plagas. Manejo Integrado de Plagas y Agroecologia 71:13–20 Pelzer E, Bazot M, Makowski D, Corre-Hellou G, Naudin C, Al Rifaï M, Baranger E, Bedoussac L, Biarnès V, Boucheny P, Carrouée B, Dorvillez D, Foissy D, Gaillard B, Guichard L, Mansard MC, Omon B, Prieur L, Yvergniaux M, Justes E, Jeuffroy MH (2012) Pea–wheat intercrops in low-input conditions combine high economic performances and low environmental impacts. Eur J Agron 40:39–53 Perrin RM, Phillips ML (1978) Some effects of mixed cropping on the population dynamics of insect pests. Entomol Exp Appl 24:385–393 Rämert B, Ekbom B (1996) Intercropping as a pest management strategy against the carrot rust fly (Diptera: Psilidae): a test of enemies and resource concentration hypothesis. Environ Entomol 25:1092–1100 Randlkofer B, Obermaier E, Hilker M, Meiners T (2010) Vegetation complexity—the influence of plant species diversity and plant structures on plant chemical complexity and arthropods. Basic Appl Ecol 11:383–395 Risch SJ (1981) Insect herbivory abundance in tropical monocultures and polycultures: an experimental test of two hypotheses. Ecology 62: 1325–1340
Lopes et al Risch S, Andow D, Altieri A (1983) Agroecosystem diversity and pest control: data, tentative conclusions, and new research directions. Environ Entomol 12:625–629 Rodriguez-Saona C, Blaauw BR, Isaacs R (2012) Manipulation of natural enemies in agroecosystems: habitat and semiochemicals for sustainable insect pest control. In: Larramendy ML, Soloneski S (eds) Integrated pest management and pest control—current and future tactics. InTech, Rijeka, pp 89–126 Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124 Seidenglanz M, Huňady I, Poslušna J, Loes AK (2011) Influence of intercropping with spring cereals on the occurrence of pea aphids (Acyrthosiphon pisum Harris, 1776) and their natural enemies in field pea (Pisum sativum L.). Plant Prot Sci 47:25–36 Smith JG (1969) Some effects of crop background on the populations of aphids and their natural enemies on Brussels sprouts. Ann Appl Biol 63:326–330 Smith JG (1976) Influence of crop backgrounds on aphids and other phytophagous insects on Brussels sprouts. Ann Appl Biol 83:1–13 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 Turlings TCJ, Tumlinson JH, Eller FJ, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253
Verheggen FJ, Arnaud L, Bartram S, Gohy M, Haubruge E (2008) Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly. J Chem Ecol 34(3):301–307 Wang G, Cui LL, Dong J, Francis F, Liu Y, Tooker J (2011) Combining intercropping with semiochemical releases: optimization of alternative control of Sitobion avenae in wheat crops in China. Entomol Exp Appl 140:189–195 Wanlei W, Yong L, Julian C, Xianglong J, Haibo Z, Guang W (2009) Impact of intercropping aphid-resistant wheat cultivars with oilseed rape on wheat aphid (Sitobion avenae) and its natural enemies. Acta Ecol Sin 29:186–191 WHO (World Health Organization) (1990) Public health impact of pesticides used in agriculture. World Health Organization, Geneva, p 128 Williams IS, Dixon AFG (2007) Life cycles and polymorphism. In: van Emden HF, Harrington R (eds) Aphids as crop pests. CAB International, Wallingford, pp 69–85 Wratten SD, Gurr GM, Tylianakis JM, Robinson KA (2007) Cultural control. In: van Emden HF, Harrington R (eds) Aphids as crop pests. CAB International, Wallingford, pp 423–445 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. J Econ Entomol 105(3):854–859 Zhu J, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31:1733–1746
