REVIEW ARTICLE Functional characteristics of ...

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International Journal of Pest Management Vol. 00, No. 0, Month 2012, 1–9

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REVIEW ARTICLE Functional characteristics of secondary plants for increased pest management

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Pia Parolin*, Ce´cile Bresch, Christine Poncet and Nicolas Desneux 10

French National Institute for Agricultural Research (INRA), ISA– TEAPEA 1355, BP 167, 06903 Sophia Antipolis, France (Received 10 April 2012; final version received 9 July 2012)

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Secondary plants may be added to a cropping system for the purpose of improving pest control. In a recent article (Parolin P, Bresch C, Brun R, Bout A, Boll R, Desneux N, Poncet C (2012) Secondary plants used in biological AQ1 control: a review. International Journal of Pest Management 00, 000–00) we defined different categories of secondary plants used to enhance biological control: companion, repellent, barrier, indicator, trap, insectary, and banker plants are intentionally added to agricultural systems in order to improve pest management through either top-down or bottom-up processes. In the present paper, we focus on the functional characteristics of secondary plants and on the mechanisms which contribute to reducing the presence of pests. If we understand and integrate the effects that such plants have on pests and beneficial arthropods, together with the multitrophic interactions in which these organisms are involved, the application of pesticides in crop systems can be reduced and enhanced productivity in agroecosystems achieved. Here, we identify the main characteristics of, and the prerequisites for, plants which can enhance crop protection in agro-ecosystems. Keywords: banker plant; barrier plant; companion plant; indicator plant; insectary plant; integrated pest management; plant morphology; repellent plant; trap plant

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Introduction

Sustainable crop protection strategies which reduce the use of pesticides are urgently needed for the demands of modern agriculture. The extensive use of chemical pesticides for pest control has multiple negative effects on human health and non-target organisms (Weisenburger 1993; Desneux et al. 2007; Biondi et al. 2012). In addition, the need for increased crop production, problems related to large monocultured areas, pest resistance and the continuous arrival of new invasive pests (Landis et al. 2000; Desneux et al. 2010; Suckling and Brockerhoff 2010; Ragsdale et al. 2011) hamper the implementation of sustainable and environmentally-friendly pest control strategies. Integrated pest management (IPM) is a promising alternative, particularly as it ideally involves an allencompassing approach that relies on a combination of tactics and tools and takes into account the environmental and socio-economic viability of those tactics. Here, we focus on the effects of secondary plants on arthropod pests and their predators, the latter hereafter named ‘‘beneficials’’. Factors related to the requirements of these beneficials, such as diet breadth, dispersal abilities and intrinsic rate of increase, differ largely among species (Frank 2010). Thus there are different requirements in the morphological, physiological or phenological characteristics of their host plants.

Adding non-crop plants to a crop system in order to enhance biological control was proposed as early as 1901 (Clark 1901) and is summarized by Jervis et al. (1993). Secondary plants, which are often non-crop plants, are added to a given crop area and influence multitrophic interactions by providing additional shelter or food to beneficial organisms. Doing so can have indirect positive effects on the crop plants through positive effects on beneficials (Tscharntke and Hawkins 2002; Wa¨ckers et al. 2005; Lundgren et al. 2009). Secondary plants can also have direct bottom-up effects on crop plants, for example, either a positive influence by fixing nitrogen or a negative one by competition. Several secondary plant species can be used in IPM in greenhouses and open fields (Enkegaard 2008). The most frequently employed categories – companion, repellent, barrier, indicator, trap, insectary, and banker plants – have been recently reviewed and defined (Parolin et al. in press). However, the criteria for their selection as efficient enhancers of biological control are not always clear. Therefore, a main issue is to identify the particular plant characteristics that influence arthropods – pests and as well as beneficial organisms – crops and their interactions (Cortesero et al. 2000; Romero and Benson 2005; Frank 2010; Jindal et al. 2012; Parolin et al 2012a). This knowledge would aid the selection of suitable plant species which enhance

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55 115 *Corresponding author. Email: [email protected] ISSN 0967-0874 print/ISSN 1366-5863 online Ó 2012 Taylor & Francis http://dx.doi.org/10.1080/09670874.2012.734869 http://www.tandfonline.com

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biological control. To date, the reasons why certain plant species have been chosen for use in biological control have not been summarized, and the relative effectiveness of such plants has not been reviewed. Here, we attempt to remedy this situation. We describe those plant traits which may help to enhance pest control, be it by suppression, that is, by inhibiting pests, or by providing shelter and/or food to beneficial organisms (Wa¨ckers et al. 2005). By highlighting the most important characteristics which enable plants to act as efficient biocontrol tools, our aim is to facilitate the selection of more plant species from among endemic floras. By doing so, the introduction of

potentially invasive plant species would be precluded 175 to some extent. 2.

Potential interactions influenced by secondary plants

Secondary plants may have effects on pests, beneficial 180 organisms and crop plants. The interactions between them are multifaceted. In the specific case of pest suppression and regulation and its influence on crop productivity, we have identified some principal processes (Figure 1). Without a secondary plant, in the 185 simplest interaction, pests have direct negative effects on the crops, beneficial organisms have direct negative

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Figure 1. Main potential interactions between secondary plants, pests, beneficials and crop plants. The processes of multitrophic interaction are non-exclusive. Solid lines indicate direct interactions, and dashed lines indicate indirect interactions (mediated by another component of the system). Lines with arrows indicate a positive effect in the direction of the arrows, and lines with circles indicate negative effects in the direction of the circles. Processes described were based on the available literature sources. Other 225 processes not well identified in the literature also may occur. Process A: indirect positive effect of the secondary plant on the crop through a direct positive effect on the beneficial organisms, which have direct negative effects on the pests and indirect positive effects on the crop plants. The secondary plant has indirect negative effects on the pests. Process B: pests have a direct negative effect on the secondary plant by attacking them and this way are less concentrated on the crop plants, leading to an indirect positive effect of the secondary plant on the crop plant. Process C: direct negative effects of the secondary plant on the crop via competition, or direct positive effects of the secondary plant on the pest, which leads to indirect negative effects on the crop, that 230 is, undesired interactions. Process D: direct positive effects of the secondary plant on the crop via influences on the nutritional status of the plant, and thus indirect negative effects of the secondary plant on the pest.

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effects on the pests, and thus indirect positive effects on the crop. When a secondary plant is present (Figure 1, process A), it has an indirect positive effect on the crop, that is, through positive effects on density, prevalence and/or activity of the beneficial organisms – for example, a banker plant enhances the establishment of a given predator species. The beneficials, then, have a direct negative effect on the pests which in turn indirectly benefits the crop plants so that they are less affected by pests and thus more productive. In process B (Figure 1), pests attack the secondary plant and are thus less concentrated on the crop plants. This may lead to a direct negative impact of the pests on the secondary plant and to an indirect beneficial influence of the secondary plant on the crop plant, as is the case in trap, indicator and barrier plants. Other processes involving secondary plants can either have negative effects on crop plants or direct positive effects on the crop plants without beneficials mediating in the interactions. Despite predominantly positive functions, secondary plants added to crops may also have undesired indirect negative effects on the crop plants. For example, if secondary plants enhance the pest reproduction, this may lead to decreased crop productivity (Figure 1, process C). Moreover, there may be negative effects of the secondary plants on the crop plants due to competition (e.g. for light, water or nutrients) as is the case when some insectary plants are present (Cranshaw 1996; Fiedler et al. 2007). This is also true for flowering plants which increase resources for pollinators, mainly bees, in agricultural landscapes (Decourtye et al. 2010) as they might also benefit pests and thus compromise the sustainability of IPM programmes. A further important indirect negative effect of secondary plants added to a crop is that it could be more difficult for some natural enemies to find their host in a more diverse and complex crop system (Andow and Prokrym 1990; Coll and Bottrell 1996). In bottom-up processes (Figure 1, process D), secondary plants, namely companion plants (Kuepper and Dodson 2001; Finch et al. 2003), may increase crop plant productivity – for example, by fixing nitrogen – and influence pest control since fertilization has an effect on pest and predator presence (Gruner et al. 2008). The implications for multitrophic interactions described here are non-exclusive, and these processes can occur simultaneously, depending on the characteristics of the plants, pests and beneficial organisms. Other interactions may exist which have not been documented in Figure 1.

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3. Plant types added to crops Several categories of secondary plants added to crops have been reported, most of them based on

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entomological studies. Among the common terms the ones used most are companion, repellent, barrier, indicator, trap, insectary, and banker plant. These terms are often employed for a wide range of functions, and only in the recent paper by Parolin et al. (2012b) 295 were they accurately defined. We have summarized the knowledge of the most commonly employed secondary plants, including definitions and clarifications, in Table 1. 300 4.

Functional characteristics of secondary plants

Many functional characteristics provided by a plant can influence tritrophic interactions, be it through topdown effects, enhancing arthropod reproduction and survival, or through bottom-up effects. Suitability as a secondary plant depends on plant morphology, taxonomy, chemical composition, as well as several other intrinsic factors. We have listed here the main plant characteristics that can affect pest control and which may thus play a role on the efficiency of secondary plants. Cortesero et al. (2000) suggested ways of manipulating the most important plant attributes which influence the efficiency of beneficial organisms and which should be genetically implanted into crop plants to enhance biological control practices. However, we suggest taking advantage of the naturally available local plants which possess these attributes. It may be better environmentally to employ these as secondary plants rather than introducing potentially invasive species from elsewhere or using genetically modified organisms. 4.1.

Plant architecture

High structural complexity is an asset when employing a secondary plant. The efficiency of the secondary plant increases with increasing plant structural complexity (Cortesero et al. 2000; Skirvin et al. 2002). Plant architecture may influence the behavior, the quantity and the distribution of pests as well as the natural enemies of the crop plant (Halaji et al. 2000; Gurr et al. 2004; Grechi et al. 2008), because it affects searching time and foraging success of arthropods (Desneux and O’Neil 2008). However, it may also have a positive effect on biological control because it can decrease negative interactions among beneficial organisms, that is, intraguild predation (Finke and Denno 2006; Langellotto and Denno 2006), thus increasing opportunities for niche-complementarity. Phytophagous insect communities are richer when plants are bigger, more structurally complex, or the characteristics of the above-ground parts more diverse (Lawton 1983). Therefore, plant architecture may be intentionally manipulated using practices such as budpruning, stem-pruning, and control of edaphic factors such as nutrients, light, or climate (Gingras et al. 2002; Boege 2005; Grechi et al. 2008).

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effects on the pests, and thus indirect positive effects on the crop. When a secondary plant is present (Figure 1, process A), it has an indirect positive effect on the crop, that is, through positive effects on density, prevalence and/or activity of the beneficial organisms – for example, a banker plant enhances the establishment of a given predator species. The beneficials, then, have a direct negative effect on the pests which in turn indirectly benefits the crop plants so that they are less affected by pests and thus more productive. In process B (Figure 1), pests attack the secondary plant and are thus less concentrated on the crop plants. This may lead to a direct negative impact of the pests on the secondary plant and to an indirect beneficial influence of the secondary plant on the crop plant, as is the case in trap, indicator and barrier plants. Other processes involving secondary plants can either have negative effects on crop plants or direct positive effects on the crop plants without beneficials mediating in the interactions. Despite predominantly positive functions, secondary plants added to crops may also have undesired indirect negative effects on the crop plants. For example, if secondary plants enhance the pest reproduction, this may lead to decreased crop productivity (Figure 1, process C). Moreover, there may be negative effects of the secondary plants on the crop plants due to competition (e.g. for light, water or nutrients) as is the case when some insectary plants are present (Cranshaw 1996; Fiedler et al. 2007). This is also true for flowering plants which increase resources for pollinators, mainly bees, in agricultural landscapes (Decourtye et al. 2010) as they might also benefit pests and thus compromise the sustainability of IPM programmes. A further important indirect negative effect of secondary plants added to a crop is that it could be more difficult for some natural enemies to find their host in a more diverse and complex crop system (Andow and Prokrym 1990; Coll and Bottrell 1996). In bottom-up processes (Figure 1, process D), secondary plants, namely companion plants (Kuepper and Dodson 2001; Finch et al. 2003), may increase crop plant productivity – for example, by fixing nitrogen – and influence pest control since fertilization has an effect on pest and predator presence (Gruner et al. 2008). The implications for multitrophic interactions described here are non-exclusive, and these processes can occur simultaneously, depending on the characteristics of the plants, pests and beneficial organisms. Other interactions may exist which have not been documented in Figure 1.

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3. Plant types added to crops Several categories of secondary plants added to crops have been reported, most of them based on

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entomological studies. Among the common terms the ones used most are companion, repellent, barrier, indicator, trap, insectary, and banker plant. These terms are often employed for a wide range of functions, and only in the recent paper by Parolin et al. (2012b) 295 were they accurately defined. We have summarized the knowledge of the most commonly employed secondary plants, including definitions and clarifications, in Table 1. 300 4.

Functional characteristics of secondary plants

Many functional characteristics provided by a plant can influence tritrophic interactions, be it through topdown effects, enhancing arthropod reproduction and survival, or through bottom-up effects. Suitability as a secondary plant depends on plant morphology, taxonomy, chemical composition, as well as several other intrinsic factors. We have listed here the main plant characteristics that can affect pest control and which may thus play a role on the efficiency of secondary plants. Cortesero et al. (2000) suggested ways of manipulating the most important plant attributes which influence the efficiency of beneficial organisms and which should be genetically implanted into crop plants to enhance biological control practices. However, we suggest taking advantage of the naturally available local plants which possess these attributes. It may be better environmentally to employ these as secondary plants rather than introducing potentially invasive species from elsewhere or using genetically modified organisms. 4.1.

Plant architecture

High structural complexity is an asset when employing a secondary plant. The efficiency of the secondary plant increases with increasing plant structural complexity (Cortesero et al. 2000; Skirvin et al. 2002). Plant architecture may influence the behavior, the quantity and the distribution of pests as well as the natural enemies of the crop plant (Halaji et al. 2000; Gurr et al. 2004; Grechi et al. 2008), because it affects searching time and foraging success of arthropods (Desneux and O’Neil 2008). However, it may also have a positive effect on biological control because it can decrease negative interactions among beneficial organisms, that is, intraguild predation (Finke and Denno 2006; Langellotto and Denno 2006), thus increasing opportunities for niche-complementarity. Phytophagous insect communities are richer when plants are bigger, more structurally complex, or the characteristics of the above-ground parts more diverse (Lawton 1983). Therefore, plant architecture may be intentionally manipulated using practices such as budpruning, stem-pruning, and control of edaphic factors such as nutrients, light, or climate (Gingras et al. 2002; Boege 2005; Grechi et al. 2008).

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AQ11 Table 1. Type of secondary plant Banker plant

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Barrier plant

Definition and main characteristics of different types of secondary plants.

Definition

Increase the probability of A banker plant is the plant establishment of beneficial component of the banker plant organisms. Sustain a system, which, together with reproducing population of alternative food and beneficial beneficial organisms, within a organisms, is ‘‘a rearing and cropping system, that will release system purposefully provide long-term pest added to or established in a suppression. crop for control of pests in greenhouses or open field’’ (Huang et al. 2011) Plants are ‘‘used within or Disease suppression and/or bordering a primary crop for interception of pests and/or the purpose of disease pathogens. Reduce spread of suppression’’ (Deol and Rataul diseases or pests. 1978).

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Companion A companion plant is an plant intercrop that influences the first trophic level by enhancing nutrition and/or chemical defence of the crop plants. In addition, it might have repelling and/or intercepting effects on pests and pathogens and attract natural enemies, or provide food for natural enemies (Parolin et al. in press). Indicator plant

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Repellent plant

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Trap plant

Characteristics and functions

Aims

Biological control agents are released onto the banker plants and as they reproduce and increase in numbers, they spread out into the rest of the crops, representing a mini-rearing system for the beneficial organisms. An advantage of banker plant systems over augmentative biological control is preventive control without repeated, expensive releases of beneficial organisms (Frank 2010).

They are used within or bordering a primary crop. High, tall plants may act as mechanical barriers that reduce the total number of aphids landing on the protected crop (Fereres 2000). A nonsusceptible crop can be mixed with the crop to be protected, so that the intercrop provides camouflage, decreases the movement and spread, and possibly also acts as a source of beneficial organisms (Thresh 1982). Enhance the growing conditions Plants are grown close to a crop plant in horticulture for the crop plants. and agriculture, they directly influence the first trophic level (Kuepper and Dodson 2001; Finch et al. 2003) by (i) enhancing flavour: some plants alter the flavour of other plants, (ii) fixing nitrogen: legumes are able to fix atmospheric nitrogen with Rhizobium bacteria; this is for their own use but also benefits neighbouring plants, (iii) shelter and protection: tall plants may protect other species through shading or by providing a windbreak, (iv) biochemical pest suppression: some plants produce chemicals that suppress or repel pests and protect neighbouring plants (Ode 2006). Species or varieties that are more The plant provides characteristics which enable a pest prone to an insect or disease to establish earlier than on the crops, thus than the desired crop. May providing enough time for IPM to be installed on intercept pests. the crops.

Species or variety which makes early detection of pests and pathogens easier, and thus is more cost-effective in detecting pest and disease symptoms on a crop (Parolin et al., in press). An insectary plant is a flowering Provide extended season of floral Selecting plants which flower from early to late in the season, and/or have specific floral structures, resources for insects (Fiedler plant which attracts and beneficial organisms are attracted by plants with et al. 2007). Attract beneficial possibly maintains, with its extrafloral nectaries or by flowers with readily organisms such as parasitic nectar and pollen resources, a accessible pollen and nectaries (Colley and Luna wasps and hoverflies (Heimpel population of natural enemies 2000; Ambrosino et al. 2006). Beneficial organisms and Jervis 2005). which contribute to biological produced on insectary plants may disperse into the pest management on crops crops and thus protect them from pests (Quarles (Parolin et al. in press). and Grossman 2002; Heimpel and Jervis 2005; Pontin et al. 2006). Used to keep pest organisms These plants are part of an intercropping culture Intercropping culture which away from the main culture. which repels pests and/or pathogens (Ibrahim et al. repels pests and/or pathogens 2001) thanks to the aversion caused by natural thanks to the aversion caused chemical substances emitted by these plants (Hay by natural chemical substances 1986; Pfister and Hay 1988; Parolin et al. in press). emitted by these plants (Parolin et al. in press). Trap plants are more attractive to a particular pest Allow early detection and Plants grown in ‘‘plant stands species than the main crop (Murphy 2004; Jindal monitoring of pests and that are, per se or via et al. 2012), i.e., the pest is concentrated on the trap diseases. Also used as a manipulation, deployed to plants (Lamb 2006). Some types of trap plants can component of pest suppression attract, divert, intercept, and/ only support low levels of pest survival, thereby strategies (Shelton and or retain targeted insects or the giving a similar effect as spraying with insecticides Badenes-Perez 2006) because pathogens they vector in order (Khan et al. 2007). trap plants can be sprayed with to reduce damage to the main pesticides when pests reach crop’’ (Shelton and Badeneshigh densities on these plants Perez 2006). (thus acting as a dead end for pest populations).

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460 4.2. Pubescence and trichomes Locomotion of beneficials is often more efficient on smooth surfaces than on complex ones (Andow and

Prokrym 1990). Trichomes may confer physical resistance to insect herbivores by impeding locomotion, feeding, and oviposition (Styrsky et al. 2006). Thus,

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International Journal of Pest Management hairs and trichomes decrease herbivore suppression by parasitoids and predators (Styrsky et al. 2006). However, pubescence can also impede the movements of beneficials such as very small-bodied parasitoid wasps (Lukianchuk and Smith 1997; Smith 2005). Glandular trichomes especially may confer chemical resistance by exuding noxious secondary plant metabolites which influence predator and parasitoid movement, and thus negatively influence the encounter rate with hosts or prey (Su¨tterlin and van Lenteren 1997; Cortesero et al. 2000; Stavrinides and Skirvin 2003). However, findings also suggest that predators can adapt to pubescence more quickly than the pest (Croft et al. 1999), which implies that plants bearing these hairs enhance predator establishment. Thus, it is evident that the effects of pubescence are varied, and empirical analyses may be needed when screening for new local plants suited as secondary plants. 4.3.

Domatia

Domatia are small invaginations and hair tufts usually found at vein junctions on the undersides of leaves (Pemberton and Turner 1989). More than 2000 plant species of several families have domatia which may intercede by mutual interactions between plants and predators (Lundstro¨m 1887; Agrawal et al. 2000). Domatia – or acarodomatia in the case of mites (Ferreira et al. 2010) – are frequently inhabited by predatory and mycophagous mites, sometimes at high densities (for review, see Walter 1996 and citations therein). They offer protection against adverse weather conditions and other predators and intraguild predation. The presence of domatia favours the presence of beneficial organisms and pest suppression (O’Dowd and Willson 1991; Parolin et al. 2011). Plants may benefit from the presence of domatia because (e.g. in banker plants) predators can multiply and also protect the crops next to the secondary plants where they reduce pest or fungal pathogen densities.

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4.4.

Waxes

Epicuticular waxes and lipids play an important role in mediating insect–plant interactions (Juniper and Southwood 1986) as they affect predator and parasitoid movement and therefore influence the encounter rate with hosts or prey (Cortesero et al. 2000; Desneux and Ramirez-Romero 2009). The aerial parts of plants are covered by epicuticular waxes, usually composed of a lipid polymer and extractable lipids, which serve mainly to protect plants from dehydration (Baker 1982; Hadley 1985; Muller and Riederer 2005). The lipids contained therein can also absorb pesticides and therefore reduce their overall toxicity to insects (Desneux et al. 2005). Surface lipids not only contribute to plant defence by adversely affecting insects through direct toxicity, but also by physical effects,

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such as interfering with movement (Eigenbrode 2004). The epicuticular lipids can vary; for example, those of field-grown plants can be very different from those of 525 plants grown in growth chambers or greenhouses (Woodhead 1981; Yang et al. 1994). Furthermore, how waxes influence arthropods depends on variations among plant genotypes within a species (including crop species) (Eigenbrode and Espelie 1995; Bottrell et al. 530 1998; Johnson et al. 2006; Crutsinger et al. 2008). 4.5.

Pollen and nectar

Providing pollen and nectar on a fine scale may increase the fitness of beneficial organisms and, as a consequence, result in pest population suppression (Wratten et al. 2000; Heimpel and Jervis 2005; Koptur 2005; Wa¨ckers et al. 2005, 2007). Experiments have demonstrated that beneficial organisms are more abundant within high densities of floral resource plants than in environments without (Tylianakis et al. 2004; Rebek et al. 2005). Nectar-producing plants can improve biological control of pests by supplying parasitoids with sugar, which is often limited in monocultures (Heimpel and Jervis 2005). This improved biological control and the underlying nectarfeeding mechanism was named ‘‘parasitoid nectar provision hypothesis’’ (Heimpel and Jervis 2005). However, as it is an extremely complex system (Heimpel and Jervis 2005), there can be negative effects on the crops if the pest populations take advantage of the added plant resources (Wratten et al. 2000; Wilkinson and Landis 2005).

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Plant chemical attributes

Plant chemical attributes can directly influence the survival, fecundity, and foraging success of beneficial organisms on hosts or preys (Adeyemi 2010). They 560 affect the interactions and consequently increase or decrease the intensity of protection. Secondary metabolites may act directly on deterring herbivores or influence the entire ecological system by cascade effects (Finke and Denno 2006; Adeyemi 2010). When 565 selecting trap and repellent plants, as well as insectary plants, secondary metabolites are important characteristics which determine the interactions with pests and predators, as they play a role in orientating predator species towards their prey (Cortesero et al. 2000). 570 Besides their effects on interactions, chemical compounds of secondary plants have been successfully used to control soil-borne plant pathogens and to inhibit mycelial growth (Bekesi 1979; Hajieghrari et al. 2008). 575 5.

Trade-offs in the selection of secondary plants

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The secondary plants must yield the maximum amount of interactions which have positive impacts on the crop plants and a minimum amount of negative ones (Figure 1). When choosing a secondary plant, the complexity of all interactions has to be considered for most favourable use. Any potential negative sideeffects of secondary plants on crop plants should therefore be carefully assessed before adding such plants to cropping systems: secondary plants can lead to competition, that is, bi-directional negative interactions with the crop plants. If this is the case, the efficiency of biological control decreases either by intraguild predation or undesired interactions. This may also happen in systems which are not fully understood; for example, when additional plants increase the number of pests rather than the target beneficial organisms as has been documented a number of times (Rosenheim et al. 1995; Gurr et al. 2004, Irvin et al. 2006; Straub et al. 2008; Frank 2010). Many secondary plants are typically generalists rather than specialists, and are very tolerant of suboptimal conditions; for example, fast-growing annuals as well as resistant perennials which grow even under hydric stress and are not easily destroyed by a large number of pests. As a consequence, they often share the typical characteristics of invasive species, which is a reason why native plants should preferably be chosen over exotic plant species in order to prevent introducing potentially invasive alien plant species into new areas.

secondary plants may have effects on several ecosystem services besides pest suppression and regulation, such as biodiversity and ecological restoration, or cultural values (Hooper et al. 2005; Fiedler et al. 2008). Our contribution aims at increasing the knowledge and understanding of the functioning of secondary plants in order to support their potential implementation in IPM programmes, especially by ensuring that the plants used provide both positive effects on beneficial organisms and negative ones on pests. Establishing novel and more efficient pest management strategies for environmentally-sound and economically-sustainable agriculture is a vital issue. Thorough analyses and real understanding of the interactions and their likely causes are fundamental for the implementation of secondary plants in cropping systems. We hope that this paper will contribute to this aim, and that biological control may be improved even further by implementing various plant types grouped as secondary plants, with well-identified plant characteristics and related top-down and/or bottom-up effects.

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660 Acknowledgements We thank Roger Boll, Alexandre Bout, Richard Brun, three anonymous reviewers and Mark Jervis for helpful comments on an earlier version of the manuscript. The English was corrected by Irma Mascio. This work was supported by a 665 Post-Doc grant from INRA’s Department Plant Health and Environment, for which we are grateful.

References 6. Conclusions In this review, we have described the most important characteristics and morpho-anatomical traits of secondary plants which may enhance pest control through multiple mechanisms. Knowledge of how these mechanisms operate and integrate is beneficial for the development of efficient strategies in order to employ secondary plants. The main demands of secondary plants are that they should be easy to cultivate, longlasting, and not compete with the crop for light, space and nutrients. Temperature, humidity, light, and nutrient requirements should be similar to those of the crop to be protected and be compatible with the needs of the crops grown alongside them. Moreover, plants should grow quickly and inexpensively to be incorporated into IPM programmes (Irvin et al. 2006). Awareness is increasing as regards the importance of biological control as an alternative to chemical control in crop production, especially in Europe (Enkegaard 2008; Jonsson et al. 2008). Alternative management strategies are needed because many arthropod pests have developed resistance to pesticides (McCaffery 1998; Landis et al. 2000; Zehnder et al. 2007). Therefore, research and application of IPM methods should be fostered (National Research Council 2010; Pretty et al. 2010). Furthermore,

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Adeyemi MMH. 2010. The potential of secondary metabo- 670 lites in plant material as deterents against insect pests: A review. Afr J Pure Appl Chem. 4:243–246. Agrawal AA, Karban R, Colfer RG. 2000. How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos. 89:70–80. Ambrosino MD, Luna JM, Jepson PC, Wratten SD. 2006. Relative frequencies of visits to selected insectary plants by predatory hoverflies (Diptera: Syrphidae), other beneficial insects, and herbivores. Environ Entomol. 35:394–400. Andow DA, Prokrym DR. 1990. Plant structural complexity and host-finding by a parasitoid. Oecologia. 82:162–165. Baker EA. 1982. Chemistry and morphology of plant epicuticular waxes. In: Cutler DF, Alvin KL, Price CE, editors. The plant cuticle. London: Academic Press. p. 139–165. Bekesi P. 1979. The effect of the pollen of some weed species on germination of conidia of Botrytis cinerea. Acta Phytopathol. 14:379–382. Biondi A, Desneux N, Siscaro G, Zappala` L. 2012. Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere. 87:803–812. Boege K. 2005. Herbivore attack of Caesaria nitida influenced by plant ontogenetic variation in foliage quality and plant architecture. Oecologia. 143:117–125. Bottrell, DG, Barbosa P, Gould F. 1998. Manipulating natural enemies by plant variety selection and modification: A realistic strategy? Annu Rev Entomol. 43:347– 367.

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