Do interactions between plant roots and the rhizosphere affect parasitoid behaviour?

Multitrophic interactions are powerful forces shaping the structure of living communities. Plants encounter a great diversity of organisms in their environment: some of these interactions are beneficial (e.g. symbiotic fungi and insect pollinators) while some are detrimental (e.g. herbivorous insects and pathogenic micro-organisms). Multitrophic interactions between below-ground and above-ground organisms are receiving increasing attention because they may influence plant defences against biotic and abiotic stresses (van Dam et al., 2003). Plant defences can be constitutive or induced (Agrawal et al., 1999; Walling, 2000), and may also be direct (e.g. toxic compounds like glucosinolates in Brassicaceae) or indirect. Indirect defences typically involve the production of volatile semiochemicals that are attractive towards natural enemies of herbivorous insects (Dicke, 1999). These semiochemicals have been referred to as synomones to stress the mutual benefit of the partners involved (Vet & Dicke, 1992). Some of these volatiles are released as a specific response to the attack of a specific herbivore (see Agrawal et al., 1999 and references therein), a feature termed induced indirect defence. Several studies show that the release of induced volatiles is not confined exclusively to the organ attacked but involves all the plant through the circulation of systemic elicitors (Mattiacci et al., 1995; Alborn et al., 1997; Guerrieri et al., 1999; Dicke & Dijkman, 2001). The growing evidence that any colonising organism alters the profile of plant volatiles suggests that this may have intriguing and often unpredictable consequences for the performance of higher trophic levels (Dicke et al., 2003). In this paper we report on the interactions between below-ground interactions and indirect defences. Arbuscular mycorrhizal symbioses are mutualistic interactions between plant roots and soil fungi, and have been reported for more than 80% of higher plants (Smith & Read, 1997). Colonisation by arbuscular mycorrhizal fungi induces resistance or tolerance to a variety of pathogens in tomato and in other plants (Cordier et al., 1996; Trotta et al., 1996; Lingua et al., 2002). These changes are mediated by a variety of mechanisms, including the up-regulation and down-regulation of specific genes (TahiriAlaoui & Antoniw, 1996) that result in localised and systemic responses by the plant. These responses include the synthesis of new isoforms of chitinases and glucanases and the thickening of the cell walls (Azcón-Aguilar et al., 2002; Pozo et al., 2002) that may affect herbivore colonisation. The effects of arbuscular mycorrhizal symbiosis on aboveground herbivores has been investigated with contrasting results (van Dam et al., 2003 and references therein). More recently, the effects of different species of arbuscular mycorrhizal fungi on parasitism rates have been reported (Gange et al., 2003) but this study did not demonstrate a direct link between arbuscular mycorrhizae and attraction of insect parasitoids. In this study we tested the hypothesis that an arbuscular mycorrhizal symbiosis makes tomato plants significantly more attractive towards aphid parasitoids. Fig. 1a shows the multitrophic system used for this study: at the base of the system is tomato (Lycopersicon esculentum Miller) whose roots were colonised by the arbuscular mycorrhizal fungus Glomus mosseae Nicol & Gerd (Gerdemann & Trappe) BEG 12. Although tomato plants are characterised by high levels of constitutive defences (e.g. glandular trichomes, a-tomatine, Kennedy, 2003), induced defence mechanisms are nevertheless important (reviewed in Agrawal et al., 1999 and references therein). The herbivore (the potato aphid, Macrosiphum euphorbiae Thomas) is a key pest of tomato all over the world, causing direct and indirect damage to plants, including Correspondence: Emilio Guerrieri, Istituto per la Protezione delle Piante, CNR, Sez. Portici, Via Università 133, 80055 Portici (NA), Italy. E-mail: guerrieri@ipp.cnr. it Ecological Entomology (2004) 29, 753–756