Functional Ecology 2012, 26, 305–306
doi: 10.1111/j.1365-2435.2011.01957.x
FE SPOTLIGHT
Pushing boundaries in above–belowground interactions Alison Bennett* James Hutton Institute, Dundee DD2 5DA, UK
Belowground organisms, such as arbuscular mycorrhizal (AM) fungi, have long been credited with altering plant fitness. More recently, research on belowground organisms has revealed that AM fungi also influence a wide variety of aboveground organisms via plants (reviewed in Van Dam & Heil 2011; Bennett 2010). Schausberger et al. (2012) demonstrate that the presence of an AM fungus in the roots of a host plant alters volatile emissions and host plant attractiveness to parasitoids in the presence of herbivores. This extends previous studies that have focused on direct interactions of AM with plants (e.g. mycorrhizal fungal–plant– herbivore interactions; reviewed in Gehring & Bennett 2009), but have not conclusively demonstrated how belowground organisms, and AM fungi in particular, influence third trophic level organisms such as parasitoids (Gange, Brown & Aplin 2003; Guerrieri et al. 2004; Hempel et al. 2009; Leitner et al. 2010; Hoffmann, Vierheilig & Schausberger 2011a,b; Wooley & Paine 2011) via the release of plant volatiles that attract parasitoids that attack herbivores on host plants. Until recently, these studies failed to conclusively document the effects of AM fungi on both volatile release and attraction of parasitoids. For example, Wooley & Paine (2011) and Gange, Brown & Aplin (2003) have shown variation in parasitoid attraction to plants hosting different strains and species of Glomus as compared to nonmycorrhizal plants. Hoffmann, Vierheilig & Schausberger (2011a) also showed greater preference by parasitoids for eggs oviposited on plants associated with a single AM fungus. In addition, a single AM fungus in the roots of a host plant has been shown to positively influence parasitoid life-history characteristics (Hempel et al. 2009; Hoffmann, Vierheilig & Schausberger 2011b). However, none of these studies measured volatile profiles for host plants, so parasitoid attraction could not be directly attributed to volatiles. A study on AM fungal influenced volatile release revealed differences but did not test whether changes in volatiles influenced parasitoids (Leitner et al. 2010). One study combined both parasitoid attractiveness and measurement of volatiles, but they primarily tested effects of attraction to plants in the absence of herbivory and never made comparisons between mycorrhizal and non-mycorrhizal plants *Correspondence author. E-mail:
[email protected]
experiencing herbivory (Guerrieri et al. 2004). Unlike these previous experiments, Schausberger et al. measured both changes in volatile chemistry as well as parasitoid attraction in a fully factorial design. The results presented by Shausberger et al. open up multiple future opportunities in above–belowground research. The first of these opportunities involves identifying the mechanisms by which AM fungi alter parasitoid attraction. For example, what are the biochemical or transcriptional changes that occur following AM fungal colonization that result in altered volatile profiles? Are the mechanisms suggested for AM fungal alteration of direct chemical defences the same mechanisms that alter volatile profiles? Colonization by AM fungi has been shown to turn on the salicylic acid pathway temporarily, a process that may prime the jasmonic acid pathway for herbivore attack (reviewed in Pozo & Azcon-Aguilar 2007). The induction of volatiles is linked to the jasmonic acid pathway (reviewed in Heil 2008), and therefore, plants may be primed for a faster or greater release of volatiles when colonized by AM fungi. However, there may be other mechanisms by which AM fungi influence volatile release. For example, given that AM fungi increase plant biomass and fitness in the Phaseolus vulgaris system studied by Shausberger et al. (as well as many other systems), it could simply be that the increased resources provided by the mutualism allow plants to allocate more resources to plant defensive characteristics (e.g. direct constitutive and induced defences as well as indirect defences via volatile attraction; Bennett, Alers-Garcia & Bever 2006) or that changes in plant size or structure in association with AM fungi benefit or hinder parasitoid searching capabilities (Gange, Brown & Aplin 2003). What characteristics of the volatile blends produced in the presence of AM fungi are attractive for parasitoids? Shausberger et al. showed there were fewer chemicals present in the volatile blends of AM fungal plants before herbivory (relative to plants not hosting AM fungi), but this difference disappeared after herbivory. However, different volatile chemicals were released from plants experiencing herbivory and colonized or not by AM fungi (see also Leitner et al. 2010). Shausberger et al. did not address whether increased attraction to plants hosting AM fungi is associated with a particular volatile or blend of volatiles. Answering this question will allow us
Ó 2012 The Author. Functional Ecology Ó 2012 British Ecological Society
306 FE Spotlight to better understand the biological system, create applications for pest control and inform our understanding of the biochemical or transcriptional mechanisms via which AM fungi alter plants. The second great opportunity presented by Schausberger et al.’s results is determining the ecological relevance of AM fungal communities for alteration of host plant volatile blends. Most of the studies on AM fungal influence of indirect defences (Guerrieri et al. 2004; Hempel et al. 2009, Leitner et al. 2010; Hoffmann, Vierheilig & Schausberger 2011a,b; Wooley & Paine 2011) have compared plants in sterile soil with one or two AM fungal species within a greenhouse or laboratory setting (but see Gange, Brown & Aplin 2003). Plants never grow in sterile soil in the field, nor do plants grow in environments lacking AM fungi in the field (reviewed in Smith & Read 2008). As a result, it is important to examine whether the effects seen in the greenhouse are applicable in the field. We should ask whether and how different AM fungal species, or different communities of AM fungi (e.g. an undisturbed community or a disturbed community), also influence the volatile blends produced by plants. Comparisons of plants hosting different AM fungal species and combinations of two or three species have showed that attractiveness to parasitoids varies with AM fungal combination (Gange, Brown & Aplin 2003), suggesting that effects may vary strikingly under field conditions containing multiple different combinations of AM fungal species. These types of questions have implications for not only our understanding of above–belowground systems, but also for agriculture, restoration and conservation. Agricultural systems often have reduced AM fungal diversity (e.g. Daniell et al. 2001) because of soil disturbance, fertilization and repeated monocultures. Reduced diversity AM fungal communities could alter host plant volatile blends to increase or decrease attractiveness to parasitoids in the presence of herbivory. Restoration projects often focus on establishing the plant community and rarely consider the soil community (Bennett 2010), yet the restoration of an AM fungal community in conjunction with the plant community may play a role
in the attraction of aboveground parasitoids and therefore insect diversity within a restoration.
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Ó 2012 The Author. Functional Ecology Ó 2012 British Ecological Society, Functional Ecology, 26, 305–306
