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 fit-

ness. 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) demon-

strate that the presence of an AM fungus in the roots of a

host plant alters volatile emissions and host plant attractive-

ness to parasitoids in the presence of herbivores. This

extends previous studies that have focused on direct inter-

actions of AM with plants (e.g. mycorrhizal fungal–plant–

herbivore interactions; reviewed in Gehring & Bennett

2009), but have not conclusively demonstrated how below-

ground 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 & Schaus-

berger 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 conclu-

sively 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 non-

mycorrhizal 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 parasit-

oid 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 com-

bined both parasitoid attractiveness and measurement of

volatiles, but they primarily tested effects of attraction to

plants in the absence of herbivory and never made compari-

sons between mycorrhizal and non-mycorrhizal plants

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 multi-

ple future opportunities in above–belowground research. The

first of these opportunities involves identifying the mecha-

nisms 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 path-

way 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 colo-

nized byAM 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 constit-

utive and induced defences as well as indirect defences via vol-

atile 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? Shaus-

berger 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 disap-

peared after herbivory. However, different volatile chemicals

were released from plants experiencing herbivory and colo-

nized or not byAM fungi (see also Leitner et al. 2010). Shaus-

berger et al. did not address whether increased attraction to

plants hosting AM fungi is associated with a particular vola-

tile or blend of volatiles. Answering this question will allow us*Correspondence author. E-mail: alibenne@bio.indiana.edu

� 2012 The Author. Functional Ecology � 2012 British Ecological Society

Functional Ecology 2012, 26, 305–306 doi: 10.1111/j.1365-2435.2011.01957.x

to better understand the biological system, create applications

for pest control and inform our understanding of the bio-

chemical 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 onAM 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 fun-

gal species, or different communities of AM fungi (e.g. an

undisturbed community or a disturbed community), also

influence the volatile blends produced by plants. Compari-

sons of plants hosting different AM fungal species and combi-

nations of two or three species have showed that

attractiveness to parasitoids varies with AM fungal combina-

tion (Gange, Brown & Aplin 2003), suggesting that effects

may vary strikingly under field conditions containingmultiple

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 sys-

tems often have reduced AM fungal diversity (e.g. Daniell

et al. 2001) because of soil disturbance, fertilization and

repeated monocultures. Reduced diversity AM fungal com-

munities could alter host plant volatile blends to increase or

decrease attractiveness to parasitoids in the presence of her-

bivory. Restoration projects often focus on establishing the

plant community and rarely consider the soil community

(Bennett 2010), yet the restoration of an AM fungal commu-

nity in conjunction with the plant community may play a role

in the attraction of aboveground parasitoids and therefore

insect diversity within a restoration.

References

Bennett, A.E. (2010) The role of soil community biodiversity in insect biodiver-

sity. Insect Conservation and Diversity, 3, 157–171.

Bennett, A.E., Alers-Garcia, J. & Bever, J.D. (2006) Three-way interactions

amongmutualistic mycorrhizal fungi, plants, and plant enemies: Hypotheses

and synthesis.AmericanNaturalist, 167, 141–152.

Daniell, T.J., Husband, R., Fitter, A.H. & Young, J.P.W. (2001) Molecular

diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS

Microbiology Ecology, 36, 203–209.

Gange, A.C., Brown, V.K. & Aplin, D.M. (2003) Multitrophic links between

arbuscular mycorrhizal fungi and insect parasitoids. Ecology Letters, 6,

1051–1055.

Gehring, C. & Bennett, A. (2009) Mycorrhizal fungal-plant-insect interactions:

the importance of a community approach. Environmental Entomology, 38,

93–102.

Guerrieri, E., Lingua,G., Digilio,M.C.,Massa, N.&Berta, G. (2004)Do inter-

actions between plant roots and the rhizosphere affect parasitoid behaviour?

Ecological Entomology, 29, 753–756.

Heil, M. (2008) Indirect defence via tritrophic interactions. New Phytologist,

178, 41–61.

Hempel, S., Stein, C., Unsicker, S.B., Renker, C., Auge, H., Weisser, W.W.

& Buscot, F. (2009) Specific bottom-up effects of arbuscular mycorrhizal

fungi across a plant-herbivore-parasitoid system. Oecologia, 160,

267–277.

Hoffmann, D., Vierheilig, H. & Schausberger, P. (2011a) Arbuscular mycor-

rhiza enhances preference of ovipositing predatory mites for direct prey-

related cues.Physiological Entomology, 36, 90–95.

Hoffmann, D., Vierheilig, H. & Schausberger, P. (2011b) Mycorrhiza-induced

trophic cascade enhances fitness and population growth of an acarine preda-

tor.Oecologia, 166, 141–149.

Leitner, M., Kaiser, R., Hause, B., Boland,W. &Mithofer, A. (2010) Does my-

corrhization influence herbivore-induced volatile emission in Medicago

truncatula?Mycorrhiza, 20, 89–101.

Pozo, M.J. & Azcon-Aguilar, C. (2007) Unraveling mycorrhiza-induced resis-

tance.Current Opinion in Plant Biology, 10, 331–432.

Schausberger, P., Peneder, S., Jurschik, S. & Hoffmann, D. (2012) Mycorrhiza

changes plant volatiles to attract spider mite enemies. Functional Ecology,

26, 441–449.

Smith, S.E. & Read, D.J. (2008)Mycorrhizal Symbiosis. Academic Press, New

York, NY,USA.

Van Dam, N.M. & Heil, M. (2011) Multitrophic interactions below and above

ground: en route to the next level. Journal of Ecology, 99, 77–88.

Wooley, S.C. & Paine, T.D. (2011) Infection by Mycorrhizal fungi increases

natural enemy abundance on tobacco (Nicotiana rustica). Environmental

Entomology, 40, 36–41.

� 2012 The Author. Functional Ecology � 2012 British Ecological Society, Functional Ecology, 26, 305–306

306 FE Spotlight