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. In this study we show that an arbuscular mycorrhizal symbiosis makes tomato plants significantly more resistant towards aphids, by enhancing both direct defences, both attractivity towards aphid parasitoids

DIGILIO, MARIA CRISTINA

GUERRIERI E.

LINGUA G.

MASSA N. G. BERTA

English

Archivio della ricerca - Università degli studi di Napoli Federico II

NEW P ER S P E C T I V E SDo interactions between plant roots and the rhizosphereaffect parasitoid behaviour?EMIL IO GUERRIER I 1 , GU IDO L INGUA2 , MARIA CRI ST INADIG IL IO 3 , NADIA MASSA 2 and GRAZ IELLA BERTA2 1Istituto per laProtezione delle Piante, CNR, Sez. Portici (NA), 2Dipartimento di Scienze dell’Ambiente e della Vita, Università delPiemonte Orientale ‘Amedeo Avogadro’, Alessandria and 3Dipartimento di Entomologia e Zoologia agraria, Universitàdi Napoli ‘Federico II’, ItalyKey words. Aphid parasitoids, arbuscular mycorrhizal, biological control,mycorrhizal symbioses.Multitrophic interactions are powerful forces shaping thestructure of living communities. Plants encounter a greatdiversity of organisms in their environment: some of theseinteractions are beneficial (e.g. symbiotic fungi and insectpollinators) while some are detrimental (e.g. herbivorousinsects and pathogenic micro-organisms). Multitrophicinteractions between below-ground and above-groundorganisms are receiving increasing attention because theymay influence plant defences against biotic and abioticstresses (van Dam et al., 2003). Plant defences can beconstitutive or induced (Agrawal et al., 1999; Walling,2000), and may also be direct (e.g. toxic compounds likeglucosinolates in Brassicaceae) or indirect. Indirect defencestypically involve the production of volatile semiochemicalsthat are attractive towards natural enemies of herbivorousinsects (Dicke, 1999). These semiochemicals have beenreferred to as synomones to stress the mutual benefit ofthe partners involved (Vet & Dicke, 1992). Some of thesevolatiles are released as a specific response to the attack of aspecific herbivore (see Agrawal et al., 1999 and referencestherein), a feature termed induced indirect defence. Severalstudies show that the release of induced volatiles is notconfined exclusively to the organ attacked but involves allthe 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 thatany colonising organism alters the profile of plant volatilessuggests that this may have intriguing and oftenunpredictable consequences for the performance of highertrophic levels (Dicke et al., 2003). In this paper we report onthe interactions between below-ground interactions andindirect defences.Arbuscular mycorrhizal symbioses are mutualistic inter-actions between plant roots and soil fungi, and have beenreported for more than 80% of higher plants (Smith &Read, 1997). Colonisation by arbuscular mycorrhizalfungi induces resistance or tolerance to a variety of patho-gens in tomato and in other plants (Cordier et al., 1996;Trotta et al., 1996; Lingua et al., 2002). These changesare mediated by a variety of mechanisms, including theup-regulation and down-regulation of specific genes (Tahiri-Alaoui & Antoniw, 1996) that result in localised and sys-temic responses by the plant. These responses include thesynthesis of new isoforms of chitinases and glucanases andthe 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 above-ground herbivores has been investigated with contrastingresults (van Dam et al., 2003 and references therein). Morerecently, the effects of different species of arbuscularmycorrhizal fungi on parasitism rates have been reported(Gange et al., 2003) but this study did not demonstrate adirect link between arbuscular mycorrhizae and attractionof insect parasitoids. In this study we tested the hypo-thesis that an arbuscular mycorrhizal symbiosis makestomato plants significantly more attractive towards aphidparasitoids.Fig. 1a shows the multitrophic system used for this study:at the base of the system is tomato (Lycopersicon esculentumMiller) whose roots were colonised by the arbuscularmycorrhizal fungus Glomus mosseae Nicol & Gerd (Gerde-mann & Trappe) BEG 12. Although tomato plants arecharacterised by high levels of constitutive defences (e.g.glandular trichomes, a-tomatine, Kennedy, 2003), induceddefence mechanisms are nevertheless important (reviewed inAgrawal et al., 1999 and references therein).The herbivore (the potato aphid, Macrosiphum euphor-biae Thomas) is a key pest of tomato all over the world,causing direct and indirect damage to plants, includingCorrespondence: Emilio Guerrieri, Istituto per la Protezionedelle Piante, CNR, Sez. Portici, Via Università 133, 80055 Portici(NA), Italy. E-mail: guerrieri@ipp.cnr.itEcological Entomology (2004) 29, 753–756# 2004 The Royal Entomological Society 753transmission of phytopathogenic viruses (Lange & Bronson,1980). The parasitoid Aphidius ervi (Haliday) is well knownfor its efficiency against the potato aphid (van Lenterenet al., 1997).The parasitoid used in this study is considered to be ageneralist as it can develop in several different aphid speciesattacking different plant families (mainly Solanaceae andLeguminosae). Aphidius ervi has become a model in thestudy of foraging behaviour (Guerrieri et al., 1993, 1997,1999, 2002), and is reported to discern between volatilesreleased by broad bean plant when attacked by host andnon-host aphid species (Du et al., 1997; Guerrieri et al.,1999). Moreover, the increasing response of this parasitoidto plant volatiles following successful encounters with itshost has shown the existence of a link between ovipositionexperience and foraging efficiency (associative learning)(Du et al., 1997; Guerrieri et al., 1997).To test the hypothesis that mycorrhizal colonisationenhances the attractiveness of tomato plants towards theparasitic wasp A. ervi, arbuscular mycorrhizal and non-mycorrhizal plants were tested in a wind tunnel bioassay.For each plant target, 200 female parasitoids were tested byreleasing them individually in the glass chamber of the windtunnel, 30 cm downwind from the target. The attractivenessof each target plant was calculated in terms of percentage offemale parasitoids that flew directly upwind and landed onit. Bioassays were conducted on a minimum of 3 days andplant targets were presented in a random order to reduceany effect of temporal variability of behavioural responses.None of the plants was infested with aphids, allowing theeffects of arbuscular mycorrhizae on parasitoid behaviourto be tested in the absence of their hosts. Mycorrhizal plantswere twice as attractive towards the parasitoid as controlplants, with percentages of attraction close to 80% (Fig.1b), despite the fact that there were no host aphids feedingon these plants. Moreover, these percentages of parasitoidsattracted to the mycorrhizal plants were not significantlydifferent from those recorded in a second experimentagainst a non-mycorrhizal plant that had been infested byhundreds of M. euphorbiae for a week (Fig. 1c).The hypothesis that the arbuscular mycorrhizalsymbiosis would affect the development and reproduction020406080100Cphc M(c)NS020406080C***(d)M020406080100***C(b)(a)MInsectparasitoidPotato aphidTomato plantAM fungusFig. 1. (a) The multitrophic system used in this study consisted of tomato plant, cultivar M82, colonised by the arbuscular mycorrhizal (AM)fungus Glomus mosseae (enlarged in the box, bottom left), the potato aphid Macrosiphum euphorbiae and its natural enemy, the braconidparasitoid Aphidius ervi; þ indicates a positive interaction, – indicates a negative interaction. (b) Percentages of parasitic wasps (n¼ 200)attracted by uninfested control (C) and uninfested mycorrhizal (M) plants of tomato in a wind tunnel bioassay. (***P < 0.001, G-test forIndependence, Sokal & Rohlf, 1995; Rohlf & Sokal, 1995). (c) Percentages of parasitic wasps (n¼ 200) attracted by control tomato plantsinfested by Macrosiphum euphorbiae (Cphc) and by uninfested mycorrhizal (M) tomato plants in a wind tunnel bioassay (G-test forIndependence, Sokal & Rohlf, 1995; Rohlf & Sokal, 1995). (d) Percentages of potato aphids (n¼ 100) reaching adult stage (filled bars) andreproducing (open bars) on control (C) and mycorrhizal (M) plants of tomato (***P< 0.001, G-test for Independence, Sokal & Rohlf, 1995;Rohlf & Sokal, 1995).754 Emilio Guerrieri et al.# 2004 The Royal Entomological Society, Ecological Entomology, 29, 753–756of the aphid hosts was also tested. Only 16% of aphidssuccessfully completed their development on arbuscularmycorrhizal plants, and only 8% reproduced, percentagessignificantly lower that those recorded on control, non-mycorrhizal plants (Fig. 1d).The results of these studies raise interesting questionsabout the reliability of plant signalling for insect parasitoidsand the efficacy of biological control when plants havemycorrhizal symbioses. One of the most intriguing implica-tions of this study is that it suggests that parasitoids mayarrive on mycorrhizal plants that have few or no aphidhosts. In the system used here, A. ervi showed similarresponses to plants with an arbuscular mycorrhizal symbio-sis and to plants with large M. euphorbiae populations(65.5%, data not shown). Since A. ervi displays associativelearning (Guerrieri et al., 1997), the long-term implicationsof these results for biological control in this system are notclear. In other similar systems, a minimum threshold ofaphid infestation (in terms of the number of aphids andthe duration of their feeding activity) is required to make ahost plant attractive towards A. ervi (Guerrieri et al., 1999).In this study, arbuscular mycorrhizal plants and plantsinfested with aphids were significantly more attractive toparasitoids than plants without the symbiosis (Fig. 1b) orplants without aphids (32.3%, data not shown, P< 0.01,G-test for Independence, Rohlf & Sokal, 1995; Sokal &Rohlf, 1995), and hence the final outcome of the interactionbetween tomatoes and A. ervi was similar regardless ofwhether the plant was colonised by a beneficial soil fungusor populations of a sap-feeding herbivore. This combinationof partial resistance to aphid infestation (Fig. 1d) and theproduction of semiochemicals attractive towards natural ene-mies of aphids, may result in an effective defence strategy forarbuscular mycorrhizal plants against herbivore populations.Although this study suggests that tomato plants maybenefit from the arbuscular mycorrhizal symbiosis theeffects of this interaction on the performance of the para-sitoid are less clear. A fascinating possibility is that thearbuscular mycorrhizal symbiosis may allow the parasitoidsto locate hosts at low, and perhaps otherwise undetectable,aphid population densities.It would also have been interesting to assess whether thequality of the few aphids that survived on the arbuscularmycorrhizal plants is high enough to support parasitoiddevelopment (Awmack & Leather, 2002), but this wasbeyond the scope of this study. Although it is possible thatin the long term aphids will evolve resistance to the changesin plant quality induced by the arbuscular mycorrhizalsymbiosis, the high levels of attractiveness of these plantsto aphid parasitoids may provide an indirect plant defencethat exerts no evolutionary pressure on the pest because it isnot herbivore mediated. This apparent decrease in reliabil-ity of plant cues for the parasitoid may, however, be com-pensated for by the relatively high fecundity of braconidparasitoids of aphids compared with other parasitoids suchas aphelinids (Digilio & Pennacchio, 1989; Couty et al., 2001).This study highlights the novel and complex net ofinteractions that exist even in this simplified model system.Further experiments (especially field experiments) toinvestigate the long-term stability of the interactions wouldclearly be of value, as would an investigation to determinewhether aphids and the mycorrhizal symbiosis have similareffects on the expression of genes associated with plantdefences (Fidantsef et al., 1999; Birkett et al., 2000). Simi-larly, the results of a recent study suggesting that plant-mediated effects of mycorrhizal symbiosis on the highertrophic levels may be affected by the fungal species involved(Gange et al., 2003) also merit further investigation.The positive effect of mycorrhizal colonisation on theattraction of parasitic wasps to their host plants and anegative effect on insect pest populations observed in thisstudy have important implications for our understanding ofinsect population dynamics. We will only be able to predictthe course of the evolution of plant defence mechanismsthat could be used to improve the efficacy of biologicalcontrol if we understand these interactions.AcknowledgementsThis project was supported by the Italian CNR and by theUniversità degli Studi del Piemonte Orientale ‘AmedeoAvogadro’. We would like to thank Caroline S. Awmackfor helpful comments and discussions.ReferencesAgrawal, A.A., Tuzun, S. & Bent, E. (1999) Induced Plant DefensesAgainst Pathogens and Herbivores. APS Press, The AmericanPhytopathological Society, St Paul, Minnesota.Alborn, H.T., Turlings, T.C.J., Jones, T.H., Stenhagen, G.,Loughrin, J.H. & Tumlinson, J.H. (1997) An elicitor of plantvolatiles from beet armyworm oral secretion. Science, 276,945–949.Awmack, C.S. & Leather, S.R. (2002) Host plant quality andfecundity in herbivorous insects. Annual Review of Entomology,47, 817–844.Azcón-Aguilar, C., Jaizme-Vega, M.C. & Calvet, C. (2002) Plantdefense responses induced by arbuscular mycorrhizal fungi.Mycorrhizal Technology in Agriculture (ed. by S. Gianinazzi, H.Schüepp, and J. M. Barea), pp. 187–198. Birkhauser, Basel.Birkett, M.A., Campbell, C.A.M., Chamberlain, K., Guerrieri, E.,Hick, A.J. & Martin, J.L. et al. (2000) New roles for cis-jasmoneas an insect semiochemical and in plant defence. Proceedings ofthe National Academy of Sciences of the United States ofAmerica, 97, 9329–9334.Cordier, C., Gianinazzi, S. & Gianinazzi-Pearson, V. (1996) Colo-nisation patterns of root tissues by Phytophthora nicotianae var.parasitica related to reduced disease in mycorrhizal tomato.Plant and Soil, 185, 223–232.Couty, A., Clark, S.J. & Poppy, G.M. (2001) Are fecundity andlongevity of female Aphelinus abdominalis affected by develop-ment in GNA-dosed Macrosiphum euphorbiae? PhysiologicalEntomology, 26, 287–293.van Dam, N.M., Harvey, J.A., Wäkers, F.L., Bezemer, T.M., vander Putten, W.H. & Vet, L.E.M. (2003) Interactions betweenInteractions between mycorrhizae and parasitoids 755# 2004 The Royal Entomological Society, Ecological Entomology, 29, 753–756aboveground and belowground induced responses againstphytophages. Basic and Applied Ecology, 4, 63–77.Dicke, M. (1999) The ecology and evolution of induced defenses.Evolution of Induced Indirect Defenses of Plants (ed. byR. Tollrian and C. J. Harvell), pp. 62–88. Princeton UniversityPress, Princeton, New Jersey.Dicke, M. & Dijkman, H. (2001) Within-plant circulation ofsystemic elicitor of induced defence and release from roots ofelicitor that affects neighbouring plants. Biochemical Systematicsand Ecology, 29, 1075–1087.Dicke, M., van Pecke, R.M.P. & de Boer, J.G. (2003) Inducibleindirect defence of plants: from mechanisms to ecologicalfunctions. Basic and Applied Ecology, 4, 27–42.Digilio, M.C. & Pennacchio, F. (1989) Analisi quantitativa dialcuni parametri biologici caratterizzanti una popolazioneitaliana di Aphidius ervi Haliday (Hymenoptera, Braconidae,Aphidiinae). Bollettino del Laboratorio di Entomologia Agraria‘Filippo Silvestri’, 46, 59–74.Du, Y., Poppy, G.M., Powell, W. & Wadhams, L.J. (1997)Chemically mediated associative learning in the host foragingbehavior of the aphid parasitoid Aphidius ervi (Hymenoptera:Braconidae). Journal of Insect Behavior, 10, 509–522.Fidantsef, A.L., Stout, M.J., Thaler, J.S., Duffey, S.S. & Bostock, R.M.(1999) Signal interactions in pathogen and insect attack:expression of lipoxigenase, proteinase inhibitor II, and patho-genesis-related protein P4 in the tomato Lycopersicon esculen-tum. Physiological and Molecular Plant Pathology, 54, 97–114.Gange, A.C., Brown, V.K. & Aplin, D.M. (2003) Multitrophic linksbetween arbuscular mycorrhizal fungi and insect parasitoids.Ecology Letters, 6, 1051–1055.Guerrieri, E., Pennacchio, F. & Tremblay, E. (1993) Flightbehaviour of the aphid parasitoid Aphidius ervi Haliday(Hymenoptera: Braconidae) in response to plant and hostvolatiles. European Journal of Entomology, 90, 415–421.Guerrieri, E., Pennacchio, F. & Tremblay, E. (1997) Effect of adultexperience on in-flight orientation to plant and plant-hostcomplex volatiles in Aphidius ervi Haliday (Hymenoptera,Braconidae). Biological Control, 10, 159–165.Guerrieri, E., Poppy, G.M., Powell, W., Rao, R. & Pennacchio, F.(2002) Plant to plant communication mediating in-flight orienta-tion of Aphidius ervi. Journal of Chemical Ecology, 28, 1703–1715.Guerrieri, E., Poppy, G.M., Powell,W., Tremblay, E. &Pennacchio, F.(1999) Induction and systemic release of herbivore-induced plantvolatiles mediating in-flight orientation of Aphidius ervi (Hyme-noptera: Braconidae). Journal of Chemical Ecology, 25, 1247–1261.Kennedy, G.G. (2003) Tomato, pests, parasitoids and predators:tritrophic interactions involving the genus Lycopersicon. AnnualReview of Entomology, 48, 51–72.Lange, W.H. & Bronson, L. (1980) Insect pests of tomato. AnnualReview of Entomology, 26, 345–371.van Lenteren, J.C., Roskam,M.M.&Timmer, R. (1997) Commercialmass production and pricing of organisms for biological control ofpests in Europe. Biological Control, 10, 143–149.Lingua, G., D’Agostino, G., Massa, N., Antosiano, M. & Berta, G.(2002) Mycorrhiza-induced differential response to a yellowsdisease in tomato. Mycorrhiza, 12, 191–198.Mattiacci, L., Dicke, M. & Posthumus, M.A. (1995) b-Glucosidase:an elicitor of herbivore induced plant odor that attractshost-searching parasitic wasps. Proceedings of the NationalAcademy of Sciences of the United States of America, 92,2036–2040.Pozo,M.J., Slezack-Deschaumes, S., Dumas-Gaudot, E., Gianinazzi, S.& Azcón-Aguilar, C. (2002) Plant defense responses induced byarbuscular mycorrhizal fungi.Mycorrhizal Technology in Agriculture(ed. by S. Gianinazzi, H. Schüepp and J. M. Barea), pp. 103–112.Birkhauser, Basel.Rohlf, F.J. & Sokal, R.R., eds (1995) Statistical Tables, 3rd edn.W.H. Freeman, New York.Smith, S.E. & Read, D.J. (1997)Mycorrhizal Symbiosis. AcademicPress, London.Sokal, R.R. & Rohlf, F.J., eds (1995) Biometry, 3rd edn.W.H. Freeman, New York.Tahiri-Alaoui, A. & Antoniw, J.F. (1996) Cloning of genesassociated with the colonisation of tomato roots by thearbuscular mycorrhizal fungus Glomus mosseae. Agronomie,16, 699–707.Trotta, A., Varese, G.C., Gnavi, E., Fusconi, A., Sampò, S. &Berta, G. (1996) Interactions between the soil-borne rootpathogen Phytophthora nicotianae var. parasitica and thearbuscular mycorrhizal fungus Glomus mosseae in tomatoplants. Plant and Soil, 185, 199–209.Vet, L.E.M. & Dicke, M. (1992) Ecology of infochemical use bynatural enemies in a tritrophic context. Annual Review ofEntomology, 37, 141–172.Walling, L. (2000) The myriad plant responses to herbivory.Journal of Plant Growth Regulation, 19, 195–216.Accepted 6 April 2004756 Emilio Guerrieri et al.# 2004 The Royal Entomological Society, Ecological Entomology, 29, 753–756

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

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

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