Abstract
A large body of evidence shows that plants release volatile chemicals upon attack by herbivores. These volatiles influence the performance of natural enemies. Nearly all the evidence on the effect of plant volatiles on natural enemies of herbivores concerns predators, parasitoids, and entomophagous nematodes. However, other entomopathogens, such as fungi, have not been studied yet for the way they exploit the chemical information that the plant conveys on the presence of herbivores. We tested the hypothesis that volatiles emanating from cassava plants infested by green mites (Mononychellus tanajoa) trigger sporulation in three isolates of the acaropathogenic fungus Neozygites tanajoae. Tests were conducted under climatic conditions optimal to fungal conidiation, such that the influence of the plant volatiles could only alter the quantity of conidia produced. For two isolates (Altal.brz and Colal.brz), it was found that, compared with clean air, the presence of volatiles from clean, excised leaf discs suppressed conidia production. This suppressive effect disappeared in the presence of herbivore-damaged leaves for the isolate Colal.brz. For the third isolate, no significant effects were observed. Another experiment differing mainly in the amount of volatiles showed that two isolates produced more conidia when exposed to herbivore-damaged leaves compared with clean air. Taken together, the results show that volatiles from clean plants suppress conidiation, whereas herbivore-induced plant volatiles promote conidiation of N. tanajoae. These opposing effects suggest that the entomopathogenic fungus tunes the release of spores to herbivore-induced plant signals indicating the presence of hosts.
Similar content being viewed by others
References
A. A. Agrawal A. Janssen J. Bruin M. A. Posthumus M. W. Sabelis (2002) ArticleTitleAn ecological cost of plant defence: Attractiveness of bitter cucumber plants to natural enemies of herbivores Ecol. Lett. 5 377–385
P. Agudelo-Silva (1986) ArticleTitleA species of Triplosporium (Zygomycetes: Entomophthoraceae) infecting Mononychellus progressivus (Acari: Tetranychidae) in Venezuela Fla. Entomol. 69 444–446
J. M. Alvarez-Afanador A. Acosta C. A. Belloti A. R. Braun (1993) ArticleTitleEstudios de patogenicidad de un hongo asociado a Mononychellus tanajoa (Bondar) acaro plaga de la yuca (Manihot esculenta Crantz) Rev. Colomb. Entomol. 19 3–5
N. S. Aratchige I. Lesna M. W. Sabelis (2004) ArticleTitleBelow-ground plant parts emit herbivore-induced plant volatiles: Olfactory responses of a predatory mite to tulip bulbs infested by rust mites Exp. Appl. Acarol. 33 21–30
J. A. Baily (1970) Phytoalexins and the ability of leaf tissues to inhibit fungal growth T. Preece (Eds) Ecology of Leaf Surface Micro-organisms Academic Press London 519–528
J. Bartkowski M. O. Odindo W. A. Otieno (1988) ArticleTitleSome fungal pathogens of the cassava green spider mites Mononychellus spp. (Tetranychidae) in Kenya Insect Sci. Appl. 9 457–459
M. I. C. Boff P. H. Smits (2001) ArticleTitleEffects of density, age and host cues on the dispersal of Heterorhabditis megidis Biocontrol Sci. Technol. 11 505–514
M. I. C. Boff F. C. Zoon P. H. Smits (2001) ArticleTitleOrientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer Entomol. Exp. Appl. 98 329–337
G. C. Brown G. L. Prochaska D. F. Hildebrand G. L. Nordin D. M. Jackson (1995) ArticleTitleGreen leaf volatiles inhibit conidial germination of the entomopathogen Pandora neoaphidis (Entomopthorales: Entomophthoraceae) Environ. Entomol. 24 1637–1643
G. S. Chitarra T. Abee F. M. Rombouts M. A. Posthumus J. Dijksterhuis (2004) ArticleTitleGermination of Penicillium paneum conidia is regulated by 1-Octen-3-ol, a volatile self-inhibitor Appl. Environ. Microbiol. 70 2823–2829
H. Y. Choo H. K. Kaya T. M. Burlando R. Gaugler (1989) ArticleTitleEntomopathogenic nematodes: Host finding ability in the presence of plant roots Environ. Entomol. 18 1136–1140
G. C. Cutler J. M. Webster (2003) ArticleTitleHost-finding ability of three entomopathogenic nematode isolates in the presence of plant roots Nematology 5 601–608
Dara, S. K., Lomer, C. J., Hountondji, F. C. C., and Yaninek, S. J. 2001a. Seasonal incidence of two fungal pathogens Neozygites floridana (Zygomycotina: Zygomycetes) and Hirsutella thompsonii (Deuteromycotina: Hyphomycetes), in mite populations on cassava in Benin, pp. 503–507, in M. O. Akoroda and J. M. Ngeve (eds.). Proceedings of 7th Triennial Symposium of the International Society for Tropical Root Crops—Africa Branch (ISTRC-AB), Cotonou, Benin, 11–17 October 1998.
Dara, S. K., Lomer, C. J., and Hountondji, F. C. C. 2001b. Release of the entomopathogenic fungus, Neozygites floridana (Zygomycetes: Entomophthorales) for control of the cassava green mite Mononychellus tanajoa (Acari: Tetranychidae): An in vivo approach, pp. 559–562, in M. O. Akoroda and J. M. Ngeve (eds.). Proceedings of the 7th Triennial Symposium of the International Society for Tropical Root Crops—Africa Branch (ISTRC-AB), Cotonou, Benin, 11–17 October 1998.
I. Delalibera D. R. Sosa-Gomes SuffixJr G. J. De Moraes J. A. De Alencar W. Farias-Araujo (1992) ArticleTitleInfection of Mononychellus tanajoa (Acari: Tetranychidae) by the fungus Neozygites sp. (Entomophthorales) in Northeastern Brazil Fla. Entomol. 75 145–147
M. Dicke M. W. Sabelis (1988) ArticleTitleHow plants obtain predatory mites as bodyguards Neth. J. Zool. 38 148–165
M. Dicke M. W. Sabelis J. Takabayashi J. Bruin M. A. Posthumus (1990) ArticleTitlePlant strategies of manipulating predator–prey interactions through allelochemicals: Prospects for application in pest control J. Chem. Ecol. 16 3091–3118
S. L. Elliot M. W. Sabelis A. Janssen L. P. S. Van der Geest E. A. M. Beerling J. Fransen (2000) ArticleTitleCan plants use entomopathogens as bodyguards? Ecol. Lett. 3 228–235
S. L. Elliot G. J. De Moraes J. Mumford (2002) ArticleTitleImportance of ambient saturation deficits in an epizootic of the fungus Neozygites floridana in cassava green mites (Mononychellus tanajoa) Exp. Appl. Acarol. 27 11–25
G. W. Felton S. S. Duffey (1990) ArticleTitleInactivation of baculovirus by quinones formed in insect-damaged plant-tissues J. Chem. Ecol. 16 1221–1236
A. K. Fraser (1970) Growth restriction of pathogenic fungi on the leaf surface T. Preece (Eds) Ecology of Leaf Surface Micro-organisms Academic Press London 529–536
D. Gnanvossou R. Hanna M. Dicke J. S. Yaninek (2001) ArticleTitleAttraction of the predatory mites Typhlodromalus manihoti and Typhlodromalus aripo to cassava plants infested by cassava green mite Entomol. Exp. Appl. 101 291–298
D. Gnanvossou R. Hanna M. Dicke (2003) ArticleTitleInfochemical-mediated niche use by the predatory mites Typhlodromalus manihoti and T. aripo (Acari: Tetranychidae) J. Insect Behav. 16 523–535
P. S. Grewal R. Gaugler S. Selvan (1993a) ArticleTitleHost recognition of entomopathogenic nematodes: Behavioral response to contact with host feces J. Chem. Ecol. 19 1219–1231
P. S. Grewal R. Gaugler E. E. Lewis (1993b) ArticleTitleHost recognition behavior by entomopathogenic nematodes during contact with insect gut contents J. Parasitol. 79 495–503
P. S. Grewal E. E. Lewis R. Gaugler J. F. Campbell (1994) ArticleTitleHost finding behavior as a predictor of foraging strategy in entomopathogenic nematodes Parasitology 108 207–215
K. Hoover M. J. Stout S. A. Alaniz B. D. Hammock S. S. Duffey (1998) ArticleTitleInfluence of induced plant defenses in cotton and tomato on the efficacy of baculoviruses on noctuid larvae J. Chem. Ecol. 24 253–271
F. C. C. Hountondji C. J. Lomer R. Hanna A. J. Cherry S. K. Dara (2002) ArticleTitleField evaluation of Brazilian isolates of Neozygites floridana (Entomophthorales: Neozygitaceae) for the microbial control of the cassava green mite in Benin, West Africa Biocontrol Sci. Technol. 12 361–370
Hountondji, F. C. C., Hanna, R., and Cherry, A. 2003. Microbial control of cassava green mite by the fungus Neozygites tanajoae in Benin, pp. 122–125, in R. Hanna and M. Toko (eds.). Proceedings of the 3rd Inter-regional Meeting of the Africa-wide Cassava Green Mite Biocontrol Project. International Institute of Tropical Agriculture, Biological Control Centre for Africa, 20–22 February 2002, Cotonou, Republic of Benin.
A. Janssen C. D. Hofker A. R. Braun N. Mesa M. W. Sabelis A. C. Bellotti (1990) ArticleTitlePreselecting predatory mites for biological control: The use of an olfactometer Bull. Entomol. Res. 80 177–181
J. M. N. Kanagy H. K. Kaya (1996) ArticleTitleThe possible role of marigold roots and α-terthienyl in mediating host finding behaviour by steinernematid nematodes Nematologica 42 220–231
I. Klingen A. Hajek R. Meadow J. A. A. Renwick (2002) ArticleTitleEffect of brassicaceous plants on the survival and infectivity of insect pathogenic fungi BioControl 47 411–425
Z. Lei T. A. Rutherford J. M. Webster (1992) ArticleTitleHeterorhabditid behavior in the presence of the cabbage maggot, Delia radicum, and its host plants J. Nematol. 24 9–15
E. E. Lewis R. Gaugler R. Harrison (1992) ArticleTitleEntomopathogenic nematode host finding: Response to host contact cues by cruise and ambush foragers Parasitology 105 309–315
E. E. Lewis R. Gaugler R. Harrison (1993) ArticleTitleResponse of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues Can. J. Zool. 71 765–769
E. E. Lewis M. Ricci R. Gaugler (1996) ArticleTitleHost recognition behavior predicts host suitability in the entomopathogenic nematode Steinernema carpocapsae (Rhabditidae: Steinernematidae) Parasitology 113 573–579
MARGOLIES, D. C., SABELIS, M. W., and BOYER, J. E. JR. 1997. Response of a phytoseiid predator to herbivore-induced plant volatiles: Selection on attraction and effect on prey exploitation. J. Insect Behav. 10:695–709.
Oduor, G. I. 1995. Abiotic factors and epizootiology of Neozygites cf. floridana, a fungus pathogenic to the cassava green mite. Ph.D. thesis, University of Amsterdam, 101 p.
G. I. Oduor J. S. Yaninek L. P. S. Van der Geest G. J. De Moraes (1995) ArticleTitleSurvival of Neozygites cf. floridana (Zygomycetes: Entomophthorales) in mummified cassava green mites and the viability of its primary conidia Exp. Appl. Acarol. 19 479–488
G. I. Oduor G. J. De Moraes L. P. S. Van der Geest J. S. Yaninek (1996a) ArticleTitleProduction and germination of primary conidia of Neozygites floridana (Zygomycetes: Entomophthorales) under constant temperature, humidity, and light conditions J. Invertebr. Pathol. 68 213–222
G. I. Oduor J. S. Yaninek L. P. S. Van der Geest G. J. De Moraes (1996b) ArticleTitleGermination and viability of capilliconidia of Neozygites floridana (Zygomycetes: Entomophthorales) under constant temperatures, humidities and light conditions J. Invertebr. Pathol. 67 267–278
B. Papierok A. E. Hajek (1997) Entomophthorales L. Lacey (Eds) Manual of Techniques in Insect Pathology Academic Press San Diego 187–212
P. W. Price C. E. Bouton P. Gross B. A. McPheron J. N. Thompson A. E. Weis (1980) ArticleTitleInteractions among three trophic levels: Influence of plant on interactions between insect herbivores and natural enemies Ann. Rev. Ecolog. Syst. 11 41–65
Sabelis, M. W., Afman, B. P., and Slim, P. J. 1984. Location of distant spider-mite colonies by Phytoseiulus persimilis: Localisation and extraction of a kairomone, pp. 431–440, in D. A. Griffiths & C. E. Bowman (eds.). Acarology VI, Vol. 1.
SAS Institute. (1999). SAS System for Windows, Statistics, Release 6.12, version 8. SAS Institute, Cary, NC.
R. R. Sokal F. J. Rohlf (1997) Biometry: The Principles and Practice of Statistics in Biological Research EditionNumber3rd edn. Freeman and Company New York
T. C. J. Turlings J. H. Tumlinson W. J. Lewis (1990) ArticleTitleExploitation of herbivore-induced plant odors by host-seeking parasitic wasps Science 250 1251–1253
R. W. H. M. Van Tol T. C. Van der Sommen M. I. C. Boff J. Van Bezooijen M. W. Sabelis P. H. Smits (2001) ArticleTitlePlants protect their roots by alerting the enemies of grubs Ecol. Lett. 4 292–294
Y. Wang R. Gaugler (1998) ArticleTitleHost and penetration site location by entomopathogenic nematodes against Japanese beetle larvae J. Invertebr. Pathol. 72 313–318
Yaninek, J. S., De Moraes, G. J., and Markham, R. H. 1989. Handbook on the cassava green mite (Mononychellus tanajoa): A guide to its biology and procedures for implementing classical biological control. International Institute of Tropical Agriculture, Ibadan, 140 p.
J. S. Yaninek S. Saizonou A. Onzo I. Zannou D. Gnanvossou (1996) ArticleTitleSeasonal and habitat variability in the fungal pathogens: Neozygites cf. floridana and Hirsutella thompsonii, associated with cassava mites in Benin Biocontrol Sci. Technol. 6 23–33
Acknowledgments
We are grateful to Andy Cherry for supporting the realization of this study and Honoré Dossounon, Roland Bocco, and Kevin Yenou for their technical assistance. We also thank Martijn Egas, Michiel van Wijk, Alexis Onzo, and Désiré Gnanvossou for constructive comments on the manuscript. This research was supported by the International Institute of Tropical Agriculture with funds from Danish International Development Assistance (Danida) and the International Fund for Agricultural Development (IFAD), and by the University of Amsterdam.
This is IITA Ms. number IITA/04/JA/15.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hountondji, F.C.C., Sabelis, M.W., Hanna, R. et al. Herbivore-induced Plant Volatiles Trigger Sporulation in Entomopathogenic Fungi: The Case of Neozygites tanajoae Infecting the Cassava Green Mite. J Chem Ecol 31, 1003–1021 (2005). https://doi.org/10.1007/s10886-005-4244-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-005-4244-2