Abstract
Chemical footprints left behind by true bugs are perceived as contact kairomones by scelionid egg parasitoids. Female wasps encountering a contaminated artificial substrate display a characteristic arrestment posture, holding the body motionless and antennating the surface. In the system Nezara viridula (L.) and its egg parasitoid Trissolcus basalis (Wollaston), previous studies have shown that the kairomone mediating such behavior is part of N. viridula’s cuticular hydrocarbons (CHC) and furthermore that the wasp’s ability to discriminate host male and female footprints is mainly based on the presence/absence of nonadecane (nC19). In this study, the effect of epicuticular waxes of leaves of broad bean, Vicia faba, on wasp responses to footprints of N. viridula females were investigated. Approximately 20% of T. basalis females displayed an arrestment posture when released on the adaxial leaf surfaces of broad bean plants with intact wax layer and without host chemical contamination; whereas ∼70% of wasps displayed the arrestment posture when intact leaves were contaminated by host female footprints. Adaxial leaf surfaces of broad bean plants dewaxed with an aqueous solution of gum arabic and afterwards contaminated by N. viridula females induced arrestment responses in about 10% of female wasps; the same percentage of arrestment (10%) was observed when the wasps were released on leaves contaminated by host females and subsequently dewaxed. The side of the polymer film that was appressed to the leaf surface, peeled from the contaminated leaves, induced an arrestment posture in about 95% of observed wasps. Scanning electron microscopy (SEM) revealed that the epicuticular waxes occurred as a film densely crystallized as irregularly shaped platelets with spherical granules randomly distributed. These findings demonstrated that epicuticular waxes of broad bean leaves can mediate the foraging behavior of T. basalis females by absorbing contact kairomones of the host.
References
Andow DA, Prokrym DR (1990) Plant structural complexity and host-finding by a parasitoid. Oecologia 82:162–165
Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Bot J Linn Soc 126:237–260
Baker EA (1982) Chemistry and morphology of plant epicuticular waxes. In: Cutler DF, Alvin KL, Price CE (eds) The plant cuticle. Academic, London, pp 139–165
Borges M, Colazza S, Ramirez-Lucas P, Chauhan KR, Kramer M, Moraes MCB, Aldrich JR (2003) Kairomonal effect of walking traces from Euschistus heros (Heteroptera: Pentatomidae) on two strains of Telenomus podisi (Hymenoptera: Scelionidade). Physiol Entomol 28:349–355
Colazza S, Salerno G, Wajnberg E (1999) Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol Control 16:310–317
Colazza S, Aquila G, De Pasquale C, Peri E, Millar J (2007) The egg parasitoid Trissolcus basalis uses n-nonadecane, a cuticular hydrocarbon from its stink bug host Nezara viridula, to discriminate between female and male hosts. J Chem Ecol 33:1405–1420
Chang GC, Neufeld J, Durr D, Duetting PS, Eigenbrode SD (2004) Waxy bloom in peas influences the performance and behavior of Aphidius ervi, a parasitoid of the pea aphid. Entomol Exp Appl 110:257–265
Conti E, Salerno G, Bin F, Vinson SB (2004) The role of host semiochemicals in parasitoid specificity: a case study with Trissolcus brochymenae and Trissolcus simoni on pentatomid bugs. Biol Control 29:435–444
Dauphin G, Coquillard P, Colazza S, Peri E, Wajnberg E (2009) Host kairomone learning and foraging success in an egg parasitoid: a simulation model. Ecol Entomol 34:193–203
Eigenbrode SD (2004) The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthropod Struct Develop 33:91–102
Eigenbrode SD, Espelie KE (1995) Effects of plant epicuticular lipids on insect herbivores. Annu Rev Entomol 40:171–194
Eigenbrode SD, Jetter R (2002) Attachment to plant surface waxes by an insect predator. Integr Comp Biol 42:1091–1099
Eigenbrode SD, Kabalo NN (1999) Effects of Brassica oleracea waxblooms on predation and attachment by Hippodamia convergens. Entomol Exp Appl 91:125–130
Eigenbrode SD, White C, Rohde M (1998) Epicuticular wax phenotype of the wel mutation and its effect on pea aphid populations in the greenhouse and in the field. Pisum Genetics 29:13–17
Espelie KE, Bernays EA, Brown JJ (1991) Plant and insect cuticular lipids serve as behavioral cues for insects. Arch Insect Biochem Physiol 17:223–233
Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689
Gentry GL, Barbosa P (2006) Effects of leaf epicuticular wax on the movement, foraging behavior, and attack efficacy of Diaeretiella rapae. Entomol Exp Appl 121:115–122
Godfray HCJ (1994) Parasitoids. Behavioral and evolutionary ecology. Princeton University Press, Princeton, New Jersey
Griffiths DW, Robertson GW, Shepard T, Ramsay G (1999) Epicuticular waxes and volatiles from faba bean (Vicia Faba) flowers. Phytochemistry 52:607–612
Jetter R, Schäffer S (2001) Chemical composition of the Prunus laurocerasus leaf surface. Dynamic changes of the epicuticular wax film during leaf development. Plant Physiol 126:1725–1737
Koch K, Ensikat HJ (2008) The hydrophobic coatings of plant surfaces: epicuticular wax crystals and their morphologies, crystallinity and molecular self-assembly. Micron 39:759–772
Kolattukudy PE, Walton TJ (1972) Structure and biosynthesis of the hydroxyl fatty acids of cutin in Vicia faba leaves. Biochemistry 11:1897–1907
Lo Giudice D (2009) Contact chemo-orientation in insect parasitoids: the case study of mate-finding in Metaphycus luteolus and host-finding in Trissolcus basalis. PhD dissertation. University of Palermo, Palermo
Mc Auslane HJ, Simmons AM, Jackson DM (2000) Parasitism of Bemisia argentifolii on collard with reduced or normal leaf wax. Flo Entomol 83:428–437
Müller C, Hilker M (2001) Host finding and oviposition behavior in a chrysomelid specialist—the importance of host plant surface waxes. J Chem Ecol 27:985–994
Müller C, Riederer M (2005) Plant surface properties in chemical ecology. J Chem Ecol 31:2621–2651
Nakashima Y, Birkett MA, Pye BJ, Pickett JA, Powell W (2004) The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi. J Chem Ecol 30:1103–1116
Noldus LPJJ, Potting RPJ, Barendregt HE (1991) Moth sex-pheromone adsorption to leaf surface—bridge in time for chemical spies. Physiol Entomol 16:329–344
Obrycki JJ (1986) The influence of foliar pubescence on entomophagous species. In: Boethel DJ, Eikenbarry RD (eds) Interactions of plant resistance and parasitoids and predators of insects. Wiley, New York, 200 pp
Pathan AK, Bond J, Gaskin RE (2008) Sample preparation for scanning electron microscopy of plant surfaces—horses for courses. Micron 39:1049–1061
Peri E, Sole MA, Wajnberg E, Colazza S (2006) Effect of host kairomones and oviposition experience on the arrestment behaviour of an egg parasitoid. J Exp Biol 209:3629–3635
Powell W (1999) Parasitoid hosts, pp. 405–427. In: Hardie J, Minks AK (eds) Pheromones of non-lepidopteran insects associated with agricultural plants. CABI, Wallingford (UK), pp 405–427
Powell G, Maniar SP, Picket JA, Hardie J (1999) Aphid responses to non-host epicuticular lipids. Entomol Exp Appl 91:115–123
Quicke DLJ (1997) Parasitic wasps. Chapman & Hall, London
Romeis J, Shanower TG, Zebitz CPW (2003) Physical and chemical plant characters inhibiting the searching behaviour of Trichogramma chilonis. Entomol Exp Appl 87:275–284
Rostás M, Wölfling M (2009) Caterpillar footprints as host location kairomones for Cotesia marginiventris: persistence and chemical nature. J Chem Ecol 35:20–27
Rostás M, Ruf D, Zabka V, Hildebrandt U (2008) Plant surface wax affects parasitoid’s response to host footprints. Naturwissenschaften 95:997–1002
Rutledge CE, Robinson AP, Eigenbrode SD (2003) Effects of a simple plant mutation on the arthropod community and the impacts of predators on a principle insect herbivore. Oecologia 135:39–50
Rutledge CE, Eigenbrode SD, Ding H (2008) A plant surface mutation mediates predator interference among ladybird larvae. Ecol Entomol 33:464–472
Salerno G, Conti E, Peri E, Colazza S, Bin F (2006) Kairomone involvement in the host specificity of the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Eur J Entomol 103:311–318
Siegel S, Castellan NJJr (1988) Nonparametric statistics for behavioral sciences. McGraw-Hill Book Company
Strand MR (1986) The physiological interactions of parasitoids with their hosts and their influence on reproductive strategies. In: Waage JK, Greathead DJ (eds) Insect parasitoids 13th Symposium of the Royal Entomological Society of London, 18–19 September 1985, London. Academic, London, pp 97–136
Todd JW, Herzog DC (1980) Sampling phytophagous Pentatomidae on soybean, p. 438–478. In: Kogan M, Herzog DC (eds) Sampling methods in soybean entomology. Springer-Verlag, New York, 587 p
Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172
Vinson SB (1985) The behaviour of parasitoids. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology. Pergamon, New York, pp 417–469
Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–97
Wen M, Buschhaus C, Jetter R (2006) Nanotubules on plant surfaces: Chemical composition of epicuticular wax crystals on needles of Taxus baccata L. Phytochemistry 67:1808–1817
White C, Eigenbrode SD (2000) Effects of surface wax variation in Pisum sativum L. on herbivorous and entomophagous insects in the field. Environ Entomol 29:776–780
Acknowledgements
We thank Jocelyn Millar and Sanford Eigenbrode for critically reading and commenting on an earlier version of this manuscript. SEM investigations have been done at the Department of “Ingegneria Chimica dei Processi e dei Materiali—University of Palermo,” under the technical assistance of Dr. Paolo Guerra. This work is part of the European Science Foundation (ESF)—Behavioural Ecology of Insect Parasitoids (BEPAR) scientific program. Funding for this work was provided by “Progetti di ricerca di interesse nazionale—cofinanziamento 2007” entitled “Enhancing foraging behaviour of insect egg parasitoids: the role of the volatile organic compounds and the epicuticular layers of the plants,” Chairperson Prof. Stefano Colazza.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Colazza, S., Lo Bue, M., Lo Giudice, D. et al. The response of Trissolcus basalis to footprint contact kairomones from Nezara viridula females is mediated by leaf epicuticular waxes. Naturwissenschaften 96, 975–981 (2009). https://doi.org/10.1007/s00114-009-0548-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-009-0548-3