The third trophic level of plant defence: neotropical social wasps' use of odours of freshly damaged leaves when hunting

Raw, Anthony

doi:10.1590/S0101-81751998000400025

Abstract

An important aspect of the hunting strategy of neotropical social wasps (Hymenoptera: Vespidae) is where they hunt. Three species used two behavioural components in their selection of a place to search for prey. The wasps uti lizcd the odour of freshly damaged leaves as cues (which could be synomones) to select which leaves to inspect and also they remembered a place to which they were strongly attracted to hunt recently and returned there. Polybia ignobilis (Haliday, 1836) and Polistes satan Bequaert, 1940 hunted on a lawn of Digitaria diversinervis Stapf immediately after it was mown in significantly larger numbers than at other times. P. ignobilis and Polistes versicolor (Olivier, 1791) hunted in significantly greater numbers on freshly cut leaves of passion vine (Passiflora edulis Sims) than on uncut leaves. Sometimes wasps inspected cards rubbed with freshly crushed leaves of P. edulis, but not control cards. Preliminary data suggest that several other species of social wasps around Brasilia hunt in a similar manner on native and exotic plants. Apparently the production of ephemeral odours by freshly cut leaves attract generalist insectivorous predators which perceive these scents and the social wasps investigated are members of the third trophic level of the plants' defence against attacks by herbivores. Available information suggests a difference between the behaviour of generalists and that of specialist arthropod predators which arc attracted to the odour emitted after their particular prey have damaged the leaves.

Polybia; Polistes; wasps; plant defence; neotropics

The third trophic level of plant defence: neotropical social wasps' use of odours of freshly damaged leaves when hunting

Anthony Raw

Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz. Rodovia Ilhéus - Itabuna Km 16. 70910-900 Ilhéus, Bahia, Brasil

ABSTRACT

An important aspect of the hunting strategy of neotropical social wasps (Hymenoptera: Vespidae) is where they hunt. Three species used two behavioural components in their selection of a place to search for prey. The wasps uti lizcd the odour of freshly damaged leaves as cues (which could be synomones) to select which leaves to inspect and also they remembered a place to which they were strongly attracted to hunt recently and returned there. Polybia ignobilis (Haliday, 1836) and Polistes satan Bequaert, 1940 hunted on a lawn of Digitaria diversinervis Stapf immediately after it was mown in significantly larger numbers than at other times. P. ignobilis and Polistes versicolor (Olivier, 1791) hunted in significantly greater numbers on freshly cut leaves of passion vine (Passiflora edulis Sims) than on uncut leaves. Sometimes wasps inspected cards rubbed with freshly crushed leaves of P. edulis, but not control cards. Preliminary data suggest that several other species of social wasps around Brasilia hunt in a similar manner on native and exotic plants. Apparently the production of ephemeral odours by freshly cut leaves attract generalist insectivorous predators which perceive these scents and the social wasps investigated are members of the third trophic level of the plants' defence against attacks by herbivores. Available information suggests a difference between the behaviour of generalists and that of specialist arthropod predators which arc attracted to the odour emitted after their particular prey have damaged the leaves.

Key words: Polybia, Polistes, wasps, plant defence, neotropics.

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ACKNOWLEDGEMENTS. The present study was made possible through the understanding of a number of friends who, against their better judgement, postponed the destruction of colonies of aggressive wasps in their gardens until I had finished collecting the data. The late Dr. David Ross Gifford, University of Brasilia; Dr. J.a. Ratter, Royal Botanic Garden, Edinburgh and Dr. Vitor 0. Becker, Ministry of Agriculture (EMBRAPA, Planaltina, Distrito Federal, Brazil) provided me with the data on numbers of species of butterflies, moths and plants in the cerrados. The constructive comments of Dr. John D. Hay, Departamento de Ecologia, Universidade de Brasília have greatly improved the manuscript.

Recebido em 15.V.1997; aceito em 01.XII.1998.

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BROWN, K.S. JR.; J.R. TRIGO; R.S. FRANCINI; A.B. BARROS DE MORAIS & P.C. MOTTA. 1991. Aposematic insects on toxic host plants: coevolution, colonization, and chemical emancipation, p.375-401. In: P.W. Price; G.W. Fernandes; T.M. Lewinsohn & W.W. Benson (Eds). Plant-Animal Interactions. Evolutionary Ecology in Tropical and Temperate Regions New York, John Wiley & Sons.
CARROLL, CR. & D.H. JANZEN. 1973. Ecology of foraging by ants. Ann. Rev. Ecol. Syst.4: 231-257.
COLEY, P.D. 1988. Effects of plant growth rate and leaf lifetime on the amount of anti-herbivore defense. Oecologia 74: 531-536.
DLCKE, M.; T.A. VAN BECK; M.A. POSTHUMUS; N. BEN DOM; H. VAN BOKHOVEN & A.E. DE GROOF. 1990. Isolation and identification of volatile kairomone that affects acarine predator-prey interactions: Involvement of host plant in its production. Jour. Chem. Ecol. 16: 381-396.
DICKE. M. & M.W. SABELIS. 1988. Infochemical terminology: should it be based on cost-benefit analysis rather than origin of compounds? Functional Ecology 2: 131-138.
EVANS, H.F. 1976. The searching behaviour of Anthocoris confusas (Reuter) in relation to prey density and plant surface topography. Ecol. Entom. 1: 163-169.
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JEANNE, R.L. 1972. Social biology of the neotropical social wasp Mischocyttarus drewseni. Bul. Mus. Comp. Zool. Harvard Univ. 144: 63-150.
______. 1975. Behavior during swarm movement in Stelopolybia areata (Hymenoptera: Vespidae). Psyche 82: 259-264.
JEANNE, R.L.; J.H. HUNT & M.G. KEEPING. 1995. Foraging in social wasps: Agelaia lacks recruitment to food (Hymenoptera: Vespidae). Jour. Kansas Entomol. Soc. 68: 279-289.
LOYOLA, R. & G.W. FERNANDES. 1993. Herbivoria em Kielmeyera coriacea (Guttiferae): efeitos da idade da planta, desenvolvimento e aspectos qualitativos de folhas. Rev. Brasil. Biol., Rio de Janeiro, 53: 295-304.
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MACHADO, V.L.L.; N. GOBBI & V.V. ALVES JUNIOR. 1988. Material capturado e utilizado na alimentação de Polybia (Trichothorax) sericea (Olivier, 1791) (Hymenoptera, Vespidae). Revta bras. Ent. 5: 261-266.
MACHADO, V.L.L.; N. GOBBI & D. SIMÕES. 1987. Material capturado e utilizado na alimentação de Stelopolybiapallipes (Olivier, 1791) (Hymenoptera - Vespidae). An. Soc. Entomol. Brasil 16: 73-79.
MARQUIS, R.J. 1984. Leaf herbivores decrease fitness of a tropical plant. Science 226: 537-539.
MARQUIS, R.J.; I.R. DINIZ & H.C. MORAIS. 1993. Interspecific patterns in folivory and pathogen attack for Brazilian cerrado trees. Bul. Ecol. Soc. America 74 (2) (suppl.): 344.
MARQUIS, R.J. & C.J. WHELAN. 1994. Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75: 2007-2014.
MONTEITH, L.G. 1955. Host preferences of Drino bohemica Mesn. with particular reference to olfactory responses. Canad. Entomol. 87: 509-530.
MICHENER, CD. 1974. The Social Behavior of Bees: A Comparative Study. Cambridge, Belknap Press, University of Harvard, 404p.
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MORAIS, H.C; I.R. DINIZ & L. BAUMGARTEN. 1995. Padrões de produção de folhas e sua utilização por larvas de Lepidoptera em um cerrado de Brasília. Rev. Brasil. Biol. 18: 163-170.
NASCIMENTO, M.T. & J.D. HAY. 1993. Intraspecifíc variation in herbivory on Metrodorea pubescens (Rutaceae) in two forest types in Central Brazil. Rev. Bras. Biologia 53: 143-153.
NAUMANN, M.G. 1975. Swarming behavior: evidence for communication in social wasps. Science 189: 642-644.
ODELL, T.M. & P.A. Godwin. 1984. Host selection by Blephiripa pratensis (Meigen), a tachinid parasite of the gypsy moth, Lymantria dispar L. Jour. Chemical Ecol. 10:311-320.
OLLASON, J.G. 1980. Learning to forage - optimally ? Theoret. Pop. Biol. 18: 44-56.
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PRICE, P.W. 1986. Ecological aspects of host plant resistance and biological control. Interactions among three trophic levels, p. 11-30. In: D.J. Boethel & R.D. Etkenbarry (Eds). Interactions of Plant Resistance and Parasitoids and Predators of Insects Chichester, Ellis Horwood.
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RAW, A. 1988. Social wasps (Hymenoptera, Vespidae) and insect pests of crops of the Surui and Cinta Larga indians in Rondônia, Brazil. Entomologist 107: 104-109.
______. 1992. The forest-savanna boundary and habitat selection by Brazilian social wasps (Hymenoptera: Vespidae), p.499-511. In: P.A. Furley; J.A. Ratter & J. Proctor (Eds). The Nature and Dynamics of the Forest-Savanna Boundary London, Chapman & Hall.
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Publication Dates

Publication in this collection
06 July 2009
Date of issue
Dec 1998

History

Accepted
01 Dec 1998
Received
15 May 1997

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] AIDE, T.M. & E.C. LONDONO. 1989. The effects of leaf expansion on the growth and survivorship of a lepidopteran herbivore. Oikos 55: 66-70.

[2] BROWER, L.P. 1969. Ecological chemistry. Scient. Amer. 220: 22-29.

[3] BROWN, K.S. JR.; J.R. TRIGO; R.S. FRANCINI; A.B. BARROS DE MORAIS & P.C. MOTTA. 1991. Aposematic insects on toxic host plants: coevolution, colonization, and chemical emancipation, p.375-401. In: P.W. Price; G.W. Fernandes; T.M. Lewinsohn & W.W. Benson (Eds). Plant-Animal Interactions. Evolutionary Ecology in Tropical and Temperate Regions New York, John Wiley & Sons.

[4] CARROLL, CR. & D.H. JANZEN. 1973. Ecology of foraging by ants. Ann. Rev. Ecol. Syst.4: 231-257.

[5] COLEY, P.D. 1988. Effects of plant growth rate and leaf lifetime on the amount of anti-herbivore defense. Oecologia 74: 531-536.

[6] DLCKE, M.; T.A. VAN BECK; M.A. POSTHUMUS; N. BEN DOM; H. VAN BOKHOVEN & A.E. DE GROOF. 1990. Isolation and identification of volatile kairomone that affects acarine predator-prey interactions: Involvement of host plant in its production. Jour. Chem. Ecol. 16: 381-396.

[7] DICKE. M. & M.W. SABELIS. 1988. Infochemical terminology: should it be based on cost-benefit analysis rather than origin of compounds? Functional Ecology 2: 131-138.

[8] EVANS, H.F. 1976. The searching behaviour of Anthocoris confusas (Reuter) in relation to prey density and plant surface topography. Ecol. Entom. 1: 163-169.

[9] EVANS, H.E. & M.J. West-Eberhard. 1973. The Wasps. Ann Arbor, University of Michigan, 265p.

[10] FAETH, S.H. 1985. Host leaf selection by leafminers: interactions among three trophic levels. Ecology 66: 870-875.

[11] ______. 1994. Induced plant responses: effects on parasitoids and other natural enemies of phytophagous insects, p.245-260. In: B.A. HAWKINS & W. Sheehan (Eds). Parasitoid Community Ecology. Oxford, Oxford University Press.

[12] FRANKIE, G.W.; P.A. OPLER & K.S. BAWA. 1976. Foraging behavior of solitary bees: implications for outcrossing of a neotropical forest tree species. Jour. Ecol. 64: 1049-1057.

[13] GOBBI, N. & V.L.L. MACHADO. 1985. Material capturado e utilizado na alimentação de Polybia (Myrapetra) paulista Ihering, 1896 (Hymenoptera - Vespidae). An. Soc. Entomol. Brasil 14: 189-195.

[14] ______. 1986. Material capturado e utilizado na alimentação de Polybia (Trichothorax) ignobilis (Haliday, 1836) (Hymenoptera, Vespidae). Anais Soc. Entom. Brasil 15: 117-125.

[15] GOBBI, N.; V.L.L. MACHADO & J.A. TAVARES FILHO. 1984. Sazonalidade das presas utilizadas na alimentação de Polybia oceidentalis (Olivier, 1891) (Hym., Vespidae). An. Soc. Entomol. Brasil 13: 63-69.

[16] HASSELL, M.P. 1968. The behavioural response of a tachinid fly [Cyzenis albicans (Fall.)] to its host, the winter moth [Operophtera brumata (L)]. Jour. Anim. Ecol. 37: 627-639.

[17] HEINRICH, B. 1979. Foraging strategies of caterpillars: leaf damage and possible predator avoidance strategics. Oecologia 42: 325-347.

[18] ______. 1993. How avian predators constrain caterpillar foraging, p.224-247. In N.E. Stamp & T.M. Casey (Eds). Caterpillars; Ecological and Evolutionary Constraints on Foraging. New York, Chapman & Hall.

[19] HEINRICH, B. & S.L. COLLINS. 1983. Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64: 592-602.

[20] JANZEN, D.H. 1993. Caterpillar seasonality in a Costa Rican dry forest, p.448-477. In: N.E. Stamp & T.M. Casey (Eds). Caterpillars; Ecological and Evolutionary Constraints on Foraging. New York, Chapman & Hall.

[21] JANZEN, D.H. & P.G. WATERMAN. 1984. A seasonal census of phenolics, fibre and alkaloids in foliage of forest trees in Costa Rica: Some factors influencing their distribution and relation to host selection by Sphingidae. Jour. Linnean Soc. 21: 439-454.

[22] JEANNE, R.L. 1972. Social biology of the neotropical social wasp Mischocyttarus drewseni. Bul. Mus. Comp. Zool. Harvard Univ. 144: 63-150.

[23] ______. 1975. Behavior during swarm movement in Stelopolybia areata (Hymenoptera: Vespidae). Psyche 82: 259-264.

[24] JEANNE, R.L.; J.H. HUNT & M.G. KEEPING. 1995. Foraging in social wasps: Agelaia lacks recruitment to food (Hymenoptera: Vespidae). Jour. Kansas Entomol. Soc. 68: 279-289.

[25] LOYOLA, R. & G.W. FERNANDES. 1993. Herbivoria em Kielmeyera coriacea (Guttiferae): efeitos da idade da planta, desenvolvimento e aspectos qualitativos de folhas. Rev. Brasil. Biol., Rio de Janeiro, 53: 295-304.

[26] MACHADO, V.L.L. & N. GOBBI. 1987. Prey items utilized by some neotropical Polybia (Hymenoptera - Vespidae), p.543. In: J. Eder & H. Rembold (Eds). Chemistry and Biology of Social Insects. München Verlag J. Pepermy.

[27] MACHADO, V.L.L.; N. GOBBI & V.V. ALVES JUNIOR. 1988. Material capturado e utilizado na alimentação de Polybia (Trichothorax) sericea (Olivier, 1791) (Hymenoptera, Vespidae). Revta bras. Ent. 5: 261-266.

[28] MACHADO, V.L.L.; N. GOBBI & D. SIMÕES. 1987. Material capturado e utilizado na alimentação de Stelopolybiapallipes (Olivier, 1791) (Hymenoptera - Vespidae). An. Soc. Entomol. Brasil 16: 73-79.

[29] MARQUIS, R.J. 1984. Leaf herbivores decrease fitness of a tropical plant. Science 226: 537-539.

[30] MARQUIS, R.J.; I.R. DINIZ & H.C. MORAIS. 1993. Interspecific patterns in folivory and pathogen attack for Brazilian cerrado trees. Bul. Ecol. Soc. America 74 (2) (suppl.): 344.

[31] MARQUIS, R.J. & C.J. WHELAN. 1994. Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75: 2007-2014.

[32] MONTEITH, L.G. 1955. Host preferences of Drino bohemica Mesn. with particular reference to olfactory responses. Canad. Entomol. 87: 509-530.

[33] MICHENER, CD. 1974. The Social Behavior of Bees: A Comparative Study. Cambridge, Belknap Press, University of Harvard, 404p.

[34] MONTILLOR, C.B. & E.A. BERNAYS. 1993. Invertebrate predators and caterpillar foraging, p. 170-202. In: N.E. Stamp & T.M. Casey (Eds). Caterpillars; Ecological and Evolutionary Constraints on Foraging. New York, Chapman & Hall, 587p.

[35] MORAIS, H.C; I.R. DINIZ & L. BAUMGARTEN. 1995. Padrões de produção de folhas e sua utilização por larvas de Lepidoptera em um cerrado de Brasília. Rev. Brasil. Biol. 18: 163-170.

[36] NASCIMENTO, M.T. & J.D. HAY. 1993. Intraspecifíc variation in herbivory on Metrodorea pubescens (Rutaceae) in two forest types in Central Brazil. Rev. Bras. Biologia 53: 143-153.

[37] NAUMANN, M.G. 1975. Swarming behavior: evidence for communication in social wasps. Science 189: 642-644.

[38] ODELL, T.M. & P.A. Godwin. 1984. Host selection by Blephiripa pratensis (Meigen), a tachinid parasite of the gypsy moth, Lymantria dispar L. Jour. Chemical Ecol. 10:311-320.

[39] OLLASON, J.G. 1980. Learning to forage - optimally ? Theoret. Pop. Biol. 18: 44-56.

[40] O'TOOLE, C. & A. RAW. 1991. Bees of the World. Blandford Press, 192p.

[41] PRICE, P.W. 1986. Ecological aspects of host plant resistance and biological control. Interactions among three trophic levels, p. 11-30. In: D.J. Boethel & R.D. Etkenbarry (Eds). Interactions of Plant Resistance and Parasitoids and Predators of Insects Chichester, Ellis Horwood.

[42] Price, P.W.; C.E. Bouton; P. Gross; B.A. McPherson; J.N. Thompson & A.E. WEIS. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Ann. Rev. Ecol. Syst. 11:41-65.

[43] PRICE, P.W.; I.R. DINIZ; H.C. MORAIS & E.S.A. MARQUES. 1995. The abundance of insect herbivore species in the tropics: The high local richness of rare species. Biotropica 27: 468-478.

[44] RAVERET-RICHTER, M. 1990. Hunting social wasp interactions: influence of prey size, arrival order, and wasp species. Ecology 71: 1018-1030.

[45] RAVERET-RICHTER, M.A. & R.L. JEANNE. 1985. Predatory behavior of Polybia sericea (Olivier), a tropical social wasp (Hymenoptera: Vespidae). Behav. Ecol. Sociobiol. 16: 165-170.

[46] RAW, A. 1988. Social wasps (Hymenoptera, Vespidae) and insect pests of crops of the Surui and Cinta Larga indians in Rondônia, Brazil. Entomologist 107: 104-109.

[47] ______. 1992. The forest-savanna boundary and habitat selection by Brazilian social wasps (Hymenoptera: Vespidae), p.499-511. In: P.A. Furley; J.A. Ratter & J. Proctor (Eds). The Nature and Dynamics of the Forest-Savanna Boundary London, Chapman & Hall.

[48] ______. 1998a. Social wasps (Hymenoptera, Vespidae) of the Ilha de Maracá, p.311-325. In: J.A. Ratter & W. Milliken (Eds). Maracá. The Biodiversity and Environment of an Amazonian Rainforest Chichester, John Wiley & Sons, 508p.

[49] ______. 1998b. Population densities and biomass of neotropical social wasps (Hymenoptera, Vespidae) related to colony size, hunting range and wasp size. Revta bras. Zool. 15 (3): 815-822.

[50] RAW, A. & J.D. HAY. 1985. Fire and other factors affecting a population of Simaruba amara in "cerradão" near Brasilia, Brazil. Rev. Brasil. Bot. 8: 101-107.

[51] REID, CD. & R.L. LAMPMAN. 1989. Olfactory responses of Onus insidiosus (Hemiptera: Anthocoridae) to volatiles in corn silks. Jour. Chem. Ecol. 15: 1109-1115.

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