Abstract
We analyzed the behavioral interactions between two species of honeydew-collecting ants (Lasius niger, Myrmica laevinodis) and foraging females of four species of aphid hyperparasitoids (Aphidencyrtus aphidivorus, Dendrocerus carpenteri, Pachyneuron aphidis, Asaphes vulgaris) usingAphis fabae ssp.cirsiiacanthoidis andLysiphlebus cardui on thistles as aphid and primary parasitoid, respectively. The observed interaction patterns and foraging parameters varied within hyperparasitoid species and revealed different strategies based upon behavioral and morphological constraints.D. carpenteri generally tried to avoid ant encounters. This avoidance strategy was successful in interactions withM. laevinodis but failed when encountering the more aggressiveL. niger, which caused about 26% adult mortality. In contrast,A. aphidivorus, P. aphidis, andA. vulgaris possess jumping ability and were hardly exposed to mortality risks. The escape reaction “jump off” was used as soon as ants made physical contact with foraging females. While the flight strategy ofP. aphidis is connected with cryptic movement patterns without avoidance behavior,A. aphidivorus first avoided ants and jumped off only as a last resort. Similar patterns, but less expressive, are displayed byA. vulgaris. We suggest that these different strategies are responsible for different foraging success in ant-attended resources in field.
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Attygalle, A. B., McCormick, K. D., Blankespoor, C. L., Eisner, T., and Meinwald, J. (1993). Azamacrolides: A family of alkaloids from the pupal defense secretion of a ladybird beetle (Epilachna varivestis).Proc. Natl. Acad. Sci. USA 90: 5204–5208.
Ayre, G. L. (1962).Pseudometagea schwarzii (Ashm.) (Eucharitidae: Hymenoptera), a parasite ofLasius neoniger Emery (Formicidae: Hymenoptera).Can. J. Zool. 40: 157–164.
Bach, C. E. (1991). Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis) and plants (Pluchea indica).Oecologia 87: 233–239.
Banks, C. J. (1962). Effect of the ant,Lasius niger, on insects preying on small populations ofAphis fabae Scop. on bean plants.Ann. Appl. Biol. 50: 669–679.
Bartlett, B. R. (1961). The influence of ants upon parasites, predators and scale insects.Ann. Entomol. Soc. Am. 54: 543–551.
Bradley, G. A. (1973). Effect ofFormica obscuripes (Hymenoptera: Formicidae) on the predatorprey relationship betweenHyperaspis congressis (Coleoptera: Coccinellidae) andToumeyella numismaticum (Homoptera: Coccidae).Can. Entomol. 105: 1113–1118.
Bristow, C. (1984). Differential benefits from ant-attendance to two species of Homoptera on New York ironweed.J. Anim. Ecol. 53: 715–726.
Buckley, R. (1987). Interactions involving plants, homoptera, and ants.Annu. Rev. Ecol. Syst. 18: 111–135.
Cudjoe, J. H., Neuenschwander, P., and Copland, M. J. W. (1993). Interference by ants in biological control of the cassava mealybugPhenacoccus manihoti (Hemiptera: Pseudococcidae) in Ghana.Bull. Entomol. Res. 83: 15–22.
Dettner, K., and Liepert, C. (1994). Chemical mimicry and camouflage.Annu. Rev. Entomol. 39: 129–154.
Eisner, T., Hicks, K., Eisner, M., and Robson, D. S. (1978). “Wolf-in-sheep's-clothing” strategy of a predaceous insect larva.Science 199: 790–794.
Eisner, T., Goetz, M., Aneshansley, D., Fersting-Arnold, G., and Meinwald, J. (1986). Defensive alkaloid in blood of Mexican bean beetle (Epilachna varivestis).Experientia 42: 204–207.
Hölldobler, B., and Wilson, E. O. (1990).The Ants, Springer Verlag, Berlin, Heidelberg, New York.
Hübner, G. (1994).Interaktionen zwischen fouragierenden Blattlaushyperparasitoiden und honigtausammelnden Ameisen: Verhaltensstrategien in ameisenbelaufenen Ressourcen. Diploma thesis, University of Bayreuth.
Jiggins, C., Majerus, M. E. N., and Gough, U. (1993). Ant defence of colonies ofAphis fabae Scopoli (Hemiptera: Aphididae), against predation by ladybirds.Br. J. Entomol. Nat. Hist. 6: 129–137.
Kamijo, K., and Takada, H. (1983). A newEuneura species hyperparasitic onStomaphis aphids and a note on the genusGygaxia Delucchi.Akitu 55: 1–8.
Kanuck, M. J., and Sullivan, D. J. (1992). Ovipositional behavior and larval developement ofAphidencyrtus aphidivorus (Hymenoptera: Encyrtidae), an aphid hyperparasitoid.J. N.Y. Entomol. Soc. 100: 527–532.
Larsen, K. J., Heady, S. E., and Nault, L. R. (1992). Influence of ants (Hymenoptera: Formicidae) on honeydew excretion and escape behaviors in a myrmecophile,Dalbulus quinquenotatus (Homoptera: Cicadellidae), and its congeners.J. Insect Behav. 5: 109–122.
Liepert, C., and Dettner, K. (1993). Recognition of aphid parasitoids by honeydew-collecting ants: The role of cuticular lipids in a chemical mimicry system.J. Chem. Ecol. 19: 2143–2153.
Mackauer, M., and Völkl, W. (1993): Regulation of aphid populations by aphidiid wasps: Does parasitoid foraging behaviour of hyperparasitism limit impact?Oecologia 94: 339–350.
Novak, H. (1994). The influence of ant-attendance on larval parasitism in Hawthorn psyllids (Homoptera: Psyllidae).Oecologia 99: 72–78.
Pierce, N. E., and Easteal, S. (1986). The selective advantage of attendant ants for the larvae of a lycaenid butterfly,Glaucopsyche lygdamus.J. Anim. Ecol. 55: 451–462.
Pierce, N. E., and Mead, P. S. (1981). Parasitoids as selective agents in the symbiosis between lycaenid butterfly caterpillars and ants.Science 211: 1185–1187.
Sudd, J. H. (1987) Ant aphid mutualism. In Minks, A. K., and Harrewijn, P. (eds.),Aphids—Their Biology, Natural Enemies and Control.World Crop Pests, Vol. 2A, Elsevier, Amsterdam, pp. 355–365.
Sullivan, D. J. (1987). Insect hyperparasitism.Annu. Rev. Entomol. 32: 49–70.
Sullivan, D. J. (1988). Hyperparasites. In Minks, A. K., and Harrewijn, P. (eds.),Aphids—Their Biology, Natural Enemies and Control.World Crop Pests, Vol. 2B, Elsevier, Amsterdam, pp. 189–203.
Takada, H., and Hashimoto, Y. (1985). Association of the root aphid parasitoidsAclitus sappaphis andParalipsis eikoae (Hymenoptera, Aphidiidae) with the aphid-attending antsPheidole fervida andLasius niger (Hymenoptera, Formicidae).Kontyu 53: 150–160.
Tursch, B., Daloze, D., Dupont, M., Pasteels, J. M., and Tricot, M. C. (1971). A defensive alkaloid in a carnivorous beetle.Experientia 27: 1380–1381.
Vander Meer, R. K., Jouvenaz, D. P., and Wojcik, D. P. (1989). Chemical mimicry in a parasitoid (Hymenoptera: Eucharitidae) of fire ants (Hymenoptera: Formicidae).J. Chem. Ecol. 15: 2247–2261.
Vinson, S. B., and Scarborough, T. A. (1991). Interactions betweenSolenopsis invicta (Hymenoptera: Formicidae),Rhopalosiphum maidis (Homoptera: Aphididae) and the parasitoidLysiphlebus testaceipes Cresson (Hymenoptera: Aphidiidae).Ann. Entomol. Soc. Am. 84: 158–164.
Völkl, W. (1990).Fortpflanzungsstrategien bei Blattlausparasitoiden (Hymenoptera, Aphidiidae): Konsequenzen ihrer Interaktionen mit Wirten und Ameisen, Ph.D. thesis, University of Bayreuth, Bayreuth.
Völkl, W. (1992). Aphids or their parasitoids: Who actually benefits from ant-attendance?J. Anim. Ecol. 61: 273–281.
Völkl, W. (1995). Behavioral and morphological adaptations of the coccinellidPlatynaspis luteorubra for exploiting ant-attended resources.J. Insect Behav. 8: 653–670.
Völkl, W., and Mackauer, M. (1993). Interactions between ants attendingAphis fabae ssp. cirsiiacanthoidis on thistles and foraging parasitoid wasps.J. Insect Behav. 6: 301–312.
Völkl, W., Hübner, G., and Dettner, K. (1994). Interactions betweenAlloxysta brevis (Hymenoptera, Cynipoidea, Alloxystidae) and honeydew collecting ants: How an aphid hyperparasitoid overcomes ant aggression by chemical defense.J. Chem. Ecol. 20: 2621–2635.
Way, M. J. (1963). Mutualism between ants and honeydew-producing homptera.Annu. Rev. Entomol. 8: 307–344.
Wellenstein, G. (1930). Beiträge zur Systematik und Biologie der Rindenläuse (Lachnidae CB.).Z. Morph. Ökol. Tiere 17: 737–767.
Wojcik, D. P. (1989): Behavioral interactions between ants and their parasites.Fla. Entomol. 72: 43–51.
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Hübner, G., Völkl, W. Behavioral strategies of aphid hyperparasitoids to escape aggression by honeydew-collecting ants. J Insect Behav 9, 143–157 (1996). https://doi.org/10.1007/BF02213729
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DOI: https://doi.org/10.1007/BF02213729