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OVIPOSITION BEHAVIOUR OF APHIDIINE WASPS (HYMENOPTERA: BRACONIDAE, APHIDIINAE): MORPHOLOGICAL ADAPTATIONS AND EVOLUTIONARY TRENDS

Published online by Cambridge University Press:  31 May 2012

Wolfgang Völkl  and
Manfred Mackauer
Wolfgang Völkl
Affiliation:
Lehrstuhl für Tierökologie I, Universität Bayreuth, D-95440 Bayreuth, Germany
Manfred Mackauer*
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada V5A 1S6
*
1 Author to whom all correspondence should be addressed (E-mail: mackauer@sfu.ca).
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Abstract

We examined oviposition behaviour in 49 species representing 19 genera of Aphidiinae. All species are solitary parasitoids of aphids (Hemiptera: Aphidoidea). Six general types are described that differ in oviposition time, behaviour, and morphology. The Ephedrini have the least specialized oviposition behaviour within the subfamily, with Praini and Aphidiini displaying various adaptations for host capture and oviposition. Use of the forelegs to grasp and orient aphids for oviposition has arisen twice, in Praini and, independently, in the genus Monoctonus Haliday (Aphidiini: Monoctonina). Morphological modifications of the terminal abdominal segments for host capture are found in Trioxina and in several species of Pauesia Quilis (Aphidiina). A “quick” sting is characteristic of species in the genus Aphidius Nees and related genera. The greatest degree of behavioural diversification occurred among Pauesia species, including cryptic behaviour, ant mimicry, and “sneak” oviposition. Acquired chemical camouflage and mimicry of the host’s cuticular hydrocarbon pattern to avoid detection by guarding ants is found in Aclitus obscuripennis Foerster, the genus Paralipsis Foerster, and the two closely related genera Adialytus Foerster and Lysiphlebus Foerster. It is suggested that the main driving forces in the evolution of parasitoid oviposition behaviour were aphid defensive behaviour and avoidance of aggression by trophobiotic ants. The results are compared with phylogenetic relationships inferred from morphological and molecular data.

Résumé

Nous avons étudié le comportement de ponte chez 49 espèces appartenant à 19 genres d’Aphidiinae. Toutes ces espèces sont des parasitoïdes solitaires de pucerons (Hemiptera : Aphidoidea) et elles peuvent être regroupées en six types généraux différents par la chronologie de leur ponte, leur comportement et leur morphologie. Les Ephidrini ont le comportement le moins spécialisé de toute la sous-famille, alors que les Praini et les Aphidiini présentent des adaptations diverses pour la capture de l’hôte et pour la ponte. L’utilisation des pattes antérieures pour saisir et orienter les pucerons pour la ponte est apparue deux fois, chez les Praini et, de façon indépendante, chez le genre Monoctonus Haliday (Aphidiini : Monoctonina). Des modifications morphologiques des segments abdominaux terminaux se retrouvent chez les Trioxina et chez plusieurs espèces de Pauesia Quilis (Aphidiina). Une piqûre rapide est caractéristique des espèces du genre Aphidius Nees et des genres apparentés. La plus grande diversification comportementale a été observée chez les espèces de Pauesia, notamment le camouflage, le mimétisme et la ponte furtive. L’acquisition d’un camouflage chimique et le mimétisme des patterns cuticulaires d’hydrates de carbone des pucerons empêchent Aclitus obscuripennis Foerster de même que les espèces du genre Paralipsis Foerster et de deux autres genres apparentés, Adialytus Foerster et Lysiphlebus Foerster, d’être repérées trop facilement par les fourmis gardiennes. Nous croyons que l’évolution du comportement de ponte de ces parasitoïdes est le résultat de deux forces directrices, le comportement de défense des pucerons et la capacité des parasitoïdes d’éviter les attaques des fourmis trophobiontes. Les résultats présentés ici sont comparés aux relations phylogénétiques obtenues à partir de données morphologiques ou moléculaires.

[Traduit par la Rédaction]

Type
Articles
Information
The Canadian Entomologist , Volume 132 , Issue 2 , April 2000 , pp. 197 - 212
Copyright
Copyright © Entomological Society of Canada 2000

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References

Belshaw, R., Quicke, D.L.J. 1997. A molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae). Molecular Phylogenetics and Evolution 7: 281–93CrossRefGoogle ScholarPubMed
Belshaw, R., Quicke, D.L.J., Völkl, W., Godfray, H.J.C. 1999. Molecular markers indicate rare sex in a predominantly asexual parasitoid wasp. Evolution 53: 1189–99CrossRefGoogle Scholar
Birnbach, R. 1995. Vergleichende Untersuchungen der Kutikularlipide von Blattlausschlupfwespen der Familie Aphidiidae. Diplomarbeit, Universität Bayreuth, Bayreuth, GermanyGoogle Scholar
Bledsoe, A.H., Raikow, R.J. 1990. A quantitative assessment of congruence between molecular and nonmolecular estimates of phylogeny. Journal of Molecular Evolution 30: 247–59CrossRefGoogle Scholar
Calvert, D.J., van den Bosch, R. 1972. Behavior and biology of Monoctonus paulensis (Hymenoptera: Braconidae), a parasite of dactynotine aphids. Annals of the Entomological Society of America 65: 773–9CrossRefGoogle Scholar
Carver, M. 1989. Biological control of aphids. pp. 141–65 in Minks, A.K. and Harrewijn, P. (Eds.), Aphids: their biology, natural enemies and control. World Crop Pests, Vol. 2C. Amsterdam: ElsevierGoogle Scholar
Chau, A., Mackauer, M. 1999. Self-superparasitism in the solitary parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiinae): proximate mechanisms. The Canadian Entomologist 131: 769–77CrossRefGoogle Scholar
Chow, F.J., Mackauer, M. 1986. Host discrimination and larval competition in the aphid parasite Ephedrus californicus. Entomologia Experimentalis et Applicata 41: 243–54CrossRefGoogle Scholar
Dowton, M., Austin, A.D., Antolin, M.F. 1998. Evolutionary relationships among the Braconidae (Hymenoptera: Ichneumonoidea) inferred from partial 16. rDNA gene sequences. Insect Molecular Biology 7: 129–50CrossRefGoogle Scholar
Eastop, V.F., Hille Ris Lambers, D. 1976. Survey of the world's aphids. The Hague: W. JunkGoogle Scholar
Eidmann, H. 1924. Die Eiablage von Trioxys Hal. (Hym., Braconidae) nebst Bemerkungen über die wirtschaftliche Bedeutung dieses Blattlausparasiten. Zeitschrift für Angewandte Entomologie 10: 353–63CrossRefGoogle Scholar
Finlayson, T. 1990. The systematics and taxonomy of final-instar larvae of the family Aphidiidae (Hymenoptera). Memoirs of the Entomological Society of Canada 152: 1–74Google Scholar
Gärdenfors, U. 1986. Taxonomic and biological revision of Palearctic Ephedrus (Haliday) (Hymenoptera, Braconidae, Aphidiinae). Entomologia Scandinavica Supplement 27: 1–95Google Scholar
Griffiths, D.C. 1961. The development of Monoctonus paludum Marshall (Hym., Braconidae) in Nasonovia ribis-nigri on lettuce, and immunity reactions in other lettuce aphids. Bulletin of Entomological Research 52: 147–63CrossRefGoogle Scholar
Heie, O.E. 1980. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. I. General part. The families Mindaridae, Hormaphididae, Thelaxidae, Anoeciidae, and Pemphigidae. Fauna Entomologica Scandinavica 9: 1–236Google Scholar
Hughes, R.D. 1989. Biological control in the open field. pp. 167–98 in Minks, A.K. and Harrewijn, P. (Eds.), Aphids: their biology, natural enemies and control. World Crop Pests, Vol. 2C. Amsterdam: ElsevierGoogle Scholar
Kambhampati, S., Völkl, W., Mackauer, M. 1999. Phylogenetic relationships among genera of Aphidiinae (Hymenoptera: Braconidae) based on DNA sequence of the mitochondrial 16. rRNA gene. Systematic Entomology. In pressGoogle Scholar
Klingauf, F. 1966. Abwehr- und Meidereaktionen von Blattläusen (Aphididae) bei Bedrohung durch Räuber und Parasiten. Zeitschrift für Angewandte Entomologie 60: 269–317CrossRefGoogle Scholar
Kraus, W. 1994. Untersuchungen zur Räuber-Beute-Beziehung des Systems Kiefer – Blattlaus – Schlupfwespe (Pinus silvestris – Schizolachnus pineti – Pauesia unilachni) einschlieβlich deren fachlichen und didaktischen Exemplaritat. Hausarbeit, Erste Staatsprüfung für das Lehramt, Universität Bayreuth, Bayreuth, GermanyGoogle Scholar
Liepert, C. 1996. Chemische Mimikry bei Blattlausparasitoiden der Gattung Lysiphlebus (Hymenoptera, Aphidiidae). Bayreuther Forum Ökologie 39: 1–141Google Scholar
Liepert, C., Dettner, K. 1993. Recognition of aphid parasitoids by honeydew-collecting ants: the role of cuticular lipids in a chemical mimicry system. Journal of Chemical Ecology 19: 2143–53CrossRefGoogle Scholar
Losey, J.E., Denno, R.F. 1998. The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecological Entomology 23: 53–61CrossRefGoogle Scholar
Mackauer, M. 1961. Die Gattungen der Familie Aphidiidae und ihre verwandtschaftliche Zuordnung (Hymenoptera; Ichneumonoidea). Beiträge zur Entomologie 11: 792–803Google Scholar
Mackauer, M. 1965. Parasitological data as an aid in aphid classification. The Canadian Entomologist 97: 1016–27CrossRefGoogle Scholar
Mackauer, M., Chow, F.J. 1990. The effect of stinging: aphidiid parasitoids (Hymenoptera) “prefer” pseudoparasitized pea aphids. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 63: 309–15Google Scholar
Mackauer, M., Starý, P. 1967. World Aphidiidae (Hym. Ichneumonoidea). Paris: Le FrançoisGoogle Scholar
Mackauer, M., Völkl, W. 1993. Regulation of aphid populations by aphidiid wasps: does parasitoid foraging behaviour or hyperparasitism limit impact? Oecologia 94: 339–50CrossRefGoogle ScholarPubMed
Mackauer, M., Michaud, J.P., Völkl, W. 1996. Host choice by aphidiid parasitoids (Hymenoptera: Aphidiidae): host recognition, host quality, and host value. The Canadian Entomologist 128: 959–80CrossRefGoogle Scholar
Michaud, J.P., Mackauer, M. 1995 a. The use of visual cues in host evaluation by aphidiid wasps. II. Comparison between Ephedrus californicus, Monoctonus paulensis, and Praon pequodorum. Entomologia Experimentalis et Applicata 74: 267–75CrossRefGoogle Scholar
Michaud, J.P., Mackauer, M. 1995 b. Oviposition behavior of Monoctonus paulensis (Hymenoptera: Aphidiidae): factors influencing reproductive allocation to hosts and host patches. Annals of the Entomological Society of America 88: 220–6CrossRefGoogle Scholar
Piek, T., Spanjer, W. 1986. Chemistry and pharmacology of solitary wasp venoms. pp. 161–307in Piek, T. (Ed.), Venoms of the Hymenoptera: biochemical, pharmacological and behavioural aspects. London: Academic PressCrossRefGoogle Scholar
Schlinger, E.I. 1974. Continental drift, Nothofagus, and some ecologically associated insects. Annual Review of Entomology 19: 323–43CrossRefGoogle Scholar
Schlinger, E.I., Hall, J.C. 1961. The biology, behavior, and morphology of Trioxys (Trioxys) utilis, an internal parasite of the spotted alfalfa aphid, Therioaphis maculata (Hymenoptera: Braconidae, Aphidiinae). Annals of the Entomological Society of America 54: 34–45CrossRefGoogle Scholar
Sedlag, U. 1971. Struturelle Anpassungen und evolutionäre Trends in der Gattung Pauesia (Hymenoptera, Aphidiidae). pp. 298–9 in Proceedings of the 13th International Congress of Entomology, Moscow, 2–9 August 1968. Vol. 1Google Scholar
Smith, P.T., Kambhampati, S., Völkl, W., Mackauer, M. 1999. A phylogeny of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) inferred from mitochondrial NADH 1 dehydrogenase gene sequence. Molecular Phylogenetics and Evolution. 11: 236–45CrossRefGoogle ScholarPubMed
Starý, P. 1976. External female genitalia of the Aphidiidae (Hymenoptera). Acta Entomologica Bohemoslovaca 73: 102–12Google Scholar
Starý, P., Sedlag, U. 1959. Aphidius (Metaphidius) trioxyformis, eine neue Art und Untergattung der Aphidiinae (Hymenoptera Braconidae). Deutsche Entomologische Zeitschrift NF 6: 160–5CrossRefGoogle Scholar
Takada, H. 1983. Redescription and biological notes on Protaphidius nawaii (Ashmead) (Hymenoptera, Aphidiidae). Kontyu 51: 112–21Google Scholar
Takada, H., Hashimoto, Y. 1985. Association of the root aphid parasitoids Aclitus sappaphis and Paralipsis eikoae (Hymenoptera, Aphidiidae) with the aphid-attending ants Pheidole fervida and Lasius niger (Hymenoptera, Formicidae). Kontyu 53: 150–60Google Scholar
Völkl, W. 1992. Aphids or their parasitoids: who actually benefits from ant-attendance? Journal of Animal Ecology 61: 273–81CrossRefGoogle Scholar
Völkl, W. 1994. The effect of ant-attendance on the foraging behaviour of the aphid parasitoid Lysiphlebus cardui. Oikos 70: 149–55CrossRefGoogle Scholar
Völkl, W. 1997. Interactions between ants and aphid parasitoids: patterns and consequences for resource utilization. pp. 225–40 in Dettner, K., Bauer, G., and Völkl, W. (Eds.), Vertical food web interactions: evolutionary patterns and driving forces. Ecological Studies 130. Berlin: SpringerCrossRefGoogle Scholar
Völkl, W., Kraus, W. 1996. Foraging behaviour and resource utilization of the aphid parasitoid Pauesia unilachni: adaptation to host distribution and mortality risks. Entomologia Experimentalis et Applicata 79: 101–9CrossRefGoogle Scholar
Völkl, W., Mackauer, M. 1993. Interactions between ants attending Aphis fabae ssp. cirsiiacanthoidis on thistles and foraging parasitoid wasps. Journal of Insect Behavior 6: 301–12CrossRefGoogle Scholar
Völkl, W., Mackauer, M. 1996. “Sacking” the host: oviposition behavior of a parasitoid wasp, Dyscritulus planiceps (Hymenoptera: Aphidiidae). Journal of Insect Behavior 9: 975–80CrossRefGoogle Scholar
Völkl, W., Novak, H. 1997. Foraging behaviour and resource utilization of the aphid parasitoid, Pauesia pini (Hymenoptera: Aphidiidae) on spruce: influence of host species and ant attendance. European Journal of Entomology 94: 211–20Google Scholar
Völkl, W., Stadler, B. 1996. Colony orientation and successful defense behaviour in the conifer aphid, Schizolachnus pineti. Entomologia Experimentalis et Applicata 78: 197–200CrossRefGoogle Scholar
Völkl, W., Liepert, C., Birnbach, R., Hübner, G., Dettner, K. 1996. Chemical and tactile communication between the root aphid parasitoid Paralipsis enervis and trophobiotic ants: consequences for parasitoid survival. Experientia 52: 731–8CrossRefGoogle Scholar
Whitfield, J.B. 1998. Phylogeny and evolution of host–parasitoid interactions in Hymenoptera. Annual Review of Entomology 43: 129–51CrossRefGoogle ScholarPubMed