Les hyperparasitoïdes sont des guêpes parasitoïdes des parasitoïdes primaires. Au sein d’un écosystème, ils occupent le quatrième niveau trophique. Une meilleure connaissance de la biologie et du comportement des hyperparasitoïdes est indispensable pour comprendre leur relation avec les parasitoïdes et leur rôle dans les écosystèmes. Dans cette étude, quatre espèces d’hyperparasitoïdes de pucerons différant quant à leur phylogénie, mode de développement (koinobionte vs. idiobionte), stades d’hôte attaqués, et spécificité parasitaire ont été choisies: Dendrocerus carpenteri (Curtis) (Megaspilidae), Asaphes suspensus Walker (Pteromalidae), Alloxysta victrix (Westwood) (Alloxystidae) et Syrphophagus aphidivorus (Mayr) (Encyrtidae). Au laboratoire, j’ai comparé leurs paramètres d’histoire de vie et comportements de recherche par une approche comparative directe au sein du système trophique: pomme de terre ( Solanum tuberosum L.); puceron de la pomme de terre, Macrosiphum euphorbiae (Thomas); parasitoïde hôte Aphidius nigripes Ashmead.

Les résultats ont révélé une grande variation interspécifique des paramètres d’histoire de vie des hyperparasitoïdes. Cette variation n’a pu être attribuée exclusivement à la dichotomie du mode de développement (koinobionte ou idiobionte), tel que démontré pour les parasitoïdes primaires. L’hyperparasitoïde S. aphidivorus est atypique, ayant la capacité d’attaquer soit la larve parasitoïde dans le puceron vivant, soit sa pupe après la momification du puceron. Les femelles préféraient cet hôte, lequel s’est également avéré le plus convenable au développement. Des tests d’olfactométrie et des observations comportementales ont révélé que les femelles hyperparasitoïdes en quête d’hôtes ne seraient pas attirées à distance par des odeurs. Toutefois, elles utilisent des stimuli de contact sur la plante afin de localiser leur hôte. À ce niveau, le miellat de puceron est apparu comme l’un des principaux stimuli utilisés par les femelles, lesquelles discriminaient entre le miellat de puceron et celui de cochenille, Coccus hesperidum , n’abritant pas d’hôtes potentiels. Par contre, les femelles hyperparasitoïdes n’ont pas distingué le miellat de pucerons sains non-parasités, et celui de pucerons parasités par A. nigripes .

Cette étude indique que plusieurs facteurs influencent simultanément l’histoire de vie des hyperparasitoïdes de pucerons. Leur subdivision habituelle en endoparasitoïdes koinobiontes de larves parasitoïdes dans les pucerons vivants, et ectoparasitoïdes idiobiontes de pupes de parasitoïdes dans les pucerons momifiés ne traduit pas toutes les différences interspécifiques observées. Des différences d’ordre phylogénique seraient également importantes, ces espèces provenant de taxons différents. A bien des égards, les paramètres de vie et le comportement des hyperparasitoïdes de pucerons diffèrent de ceux des parasitoïdes primaires de pucerons.

Hyperparasitoids are parasitic wasps that attack primary parasitoids. They constitute the fourth trophic level in many ecosystems. A better understanding of hyperparasitoid biology and behaviour is needed to unravel the nature of parasitoid - hyperparasitoid interactions and their role in the functioning of communities and ecosystems. In this thesis, the life history traits and host searching behaviour of aphid hyperparasitoids are studied using a direct comparative approach. Four species were chosen that differ in development mode (koinobiont or idiobiont), host stage attacked and host range: Dendrocerus carpenteri (Curtis) (Megaspilidae), Asaphes suspensus Walker (Pteromalidae), Alloxysta victrix (Westwood) (Alloxystidae) et Syrphophagus aphidivorus (Mayr) (Encyrtidae) have been studied on the same potato ( Solanum tuberosum L.), potato aphid ( Macrosiphum euphorbiae (Thomas)) and primary parasitoid (Aphidius nigripes Ashmead) system.

The results revealed a large variation in life history traits between species, which could not be explained simply by dichotomy in development mode, as proposed for primary parasitoids. The hyperparasitoid S. aphidivorus is special because females can attack the parasitoid host in the still-living aphid, or in the mummified aphid. Female S. aphidivorus had a preference for aphid mummies, which also contain the most profitable host stage for hyperparasitoid development. Olfactometer tests and behavioural observations indicated that searching hyperparasitoid females were not attracted by olfactory cues. However, they clearly reacted to host-related contact cues while searching on a plant. Here, honeydew was one of the principal contact cues used by female hyperparasitoids to locate hosts. Females discriminated between honeydew from an aphid host and that from a non-host, the soft brown scale, Coccus hesperidum , but made no difference between honeydew from healthy, unparasitised aphids, and those parasitised by A. nigripes .

This study indicates that several factors probably act simultaneaously on life history strategies. The simple classification of aphid hyperparasitoids as koinobiont endoparasitoids of parasitoid larvae in living aphids, or idiobiont ectoparasitoids of parasitoid pupae in mummified aphids does not explain all observed interspecific differences. Lineage specific effects must also be important, as the species belong to different taxa. Finally, in many aspects, the life history parameters and behaviour of aphid hyperparastoids differ from those reported for primary aphid parasitoids.

Chapter 3 has been submitted for publication in Ecological Entomology: Buitenhuis, R., Boivin, G., Vet, L.E.M., and Brodeur, J. Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): Fitness consequences of selecting hosts in live aphid vs. aphid mummy

Chapter 5 has been accepted for publication in the Journal of Chemical Ecology : Buitenhuis, R., McNeil, J.M., Boivin, G. and Brodeur, J., 2004. The role of honeydew in host searching of aphid hyperparasitoids.

First of all I would like to thank Jacques Brodeur, Guy Boivin and Louise Vet. From the moment I talked to Louise on the phone about a project on hyperparasitoids in Québec, my visit to Guy in Belgium and my reception in Québec by Jacques, I knew that I was in good hands to bring my PhD to a good ending. I have come to know them as very good scientists, and wonderful persons. Even when I had to interrupt my studies, they supported me through difficult times, and afterwards I could pick up the PhD where I had left it a year before. I have learnt a lot under their direction, in science and in life. I also want to thank Conrad Cloutier and Jeremy McNeil for our discussions and their advice, which really helped improve the quality of this thesis. Conrad did also a great job on the prelecture. I am glad that Jeff Harvey accepted to be the external examinator.

I really appreciated the help of André Bouchard, Marc Fournier, Sophie Rochefort and Sébastien Jacob. As lab assistants they did a great job! Furthermore, without the help of all the students I could not have completed this research. Julie Blais, Julie Larivière, Guillaume Ménard, Mark Kleijnen, Marie-Pierre Mignault, Marie-Pierre Thibeault, Edith and Mélanie Bisson worked very hard, meticulous and patient, even when the work was repetitive and boring. One of the reasons why I spent such a great time at Laval University is because of the students in the entomology lab and the Envirotron. I have made some good friends, and I enjoyed the many activities that we did together.

Dr. A. Chow, dr. W. Völkl and dr. T. Grasswitz provided me with the hyperparasitoid species. I am also thankful to Ann Fook Yang of the Eastern Cereal and Oilseed Research Centre (Agriculture and Agri-food Canada, Ottawa) for the use of the scanning electron microscope, to the entomology lab of Guy for help with the analysis of my honeydew videos and to Geatan Daigle and Hélène Crepeau for their statistical advice.

I would like to thank the CRH (CRSNG to Jacques) and Agriculture Canada for funding.

Finally a big thank you to Sébastien, my family and my friends for their support and their encouragement.