Abstract
The relevance of the integration of preimaginal and eclosion experiences on the subsequent habitat preferences and mate finding by the adult has been rarely tested in holometabolous insects. In this work, the effect of larval and early adult experiences on the behavioural responses of adult males of the aphid parasitoid, Aphidius ervi, towards volatiles from the host–plant complex (HPC) and from conspecific females were evaluated. Two experience factors were considered: host diet (normal diet=ND; artificial diet=AD), and eclosion, i.e. extraction or non-extraction of the parasitoid larva from the parasitised aphid (extracted=EX; non-extracted=NE). Thus, four treatments were set up: ND/NE, ND/EX, AD/NE and AD/EX. Glass Y-tube olfactometers were used to investigate the responses of adult A. ervi males to the odour sources used. Males from the ND/NE treatment showed a shorter latency to the first choice of olfactometer arms, displayed a marked preference towards the HPC olfactometer arm, and spent more time in the HPC arm than males from the other treatments. Only the interaction of host diet and eclosion experiences proved to be relevant in explaining the differences in latency to first choice, time spent in olfactometers arms, and behaviours displayed in the olfactometer arms. These results show the importance of the integration of larval and eclosion experiences in the development of stereotyped responses of the adults. This process may involve memory retention from the preimaginal and emergence period, but further research is needed to disentangle the contribution of each stage. The response to conspecific females was much less affected by the treatments in relation to first arm choice and times in olfactometer arms, suggesting a pheromone-mediated behaviour, even though a prompter and more intense wing fanning courtship behaviour was registered in the ND/NE males compared to males from the AD/NE treatment. These results show that sexual behaviours are less affected by early experiences than behaviours related with finding a HPC for foraging or oviposition. Taken together, our results demonstrate for first time that larval and eclosion experiences affect in a differential way the early responses of the adult towards environment-derived cues and mate related cues.
Similar content being viewed by others
References
Ayasse M, Paxton RJ, Tengö J (2001) Mating behavior and chemical communication in the order Hymenoptera. Annu Rev Entomol 46:31–78
Barron AB (2001) The life and death of Hopkins’ host-selection principle. J Insect Behav 14:725–737
Barron AB, Corbet SA (1999) Preimaginal conditioning in Drosophila revisited. Anim Behav 58:621–628
Barron AB, Corbet SA (2000) Behavioural induction in Drosophila: timing and specificity. Entomol Exp Appl 94:159–171
Bateson P (1988) The active role of behaviour in evolution. In: Ho M-W, Fox S (eds) Process and metaphors in the new evolutionary paradigm. Wiley, Chichester, pp 191–207
Battaglia D, Isidoro N, Romani R, Bin F, Pennacchio F (2002) Mating behaviour of Aphidius ervi (Hymenoptera: Braconidae): the role of antennae. Eur J Entomol 99:451–456
Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105
Blumstein DT, Evans CS, Daniel JC (2000) JWatcher 0.9. An introductory user’s guide. Animal Behaviour Laboratory, Macquarie University, Australia: http://galliform.psy.mq.edu.au/jwatcher/
Bonner JT (1988) The evolution of complexity. Princeton University Press, Princeton
Borsellino AP, Pierantoni R, Schieti-Cavazza B (1970) Survival in adult mealworm beetles (Tenebrio molitor) of learning acquired at the larval stage. Nature 225:963–964
Carlin NF, Schwartz PH (1989) Pre-imaginal experience and nestmate brood recognition in the carpenter ant, Camponotus floridanus. Anim Behav 38:89–95
Caubet Y, Jaisson P (1991) A post eclosion early learning involved in host recognition by Dinarmus basalis Rondani (Hymenoptera: Pteromalidae). Anim Behav 40:977–980
Corbet SA (1985) Insect chemosensory responses. A chemical legacy hypothesis. Ecol Entomol 10:143–153
Daza-Bustamante P, Fuentes-Contreras E, Rodríguez LC, Figueroa CC, Niemeyer HM (2002) Behavioural differences between Aphidius ervi populations from two tritrophic systems are due to phenotypic plasticity. Entomol Exp Appl 104:321–328
Gandolfi M, Mattiacci L, Dorn S (2003) Preimaginal learning determines adult responses to chemical stimuli in a parasitic wasp. Proc R Soc London, B Series 270:2623–2629
Godfray HCJ (1994) Parasitoids, behavioral and evolutionary ecology. Princeton University Press, Princeton, New Jersey
Hérard F, Keller MA, Lewis WJ, Tumlinson JH (1988) Beneficial arthropod behaviour mediated by airborne semiochemicals. IV. Influence of host diet on host-oriented flight chamber responses of Microplitis demolitor Wilkinson. J Chem Ecol 14:1597–1606
Hirsch HVB, Tompkins L (1994) The flexible fly: experience-dependent development of complex behaviors in Drosophila melanogaster. J Exp Biol 195:1–18
Kateri M, Papaioannu T, Dellaportas P (2001) Bayesian analysis of correlated proportions. Sankhya 63:270–285
Kester KM, Barbosa P (1991) Post-emergence learning in the insect parasitoid, Cotesia congregata (Say) (Hymenoptera, Braconidae). J Insect Behav 4:727–742
Lehrman DS (1970) Semantic and conceptual issues in the nature-nurture problem. In: Aronson L, Tobach E, Lehrman DS, Rosenblatt J (eds) Development and evolution of behavior. Freeman, San Francisco, pp 17–52
Löfstedt C, Vickers NJ, Roelofs WL, Baker T (1989) Diet related courtship success in the Oriental fruit moth, Grapholita molesta (Tortricidae). Oikos 55:402–408
Mackauer M (1969) Sexual behaviour of and hybridization between three species of Aphidius Nees parasitic on the pea aphid. Proc Entomol Soc Wash 71:339–351
Mackauer M, Finlayson T (1967) The hymenopterous parasites (Hymenoptera: Aphidiidae et Aphelinidae) of the pea aphid in eastern North America. Can Entomol 99:1051–1082
Maturana H, Mpodozis J (2000) The origin of species by means of natural drift. Rev Chil Hist Nat 73:261–310
McNeil JN, Brodeur J (1995) Pheromone-mediated mating in the aphid parasitoid Aphidius nigripes (Hymenoptera: Aphididae). J Chem Ecol 21:959–972
McNemar Q (1947) Note on the sampling error of the difference between correlated proportions or percentages. Psychometrika 12:153–157
Němec V, Starý P (1985) Genetic diversity of the parasitoid Aphidius ervi on the pea aphid, Acyrthosiphon pisum in Czechoslovakia (Hymenoptera: Aphidiidae; Homoptera, Aphididae). Acta Entomol Bohemoslov 82:88–94
Olson DM, Rains GC, Meiners T, Takasu K, Tertuliano M, Tumlinson JH, Wäckers FL, Lewis WJ (2003) Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors. Chem Senses 28:545–549
Papaj DJ, Lewis AC (1993) Insect learning. Ecological and evolutionary perspectives. Chapman & Hall, New York
Pennacchio F, Strand MR (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annu Rev Entomol 51:233–258
Pennacchio F, Tremblay E (1989) A new species of Aphidius Nees from Italy (Hymenoptera, Braconidae, Aphidiinae). Boll Lab Entomol Agrar “Filippo Silvestri” 45:167–169
Pennacchio F, Digilio MC, Tremblay E, Tranfaglia A (1994) Host recognition and acceptance behaviour in two aphid parasitoid species: Aphidius ervi Haliday and Aphidius microlophii Pennacchio & Tremblay (Hymenoptera, Braconidae). Bull Entomol Res 84:57–64
Pennacchio F, Fanti P, Falabella P, Digilio MC, Biscaccia F, Tremblay E (1999) Development and nutrition of the braconid wasp, Aphidius ervi in aposymbiotic host aphids. Arch Insect Biochem Physiol 40:53–63
Powell W, Pennacchio F, Poppy GM, Tremblay E (1998) Strategies involved in the location of hosts by the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae). Biol Control 11:104–112
Rietdorf K, Steidle JLM (2002) Was Hopkins right? Influence of larval experience and early adult experience on the olfatory response in the granary weevil Sitophilus granarius (Coleptera, Curculionidae). Physiol Entomol 27:223–227
Rossiter MC (1996) Incidence and consequence of inherited environmental effects. Ann Rev Ecolog Syst 27:451–476
Salin C, Deprez B, Van Bockstaele DR, Mahillon J, Hance T (2004) Sex determination mechanism in the hymenopteran parasitoid Aphidius rhopalosiphi De Stefani-Peres (Braconidae: Aphidiinae). Belg J Zool 134:15–21
Schneirla TC (1956) Interrelationships of the “innate” and the “acquired” in the instinctive behaviour. In: Grassé P (ed) Instinct dans le comportement des animaux et de l’homme. Masson et Cie, Paris, pp 131–187
Sokal R, Rohlf JF (1998) Biometry, the principles and practice of statistics in biological research. WH Freeman and Company, New York
Sumana A, Starks PT (2004) Grooming patterns in the primitively eusocial wasp Polistes dominulus. Ethology 110:825–833
Takada H, Tada E (2000) A comparison between two strains from Japan and Europe of Aphidius ervi. Entomol Exp Appl 97:11–20
Tierney AJ (1986) The evolution of learned and innate behaviour: contributions from genetics and neurobiology to a theory of behavioral evolution. Anim Learn Behav 14:339–348
Tully T, Cambiazo V, Kruse L (1994) Memory through metamorphosis in normal and mutant Drosophila. J Neurosci 14:68–74
Turlings TCJ, Wäckers FL, Vet LEM, Lewis WJ, Tumlinson JH (1992) Learning of host-finding cues by hymenopterous parasitoids. In: Papaj DR, Lewis AC (eds) Insect learning, ecological and evolutionary aspects. Chapman & Hall, New York, pp 51–78
van Emden HF, Sponagl B, Baker T, Ganguly S, Douloumpaka S (1996) Hopkins’ ‘host selection principle’, another nail in its coffin. Physiol Entomol 21:325–328
van Emden HF, Eletherianos I, Rose J, Douloumpakata S, Pettersson J (2002) Aphid parasitoids detect that an alien plant was present nearby during their development. Physiol Entomol 27:199–205
Vet LEM, Lewis WJ, Cardé RT (1995) Parasitoid foraging and learning. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects 2. Chapman & Hall, New York, pp 65–101
Villagra CA, Vásquez RA, Niemeyer HM (2005) Associative odour learning affects mating behaviour in Aphidius ervi males (Hymenoptera: Braconidae). Eur J Entomol 102:557–559
Wcislo WT (1989) Behavioral environments and evolutionary change. Ann Rev Ecolog Syst 20:137–169
West MJ, King AP (1987) Settling nature and nurture into an ontogenetic niche. Develop Psychobiol 20:549–562
Wuellner CT, Porter SD, Gilbert LE (2002) Eclosion, mating, and grooming behavior of the parasitoid fly Pseudacteon curvatus (Diptera: Phoridae). Fla Entomol 85:563–566
Acknowledgements
This study received financial support from CONICYT, Universidad de Chile, and MECESUP. CAV is grateful to CONICYT for a doctoral fellowship and a research grant (AT-4040221), to Universidad de Chile for thesis financial support (No. 31-2004), and to MECESUP for a travel grant to visit the Dipartimento di Biologia, Università della Basilicata at Potenza, where the experiments described were started. CAV is also indebted to people at the laboratory in Potenza and at the Laboratorio de Química Ecológica at Universidad de Chile, to the Decenio Evolutionary Biology Discussion Group, and to Macarena Faunes for valuable suggestions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Villagra, C.A., Pennacchio, F. & Niemeyer, H.M. The effect of larval and early adult experience on behavioural plasticity of the aphid parasitoid Aphidius ervi (Hymenoptera, Braconidae, Aphidiinae). Naturwissenschaften 94, 903–910 (2007). https://doi.org/10.1007/s00114-007-0269-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-007-0269-4