Associative learning and memory retention of nectar yeast volatiles in a generalist parasitoid

Abstract

Understanding how animals learn is crucial to interpreting animal behaviour. Flower-visiting insects, such as bees and parasitoids, are excellent animal models to study visual and olfactory learning, including memory phenomena. The diversity of resources flower-visiting insects exploit predisposes them to learn and remember the colours, shapes and odours associated with rewarding experiences (e.g. flowers), allowing them to focus on the most rewarding resources. Recent research has shown that nectar-living microbes release volatile organic compounds (VOCs) that contribute to overall flower scent. Nevertheless, little is known about the extent to which nectar microbiota mediate insect learning of floral preferences. In this study, we investigated whether VOCs produced by nectar microbes serve as a learning cue to parasitoids and how long any developed preference is maintained. Experiments were performed using the generalist aphid parasitoid Aphidius ervi and three nectar yeasts, including the nectar specialist Metschnikowia reukaufii and the generalist species Hanseniaspora uvarum and Sporobolomyces roseus. Results showed that naïve parasitoids had an innate preference for nectar fermented by the nectar specialist M. reukaufii, but not by the other two yeasts which had either a neutral (H. uvarum) or deterrent (S. roseus) effect. When parasitoids were conditioned with yeast-fermented nectar, they were strongly attracted to their odours 2 and 24h after conditioning, but not after 48h. Furthermore, when parasitoids were conditioned to one yeast-fermented nectar, they also showed increased attraction to other yeast-fermented nectars. This generalization suggests that their learning ability may have broader ecological consequences. However, this generalized response to other yeast VOCs lasted for only 2h. We conclude that parasitoids show conditioned responses to the scent of yeast-fermented nectar, and yeasts, therefore, may play an important but understudied role in shaping their foraging behaviour.