Associative learning of host presence in non‐host environments influences parasitoid foraging

Abstract

1. Parasitoids are known to utilise learning of herbivore-induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non-suitable herbivores (non-hosts). Simultaneous infestation of plants by hosts and non-hosts has been found to result in induction of HIPVs that differ from host-infested plants. Each non-host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non-host herbivore also contain the host.2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non-hosts in the laboratory and in semi-field experiments.3. In two-choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant-host-non-host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non-host caterpillar Mamestra brassicae or the non-host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non-host caterpillars or aphids in a semi-field situation.4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.

Costs of Persisting Unreliable Memory: Reduced Foraging Efficiency for Free-Flying Parasitic Wasps in a Wind Tunnel

“…Since most parasitoids are time-limited, they should utilize their time as efficiently as possible, since the way they exploit their environment directly determines their realized fitness (Van Baalen and Hemerik, 2007). While most studies focusing on the effect of learning on foraging efficiency provide the wasp with a foraging situation highly similar to what they have been trained in Geervliet et al (1998), Takasu and Lewis (2003), Bleeker et al (2006), Smid et al (2007), Kruidhof et al (2015), De Rijk et al (2018, and Desurmont et al…”

“…The generalist larval parasitoid Cotesia glomerata, is well known for its ability to learn in both laboratory and (semi-)field studies (Geervliet et al, 1998;Perfecto and Vet, 2003;Smid et al, 2007;De Rijk et al, 2018;Vosteen et al, manuscript in preparation). Unlike general theory, it consolidates LTM for oviposition events on certain host plants within 4 h after only a single oviposition in its host Pieris brassicae (Smid et al, 2007).…”

Effect of fruit and host fly species on the associative learning by Fopius arisanus

“…We are yet to understand to what extent F. arisanus is able to recognize the species of fruit flies and what are the criteria for the parasitoid to accept or reject fruit fly eggs. Further studies about the extent to which laboratory results can be translated into the field are needed, as the learning and change in preference obtained in laboratory assays might not always translate in preference change in the field (De Rijk et al ., 2018). The development of mass-rearing methods to enhance searching behaviour in biological control agents is of interest, e.g.…”

“…A priori host exposition stimulates host discrimination and enhances fruit fly parasitism (Gonçalves et al ., 2017). However, a learned preference in laboratory does not always translate into a change in parasitization preferences in semi-field, as observed for the parasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) (De Rijk et al ., 2018).…”

Getting confused: learning reduces parasitoid foraging efficiency in some environments with non-host-infested plants

“…Search templates are constantly updated during foraging (Aartsma et al 2019 ) and foraging experience on host- and/or non-host-infested plants may help parasitoids to fine-tune their foraging behaviour, hence reducing the distraction by non-host-infested plants (De Rijk et al 2018 ). C. glomerata readily learns volatile cues during host oviposition and already forms long-term memory 4 h after a single oviposition in Pieris brassicae (Smid et al 2007 ), a learning strategy that is thought to be adaptive during foraging for a patchily distributed gregarious host (Hoedjes et al 2011 ; Smid and Vet 2016 ).…”