Multi-camera field monitoring reveals costs of learning for parasitoid foraging behaviour

Abstract

Dynamic conditions in nature have led to the evolution of behavioural traits that allow animals to use information on local circumstances and adjust their behaviour accordingly, for example through learning. Although learning can improve foraging efficiency, the learned information can become unreliable as the environment continues to change. This could lead to potential fitness costs when memories holding such unreliable information persist. Indeed, persistent unreliable memory was found to reduce the foraging efficiency of the parasitoid Cotesia glomerata under laboratory conditions. Here, we evaluated the effect of such persistent unreliable memory on the foraging behaviour of C. glomerata in the field. This is a critical step in studies of foraging theory, since animal behaviour evolved under the complex conditions present in nature. Existing methods provide little detail on how parasitoids interact with their environment in the field, therefore we developed a novel multi-camera system that allowed us to trace parasitoid foraging behaviour in detail. With this multi-camera system, we studied how persistent unreliable memory affected the foraging behaviour of C. glomerata when these memories led parasitoids to plants infested with non-host caterpillars in a semi-field set-up. Our results demonstrate that persistent unreliable memory can lead to maladaptive foraging behaviour in C. glomerata under field conditions and increased the likelihood of oviposition in the non-host caterpillar Mamestra brassica. Furthermore, these time- and egg-related costs can be context dependent, since they rely on the plant species used. These results provide us with new insight on how animals use previously obtained information in naturally complex and dynamic foraging situations and confirm that costs and benefits of learning depend on the environment animals forage in. Although behavioural studies of small animals in natural habitats remain challenging, novel methods such as our multi-camera system contribute to understanding the nuances of animal foraging behaviour.

Keywords: associative learning; brassicaceous plant species; cabbage moth; foraging efficiency; large cabbage white butterfly; memory reliability; non-host; parasitic wasp.

FIGURE 1

Overview of the experimental approach, including conditioning method of the colour marked Cotesia glomerata parasitoids (top panel) and the semi‐field set‐up for the observation of parasitoid foraging behaviour with the multi‐camera set‐up (bottom panels). Colour marked parasitoids were given three spaced oviposition experiences on either a Brassica nigra or Sinapis arvensis host‐infested plant (top panel) or were kept unconditioned (not shown). They were released in the two test situations 24 hr after conditioning, as described in the middle panels. The bottom panels show the layout of the field tent, with the locations of the host‐ and non‐host‐infested plants, their associated video cameras, their connection to the video recorder and the display of the 15 video channels, with the multi‐channel mode to observe parasitoid activity on all plants and the single‐channel mode for a more detailed view. See text for a more detailed description

FIGURE 2

Survival plots of the fraction of Cotesia glomerata parasitoids with congruent and conflicting memory that have not found the host within 5 hr (FP 3) in foraging situation 1 (a) and foraging situation 2 (b), and the fraction of parasitoids that have not been seen, that is, have not landed on an infested plant (FP 4) in foraging situation 1 (c) and foraging situation 2 (d). These parasitoids foraged in a semi‐field set‐up with Pieris brassicae (host) and Mamestra brassicae (non‐host) infested plants. p‐values are based on Cox's proportional hazard models with frailty and indicate whether the survival curves of parasitoids with conflicting and congruent memory are significantly different

FIGURE 3

The foraging behaviour of Cotesia glomerata parasitoids with conflicting and congruent memory on and around host‐ and non‐host‐infested plants. Various behavioural parameters were measured in foraging situation 1 (a–f) and foraging situation 2 (g–l). Panels show how long parasitoids foraged (FP 5, a/g), how much time they spent in total on the non‐host (NH) plants (FP 8, b/h), how many visits parasitoids made to NH plants (FP 11, d/j), how many NH plants were visited (FP 12, c/i), the percentage of parasitoids that oviposited in the non‐host (FP 13, e/k) and the number of ovipositions in the non‐host (FP 14, f/l). Average values are shown with error bars representing the SE, except for panels e and k, which show overall percentages. Numbers of wasps per treatment are indicated inside bars. p‐values show whether the behavioural parameter was significantly different between parasitoids with conflicting and congruent memory