Role of conspecifics and personal experience on behavioral avoidance of contaminated flowers by bumblebees

Abstract

Pollinators use multiple cues whilst foraging including direct cues from flowers and indirect cues from other pollinators. The use of indirect social cues is common in social insects, such as honeybees and bumblebees, where a social environment facilitates the ability to use such cues. Bumblebees use cues to forage on flowers according to previous foraging experiences. Flowers are an essential food source for pollinators but also pose a high risk of parasite infection through the shared use of flowers leading to parasite spillover. Nevertheless, bumblebees have evolved behavioral defense mechanisms to limit parasite infection by avoiding contaminated flowers. Mechanisms underlying the avoidance of contaminated flowers by bumblebees are poorly understood. Bumblebees were recorded having the choice to forage on non-contaminated flowers and flowers contaminated by a trypan osome gut parasite, Crithidia bombi. The use of different treatments with presence or absence of conspecifics on both contaminated and non-contaminated flowers allowed to investigate the role of social visual cues on their pathogen avoidance behavior. Bumblebees are expected to use social visual cues to avoid contaminated flowers. Our study reveals that the presence of a conspecific on flowers either contaminated or not does not help bumblebee foragers avoiding contaminated flowers. Nevertheless, bumblebees whereas gaining experience tend to avoid their conspecific when placed on contaminated flower and copy it when on the non-contaminated flower. Our experiment suggests a detrimental impact of floral scent on disease avoidance behavior.

Keywords: Host-parasite interactions; behavioral immunity; copying behavior; inadvertent social information; pollinators; social learning.

Figure 1.

Time spent by a bumblebee before landing on flowers among the 3 treatments. (A) Time spent by a bumblebee before landing on a flower in relation to the bumblebee’s experience (naive bumblebee fed only on 1 type of flower, expert bumblebee fed on both flowers). (B) Time spent by a bumblebee before landing on a flower in relation to flower contamination status and position. Box plots depict median, interquartile range, and non-outliers range; the dots represent the outliers. The dashed line represents the linear regression between feeding duration and foraging bout. Cont., contaminated flower; Non-Cont., non-contaminated flower. * and ** represent P-values below 0.05 and 0.01, respectively, according to post hoc Tukey tests.

Figure 2.

Time spent by a bumblebee feeding on flowers among the 3 treatments. (A) Feeding duration of a bumblebee on flowers in relation to the number of times (foraging bout) it fed on flower. (B) Feeding duration of a bumblebee on flowers in relation to flower contamination status without outliers below 11 s. (C) Feeding duration of a bumblebee on flowers in relation to flower contamination status with outliers below 11 s. Box plots depict median, interquartile range and non-outliers range; the dots represent the outliers. The dashed line represents the linear regression between feeding duration and foraging bout. Cont., contaminated flower; Non-Cont., non-contaminated flower.

Figure 3.

Proportion of visits by bumblebees on the non-contaminated flowers in relation to the period (learning [Day 1–3: 3 first days with social visual cue] vs. choice [Day 4: last day without cue]) and treatments. The histograms represent the means and bars represent their 95% confidence interval. V_C, treatment with visual cue on the contaminated flower; Ctrl, control treatment; V_NC, treatment with visual cue on the non-contaminated flower. ** represents P-values below 0.01 according to post hoc Tukey tests.

Figure 4.

Proportion of visits by bumblebees on the non-contaminated flower and on the flower with social visual cue among treatments during the learning period (the first 3 days). (A) Proportion of non-contaminated flower visitation during the learning period (Days 1–3) among the 3 treatments. (B) Proportion of visits by bumblebees on flowers with social visual cue in relation to the contamination status of the flower where the social visual cue is present. Only the learning period is represented (Days 1–3), since only during this period conspecifics were present on flowers. The points represent the means between the different bumblebees and treatment and bars represent their 95% confidence interval.