Sucrose acceptance and different forms of associative learning of the honey bee (apis mellifera L.) in the field and laboratory

Abstract

The experiments analyze different forms of learning and 24-h retention in the field and in the laboratory in bees that accept sucrose with either low (</=3%) or high (>/=30% or >/=50%) concentrations. In the field we studied color learning at a food site and at the hive entrance. In the laboratory olfactory conditioning of the proboscis extension response (PER) was examined. In the color learning protocol at a feeder, bees with low sucrose acceptance thresholds (</=3%) show significantly faster and better acquisition than bees with high thresholds (>/=50%). Retention after 24 h is significantly different between the two groups of bees and the choice reactions converge. Bees with low and high acceptance thresholds in the field show no differences in the sucrose sensitivity PER tests in the laboratory. Acceptance thresholds in the field are thus a more sensitive behavioral measure than PER responsiveness in the laboratory. Bees with low acceptance thresholds show significantly better acquisition and 24-h retention in olfactory learning in the laboratory compared to bees with high thresholds. In the learning protocol at the hive entrance bees learn without sucrose reward that a color cue signals an open entrance. In this experiment, bees with high sucrose acceptance thresholds showed significantly better learning and reversal learning than bees with low thresholds. These results demonstrate that sucrose acceptance thresholds affect only those forms of learning in which sucrose serves as the reward. The results also show that foraging behavior in the field is a good predictor for learning behavior in the field and in the laboratory.

Keywords: Apis mellifera; color learning; hive entrance learning; olfactory PER conditioning; retention; reward value; sucrose acceptance.

Figure 1

Color learning experiment at an artificial feeder in the field for bees which either had acceptance thresholds ≤3% or ≥50%. The bees could choose between a green and blue alternative (for details see text). The abscissa shows the spontaneous choice (spont), choice tests after seven learning trials on green, and retention after 24 h (24 h). The ordinate shows the mean percentages of approaches with the respective standard deviations for the rewarded green alternative. The stars indicate significant differences of the choice reaction in the 24-h retention test (2-sided t-test, p < 0.01); other significant differences are not indicated in the figure, for details see text. 20 bees were tested in each group. Bees in the 50% acceptance group made between 4 and 17 approaches in the tests, resulting in a total of 3143 approaches for this group. Bees in the 3% acceptance group made between 5 and 17 approaches in the tests, resulting in a total of 3370 approaches for this group.

Figure 2

PER responsiveness for different concentrations of sucrose in two groups of bees which either had acceptance thresholds ≤3% or ≥50% in the field. (A) Sucrose concentration dependence of the PER. The abscissa shows the applied stimuli starting from water to 50% sucrose. The ordinate shows the percentages of PER for each stimulus. (B) The gustatory response scores for the two groups (for details see text). The box plots show medians, means, quartiles, the whiskers indicate 95% percentiles. 35 bees were tested in the 3% acceptance group and 28 bees in the 50% acceptance group.

Figure 3

Olfactory PER conditioning for two groups of bees which either had acceptance thresholds ≤3% or ≥50% in the field. (A) The acquisition curves, discrimination, and 24-h retention in the two groups. The abscissa shows spontaneous choice (spont), tests after each of the seven learning trials, and 24-h retention (24h). The ordinate shows the percentages of PER to the conditioned odor cineol (CS+) and the alternative not rewarded odor clove oil (CS−). ** indicates a significant difference for the retention tests (Fischer's exact probability test, p < 0.01); other significant differences in the acquisition curves are not indicated (for details see text). (B) The acquisition scores for the two groups (for details see text). The box plots show medians, means, quartiles, the whiskers show 95% percentiles. ** indicates a significant difference between acquisition scores (Mann–Whitney U Test, p < 0.01). 35 bees were tested in the 3% acceptance group and 28 bees in the 50% acceptance group.

Figure 4

Color learning at the hive entrance for two groups of bees which had acceptance thresholds ≤3% or ≥30% in the field. The abscissa of both graphs show choice behavior before learning (spont), after 10 learning trials with a yellow plate marking the hive entrance (10× yellow), and after 10 reversal learning trials with a blue plate marking the hive entrance (10× blue). (A) The ordinate shows mean percentages of approaches and the respective standard deviations toward the yellow plate compared with the approaches toward a blue plate (for details see text). (B) The ordinate shows mean percentages of times and the respective standard deviations spent in front or on the yellow plate compared with the times for a blue plate (for details see text). Significant differences of Bonferroni multiple comparison tests (for comparisons within an acceptance group) and of 2-sided t-tests (between acceptance groups) are indicated (** p < 0.01; *** p < 0.001; for details see text). Fifteen bees were tested in each of the two acceptance groups.