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The influence of gustatory and olfactory experiences on responsiveness to reward in the honeybee.

Ramírez GP, Martínez AS, Fernández VM, Corti Bielsa G, Farina WM - PLoS ONE (2010)

Bottom Line: This adjustment is generally associated with the fact that individuals of different ages display different response thresholds to given stimuli, which determine specific behaviors.In contrast no differences in worker responses were observed when presented with odor only in the rearing environment.This work demonstrates the accessibility of chemosensory information in the honeybee colonies with respect to incoming nectar.

View Article: PubMed Central - PubMed

Affiliation: Grupo de Estudio de Insectos Sociales, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, IFIBYNE-CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina.

ABSTRACT

Background: Honeybees (Apis mellifera) exhibit an extraordinarily tuned division of labor that depends on age polyethism. This adjustment is generally associated with the fact that individuals of different ages display different response thresholds to given stimuli, which determine specific behaviors. For instance, the sucrose-response threshold (SRT) which largely depends on genetic factors may also be affected by the nectar sugar content. However, it remains unknown whether SRTs in workers of different ages and tasks can differ depending on gustatory and olfactory experiences.

Methodology: Groups of worker bees reared either in an artificial environment or else in a queen-right colony, were exposed to different reward conditions at different adult ages. Gustatory response scores (GRSs) and odor-memory retrieval were measured in bees that were previously exposed to changes in food characteristics.

Principal findings: Results show that the gustatory responses of pre-foraging-aged bees are affected by changes in sucrose solution concentration and also to the presence of an odor provided it is presented as scented sucrose solution. In contrast no differences in worker responses were observed when presented with odor only in the rearing environment. Fast modulation of GRSs was observed in older bees (12-16 days of age) which are commonly involved in food processing tasks within the hive, while slower modulation times were observed in younger bees (commonly nurse bees, 6-9 days of age). This suggests that older food-processing bees have a higher plasticity when responding to fluctuations in resource information than younger hive bees. Adjustments in the number of trophallaxis events were also found when scented food circulated inside the nest, and this was positively correlated with the differences in timing observed in gustatory responsiveness and memory retention for hive bees of different age classes.

Conclusions: This work demonstrates the accessibility of chemosensory information in the honeybee colonies with respect to incoming nectar. The modulation of the sensory-response systems within the hive can have important effects on the dynamics of food transfer and information propagation.

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Gustatory responsiveness after withdrawl of scented sucrose solution.Gustatory response score (GRS) of caged bees that were exposed during their whole adult lifespan (15 days) to a constant reward program of unscented 15% w/w sucrose solution (A). (B) GRSs of bees that were fed until 14 days of age with an unscented solution, then fed scented sucrose (LIO, 15% w/w) for 24 hours, and then again on unscented sucrose for the following 24 hours (i.e. 15th day). Asterisks indicate statistical differences (Kruskal-Wallis test, * p< 0.05, ** p<0.01, n.s. not significant; for details see the text). The number of observations is shown in parentheses. Boxes indicate the inter-quartile range, horizontal lines within boxes indicate the medians, whiskers include all points within 1.5 times the inter-quartiles, empty circles indicate outliers.
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pone-0013498-g004: Gustatory responsiveness after withdrawl of scented sucrose solution.Gustatory response score (GRS) of caged bees that were exposed during their whole adult lifespan (15 days) to a constant reward program of unscented 15% w/w sucrose solution (A). (B) GRSs of bees that were fed until 14 days of age with an unscented solution, then fed scented sucrose (LIO, 15% w/w) for 24 hours, and then again on unscented sucrose for the following 24 hours (i.e. 15th day). Asterisks indicate statistical differences (Kruskal-Wallis test, * p< 0.05, ** p<0.01, n.s. not significant; for details see the text). The number of observations is shown in parentheses. Boxes indicate the inter-quartile range, horizontal lines within boxes indicate the medians, whiskers include all points within 1.5 times the inter-quartiles, empty circles indicate outliers.

Mentions: Since only the 14-day-old caged honeybees showed an increase in their GRSs after being exposed to LIO-scented food for 24 h, the duration of this increased response was further investigated in bees of this age. GRSs of 14 day-old bees fed with an unscented sucrose solution did not differ over the 48 hour timescale tested (K–W: H = 0.514, p = 0.916, N = 107, Fig. 4A). In contrast, bees exposed to LIO-scented food showed evidence of changes in GRS (K–W: H = 13.24, p = 0.004, N = 131 Fig. 4B). Indeed, the GRSs of these bees increased significantly during 24 hours of stimulation (Dunn comparison: p<0.001; Fig. 4B left), a result consistent with those shown in Fig. 2F. However, these values significantly decreased 48 h from the beginning of stimulation, i.e. 24 h after withdrawing the LIO-scented food (24 h vs. 48 h: Dunn comparison: p<0.001; Fig. 4B right). Moreover, these GRSs were lower than GRSs of bees tested six hours after withdrawing the LIO-scented food (i.e., 30 h from the beginning of stimulation; Dunn comparison: p<0.05; Fig. 4B right). No significant differences were found between scores after 24 h of stimulation with LIO-scented food versus scores of bees tested six hours after replacing the scented solution by an unscented one, i.e. after 30 hours (Dunn comparison: p>0.2; Fig. 4B). This indicates that six hours after removal of the LIO-scented sucrose solution, GRSs had not yet dropped significantly from the level observed after 24 hours of exposure. However, GRSs did subsequently decrease between 6–24 hours after the LIO-scented sucrose was replaced by an unscented solution. In contrast, the elevated PER levels to the solution odor recorded after 24 hours of exposure to LIO-scented sucrose solution had not decreased significantly from this level 24 hours after withdrawing this scent cue (G-test: G = 22.86, p<0.00001, N = 246, Dunn comparison: 0 h vs. 24 h p<0.0001, 0 h vs. 30 h p<0.0001 and 0 h vs. 48 h p<0.001; Fig. 5).


The influence of gustatory and olfactory experiences on responsiveness to reward in the honeybee.

Ramírez GP, Martínez AS, Fernández VM, Corti Bielsa G, Farina WM - PLoS ONE (2010)

Gustatory responsiveness after withdrawl of scented sucrose solution.Gustatory response score (GRS) of caged bees that were exposed during their whole adult lifespan (15 days) to a constant reward program of unscented 15% w/w sucrose solution (A). (B) GRSs of bees that were fed until 14 days of age with an unscented solution, then fed scented sucrose (LIO, 15% w/w) for 24 hours, and then again on unscented sucrose for the following 24 hours (i.e. 15th day). Asterisks indicate statistical differences (Kruskal-Wallis test, * p< 0.05, ** p<0.01, n.s. not significant; for details see the text). The number of observations is shown in parentheses. Boxes indicate the inter-quartile range, horizontal lines within boxes indicate the medians, whiskers include all points within 1.5 times the inter-quartiles, empty circles indicate outliers.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2958144&req=5

pone-0013498-g004: Gustatory responsiveness after withdrawl of scented sucrose solution.Gustatory response score (GRS) of caged bees that were exposed during their whole adult lifespan (15 days) to a constant reward program of unscented 15% w/w sucrose solution (A). (B) GRSs of bees that were fed until 14 days of age with an unscented solution, then fed scented sucrose (LIO, 15% w/w) for 24 hours, and then again on unscented sucrose for the following 24 hours (i.e. 15th day). Asterisks indicate statistical differences (Kruskal-Wallis test, * p< 0.05, ** p<0.01, n.s. not significant; for details see the text). The number of observations is shown in parentheses. Boxes indicate the inter-quartile range, horizontal lines within boxes indicate the medians, whiskers include all points within 1.5 times the inter-quartiles, empty circles indicate outliers.
Mentions: Since only the 14-day-old caged honeybees showed an increase in their GRSs after being exposed to LIO-scented food for 24 h, the duration of this increased response was further investigated in bees of this age. GRSs of 14 day-old bees fed with an unscented sucrose solution did not differ over the 48 hour timescale tested (K–W: H = 0.514, p = 0.916, N = 107, Fig. 4A). In contrast, bees exposed to LIO-scented food showed evidence of changes in GRS (K–W: H = 13.24, p = 0.004, N = 131 Fig. 4B). Indeed, the GRSs of these bees increased significantly during 24 hours of stimulation (Dunn comparison: p<0.001; Fig. 4B left), a result consistent with those shown in Fig. 2F. However, these values significantly decreased 48 h from the beginning of stimulation, i.e. 24 h after withdrawing the LIO-scented food (24 h vs. 48 h: Dunn comparison: p<0.001; Fig. 4B right). Moreover, these GRSs were lower than GRSs of bees tested six hours after withdrawing the LIO-scented food (i.e., 30 h from the beginning of stimulation; Dunn comparison: p<0.05; Fig. 4B right). No significant differences were found between scores after 24 h of stimulation with LIO-scented food versus scores of bees tested six hours after replacing the scented solution by an unscented one, i.e. after 30 hours (Dunn comparison: p>0.2; Fig. 4B). This indicates that six hours after removal of the LIO-scented sucrose solution, GRSs had not yet dropped significantly from the level observed after 24 hours of exposure. However, GRSs did subsequently decrease between 6–24 hours after the LIO-scented sucrose was replaced by an unscented solution. In contrast, the elevated PER levels to the solution odor recorded after 24 hours of exposure to LIO-scented sucrose solution had not decreased significantly from this level 24 hours after withdrawing this scent cue (G-test: G = 22.86, p<0.00001, N = 246, Dunn comparison: 0 h vs. 24 h p<0.0001, 0 h vs. 30 h p<0.0001 and 0 h vs. 48 h p<0.001; Fig. 5).

Bottom Line: This adjustment is generally associated with the fact that individuals of different ages display different response thresholds to given stimuli, which determine specific behaviors.In contrast no differences in worker responses were observed when presented with odor only in the rearing environment.This work demonstrates the accessibility of chemosensory information in the honeybee colonies with respect to incoming nectar.

View Article: PubMed Central - PubMed

Affiliation: Grupo de Estudio de Insectos Sociales, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, IFIBYNE-CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina.

ABSTRACT

Background: Honeybees (Apis mellifera) exhibit an extraordinarily tuned division of labor that depends on age polyethism. This adjustment is generally associated with the fact that individuals of different ages display different response thresholds to given stimuli, which determine specific behaviors. For instance, the sucrose-response threshold (SRT) which largely depends on genetic factors may also be affected by the nectar sugar content. However, it remains unknown whether SRTs in workers of different ages and tasks can differ depending on gustatory and olfactory experiences.

Methodology: Groups of worker bees reared either in an artificial environment or else in a queen-right colony, were exposed to different reward conditions at different adult ages. Gustatory response scores (GRSs) and odor-memory retrieval were measured in bees that were previously exposed to changes in food characteristics.

Principal findings: Results show that the gustatory responses of pre-foraging-aged bees are affected by changes in sucrose solution concentration and also to the presence of an odor provided it is presented as scented sucrose solution. In contrast no differences in worker responses were observed when presented with odor only in the rearing environment. Fast modulation of GRSs was observed in older bees (12-16 days of age) which are commonly involved in food processing tasks within the hive, while slower modulation times were observed in younger bees (commonly nurse bees, 6-9 days of age). This suggests that older food-processing bees have a higher plasticity when responding to fluctuations in resource information than younger hive bees. Adjustments in the number of trophallaxis events were also found when scented food circulated inside the nest, and this was positively correlated with the differences in timing observed in gustatory responsiveness and memory retention for hive bees of different age classes.

Conclusions: This work demonstrates the accessibility of chemosensory information in the honeybee colonies with respect to incoming nectar. The modulation of the sensory-response systems within the hive can have important effects on the dynamics of food transfer and information propagation.

Show MeSH
Related in: MedlinePlus