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Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults.

Scofield HN, Mattila HR - PLoS ONE (2015)

Bottom Line: The negative effects on adult behavior of juvenile undernourishment are well documented in vertebrates, but relatively poorly understood in invertebrates.Pollen stress during larval development had far-reaching physical and behavioral effects on adult workers.Furthermore, the effects of brief pollen shortages reported here mirror the effects of other environmental stressors that limit worker access to nutrients, suggesting the likelihood of their synergistic interaction.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Wellesley College, Wellesley, Massachusetts, United States of America.

ABSTRACT
The negative effects on adult behavior of juvenile undernourishment are well documented in vertebrates, but relatively poorly understood in invertebrates. We examined the effects of larval nutritional stress on the foraging and recruitment behavior of an economically important model invertebrate, the honey bee (Apis mellifera). Pollen, which supplies essential nutrients to developing workers, can become limited in colonies because of seasonal dearths, loss of foraging habitat, or intensive management. However, the functional consequences of being reared by pollen-stressed nestmates remain unclear, despite growing concern that poor nutrition interacts with other stressors to exacerbate colony decline. We manipulated nurse bees' access to pollen and then assessed differences in weight, longevity, foraging activity, and waggle-dance behavior of the workers that they reared (who were co-fostered as adults). Pollen stress during larval development had far-reaching physical and behavioral effects on adult workers. Workers reared in pollen-stressed colonies were lighter and shorter lived than nestmates reared with adequate access to pollen. Proportionally fewer stressed workers were observed foraging and those who did forage started foraging sooner, foraged for fewer days, and were more likely to die after only a single day of foraging. Pollen-stressed workers were also less likely to waggle dance than their unstressed counterparts and, if they danced, the information they conveyed about the location of food was less precise. These performance deficits may escalate if long-term pollen limitation prevents stressed foragers from providing sufficiently for developing workers. Furthermore, the effects of brief pollen shortages reported here mirror the effects of other environmental stressors that limit worker access to nutrients, suggesting the likelihood of their synergistic interaction. Honey bees often experience the level of stress that we created, thus our findings underscore the importance of adequate nutrition for supporting worker performance and their potential contribution to colony productivity and quality pollination services.

No MeSH data available.


Related in: MedlinePlus

Waggle-dance behavior of adult workers was not affected by access to pollen when focal workers were larvae.Provided are mean per dancer measures of dance performance (± SEM) as focal individuals foraged at unknown food sources in trial 3. All workers were uniquely tagged and individually identifiable. Waggle-dance activity was monitored for 1–2 h/day (as weather and foraging permitted) from the time that workers were min. 12 days to max. 45 days of age (see gray box in Fig. 2). Means were calculated considering only those workers who danced (i.e., zero values were not included for non-foraging or non-dancing focal workers; n = 9 workers reared in pollen-limited, confined colonies; n = 66 workers reared in abundantly supplied, confined controls; n = 41 workers reared in abundantly supplied, unconfined controls). Mean waggle-run duration (number of frames at 30 frames per second, a proxy for distance to advertised food source) was estimated for the first dance performed by each pollen-limited worker and compared to means for the first dances performed by control workers during the same hours of videotape (n = 9 workers reared in pollen-limited, confined colony subunits; n = 20 workers reared in abundantly supplied, confined controls; n = 13 workers reared in abundantly supplied, unconfined controls).
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pone.0121731.g003: Waggle-dance behavior of adult workers was not affected by access to pollen when focal workers were larvae.Provided are mean per dancer measures of dance performance (± SEM) as focal individuals foraged at unknown food sources in trial 3. All workers were uniquely tagged and individually identifiable. Waggle-dance activity was monitored for 1–2 h/day (as weather and foraging permitted) from the time that workers were min. 12 days to max. 45 days of age (see gray box in Fig. 2). Means were calculated considering only those workers who danced (i.e., zero values were not included for non-foraging or non-dancing focal workers; n = 9 workers reared in pollen-limited, confined colonies; n = 66 workers reared in abundantly supplied, confined controls; n = 41 workers reared in abundantly supplied, unconfined controls). Mean waggle-run duration (number of frames at 30 frames per second, a proxy for distance to advertised food source) was estimated for the first dance performed by each pollen-limited worker and compared to means for the first dances performed by control workers during the same hours of videotape (n = 9 workers reared in pollen-limited, confined colony subunits; n = 20 workers reared in abundantly supplied, confined controls; n = 13 workers reared in abundantly supplied, unconfined controls).

Mentions: Once engaged in dancing, the level of pollen stress that workers experienced during development did not affect the amount of dancing that they did, but it did affect the precision of their dances. As tagged workers foraged at unknown food sources, the mean total number of days that each focal dancer danced, the total number of dances observed per dancer over those days, the total waggle runs performed, mean number of waggle runs per dance, and mean waggle-run duration (a proxy for distance to advertised food sources) did not differ across treatments (Fig. 3; F2,113 = 0.3, P = 0.72; F2,113 = 0.1, P = 0.88; F2,113 = 0.6, P = 0.58; F2,113 = 1.1, P = 0.33; F2,39 = 1.2, P = 0.32; respectively). Similarly, paint-marked and tagged workers from all treatments performed similar numbers of waggle runs upon return from the sucrose-solution feeder (Fig. 4; based on the number of painted and tagged workers: 27 dances performed by at least 6 different workers reared in pollen-limited colonies, 63 dances by at least 18 different workers from confined control colonies, and 35 dances by at least 9 different workers from unconfined control colonies; F2,122 = 2.2, P = 0.11). However, feeder dances performed by pollen-limited workers conveyed more variable information about the direction of the feeder (i.e., angles of waggle runs in each dance) than dances performed by control workers (Fig. 4; F2,122 = 5.7, P = 0.002). Variability in the distance component of the dances (i.e., durations of waggle runs in each dance) was similar among treatments (Fig. 4; F2,122 = 0.4, P = 0.88).


Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults.

Scofield HN, Mattila HR - PLoS ONE (2015)

Waggle-dance behavior of adult workers was not affected by access to pollen when focal workers were larvae.Provided are mean per dancer measures of dance performance (± SEM) as focal individuals foraged at unknown food sources in trial 3. All workers were uniquely tagged and individually identifiable. Waggle-dance activity was monitored for 1–2 h/day (as weather and foraging permitted) from the time that workers were min. 12 days to max. 45 days of age (see gray box in Fig. 2). Means were calculated considering only those workers who danced (i.e., zero values were not included for non-foraging or non-dancing focal workers; n = 9 workers reared in pollen-limited, confined colonies; n = 66 workers reared in abundantly supplied, confined controls; n = 41 workers reared in abundantly supplied, unconfined controls). Mean waggle-run duration (number of frames at 30 frames per second, a proxy for distance to advertised food source) was estimated for the first dance performed by each pollen-limited worker and compared to means for the first dances performed by control workers during the same hours of videotape (n = 9 workers reared in pollen-limited, confined colony subunits; n = 20 workers reared in abundantly supplied, confined controls; n = 13 workers reared in abundantly supplied, unconfined controls).
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Related In: Results  -  Collection

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pone.0121731.g003: Waggle-dance behavior of adult workers was not affected by access to pollen when focal workers were larvae.Provided are mean per dancer measures of dance performance (± SEM) as focal individuals foraged at unknown food sources in trial 3. All workers were uniquely tagged and individually identifiable. Waggle-dance activity was monitored for 1–2 h/day (as weather and foraging permitted) from the time that workers were min. 12 days to max. 45 days of age (see gray box in Fig. 2). Means were calculated considering only those workers who danced (i.e., zero values were not included for non-foraging or non-dancing focal workers; n = 9 workers reared in pollen-limited, confined colonies; n = 66 workers reared in abundantly supplied, confined controls; n = 41 workers reared in abundantly supplied, unconfined controls). Mean waggle-run duration (number of frames at 30 frames per second, a proxy for distance to advertised food source) was estimated for the first dance performed by each pollen-limited worker and compared to means for the first dances performed by control workers during the same hours of videotape (n = 9 workers reared in pollen-limited, confined colony subunits; n = 20 workers reared in abundantly supplied, confined controls; n = 13 workers reared in abundantly supplied, unconfined controls).
Mentions: Once engaged in dancing, the level of pollen stress that workers experienced during development did not affect the amount of dancing that they did, but it did affect the precision of their dances. As tagged workers foraged at unknown food sources, the mean total number of days that each focal dancer danced, the total number of dances observed per dancer over those days, the total waggle runs performed, mean number of waggle runs per dance, and mean waggle-run duration (a proxy for distance to advertised food sources) did not differ across treatments (Fig. 3; F2,113 = 0.3, P = 0.72; F2,113 = 0.1, P = 0.88; F2,113 = 0.6, P = 0.58; F2,113 = 1.1, P = 0.33; F2,39 = 1.2, P = 0.32; respectively). Similarly, paint-marked and tagged workers from all treatments performed similar numbers of waggle runs upon return from the sucrose-solution feeder (Fig. 4; based on the number of painted and tagged workers: 27 dances performed by at least 6 different workers reared in pollen-limited colonies, 63 dances by at least 18 different workers from confined control colonies, and 35 dances by at least 9 different workers from unconfined control colonies; F2,122 = 2.2, P = 0.11). However, feeder dances performed by pollen-limited workers conveyed more variable information about the direction of the feeder (i.e., angles of waggle runs in each dance) than dances performed by control workers (Fig. 4; F2,122 = 5.7, P = 0.002). Variability in the distance component of the dances (i.e., durations of waggle runs in each dance) was similar among treatments (Fig. 4; F2,122 = 0.4, P = 0.88).

Bottom Line: The negative effects on adult behavior of juvenile undernourishment are well documented in vertebrates, but relatively poorly understood in invertebrates.Pollen stress during larval development had far-reaching physical and behavioral effects on adult workers.Furthermore, the effects of brief pollen shortages reported here mirror the effects of other environmental stressors that limit worker access to nutrients, suggesting the likelihood of their synergistic interaction.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Wellesley College, Wellesley, Massachusetts, United States of America.

ABSTRACT
The negative effects on adult behavior of juvenile undernourishment are well documented in vertebrates, but relatively poorly understood in invertebrates. We examined the effects of larval nutritional stress on the foraging and recruitment behavior of an economically important model invertebrate, the honey bee (Apis mellifera). Pollen, which supplies essential nutrients to developing workers, can become limited in colonies because of seasonal dearths, loss of foraging habitat, or intensive management. However, the functional consequences of being reared by pollen-stressed nestmates remain unclear, despite growing concern that poor nutrition interacts with other stressors to exacerbate colony decline. We manipulated nurse bees' access to pollen and then assessed differences in weight, longevity, foraging activity, and waggle-dance behavior of the workers that they reared (who were co-fostered as adults). Pollen stress during larval development had far-reaching physical and behavioral effects on adult workers. Workers reared in pollen-stressed colonies were lighter and shorter lived than nestmates reared with adequate access to pollen. Proportionally fewer stressed workers were observed foraging and those who did forage started foraging sooner, foraged for fewer days, and were more likely to die after only a single day of foraging. Pollen-stressed workers were also less likely to waggle dance than their unstressed counterparts and, if they danced, the information they conveyed about the location of food was less precise. These performance deficits may escalate if long-term pollen limitation prevents stressed foragers from providing sufficiently for developing workers. Furthermore, the effects of brief pollen shortages reported here mirror the effects of other environmental stressors that limit worker access to nutrients, suggesting the likelihood of their synergistic interaction. Honey bees often experience the level of stress that we created, thus our findings underscore the importance of adequate nutrition for supporting worker performance and their potential contribution to colony productivity and quality pollination services.

No MeSH data available.


Related in: MedlinePlus