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Nectar source profitability influences individual foraging preferences for pollen and pollen-foraging activity of honeybee colonies

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Abstract

Most foraging honeybees specialize in either pollen or nectar collection, although some do alternate between both resources. Little is known about this behavioral plasticity and the factors that control it. We studied how the profitability of nectar sources influences the transition of bees between nectar and pollen collection at the individual response level, by measuring the number of switches when the productivity of a sugar source (either sugar concentration or solution flow rate) was experimentally decreased or increased. At the social level, we studied whether the quality of the nectar that circulates inside a hive alters the rate of incoming pollen foragers. We then calculated the ratio between pollen and non-pollen foragers, before and after the hives were fed either a 3 or a 50% w/w sugar solution. In the first experiment, we showed that bees that persisted in visiting the feeder when offered low-quality solutions were more likely to switch to pollen than those foraging only on highly concentrated solutions. Looking at the collective responses, the ratio of pollen over non-pollen foragers increased after the input of a low-quality sugar solution and decreased after the input of a high-quality sugar solution. We conclude that the profitability of nectar sources interacts with the sugar responsiveness of bees, thus driving foraging preferences for pollen and modifying the pollen foraging activity of the colony. The results also show that bees integrate gustatory information from both rewarding resources based on local cues available either at the foraging site or inside the hive.

Significance statement

Switching between resource types could be adaptive for honeybees that specialize in either nectar or pollen foraging. This would allow them to react to changes in the foraging environment. Although we observed that switching behavior is constrained by the responsiveness of bees to sugar, the switch from nectar to pollen (and vice versa) is an active decision of the bees in response to the decreasing or increasing profitability of pollen versus nectar sources. Given the ability of some bees to switch between foraging tasks based solely on gustatory cues available at the foraging site, we investigated whether source-related information conveyed inside the hive also affects colony foraging activity towards nectar and pollen resources. We observed that behavioral plasticity of individuals can be integrated into a social response by colonies reallocating their foraging forces according to the food-related information available inside the hive.

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References

  • Arenas A, Farina WM (2012) Learned olfactory cues affect pollen-foraging preferences in honeybees, Apis mellifera. Anim Behav 83:1023–1033

    Article  Google Scholar 

  • Arenas A, Farina WM (2014) Bias to pollen odors is affected by early exposure and foraging experience. J Insect Physiol 66:28–36

    Article  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker B (2011) lme4: linear mixed effects model using S4 classes. R package version 0.999375–42

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  Google Scholar 

  • Camazine S (1993) The regulation of pollen foraging by honey bees: how foragers assess the colony’s need for pollen. Behav Ecol Sociobiol 32:265–272

    Article  Google Scholar 

  • Conti I, Medrzycki P, Argenti C, Meloni M, Vecchione V, Boi M, Mariotti MG (2016) Sugar and protein content in different monofloral pollens-building a database. B Insectol 69:318–320

  • Crailsheim K (1998) Trophallactic interactions in the adult honeybee (Apis mellifera L.). Apidologie 29:97–112

    Article  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, West Sussex

  • Dreller C, Page RE Jr, Fondrk MK (1999) Regulation of pollen foraging in honeybee colonies: effects of young brood, stored pollen, and empty space. Behav Ecol Sociobiol 45:227–233

    Article  Google Scholar 

  • Eckert CD, Winston ML, Ydenberg RC (1994) The relationship between population size, amount of brood, and individual foraging behaviour in the honey bee, Apis mellifera L. Oecologia 97:248–255

    Article  CAS  Google Scholar 

  • Farrar CL (1944) Productive management of honeybee colonies in the Northern States (No. Folleto 1645)

  • Fewell JH, Page RE (1993) Genotypic variation in foraging responses to environmental stimuli by honey bees, Apis mellifera. Cell Mol Life Sci 49:1106–1112

    Article  Google Scholar 

  • Fewell JH, Winston ML (1992) Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behav Ecol Sociobiol 30:387–393

    Article  Google Scholar 

  • Free JB (1963) The flower constancy of honeybees. J Anim Ecol 32:119–131

    Article  Google Scholar 

  • Free JB (1964) The behaviour of honeybees on sunflowers (Helianthus annuus L.). J Appl Ecol 1:19–27

    Article  Google Scholar 

  • Gil M, De Marco RJ, Menzel R (2007) Learning reward expectations in honeybees. Learn Mem 14:491–496

    Article  Google Scholar 

  • Grosclaude FE, Núñez JA (1998) Foraging pauses and their meaning as an economic strategy in the honeybee Apis mellifera L. J Comp Physiol A 183:61–68

    Article  Google Scholar 

  • Hanley ME, Franco M, Pichon S, Darvill B, Goulson D (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Funct Ecol 22:592–598

    Article  Google Scholar 

  • Herbert EW Jr, Shimanuki H (1978) Chemical composition and nutritive value of bee-collected and bee-stored pollen. apidologie 9:33–40

    Article  Google Scholar 

  • Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432. https://doi.org/10.2307/1934352

    Article  Google Scholar 

  • Hrassnigg N, Crailsheim K (1998) The influence of brood on the pollen consumption of worker bees (Apis mellifera L.). J Insect Physiol 44:393–404

    Article  CAS  Google Scholar 

  • Jeanne RL (1986) The evolution of the organization of work in social insects. Monit Zool Ital 20:19–33

  • Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Boulder

    Google Scholar 

  • Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33

    Article  Google Scholar 

  • Lindauer M (1952) Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z Vergi Physiol 34:299–345

    Article  Google Scholar 

  • Lindauer M (1955) The water economy and temperature regulation of the honeybee colony. Bee World 62-72(81–92):105–1I1

    Article  Google Scholar 

  • Martinez A, Farina WM (2008) Honeybees modify gustatory responsiveness after receiving nectar from foragers within the hive. Behav Ecol Sociobiol 62:529–535

    Article  Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models, vol 37. CRC press

  • Moeller FE (1961) The relationship between colony populations and honey production as affected by honey bee stock lines. Prod Res Rep US Dept Agric

  • Núñez JA (1977) Nectar flow by melliferous flora and gathering flow by Apis mellifera Ligustica. J Insect Physiol 23:265–275

    Article  Google Scholar 

  • Núñez JA (1979) Comparative study of thermoregu1ation between European and Africanized Apis mellifera in Brazil. J Apic Res 18:116–121

    Article  Google Scholar 

  • Nye WP, Mackensen O (1965) Preliminary report on selection and breeding of honeybees for alfalfa pollen collection. J Apic Res 4:43–48

    Article  Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton Univ Press, Princeton

    Google Scholar 

  • Page RE Jr, Erber J, Fondrk MK (1998) The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 182:489–500

    Article  Google Scholar 

  • Page RE Jr, Scheiner R, Erber J, Amdam GV (2006) The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr Top Dev Biol 74:253–286

    Article  CAS  Google Scholar 

  • Page RE, Robinson GE, Fondrk MK, Nasr M (1995) Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav Ecol Sociobiol 36:387–396

    Article  Google Scholar 

  • Pankiw T, Nelson M, Page RE, Fondrk MK (2004) The communal crop: modulation of sucrose response thresholds of pre-foraging honey bees with incoming nectar quality. Behav Ecol Sociobiol 55:286-292.

    Article  Google Scholar 

  • Pankiw T, Page RE Jr (2000) Response thresholds to sucrose predict foraging behavior in the honey bee (Apis mellifera L.). Behav Ecol Sociobiol 47:265–267

    Article  Google Scholar 

  • Pankiw T, Waddington KD, Page RE (2001) Modulation of sucrose response thresholds in honey bees (Apis mellifera L.): influence of genotype, feeding, and foraging experience. J Comp Physiol A 187:293–301

    Article  CAS  Google Scholar 

  • Percival MS (1955) The presentation of pollen in certain angio-sperms and tis collection by Apis mellifera. New Phytol 54:353–368

    Article  Google Scholar 

  • Pernal SF, Currie RW (2002) Discrimination and preferences for pollen-based cues by foraging honeybees, Apis mellifera L. Anim Behav 63:369–390

    Article  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna, Austria Available online at: http://www.R-project.org/

    Google Scholar 

  • Robinson GE, Page RE (1989) Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav Ecol Sociobiol 24:317–323

    Article  Google Scholar 

  • Rotjan R, Calderone N, Seeley T (2002) How a honey bee colony mustered additional labor for the task of pollen foraging. Apidologie 33:367–373

    Article  Google Scholar 

  • Scheiner R, Page RE, Erber J (2004) Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 35:133–142

    Article  Google Scholar 

  • Seeley TD (1985) Honey bee ccology: a stud in adaptation in social lie. Princeton Univ. Press, Princeton, NJ

  • Seeley TD (1986) Social foraging by honeybees: how colonies allocate foragers among patches of flowers. Behav Ecol Sociobiol 19:343–354

    Article  Google Scholar 

  • Seeley TD (1989) Social foraging in honey bees: how nectar foragers assess their colony's nutritional status. Behav Ecol Sociobiol 24:181–199

    Article  Google Scholar 

  • Seeley T (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge, Massachusetts

    Google Scholar 

  • Seeley TD, Towne WF (1992) Tactics of dance choice in honey bees: do foragers compare dances? Behav Ecol Sociobiol 30:59–69

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap Press of Harvard Univ Press, Cambridge

    Google Scholar 

  • Wilson EO (1985) The sociogenesis of insect colonies. Science 228:1489–1495

    Article  CAS  Google Scholar 

  • Winston ML (1987) The Biology of the Honey Bee. Harvard Univ. Press, Cambridge, MA

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) GLM and GAM for count data. In: Mixed effects models and extensions in ecology with R. Springer, New York, pp 209–243

    Chapter  Google Scholar 

Download references

Acknowledgements

We thank W. Farina for the fruitful comments and discussions at the early stage of this project and to MJ. Corriale for help with statistical analyses.

Funding

This study was partly supported by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and by grants from Agencia Nacional de Promoción Científica y Tecnológica (ANPCYT), University of Buenos Aires and CONICET to A. Arenas.

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Correspondence to Andrés Arenas.

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Figure 1S

Switching behaviour from pollen to sugar feeders of increasing sugar concentration. Percentage of labeled honeybees that changed their foraging preferences to sugar solutions throughout 4 tests of increasing concentrations. Bars show medians ± SE of 9 independent groups of bees. Different letters indicate statistically significant differences (p < 0.05; Tukey’s test). (PNG 165 kb)

High resolution image (EPS 68 kb)

Figure 2S

Ratio of incoming pollen over incoming non-pollen foragers according to the gustatory input offered into the hive. Ratio of incoming foragers with and without pollen loads were counted before (T0) and after (T1) the offering of 3% and 50% w/w sugar solutions or at the same time (T0 and T1) even when no solution was offered. Box plots show medians, quartiles and 5th and 95th percentiles from 19 hives. Asterisks indicate statistical differences among ratios (**p < 0.01; ***p < 0.001; simple effects). (PNG 87 kb)

High resolution image (EPS 73 kb)

Figure 3S

Sugar responsiveness of in-hive bees according to the quality of the sugar solution offered inside the hive. Mean proboscis extension response (PER) scores of bees captured from two groups of hives before (T0) and 60 min after (T1) they were fed either 3% or 50% w/w sugar solution. Box plots show medians, quartiles and 5th and 95th percentiles and outliers from 10 hives. Different letters indicate statistically significant differences among PER scores (p < 0.05; simple effects). (PNG 75 kb)

High resolution image (EPS 85 kb)

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Arenas, A., Kohlmaier, M.G. Nectar source profitability influences individual foraging preferences for pollen and pollen-foraging activity of honeybee colonies. Behav Ecol Sociobiol 73, 34 (2019). https://doi.org/10.1007/s00265-019-2644-5

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  • DOI: https://doi.org/10.1007/s00265-019-2644-5

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