Skip to main content
Log in

Effects of protein-constrained brood food on honey bee (Apis mellifera L.) pollen foraging and colony growth

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Pollen is the sole source of protein for honey bees, most importantly used to rear young. Honey bees are adept at regulating pollen stores in the colonies based on the needs of the colony. Mechanisms for regulation of pollen foraging in honey bee are complex and remain controversial. In this study, we used a novel approach to test the two competing hypothesis of pollen foraging regulation. We manipulated nurse bee biosynthesis of brood food using a protease inhibitor that interferes with midgut protein digestion, significantly decreasing the amount of protein extractable from hypopharyngeal glands. Experimental colonies were given equal amounts of protease inhibitor-treated and untreated pollen. Colonies receiving protease inhibitor treatment had significantly lower hypopharyngeal gland protein content than controls. There was no significant difference in the ratio of pollen to nonpollen foragers between the treatments. Pollen load weights were also not significantly different between treatments. Our results supported the pollen foraging effort predictions generated from the direct independent effects of pollen on the regulation of pollen foraging and did not support the prediction that nurse bees regulate pollen foraging through amount of hypopharyngeal gland protein biosynthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Al-Tikrity WS, Benton AW, Hillman RC, Clarke WW Jr (1972) The relationship between the amount of unsealed brood in honeybee colonies and their pollen collection. J Apic Res 11:9–12

    Google Scholar 

  • Allison PD (1998) Survival analysis using the SAS system. A practical guide. SAS Institute, Cary, NC

    Google Scholar 

  • Babendreier D, Kalberer N, Romeis J, Fluri P, Bigler F (2004) Pollen consumption in honey bee larvae: a step forward in the risk assessment of transgenic plants. Apidologie 35:293–300

    Article  Google Scholar 

  • Babendreier D, Kalberer NM, Romeis J, Fluri P, Mulligan E, Bigler F (2005) Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees. Apidologie 36:585–594

    Article  CAS  Google Scholar 

  • Barker RJ (1971) The influence of food inside the hive on pollen collection. J Apic Res 10:23–26

    Google Scholar 

  • Burgess EPJ, Malone LA, Christeller JT (1996) Effects of two proteinase inhibitors on the digestive enzymes and survival of honey bees (Apis mellifera). J Insect Physiol 42:823–828

    Article  CAS  Google Scholar 

  • Camazine S (1991) Self-organization pattern formation on the comb of honey bee colonies. Behav Ecol Sociobiol 28:61–76

    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 

  • Camazine S, Crailsheim K, Hrassnigg N, Robinson GE, Leonhard B, Kropiunigg H (1998) Protein trophallaxis and the regulation of pollen foraging by honey bees (Apis mellifera L.) Apidologie 29:113–126

    CAS  Google Scholar 

  • Cole BJ (1984) Colony efficiency and the reproductivity effect in Leptothorax allardycei (Mann.). Insectes Soc 31:403–407

    Article  Google Scholar 

  • Danka RG, Hellmich II, Rinderer TE, Collins AM (1987) Diet selection ecology of tropically and temperately adapted honey bees. Anim Behav 35:1858–1863

    Article  Google Scholar 

  • Dreller C, Tarpy DR (2000) Perception of the pollen need by foragers in a honeybee colony. Anim Behav 59:91–96

    Article  Google Scholar 

  • Dreller C, Page RE, 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  Google Scholar 

  • Farrar CL (1944) Productive management of honeybee colonies in the Northern States, vol 702. USDA Circular, pp 28

  • 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 

  • Fewell JH, Bertram SM (1999) Division of labor in a dynamic environment: response by honeybees (Apis mellifera) to graded changes in colony pollen stores. Behav Ecol Sociobiol 46:171–179

    Article  Google Scholar 

  • Filmer RS (1932) Brood area and colony size as factors in activity of pollination units. J Econ Entomol 25:336–343

    Google Scholar 

  • Free JB (1967) Factors determining the collection of pollen by honeybee foragers. Anim Behav 15:134–144

    Article  PubMed  CAS  Google Scholar 

  • Free JB (1979) Managing honeybee colonies to enhance the pollen-gathering stimulus from brood pheromones. Appl Anim Ethol 5:173–178

    Article  Google Scholar 

  • Free JB, Racey PA (1968) The effect of the size of honeybee colonies on food consumption, brood rearing, and the longevity of the bees during winter. Entomol Exp Appl 11:241–249

    Article  Google Scholar 

  • Huang Z-Y, Robinson GE (1992) Honeybee colony integration: worker-interactions mediate hormonally regulated plasticity in division of labor. Proc Natl Acad Sci USA 89:11726–11729

    Article  PubMed  CAS  Google Scholar 

  • Korpela S, Aarhus A, Fries I, Hansen H (1992) Varroa jacobsoni Oud. in cold climates: population growth, winter mortality and influence on the survival of honey bee colonies. J Apic Res 31:157–164

    Google Scholar 

  • Le Conte Y, Mohammedi A, Robinson GE (2001) Primer effects of a brood pheromone on honeybee behavioural development. Proc R Soc Lond B 268:1–6

    Article  Google Scholar 

  • Lee PC, Winston ML (1987) Effects of reproductive timing and colony size on survival, offspring colony size and drone production in the honey bee (Apis mellifera L.). Ecol Entomol 12:187–195

    Google Scholar 

  • Little M (1979) Mischocyttaerus flayipes in Arizona: social and nesting biology of a polistine wasp. Z Tierpsychol 50:282–312

    Google Scholar 

  • Malone LA, Burgess EPJ, Gatehouse HS, Voisey CR, Tregidga EL, Philip BA (2001) Effects of ingestion of a Bacillus thuringiensis toxin and a trypsin inhibitor on honey bee flight activity and longevity. Apidologie 32:57–68

    Article  CAS  Google Scholar 

  • Michaud D, Cantin L, Vrain TC (1995) Carboxy-terminal truncation of oryzacystatin-II by oryzacystatin-insensitive insect digestive proteinases. Arch Biochem Biophys 322:469–474

    Article  PubMed  CAS  Google Scholar 

  • Michener CD (1964) Reproductive efficiency in relation to colony size in hymenopterous societies. Insectes Soc 11:317–342

    Article  Google Scholar 

  • Mitchell SD (2002) Integrative pluralism. Biol Philos 17:55–70

    Article  Google Scholar 

  • Moeller FE (1958) The relation between egg-laying capacity of queen bee and population as affected by honeybee stock-lines. Am Bee J 98:401–402

    Google Scholar 

  • Moeller FE (1961) The relationship between colony populations and honey production as affected by honeybee stock-lines. In: Production Research of USDA, pp 55

  • Moeller FE (1972) Honey bee collection of corn pollen reduced by feeding pollen in the hive. Am Bee J 112:210–212

    Google Scholar 

  • Nelson DL, Jay SC (1972) Population growth and honey yield studies of package bee colonies in Manitoba. II. Colonies initiated with four package sizes on one date. Manit Entomol 6:17–22

    Google Scholar 

  • Page RE, Mitchell SR (1998) Self organization and the evolution of division of labor. Apidologie 29:101–120

    Google Scholar 

  • Page RE, Erber J (2002) Levels of behavioral organization and the evolution of division of labor. Naturwissenschaften 89:91–106

    Article  PubMed  CAS  Google Scholar 

  • Pankiw T (2003) Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (Apis mellifera L.). Behav Ecol Sociobiol 54:458–464

    Article  Google Scholar 

  • Pankiw T (2004a) Cued in: honey bee pheromones as information flow and colony decision-making. Apidologie 35:217–226

    Article  Google Scholar 

  • Pankiw T (2004b) Worker honey bee pheromone regulation of foraging ontogeny. Naturwissenschaften 91:178–181

    Article  PubMed  CAS  Google Scholar 

  • Pankiw T (2004c) Brood pheromone regulates foraging activity of honey bees (Hymenoptera: Apidae). J Econ Entomol 97:748–751

    Article  PubMed  Google Scholar 

  • Pankiw T, Page RE (2001) Brood pheromone modulates sucrose response thresholds in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 49:206–213

    Article  Google Scholar 

  • Pankiw T, Rubink WL (2002) Pollen foraging response to brood pheromone by Africanized and European honey bees (Apis mellifera L.). Ann Entomol Soc Am 95:761–767

    Article  Google Scholar 

  • Pankiw T, Page RE, Fondrk MK (1998) Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav Ecol Sociobiol 44:193–198

    Article  Google Scholar 

  • Pankiw T, Roman R, Sagili RR, Zhu-Salzman K (2004) Pheromone-modulated behavioral suites influence colony growth in the honey bee (Apis mellifera). Naturwissenschaften 91:575–578

    Article  PubMed  CAS  Google Scholar 

  • Pomeroy N (1979) Brood bionomics of Bombus ruderatus in New Zealand (Hymenoptera: Apidae) Can Entomol 111:865–874

    Google Scholar 

  • Richards OW, Richards WJ (1951) Observations on the social wasps in South America (Hymenoptera: Vespidae). Trans R Entomol Soc 102:1–170

    Google Scholar 

  • Sagili RR, Pankiw T, Zhu-Salzman K (2005) Effects of soybean trypsin inhibitor on hypopharyngeal gland protein content, total midgut protease activity and survival of the honey bee (Apis mellifera L.). J Insect Physiol 51:953–957

    Article  PubMed  CAS  Google Scholar 

  • SAS (2000) The SAS system version 8.01. SAS Institute Inc., Cary, NC

    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 

  • Schulz DJ, Robinson GE (2002) Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187:53–61

    Article  Google Scholar 

  • Schulz DJ, Huang Z-Y, Robinson GE (1998) Effects of colony food shortage on behavior development in honey bees. Behav Ecol Sociobiol 42:295–303

    Article  Google Scholar 

  • Seeley TD (1985a) Honeybee ecology. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Seeley TD (1985b) The information-center strategy of honeybee foraging. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology. Fischer, New York, pp 75–90

    Google Scholar 

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

    Google Scholar 

  • Seeley TD, Visscher PK (1985) Survival of honey bees in cold climates: timing of colony growth and reproduction. Ecol Entomol 10:81–88

    Google Scholar 

  • Seeley TD, Camazine S, Sneyd J (1991) Collective decision-making in honey bees: how colonies choose among nectar sources. Behav Ecol Sociobiol 28:277–290

    Article  Google Scholar 

  • Sherman PW (1988) The levels of analysis. Anim Behav 36:616–619

    Article  Google Scholar 

  • Smirl CB, Jay SC (1972) Population growth and honey yield studies of package bee colonies in Manitoba. I. Colonies initiated with two package sizes on three dates. Manit Entomol 6:9–16

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York

    Google Scholar 

  • SPSS (2000) SPSS for Windows, Version 13.0, SPSS Inc., Chicago

  • Tofts C, Franks NR (1992) Doing the right thing: ants, honeybees and naked mole-rats. Trends Ecol Evol 7:346–349

    Article  Google Scholar 

  • Weidenmüller A, Tautz J (2002) In-hive behavior of pollen foragers (Apis mellifera) in honey bee colonies under conditions of high and low pollen need. Ethology 108:205–221

    Article  Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge, MA

    Google Scholar 

Download references

Acknowledgements

This research was supported by grants from the USDA 58-6204-1-009, 2004-35302-15031 and the Almond Board of California to T Pankiw, as well as support from the Texas Honey Bee Legislative Initiative. Appreciated assistance was provided by Keyan Zhu-Salzman, GW Burlin, and Brad Metz. Bees were handled in compliance with current laws of the United States of America.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ramesh R. Sagili.

Additional information

Communicated by R.F.A. Moritz

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sagili, R.R., Pankiw, T. Effects of protein-constrained brood food on honey bee (Apis mellifera L.) pollen foraging and colony growth. Behav Ecol Sociobiol 61, 1471–1478 (2007). https://doi.org/10.1007/s00265-007-0379-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-007-0379-1

Keywords

Navigation