Behavioral Ecology and Sociobiology

, Volume 61, Issue 9, pp 1471–1478 | Cite as

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

Original Paper


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.


Honey bee Pollen foraging Protease inhibitor Brood food Hypopharyngeal glands 


  1. 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 11:9–12Google Scholar
  2. Allison PD (1998) Survival analysis using the SAS system. A practical guide. SAS Institute, Cary, NCGoogle Scholar
  3. 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 35:293–300CrossRefGoogle Scholar
  4. 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 36:585–594CrossRefGoogle Scholar
  5. Barker RJ (1971) The influence of food inside the hive on pollen collection. J Apic Res 10:23–26Google Scholar
  6. 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 42:823–828CrossRefGoogle Scholar
  7. Camazine S (1991) Self-organization pattern formation on the comb of honey bee colonies. Behav Ecol Sociobiol 28:61–76CrossRefGoogle Scholar
  8. Camazine S (1993) The regulation of pollen foraging by honey bees: how foragers assess the colony’s need for pollen. Behav Ecol Sociobiol 32:265–272CrossRefGoogle Scholar
  9. 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 29:113–126Google Scholar
  10. Cole BJ (1984) Colony efficiency and the reproductivity effect in Leptothorax allardycei (Mann.). Insectes Soc 31:403–407CrossRefGoogle Scholar
  11. Danka RG, Hellmich II, Rinderer TE, Collins AM (1987) Diet selection ecology of tropically and temperately adapted honey bees. Anim Behav 35:1858–1863CrossRefGoogle Scholar
  12. Dreller C, Tarpy DR (2000) Perception of the pollen need by foragers in a honeybee colony. Anim Behav 59:91–96CrossRefGoogle Scholar
  13. 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 45:227–233CrossRefGoogle Scholar
  14. 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 97:248–255CrossRefGoogle Scholar
  15. Farrar CL (1944) Productive management of honeybee colonies in the Northern States, vol 702. USDA Circular, pp 28Google Scholar
  16. Fewell JH, Winston ML (1992) Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behav Ecol Sociobiol 30:387–393CrossRefGoogle Scholar
  17. 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 46:171–179CrossRefGoogle Scholar
  18. Filmer RS (1932) Brood area and colony size as factors in activity of pollination units. J Econ Entomol 25:336–343Google Scholar
  19. Free JB (1967) Factors determining the collection of pollen by honeybee foragers. Anim Behav 15:134–144PubMedCrossRefGoogle Scholar
  20. Free JB (1979) Managing honeybee colonies to enhance the pollen-gathering stimulus from brood pheromones. Appl Anim Ethol 5:173–178CrossRefGoogle Scholar
  21. 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 11:241–249CrossRefGoogle Scholar
  22. Huang Z-Y, Robinson GE (1992) Honeybee colony integration: worker-interactions mediate hormonally regulated plasticity in division of labor. Proc Natl Acad Sci USA 89:11726–11729PubMedCrossRefGoogle Scholar
  23. 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 31:157–164Google Scholar
  24. Le Conte Y, Mohammedi A, Robinson GE (2001) Primer effects of a brood pheromone on honeybee behavioural development. Proc R Soc Lond B 268:1–6CrossRefGoogle Scholar
  25. 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 12:187–195Google Scholar
  26. Little M (1979) Mischocyttaerus flayipes in Arizona: social and nesting biology of a polistine wasp. Z Tierpsychol 50:282–312Google Scholar
  27. 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 32:57–68CrossRefGoogle Scholar
  28. Michaud D, Cantin L, Vrain TC (1995) Carboxy-terminal truncation of oryzacystatin-II by oryzacystatin-insensitive insect digestive proteinases. Arch Biochem Biophys 322:469–474PubMedCrossRefGoogle Scholar
  29. Michener CD (1964) Reproductive efficiency in relation to colony size in hymenopterous societies. Insectes Soc 11:317–342CrossRefGoogle Scholar
  30. Mitchell SD (2002) Integrative pluralism. Biol Philos 17:55–70CrossRefGoogle Scholar
  31. Moeller FE (1958) The relation between egg-laying capacity of queen bee and population as affected by honeybee stock-lines. Am Bee J 98:401–402Google Scholar
  32. Moeller FE (1961) The relationship between colony populations and honey production as affected by honeybee stock-lines. In: Production Research of USDA, pp 55Google Scholar
  33. Moeller FE (1972) Honey bee collection of corn pollen reduced by feeding pollen in the hive. Am Bee J 112:210–212Google Scholar
  34. 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 6:17–22Google Scholar
  35. Page RE, Mitchell SR (1998) Self organization and the evolution of division of labor. Apidologie 29:101–120Google Scholar
  36. Page RE, Erber J (2002) Levels of behavioral organization and the evolution of division of labor. Naturwissenschaften 89:91–106PubMedCrossRefGoogle Scholar
  37. Pankiw T (2003) Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (Apis mellifera L.). Behav Ecol Sociobiol 54:458–464CrossRefGoogle Scholar
  38. Pankiw T (2004a) Cued in: honey bee pheromones as information flow and colony decision-making. Apidologie 35:217–226CrossRefGoogle Scholar
  39. Pankiw T (2004b) Worker honey bee pheromone regulation of foraging ontogeny. Naturwissenschaften 91:178–181PubMedCrossRefGoogle Scholar
  40. Pankiw T (2004c) Brood pheromone regulates foraging activity of honey bees (Hymenoptera: Apidae). J Econ Entomol 97:748–751PubMedCrossRefGoogle Scholar
  41. Pankiw T, Page RE (2001) Brood pheromone modulates sucrose response thresholds in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 49:206–213CrossRefGoogle Scholar
  42. Pankiw T, Rubink WL (2002) Pollen foraging response to brood pheromone by Africanized and European honey bees (Apis mellifera L.). Ann Entomol Soc Am 95:761–767CrossRefGoogle Scholar
  43. Pankiw T, Page RE, Fondrk MK (1998) Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav Ecol Sociobiol 44:193–198CrossRefGoogle Scholar
  44. Pankiw T, Roman R, Sagili RR, Zhu-Salzman K (2004) Pheromone-modulated behavioral suites influence colony growth in the honey bee (Apis mellifera). Naturwissenschaften 91:575–578PubMedCrossRefGoogle Scholar
  45. Pomeroy N (1979) Brood bionomics of Bombus ruderatus in New Zealand (Hymenoptera: Apidae) Can Entomol 111:865–874Google Scholar
  46. Richards OW, Richards WJ (1951) Observations on the social wasps in South America (Hymenoptera: Vespidae). Trans R Entomol Soc 102:1–170Google Scholar
  47. 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 51:953–957PubMedCrossRefGoogle Scholar
  48. SAS (2000) The SAS system version 8.01. SAS Institute Inc., Cary, NCGoogle Scholar
  49. Scheiner R, Page RE, Erber J (2004) Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 35:133–142CrossRefGoogle Scholar
  50. Schulz DJ, Robinson GE (2002) Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187:53–61CrossRefGoogle Scholar
  51. Schulz DJ, Huang Z-Y, Robinson GE (1998) Effects of colony food shortage on behavior development in honey bees. Behav Ecol Sociobiol 42:295–303CrossRefGoogle Scholar
  52. Seeley TD (1985a) Honeybee ecology. Princeton University Press, Princeton, NJGoogle Scholar
  53. Seeley TD (1985b) The information-center strategy of honeybee foraging. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology. Fischer, New York, pp 75–90Google Scholar
  54. Seeley TD (1995) The wisdom of the hive. The social physiology of honey bee colonies. Harvard University Press, Cambridge, MAGoogle Scholar
  55. Seeley TD, Visscher PK (1985) Survival of honey bees in cold climates: timing of colony growth and reproduction. Ecol Entomol 10:81–88Google Scholar
  56. Seeley TD, Camazine S, Sneyd J (1991) Collective decision-making in honey bees: how colonies choose among nectar sources. Behav Ecol Sociobiol 28:277–290CrossRefGoogle Scholar
  57. Sherman PW (1988) The levels of analysis. Anim Behav 36:616–619CrossRefGoogle Scholar
  58. 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 6:9–16Google Scholar
  59. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New YorkGoogle Scholar
  60. SPSS (2000) SPSS for Windows, Version 13.0, SPSS Inc., ChicagoGoogle Scholar
  61. Tofts C, Franks NR (1992) Doing the right thing: ants, honeybees and naked mole-rats. Trends Ecol Evol 7:346–349CrossRefGoogle Scholar
  62. 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 108:205–221CrossRefGoogle Scholar
  63. Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge, MAGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of EntomologyTexas A&M UniversityCollege StationUSA

Personalised recommendations