Advertisement

Behavioral Ecology and Sociobiology

, Volume 64, Issue 6, pp 955–966 | Cite as

Sensory allometry, foraging task specialization and resource exploitation in honeybees

  • Andre J. Riveros
  • Wulfila Gronenberg
Original Paper

Abstract

Insect societies are important models for evolutionary biology and sociobiology. The complexity of some eusocial insect societies appears to arise from self-organized task allocation and group cohesion. One of the best-supported models explaining self-organized task allocation in social insects is the response threshold model, which predicts specialization due to inter-individual variability in sensitivity to task-associated stimuli. The model explains foraging task specialization among honeybee workers, but the factors underlying the differences in individual sensitivity remain elusive. Here, we propose that in honeybees, sensory sensitivity correlates with individual differences in the number of sensory structures, as it does in solitary species. Examining European and Africanized honeybees, we introduce and test the hypothesis that body size and/or sensory allometry is associated with foraging task preferences and resource exploitation. We focus on common morphological measures and on the size and number of structures associated with olfactory sensitivity. We show that the number of olfactory sensilla is greater in pollen and water foragers, which are known to exhibit higher sensory sensitivity, compared to nectar foragers. These differences are independent of the distribution of size within a colony. Our data also suggest that body mass and number of olfactory sensilla correlate with the concentration of nectar gathered by workers, and with the size of pollen loads they carry. We conclude that sensory allometry, but not necessarily body size, is associated with resource exploitation in honeybees and that the differences in number of sensilla may underlie the observed differences in sensitivity between bees specialized on water, pollen and nectar collection.

Keywords

Response threshold model Pollen syndrome Social insects Apis mellifera Division of labor Self-organization 

Notes

Acknowledgments

We thank Jorge Palacios for helping to collect bees, Ashley Wiede, Jonathan Kim, Chirag Patel, and Elizabeth Collier for preparing samples, taking pictures, and measuring bees. We thank Fabiola Santos for help measuring pollen loads. We thank Angelique Paulk for helpful suggestions on methods and Ruben Alarcon for help with the statistical analysis. We thank Gloria Degrandi-Hoffman and the USDA Carl Hayden Honey Bee Research Center for generously providing us with European honeybees. We thank Ruben Alarcon, Daniel Papaj, Diana Wheeler and two anonymous reviewers for constructive criticisms that contributed to improve this manuscript. This work was supported by a grant of the National Science Foundation of the United States of America (IOB-0519483) to WG. Additional support was provided by the Center for Insect Science (University of Arizona) to AJR.

References

  1. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  2. Apfelbach R, Russ D, Slotnick BM (1991) Ontogenetic changes in odor sensitivity, olfactory receptor area and olfactory receptor density in the rat. Chem Sens 16:209–218CrossRefGoogle Scholar
  3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300Google Scholar
  4. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440CrossRefPubMedGoogle Scholar
  5. Beshers SN, Robinson GE, Mittenthal JE (1999) Response thresholds and division of labor in insect colonies. In: Detrain C, Deneubourg JL, Pasteels JM (eds) Information processing in social insects. Birkhauser, Basel, pp 115–139Google Scholar
  6. Bonabeau E, Theraulaz G, Deneubourg JL, Aron S, Camazine S (1997) Self-organization in social insects. Trends Ecol Evol 12:188–193CrossRefGoogle Scholar
  7. Bonabeau E, Theraulaz G, Deneubourg JL (1999) Dominance order in animal societies: the self-organization hypothesis revisited. B Math Biol 61:727–757CrossRefGoogle Scholar
  8. Bosch J, Vicens N (2006) Relationship between body size, provisioning rate, longevity and reproductive success in females of the solitary bee Osmia cornuta. Behav Ecol Sociobiol 60:26–33CrossRefGoogle Scholar
  9. Calderone NW, Page RE (1988) Genotypic variability in age polyethism and task specialization in the honeybee, Apis mellifera (Hymenoptera: Apidae). Behav Ecol Sociobiol 30:219–226CrossRefGoogle Scholar
  10. Chapman RF (1998) The Insects: structure and function, 4th edn. Cambridge University PressGoogle Scholar
  11. Cideciyan M (1984) The relationship between size and behavior in worker honey bees (Apis mellifera). Thesis. University of MiamiGoogle Scholar
  12. Domínguez M, Casares F (2005) Organ specification-growth control connection: new in-sights from the Drosophila eye-antennal disc. Dev Dynam 232:673–684CrossRefGoogle Scholar
  13. Erber J, Hoorman J, Scheiner R (2006) Phototactic behaviour correlates with gustatory responsiveness in honeybees (Apis mellifera L.). Behav Brain Res 174:174–180CrossRefPubMedGoogle Scholar
  14. Farooqui T (2007) Octopamine-mediated neuromodulation of insect senses. Neurochem Res 32:1511–1529CrossRefPubMedGoogle Scholar
  15. Fjerdingstad EJ, Crozier RH (2006) The evolution of worker caste diversity in social insects. Amer Nat 167:390–400CrossRefGoogle Scholar
  16. Frederiksen R, Warrant EJ (2008) Visual sensitivity in the crepuscular owl butterfly Caligo memnon and the diurnal blue morpho Morpho peleides: a clue to explain the evolution of nocturnal apposition eyes? J Exp Biol 211:844–851CrossRefPubMedGoogle Scholar
  17. Harrison JM (1986) Caste-specific changes in honeybee flight capacity. Physiol Zool 59:175–187Google Scholar
  18. Hayes EJ, Wall R (1999) Age-grading adult insects: a review of techniques. Physiol Entomol 24:1–10CrossRefGoogle Scholar
  19. Hellmich RL, Kulincevic JM, Rothenbuhler WC (1985) Selection for high and low pollen hoarding honey bees (Apis mellifera). J Hered 76:155–158Google Scholar
  20. Higashi M, Yamamura N, Abe T (2000) Theories on the sociality of termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, pp 169–187Google Scholar
  21. Higginson AD, Barnard CJ (2004) Accumulating wing damage affects foraging decisions in honeybees (Apis mellifera L.). Ecol Entomol 29:52–59CrossRefGoogle Scholar
  22. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, CambridgeGoogle Scholar
  23. Hölldobler B, Wilson EO (2008) The superorganism: the beauty, elegance, and strangeness of insect societies. W.W. Norton & Co, New YorkGoogle Scholar
  24. Humphries MA, Fondrk MK, Page RE (2005) Locomotion and the pollen hoarding behavioral syndrome of the honey bee (Apis mellifera L.). J Comp Physiol A 191:669–674CrossRefGoogle Scholar
  25. Jander U, Jander R (2002) Allometry and resolution of bee eyes (Apoidea). Arthropod Struct Dev 30:179–193CrossRefPubMedGoogle Scholar
  26. Jeanson R, Fewell JH, Gorelick R, Bertram SM (2007) Emergence of increased division of labor as a function of group size. Behav Ecol Sociobiol 62:289–298CrossRefGoogle Scholar
  27. Johnson BR (2002) Reallocation of labor in honeybee colonies during heat stress: the relative roles of task switching and the activation of reserve labor. Behav Ecol Sociobiol 51:188–196CrossRefGoogle Scholar
  28. Kapustjanskij A, Streinzer M, Paulus HF, Spaethe J (2007) Bigger is better: implications for flight ability under different conditions and evolution of alloethism in bumblebees. Funct Ecol 21:1130–1136CrossRefGoogle Scholar
  29. Kelber A, Warrant EJ, Pfaff M, Wallen R, Theobald JC, Wcislo WT (2006) Light intensity limits foraging activity in nocturnal and crepuscular bees. Behav Ecol 17:63–72CrossRefGoogle Scholar
  30. Kerr WE, Hebling NJ (1964) Influence of the weight of worker bees on division of labor. Evolution 18:267–270CrossRefGoogle Scholar
  31. Lindauer M (1952) Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Zeitschrift fur Vergleichende Physiologie 34:299–345CrossRefGoogle Scholar
  32. Linksvayer TA, Fondrk MK, Page RE Jr (2009) Honeybee social regulatory networks are shaped by colony level selection. Am Nat 173:E99–E107CrossRefPubMedGoogle Scholar
  33. Mertl AL, Traniello JFA (2009) Behavioral evolution in the major worker subcaste of twig-nesting Pheidole (Hymenoptera: Formicidae): does morphological specialization influence task plasticity? Behav Ecol Sociobiol. doi: 10.1007/s00265-009-0797-3 Google Scholar
  34. Michener CD (1974) The social behavior of the bees. Harvard University Press, CambridgeGoogle Scholar
  35. Milne CP (1985) An estimate of heritability of corbicular area of the honeybee. J Apicul Res 24:137–139Google Scholar
  36. Milne CP, Friars GF (1984) An estimate of the heritability of honeybee pupal weight. J Hered 75:509–510Google Scholar
  37. Milne CP, Hellmich RL, Pries KJ (1986) Corbicular size in workers from honeybee lines selected for high or low pollen hoarding. J Apicult Res 25:50–52Google Scholar
  38. Moritz R, Page RE (1999) Behavioral threshold variability, cost and benefits in insect societies. In: Detrain C, Deneubourg JL, Pasteels JM (eds) Information processing in social insects. Birkhauser, Basel, pp 203–218Google Scholar
  39. Nijhout HF (2003) The control of growth. Development 130:5863–5867CrossRefPubMedGoogle Scholar
  40. Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22:408–413CrossRefPubMedGoogle Scholar
  41. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, PrincetonGoogle Scholar
  42. Page RE, Fondrk MK (1995) The effects of colony-level selection on the social organization of honey bee (Apis mellifera L.) colonies: colony-level components of pollen hoarding. Behav Ecol Sociobiol 36:135–144CrossRefGoogle Scholar
  43. Page RE, Mitchell SD (1998) Self-organization and the evolution of division of labor. Apidologie 29:171–190CrossRefGoogle Scholar
  44. Page RE, Amdam GV (2007) The making of a social insect: developmental architectures of social design. Bioessays 29:334–343CrossRefPubMedGoogle Scholar
  45. Page RE Jr, Erber J, Fondrk MK (1998) The effect of genotype on response thresholds to sucrose and foraging behavior of honeybees (Apis mellifera). J Comp Physiol A 182:489–500CrossRefPubMedGoogle Scholar
  46. 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. Curr Top Dev Biol 74:253–286CrossRefPubMedGoogle Scholar
  47. Page RE, Linksvayer TA, Amdam GV (2009) Social life from solitary regulatory networks: a paradigm for insect sociality. In: Gadau J, Fewell F (eds) Organization of insect societies: from genomes to socio-complexity. Harvard University Press, Cambridge, pp 357–376Google Scholar
  48. Pankiw T, Page RE Jr (1999) The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honeybees (Apis mellifera). J Comp Physiol A 185:207–213CrossRefPubMedGoogle Scholar
  49. Pankiw T, Page RE Jr (2000) Response thresholds to sucrose predict foraging behavior in the honey bee (Apis mellifera L.). Behav Ecol Sociobiol 47:265–267CrossRefGoogle Scholar
  50. Pankiw T, Page RE Jr (2001) Genotype and colony environment affect honeybee (Apis mellifera L.) developmental and foraging behavior. Behav Ecol Sociobiol 51:87–94CrossRefGoogle Scholar
  51. Pankiw T, Tarpy DR, Page RE Jr (2002) Genotype and rearing environment affect honeybee perception and foraging behaviour. Anim Behav 64:663–672CrossRefGoogle Scholar
  52. Poklukar J, Kezic N (1994) Estimation of heritability of some characteristics of hind legs and wings of honeybee workers (Apis mellifera carnica) using the half-sibs method. Apidologie 25:3–11CrossRefGoogle Scholar
  53. Scheiner R, Erber J (2009) Sensory thresholds, learning and the division of foraging labor in the honey bee. In: Gadau J, Fewell J (eds) Organization of insect societies: from genomes to socio-complexity. Harvard University Press, Cambridge, pp 335–356Google Scholar
  54. Scheiner R, Page RE, Erber J (2004) Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 35:133–142CrossRefGoogle Scholar
  55. Scheiner R, Baumann A, Blenau W (2006) Aminergic control and modulation of honeybee behaviour. Curr Neuropharmacol 4:259–276CrossRefPubMedGoogle Scholar
  56. Schippers MP, Dukas R, Smith RW, Wang J, Smolen K, McClelland GB (2006) Lifetime performance in foraging honeybees: behaviour and physiology. J Exp Biol 209:3828–3836CrossRefPubMedGoogle Scholar
  57. Schneider D, Steinbrecht RA (1968) Checklist of insect olfactory sensilla. Sym Zool S 23:279–297Google Scholar
  58. Schulz DJ, Pankiw T, Fondrk MK, Robinson GE, Page RE Jr (2004) Comparison of juvenile hormone hemolymph and octopamine brain titers in honey bees (Hymenoptera: Apidae) selected strains for high and low pollen hoarding. Ann Entomol Soc Am 97:1313–1319CrossRefGoogle Scholar
  59. Smith AR, Wcislo WT, O’Donnell S (2008) Body size shapes caste expression, and cleptoparasitism reduces body size in the facultatively eusocial bees Megalopta (Hymenoptera: Halictidae). J Insect Behav 21:394–406CrossRefGoogle Scholar
  60. Spaethe J, Weidenmüller A (2002) Size variation and foraging rate in bumblebees (Bombus terrestris). Insect Soc 142–146Google Scholar
  61. Spaethe J, Chittka L (2003) Interindividual variation of eye optics and single object resolution in bumblebees. J Exp Biol 206:3447–3453CrossRefPubMedGoogle Scholar
  62. Spaethe J, Brockmann A, Halbig C, Tautz J (2007) Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers. Naturwissenschaften 94:733–739CrossRefPubMedGoogle Scholar
  63. Vareschi E (1971) Duftunterscheidung bei der Honigbiene—Einzelzellableitungen und Verhaltensreaktionen. Zeitschrift fur Vergleichende Physiologie 75:143–173Google Scholar
  64. Verhoeven KJF, Simonsen KL, McIntyre M (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647CrossRefGoogle Scholar
  65. Waddington KD (1981) Patterns of size variation in bees and evolution of communication systems. Evolution 35:813–814CrossRefGoogle Scholar
  66. Waddington KD (1988) Body size, individual behavior and social behavior in honey bees. In: Jeanne RL (ed) Interindividual behavioral variability in social insects. Westview Press, Boulder, pp 385–417Google Scholar
  67. Waddington KD (2005) Implications of variation in worker body size for the honey bee recruitment system. J Insect Behav 2:91–103CrossRefGoogle Scholar
  68. Waddington KD, Herbst LH, Roubik DW (1986) Relationship between recruitment systems of stingless bees and within-nest worker size. J Kansas Entomol Soc 59:95–102Google Scholar
  69. Wcislo WT (1995) Sensilla numbers and antennal morphology of parasitic and non-parasitic bees (Hymenoptera: Apoidea). Int J Insect Morphol 24:63–81CrossRefGoogle Scholar
  70. Wcislo WT, Tierney SM (2009) Behavioural environments and niche construction: the evolution of dim-light foraging in bees. Biol Rev 84:19–37CrossRefPubMedGoogle Scholar
  71. Wheeler DE, Buck N, Evans JD (2006) Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol Biol 15:597–602CrossRefPubMedGoogle Scholar
  72. Wilson EO (1975) [2000] Sociobiology: the new synthesis. 25th anniversary edition. Belknap, CambridgeGoogle Scholar
  73. Wilson EO (1985) The principles of caste evolution. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Sinauer, New York, pp 307–324Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Center for Insect Science and Department of NeuroscienceUniversity of ArizonaTucsonUSA
  2. 2.Department of NeuroscienceThe University of ArizonaTucsonUSA

Personalised recommendations