Proximate mechanisms of age polyethism in the honey bee, Apis mellifera L.

Apidologie

Volumn 29, Issue 1-2, 1998, Pages 127-158

  Calderone, Nicholas W ^a  

^a Cornell University ^*  (United States)

Author keywords

Age polyethism; Apis mellifera; Division of labor; Emergent property; Self organization; Social behavior; Social insects

Indexed keywords

AGE POLYETHISM; DIVISION OF LABOUR; HONEYBEE; WORKER;

AGING; GENOTYPE; HONEYBEE; INSECT; NONHUMAN; ONTOGENY; REVIEW; SOCIAL BEHAVIOR; TASK PERFORMANCE; WORK;

APIDAE; APINAE; APIS MELLIFERA; APOIDEA; HEXAPODA; HYMENOPTERA; INSECTA; INVERTEBRATA;

EID: 0031966286     PISSN: 00448435     EISSN: None     Source Type: Journal    
DOI: 10.1051/apido:19980108     Document Type: Review

References (152)

1. Beshers SN, Traniello JFA (1994) The adaptiveness of worker demography in the attine ant Trachymyrmex septentrionalis. Ecology 75, 763-775
2. Bonabeau E, Theraulaz G, Deneubourg JL, Aron S, Camazine S (1997) Self-organization in social insects. Trends Ecol Evol 12, 188-193.
3. Bourke AFG, Franks NR (1995) Social Evolution in Ants. Princeton Univ Press, Princeton, NJ, 529 pp
4. Breed MD, Robinson GE, Page RE Jr (1990) Division of labor during honey bee colony defense. Behav Ecol Sociobiol 27, 395-401
5. Burrell BD, Smith BH (1994) Age-but not caste-related regulation of abdominal mechanisms underlying the sting reflex of the honey bee, Apis mellifera. J Comp Physiol A, Sens, Neural, and Behav Physiol 174, 581-592
6. Calabi P (1988) Behavioral flexibility in Hymenoptera: a re-examination of the concept of caste. In: Advances in Myrmecology (JC Trager, ed), EJ Brill, NY
7. Calderone NW (1995) Temporal polyethism in the honey bee, Apis mellifera: developmental process or epiphenomenon? Can J Zool 73, 1410-1416
8. Calderone NW, Page RE, Jr (1988) Genotypic variability in age polyethism and task specialization in the honey bee, Apis mellifera (Hymenoptera: Apidae). Behav Ecol Sociobiol 22, 17-25
9. Calderone NW, Page RE, Jr (1991) Evolutionary genetics of division of labor in colonies of the honey bee, Apis mellifera. Am Nat 138, 69-92
10. Calderone NW, Page RE, Jr (1992) Effects of interactions among genotypically diverse nestmates on task specialization by foraging honey bees, Apis mellifera. Behav Ecol Sociobiol 30, 219-226
11. Calderone NW, Page RE, Jr (1996) Temporal polyethism and behavioral canalization in the honey bee, Apis mellifera. Anim Behav 51, 631-643
12. Cameron SA, Robinson GE (1990) Juvenile Hormone does not affect division of labor in bumble bee colonies (Hymenoptera: Apidae). Ann Entomol Soc Am 83, 626-631
13. Camazine S (1991) Self-organizing pattern formation on the combs of honey bee colonies. Behav Ecol Sociobiol 28, 61-76
14. 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
15. Camazine S, Sneyd J, Jenkins MJ, Murray JD (1990) A mathematical model of self-organized pattern formation on the combs of honeybee colonies. J Theor Biol 147, 553-571
16. Camazine S, Sneyd J (1991) A model of collective nectar source selection by honey bees: self-organization through simple rules. J Theor Biol 149, 547-571
17. Cole BJ (1991) Short-term activity cycles in ants: generation of periodictiy by worker interactions. Am Nat 137, 244-259
18. Crailsheim K (1990) Protein synthesis in the honey bee (Apis mellifera L) and trophallactic distribution of jelly among imagos in laboratory experiments. Zool J Physiol 94, 303-312
19. Crailsheim K (1991) Interadult feeding of jelly in honeybee colonies (Apis mellifera L). J Comp Physiol B 161, 55-60
20. Crailsheim K (1992) The flow of jelly within a honeybee colony. J Comp Physiol B 162, 681-689
21. Deneubourg JL, Goss S (1989) Collective patterns and decision-making. Ethol Ecol Evol 1, 295-311.
22. Dönhoff (1855a) Über das Geruchsorgan der Biene. In: Beiträge zur Bienenkunde, Pfenningstorff, Berlin
23. Dönhoff (1855b) Über das Herrschen verschiedener Triebe in verschieden Lebensaltern bei den Bienen. In: Beiträge zur Bienenkunde, Pfenningstorff, Berlin
24. Downing HA, Jeanne RL (1988) Nest construction by the paper wasp, Polistes: a test of stigmergy theory. Anim Behav 36, 1729-1739
25. Fahrbach SE (1997) Regulation of age polyethism in bees and wasps by juvenile hormone. Adv Stud Behav 26, 285-316
26. Farrar CL (1949) The overwintering of productive colonies. In: The Hive and the Honey Bee, Dadant, Hamilton, IL
27. Fergusson LA, Winston ML (1988) The influence of wax deprivation on temporal polyethism in honey bee (Apis mellifera L) colonies. Can J Zool 66, 1997-2001
28. Fluri P (1990) How long do worker honeybees live? Schweiz Bienen-Zeitung 113, 620-625.
29. Fluri P (1993) On the regulation of lifespan in the honey bee. Deutsches Bienen J 1, 588-591.
30. Franks NR (1994) Is age polyethism a myth? In: Les Insectes Sociaux, 12th Congress of the IUSSI Paris, Sorbonne, Université Paris Nord, Paris
31. Franks NR, Bryant S, Griffiths R, Hemerik L (1990) Synchronization of the behavior within nests of the ant leptothorax-acervorum fabricius I. Discovering the phenomenon and its relation to the level of starvation. Bull Math Biol 52, 597-612
32. Franks NR, Sendova-Franks AB (1992) Brood sorting by ants distributing the workload over the work-surface. Behav Ecol Sociobiol 30, 109-123
33. Franks NR, Tofts C (1994) Foraging for work: how tasks allocate workers. Anim Behav 48, 470-472
34. Free JB (1957) The transmission of food between worker honeybees. Br J Anim Behav 5, 41-47
35. Free JB (1961) Hypopharyngeal gland development and division of labour in honey-bee (Apis mellifera L) colonies. Proc R Entomol Soc Lond 36A, 5-8
36. Free JB (1965) The allocation of duties among worker honeybees. Symp Zool Soc Lond 14, 39-59
37. Frumhoff PC, Baker J (1988) A genetic component to division of labor within honey bee colonies. Nature 333, 358-361
38. Gerstung F (1891-1926) Der Bien und Seine Zucht, 7 ed. Pfenningstorff, Berlin
39. Giray T, Robinson GE (1994) Effects in intracolony variability in behavioral development on plasticity of division of labor in honey bee colonies. Behav Ecol Sociobiol 35, 13-20
40. Gordon DM (1989a) Dynamics of task switching in harvester ants. Anim Behav 38, 194-204
41. Gordon DM (1989b) Caste and change in social insects. In: Oxford Surveys in Evolutionary Biology 6 (PH Harvey, L Partridge, eds), Oxford Univ Press, Oxford, pp 55-72
42. Gordon DM (1996) The organization of work in social insects. Nature 380, 121-124
43. Gordon DM, Goodwin BC, Trainor LEH (1992) A parallel distributed model of the behavior of ant colonies. J Theor Biol 156, 293-307
44. Guzman-Novoa E, Gary NE (1993) Genotypic variability of components of foraging behavior in honey bees (Hymenoptera: Apidae). J Econ Entomol 86, 715-721
45. Guzman-Novoa E, Page RE Jr, Gary N E (1994) Behavioral and life-history components of division of labor in honey bees (Apis mellifera L.). Behav Ecol Sociobiol 34, 409-417
46. Harrison J (1986) Caste-specific changes in honeybee flight capacity Physiol Zool 59, 175-187
47. Hellmich RL II, Kulincevic JM, Rothenbuhler WC (1985) Selection for high and low pollen-hoarding honey bees. J Hered 76, 155-158
48. Hersch MI, Crewe RM, Hepburn HR, Thompson PR, Savage N (1978) Sequential development of glycolytic competence in the muscles of worker honeybees. Comp Biochem Physiol 61B, 427-431
49. Himmer A (1930) Von der Arbeitsteilung im Bienenstaat. Leipzig Bienenztg 45, 39-43, 64-67
50. Hogeweg P, Hesper B (1983) The ontogeny of the interaction structure in bumble bee colonies: a MIRROR model. Behav Ecol Sociobiol 12, 271-283
51. Hogeweg P, Hesper B (1985) Socioinformatic processes: MIRROR modelling methodology. J Theor Biol 113, 311-330
52. Hölldobler B, Wilson EO (1990) The Ants. Belknap Press, Cambridge, MA
53. Hrassnigg N, Crailsheim K (1996) Trophallaxis of proteinaceous jelly in middle-aged honey bees. Apidologie 1996 27, 311-313
54. Huang ZY, Robinson GE (1992) Honeybee colony integration: Worker-worker interactions mediate hormonally regulated plasticity in division of labor. Proc Natl Acad Sci USA 89, 11726-11729
55. Huang ZY, Robinson GE (1996) Regulation of honey bee division of labor by colony age demography. Behav Ecol Sociobiol 39, 147-158
56. Jaycox ER (1974) Behavioral changes in worker honey bees (Apis mellifera L.) induced by injections of a juvenile hormone mimic. Ann Entomol Soc Am 67, 529-534
57. Jaycox ER (1976) Behavioral changes in worker honey bees (Apis mellifera L.) after injection with synthetic juvenile hormone (Hymenoptera: Apidae). J Kans Entomol Soc 49, 165-170
58. Jeanne RL (1986) The evolution of the organization of work in social insects. Monit Zool Ital 20, 119-133
59. Jeanne RL (1991) Polyethism. In: The Social Biology of Wasps (KG Ross and RW Matthews, eds), Cornell Univ Press, Ithaca, NY
60. Kolmes SA (1985a) A quantitative study of the division of labor among worker honey bees. Z Tierpsychol 68, 287-302
61. Kolmes SA (1985b) An information theory analysis of task specialization among worker honey bees performing hive duties. Anim Behav 33, 181-187
62. Kolmes SA (1986) Age polyethism in worker honey bees. Ethology 71, 252-255
63. Kolmes SA (1989) Grooming specialists among worker honey bees, Apis mellifera. Anim Behav 37, 1048-1049
64. Kolmes SA, Winston ML, Fergusson LA (1989) The division of labor among worker honey bees (Hymenoptera: Apidae): The effects of multiple patrilines. J Kans Entomol Soc 62, 80-95
65. Laidlaw HH (1974) Relationships of bees within a colony. Apiacta 9, 49-52
66. Lenoir A (1987) Factors determining polyethism in social insects. In: From Individual to Collective Behavior in Social Insects (Pasteels JM, Deneubourg J-L, eds), Birkhauser, Basel, 219-240
67. Lindauer M (1952) Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z vergl Physiol 34, 299-345
68. Lindauer, M (1953) Division of labor in the honeybee colony. Bee World 34, 63-73
69. Lloyd JE (1983) Bioluminescence and communication in insects. Annu Rev Entomol 28, 131-160
70. Masson C, Arnold, G (1984) Ontogeny, maturation and plasticity of the olfactory system in the worker bee. J Insect Physiol 30, 7-14
71. Maurizio A (1950) The influence of pollen feeding and brood rearing on the length of life and physiological condition of the honeybee. Preliminary report. Bee World 31, 9-12
72. Michener CD (1974) The Social Bees. Belknap Press, Cambridge, MA
73. Moore D, Angel JE, Cheeseman IM, Robinson GE, Fahrbach SE (1995) A highly specialized social grooming honey bee (Hymenoptera: Apidae). J Insect Behav 8, 855-861
74. Moore AJ, Breed MD, Moor MJ (1987) The guard honey bee: ontogeny and behavioural variability of workers performing a specialized task. Anim Behav 35, 1159-1167
75. Morland DMT (1930) On the causes of swarming in the honey bee (Apis mellifera L) An examination of the brood food theory. Ann Appl Biol 17, 137-149
76. Milojeciv BD (1940) A new interpretation of the social life of the honeybee. Bee World 21, 39-41
77. Naumann K, Winston ML (1990) Effects of swarm type on temporal caste polyethism in the honey bee, Apis Mellifera L (Hymenoptera: Apidae). Insectes Soc 37, 58-72
78. Nelson FC (1927) Adaptability of young bees under adverse conditions. Am Bee J 67, 242-243
79. Nenadovic V, Jankovic Hladni-M, Ivanovic J, Stanic V (1985) Cytological changes in corpora allata of newly emerged adult worker bees Apis mellifera L (Hym, Apidae). Acta Entomol Jugoslavica 21, 79-85
80. Nicolis G, Prigogine I (1977) Self-organization in Non-equilibrium Systems. Wiley
81. Nixon HL, Ribbands CR (1952) Food transmission within the honeybee community. Proc R Soc Lond Ser B 140, 43-50
82. Nolan WJ (1924) The division of labor in the honeybee. NC Beekeeper (Oct), 10-15
83. O'Donnell S, Jeanne RL (1993) Methoprene accelerates age polyethism in workers of a social wasp (Polybia occidentalis). Physiol Entomol 18, 189-194
84. O'Donnell S, Jeanne RL (1995) Implications of senescence patterns for the evolution of age polyethism in eusocial insects. Behav Ecol 6, 269-273
85. Omholt SW (1988) Relationships between worker longevity and the intracolonial population dynamics of the honeybee. J Theor Biol 130, 275-284
86. Oster GF, Wilson EO (1978) Caste and Ecology in the Social Insects. Princeton Univ Press, Princeton, NY
87. Pacala SW, Gordon D, Godfray HCJ (1996) Effects of social group size on information transfer and task allocation. Evol Ecol 10, 127-165
88. Page RE, Jr, Robinson GE (1991) The genetics of division of labour in honey bee colonies. Adv Insect Physiol 23, 117-169
89. Page RE, Jr, Robinson GE, Britton DS, Fondrk MK (1992) Genotypic variability for rates of behavioral development in worker honeybees (Apis mellifera L). Behav Ecol 3, 173-180
90. Page RE, Jr, Mitchell SD (1998) Self organization and division of labor in insect societies. Apidologie 29, 171-190
91. Pham-Delègue MH, Trouiller J, Bakchine E, Roger B, Masson C (1991) Age dependency of worker bee response to queen pheromone in a four-armed olfactometer. Insectes Soc 38, 283-292
92. Pham-Delègue MH, Trouiller J, Caillaud CM, Roger B, Masson C (1993) Effect of queen pheromone on worker bees of different ages: Behavioural and electrophysiological responses. Apidologie 24, 267-281
93. Porter SD, Jorgensen CD (1981) Foragers of the harvester ant, Pogonomyrmex owyheei: a disposable caste? Behav Ecol Sociobiol 9, 247-256
94. Ribbands CR (1952) Division of labour in the honeybee community. Proc R Soc Lond B 142, 515-524
95. Robinson GE (1985) Effects of a juvenile hormone analogue on honey bee foraging behvaiour and alarm pheromone production. J Insect Physiol 31, 277-282
96. Robinson GE (1987a) Regulation of honey bee age polyethism by juvenile hormone. Behav Ecol Sociobiol 20, 329-338
97. Robinson GE (1987b) Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally regulated response thresholds. J Comp Physiol A 160, 613-619
98. Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37, 637-665
99. Robinson G E, Underwood BA, Henderson CEA (1984) A highly specialized water-collecting honey bee. Apidologie 15, 355-358
100. Robinson GE, Page RE, Jr, Strambi C, Strambi A (1992) Colony integration in honey bees: Mechanisms of behavioral reversion. Ethology 90, 336-348
101. Robinson GE, Page RE, Huang ZY (1994) Temporal polyethism in social insects is a developmental process. Anim Behav 47, 1-3
102. Robinson GE, Page RE, Jr (1995) Genotypic constraints on plasticity for corpse removal in honey bee colonies. Anim Behav 49, 867-876
103. Robinson GE, Vargo EL (1997) Juvenile hormone in adult eusocial Hymenoptera: Gonadotropin and behavioral pacemaker. Arch Insect Biochem Physiol 35, 559-583
104. Robinson GE, Huang ZY (1998) Colony integration in honey bees: genetic, endocrine, and social control of division of labor. Apidologie 29, 159-170
105. Robson SK, Beshers SN (1997) Division of labour and 'foraging for work': simulating reality versus reality of simulations. Anim Behav 53, 214-218
106. Rosengaus RB, Traniello JFA (1993) Temporal polyethism in incipient colonies of the primitive termite Zootermopsis angusticollis: A single multiage caste. J Insect Behav 6, 237-252
107. Rösch GA (1925) Untersuchungen über die Arbeitsteilung im Bienenstaat, I Teil: die Tätigkeiten im normalen Bienstaate und ihre Beziehungen zum Alter der Arbeitsbienen. Z Vergl Physiol 2, 571-631
108. Rösch GA (1927) Über die Bautätigkeit im Bienenvolk und das Alter der Baubienen Weiterer Beitrag zur Frage nach der Arbeitsteilung im Bienenstaat. Z Vergl Physiol 6, 265-298
109. Rösch GA (1930) Untersuchungen über die Arbeitsteilung im Bienenstaat, II Teil: die Tätigkeiten der Arbeitsbienen unter experimentell veränderten Bedingungen. Z Vergl Physiol 12, 1-71
110. Rösch GA (1931) Neue Beobachtungen und Versuche über die Arbeitsteilung im Bienenstaat. Forsch Fortschr Dtsch Wiss 7, 86
111. Ross KG, Matthews RW (eds) (1991) The Social Biology of the Wasps, Cornell Univ Press, Ithaca, NY
112. Sakagami SF, Fukuda H (1968) Life tables for worker honeybees. Res Pop Ecol 10, 127-139
113. Schmid-Hempel P (1992) Worker castes and adaptive demography. J Evol Biol 5, 1-12
114. Schmid-Hempel P, Schmid-Hempel R (1984) Life duration and turnover of foragers in the ant Cataglyphis bicolor (Hymenoptera: Formicidae). Insectes Soc 31, 345-360
115. Seeley TD (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav Ecol Sociobiol 11, 287-293
116. Seeley TD (1985) Honeybee Ecology. Princeton Univ Press, NJ
117. Seeley TD (1989) Social foraging in honey bees: how nectar foragers assess their colony's nutritional status. Behav Ecol Sociobiol 24, 181-199
118. Seeley TD (1995) The Wisdom of the Hive. Harvard Univ Press, Cambridge, MA
119. Seeley TD, Morse RA (1976) The nest of the honey bee (Apis mellifera L). Insectes Soc 23, 495-512
120. 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
121. Seeley TD, Kolmes SA (1991) Age polyethism for hive duties in honey bees - illusion or reality. Ethology 87, 284-297
122. Seeley TD, Kuhnholtz S, Weidenmuller A (1996) The honey bee's tremble dance stimulates additional bees to function as nectar receivers. Behav Ecol Sociobiol 39, 419-427
123. Sekiguchi K, Sakagami SF (1966) Structure of foraging populations and related problems in the honeybee, with consideration s on the division of labour in bee colonies. Hokkaido Natl Agric Exp Sta Rep 69, 1-65
124. Sendova-Franks A, Franks NR (1993) Task allocation in ant colonies within variable environments (a study of temporal polyethism: experimental). Bull Math Biol 55, 75-96
125. Sorensen AA, Busch TM, Vinson SB (1985) Trophallaxis by temporal subcastes in the fire ant, Solenopsis invicta, in response to honey. Physiol Entomol 10, 105-111
126. Skarka V, Deneugourg JL, Belic MR (1990) Mathematical model of building behavior of Apis mellifera. J Theor Biol 147, 1-16
127. Stuart RJ (1997) Division of labor in social insect colonies: self-organization and recent revelations regarding age, size and genetic differences. In: Comparative Psychology of Invertebrates : the Field and Laboratory Study of Insect Behavior (G Greenberg, E Tobach, eds), Garland Press, NY
128. Szolderits MJ, Crailsheim K (1993) A comparison of pollen consumption and digestion in honeybee (Apis mellifera carnica) drones and workers. J Insect Physiol 39, 877-881
129. Theraulaz G, Bonabeau E, Deneubourg J-L (1995) Self-organization of hierarchies in animal societies: the case of the primitively eusocial wasp Polistes dominulus Christ. J Theor Biol 174, 313-323
130. Tofts C (1993) Algorithms for task allocation in ants (A study of temporal polyethism: Theory). Bull Math Biol 55, 891-918
131. Tofts C, Franks NR (1992) Doing the right thing: Ants, honeybees and naked mole-rats. Trends Ecol Evol 7, 346-349
132. Trainello JFA (1978) Caste in a primitive ant: absence of age polyethism in Amblyopone. Science 202, 770-772
133. Trainello JFA, Rosengaus R (1997) Ecology, evolution and division of labour in social insects. Anim Behav 53, 209-213
134. Van der Blom J (1992) Individual involvement in queen-attending of worker honeybees. Insectes Soc 39, 237-249
135. Van der Blom J (1993) Individual differentiation in behaviour of honey bee workers (Apis mellifera L). Insectes Soc 40, 345-361
136. Visscher PK (1983) The honey bee way of death: necrophoric behaviour in Apis mellifera colonies. Anim Behav 31, 1070-1076
137. Visscher PK, Dukas R (1997) Survivorship of foraging honey bees. Insectes Soc 44, 1-5
138. Watmough J, Camazine S (1995) Self-organized thermoregulation of honeybee clusters. J Theor Biol 176, 391-402
139. West-Eberhard MJ (1981) Intragroup selection and the evolution of insect societies In: Natural Selection and Social Behavior (Alexander R, Tinkle DW, eds), Chiron Press, NY
140. Wilson EO (1971) The Insect Societies. Belknap Press of the Harvard Univ Press, Cambridge, MA
141. Wilson EO (1976) Behavioral discretization and the number of castes in an ant species. Behav Ecol Sociobiol 1, 141-154
142. Wilson EO (1978) Division of labor in fire ants based on physical castes (Hymenoptera: Formicidae: Solenopsis). J Kans Entomol Soc 51, 615-636
143. Wilson EO (1980a) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta) I. The overall pattern in A. sexdens. Behav Ecol Sociobiol 7, 143-156
144. Wilson EO (1980b) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta) II. The ergonomic optimization of leaf-cutting. Behav Ecol Sociobiol 7, 157-165
145. Wilson EO (1985) The sociogenesis of insect colonies. Science 228, 1489-1496
146. Wilson EO (1987) Causes of ecological success: The case of the ants. J Anim Ecol 56, 1-9
147. Wilson EO, Eisner T (1957) Qualitative studies of liquid food transmission in ants. Insectes Soc 4, 11-166
148. Winston ML (1987) The Biology of the Honey Bee. Harvard Univ Press, Cambridge, MA
149. Winston ML, Katz SJ (1982) Longevity of cross-fostered honey bee workers (Apis mellifera) of European and Africanized races. Behav Ecol Sociobiol 10, 125-129
150. Winston ML, Punnett EN (1982) Factors determining temporal division of labor in honeybees. Can J Zool 60, 2947-2952
151. Winston ML, Fergusson LA (1985) The effect of worker loss on temporal caste structure in colonies of the honey bee (Apis mellifera L). Can J Zool 63, 777-780
152. Winston ML, Fergusson LA (1986) Influence of the amount of eggs and larvae in honeybee colonies on temporal division of labour. J Apic Res 25, 238-241