Inner nest homeostasis in a changing environment with special emphasis on honey bee brood nursing and pollen supply

To reproduce successfully, a honey bee colony has to rear brood efficiently. This requires a fecund queen and depends on the coordinated activities of workers in brood care, in foraging, and in maintaining inner nest homeostasis. Maintaining homeostasis involves thermal regulation of the brood area and providing a steady supply of nutrients, which requires building food reserves during favorable weather so that the brood can be well fed even during times of low nutritional influx. The workforce of adult bees is appropriately divided among the required tasks, and the wax comb itself is spatially organized in a way that saves energy and supports brood nursing. The ability to achieve this homeostasis results from a set of individual behaviors and communication processes performed in parallel by thousands of bees. In this review, we discuss these proximate individual mechanisms that lead to the precise regulation of the complex system that is a honey bee society. Apis mellifera / homeostasis / nursing / pollen / self-organization

[1]  W. Farina,et al.  Trophallaxis in forager honeybees (Apis mellifera): resource uncertainty enhances begging contacts? , 2003, Journal of Comparative Physiology A.

[2]  F. Ratnieks,et al.  Task Partitioning in Insect Societies. I. Effect of Colony Size on Queueing Delay and Colony Ergonomic Efficiency , 1999, The American Naturalist.

[3]  M. Lindauer,et al.  Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat , 1952, Zeitschrift für vergleichende Physiologie.

[4]  T. Seeley,et al.  Why search time to find a food-storer bee accurately indicates the relative rates of nectar collecting and nectar processing in honey bee colonies , 1994, Animal Behaviour.

[5]  J. Free The transmission of food between Worker Honeybees , 1957 .

[6]  Scott Camazine,et al.  The regulation of pollen foraging by honey bees: how foragers assess the colony's need for pollen , 1993, Behavioral Ecology and Sociobiology.

[7]  Gerhard Heldmaier,et al.  Temperature Control in Honey Bee Colonies , 1987 .

[8]  W. V. D. Ohe,et al.  EINFLUß VON KÄLTEEINBRÜCHEN AUF DIE FRÜHJAHRSENTWICKLUNG VON BIENENVÖLKERN (APIS MELLIFERA L.) , 1988 .

[9]  H. Rembold,et al.  [ANALYTICAL AND HISTOLOGICAL STUDIES ON THE CEPHALIC AND THORACIC GLANDS IN THE HONEYBEE APIS MELLIFICA]. , 1964, Zeitschrift fur Naturforschung. Teil B, Chemie, Biochemie, Biophysik, Biologie und verwandte Gebiete.

[10]  E. Southwick Cooperative metabolism in honey bees: An alternative to antifreeze and hibernation , 1987 .

[11]  Mark L. Winston,et al.  Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. , 1992, Behavioral Ecology and Sociobiology.

[12]  K. Weiß REGULIERUNG DES PROTEINHAUSHALTES IM BIENENVOLK (APIS MELLIFICA L.) DURCH BRUTKANNIBALISMUS , 1984 .

[13]  T. Seeley,et al.  Collective decision-making in honey bees: how colonies choose among nectar sources , 1991, Behavioral Ecology and Sociobiology.

[14]  Untersuchungen über die Arbeitsteilung im Bienenstaat , 1930 .

[15]  D. Varjú,et al.  What do foraging honeybees optimize? , 1991, Journal of Comparative Physiology A.

[16]  Michael T. Turvey,et al.  Self-organization, flow fields, and information , 1988 .

[17]  Adam G. Hart,et al.  Why do honey-bee (Apis millifera) foragers transfer nectar to several receivers? Information improvement through multiple sampling in a biological system , 2001, Behavioral Ecology and Sociobiology.

[18]  F. S. Bodenheimer Studies in Animal Populations. II. Seasonal Population-Trends of the Honey-Bee , 1937, The Quarterly Review of Biology.

[19]  R. J. Barker The Influence of Food Inside the Hive on Pollen Collection by a Honeybee Colony , 1971 .

[20]  R. Moritz,et al.  Trophallaxis of worker honeybees (Apis mellifera L.) of different ages , 1986, Insectes Sociaux.

[21]  W. C. Rothenbuhler,et al.  Some Effects of Nursing on Nurse Bees , 1984 .

[22]  Effect of Distance on the Attraction of Pollen to Honeybees in the Hive , 1974 .

[23]  T. Schmickl,et al.  How honeybees (Apis mellifera L.) change their broodcare behaviour in response to non-foraging conditions and poor pollen conditions , 2002, Behavioral Ecology and Sociobiology.

[24]  Carl Anderson Simulation of the Feedbacks and Regulation of Recruitment Dancing in Honey Bees , 1998, Adv. Complex Syst..

[25]  E. Brouwers Glucose/fructose ratio in the food of honeybee larvae during caste differentiation , 1984 .

[26]  Karl Crailsheim,et al.  Trophallactic interactions in the adult honeybee , 1997 .

[27]  M. Winston,et al.  Influence of the Amount of Eggs and Larvae in Honeybee Colonies on Temporal Division of Labour , 1986 .

[28]  M. Winston,et al.  The influence of pollen storage area and Varroa jacobsoni Oudemans parasitism on temporal caste structure in honey bees (Apis mellifera L.) , 2000, Insectes Sociaux.

[29]  J. Murray,et al.  A mathematical model of self-organized pattern formation on the combs of honeybee colonies , 1990 .

[30]  M. Winston,et al.  Condition-dependent response to changes in pollen stores by honey bee (Apis mellifera) colonies with different parasitic loads , 2000, Behavioral Ecology and Sociobiology.

[31]  Karl Crailsheim,et al.  Protein trophallaxis and the regulation of pollen foraging by honey bees (Apis mellifera L.) , 1998 .

[32]  T. Seeley Honey bee foragers as sensory units of their colonies , 2004, Behavioral Ecology and Sociobiology.

[33]  Robert E. Page,et al.  The effects of colony-level selection on the social organization of honey bee (Apis mellifera L.) colonies: colony-level components of pollen hoarding , 1995, Behavioral Ecology and Sociobiology.

[34]  G. Robinson,et al.  Hormonal and Genetic Control of Behavioral Integration in Honey Bee Colonies , 1989, Science.

[35]  G. DeGrandi-Hoffman,et al.  The flow of incoming nectar through a honey bee (Apis mellifera L.) colony as revealed by a protein marker , 2000, Insectes Sociaux.

[36]  J. Harbo Effect of Population Size on Brood Production, Worker Survival and Honey Gain in Colonies of Honeybees , 1986 .

[37]  T. Seeley Social foraging in honey bees: how nectar foragers assess their colony's nutritional status , 1989, Behavioral Ecology and Sociobiology.

[38]  Stanley Friedman,et al.  Self-Selection of Optimal Diets by Insects , 1991 .

[39]  Passage of cannibalized tissue among honey bee (Hymenoptera: Apidae) colony members , 1987 .

[40]  Honey Bee Foraging Behavior: Responses to Queens, Larvae, and Extracts of Larvae , 1970 .

[41]  W. Farina,et al.  Trophallaxis in the honeybee Apis mellifera (L.): the interaction between flow of solution and sucrose concentration of the exploited food sources , 2000, Animal Behaviour.

[42]  S. Duffey,et al.  Conservation of nutrients in larval tissue by cannibalizing honey bees , 1987 .

[43]  R. Currie,et al.  Discrimination and preferences for pollen-based cues by foraging honeybees, Apis mellifera L. , 2002, Animal Behaviour.

[44]  K. Crailsheim Interadult feeding of jelly in honeybee (Apis mellifera L.) colonies , 1991, Journal of Comparative Physiology B.

[45]  G. Robinson,et al.  Regulation of honey bee division of labor by colony age demography , 1996, Behavioral Ecology and Sociobiology.

[46]  Scott Camazine,et al.  Self-organizing pattern formation on the combs of honey bee colonies , 2004, Behavioral Ecology and Sociobiology.

[47]  Mark L. Winston,et al.  Factors determining temporal division of labor in honeybees , 1982 .

[48]  Henry A. Stabe The rate of growth of worker, drone, and queen larvae of the honeybee, Apis mellifera Linn , 1930 .

[49]  J. Tautz,et al.  In-Hive Behavior of Pollen Foragers (Apis mellifera) in Honey Bee Colonies Under Conditions of High and Low Pollen Need , 2002 .

[50]  Zhi-Yong Huang,et al.  Inspection and feeding of larvae by worker honey bees (Hymenoptera: Apidae): Effect of starvation and food quantity , 1991, Journal of Insect Behavior.

[51]  H. H. W. Velthuis,et al.  The nature of trophallaxis in honeybees , 1982, Insectes Sociaux.

[52]  R. Filmer Brood Area and Colony Size as Factors in Activity of Pollination Units , 1932 .

[53]  Gene E. Robinson,et al.  Regulation of honey bee age polyethism by juvenile hormone , 1987, Behavioral Ecology and Sociobiology.

[54]  J. Free,et al.  Brood recognition by honeybee (Apis mellifera) workers , 1983, Animal Behaviour.

[55]  H. Fukuda The relationship between work efficiency and population size in a honeybee colony , 1983, Researches on Population Ecology.

[56]  Robert E. Page,et al.  Genetic variability for temporal polyethism in colonies consisting of similarly-aged worker honey bees , 1989 .

[57]  T. Pankiw,et al.  Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera) , 1998, Behavioral Ecology and Sociobiology.

[58]  K. Crailsheim,et al.  Impact of bad weather on the development of the broodnest and pollen stores in a honeybee colony (Hymenoptera: Apidae) , 1999 .

[59]  M. Fondrk,et al.  Genetic determinants of honey bee foraging behaviour , 1995, Animal Behaviour.

[60]  Thomas D. Seeley,et al.  Adaptive significance of the age polyethism schedule in honeybee colonies , 1982, Behavioral Ecology and Sociobiology.

[61]  M. Haydak Influence of Storage on the Nutritive Value of Pollen for Brood Rearing by Honeybees , 1963 .

[62]  C. A. Garófalo Brood Viability in Normal Colonies of Apis Mellifera , 1977 .

[63]  H. L. Nixon,et al.  Food transmission within the honeybee community , 1952, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[64]  R. Hellmich,et al.  Pollen hoarding and use by high and low pollen-hoarding honeybees during the course of brood rearing , 1986 .

[65]  J. Free Factors determining the collection of pollen by honeybee foragers. , 1967, Animal behaviour.

[66]  D. Gilley,et al.  Heat Shielding: A Novel Method of Colonial Thermoregulation in Honey Bees , 1999, Naturwissenschaften.

[67]  F. Ratnieks,et al.  Task partitioning in insect societies , 1999, Insectes Sociaux.

[68]  K. Crailsheim Protein synthesis in the Honeybee (Apis mellifera L.) and trophallactic distribution of Jelly among imagos in laboratory experiments , 1990 .

[69]  J. Free,et al.  The Effect of Giving Pollen and Pollen Supplement to Honeybee Colonies on the Amount of Pollen Collected , 1971 .

[70]  J. Beetsma Feeding behaviour of nurse bees, larval food composition and caste differentiation in the honey bee (Apis mellifera L.) , 1985 .

[71]  L. Standifer Honey Bee Nutrition , 1969 .

[72]  J. Simpson,et al.  Results of Restricting the Brood Space of Honeybee Colonies , 1975 .

[73]  S. Sakagami Untersuchungen uber die Arbeitsteilung in einen Zwergvolk der Honigbienen. Beitrage zur Biologie des Bienenvolkes, Apis mellifera L., I , 1953 .

[74]  F. Ratnieks,et al.  Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies , 1993, Behavioral Ecology and Sociobiology.

[75]  T. Schmickl,et al.  Cannibalism and early capping: strategy of honeybee colonies in times of experimental pollen shortages , 2001, Journal of Comparative Physiology A.

[76]  E. P. Jeffree,et al.  THE INFLUENCE OF STORED POLLEN AND OF COLONY SIZE ON THE BROOD REARING OF HONEYBEES , 1956 .

[77]  Age of Nurse Bees and Brood Rearing , 1963 .

[78]  T. Schmickl,et al.  Collective and individual nursing investment in the queen and in young and old honeybee larvae during foraging and non-foraging periods , 2003, Insectes Sociaux.

[79]  Y. Le Conte,et al.  Brood Pheromone Can Modulate the Feeding Behavior of Apis mellifera Workers (Hytnenoptera: Apidae) , 1995 .

[80]  David R. Tarpy,et al.  Perception of the pollen need by foragers in a honeybee colony , 2000, Animal Behaviour.

[81]  J. Woyke Cannibalism and Brood-Rearing Efficiency in the Honeybee , 1977 .

[82]  Mark L. Winston,et al.  The effect of worker loss on temporal caste structure in colonies of the honeybee (Apis mellifera L.) , 1985 .

[83]  David C. Newton,et al.  Cannibalism as an Indication of Pollen Insufficiency in Honeybees: Ingestion or Recapping of Manually Exposed Pupae , 1974 .

[84]  Karl Crailsheim,et al.  Trophallactic interactions in the adult honeybee (Apis mellifera L.) , 1998 .

[85]  M. F. Ribeiro Growth in bumble bee larvae: relation between development time, mass, and amount of pollen ingested , 1994 .

[86]  F. Bigler,et al.  Pollen consumption in honey bee larvae: a step forward in the risk assessment of transgenic plants , 2004 .

[87]  G. Robinson,et al.  Effects of colony food shortage on behavioral development in honey bees , 1998, Behavioral Ecology and Sociobiology.

[88]  J. Woyke Brood Survival in Productive Bee Apiaries in Australia as a Test for Breeding Honeybees in Closed Populations , 1988 .

[89]  Z. Y. Huang,et al.  Effects of colony food shortage on social interactions in honey bee colonies , 2002, Insectes Sociaux.

[90]  J. Harbo Effect of brood rearing on honey consumption and the survival of worker honey bees , 1993 .

[91]  S. Sakagami,et al.  Worker brood survival in honeybees , 1968, Researches on Population Ecology.

[92]  W. C. Rothenbuhler,et al.  Brood Rearing Associated with a Range of Worker-Larva Ratios in the Honeybee , 1983 .

[93]  T. Seeley,et al.  How a honey bee colony mustered additional labor for the task of pollen foraging , 2002 .

[94]  A. Benton,et al.  The Relationship Between the Amount of Unsealed Brood in Honeybee Colonies and Their Pollen Collection , 1972 .

[95]  Karl Crailsheim,et al.  The flow of jelly within a honeybee colony , 1992, Journal of Comparative Physiology B.

[96]  W. C. Rothenbuhler,et al.  Length of life and Dry Weight of Worker Honeybees Reared in Colonies with Different Worker-Larva Ratios , 1982 .

[97]  W. R. Hess Die Temperaturregulierung im Bienenvolk , 2004, Zeitschrift für vergleichende Physiologie.

[98]  R. Thorp,et al.  Effects of Pollen Traps on Honey Bee (Hymenoptera: Apidae) Foraging and Brood Rearing During Almond and Prune Pollination , 1985 .

[99]  R. Currie,et al.  The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.) , 2001, Behavioral Ecology and Sociobiology.

[100]  H. Arathi,et al.  Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. , 2000 .

[101]  G. Theraulaz,et al.  Joint memory , 1995, Behavioural Processes.

[102]  Richard L. Hellmich,et al.  Relationship Between Different Amounts of Brood and the Collection and Use of Pollen by the Honey Bee (Apis Mellifera) , 1986 .

[103]  A. Himmer DIE TEMPERATURVERHÄLTNISSE BEI DEN SOZIALEN HYMENOPTEREN , 1932 .

[104]  J. Free The food of adult drone honeybees (Apis mellifera). , 1957 .

[105]  Der-I Wang,et al.  Growth Rates of Young Queen and Worker Honeybee Larvae , 1965 .

[106]  M. Haydak Brood Rearing by Honeybees Confined to a Pure Carbohydrate Diet , 1935 .

[107]  Assessment of pollen stores by foragers in colonies of the honey bee, Apis mellifera L. , 2002, Insectes Sociaux.

[108]  Tanya Pankiw,et al.  Genotype and rearing environment affect honeybee perception and foraging behaviour , 2002, Animal Behaviour.

[109]  Zhi-Yong Huang,et al.  Nonrandom visitation of brood cells by worker honey bees (Hymenoptera: Apidae) , 1991, Journal of insect behavior.

[110]  K. Crailsheim,et al.  Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): Dependence on individual age and function , 1992 .

[111]  S. Pratt,et al.  A modelling framework for understanding social insect foraging , 2003, Behavioral Ecology and Sociobiology.

[112]  I. van der Tweel,et al.  Feeding frequency and caste differentiation in Bombus terrestris larvae , 1999, Insectes Sociaux.

[113]  Preliminary observations on thermoregulation, clustering, and energy utilization in African and European honey bees. , 1987 .

[114]  T. Pankiw,et al.  Genotype and colony environment affect honeybee (Apis mellifera L.) development and foraging behavior , 2001, Behavioral Ecology and Sociobiology.

[115]  T. Szabo Effect of Weather Factors on Honeybee Flight Activity and Colony Weight Gain , 1980 .

[116]  Karl Crailsheim,et al.  Short-term effects of simulated bad weather conditions upon the behaviour of food-storer honeybees during day and night (Apis mellifera carnica Pollmann) , 1999 .

[117]  Carl Anderson,et al.  Task Partitioning in Insect Societies. II. Use of Queueing Delay Information in Recruitment , 1999, The American Naturalist.

[118]  E. Brouwers,et al.  Behavioural and physiological aspects of nurse bees in relation to the composition of larval food during caste differentiation in the honeybee. , 1987 .

[119]  Thomas D. Seeley,et al.  Fever in honeybee colonies , 2000, Naturwissenschaften.