A Socio‐Spatial Combined Approach Confirms a Highly Compartmentalised Structure in Honeybees

Complex insect societies are formed by thousands to millions of individuals which incessantly interact in the sheltered nest space under the constant pressure of different challenges, such as infectious disease and group coordination. Understanding how colony members interact in space and time may therefore help unravelling how different evolutionary pressures have moulded insect societies. We investigated the spatial positions and the association network of workers and the queen in the honeybee (Apis mellifera) society using high-resolution recordings of spatial behaviour and ‘network connections’ at the individual level. Our socio-spatial combined approach highlighted a highly compartmentalised structure inside honeybee colony. Connectivity and spatial overlap are high among same-age workers but low among different-age workers. Foragers are at the periphery of the social network, while the colony core is formed by young bees and the queen. Our study presents the first empirical quantitative description of socio-spatial organisation of a honeybee hive, confirming a highly compartmentalised structure and highlighting how the pressures exerted by ergonomics requirements could have shaped insect societies.

[1]  Martin G. Everett,et al.  A Graph-theoretic perspective on centrality , 2006, Soc. Networks.

[2]  Martin G. Everett,et al.  Analyzing social networks , 2013 .

[3]  N. Franks,et al.  Spatial relationships within nests of the ant Leptothorax unifasciatus (Latr.) and their implications for the division of labour , 1995, Animal Behaviour.

[4]  N. Franks,et al.  Social Evolution in Ants , 2019 .

[5]  S. Camazine,et al.  Implications of horizontal and vertical pathogen transmission for honey bee epidemiology , 2001 .

[6]  M. Keeling The implications of network structure for epidemic dynamics. , 2005, Theoretical population biology.

[7]  Tanya Pankiw,et al.  Cued in: honey bee pheromones as information flow and collective decision-making , 2004 .

[8]  E. Wilson,et al.  Caste and ecology in the social insects. , 1979, Monographs in population biology.

[9]  S. Turillazzi,et al.  Home Range Analysis in the Study of Spatial Organization on the Comb in the Paper Wasp Polistes Dominulus , 2010 .

[10]  M. Kretzschmar,et al.  Perspective: human contact patterns and the spread of airborne infectious diseases. , 1999, Trends in microbiology.

[11]  S. Turillazzi,et al.  Basic social biology and nest architecture of Liostenogaster topographica Turillazzi 1999 (Hymenoptera Stenogastrinae) , 2009 .

[12]  M. Lindauer Communication Among Social Bees , 1961 .

[13]  Thomas D. Seeley,et al.  Age Polyethism for Hive Duties in Honey Bees — Illusion or Reality? , 2010 .

[14]  James S. Waters,et al.  Information Processing in Social Insect Networks , 2012, PloS one.

[15]  P. J. Clark,et al.  Distance to Nearest Neighbor as a Measure of Spatial Relationships in Populations , 1954 .

[16]  S. Turillazzi,et al.  Beyond the antipredatory defence: honey bee venom function as a component of social immunity. , 2011, Toxicon : official journal of the International Society on Toxinology.

[17]  Deborah M. Gordon,et al.  The effect of individual variation on the structure and function of interaction networks in harvester ants , 2011, Journal of The Royal Society Interface.

[18]  Brian R. Johnson Global information sampling in the honey bee , 2008, Naturwissenschaften.

[19]  Anna Dornhaus,et al.  Time-Ordered Networks Reveal Limitations to Information Flow in Ant Colonies , 2011, PloS one.

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

[21]  D. Lusseau,et al.  Animal social networks: an introduction , 2009, Behavioral Ecology and Sociobiology.

[22]  J. Krause,et al.  Social network theory in the behavioural sciences: potential applications , 2007, Behavioral Ecology and Sociobiology.

[23]  Dhruba Naug,et al.  Experimentally induced change in infectious period affects transmission dynamics in a social group , 2007, Proceedings of the Royal Society B: Biological Sciences.

[24]  F. Ratnieks,et al.  Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leafcutting ant Atta cephalotes , 2001, Behavioral Ecology and Sociobiology.

[25]  Brian R. Johnson Within-nest temporal polyethism in the honey bee , 2008, Behavioral Ecology and Sociobiology.

[26]  Walter R. Tschinkel,et al.  Sociometry and sociogenesis of colony-level attributes of the Florida harvester ant (Hymenoptera : Formicidae) , 1999 .

[27]  B. Johnson Spatial effects, sampling errors, and task specialization in the honey bee , 2010, Insectes Sociaux.

[28]  S. O’Donnell,et al.  Worker connectivity: a review of the design of worker communication systems and their effects on task performance in insect societies , 2007, Insectes Sociaux.

[29]  M. Gardner,et al.  Transmission mode and distribution of parasites among groups of the social lizard Egernia stokesii , 2006, Parasitology Research.

[30]  P. Schmid-Hempel,et al.  Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects , 1993, Behavioral Ecology and Sociobiology.

[31]  M. Chapuisat,et al.  Evidence for collective medication in ants , 2003 .

[32]  A. Crespi,et al.  Tracking Individuals Shows Spatial Fidelity Is a Key Regulator of Ant Social Organization , 2013, Science.

[33]  B. Worton Kernel methods for estimating the utilization distribution in home-range studies , 1989 .

[34]  S. Turillazzi,et al.  Differences in venom and cuticular peptides in individuals of Apis mellifera (Hymenoptera: Apidae) determined by MALDI-TOF MS. , 2010, Journal of insect physiology.

[35]  Dhruba Naug,et al.  Structure of the social network and its influence on transmission dynamics in a honeybee colony , 2008, Behavioral Ecology and Sociobiology.

[36]  E. Wilson,et al.  Dense heterarchies and mass communication as the basis of organization in ant colonies. , 1988, Trends in ecology & evolution.

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

[38]  T. Seeley,et al.  Honeybee Ecology: A Study of Adaptation in Social Life , 1985 .

[39]  James D. Thomson,et al.  Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies , 2007, Oecologia.

[40]  R. Laine,et al.  Termites fumigate their nests with naphthalene , 1998, Nature.

[41]  G. Theraulaz,et al.  Inspiration for optimization from social insect behaviour , 2000, Nature.

[42]  G. Robinson Regulation of division of labor in insect societies. , 1992, Annual review of entomology.

[43]  B. Hart The evolution of herbal medicine: behavioural perspectives , 2005, Animal Behaviour.

[44]  R. Jeanne THE EVOLUTION OF THE ORGANIZATION OF WORK IN SOCIAL INSECTS , 2013 .

[45]  Jürgen Tautz,et al.  Honeybees establish specific sites on the comb for their waggle dances , 1997, Journal of Comparative Physiology A.

[46]  J. Evans,et al.  Resin Collection and Social Immunity in Honey Bees , 2009, Evolution; international journal of organic evolution.

[47]  Deborah M. Gordon The organization of work in social insect colonies , 2002 .

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

[49]  R. May,et al.  Population biology of infectious diseases: Part II , 1979, Nature.

[50]  P. Schmid-Hempel Parasites in Social Insects , 1998 .

[51]  J. Fewell Social Insect Networks , 2003, Science.

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

[53]  Spores of Ascosphaera apis contained in wax foundation can infect honeybee brood. , 2005, Veterinary microbiology.

[54]  Robert M. May,et al.  The spatial dynamics of host-parasitoid systems , 1992 .

[55]  Anna Dornhaus,et al.  Spatial organization and division of labour in the bumblebee Bombus impatiens , 2009, Animal Behaviour.

[56]  M. Keeling,et al.  Disease evolution on networks: the role of contact structure , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[57]  E O Wilson,et al.  The Sociogenesis of Insect Colonies , 1985, Science.

[58]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[59]  Scott Camazine,et al.  The role of colony organization on pathogen transmission in social insects. , 2002, Journal of theoretical biology.