Automated computer-based detection of encounter behaviours in groups of honeybees

Honeybees form societies in which thousands of members integrate their behaviours to act as a single functional unit. We have little knowledge on how the collaborative features are regulated by workers’ activities because we lack methods that enable collection of simultaneous and continuous behavioural information for each worker bee. In this study, we introduce the Bee Behavioral Annotation System (BBAS), which enables the automated detection of bees’ behaviours in small observation hives. Continuous information on position and orientation were obtained by marking worker bees with 2D barcodes in a small observation hive. We computed behavioural and social features from the tracking information to train a behaviour classifier for encounter behaviours (interaction of workers via antennation) using a machine learning-based system. The classifier correctly detected 93% of the encounter behaviours in a group of bees, whereas 13% of the falsely classified behaviours were unrelated to encounter behaviours. The possibility of building accurate classifiers for automatically annotating behaviours may allow for the examination of individual behaviours of worker bees in the social environments of small observation hives. We envisage that BBAS will be a powerful tool for detecting the effects of experimental manipulation of social attributes and sub-lethal effects of pesticides on behaviour.

[1]  Thomas Schmickl,et al.  Standard methods for behavioural studies of Apis mellifera , 2013 .

[2]  Robert E. Page,et al.  Levels of behavioral organization and the evolution of division of labor , 2002, Naturwissenschaften.

[3]  W. Farina,et al.  Trophallaxis in the honeybee, Apis mellifera (L.) as related to the profitability of food sources , 1991, Animal Behaviour.

[4]  Kristin Branson,et al.  JAABA: interactive machine learning for automatic annotation of animal behavior , 2013, Nature Methods.

[5]  Robert E. Page,et al.  Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.) , 1995, Behavioral Ecology and Sociobiology.

[6]  William A. Dreyer,et al.  The Behaviour and Social Life of Honeybees , 1955, Ecology.

[7]  N. Koeniger The biology of the honey bee , 1988, Insectes Sociaux.

[8]  G. Robinson,et al.  Social inhibition and the regulation of temporal polyethism in honey bees. , 2001, Journal of theoretical biology.

[9]  Michael D. Breed,et al.  The Biology of Social Insects , 1982 .

[10]  J. Goyret,et al.  Descriptive study of antennation during trophallactic unloading contacts in honeybees Apis mellifera carnica , 2003, Insectes Sociaux.

[11]  Werner Backhaus,et al.  Color opponent coding in the visual system of the honeybee , 1991, Vision Research.

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

[13]  William J. Bell,et al.  Social behaviour as a function of context in a cockroach , 1983, Animal Behaviour.

[14]  E. Wilson,et al.  The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies , 2008 .

[15]  Deborah M. Gordon,et al.  From division of labor to the collective behavior of social insects , 2015, Behavioral Ecology and Sociobiology.

[16]  M. Lindauer,et al.  Über die Einwirkung von Duft- und Geschmacksstoffen sowie anderer Faktoren auf die Tänze der Bienen , 1949, Zeitschrift für vergleichende Physiologie.

[17]  G. Theraulaz,et al.  Response threshold reinforcements and division of labour in insect societies , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  Zhengzheng S Liang,et al.  Molecular Determinants of Scouting Behavior in Honey Bees , 2012, Science.

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

[20]  J. Free,et al.  A study of the stimuli which release the food begging and offering responses of worker honeybees , 1956 .

[21]  Axel Decourtye,et al.  A Locomotor Deficit Induced by Sublethal Doses of Pyrethroid and Neonicotinoid Insecticides in the Honeybee Apis mellifera , 2015, PloS one.

[22]  J. Fewell,et al.  Models of division of labor in social insects. , 2001, Annual review of entomology.

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

[24]  Tom Wenseleers The superorganism revisited (Review of "The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies" by B. Hoelldobler & E.O. Wilson and "The Buzz about Bees: Biology of a Superorganism" by J. Tautz) , 2009 .

[25]  A. Lenoir,et al.  An informational analysis of antennal communication during trophallaxis in the ant Myrmica Rubra L. , 1982, Behavioural Processes.

[26]  Karl von Frisch,et al.  Tanzsprache und Orientierung der Bienen , 1965 .

[27]  J. Božič,et al.  Attendants and followers of honey bee waggle dances , 1991 .

[28]  Rodrigo De Marco,et al.  Changes in food source profitability affect the trophallactic and dance behavior of forager honeybees (Apis mellifera L.) , 2001, Behavioral Ecology and Sociobiology.

[29]  Joaquín Goyret,et al.  Trophallactic chains in honeybees: a quantitative approach of the nectar circulation amongst workers , 2005 .

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

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

[32]  T. Seeley Social foraging by honeybees: how colonies allocate foragers among patches of flowers , 1986, Behavioral Ecology and Sociobiology.

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

[34]  W. Farina,et al.  Food-exchange by foragers in the hive – a means of communication among honey bees? , 1996, Behavioral Ecology and Sociobiology.

[35]  Chris Tofts Algorithms for task allocation in ants. (A study of temporal polyethism: Theory) , 1993 .

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

[37]  T. Seeley The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies , 1995 .

[38]  W. J. Bell,et al.  Comparison of male agonistic behavior in five species of cockroaches , 1979, Insectes Sociaux.

[39]  M. Gil,et al.  Olfactory learning by means of trophallaxis in Apis mellifera , 2005, Journal of Experimental Biology.

[40]  W. Farina,et al.  Thermographic recordings show that honeybees may receive nectar from foragers even during short trophallactic contacts , 2001, Insectes Sociaux.

[41]  Martin Beye,et al.  Mixing of Honeybees with Different Genotypes Affects Individual Worker Behavior and Transcription of Genes in the Neuronal Substrate , 2012, PloS one.

[42]  Edwin Olson,et al.  AprilTag: A robust and flexible visual fiducial system , 2011, 2011 IEEE International Conference on Robotics and Automation.

[43]  Thomas D. Seeley,et al.  The control of water collection in honey bee colonies , 1997, Behavioral Ecology and Sociobiology.

[44]  Martin Beye,et al.  Highly efficient integration and expression of piggyBac-derived cassettes in the honeybee (Apis mellifera) , 2014, Proceedings of the National Academy of Sciences.

[45]  W. Farina,et al.  Trophallaxis within the dancing context: a behavioral and thermographic analysis in honeybees (Apis mellifera) , 2005 .

[46]  Karl von Frisch,et al.  Über die "Sprache" der bienen : Eine tierpsychologische Untersuchung , 1923 .

[47]  E. Bonabeau,et al.  Fixed response thresholds and the regulation of division of labor in insect societies , 1998 .

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