Honey bees live in colonies of thousands of individuals, that not only need to collaborate with each other but also to interact intensively with their ecosystem. A small group of robots operating in a honey bee colony and interacting with the queen bee, a central colony element, has the potential to change the collective behavior of the entire colony and thus also improve its interaction with the surrounding ecosystem. Such a system can be used to study and understand many elements of bee behavior within hives that have not been adequately researched. We discuss here the applicability of this technology for ecosystem protection: A novel paradigm of a minimally invasive form of conservation through "Ecosystem Hacking". We discuss the necessary requirements for such technology and show experimental data on the dynamics of the natural queen's court, initial designs of biomimetic robotic surrogates of court bees, and a multi-agent model of the queen bee court system. Our model is intended to serve as an AI-enhanceable coordination software for future robotic court bee surrogates and as a hardware controller for generating nature-like behavior patterns for such a robotic ensemble. It is the first step towards a team of robots working in a bio-compatible way to study honey bees and to increase their pollination performance, thus achieving a stabilizing effect at the ecosystem level.

Artificial Intelligence Centre Faculty of Electrical Engineering Czech Technical University Prague Czechia

Artificial Life Lab Institute of Biology University of Graz Graz Austria

Department of Computer Engineering Middle East Technical University Ankara Türkiye

Department of Mechanical Engineering Middle East Technical University Ankara Türkiye

ROMER Center for Robotics and Artificial Intelligence Middle East Technical University Ankara Türkiye

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Front Robot AI. 2022 Nov 02;9:1058324. doi: 10.3389/frobt.2022.1058324. PubMed

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Allen M. D. (1955). Observations on Honeybees Attending Their Queen. Br. J. Anim. Behav. 3, 66–69. 10.1016/s0950-5601(55)80015-9 DOI

Baracchi D., Devaud J. M., d'Ettorre P., Giurfa M. (2017). Pheromones Modulate Reward Responsiveness and Non-associative Learning in Honey Bees. Sci. Rep. 7, 9875–9879. 10.1038/s41598-017-10113-7 PubMed DOI PMC

Barlow S. E., O’Neill M. A. (2020). Technological Advances in Field Studies of Pollinator Ecology and the Future of E-Ecology. Curr. Opin. Insect Sci. 38, 15–25. 10.1016/j.cois.2020.01.008 PubMed DOI

Beekman M., Ratnieks F. L. W. (2000). Long-range Foraging by the Honey-Bee, Apis mellifera L. Funct. Ecol. 14, 490–496. 10.1046/j.1365-2435.2000.00443.x DOI

Bertelsmeier C. (2021). Globalization and the Anthropogenic Spread of Invasive Social Insects Special Section on Pollinator Decline: Human and Policy Dimensions * Social Insects. Curr. Opin. Insect Sci. 46, 16–23. 10.1016/j.cois.2021.01.006 PubMed DOI

Bierbach D., Landgraf T., Romanczuk P., Lukas J., Nguyen H., Wolf M., et al. (2018). Using a Robotic Fish to Investigate Individual Differences in Social Responsiveness in the Guppy. R. Soc. Open Sci. 5, 181026. 10.1098/rsos.181026 PubMed DOI PMC

Bonabeau E., Theraulaz G., Deneubourg J.-L. (1998). Fixed Response Thresholds and the Regulation of Division of Labor in Insect Societies. Bull. Math. Biol. 60, 753–807. 10.1006/bulm.1998.0041 DOI

Bonabeau E., Theraulaz G., Deneubourg J.-L. (1996). Quantitative Study of the Fixed Threshold Model for the Regulation of Division of Labour in Insect Societies. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 263, 1565–1569.

Bonabeau E., Theraulaz G., Dorigo M. (1999). Swarm Intelligence. Springer.

Bonnet F., Mills R., Szopek M., Schönwetter-Fuchs S., Halloy J., Bogdan S., et al. (2019). Robots Mediating Interactions between Animals for Interspecies Collective Behaviors. Sci. Robot. 4. 10.1126/scirobotics.aau7897 PubMed DOI

Bonnet F., Cazenille L., Séguret A., Gribovskiy A., Collignon B., Halloy J., et al. (2017). Design of a Modular Robotic System that Mimics Small Fish Locomotion and Body Movements for Ethological Studies. Int. J. Adv. Robotic Syst. 14, 1729881417706628. 10.1177/1729881417706628 DOI

Bonnet F., Gribovskiy A., Halloy J., Mondada F. (2018). Closed-loop Interactions between a Shoal of Zebrafish and a Group of Robotic Fish in a Circular Corridor. Swarm Intell. 12, 227–244. 10.1007/s11721-017-0153-6 DOI

Bossert W. H., Wilson E. O. (1963). The Analysis of Olfactory Communication Among Animals. J. Theor. Biol. 5, 443–469. 10.1016/0022-5193(63)90089-4 PubMed DOI

Boswell G. P., Britton N. F., Franks N. R. (1998). Habitat Fragmentation, Percolation Theory and the Conservation of a Keystone Species. Proc. R. Soc. Lond. B 265, 1921–1925. 10.1098/rspb.1998.0521 DOI

Brian M. V. (2013). Social Insect Populations. Elsevier.

Camazine S., Deneubourg J.-L., Franks N. R., Sneyd J., Theraula G., Bonabeau E. (2020). Self-organization in Biological Systems. Princeton University Press.

Castellucci V., Pinsker H., Kupfermann I., Kandel E. R. (1970). Neuronal Mechanisms of Habituation and Dishabituation of the Gill-Withdrawal Reflex in aplysia. Science 167, 1745–1748. 10.1126/science.167.3926.1745 PubMed DOI

Correll N., Schwager M., Rus D. (2008). “Social Control of Herd Animals by Integration of Artificially Controlled Congeners,” in International Conference on Simulation of Adaptive Behavior (Springer; ), 437–446.

Crailsheim K., Eggenreich U., Ressi R., Szolderits M. J. (1999). Temperatur-Präferenz von männlichen Honigbienen (Hymenoptera: Apidae). Entomol. Gen. 24, 37–47. 10.1127/entom.gen/24/1999/37 DOI

Detrain C., Tasse O. (2000). Seed Drops and Caches by the Harvester Ant Messor Barbarus : Do They Contribute to Seed Dispersal in Mediterranean Grasslands? Naturwissenschaften 87, 373–376. 10.1007/s001140050744 PubMed DOI

Easton-Calabria A., Demary K. C., Oner N. J. (2019). Beyond Pollination: Honey Bees (apis Mellifera) as Zootherapy Keystone Species. Front. Ecol. Evol. 6, 161–177. 10.3389/fevo.2018.00161 DOI

Edwards-Murphy F., Magno M., Whelan P. M., O’Halloran J., Popovici E. M. (2016). b+WSN: Smart Beehive with Preliminary Decision Tree Analysis for Agriculture and Honey Bee Health Monitoring. Comput. Elect. Agric. 124, 211–219. 10.1016/j.compag.2016.04.008 DOI

Eubanks M. D., Lin C., Tarone A. M. (2019). The Role of Ants in Vertebrate Carrion Decomposition. Food Webs 18, e00109. 10.1016/j.fooweb.2018.e00109 DOI

Faria J. J., Dyer J. R. G., Clément R. O., Couzin I. D., Holt N., Ward A. J. W., et al. (2010). A Novel Method for Investigating the Collective Behaviour of Fish: Introducing 'Robofish'. Behav. Ecol. Sociobiol. 64, 1211–1218. 10.1007/s00265-010-0988-y DOI

Feltell D., Bai L., Jensen H. J. (2008). An Individual Approach to Modelling Emergent Structure in Termite Swarm Systems. Int. J. Model. Identif. Control. 3, 29–40. 10.1504/ijmic.2008.018181 DOI

Fewell J. H., Winston M. L. (1992). Colony State and Regulation of Pollen Foraging in the Honey Bee, Apis mellifera L. Behav. Ecol. Sociobiol. 30, 387–393. 10.1007/bf00176173 DOI

Free J. B., Ferguson A. W., Simpkins J. R. (1992). The Behaviour of Queen Honeybees and Their Attendants. Physiol. Entomol. 17, 43–55. 10.1111/j.1365-3032.1992.tb00988.x DOI

Gallai N., Salles J.-M., Settele J., Vaissière B. E. (2009). Economic Valuation of the Vulnerability of World Agriculture Confronted with Pollinator Decline. Ecol. Econ. 68, 810–821. 10.1016/j.ecolecon.2008.06.014 DOI

Gauch H. G., Jr, Gauch H. G., Jr, Gauch H. G. (2003). Scientific Method in Practice. Cambridge University Press.

Gautrais J., Theraulaz G., Deneubourg J.-L., Anderson C. (2002). Emergent Polyethism as a Consequence of Increased Colony Size in Insect Societies. J. Theor. Biol. 215, 363–373. 10.1006/jtbi.2001.2506 PubMed DOI

Griparić K., Haus T., Miklić D., Polić M., Bogdan S. (2017). A Robotic System for Researching Social Integration in Honeybees. PloS one 12, e0181977. 10.1371/journal.pone.0181977 PubMed DOI PMC

Hallmann C. A., Sorg M., Jongejans E., Siepel H., Hofland N., Schwan H., et al. (2017). More Than 75 Percent Decline over 27 Years in Total Flying Insect Biomass in Protected Areas. PloS one 12, e0185809. 10.1371/journal.pone.0185809 PubMed DOI PMC

Halloy J., Sempo G., Caprari G., Rivault C., Asadpour M., Tâche F., et al. (2007). Social Integration of Robots into Groups of Cockroaches to Control Self-Organized Choices. Science 318, 1155–1158. 10.1126/science.1144259 PubMed DOI

He X.-J., Tian L.-Q., Wu X.-B., Zeng Z.-J. (2016). RFID Monitoring Indicates Honeybees Work Harder before a Rainy Day. Insect Sci. 23, 157–159. 10.1111/1744-7917.12298 PubMed DOI

Hofstadler D. N., Wahby M., Heinrich M. K., Hamann H., Zahadat P., Ayres P., et al. (2017). Evolved Control of Natural Plants. ACM Trans. Auton. Adapt. Syst. 12, 1–24. 10.1145/3124643 DOI

Hoover S. E. R., Keeling C. I., Winston M. L., Slessor K. N. (2003). The Effect of Queen Pheromones on Worker Honey Bee Ovary Development. Naturwissenschaften 90, 477–480. 10.1007/s00114-003-0462-z PubMed DOI

Hristov P., Shumkova R., Palova N., Neov B. (2020). Factors Associated with Honey Bee colony Losses: a Mini-Review. Vet. Sci. 7, 166. 10.3390/vetsci7040166 PubMed DOI PMC

Hung K.-L. J., Kingston J. M., Albrecht M., Holway D. A., Kohn J. R. (2018). The Worldwide Importance of Honey Bees as Pollinators in Natural Habitats. Proc. R. Soc. B. 285, 20172140. 10.1098/rspb.2017.2140 PubMed DOI PMC

Ilgün A., Angelov K., Stefanec M., Schönwetter-Fuchs S., Stokanic V., Vollmann J., et al. (2021). “Bio-hybrid Systems for Ecosystem Level Effects,” in ALIFE 2021: The 2021 Conference on Artificial Life (MIT Press; ), 41. 10.1162/isal_a_00396 DOI

Katzav-Gozansky T., Boulay R., Soroker V., Hefetz A. (2006). Queen Pheromones Affecting the Production of Queen-like Secretion in Workers a Neuroethology, Sensory, Neural, and Behavioral Physiology. J. Comp. Physiol. A. PubMed

Klein A.-M., Vaissière B. E., Cane J. H., Steffan-Dewenter I., Cunningham S. A., Kremen C., et al. (2007). Importance of Pollinators in Changing Landscapes for World Crops. Proc. R. Soc. B. 274, 303–313. 10.1098/rspb.2006.3721 PubMed DOI PMC

Kleinhenz M., Bujok B., Fuchs S., Tautz J. (2003). Hot Bees in Empty Broodnest Cells: Heating from Within. J. Exp. Biol. 206, 4217–4231. 10.1242/jeb.00680 PubMed DOI

Landgraf T., Bierbach D., Nguyen H., Muggelberg N., Romanczuk P., Krause J. (2016). Robofish: Increased Acceptance of Interactive Robotic Fish with Realistic Eyes and Natural Motion Patterns by Live Trinidadian Guppies. Bioinspir. Biomim. 11, 015001. 10.1088/1748-3190/11/1/015001 PubMed DOI

Landgraf T., Oertel M., Rhiel D., Rojas R. (2010). “A Biomimetic Honeybee Robot for the Analysis of the Honeybee Dance Communication System,” in 2010 IEEE/RSJ International Conference on Intelligent Robots and Systems (IEEE; ), 3097–3102. 10.1109/iros.2010.5650930 DOI

Landgraf T., Rojas R., Nguyen H., Kriegel F., Stettin K. (2011). Analysis of the Waggle Dance Motion of Honeybees for the Design of a Biomimetic Honeybee Robot. PloS one 6, e21354. 10.1371/journal.pone.0021354 PubMed DOI PMC

Lazic D., Schmickl T. (2021). “Can Robots Inform a Honeybee colony’s Foraging Decision-Making?,” in ALIFE 2021: The 2021 Conference on Artificial Life (MIT Press; ), 42.

Le Conte Y., Navajas M. (2008). Climate Change: Impact on Honey Bee Populations and Diseases. Rev. Sci. Tech. 27, 499–510. 10.20506/rst.27.2.1819 PubMed DOI

Lorenz K. (1970). On Killing Members of One's Own Species. Bull. At. Scientists 26, 2–56. 10.1080/00963402.1970.11457850 DOI

McGlynn T. P., Poirson E. K. (2012). Ants Accelerate Litter Decomposition in a Costa Rican Lowland Tropical Rain forest. J. Trop. Ecol. 28, 437–443. 10.1017/s0266467412000375 DOI

Mello M. A. R., Santos G. M. d. M., Mechi M. R., Hermes M. G. (2011). High Generalization in Flower-Visiting Networks of Social Wasps. Acta Oecologica 37, 37–42. 10.1016/j.actao.2010.11.004 DOI

Menzel F., Feldmeyer B. (2021). How Does Climate Change Affect Social Insects? Curr. Opin. Insect Sci. 46, 10–15. 10.1016/j.cois.2021.01.005 PubMed DOI

Nguyen D. M. T., Iuzzolino M. L., Mankel A., Bozek K., Stephens G. J., Peleg O. (2021). Flow-mediated Olfactory Communication in Honeybee Swarms. Proc. Natl. Acad. Sci. 118. 10.1073/pnas.2011916118 PubMed DOI PMC

Pascual-Garrido A., Umaru B., Allon O., Sommer V. (2013). Apes Finding Ants: Predator-Prey Dynamics in a Chimpanzee Habitat in Nigeria. Am. J. Primatol. 75, 1231–1244. 10.1002/ajp.22187 PubMed DOI

Petz M., Stabentheiner A., Crailsheim K. (2004). Respiration of Individual Honeybee Larvae in Relation to Age and Ambient Temperature. J. Comp. Physiol. B 174, 511–518. 10.1007/s00360-004-0439-z PubMed DOI

Poulsen M., Hu H., Li C., Chen Z., Xu L., Otani S., et al. (2014). Complementary Symbiont Contributions to Plant Decomposition in a Fungus-Farming Termite. Proc. Natl. Acad. Sci. U.S.A. 111, 14500–14505. 10.1073/pnas.1319718111 PubMed DOI PMC

Prezoto F., Maciel T. T., Detoni M., Mayorquin A. Z., Barbosa B. C. (2019). Pest Control Potential of Social Wasps in Small Farms and Urban Gardens. Insects 10, 192. 10.3390/insects10070192 PubMed DOI PMC

Rajewicz W., Romano D., Varughese J. C., Vuuren G. J. V., Campo A., Thenius R., et al. (2021). Freshwater Organisms Potentially Useful as Biosensors and Power-Generation Mediators in Biohybrid Robotics. Biol. Cybern. 115, 615–628. 10.1007/s00422-021-00902-9 PubMed DOI PMC

Sanchez C. J., Chiu C.-W., Zhou Y., González J. M., Vinson S. B., Liang H. (2015). Locomotion Control of Hybrid Cockroach Robots. J. R. Soc. Interf. 12, 20141363. 10.1098/rsif.2014.1363 PubMed DOI PMC

Schmickl T., Blaschon B., Gurmann B., Crailsheim K. (2003). Collective and Individual Nursing Investment in the Queen and in Young and Old Honeybee Larvae during Foraging and Non-foraging Periods. Insectes. Soc. 50, 174–184.

Schmickl T., Bogdan S., Correia L., Kernbach S., Mondada F., Bodi M., et al. (2013a). “Assisi: Mixing Animals with Robots in a Hybrid Society,” in Conference on Biomimetic and Biohybrid Systems (Springer; ), 441–443. 10.1007/978-3-642-39802-5_60 DOI

Schmickl T., Szopek M., Bodi M., Hahshold S., Radspieler G., Thenius R., et al. (2013b). “Assisi: Charged Hot Bees Shakin’in the Spotlight,” in 2013 IEEE 7th International Conference on Self-Adaptive and Self-Organizing Systems (IEEE; ), 259–260. 10.1109/saso.2013.26 DOI

Schmickl T., Szopek M., Mondada F., Mills R., Stefanec M., Hofstadler D. N., et al. (2021). Social Integrating Robots Suggest Mitigation Strategies for Ecosystem Decay. Front. Bioeng. Biotechnol. 9, 612605–612616. 10.3389/fbioe.2021.612605 PubMed DOI PMC

Schmickl T., Thenius R., Crailsheim K. (2012). Swarm-intelligent Foraging in Honeybees: Benefits and Costs of Task-Partitioning and Environmental Fluctuations. Neural Comput. Applic. 21, 251–268. 10.1007/s00521-010-0357-9 DOI

Seeley T. D. (1979). Queen Substance Dispersal by Messenger Workers in Honeybee Colonies. Behav. Ecol. Sociobiol. 5, 391–415.

Seeley T. D. (2009). The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies. Harvard University Press.

Sober E. (2002). What Is the Problem of Simplicity? Simplicity, Inference, Econometric Model., 13–31. 10.1017/cbo9780511493164.002 DOI

Stefanec M., Oberreiter H., Becher M. A., Haase G., Schmickl T. (2021). Effects of Sinusoidal Vibrations on the Motion Response of Honeybees. Front. Phys. 9, 318. 10.3389/fphy.2021.670555 DOI

Szopek M., Schmickl T., Thenius R., Radspieler G., Crailsheim K. (2013). Dynamics of Collective Decision Making of Honeybees in Complex Temperature fields. PloS one 8, e76250. 10.1371/journal.pone.0076250 PubMed DOI PMC

Szopek M., Stokanic V., Radspieler G., Schmickl T. (2021a). Simple Physical Interactions Yield Social Self-Organization in Honeybees. Front. Phys. 576. 10.3389/fphy.2021.670317 DOI

Szopek M., Thenius R., Stefanec M., Hofstadler D., Varughese J., Vogrin M., et al. (2021b). Autonome Roboterschwärme als Stabilisatoren gefährdeter Ökosysteme. Navigationen-Zeitschrift für Medien-und Kulturwissenschaften 21, 149–180.

Theraulaz G., Bonabeau E., Denuebourg J.-N. (1998). Response Threshold Reinforcements and Division of Labour in Insect Societies. Proc. R. Soc. Lond. B 265, 327–332. 10.1098/rspb.1998.0299 DOI

Tinbergen N. (1948). Social Releasers and the Experimental Method Required for Their Study. Wilson Bull., 6–51.

Velthuis H. H. W. (1972). Observations on the Transmission of Queen Substances in the Honey Bee colony by the Attendants of the Queen. Behav. 41, 105–128. 10.1163/156853972x00239 DOI

Wahby M., Heinrich M. K., Hofstadler D. N., Neufeld E., Kuksin I., Zahadat P., et al. (2018). Autonomously Shaping Natural Climbing Plants: a Bio-Hybrid Approach. R. Soc. Open Sci. 5, 180296. 10.1098/rsos.180296 PubMed DOI PMC

Way M. J., Khoo K. C. (1992). Role of Ants in Pest Management. Annu. Rev. Entomol. 37, 479–503. 10.1146/annurev.en.37.010192.002403 DOI

Williams G. R., Tarpy D. R., vanEngelsdorp D., Chauzat M.-P., Cox-Foster D. L., Delaplane K. S., et al. (2010). Colony Collapse Disorder in Context. Bioessays 32, 845–846. 10.1002/bies.201000075 PubMed DOI PMC

On the movement of the honeybee queen in the hive

Evolutionary optimization for risk-aware heterogeneous multi-agent path planning in uncertain environments