Abstract
Living organisms are far superior to state-of-the-art robots as they have evolved a wide number of capabilities that far encompass our most advanced technologies. The merging of biological and artificial world, both physically and cognitively, represents a new trend in robotics that provides promising prospects to revolutionize the paradigms of conventional bio-inspired design as well as biological research. In this review, a comprehensive definition of animal–robot interactive technologies is given. They can be at animal level, by augmenting physical or mental capabilities through an integrated technology, or at group level, in which real animals interact with robotic conspecifics. Furthermore, an overview of the current state of the art and the recent trends in this novel context is provided. Bio-hybrid organisms represent a promising research area allowing us to understand how a biological apparatus (e.g. muscular and/or neural) works, thanks to the interaction with the integrated technologies. Furthermore, by using artificial agents, it is possible to shed light on social behaviours characterizing mixed societies. The robots can be used to manipulate groups of living organisms to understand self-organization and the evolution of cooperative behaviour and communication.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abaid N, Bartolini T, Macrì S, Porfiri M (2012) Zebrafish responds differentially to a robotic fish of varying aspect ratio, tail beat frequency, noise, and color. Behav Brain Res 233(2):545–553
Abaid N, Marras S, Fitzgibbons C, Porfiri M (2013) Modulation of risk-taking behaviour in golden shiners (Notemigonus crysoleucas) using robotic fish. Behav Process 100:9–12
Aktakka EE, Kim H, Najafi K (2011) Energy scavenging from insect flight. J Micromech Microeng 21(9):095016
Ando N, Kanzaki R (2017) Using insects to drive mobile robots—hybrid robots bridge the gap between biological and artificial systems. Arthropod Struct Dev. https://doi.org/10.1016/j.asd.2017.02.003
ASAB/ABS (2004) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 99:1–9
Aureli M, Fiorilli F, Porfiri M (2012) Portraits of self-organization in fish schools interacting with robots. Phys D 9:908–920
Ayers J, Clarac F (1978) Neuromuscular strategies underlying different behavioural acts in a multifunctional crustacean leg joint. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 128(1):81–94
Ayers JL Jr, Davis WJ (1977) Neuronal control of locomotion in the lobster, Homarus americanus. J Comp Physiol 115(1):1–27
Bao L, Zheng N, Zhao H, Hao Y, Zheng H, Hu F, Zheng X (2011) Flight control of tethered honeybees using neural electrical stimulation. In: 2011 5th international IEEE/EMBS conference on neural engineering (NER). IEEE, pp 558–561
Bartolini T, Mwaffo V, Showler A, Macrì S, Butail S, Porfiri M (2016) Zebrafish response to 3D printed shoals of conspecifics: the effect of body size. Bioinspir Biomim 11(2):026003
Beer RD, Quinn RD, Chiel HJ, Ritzmann RE (1997) Biologically inspired approaches to robotics: What can we learn from insects? Commun ACM 40(3):30–38
Benelli G, Romano D, Rocchigiani G, Caselli A, Mancianti F, Canale A, Stefanini C (2018) Behavioral asymmetries in ticks–lateralized questing of Ixodes ricinus to a mechatronic apparatus delivering host-borne cues. Acta Trop 178:176–181
Bierbach D, Lukas JA, Bergmann A, Elsner K, Höhne L, Weber C, Weimar N, Arias-Rodriguez L, Mönk HJ, Nguyen H, Romanczuk P, Landgraf T, Krause J (2018a) Insights into the social behavior of surface and cave-dwelling fish (Poecilia mexicana) in light and darkness through the use of a biomimetic robot. Front Robot AI 5:3. https://doi.org/10.3389/frobt.2018.00003
Bierbach D, Landgraf T, Romanczuk P, Lukas J, Nguyen H, Wolf M, Krause J (2018b) Using a robotic fish to investigate individual differences in social responsiveness in the guppy. bioRxiv https://doi.org/10.1101/304501
Bodi M, Möslinger C, Thenius R, Schmickl T (2015) BEECLUST used for exploration tasks in autonomous underwater vehicles. IFAC PapersOnLine 48(1):819–824
Bonnet F, Binder S, de Oliveria M E, Halloy J, Mondada F (2014) A miniature mobile robot developed to be socially integrated with species of small fish. In: 2014 IEEE international conference on robotics and biomimetics (ROBIO). IEEE, pp 747–752
Bonnet F, Crot N, Burnier D, Mondada F (2016a) Design methods for miniature underwater soft robots. In: 2016 6th IEEE international conference on biomedical robotics and biomechatronics (BioRob). IEEE, pp 1365–1370
Bonnet F, Kato Y, Halloy J, Mondada F (2016b) Infiltrating the zebrafish swarm: design, implementation and experimental tests of a miniature robotic fish lure for fish–robot interaction studies. Artif Life Robot 21(3):239–246
Bonnet F, Cazenille L, Séguret A, Gribovskiy A, Collignon B, Halloy J, Mondada F (2017a) Design of a modular robotic system that mimics small fish locomotion and body movements for ethological studies. Int J Adv Robot Syst 14(3):1729881417706628
Bonnet F, Cazenille L, Gribovskiy A, Halloy J, Mondada F (2017b) Multi-robot control and tracking framework for bio-hybrid systems with closed-loop interaction. In: 2017 IEEE international conference on robotics and automation (ICRA). IEEE, pp 4449–4456
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 Intelligence 12:1–18
Bonsignori G, Stefanini C, Scarfogliero U, Mintchev S, Benelli G, Dario P (2013) The green leafhopper, Cicadella viridis (Hemiptera, Auchenorrhyncha, Cicadellidae), jumps with near-constant acceleration. J Exp Biol 216(7):1270–1279
Bozkurt A, Paul A, Pulla S, Ramkumar A, Blossey B, Ewer J et al (2007) Microprobe microsystem platform inserted during early metamorphosis to actuate insect flight muscle. In: IEEE 20th international conference on micro electro mechanical systems, 2007. MEMS. IEEE, pp 405–408
Bozkurt A, Gilmour R, Stern D, Lal A (2008) MEMS based bioelectronic neuromuscular interfaces for insect cyborg flight control. In: IEEE 21st international conference on micro electro mechanical systems, 2008. MEMS 2008. IEEE, pp 160–163
Bozkurt A, Lal A, Gilmour R (2009) Radio control of insects for biobotic domestication. In: 4th international IEEE/EMBS conference on neural engineering, 2009. NER’09. IEEE, pp 215–218
Bozkurt A, Lobaton E, Sichitiu M (2016) A biobotic distributed sensor network for under-rubble search and rescue. Computer 49(5):38–46
Breazeal C, Dautenhahn K, Kanda T (2016) Social robotics. Springer handbook of robotics. Springer, Cham, pp 1935–1972
Brian Smith C, Martins EP (2006) Display plasticity in response to a robotic lizard: signal matching or song sharing in lizards? Ethology 112(10):955–962
Brown MF, Brown AA (2017) The promise of cyborg intelligence. Learn Behav 45(1):5–6
Butail S, Bartolini T, Porfiri M (2013) Collective response of zebrafish shoals to a free-swimming robotic fish. PLoS ONE 8(10):e76123
Butail S, Polverino G, Phamduy P, Del Sette F, Porfiri M (2014) Influence of robotic shoal size, configuration, and activity on zebrafish behaviour in a free-swimming environment. Behav Brain Res 275:269–280
Butail S, Mwaffo V, Porfiri M (2016) Model-free information-theoretic approach to infer leadership in pairs of zebrafish. Phys Rev E 93(4):042411
Butail S, Mwaffo V, Porfiri M (2017) Inferring leadership in zebrafish pairs: an information-theoretic approach. In: American control conference (ACC), 2017. IEEE, pp 2040–2040
Butler SR, Fernández-Juricic E (2014) European starlings recognize the location of robotic conspecific attention. Biol Lett 10(10):20140665
Cao F, Zhang C, Choo HY, Sato H (2016) Insect–computer hybrid legged robot with user-adjustable speed, step length and walking gait. J R Soc Interface 13(116):20160060
Cazenille L, Chemtob Y, Bonnet F, Gribovskiy A, Mondada F, Bredeche N, Halloy J (2017) Automated calibration of a biomimetic space-dependent model for zebrafish and robot collective behaviour in a structured environment. In: Conference on biomimetic and biohybrid systems. Springer, Cham, pp 107–118
Cazenille L, Collignon B, Chemtob Y, Bonnet F, Gribovskiy A, Mondada F, Bredeche N, Halloy J (2018a) How mimetic should a robotic fish be to socially integrate into zebrafish groups? Bioinspir Biomim 13(2):025001. https://doi.org/10.1088/1748-3190/aa8f6a
Cazenille L, Chemtob Y, Bonnet F, Gribovskiy A, Mondada F, Bredeche N, Halloy J (2018b) How to blend a robot within a group of zebrafish: achieving social acceptance through real-time calibration of a multi-level behavioural model. arXiv preprint arXiv:1805.11371
Cham JG, Bailey SA, Clark JE, Full RJ, Cutkosky MR (2002) Fast and robust: hexapedal robots via shape deposition manufacturing. Int J Robot Res 21(10–11):869–882
Choo HY, Li Y, Cao F, Sato H (2016) Electrical stimulation of coleopteran muscle for initiating flight. PLoS ONE 11(4):e0151808
Cianca V, Bartolini T, Porfiri M, Macrì S (2013) A robotics-based behavioural paradigm to measure anxiety-related responses in zebrafish. PLoS ONE 8(7):e69661
Cole J, Mohammadzadeh F, Bollinger C, Latif T, Bozkurt A, Lobaton E (2017) A study on motion mode identification for cyborg roaches. In: 2017 IEEE international conference on acoustics, speech and signal processing (ICASSP). IEEE, pp 2652–2656
Cord-Cruz G, Ruberto T, Neri D, Porfiri M (2017) Zebrafish response to live predator and biologically-inspired robot in a circular arena. In: SPIE smart structures and materials + nondestructive evaluation and health monitoring. International Society for Optics and Photonics, p 101620P
Couzin ID (2009) Collective cognition in animal groups. Trends in Cognitive Sciences 13(1):36–43
De Margerie E, Lumineau S, Houdelier C, Yris MR (2011) Influence of a mobile robot on the spatial behaviour of quail chicks. Bioinspir Biomim 6(3):034001
De Margerie E, Peris A, Pittet F, Houdelier C, Lumineau S, Richard-Yris MA (2013) Effect of mothering on the spatial exploratory behaviour of quail chicks. Dev Psychobiol 55(3):256–264
Decker M, Dillmann R, Dreier T, Fischer M, Gutmann M, Ott I, genannt Döhmann IS (2011) Service robotics: Do you know your new companion? Framing an interdisciplinary technology assessment. Poiesis Prax 8(1):25–44
Dirafzoon A, Bozkurt A, Lobaton E (2017a) A framework for mapping with biobotic insect networks: from local to global maps. Robot Auton Syst 88:79–96
Dirafzoon A, Bozkurt A, Lobaton E (2017b) Geometric learning and topological inference with biobotic networks. IEEE Trans Signal Inf Process Netw 3(1):200–215
Doan TTV, Sato H (2016) Insect-machine hybrid system: remote radio control of a freely flying beetle (Mercynorrhina torquata). J Vis Exp 115:e54260–e54260
Dodd A (2014) The trouble with insect cyborgs. Soc Anim 22(2):153–173
Donati E, Worm M, Mintchev S, Van Der Wiel M, Benelli G, Von Der Emde G, Stefanini C (2016) Investigation of collective behaviour and electrocommunication in the weakly electric fish, Mormyrus rume, through a biomimetic robotic dummy fish. Bioinspir Biomim 11(6):066009
El Ichi-Ribault S, Alcaraz JP, Boucher F, Boutaud B, Dalmolin R, Boutonnat J, Cinquin P, Zebda A, Martin DK (2018) Remote wireless control of an enzymatic biofuel cell implanted in a rabbit for 2 months. Electrochim Acta 269:360–366
El Khoury R, Ventura R B, Cord-Cruz G, Ruberto T, Porfiri M (2018) Interactive experiments in a robotics-based platform to simulate zebrafish response to a predator. In: Bioinspiration, biomimetics, and bioreplication VIII. International Society for Optics and Photonics, vol 10593. SPIE, p 105930I
Ellington CP (1999) The novel aerodynamics of insect flight: applications to micro-air vehicles. J Exp Biol 202(23):3439–3448
Erickson JC, Herrera M, Bustamante M, Shingiro A, Bowen T (2015) Effective stimulus parameters for directed locomotion in Madagascar hissing cockroach biobot. PLoS ONE 10(8):e0134348
Faria JJ, Dyer JR, Clément RO, Couzin ID, Holt N, Ward AJ et al (2010) A novel method for investigating the collective behaviour of fish: introducing ‘Robofish’. Behav Ecol Sociobiol 64(8):1211–1218
Fernández-Juricic E, Kowalski V (2011) Where does a flock end from an information perspective? A comparative experiment with live and robotic birds. Behav Ecol 22(6):1304–1311
Fernández-Juricic E, Gilak N, Mcdonald JC, Pithia P, Valcarcel A (2006) A dynamic method to study the transmission of social foraging information in flocks using robots. Anim Behav 71(4):901–911
Folkertsma GA, Straatman W, Nijenhuis N, Venner CH, Stramigioli S (2017) Robird: a robotic bird of prey. IEEE Robot Autom Mag 24(3):22–29
Forlizzi J and DiSalvo C (2006) Service robots in the domestic environment: a study of the roomba vacuum in the home. In: Proceedings of the 1st ACM SIGCHI/SIGART conference on human–robot interaction. ACM, pp 258–265
Frohnwieser A, Murray JC, Pike TW, Wilkinson A (2016) Using robots to understand animal cognition. J Exp Anal Behav 105(1):14–22
Fry SN, Rohrseitz N, Straw AD, Dickinson MH (2009) Visual control of flight speed in Drosophila melanogaster. J Exp Biol 212(8):1120–1130
Fujiwara D, Iizuka K, Matsumura Y, Moriyama T, Watanabe R, Enomoto K et al (2012) The effect of mobile robot on group behaviour of animals. J Robot Mechatron 24(6):1071–1079
Garnier S (2011) From ants to robots and back: How robotics can contribute to the study of collective animal behaviour. Bio-inspired self-organizing robotic systems. Springer, Berlin, pp 105–120
Giampalmo SL, Absher BF, Bourne WT, Steves LE, Vodenski VV, O’Donnell P M, Erickson JC (2011) Generation of complex motor patterns in American grasshopper via current-controlled thoracic electrical interfacing. In: 2011 annual international conference of the IEEE engineering in medicine and biology society, EMBC. IEEE, pp 1275–1278
Göth A, Evans CS (2004) Social responses without early experience: Australian brush-turkey chicks use specific visual cues to aggregate with conspecifics. J Exp Biol 207(13):2199–2208
Gribovskiy A, Halloy J, Deneubourg JL, Bleuler H, Mondada F (2010) Towards mixed societies of chickens and robots. In: 2010 IEEE/RSJ international conference on intelligent robots and systems (IROS). IEEE, pp 4722–4728
Gribovskiy A, Mondada F, Deneubourg JL, Cazenille L, Bredeche N, Halloy J (2015) Automated analysis of behavioural variability and filial imprinting of chicks (G. gallus), using autonomous robots. arXiv:1509.01957
Gribovskiy A, Halloy J, Deneubourg JL, Mondada F (2018) Designing a socially integrated mobile robot for ethological research. Robot Auton Syst 103:42–55
Grillner S, Kozlov A, Dario P, Stefanini C, Menciassi A, Lansner A, Kotaleski JH (2007) Modeling a vertebrate motor system: pattern generation, steering and control of body orientation. Prog Brain Res 165:221–234
Griparić K, Haus T, Miklić D, Polić M, Bogdan S (2017) A robotic system for researching social integration in honeybees. PLoS ONE 12(8):e0181977
Halámková L, Halámek J, Bocharova V, Szczupak A, Alfonta L, Katz E (2012) Implanted biofuel cell operating in a living snail. J Am Chem Soc 134(11):5040–5043
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(5853):1155–1158
Halloy J, Mondada F, Kernbach S, Schmickl T (2013) Towards bio-hybrid systems made of social animals and robots. Biomimetic and biohybrid systems. Springer, Berlin, pp 384–386
Hamann H, Wahby M, Schmickl T, Zahadat P, Hofstadler D, Stoy K, Risi S, Faina A, Veenstra F, Kernbach S, Kuksin I, Kernbach O, Ayres P, Wojtaszek P (2015) Flora robotica-mixed societies of symbiotic robot-plant bio-hybrids. In: 2015 IEEE symposium series on computational intelligence. IEEE, pp 1102–1109
Henderson JV, Nicol CJ, Lines JA, White RP, Wathes CM (2001) Behaviour of domestic ducks exposed to mobile predator stimuli. 1. Flock responses. Br Poult Sci 42(4):433–438
Holzer R, Shimoyama I (1997) Locomotion control of a bio-robotic system via electric stimulation. In: Proceedings of the 1997 IEEE/RSJ international conference on intelligent robots and systems, 1997. IROS’97. IEEE, vol 3, pp 1514–1519
Huai R, Yang J, Wang H, Su X (2009) A new robo-animals navigation method guided by the remote control. In: 2nd international conference on biomedical engineering and informatics, 2009. BMEI’09. IEEE, pp 1–4
Huai RT, Yang JQ, Wang H (2016) The robo-pigeon based on the multiple brain regions synchronization implanted microelectrodes. Bioengineered 7(4):213–218
Huntingford FA (1984) Some ethical issues raised by studies of predation and aggression. Anim Behav 32(1):210–215
Ioannou CC (2017) Swarm intelligence in fish? The difficulty in demonstrating distributed and self-organised collective intelligence in (some) animal groups. Behav Process 141:141–151
Ishii H, Shi Q, Fumino S, Konno S, Kinoshita S, Okabayashi S et al (2013) A novel method to develop an animal model of depression using a small mobile robot. Adv Robot 27(1):61–69
Jacobs JA, Siegford JM (2012) Invited review: the impact of automatic milking systems on dairy cow management, behavior, health, and welfare. J Dairy Sci 95:2227–2247
Jadhav AD, Aimo I, Cohen D, Ledochowitsch P, Maharbiz MM (2012) Cyborg eyes: microfabricated neural interfaces implanted during the development of insect sensory organs produce stable neurorecordings in the adult. In: 2012 IEEE 25th international conference on micro electro mechanical systems (MEMS). IEEE, pp 937–940
Jolly L, Pittet F, Caudal JP, Mouret JB, Houdelier C, Lumineau S, De Margerie E (2016) Animal-to-robot social attachment: initial requisites in a gallinaceous bird. Bioinspir Biomim 11(1):016007
JrJH Long, Schumacher J, Livingston N, Kemp M (2006) Four flippers or two? Tetrapodal swimming with an aquatic robot. Bioinspir Biomim 1(1):20
Katz E (2014) Implantable bioelectronics–editorial introduction. In: Implantable bioelectronics. Wiley, Weinheim. https://doi.org/10.1002/9783527673148.ch1
Katz E, MacVittie K (2013) Implanted biofuel cells operating in vivo–methods, applications and perspectives–feature article. Energy Environ Sci 6(10):2791–2803
Katzschmann RK, DelPreto J, MacCurdy R, Rus D (2018) Exploration of underwater life with an acoustically controlled soft robotic fish. Science Robotics. https://doi.org/10.1126/scirobotics.aar3449
Kawabata K, Aonuma H, Hosoda K, Xue J (2013) Controlled interaction with the cricket based on on-line pose estimation of mobile robot. In: 2013 IEEE international conference on robotics and biomimetics (ROBIO). IEEE, pp 1347–1352
Kawabata K, Aonuma H, Hosoda K, Sugimoto Y, Xue J (2014) Experimental study on robotic interactions to the cricket. In: 2014 IEEE international conference on robotics and biomimetics (ROBIO). IEEE, pp. 949–954
Kim S, Spenko M, Trujillo S, Heyneman B, Santos D, Cutkosky MR (2008) Smooth vertical surface climbing with directional adhesion. IEEE Trans Robot 24(1):65–74
Kim CH, Choi B, Kim DG, Lee S, Jo S, Lee PS (2016) Remote navigation of turtle by controlling instinct behaviour via human brain–computer interface. J Bionic Eng 13(3):491–503
Kim C, Ruberto T, Phamduy P, Porfiri M (2018) Closed-loop control of zebrafish behaviour in three dimensions using a robotic stimulus. Sci Rep 8(1):657
King A (2017) The future of agriculture. Nature 544(7651):S21–S23
Kobayashi N, Yoshida M, Matsumoto N, Uematsu K (2009) Artificial control of swimming in goldfish by brain stimulation: confirmation of the midbrain nuclei as the swimming center. Neurosci Lett 452(1):42–46
Kopman V, Laut J, Polverino G, Porfiri M (2013) Closed-loop control of zebrafish response using a bioinspired robotic-fish in a preference test. J R Soc Interface 10(78):20120540
Krause J, Winfield AF, Deneubourg JL (2011) Interactive robots in experimental biology. Trends Ecol Evol 26(7):369–375
Kubinyi E, Miklósi Á, Kaplan F, Gácsi M, Topál J, Csányi V (2004) Social behaviour of dogs encountering AIBO, an animal-like robot in a neutral and in a feeding situation. Behav Process 65(3):231–239
Kuwana Y, Shimoyama I, Miura H (1995) Steering control of a mobile robot using insect antennae. In: 1995 IEEE/RSJ international conference on intelligent robots and systems 95.’Human Robot Interaction and Cooperative Robots’, Proceedings. IEEE, vol 2, pp 530–535
Kuwana Y, Nagasawa S, Shimoyama I, Kanzaki R (1999) Synthesis of the pheromone-oriented behaviour of silkworm moths by a mobile robot with moth antennae as pheromone sensors. Biosens Bioelectron 14(2):195–202
Ladu F, Bartolini T, Panitz SG, Chiarotti F, Butail S, Macrì S, Porfiri M (2015) Live predators, robots, and computer-animated images elicit differential avoidance responses in zebrafish. Zebrafish 12(3):205–214. https://doi.org/10.1089/zeb.2014.1041
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 (IROS). IEEE, pp 3097–3102
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(8):e21354
Landgraf T, Oertel M, Kirbach A, Menzel R, Rojas R (2012) Imitation of the honeybee dance communication system by means of a biomimetic robot. In: Conference on biomimetic and biohybrid systems. Springer, Berlin, pp 132–143
Landgraf T, Nguyen H, Forgo S, Schneider J, Schröer J, Krüger C et al (2013) Interactive robotic fish for the analysis of swarm behaviour. In: International conference in swarm intelligence. Springer, Berlin, pp 1–10
Landgraf T, Nguyen H, Schröer J, Szengel A, Clément RJ, Bierbach D, Krause J (2014) Blending in with the shoal: robotic fish swarms for investigating strategies of group formation in guppies. In: Conference on biomimetic and biohybrid systems. Springer International Publishing, pp 178–189
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(1):015001
Laschi C, Mazzolai B, Patanè F, Mattoli V, Dario P, Ishii H et al (2006) Design and development of a legged rat robot for studying animal–robot interaction. In: The first IEEE/RAS-EMBS international conference on biomedical robotics and biomechatronics, 2006. BioRob 2006. IEEE, pp 631–636
Latif T, Whitmire E, Novak T, Bozkurt A (2014) Towards fenceless boundaries for solar powered insect biobots. In: 2014 36th annual international conference of the IEEE engineering in medicine and biology society (EMBC). IEEE, pp 1670–1673
Latif T, Whitmire E, Novak T, Bozkurt A (2016) Sound localization sensors for search and rescue biobots. IEEE Sens J 16(10):3444–3453
Li G, Zhang D (2016) Brain–computer interface controlled cyborg: establishing a functional information transfer pathway from human brain to cockroach brain. PLoS ONE 11(3):e0150667
Li G, Zhang D (2017) Brain–computer interface controlling cyborg: a functional brain-to-brain interface between human and cockroach. Brain–computer interface research. Springer International Publishing, Cham, pp 71–79
Li Y, Wu J, Sato H (2018) Feedback control-based navigation of a flying insect-machine hybrid robot. Soft Robotics. https://doi.org/10.1089/soro.2017.0118
Lin JY, Yu CN, Jia J, Zhang SM, Wang YW, Chen WD, Zheng XX (2010) Using dlPAG-evoked immobile behaviour in animal–robotics navigation. In: 2010 5th international conference on computer science and education (ICCSE). IEEE, pp 1295–1298
Lin HT, Leisk GG, Trimmer B (2011) GoQBot: a caterpillar-inspired soft-bodied rolling robot. Bioinspir Biomim 6(2):026007
Lockwood JA (1988) Not to harm a fly: our ethical obligations to insects. Between Species 4(3):12
Lorenz K (1935) Der kumpan in der umwelt des vogels. J Ornithol 83(3):289–413. [Translated in K. Lorenz. 1970. Studies in Animal and Human Behaviour. Harvard University Press, Cambridge.]
Macrì S, Neri D, Ruberto T, Mwaffo V, Butail S, Porfiri M (2017) Three-dimensional scoring of zebrafish behaviour unveils biological phenomena hidden by two-dimensional analyses. Sci Rep 7(1):1962
MacVittie K, Halámek J, Halámková L, Southcott M, Jemison WD, Lobel R, Katz E (2013) From “cyborg” lobsters to a pacemaker powered by implantable biofuel cells. Energy Environ Sci 6(1):81–86
Manfredi L, Assaf T, Mintchev S, Marrazza S, Capantini L, Orofino S et al (2013) A bioinspired autonomous swimming robot as a tool for studying goal-directed locomotion. Biol Cybern 107(5):513–527
Marras S, Porfiri M (2012) Fish and robots swimming together: attraction towards the robot demands biomimetic locomotion. J R Soc Interface 9(73):1856–1868
Martinez D, Arhidi L, Demondion E, Masson JB, Lucas P (2014) Using insect electroantennogram sensors on autonomous robots for olfactory searches. J Vis Exp 90:e51704
Martins EP, Ord TJ, Davenport SW (2005) Combining motions into complex displays: playbacks with a robotic lizard. Behav Ecol Sociobiol 58(4):351–360
Mehta D, Altan E, Chandak R, Raman B, Chakrabartty S (2017) Behaving cyborg locusts for standoff chemical sensing. In: 2017 IEEE international symposium on circuits and systems (ISCAS). IEEE, pp 1–4
Michelsen A, Andersen BB, Storm J, Kirchner WH, Lindauer M (1992) How honeybees perceive communication dances, studied by means of a mechanical model. Behav Ecol Sociobiol 30(3–4):143–150
Mitri S, Wischmann S, Floreano D, Keller L (2013) Using robots to understand social behaviour. Biolo Rev 88(1):31–39
Mondada F, Martinoli A, Correll N, Gribovskiy A, Halloy JI, Siegwart R, Deneubourg JL (2013) A general methodology for the control of mixed natural-artificial societies. Pan Stanford Publishing, Stanford, pp 547–586
Myrick AJ, Baker TC (2010) Locating a compact odor source using a four-channel insect electroantennogram sensor. Bioinspir Biomim 6(1):016002
Narins PM, Grabul DS, Soma KK, Gaucher P, Hödl W (2005) Cross-modal integration in a dart-poison frog. Proc Natl Acad Sci USA 102(7):2425–2429
Park SJ, Gazzola M, Park KS, Park S, Di Santo V, Blevins EL et al (2016) Phototactic guidance of a tissue-engineered soft-robotic ray. Science 353(6295):158–162
Partan SR, Larco CP, Owens MJ (2009) Wild tree squirrels respond with multisensory enhancement to conspecific robot alarm behaviour. Anim Behav 77(5):1127–1135
Partan SR, Fulmer AG, Gounard MA, Redmond JE (2010) Multimodal alarm behaviour in urban and rural gray squirrels studied by means of observation and a mechanical robot. Curr Zool 56(3):313–326
Partan SR, Otovic P, Price VL, Brown SE (2011) Assessing display variability in wild brown anoles Anolis sagrei using a mechanical lizard model. Curr Zool 57(2):140–152
Pastell M, Takko H, Gröhn H, Hautala M, Poikalainen V, Praks J, Veermäe I, Kujala M, Ahokas J (2006) Assessing cows’ welfare: weighing the cow in a milking robot. Biosyst Eng 93(1):81–87
Patanè F, Mattoli V, Laschi C, Mazzolai B, Dario P, Ishii H, Takanishi A (2007) Biomechatronic design and development of a legged rat robot. In: IEEE international conference on robotics and biomimetics, 2007. ROBIO 2007. IEEE, pp 847–852
Patricelli GL, Krakauer AH (2009) Tactical allocation of effort among multiple signals in sage grouse: an experiment with a robotic female. Behav Ecol 21(1):97–106
Patricelli GL, Uy JAC, Walsh G, Borgia G (2002) Sexual selection: male displays adjusted to female’s response. Nature 415(6869):279–280
Patricelli GL, Coleman SW, Borgia G (2006) Male satin bowerbirds, Ptilonorhynchus violaceus, adjust their display intensity in response to female startling: an experiment with robotic females. Anim Behav 71(1):49–59
Peng Y, Wu Y, Yang Y, Huang R, Wu C, Qi X et al (2011) Study on the control of biological behaviour on carp induced by electrophysiological stimulation in the corpus cerebelli. In: 2011 international conference on electronic and mechanical engineering and information technology (EMEIT). IEEE, vol 1, pp 502–505
Pennisi P, Tonacci A, Tartarisco G, Billeci L, Ruta L, Gangemi S, Pioggia G (2016) Autism and social robotics: a systematic review. Autism Res 9(2):165–183
Pfeifer R, Bongard J (2006) How the body shapes the way we think: a new view of intelligence. MIT press, Cambridge
Phamduy P, Polverino G, Fuller RC, Porfiri M (2014) Fish and robot dancing together: bluefin killifish females respond differently to the courtship of a robot with varying color morphs. Bioinspir Biomim 9(3):036021
Polverino G, Porfiri M (2013) Mosquitofish (Gambusia affinis) responds differentially to a robotic fish of varying swimming depth and aspect ratio. Behav Brain Res 250:133–138
Polverino G, Abaid N, Kopman V, Macrì S, Porfiri M (2012) Zebrafish response to robotic fish: preference experiments on isolated individuals and small shoals. Bioinspir Biomim 7(3):036019
Polverino G, Phamduy P, Porfiri M (2013) Fish and robots swimming together in a water tunnel: robot color and tail-beat frequency influence fish behaviour. PLoS ONE 8(10):e77589
Poon KC, Tan DCL, Li Y, Cao F, Doan TTV, Sato H (2016) Cyborg insect: insect computer hybrid robot. In: Meeting abstracts. Electrochemical Society, vol 44. ECS, p 3221
Rashid MT, Frasca M, Ali AA, Ali RS, Fortuna L, Xibilia MG (2012) Artemia swarm dynamics and path tracking. Nonlinear Dyn 68(4):555–563
Reaney LT, Sims RA, Sims SW, Jennions MD, Backwell PR (2008) Experiments with robots explain synchronized courtship in fiddler crabs. Curr Biol 18(2):R62–R63
Romano D, Benelli G, Donati E, Remorini D, Canale A, Stefanini C (2017a) Multiple cues produced by a robotic fish modulate aggressive behaviour in Siamese fighting fishes. Sci Rep. https://doi.org/10.1038/s41598-017-04840-0
Romano D, Benelli G, Stefanini C (2017b) Escape and surveillance asymmetries in locusts exposed to a Guinea fowl-mimicking robot predator. Sci Rep. https://doi.org/10.1038/s41598-017-12941-z
Romano D, Stefanini C, Canale A, Benelli G (2018) Artificial blood feeders for mosquito and ticks—Where from, where to? Acta Trop 183:43–56
Ruberto T, Mwaffo V, Singh S, Neri D, Porfiri M (2016) Zebrafish response to a robotic replica in three dimensions. R Soc Open Sci 3(10):160505
Ruberto T, Polverino G, Porfiri M (2017) How different is a 3D-printed replica from a conspecific in the eyes of a zebrafish? J Exp Anal Behav 107(2):279–293
Ruhland K, Peters CE, Andrist S, Badler JB, Badler NI, Gleicher M, Mutlu B, McDonnell R (2015) A review of eye gaze in virtual agents, social robotics and hci: behaviour generation, user interaction and perception. In: Computer graphics forum, vol 34, No. 6. Wiley, pp 299–326
Rundus AS, Owings DH, Joshi SS, Chinn E, Giannini N (2007) Ground squirrels use an infrared signal to deter rattlesnake predation. Proc Natl Acad Sci 104(36):14372–14376
Sanchez CJ, Chiu CW, Zhou Y, González JM, Vinson SB, Liang H (2015) Locomotion control of hybrid cockroach robots. J R Soc Interface 12(105):20141363
Sato H, Maharbiz MM (2010) Recent developments in the remote radio control of insect flight. Front Neurosci 4:199
Sato H, Berry CW, Casey BE, Lavella G, Yao Y, VandenBrooks JM, Maharbiz MM (2008) A cyborg beetle: insect flight control through an implantable, tetherless microsystem. In: IEEE 21st international conference on micro electro mechanical systems, 2008. MEMS 2008. IEEE, pp 164–167
Sato H, Berry CW, Peeri Y, Baghoomian E, Casey BE, Lavella G et al (2009) Remote radio control of insect flight. Front Integr Neurosci 3:24
Sato H, Doan TTV, Kolev S, Huynh NA, Zhang C, Massey TL et al (2015) Deciphering the role of a coleopteran steering muscle via free flight stimulation. Curr Biol 25(6):798–803
Savard JF, Keagy J, Borgia G (2011) Blue, not UV, plumage color is important in satin bowerbird Ptilonorhynchus violaceus display. J Avian Biol 42(1):80–84
Schmickl T, Thenius R, Moslinger C, Timmis J, Tyrrell A, Read M, Hilder J, Halloy J, Campo A, Stefanini C, Manfredi L, Orofino S, Kernbach S, Dipper T, Sutantyo D (2011) CoCoRo–the self-aware underwater swarm. In: 2011 fifth IEEE conference on self-adaptive and self-organizing systems workshops (SASOW). IEEE, pp 120–126
Schwefel J, Ritzmann RE, Lee IN, Pollack A, Weeman W, Garverick S et al (2015) Wireless communication by an autonomous self-powered cyborg insect. J Electrochem Soc 161(13):H3113–H3116
Seo J, Choi GJ, Park S, Lee J, Baek C, Jang J et al (2017) Wireless navigation of pigeons using polymer-based fully implantable stimulator: a pilot study using depth electrodes. In: 2017 39th annual international conference of the IEEE engineering in medicine and biology society (EMBC). IEEE, pp 917–920
Sherman PW, Lacey EA, Reeve HK, Keller L (1995) Forum the eusociality continuum. Behav Ecol 6(1):102–108
Shi Q, Miyagishima S, Konno S, Fumino S, Ishii H, Takanishii A et al (2010) Development of the hybrid wheel-legged mobile robot WR-3 designed to interact with rats. In: 2010 3rd IEEE RAS and EMBS international conference on biomedical robotics and biomechatronics (BioRob). IEEE, pp 887–892
Shi Q, Ishii H, Kinoshita S, Takanishi A, Okabayashi S, Iida N et al (2013) Modulation of rat behaviour by using a rat-like robot. Bioinspir Biomim 8(4):046002
Shi Q, Ishii H, Tanaka K, Sugahara Y, Takanishi A, Okabayashi S et al (2015) Behaviour modulation of rats to a robotic rat in multi-rat interaction. Bioinspir Biomim 10(5):056011
Shoji K, Morishima K, Akiyama Y, Nakamura N, Ohno H (2016) Autonomous environmental monitoring by self-powered biohybrid robot. In: 2016 IEEE international conference on mechatronics and automation (ICMA). IEEE, pp 629–634
Spinello C, Macrì S, Porfiri M (2013) Acute ethanol administration affects zebrafish preference for a biologically inspired robot. Alcohol 47(5):391–398
Stefanini C, Orofino S, Manfredi L, Mintchev S, Marrazza S, Assaf T et al (2012) A novel autonomous, bioinspired swimming robot developed by neuroscientists and bioengineers. Bioinspir Biomim 7(2):025001
Stojnić A (2017) Only cyborgs and cockroaches. Perform Res 22(2):123–128
Stowers JR, Hofbauer M, Bastien R, Griessner J, Higgins P, Farooqui S, Fischer RM, Nowikovsky K, Haubensak W, Couzin ID, Tessmar-Raible K, Straw AD (2017) Virtual reality for freely moving animals. Nat Methods 14(10):995
Swain DT, Couzin ID, Leonard NE (2012) Real-time feedback-controlled robotic fish for behavioural experiments with fish schools. Proc IEEE 100(1):150–163
Takanishi A, Aoki T, Ito M, Ohkawa Y, Yamaguchi JI (1998) Interaction between creature and robot: development of an experiment system for rat and rat robot interaction. In: 1998 IEEE/RSJ international conference on intelligent robots and systems, 1998. Proceedings. IEEE, vol 3, pp 1975–1980
Talwar SK, Xu S, Hawley ES, Weiss SA, Moxon KA, Chapin JK (2002) Behavioural neuroscience: rat navigation guided by remote control. Nature 417(6884):37–38
Taylor RC, Klein BA, Stein J, Ryan MJ (2008) Faux frogs: multimodal signalling and the value of robotics in animal behaviour. Anim Behav 76(3):1089–1097
Tinbergen N (1948) Social releasers and the experimental method required for their study. Wilson Bull 60:6–51
Tsang WM, Aldworth Z, Stone A, Permar A, Levine R, Hildebrand et al (2008) Insect flight control by neural stimulation of pupae-implanted flexible multisite electrodes. In: The proceeding of µ TAS, pp 1922–1924
Tye M (2016) Are insects sentient? Animal sentience: an interdisciplinary. J Anim Feel 1(9):5
Uematsu K, Todo T (1997) Identification of the midbrain locomotor nuclei and their descending pathways in the teleost carp, Cyprinus carpio. Brain Res 773(1):1–7
Vaughan R, Sumpter N, Henderson J, Frost A, Cameron S (2000) Experiments in automatic flock control. Robot Auton Syst 31(1):109–117
Wang H, Huai RT, Yang JQ, Su XC (2013) Review of research progress in biorobot. In: Advanced materials research. Trans Tech Publications, vol 655. Springer, pp 1061–1065
Wang Y, Lu M, Wu Z, Tian L, Xu K, Zheng X, Pan G (2015) Visual cue-guided rat cyborg for automatic navigation [research frontier]. IEEE Comput Intell Mag 10(2):42–52
Wang S, Shen L, Liu X, Liao H (2016) A wearable backpack chip for honeybee biorobot. In: Semiconductor technology international conference (CSTIC), 2016 China. IEEE, pp 1–3
Wang Y, Lu M, Wu Z, Zheng X, Pan G (2017) Visual cue-guided rat cyborg. In: Brain–computer interface research. Springer, Cham, pp 65–78
Wang H, Yang J, Lv C, Huai R, Li Y (2018) Intercollicular nucleus electric stimulation encoded “walk forward” commands in pigeons. Brill. https://doi.org/10.1163/15707563-17000053
Ward AJ, Sumpter DJ, Couzin ID, Hart PJ, Krause J (2008) Quorum decision-making facilitates information transfer in fish shoals. Proc Natl Acad Sci 105(19):6948–6953
Webb B (2000) What does robotics offer animal behaviour? Anim Behav 60(5):545–558
Wenbo W, Ce G, Jiurong S, Zhendong D (2009) Locomotion elicited by electrical stimulation in the midbrain of the lizard gekko gecko. Intelligent unmanned systems: theory and applications. Springer, Berlin, pp 145–153
Worm M, Landgraf T, Nguyen H, von der Emde G (2014) Electro-communicating dummy fish initiate group behaviour in the weakly electric fish Mormyrus rume. In: Duff A, Lepora NF, Mura A, Prescott TJ, Verschure PFMJ (eds) Biomimetic and biohybrid systems LNAI, vol 8608, pp 446–448
Worm M, Landgraf T, Prume J, Nguyen H, Kirschbaum F, von der Emde G (2018) Evidence for mutual allocation of social attention through interactive signaling in a mormyrid weakly electric fish. Proc Natl Acad Sci 24:245. https://doi.org/10.1073/pnas.1801283115
Wu Z, Pan G, Zheng N (2013) Cyborg intelligence. IEEE Intell Syst 28(5):31–33
Wu Z, Yang Y, Xia B, Zhang Z, Pan G (2014) Speech interaction with a rat. Chin Sci Bull 59(28):3579–3584
Wu Z, Zhou Y, Shi Z, Zhang C, Li G, Zheng X, Zheng N, Pan G (2016) Cyborg intelligence: recent progress and future directions. IEEE Intell Syst 31(6):44–50
Xu S, Talwar SK et al (2004) A multi-channel telemetry system for brain microstimulation in freely roaming animals. J Neurosci Methods 133(1–2):57–63
Xu K, Zhang J, Zhou H, Lee JCT, Zheng X (2016) A novel turning behaviour control method for rat-robot through the stimulation of ventral posteromedial thalamic nucleus. Behav Brain Res 298:150–157
Yang J, Huai R, Wang H, Lv C, Su X (2015) A robo-pigeon based on an innovative multi-mode telestimulation system. Biomed Mater Eng 26(s1):357–363
Yu Y, Pan G, Gong Y, Xu K, Zheng N, Hua W et al (2016a) Intelligence-augmented rat cyborgs in maze solving. PLoS ONE 11(2):e0147754
Yu Y, Wu Z, Xu K, Gong Y, Zheng N, Zheng X, Pan G (2016b) Automatic training of rat cyborgs for navigation. Comput Intell Neurosci. https://doi.org/10.1155/2016/6459251
Zahadat P, Hahshold S, Thenius R, Crailsheim K, Schmickl T (2015) From honeybees to robots and back: division of labour based on partitioning social inhibition. Bioinspir Biomim 10(6):066005
Zhang C, Cao F, Li Y, Sato H (2016) Fuzzy-controlled living insect legged actuator. Sens Actuators A Phys 242:182–194
Zheng N, Jin M, Hong H, Huang L, Gu Z, Li H (2017) Real-time and precise insect flight control system based on virtual reality. Electron Lett 53(6):387–389
Funding
This work was funded by the EU project subCULTron (submarine cultures perform long-term robotic exploration of unconventional environmental niches) number 640967. The funder had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jean-Marc Fellous.
Rights and permissions
About this article
Cite this article
Romano, D., Donati, E., Benelli, G. et al. A review on animal–robot interaction: from bio-hybrid organisms to mixed societies. Biol Cybern 113, 201–225 (2019). https://doi.org/10.1007/s00422-018-0787-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00422-018-0787-5