Escape and surveillance asymmetries in locusts exposed to a Guinea fowl-mimicking robot predator

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Romano, Donato ^a   Benelli, Giovanni ^a,b   Stefanini, Cesare ^a,c  

^a SCUOLA SUPERIORE SANT ANNA   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c KHALIFA UNIVERSITY   (United Arab Emirates)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; COMPOUND EYE; COORDINATION; HEMISPHERIC DOMINANCE; HUMAN; JUMPING; LOCUSTA MIGRATORIA; NONHUMAN; NUMIDA MELEAGRIS; PREDATOR PREY INTERACTION; ROBOTICS; ANIMAL; CAELIFERA; ESCAPE BEHAVIOR; GALLIFORMES; LOCOMOTION; PHYSIOLOGY; PREDATION;

ANIMALS; ESCAPE REACTION; FUNCTIONAL LATERALITY; GALLIFORMES; GRASSHOPPERS; LOCOMOTION; PREDATORY BEHAVIOR; ROBOTICS;

EID: 85031019806     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-12941-z     Document Type: Article

References (90)

1. Bonsall, M. B. & Hassell, M. P. Predator-prey interactions. (Theoretical Ecology Principles and Applications, 3rd ed. Oxford University Press, Oxford, 46-61, 2007).
2. Millon, A. & Bretagnolle, V. Predator population dynamics under a cyclic prey regime: numerical responses, demographic parameters and growth rates. Oikos 117(10), 1500-1510 (2008).
3. Dessborn, L., Elmberg, J., Nummi, P., Pöysä, H. & Sjöberg, K. Hatching in dabbling ducks and emergence in chironomids: a case of predator-prey synchrony? Hydrobiologia 636(1), 319-329 (2009).
4. Lima, S. L. & Dill, L. M. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zoo. 68(4), 619-640 (1990).
5. Vallortigara, G., Rogers, L. J. & Bisazza, A. Possible evolutionary origins of cognitive brain lateralization. Brain Res. Rev. 30, 164-75 (1999).
6. Rogers, L. J. Lateralization in vertebrates: Its early evolution, general pattern and development. Adv. Stud. behav. 31, 107-161 (2002).
7. Lippolis, G., Bisazza, A., Rogers, L. J. & Vallortigara, G. Lateralization of predator avoidance responses in three species of toads. Laterality 7, 163-83 (2002).
8. Lippolis, G., Westerman, W., McAllan, B. M. & Rogers, L. J. Lateralization of escape responses in the striped-face dunnart, Sminthopsis macroura (Dasyuridae: Marsupialia). Laterality 10, 457-70 (2005).
9. Vallortigara, G. & Rogers, L. J. Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav. Brain Sci. 28(4), 575-588 (2005).
10. Robins, A. & Rogers, L. J. Lateralized visual and motor responses in the green tree frog, Litoria caerulea. Anim. Behav. 72(4), 843-852 (2006).
11. Bisazza, A., Rogers, L. J. & Vallortigara, G. The origins of cerebral asymmetry: a review of evidence of behavioural and brain lateralization in fishes, reptiles and amphibians. Neurosci. Biobehav. R. 22(3), 411-426 (1998).
12. Vallortigara, G. Comparative neuropsychology of the dual brain: a stroll through animals' left and right perceptual worlds. Brain Lang. 73, 189-219 (2000).
13. Vallortigara, G., Chiandetti, C. & Sovrano, V. A. Brain asymmetry (animal). Wiley. Interdiscip. Rev. Cogn. Sci. 2(2), 146-157 (2010).
14. Rogers, L. J., Vallortigara, G. & Andrew, R. J. Divided brains: the biology and behaviour of brain asymmetries. (Cambridge Univ. Press, 2013).
15. Frasnelli, E. Brain and behavioral lateralization in invertebrates. Front. Psychol. 4, 939 (2013).
16. Rogers, L. J., Zucca, P. & Vallortigara, G. Advantages of having a lateralized brain. Proc. R. Soc. Ser. B. 271(S6), S420-S422 (2004).
17. Frasnelli, E., Vallortigara, G. & Rogers, L. Left-right asymmetries of behaviour and nervous system in invertebrates. Neurosci. Biobehav. Rev. 36, 1273-1291 (2012).
18. Letzkus, P. et al. Lateralization of olfaction in the honeybee Apis mellifera. Curr. Biol. 16(14), 1471-1476 (2006).
19. Hunt, E. R. et al. Ants show a leftward turning bias when exploring unknown nest sites. Biol. Lett. 10(12), 20140945 (2014).
20. Kamimura, Y. Right-handed penises of the earwig Labidura riparia (Insecta, Dermaptera, Labiduridae): evolutionary relationships between structural and behavioral asymmetries. J. Morphol. 267, 1381-1389 (2006).
21. Benelli, G., Romano, D., Messing, R. H. & Canale, A. Population level lateralized aggressive and courtship displays make better fighters not lovers: evidence from a fly. Behav. Process. 115, 163-168 (2015).
22. Benelli, G., Romano, D., Messing, R. H. & Canale, A. First report of behavioural lateralisation in mosquitoes: right-biased kicking behaviour against males in females of the Asian tiger mosquito, Aedes albopictus. Parasitol. Res. 114, 1613-1617 (2015).
23. Benelli, G. et al. Lateralization of aggressive displays in a tephritid fly. Sci. Nat. Naturwiss. 102, 1, https://doi.org/10.1007/s00114-014-1251-6 (2015).
24. Benelli, G. et al. Asymmetry of mating behaviour affects copulation success in two stored product beetles. J. Pest. Sci.; https://doi.org/10.1007/s10340-016-0794-z (2016).
25. Benelli, G. et al. Multiple behavioural asymmetries impact male mating success in the khapra beetle, Trogoderma granarium. J. Pest. Sci. 1-9 (2017).
26. Romano, D., Canale, A. & Benelli, G. Do right-biased boxers do it better? Population-level asymmetry of aggressive displays enhances fighting success in blowflies. Behav. process. 113, 159-162 (2015).
27. Romano, D. et al. Lateralized courtship in a parasitic wasp. Laterality 21, 243-254 (2016).
28. Romano, D. et al. Impact of geographical origin and rearing medium on mating success and lateralization in the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae). J. Stored Prod. Res. 69, 106-112 (2016).
29. Eterovick, P. C., Figueira, J. E. C. & Vasconcellos-Neto, J. Cryptic coloration and choice of escape microhabitats by grasshoppers (Orthoptera: Acrididae). Biol. J. Linn. Soc. 61(4), 485-499 (1997).
30. Ruxton, G. D., Sherratt, T. N. & Speed, M. P. Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. (Oxford Univ. Press, 2004).
31. Ruxton, G. Behavioural ecology: Grasshoppers don't play possum. Nature 440(7086), 880-880 (2006).
32. Santer, R. D., Yamawaki, Y., Rind, F. C. & Simmons, P. J. Motor activity and trajectory control during escape jumping in the locust Locusta migratoria. J. Comp. Physiol. A. 191(10), 965-975 (2005).
33. Fry, C. H. & Fry, K. Kingfishers, Bee-Eaters and Rollers. (London, A&C Black, 1992).
34. Wheatstone, C. Contributions to the physiology of vision. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 142, 1-18 (1852).
35. Santer, R. D., Rind, F. C., Stafford, R. & Simmons, P. J. Role of an identified looming-sensitive neuron in triggering a flying locust's escape. J. Neurophysiol. 95(6), 3391-3400 (2006).
36. Santer, R. D., Yamawaki, Y., Rind, F. C. & Simmons, P. J. Preparing for escape: an examination of the role of the DCMD neuron in locust escape jumps. J. Comp. Physiol. A. 194(1), 69-77 (2008).
37. Bell, A. T. & Niven, J. E. Strength of forelimb lateralization predicts motor errors in an insect. Biol. Lett. 12(9), 20160547 (2016).
38. Kok, O. B. & Louw, S. Avian and mammalian predators of Orthoptera in semi-arid regions of South Africa. S. Afr. J. Wildl. Res. 30(3), 122-128 (2000).
39. Moral, J. D., Mejías, A., Jiménez, J., Pérez-Rojas, F. & Senero, M. Locust (Dociostaurus maroccanus Thunb.) pests control with "pintada" bird (Numida meleagris L.), an alternative or additional ecological method to insecticides use. Acta Científica y Tecnológica (España) (2006).
40. Ndang'ang'a, P. K., Njoroge, J. B. & Vickery, J. Quantifying the contribution of birds to the control of arthropod pests on kale, Brassica oleracea acephala, a key crop in East African highland farmland. Int. J. Pest. Manage. 59(3), 211-216 (2013).
41. Todd, D. Mobile robots-the lessons from nature. Robots and Biological Systems: Towards a New Bionics 193-206 (1993).
42. Kopman, V. & Porfiri, M. A Miniature and Low-Cost Robotic Fish for Ethorobotics Research and Engineering Education. I-Bioinspired Design (InASME 2011 Dynamic Systems and Control Conference and Bath/ASME Symposium on Fluid Power and Motion Control) 209-216 (American Society of Mechanical Engineers, 2011).
43. Partan, S. R. Animal robots. Encyclopedia of Animal Behavior (Ed. by Bekoff, M.) 952-955 (Westport, Greenwood, 2004).
44. Krause, J., Winfield, A. F. & Deneubourg, J. L. Interactive robots in experimental biology. Trends Ecol. Evol. 26(7), 369-375 (2011).
45. Mondada, F. et al. A general methodology for the control of mixed natural-artificial societies (No. EPFL-CHAPTER-154840) 547-586 (Pan Stanford Publishing, 2013).
46. Tinbergen, N. An objectivistic study of the innate behaviour of animals. Biblioth. Biotheor. 1, 39-98 (1942).
47. Tinbergen, N. The study of instinct. (Clarendon Press) 228 (Oxford, 1951).
48. Rowland, W. J. Studying visual cues in fish behavior: a review of ethological techniques. Environ. Biol. Fish. 56(3), 285-305 (1999).
49. Woo, K. L. & Rieucau, G. From dummies to animations: a review of computer-animated stimuli used in animal behavior studies. Behav. Ecol. Sociobiol. 65(9), 1671 (2011).
50. Webb, B. Using robots to model animals: a cricket test. Robot. Auton. Syst. 16(2-4), 117-134 (1995).
51. Wood, R. J. The first takeoff of a biologically inspired at-scale robotic insect. IEEE T. Robotic. 24(2), 341-347 (2008).
52. Ijspeert, A. J., Crespi, A. & Cabelguen, J. M. Simulation and robotics studies of salamander locomotion. Neuroinformatics 3(3), 171-195 (2005).
53. Stefanini, C. et al. A novel autonomous, bioinspired swimming robot developed by neuroscientists and bioengineers. Bioinspir. Biomim. 7(2), 025001 (2012).
54. Bonsignori, G. et al. The green leafhopper, Cicadella viridis (Hemiptera, Auchenorrhyncha, Cicadellidae), jumps with near-constant acceleration. J. Exp. Biol. 216(7), 1270-1279 (2013).
55. Laschi, C. et al. 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, BioRob 2006) 631-636 (IEEE, 2006).
56. Miklósi, Á. & Gerencsér, L. Potential application of autonomous and semi-autonomous robots in the study of animal behaviour. In Cognitive Infocommunications (CogInfoCom), 2012 IEEE 3rd International Conference on (pp. 759-762). IEEE (2012).
57. Mitri, S., Wischmann, S., Floreano, D. & Keller, L. Using robots to understand social behaviour. Biol. Rev. 88(1), 31-39 (2013).
58. Cianca, V., Bartolini, T., Porfiri, M. & Macri, S. A robotics-based behavioral paradigm to measure anxiety-related responses in zebrafish. PLoS ONE 8(7), e69661 (2013).
59. Ladu, F. et al. Live predators, robots, and computer-animated images elicit differential avoidance responses in zebrafish. Zebrafish 12(3), 205-214 (2015).
60. Romano, D. et al. 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 (2017).
61. Michelsen, A., Andersen, B. B., Kirchner, W. H. & Lindauer, M. Honeybees can be recruited by a mechanical model of a dancing bee. Naturwissenschaften. 76(6), 277-280 (1989).
62. Halloy, J. et al. Social integration of robots into groups of cockroaches to control self-organized choices. Science 318(5853), 1155-1158 (2007).
63. Kawabata, K., Aonuma, H., Takahashi, S., Hosoda, K. & Xue, J. Image-based pose estimation for analyzing cricket-robot interaction behavior. J. Signal. Process. 18(3), 135-141 (2014).
64. Landgraf, T., Rojas, R., Nguyen, H., Kriegel, F. & Stettin, K. Analysis of the waggle dance motion of honeybees for the design of a biomimetic honeybee robot. PloS ONE 6(8), e21354 (2011).
65. Landgraf, T., Oertel, M., Kirbach, A., Menzel, R. & Rojas, R. Imitation of the honeybee dance communication system by means of a biomimetic robot. (In Conference on Biomimetic and Biohybrid Systems) pp. 132-143 (Springer Berlin Heidelberg, 2012).
66. h International Conference on Self-Adaptive and Self-Organizing Systems) 259-260 (IEEE, 2013).
67. Ellis, P. E. Social Aggregation and Gregarious Behaviour in Hoppers of Locusta Migratoria Migratorioides (R. & F.) 1. Behaviour 5(1), 225-259 (1953).
68. Ghirlanda, S., Frasnelli, E. & Vallortigara, G. Intraspecific competition and coordination in the evolution of lateralization. Philos. T. Roy. Soc. B. 364(1519), 861-866 (2009).
69. Edwards, J. S. Postembryonic development and regeneration of the insect nervous system. Adv. Insect. Physiol. 6, 97-137 (1970).
70. Weeks, J. C. & Levine, R. B. Postembryonic neuronal plasticity and its hormonal control during insect metamorphosis. Annu. Rev. Neurosci. 13(1), 183-194 (1990).
71. Altman, J. S., Anselment, E. & Kutsch, W. Postembryonic development of an insect sensory system: ingrowth of axons from hindwing sense organs in Locusta migratoria. Philos. T. Roy. Soc. B. 202(1149), 497-516 (1978).
72. Truman, J. W. & Riddiford, L. M. The origins of insect metamorphosis. Nature 401(6752), 447-452 (1999).
73. Bazazi, S. et al. Collective motion and cannibalism in locust migratory bands. Curr. Biol. 18(10), 735-739 (2008).
74. Horridge, G. A. Learning of leg position by headless insects. Nature 193(4816), 697-698 (1962).
75. Rowell, C. F. The structure and function of the prothoracic spine of the desert locust, Schistocerca gregaria Forskål. J. Exp. Biol. 38(2), 457-469 (1961).
76. Rowell, C. F. Central control of an insect segmental reflex: I. Inhibition by different parts of the central nervous system. J. Exp. Biol. 41(3), 559-572 (1964).
77. Letzkus, P., Boeddeker, N., Wood, J. T., Zhang, S. W. & Srinivasan, M. V. Lateralization of visual learning in the honeybee. Biol. Lett. 4(1), 16-19 (2008).
78. Dempster, J. P. The population dynamics of grasshoppers and locusts. Biol. Rev. 38(4), 490-529 (1963).
79. Bell, A. T. & Niven, J. E. Individual-level, context-dependent handedness in the desert locust. Curr. Biol. 24(10), 382-383 (2014).
80. Li, F., Liu, W., Stefanini, C., Fu, X. & Dario, P. A novel bioinspired PVDF micro/nano hair receptor for a robot sensing system. Sensors 10(1), 994-1011 (2010).
81. ASAB/ABS. Guidelines for the treatment of animals in behavioural research and teaching. Anim. Behav. 99, 1-9 (2004).
82. European Commission. Commission recommendations of 18 June 2007 on guidelines for the accommodation and care of animals used for experimental and other scientific purposes. Annex II to European Council Directive 86/609. See 2007/526/EC. Retrieved from http://eurex.europa.eu/LexUriServ/LexUriServ.do?uri1/4OJ:L. 2007.197:0001:0089:EN:PDF (2007).
83. Benelli, G., Bonsignori, G., Stefanini, C., Raspi, A. & Canale, A. The production of female sex pheromone in Bactrocera oleae (Rossi) young males does not influence their mating chances. Entomol. Sci. 16(1), 47-53 (2013).
84. Romano, D. et al. Behavioral asymmetries in the mealybug parasitoid Anagyrus sp. near pseudococci: does lateralized antennal tapping predict male mating success? J. Pest. Sci. 1-9 (2017).
85. Kral, K. & Poteser, M. Motion parallax as a source of distance information in locusts and mantids. J. Insect Behav. 10(1), 145-163 (1997).
86. Horridge, G. A. Insects which turn and look. Endeavour 1(1), 7-17 (1977).
87. Binder, J. R. et al. Determination of language dominance using functional MRI A comparison with the Wada test. Neurology 46(4), 978-984 (1996).
88. Bisazza, A., Facchin, L. & Vallortigara, G. Heritability of lateralization in fish: concordance of right-left asymmetry between parents and offspring. Neuropsychologia 38(7), 907-912 (2000).
89. Seghier, M. L. Laterality index in functional MRI: methodological issues. Magn. Reson. Imaging. 26(5), 594-601 (2008).
90. Benbadis, S. R. et al. Is speech arrest during Wada testing a valid method for determining hemispheric representation of language? Brain Lang. 65(3), 441-446 (1998).