Journal of Bionic Engineering ›› 2020, Vol. 17 ›› Issue (1): 174-184.doi: 10.1007/s42235-020-0014-7

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Together We Stand – Analyzing Schooling Behavior in Naive Newborn Guppies through Biorobotic Predators

Donato Romano1,2,3*, Hadeel Elayan4, Giovanni Benelli5, Cesare Stefanini1,2,3   

  1. 1. The BioRobotics Institute, Sant’Anna School of Advanced Studies, Pontedera, Pisa 56025, Italy
    2. Healthcare Engineering Innovation Center (HEIC), Khalifa University, Abu Dhabi, PO Box 127788, United Arab Emirates
    3. Department of Excellence in Robotics & A.I., Sant’Anna School of Advanced Studies, Pisa 56127, Italy
    4. Department of Electrical and Computer Engineering, University of Toronto, ON M5S, Canada
    5. Department of Agriculture, Food and Environment, University of Pisa, Pisa 56124, Italy

  • 收稿日期:2018-10-09 修回日期:2019-10-31 接受日期:2019-12-04 出版日期:2020-01-10 发布日期:2020-01-21
  • 通讯作者: Donato Romano E-mail:donato.romano@santannapisa.it
  • 作者简介:Donato Romano1,2,3*, Hadeel Elayan4, Giovanni Benelli5, Cesare Stefanini1,2,3

Together We Stand – Analyzing Schooling Behavior in Naive Newborn Guppies through Biorobotic Predators

Donato Romano1,2,3*, Hadeel Elayan4, Giovanni Benelli5, Cesare Stefanini1,2,3   

  1. 1. The BioRobotics Institute, Sant’Anna School of Advanced Studies, Pontedera, Pisa 56025, Italy
    2. Healthcare Engineering Innovation Center (HEIC), Khalifa University, Abu Dhabi, PO Box 127788, United Arab Emirates
    3. Department of Excellence in Robotics & A.I., Sant’Anna School of Advanced Studies, Pisa 56127, Italy
    4. Department of Electrical and Computer Engineering, University of Toronto, ON M5S, Canada
    5. Department of Agriculture, Food and Environment, University of Pisa, Pisa 56124, Italy

  • Received:2018-10-09 Revised:2019-10-31 Accepted:2019-12-04 Online:2020-01-10 Published:2020-01-21
  • Contact: Donato Romano E-mail:donato.romano@santannapisa.it
  • About author:Donato Romano1,2,3*, Hadeel Elayan4, Giovanni Benelli5, Cesare Stefanini1,2,3

摘要: A major advantage of animal aggregations concerns cooperative antipredator strategies. Schooling behavior emerges earlier in many
fish species, especially in those cannibalizing their offspring. Experience is fundamental for developing schooling behavior. However, the
cognitive ability of naive newborn fish to aggregate remains unclear. Herein, Poecilia reticulata, was selected as model organism to
investigate how combinations of biomimetic robotic agents and adult conspecific olfactory cues affect collective responses in newborns.
The role of white and brown backgrounds in evoking aggregations was also assessed. Olfactory cues were sufficient for triggering aggregations
in P. reticulata newborns, although robotic agents had a higher influence on the group coalescence. The combination of robotic
agents and olfactory cues increased schooling behavior duration. Notably, schooling was longer in the escape compartment when robotic
agents were presented, except for the combination of the male-mimicking robotic fish plus adult guppy olfactory cues, with longer
schooling behavior in the exploring compartment. Regardless of the tested cues, newborn fish aggregated preferentially on the brown areas
of the arena. Overall, this research provides novel insights on the early collective cognitive ability of newborn fish, paving the way to the
use of biomimetic robots in behavioral ecology experiments, as substitutes for real predators.


关键词: animal-robot interaction technology, bio-hybrid intelligent systems, antipredator strategy, group behavior, Poecilia reticulata

Abstract: A major advantage of animal aggregations concerns cooperative antipredator strategies. Schooling behavior emerges earlier in many
fish species, especially in those cannibalizing their offspring. Experience is fundamental for developing schooling behavior. However, the
cognitive ability of naive newborn fish to aggregate remains unclear. Herein, Poecilia reticulata, was selected as model organism to
investigate how combinations of biomimetic robotic agents and adult conspecific olfactory cues affect collective responses in newborns.
The role of white and brown backgrounds in evoking aggregations was also assessed. Olfactory cues were sufficient for triggering aggregations
in P. reticulata newborns, although robotic agents had a higher influence on the group coalescence. The combination of robotic
agents and olfactory cues increased schooling behavior duration. Notably, schooling was longer in the escape compartment when robotic
agents were presented, except for the combination of the male-mimicking robotic fish plus adult guppy olfactory cues, with longer
schooling behavior in the exploring compartment. Regardless of the tested cues, newborn fish aggregated preferentially on the brown areas
of the arena. Overall, this research provides novel insights on the early collective cognitive ability of newborn fish, paving the way to the
use of biomimetic robots in behavioral ecology experiments, as substitutes for real predators.


Key words: animal-robot interaction technology, bio-hybrid intelligent systems, antipredator strategy, group behavior, Poecilia reticulata