Research ArticleANIMAL ROBOTS

Robots mediating interactions between animals for interspecies collective behaviors

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Science Robotics  20 Mar 2019:
Vol. 4, Issue 28, eaau7897
DOI: 10.1126/scirobotics.aau7897
  • Fig. 1 Automated setup for interspecies experiments composed of two animal species (zebrafish and honeybees) and two artificial devices (fish- and bee-robots).

    The two setups are composed of a metallic frame, with a camera (A1 and A2) to capture the arenas in high definition. The fish arena (B1) includes a tank filled with water and a circular corridor (G). This space constrains the zebrafish and lure, presenting a binary choice: The mixed group can move either CW or CCW (G and I). Underneath the tank (C1), a wheeled mobile robot moved, which also moved its lure via magnetic coupling. The honeybees were contained within a silicon oil–coated Plexiglas arena (B2) with two bee-robots, forming a binary choice: The honeybees decided to aggregate around one of these bee-robots (H). The “head” of each immobile robot incorporated six IR sensors (J). The main bodies were mounted below the arena floor (C2) and included a Peltier element to modulate the local temperature inside the arena. The two setups were interfaced (D1 and D2) with computers (E1 and E2) on which programs controlled the robots in a closed loop. The fish setup (in Lausanne, Switzerland) was connected virtually (F) to the bee setup (in Graz, Austria)

  • Fig. 2 The four conditions implemented to test connectivity between bee and fish experimental setups.

    (A) Control condition, where the robots interacted with the animals in a closed loop but did not exchange information between the setups. (B) Condition B → F, where the fish-robot behavior was modulated according to what was sensed by the bee-robot, which interacted in a closed loop with the honeybees in a self-contained decision-making dynamics. (C) Condition B ← F, where the bee-robot behavior was modulated according to what was sensed by the fish-robot, which was interacting in a closed loop with the zebrafish in a self-contained decision-making dynamics. (D) Condition B ⇌ F, where the bee-robot behavior was modulated according to what was sensed by the fish-robot and the fish-robot behavior was modulated according to what was sensed by the bee-robots. The setup established a long-distance closed-loop interaction between the two biohybrid systems, which could share their collective decision-making to allow the emergence of a global consensus.

  • Fig. 3 Coordinated collective decision-making.

    (A) Time series of collective decisions in each species (bees and fish) for selected runs of each condition. The fish choose their rotation direction (% CW), and the bees choose their resting place (% right side). (B) Collective decision difference coefficient QBF for all runs of each condition, reflecting closely correlated behavior across the two animal species. With bidirectional link, B ⇌ F, the low QBF values indicate a highly coordinated system. The four distributions differ statistically (Kruskal-Wallis, P < 0.05), and a post hoc analysis using Tukey’s honest significant difference criterion shows that the mean ranks of the distribution of conditions B → F, B ← F, and B ⇌ F significantly differ from condition BF, whereas conditions B → F, B ← F, and B ⇌ F do not have significantly different distributions.

  • Fig. 4 Measurements of transfer entropy (TE), a directional information-theoretic measure that can indicate dependencies between actors in a complex system.

    We measured (A) TEFB, from fish to bees, and (B) TEBF, from bees to fish. When the two biohybrid systems were connected, we found substantial TE in at least one direction. The solid markers indicate statistical significance (Mann-Whitney U test with Bonferroni correction, P < 0.05). Specifically, in B → F, we have only information flowing from bee-robots to fish-robots, and this is reflected in high TEBF only. Conversely, in B ← F, we only have high TEFB. The condition B ⇌ F shows significant bidirectional information exchange between the animals.

  • Table 1 The messages exchanged in the interspecies communication protocol.

    The 〈 and 〉 symbols imply a variable value in the protocol.

    DirectionTargetSender nameData format
    Fish→beesBee-robot IDFish-robotfish-〈direction〉
    Bees→fishFish-robotBee-robot IDbee-〈density〉

Supplementary Materials

  • robotics.sciencemag.org/cgi/content/full/4/28/eaau7897/DC1

    Text S1. Robot controllers

    Text S2. Correlation between robotic agents and animals

    Text S3. Optical flow as a measure of motion in the bee arena

    Text S4. Application of transfer entropy analysis

    Text S5. Modulation of animal collective behavior

    Text S6. Links to the software

    Fig. S1. Correlation between the animals and the robots in each biohybrid system.

    Fig. S2. Time series of the moments of the optical flow distribution, extracted from films of the bee arena.

    Fig. S3. Statistical comparison of the transfer entropy distributions, using a Mann-Whitney U test.

    Table S1. Parameters of interaction network.

    Movie S1. Example of an experiment of condition B → F.

    Movie S2. Example of an experiment of condition B ← F.

    Movie S3. Example of an experiment of condition B ⇌ F.

    References (5256)

  • Supplementary Materials

    The PDF file includes:

    • Text S1. Robot controllers
    • Text S2. Correlation between robotic agents and animals
    • Text S3. Optical flow as a measure of motion in the bee arena
    • Text S4. Application of transfer entropy analysis
    • Text S5. Modulation of animal collective behavior
    • Text S6. Links to the software
    • Fig. S1. Correlation between the animals and the robots in each biohybrid system.
    • Fig. S2. Time series of the moments of the optical flow distribution, extracted from films of the bee arena.
    • Fig. S3. Statistical comparison of the transfer entropy distributions, using a Mann-Whitney U test.
    • Table S1. Parameters of interaction network.
    • References (5256)

    Download PDF

    Other Supplementary Material for this manuscript includes the following:

    • Movie S1 (.mp4 format). Example of an experiment of condition B → F.
    • Movie S2 (.mp4 format). Example of an experiment of condition B ← F.
    • Movie S3 (.mp4 format). Example of an experiment of condition B ⇌ F.

    Files in this Data Supplement:

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