TY - JOUR
T1 - Automated monitoring of honey bees with barcodes and artificial intelligence reveals two distinct social networks from a single affiliative behavior
AU - Gernat, Tim
AU - Jagla, Tobias
AU - Jones, Beryl M.
AU - Middendorf, Martin
AU - Robinson, Gene E.
N1 - Funding Information:
We thank the University of Illinois School of Life Sciences Machine Shop for constructing bee tracking equipment; Reliance Label Solutions for printing bCodes; and the Carl R. Woese Institute for Genomic Biology Computer Network Resource Group for computational support. We are grateful to J. Peng for providing computational resources. We thank J. Cullum, S. Bransley, and A. Ray for manual image annotation; T. L. Harrison and A. L. Sankey for bee management; and A. R. Hamilton, A. Ray, S. Bransley, J. Cullum, K. Wilk, J. Falk, A. Zhang, L. Block, and V. Bagchi for assistance with field work. We also thank members of the M.M. and G.E.R. laboratories for discussions; and members of the M.M. and G.E.R. laboratories, and Jan Aerts for comments that improved the manuscript. This material is based on work supported by the National Academies Keck Futures Initiative Grant NAKFI CB4 (to T.G.), a Christopher Family Foundation Grant (to G.E.R.), National Institutes of Health Grant R01GM117467 (to G.E.R. and N. Goldenfeld), and Defense Advanced Research Projects Agency Gant HR0011-16-2-0019 (to G.E.R. and H. Zhao).
Funding Information:
We thank the University of Illinois School of Life Sciences Machine Shop for constructing bee tracking equipment; Reliance Label Solutions for printing bCodes; and the Carl R. Woese Institute for Genomic Biology Computer Network Resource Group for computational support. We are grateful to J. Peng for providing computational resources. We thank J. Cullum, S. Bransley, and A. Ray for manual image annotation; T. L. Harrison and A. L. Sankey for bee management; and A. R. Hamilton, A. Ray, S. Bransley, J. Cullum, K. Wilk, J. Falk, A. Zhang, L. Block, and V. Bagchi for assistance with field work. We also thank members of the M.M. and G.E.R. laboratories for discussions; and members of the M.M. and G.E.R. laboratories, and Jan Aerts for comments that improved the manuscript. This material is based on work supported by the National Academies Keck Futures Initiative Grant NAKFI CB4 (to T.G.), a Christopher Family Foundation Grant (to G.E.R.), National Institutes of Health Grant R01GM117467 (to G.E.R. and N. Goldenfeld), and Defense Advanced Research Projects Agency Gant HR0011-16-2-0019 (to G.E.R. and H. Zhao).
Publisher Copyright:
© 2023, This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
PY - 2023/12
Y1 - 2023/12
N2 - Barcode-based tracking of individuals is revolutionizing animal behavior studies, but further progress hinges on whether in addition to determining an individual’s location, specific behaviors can be identified and monitored. We achieve this goal using information from the barcodes to identify tightly bounded image regions that potentially show the behavior of interest. These image regions are then analyzed with convolutional neural networks to verify that the behavior occurred. When applied to a challenging test case, detecting social liquid transfer (trophallaxis) in the honey bee hive, this approach yielded a 67% higher sensitivity and an 11% lower error rate than the best detector for honey bee trophallaxis so far. We were furthermore able to automatically detect whether a bee donates or receives liquid, which previously required manual observations. By applying our trophallaxis detector to recordings from three honey bee colonies and performing simulations, we discovered that liquid exchanges among bees generate two distinct social networks with different transmission capabilities. Finally, we demonstrate that our approach generalizes to detecting other specific behaviors. We envision that its broad application will enable automatic, high-resolution behavioral studies that address a broad range of previously intractable questions in evolutionary biology, ethology, neuroscience, and molecular biology.
AB - Barcode-based tracking of individuals is revolutionizing animal behavior studies, but further progress hinges on whether in addition to determining an individual’s location, specific behaviors can be identified and monitored. We achieve this goal using information from the barcodes to identify tightly bounded image regions that potentially show the behavior of interest. These image regions are then analyzed with convolutional neural networks to verify that the behavior occurred. When applied to a challenging test case, detecting social liquid transfer (trophallaxis) in the honey bee hive, this approach yielded a 67% higher sensitivity and an 11% lower error rate than the best detector for honey bee trophallaxis so far. We were furthermore able to automatically detect whether a bee donates or receives liquid, which previously required manual observations. By applying our trophallaxis detector to recordings from three honey bee colonies and performing simulations, we discovered that liquid exchanges among bees generate two distinct social networks with different transmission capabilities. Finally, we demonstrate that our approach generalizes to detecting other specific behaviors. We envision that its broad application will enable automatic, high-resolution behavioral studies that address a broad range of previously intractable questions in evolutionary biology, ethology, neuroscience, and molecular biology.
UR - http://www.scopus.com/inward/record.url?scp=85146942151&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85146942151&partnerID=8YFLogxK
U2 - 10.1038/s41598-022-26825-4
DO - 10.1038/s41598-022-26825-4
M3 - Article
C2 - 36707534
AN - SCOPUS:85146942151
SN - 2045-2322
VL - 13
JO - Scientific reports
JF - Scientific reports
IS - 1
M1 - 1541
ER -