Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds
Animals living in and interacting with natural environments must monitor and respond to changing conditions and unpredictable situations. Using information from multiple sensory systems allows them to modify their behavior in response to their dynamic environment but also creates the challenge of integrating different, and potentially contradictory, sources of information for behavior control. Understanding how multiple information streams are integrated to produce flexible and reliable behavior is key to understanding how behavior is controlled in natural settings. Natural settings are rarely still, which challenges animals that require precise body position control, like hummingbirds, which hover while feeding from flowers. Tactile feedback, available only once the hummingbird is docked at the flower, could provide additional information to help maintain its position at the flower. To investigate the role of tactile information for hovering control during feeding, we first asked whether hummingbirds physically interact with a feeder once docked. We quantified physical interactions between docked hummingbirds and a feeder placed in front of a stationary background pattern. Force sensors on the feeder measured a complex time course of loading that reflects the wingbeat frequency and bill movement of feeding hummingbirds, and suggests that they sometimes push against the feeder with their bill. Next, we asked whether the measured tactile interactions were used by feeding hummingbirds to maintain position relative to the feeder. We created two experimental scenarios—one in which the feeder was stationary and the visual background moved and the other where the feeder moved laterally in front of a white background. When the visual background pattern moved, docked hummingbirds pushed significantly harder in the direction of horizontal visual motion. When the feeder moved, and the background was stationary, hummingbirds generated aerodynamic force in the opposite direction of the feeder motion. These results suggest that docked hummingbirds are using visual information about the environment to maintain body position and orientation, and not actively tracking the motion of the feeder. The absence of flower tracking behavior in hummingbirds contrasts with the behavior of hawkmoths, and provides evidence that they rely primarily on the visual background rather than flower-based cues while feeding.
© 2017 Goller, Segre, Middleton, Dickinson and Altshuler. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Received: 29 June 2017; Accepted: 25 October 2017; Published: 14 November 2017. Ethics Statement: This study was carried out in accordance with the recommendations of US federal regulations and the Guide for the Care and Use of Laboratory Animals, as well as the Canadian Council on Animal Care. The protocol was approved by the Institutional Animal Care and Use Committee of the California Institute of Technology and the Animal Care and Use Committee at the University of British Columbia. Author Contributions: BG, MD, and DA conceived and designed the experiments. BG and DA collected the data. BG, PS, KM, and DA analyzed the data and wrote the manuscript. All authors edited the manuscript. Funding: This study was supported by grants from the Natural Science and Engineering Research Council of Canada (402667, RGPIN-2016-05381) and the Human Frontier Science Program (RGP0003/2013). Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Acknowledgments: We thank Bobby Chi, Lev Darkhovsky, Amy Lin, Annie Liu, and Jonathon Scott for assistance with data collection or digitization of wingbeat kinematics. We also thank Joseph Bahlman, Will Dickson, Phil Matthews, Ken Savage, and Bob Shadwick for providing technical support for the experiments. Finally, we would like to acknowledge the two reviewers for providing comments that greatly improved the manuscript.
Published - fnins-11-00622.pdf
Supplemental Material - video_1.mp4
Supplemental Material - video_2.mp4