Abstract

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.

Highlights

  • Living in complex and dynamic environments requires animals to integrate—or fuse—information from multiple sensory systems to respond to changing conditions with flexible and effective behaviors

  • We measured how wingbeat kinematics differ between stationary feeding and lateral tracking flight, and surprisingly our results suggest that hummingbirds do not track the feeder, unlike hawkmoths

  • The California-caught hummingbirds were used for kinematic experiments and because they were larger than the birds in British Columbia, we report force magnitudes as a fraction of body weight using the greater body mass of 4.68 g in this experiment

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Summary

Introduction

Living in complex and dynamic environments requires animals to integrate—or fuse—information from multiple sensory systems to respond to changing conditions with flexible and effective behaviors. In destabilizing visual conditions, posture stability is improved by finger contact with a nearby stationary object (Holden et al, 1994; Jeka and Lackner, 1994; Jeka et al, 2000; Oie et al, 2002). It is less clear what role tactile information serves for body position control in non-human animals, especially during flight, when there are no ground reaction or buoyancy forces to assist with the estimation of body orientation. Tactile information may be a seldom used but highly salient signal for flight control, indicating contact with an external feature and resulting in strong behavioral responses to physical contact

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