Goller Benjamin, Segre Paolo S, Middleton Kevin M, Dickinson Michael H, Altshuler Douglas L
Department of Zoology, University of British Columbia, Vancouver, BC, Canada.
Department of Pathology and Anatomical Sciences, University of Missouri, Columbia, MO, United States.
Front Neurosci. 2017 Nov 14;11:622. doi: 10.3389/fnins.2017.00622. eCollection 2017.
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.
生活在自然环境中并与之相互作用的动物必须监测并应对不断变化的条件和不可预测的情况。利用来自多个感官系统的信息使它们能够根据动态环境改变行为,但也带来了整合不同且可能相互矛盾的信息源以进行行为控制的挑战。理解多个信息流如何整合以产生灵活可靠的行为是理解自然环境中行为如何被控制的关键。自然环境很少静止不动,这对需要精确控制身体位置的动物构成挑战,比如蜂鸟,它们在从花朵取食时会悬停。只有当蜂鸟停靠在花朵上时才会有的触觉反馈,可能会提供额外信息以帮助其在花朵处保持位置。为了研究触觉信息在取食时悬停控制中的作用,我们首先询问蜂鸟停靠后是否与喂食器有物理交互。我们量化了停靠的蜂鸟与放置在静止背景图案前的喂食器之间的物理交互。喂食器上的力传感器测量了一个复杂的加载时间过程,该过程反映了取食蜂鸟的翅膀拍动频率和喙的运动,并表明它们有时会用喙推挤喂食器。接下来,我们询问取食的蜂鸟是否利用测量到的触觉交互来维持相对于喂食器的位置。我们创建了两个实验场景——一个是喂食器静止而视觉背景移动,另一个是喂食器在白色背景前横向移动。当视觉背景图案移动时,停靠的蜂鸟在水平视觉运动方向上推得更用力。当喂食器移动而背景静止时,蜂鸟在与喂食器运动相反的方向上产生气动力。这些结果表明,停靠的蜂鸟利用关于环境的视觉信息来维持身体位置和方向,而不是主动跟踪喂食器的运动。蜂鸟缺乏花朵跟踪行为与天蛾的行为形成对比,并提供了证据表明它们在取食时主要依赖视觉背景而非基于花朵的线索。