Summary PhD thesis Pulkit Goyal:How bees land - Visual guidance and sensorimotor control of landing maneuvers in bees

Landing is arguably one of the most important behaviors that flying animals regularly perform. It involves a precise control of approach speed as an animal draws closer to the landing surface. Poor control can result in high-impact collisions with the surface which can be harmful for animals. Despite its importance in flight, how animals approach a surface for landing is not yet fully understood. In this thesis, I contribute to answering this question by examining the landing approaches of bumblebees and honeybees. Bees, including bumblebees and honeybees, perform 100 to 1000 landings in a single hour of foraging. They perform these landings relentlessly to gather nectar and pollen from flowers which are essential for their survival and reproduction. In this thesis, I use novel analyses methods to investigate how these bees land.

Many flying animals use visual cues during landing. In chapter 2, we present how bumblebees use visual expansion cues to advance towards the landing surface. For this purpose, we first designed an indoor experimental apparatus to automatically record the landing maneuvers of foraging bumblebees. We then analyzed 4,672 landing maneuvers using a novel method. This method analyses the individual maneuvers and is more comprehensive than the analysis method of averaging multiple maneuvers used in literature. Using this novel method, we found the visual guidance strategy of landing bumblebees. Our results show that the landing bumblebees exhibit a series of deceleration bouts during which they keep the relative rate of optical expansion approximately constant. This constant is referred to as a set-point and from one bout to the next, bumblebees tend to shift to a higher set-point. This newly-found guidance strategy results in the approach dynamics that is strikingly similar to that of pigeons and hummingbirds. In addition, we also found how bumblebees adjust this visual guidance strategy to travel faster when landing directly after a take-off than from a free-flight condition. Moreover, we also elucidated how bumblebees adjust this guidance strategy in the presence of different strength of optic expansion cues available from the landing surface (checkerboard versus spoke patterns) and different light intensities ranging from twilight to sunrise. This guidance strategy helps to explain how these important pollinators rapidly visit flowers and forage in challenging environmental conditions.

In addition to the deceleration phases, we found that landing bumblebees also occasionally exhibit low approach velocity phases (V < 0.05 m s^-1) while transitioning from one set-point to another. These low approach velocity phases are similar to the hovering phases identified in literature, and result in bumblebees hovering or sometimes even flying away from the surface for a short while. In chapter 2, we also proposed that these low approach velocity phases are likely the instabilities arising out of a control system that uses optical expansion rate as a control variable.

For achieving a goal such as evading a threat or reaching a set-point, animals use their sensorimotor control system to continuously parse the sensory information and change the wingbeat and body kinematics to produce the required forces and torques. In chapter 3, we focused on the sensorimotor control system that landing bumblebees use to execute their visual guidance strategy. We used the natural stepwise excitation that landing bumblebees offer to analyze how their different subsystems (sensory system, controller and motor system) function together to reach the set-points of optical expansion rate. Our results showed that their closed-loop sensorimotor control system regulates the relative rate of expansion during landing. The track segments before and during a set-point are the transient and steady-state responses of such a control system. Bumblebees use the transient response to mostly accelerate and steady-state response to always decelerate during their landing approach. We also identified how the transient response varies among the tested environmental conditions (light intensity and the strength of optic expansion cues) and starting conditions (landings from a free-flight or after a take-off). Based on these results, we propose a sensorimotor control system of landing bumblebees that facilitates a rapid and robust execution of their visual guidance strategy.

Bumblebees regularly experience winds during foraging. The winds in nature can be characterized as mean winds and fluctuations around them. In chapter 4, we investigated how the mean winds affect the visual guidance strategy, the sensorimotor control system and the landing performance of foraging bumblebees. In particular, we used six steady sidewinds ranging from 0 – 3.41m s^-1 that foraging bumblebees often encounter. We found that the visual guidance strategy and the sensorimotor control response of bumblebees in these wind conditions is similar to the still-air response, but bumblebees exhibit some important adaptations in winds. Compared to the still-air situation, bumblebees more often exhibit low approach velocity phases in higher wind speeds. This can lead to an increase in the travel time and hence, can adversely affect their foraging efficiency. But, bumblebees also exhibit faster transient responses and higher set-points with increasing wind speed which enable them to travel faster. This in turn allows bumblebees to compensate for the increase in travel time that would otherwise occur due to more low approach-velocity phases in higher winds. In addition to revealing the adverse effects of winds and the compensation mechanism of bumblebees during landing, we also use the natural excitation of the sensorimotor control system that bumblebees offer during landing to propose how they integrate information from the airspeed measuring mechanosensors with their visual feedback loop.

In chapter 5, we revise the visual guidance strategy of landing honeybees previously proposed in literature. In literature, honeybees are shown to linearly decrease their approach velocity with the reducing distance by analyzing the average of multiple landing maneuvers. Based on this result, it has been suggested that they land by holding the relative rate of optical expansion constant throughout their approach. We use the novel analysis technique developed in chapter 2 to show that the individual honeybees do not follow such a strategy. They instead stepwise modulate their set-point of optical expansion rate during landing. Moreover, we extend the analysis to find the mechanism that allows honeybees to converge to a stereotypic landing maneuver closer to the landing surface, for a large range of initial flight speeds and visual landing platform patterns.

Finally, in chapter 6, I synthesize the results of this thesis and place them in a broader context of flight control in bees specifically, and other flying animals in general. For this, I first compare the landing strategies of bumblebees and honeybees found in this thesis and elucidate the likely causes of the differences between their strategies. Then, I discuss how birds might perform control during landing. Additionally, I also discuss how the knowledge obtained in this thesis can be used for bioinspired applications. Finally, I present an outlook on the future research in the area of landing dynamics of insects and birds.

Considering all results together, in this thesis, we developed and used a novel analysis to demonstrate that bumblebees and honeybees have evolved a sophisticated flight control strategy to execute rapid landings. Moreover, we have shown that they have evolved ways to adjust this modular guidance strategy to deal with the challenges offered by the environment.