Directional cue integration at different solar elevations - from behaviour to neurons

Abstract

To escape competition for food, South African dung beetles roll balls away from the dung pile of origin along straight-line paths. To keep their desired courses, the beetles rely on flexible integration of external orientation cues. This supports robust orientation even under challenging daytime conditions. Here, I studied the orientation precision driven by this flexible cue integration in the dung beetle’s natural habitat at different times of the day. My results confirmed previously established models for cue integration with natural cues. To establish a dynamic integration of compass cues, the dung beetle brain needs to be equipped with neurons that integrate directional information from several directional cues and flexibly set the relative weighting of each of the cues. While previous studies on dung beetles have identified neurons encoding the sun’s position, the integration of wind information in the compass network of the brain remains unclear. To understand how the directional information from wind and the azimuthal position of the sun is integrated, I performed extracellular tetrode recordings from the beetle’s internal compass system while presenting the animal with a wind stimulus and an artificial sun stimulus. I found that single neurons in the brain of dung beetles respond to both the sun and wind stimulus. Thus, neurons in the dung beetle brain are suitable to combine wind and sun directional information similar to what has recently been described in other insects. In summary, this thesis confirms the flexibility of cue integration in the dung beetle compass system in its natural environment and set the basis for further investigation into neuronal mechanisms that support this dynamic integration of directional cues.

Popular Abstract

Linking Brain to Behaviour in the Dung Beetle Compass

The dung beetle Kheper lamarcki is found in South Africa, where it plays an important role in the digestion of herbivore dung. It smells a fresh dung pile while flying, and when arriving at its target, many other species of dung eating insects are already feasting. To escape this competition for food, K. lamarcki forms itself a ball of dung and leaves the dung pile as efficiently as possible. Therefore, it rolls along a straight line, making maximal distance with a minimal amount of energy. This behaviour is rather unique, as most other animals will soon start circling along their own exiting path. To keep their straight bearing, the dung beetles step on top of their own balls and perform a ‘dance’ during which they collect a snapshot of available orientation cues, before rolling away the ball in a certain bearing to cues. The external orientation cues it uses are the position of the sun, the light intensity gradient (parts of the sky closest to the sun are brightest), the pattern of polarised light (sunlight reflected by the atmosphere creates a pattern which is visible to most insects, but not to the human eye), or wind. However, during midday, when the sun is close to zenith, orientation cues such as the position of the sun, intensity gradient and polarisation patterns lose their directionality and are therefore not useful for orientation. Despite this, beetles still manage to orientate. In the savannah, winds increase in strength during midday and have been shown to be sufficient for the dung beetles to orient by. Which orientation cue the beetle uses is determined by the cue’s reliability.

In the first part of my master thesis, I defined the dung beetle’s orientation precision when steering outdoors, either presenting a natural set of orientational cues, blocking out the wind or blocking out the sky. Beetles blocked from wind were able to keep a high orientation precision that did not change significantly over the course of a day. This indicates that beetles can orient with maintained precision up to solar elevation of 83°, which is the highest the sun reached in my experiments. The precision of beetles rolling with a blocked sky showed a significant decline during midday, however skylight cues might have entered the arena and likely aided the beetle’s precision. This experiment showed that beetles under a natural set of cues were able to keep a constant high orientation precision, that did not change significantly over the course of the day.

The mechanisms guiding the flexible change of orientation cues lie within the dung beetle brain. An area within the insect brain, called the central complex, houses the internal compass system. In the second part of my master’s thesis, I recorded neuronal activity from this brain area while I presented light and wind cues to the beetle in an indoor arena. In a first experiment, I found two types of neurons which are likely processing the beetles heading and goal direction. These two types of neurons are necessary to perform movement towards a goal. While heading-direction-neurons encode for the animal’s relation in space, the goal-direction-neurons encode the wanted travelling direction. A mismatch between these neurons activates steering neurons, which steer the beetle back on track. In a second set of experiments, the beetle was presented with an artificial sun cue and afterwards an additional wind cue. Recordings have shown that an additional wind cue enhanced the firing activity of the neuron. Therefore, these neurons encode both sun and wind cues, which each show a different strength of neuronal response. Building this functional setup allows for further experiments looking into the neuronal responses to cues changing in intensity and position.

These experiments form the baseline of explaining the neuronal flexibility with which the dung beetle is able to remain a constant high orientation precision even during changing conditions.
Despite their tiny brains, insects show great ability to navigate and orientate in challenging conditions. Understanding these mechanisms therefore give great advantage in forming ways to efficiently navigate and orientate in unknown terrain.

Master’s Degree Project in Biology, 60 credits, 2023/2024
Department of Biology, Lund University
Supervisor: Marie Dacke, Vision Group, Functional Zoology, Lund University

• author: Jürgensen, Linnéa
• supervisor: Marie Dacke; Shahrzad Shaverdian
• organization: Degree Projects in Biology
• course: BION03 20231
• year: 2024
• type: H2 - Master's Degree (Two Years)
• subject: Biology and Life Sciences
• language: English
• id: 9153930
• date added to LUP: 2024-05-23 14:33:27
• date last changed: 2024-05-23 14:33:27