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Flight of the Bumblebee Reveals Optimization at Multiple Levels

Evolution News

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A biological revolution is underway. Technology has allowed field biologists to track individual animals as small as insects, allowing scientists, for the first time, to gain real-time data on their lifetime behaviors. A team using this technology says in PLOS ONE:

Recent advances in animal-tracking technology have brought within reach the goal of tracking every movement of individual animals over their entire lifetimes. The potential of such life-long tracks to advance our understanding of animal behaviour has been compared to that of the advent of DNA sequencing, but the field is still in its infancy. [Emphasis added.]

If you saw Flight: The Genius of Birds you may remember how tiny geolocators allowed Carsten Egevang’s team to monitor the pole-to-pole flight paths of Arctic terns from one year to the next. We’ve also reported on subsequent studies using geolocators on blackpoll warblers, frigate birds, and even giant flower beetles. Now, a team from Queen Mary University of London has attached radar antennas to bumblebees’ heads, allowing them to monitor the entire lifetime flight behavior of these important pollinators. The device looks like this:

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The work adds to previous research that was more limited. Earlier teams used harmonic radar to track initial flights of bees. This is the first time that the technology was used to monitor the lifetime flights of four bumblebees (Bombus terrestris) over 6-15 days until contact was lost.

The studies described above revealed a great deal about the structure of exploratory and foraging flights, but opened up a number of key questions that are unanswered as yet. Does the change in flight structure from inexperienced to experienced bees occur gradually or as a sudden transition? When and how do bees discover the forage sources they go on to exploit? No prior study has been able to track the activity of individual insects throughout their entire life history, or even a significant portion of their life, making it impossible to address these questions.

You can see the headgear worn by the test bees in a summary on PhysOrg. There will always be some doubt about measurements obtained this way. Did the headgear alter the bees’ normal behavior? Were they treated differently by other bees because they look weird? The scientists acknowledged other limitations of the study, such as the fact they were conducted sequentially, when different flowers were in bloom, and employed individuals from different colonies in different locations under different weather conditions. Nevertheless, they reached some tentative conclusions based on 15,000 minutes of data from 244 flights covering 180 kilometers.

Woodgate et al. were surprised to find more individuality than expected. “One of the most striking results to emerge from these data is the large degree to which our bees differed from one another,” they write. The bees were not like little robots following a predetermined flight strategy. Each one divided its time differently between exploration of new food sources and exploitation of known food sources. One bee was a “lifelong vagabond,” never settling down on any favorite patch. Another one, by contrast, quickly devoted most of its energy to patches with a high payoff. Overall, the pollinators seemed to balance their time between exploitation and exploration. It’s a smart strategy, Woodgate says in the PhysOrg article:

“This study provided an unprecedented look at where the bees flew, how their behaviour changed as they gained experience and how they balanced the need to explore their surroundings – looking for good patches of flowers — with the desire to collect as much food as possible from the places they had already discovered.

The bees made from 3 to 15 flights per day, depending on the distance to and quality of the resources. In general, exploratory flights occur within the first few days. That’s when they discover most of the goods that they will return to most often. They will, however, make further exploratory flights at any time. The radar maps of their flight paths show extensive exploration of their surroundings in all directions, implying substantial brain power for memory, orientation and strategy to navigate over large areas and still find their way home.

Future work with larger numbers of bees, monitored simultaneously, will undoubtedly add to knowledge about their behaviors. For now, it appears that bumblebee colonies are programmed to use optimization algorithms – an indicator of intelligent design encoded in their brains. These algorithms work at both the individual and collective level. Variability leads some individuals to bring a lot of food back from reliable sources, and some to explore the environment for new and possibly better sources.

Although it is expected that randomly chosen individuals will tend to show variation in behaviour, the extent of the inter-individual differences we observed in flight behaviour is dramatic. These differences appear to persist over the bees’ entire foraging career, and are likely to lead to high levels of variation in the contribution different foragers make to provisioning the colony.

An Instrument View of Bee Optimization

We’ve looked at lifetime flight behavior of these amazing flyers. Another article explores the flight equipment in more detail. The journal eLife reports new findings about how honeybees (Apis mellifera) position their antennae during flight. Antennae are well known as olfactory and tactile sense organs. During flight, they perform additional roles as speedometers and odometers. Experiments in wind tunnels showed that honeybees will position their antennae forward or backward in flight to measure speed, distance and odor sources:

To investigate how honeybees use different types of sensory information to position their antennae during flight, Roy Khurana and Sane first placed freely-flying and tethered bees in a wind tunnel. Flying forward causes air to flow from the front to the back of the bee. The experiments revealed that a bee brings its antennae forward and holds them in a specific position that depends on the rate of airflow. As the bee flies forward more quickly (or airflow increases), the antennae are positioned further forward.

Roy Khurana and Sane then investigated how the movement of images across the insect’s eyes causes their antennae to change position. This unexpectedly revealed that moving images across the eye from front to back, which simulates what bees see when flying forward, causes the bees to move their antennae backward. However, exposing the bees to both the frontal airflow and front-to-back image motion as normally experienced during forward flight caused the bees to maintain their antennae in a fixed position. This behaviour results from the opposing responses of the antennae to the two stimuli.

This appears to be another optimization problem solved by the bees, because the mechanosensory input from the antennae can override the visual sense:

When flying in unpredictable conditions, sensory cues from a single modality are often unreliable measures of the ambient environmental parameters. For instance, purely optic flow-based measurements of self-motion can be misleading for insects which experience sideslip while flying in a crosswind. Moreover, reliance on optic flow may be problematic under dimly lit or overcast conditions, or when flying over lakes or deserts which present sparse visual feedback. In such situations, sampling from multiple sensory cues reduces the ambiguity arising from variability in feedback from single modalities (Wehner, 2003; Sherman and Dickinson, 2004; Wasserman et al., 2015). Hence, the integration of multimodal sensory cues is essential for most natural locomotory behaviours, including insect flight manoeuvres (Willis and Arbas, 1991; Frye et al., 2003; Verspui and Gray, 2009).

The researchers found that antenna position is part of this “multimodal sensory integration” that maximizes useful information from multiple — sometimes antagonistic — sources. It’s like the IFR-trained pilot who learns to trust his instruments instead of his eyes when the sensory data seem to conflict.

Combined with bees’ electrical sense, these pollinators of flowers and crops are pretty amazing little creatures. Neither paper explained how these abilities might have evolved. The second one on antenna positioning only mentions the “evolutionary significance of its function” because flight is impaired when it’s broken. Blind processes don’t achieve such marvels.

Photo credit: Top: Bernie (Own work) [Public domain], via Wikimedia Commons. Below: © Joseph Woodgate, Queen Mary University of London, via EurekAlert.