A Simple Iterative Model Accurately Captures Complex Trapline Formation by Bumblebees Across Spatial Scales and Flower Arrangements

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Radar tracking and motion-sensitive cameras on flowers reveal the development of pollinator multi-destination routes over large spatial scales.

PublishedJournal ArticleResearch Support, Non-U.S. Gov'tCentral place foragers, such as pollinating bees, typically develop circuits (traplines) to visit multiple foraging sites in a manner that minimizes overall travel distance. Despite being taxonomically widespread, these routing behaviours remain poorly understood due to the difficulty of tracking the foraging history of animals in the wild. Here we examine how bumblebees (Bombus terrestris) develop and optimise traplines over large spatial scales by setting up an array of five artificial flowers arranged in a regular pentagon (50 m side length) and fitted with motion-sensitive video cameras to determine the sequence of visitation. Stable traplines that linked together all the flowers in an optimal sequence were typically established after a bee made 26 foraging bouts, during which time only about 20 of the 120 possible routes were tried. Radar tracking of selected flights revealed a dramatic decrease by 80% (ca. 1500 m) of the total travel distance between the first and the last foraging bout. When a flower was removed and replaced by a more distant one, bees engaged in localised search flights, a strategy that can facilitate the discovery of a new flower and its integration into a novel optimal trapline. Based on these observations, we developed and tested an iterative improvement heuristic to capture how bees could learn and refine their routes each time a shorter route is found. Our findings suggest that complex dynamic routing problems can be solved by small-brained animals using simple learning heuristics, without the need for a cognitive map.This research was supported by a combined grant from the Wellcome Trust, the Biotechnology and Biological Sciences Research Council, and the Engineering and Physical Sciences Research Council (BB/F52765X/1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Monitoring Flower Visitation Networks and Interactions between Pairs of Bumble Bees in a Large Outdoor Flight Cage

This research was supported by a combined grant from the Wellcome Trust, the Biotechnology and Biological Sciences Research Council, and the Engineering and Physical Sciences Research Council (BB/F52765X/1). While writing, ML was supported by the IDEX of the Federal University of Toulouse (Starting and Emergence grants), the Fyssen foundation and the CNRS. NER was supported as the Rebanks Family Chair in Pollinator Conservation by The W. Garfield Weston Foundation. LC was supported by ERC Advanced Grant SpaceRadarPollinator and by a Royal Society Wolfson Research Merit Award

Bumble bees strategically use ground level linear features in navigation

Extended ground level structures like roads or field edges can be important cues for navigating animals,seen for example in road-following pigeons. In a landscape devoid of skyline cues but with a rectangular grid of pathways and roads, we used harmonic radar to track free-flying bumble bees,Bombus terrestris. Individual bees consistently used ground level linear features for navigation in a wide range of behavioural contexts. Bee exploration flights, search behaviour and foraging routes were shaped by linear features, with bees frequently flying along and parallel to pathways and roads. Comparisons off light trajectories across these behavioural contexts show that individuals modulated their use of linear features strategically with respect to their individual goals and experience. Bees searching for a feeder used linear features to target their search, while foragers often followed pathways to return to their hive without overshooting. These findings on a major pollinator have important implications for the placements of bee colonies for agriculture and floral resources for conservation

Signatures of a globally optimal searching strategy in the three-dimensional foraging flights of bumblebees

Simulated annealing is a powerful stochastic search algorithm for locating a global maximum that is hidden among many poorer local maxima in a search space. It is frequently implemented in computers working on complex optimization problems but until now has not been directly observed in nature as a searching strategy adopted by foraging animals. We analysed high-speed video recordings of the three-dimensional searching flights of bumblebees (Bombus terrestris) made in the presence of large or small artificial flowers within a 0.5 m3 enclosed arena. Analyses of the three-dimensional flight patterns in both conditions reveal signatures of simulated annealing searches. After leaving a flower, bees tend to scan back-and forth past that flower before making prospecting flights (loops), whose length increases over time. The search pattern becomes gradually more expansive and culminates when another rewarding flower is found. Bees then scan back and forth in the vicinity of the newly discovered flower and the process repeats. This looping search pattern, in which flight step lengths are typically power-law distributed, provides a relatively simple yet highly efficient strategy for pollinators such as bees to find best quality resources in complex environments made of multiple ephemeral feeding sites with nutritionally variable rewards

Exploring miniature insect brains using micro-CT scanning techniques

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Mutual Mate Choice: When it Pays Both Sexes to Avoid Inbreeding

Theoretical models of sexual selection predict that both males and females of many species should benefit by selecting their mating partners. However, empirical evidence testing and validating this prediction is scarce. In particular, whereas inbreeding avoidance is expected to induce sexual conflicts, in some cases both partners could benefit by acting in concert and exerting mutual mate choice for non-assortative pairings. We tested this prediction with the gregarious cockroach Blattella germanica (L.). We demonstrated that males and females base their mate choice on different criteria and that choice occurs at different steps during the mating sequence. Males assess their relatedness to females through antennal contacts before deciding to court preferentially non-siblings. Conversely, females biased their choice towards the most vigorously courting males that happened to be non-siblings. This study is the first to demonstrate mutual mate choice leading to close inbreeding avoidance. The fact that outbred pairs were more fertile than inbred pairs strongly supports the adaptive value of this mating system, which includes no “best phenotype” as the quality of two mating partners is primarily linked to their relatedness. We discuss the implications of our results in the light of inbreeding conflict models

Unravelling the mechanisms of trapline foraging in bees

International audienceAddendum to: Lihoreau M, Raine NE, Reynolds AM, Stelzer RJ, Lim KS, Smith AD, et al.; Addendum to. Radar tracking and motion-sensitive cameras on flowers reveal the development of pollinator multi-destination routes of bumblebees over large spatial scales. PLoS Biol 2012; 10:e1001392; PMID:23049479; http://dx.doi. org/10.1371/journal.pbio.1001392. T rapline foraging (repeated sequential visits to a series of feeding locations) is a taxonomically widespread but poorly understood behavior. Investigating these routing strategies in the field is particularly difficult, as it requires extensive tracking of animal movements to retrace their complete foraging history. In a recent study, we used harmonic radar and motion-triggered video cameras to track bumblebees foraging between artificial flowers in a large open field. We describe how all bees gradually developed a near optimal trapline to link all flowers and have identified a simple learning heuristic capable of replicating this optimization behavior. Our results provide new perspectives to clarify the sequence of decisions made by pollinat-ing insects during trapline foraging, and explore how spatial memory is organized in their small brains. " I have always regretted that I did not mark the bees by attaching bits of cotton wool or eiderdown to them with rubber, because this would have made it much easier to follow their paths. " Charles Darwin

Strategies of the honeybee Apis mellifera during visual search for vertical targets presented at various heights: a role for spatial attention?

When honeybees are presented with a colour discrimination task, they tend to choose swiftly and accurately when objects are presented in the ventral part of their frontal visual field. In contrast, poor performance is observed when objects appear in the dorsal part. Here we investigate if this asymmetry is caused by fixed search patterns or if bees can use alternative search mechanisms such as spatial attention, which allows flexible focusing on different areas of the visual field. We asked individual honeybees to choose an orange rewarded target among blue distractors. Target and distractors were presented in the ventral visual field, the dorsal field or both. Bees presented with targets in the ventral visual field consistently had the highest search efficiency, with rapid decisions, high accuracy and direct flight paths. In contrast, search performance for dorsally located targets was inaccurate and slow at the beginning of the test phase, but bees increased their search performance significantly after a few learning trials: they found the target faster, made fewer errors and flew in a straight line towards the target. However, bees needed thrice as long to improve the search for a dorsally located target when the target's position changed randomly between the ventral and the dorsal visual field. We propose that honeybees form expectations of the location of the target's appearance and adapt their search strategy accordingly. Different possible mechanisms of this behavioural adaptation are discussed.L.M. was recipient of a DOC-fFORTE fellowship of the Austrian Academy of Science at the Department of Integrative Zoology, University of Vienna. L.C. is supported by an ERC Advanced Grant and a Royal Society Wolfson Research Merit Award

Life-Long Radar Tracking of Bumblebees

This work was supported by European Research Council Advanced Grant no. 339347