The Ontogeny of Bumblebee Flight Trajectories: From Naïve Explorers to Experienced Foragers

et al. (2013) The Ontogeny of Bumblebee Flight Trajectories: From Nave Explorers to Experienced Foragers. PLoS ONE 8(11): e78681. doi:10.1371/journal.pone.0078681 The Ontogeny of Bumblebee Flight Trajectories: From Nave Explorers to Experienced Foragers Juliet L. Osborne 0 Alan Smith 0 Suzanne J. Clark 0 Don R. Reynolds 0 Mandy C. Barron 0 Ka S. Lim 0 Andy M. Reynolds 0 Guy Smagghe, Ghent University, Belgium 0 1 Environment & Sustainability Institute, University of Exeter , Penryn, Cornwall , United Kingdom , 2 Rothamsted Research, Harpenden, Hertfordshire , United Kingdom , 3 Natural Resources Institute , University of Greenwich , Chatham, Kent , United Kingdom , 4 Landcare Research, Lincoln , New Zealand Understanding strategies used by animals to explore their landscape is essential to predict how they exploit patchy resources, and consequently how they are likely to respond to changes in resource distribution. Social bees provide a good model for this and, whilst there are published descriptions of their behaviour on initial learning flights close to the colony, it is still unclear how bees find floral resources over hundreds of metres and how these flights become directed foraging trips. We investigated the spatial ecology of exploration by radar tracking bumblebees, and comparing the flight trajectories of bees with differing experience. The bees left the colony within a day or two of eclosion and flew in complex loops of everincreasing size around the colony, exhibiting Le vy-flight characteristics constituting an optimal searching strategy. This mathematical pattern can be used to predict how animals exploring individually might exploit a patchy landscape. The bees' groundspeed, maximum displacement from the nest and total distance travelled on a trip increased significantly with experience. More experienced bees flew direct paths, predominantly flying upwind on their outward trips although forage was available in all directions. The flights differed from those of nave honeybees: they occurred at an earlier age, showed more complex looping, and resulted in earlier returns of pollen to the colony. In summary bumblebees learn to find home and food rapidly, though phases of orientation, learning and searching were not easily separable, suggesting some multitasking. - Funding: JLO is partly funded under the Insect Pollinator Initiative (project BB/I000097/1) which is jointly funded by the Biotechnology and Biological Sciences Research Council (BBSRC), the Natural Environment Research Council (NERC), Defra, the Scottish Government and The Wellcome Trust. Rothamsted Research receives grant-aided funding from the BBSRC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Constantly changing temporal and spatial distributions of resources provide complex challenges to animals. Understanding how they explore the landscape can give insight into how they find and selectively exploit these resources efficiently. The impressive abilities of bumblebees and honeybees to exploit a landscape for nectar and pollen for their colony have been investigated in terms of their ability to learn and memorize visually complex routes in pursuit of these rewards, their sophisticated spatial navigational abilities, and their energetic efficiency at reward collection [15]. However, most deductions have been made without researchers being able to map the complete flight paths taken by bees in real landscapes whilst they learn, search and forage. Instead, researchers have analyzed detailed sections of flight such as flying near the colony entrance [69] or at flower patches [5,10,11], or designed elegant experiments to measure flight characteristics in a simulated foraging environment [1215]. The objective of this study was, for the first time, to map and characterize the flights of bumblebee workers, starting with nave bees on their first exploratory flights. We examined whether the shapes of these flights indicate an optimal strategy for searching or learning, and analyzed the changes in flight trajectories with experience as they developed into successful foraging flights. Learning About the Colony Entrance When a bumblebee first leaves the colony, she makes short flights which have been described as learning flights or orientation flights [6,8,16]. Learning flights in social and solitary Hymenoptera start with circumscribed movements close to the nest, backing away in a series of zigzags or arcs of constant angular velocity, but increasing radius, roughly centered on the entrance hole [16]. During these arcing maneuvers a bee gathers visiospatial information (and possibly olfactory information) relating to the colony entrance and nearby landmarks to enable a successful return at the end of a trip (reviewed in [8,9]). The description of these learning flights has previously focused on the portion visible to an observer or video at the colony [8,9,17], and indeed sometimes the flights only cover this short range. However, the bee may fly beyond view and there are no published data on what the bees do next. During the unseen portions of these preliminary flights, away from the colony entrance, not only is the bee likely to be learning the landscape, but it is also the bees first opportunity to search for flowers and to manipulate flowers to gather nectar and pollen. Since the flights studied here are likely to include learning, orientation, searching and possibly some foraging; then we refer to them as preliminary flights rather than orientation flights to avoid confusion with previous literature. Exploring the Landscape and Searching for Forage How do bumblebees explore and choose where to forage in a heterogeneous environment? They show constancy to plant species and to forage area over several days [1,4,18], but how do they make these choices in the first place? As [19] note with respect to honeybees little is known about the actual process of searching, because of the difficulty of following individual bees in the field. Does a bumblebee, leaving the nest for the first time, fly in one direction until suitable forage is reached and then start feeding? Or does the bee make several flights to learn about the vicinity before starting to forage? In exploring, they may use an optimal strategy in terms of the energy and time utilized to find patches of flowers, such as a random walk, or spiral pattern or random looping pattern [20 22]. Honeybees fly in distinctive looped search patterns when attempting to locate their hive, after their hive-centred navigation mechanisms have been disrupted [23], and when attempting to relocate a food source [24] and the tendency for loop sizes to increase over time results in scale-free (Levy flight) characteristics. This strategy is considered optimal in these circumstances because (a) it ensu (...truncated)