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

Bumblebees exhibit the memory spacing effect

Associative learning is key to how bees recognize and return to rewarding floral resources. It thus plays a major role in pollinator floral constancy and plant gene flow. Honeybees are the primary model for pollinator associative learning, but bumblebees play an important ecological role in a wider range of habitats, and their associative learning abilities are less well understood. We assayed learning with the proboscis extension reflex (PER), using a novel method for restraining bees (capsules) designed to improve bumblebee learning. We present the first results demonstrating that bumblebees exhibit the memory spacing effect. They improve their associative learning of odor and nectar reward by exhibiting increased memory acquisition, a component of long-term memory formation, when the time interval between rewarding trials is increased. Bombus impatiens forager memory acquisition (average discrimination index values) improved by 129% and 65% at inter-trial intervals (ITI) of 5 and 3 min, respectively, as compared to an ITI of 1 min. Memory acquisition rate also increased with increasing ITI. Encapsulation significantly increases olfactory memory acquisition. Ten times more foragers exhibited at least one PER response during training in capsules as compared to traditional PER harnesses. Thus, a novel conditioning assay, encapsulation, enabled us to improve bumblebee-learning acquisition and demonstrate that spaced learning results in better memory consolidation. Such spaced learning likely plays a role in forming long-term memories of rewarding floral resources

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

Neonicotinoid pesticide limits improvement in buzz pollination by bumblebees

Neonicotinoid pesticides have been linked to global declines of beneficial insects such as bumblebees. Exposure to trace levels of these chemicals causes sub-lethal effects, such as reduced learning and foraging efficiency. Complex behaviours may be particularly vulnerable to the neurotoxic effects of neonicotinoids. Such behaviours may include buzz pollination (sonication), in which pollinators, usually bees, use innate and learned behaviours to generate high-frequency vibrations to release pollen from flowers with specialised anther morphologies. This study assesses the effect of field-realistic, chronic exposure to the widely-used neonicotinoid thiamethoxam on the development of sonication buzz characteristics over time, as well as the collection of pollen from buzz-pollinated flowers. We found that the pollen collection of exposed bees improved less with increasing experience than that of unexposed bees, with exposed bees collecting between 47% and 56% less pollen by the end of 10 trials. We also found evidence of two distinct strategies for maximising pollen collection: (1) extensions to the duration of individual buzzes and (2) extensions of the overall time spent buzzing. We find new complexities in buzz pollination, and conclude that the impacts of field-realistic exposure to a neonicotinoid pesticide may seriously compromise this important ecosystem service

Inherited biotic protection in a Neotropical pioneer plant

Chelonanthus alatus is a bat-pollinated, pioneer Gentianaceae that clusters in patches where still-standing, dried-out stems are interspersed among live individuals. Flowers bear circum-floral nectaries (CFNs) that are attractive to ants, and seed dispersal is both barochorous and anemochorous. Although, in this study, live individuals never sheltered ant colonies, dried-out hollow stems - that can remain standing for 2 years - did. Workers from species nesting in dried-out stems as well as from ground-nesting species exploited the CFNs of live C. alatus individuals in the same patches during the daytime, but were absent at night (when bat pollination occurs) on 60.5% of the plants. By visiting the CFNs, the ants indirectly protect the flowers - but not the plant foliage - from herbivorous insects. We show that this protection is provided mostly by species nesting in dried-out stems, predominantly Pseudomyrmex gracilis. That dried-out stems remain standing for years and are regularly replaced results in an opportunistic, but stable association where colonies are sheltered by one generation of dead C. alatus while the live individuals nearby, belonging to the next generation, provide them with nectar; in turn, the ants protect their flowers from herbivores. We suggest that the investment in wood by C. alatus individuals permitting stillstanding, dried-out stems to shelter ant colonies constitutes an extended phenotype because foraging workers protect the flowers of live individuals in the same patch. Also, through this process these dried-out stems indirectly favor the reproduction (and so the fitness) of the next generation including both their own offspring and that of their siblings, alladding up to a potential case of inclusive fitness in plants

Observational Conditioning in Flower Choice Copying by Bumblebees (Bombus terrestris): Influence of Observer Distance and Demonstrator Movement

A. Avargues-Weber was funded by a postdoctoral fellowship from Fyssen fondation: http://www.fondationfyssen.fr/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Floral sonication is an innate behaviour in bumblebees that can be fine-tuned with experience in manipulating flowers

Bumblebees demonstrate an extensive capacity for learning complex motor skills to maximise exploitation of floral rewards. This ability is well studied in nectar collection but its role in pollen foraging is less well understood. Floral sonication is used by bees to extract pollen from some plant species with anthers which must be vibrated (buzzed) to release pollen. Pollen removal is determined by sonication characteristics including frequency and amplitude, and thus the ability to optimise sonication should allow bees to maximise the pollen collection. We investigated the ability of the buff-tailed bumblebee (Bombus terrestris) to modify the frequency and amplitude of their buzzes with increasing experience manipulating flowers of the buzz-pollinated plantSolanum rostratum. We analysed flight and feeding vibrations generated by naïve workers across feeding bouts. Feeding buzzes were of a higher frequency and a lower amplitude than flight buzzes. Both flight and feeding buzzes had reduced amplitudes with increasing number of foraging trips. However, the frequency of their feeding buzzes was reduced significantly more than their flight buzzes as bumblebee workers gained experience manipulating flowers. These results suggest that bumblebees are able to modify the characteristics of their buzzes with experience manipulating buzz-pollinated flowers. We discuss our findings in the context of bumblebee learning, and the current understanding of the optimal sonication characteristics for releasing pollen in buzz-pollinated species. Our results present a tantalising insight into the potential role of learning in floral sonication, paving the way for future research in this area

Strategies of a parasite of the ant–Acacia mutualism

Mutualisms can be exploited by parasites—species that obtain resources from a partner but provide no services. Though the stability of mutualisms in the presence of such parasites is under intensive investigation, we have little information on life history traits that allow a species to be a successful mutualist or rather a parasite, particularly in cases where both are closely related. We studied the exploitation of Acacia myrmecophytes by the ant, Pseudomyrmex gracilis, contrasting with the mutualistic ant Pseudomyrmex ferrugineus. P. gracilis showed no host-defending behavior and had a negative effect on plant growth. By preventing the mutualist from colonization, P. gracilis imposes opportunity costs on the host plant. P. gracilis produced smaller colonies with a higher proportion of alates than did the mutualist and thus showed an “r-like” strategy. This appears to be possible because P. gracilis relies less on host-derived food resources than does the mutualist, as shown by behavioral and stable isotope studies. We discuss how this system allows the identification of strategies that characterize parasites of mutualisms

Specialized Learning in Antlions (Neuroptera: Myrmeleontidae), Pit-Digging Predators, Shortens Vulnerable Larval Stage

Unique in the insect world for their extremely sedentary predatory behavior, pit-dwelling larval antlions dig pits, and then sit at the bottom and wait, sometimes for months, for prey to fall inside. This sedentary predation strategy, combined with their seemingly innate ability to detect approaching prey, make antlions unlikely candidates for learning. That is, although scientists have demonstrated that many species of insects possess the capacity to learn, each of these species, which together represent multiple families from every major insect order, utilizes this ability as a means of navigating the environment, using learned cues to guide an active search for food and hosts, or to avoid noxious events. Nonetheless, we demonstrate not only that sedentary antlions can learn, but also, more importantly, that learning provides an important fitness benefit, namely decreasing the time to pupate, a benefit not yet demonstrated in any other species. Compared to a control group in which an environmental cue was presented randomly vis-à-vis daily prey arrival, antlions given the opportunity to associate the cue with prey were able to make more efficient use of prey and pupate significantly sooner, thus shortening their long, highly vulnerable larval stage. Whereas “median survival time,” the point at which half of the animals in each group had pupated, was 46 days for antlions receiving the Learning treatment, that point never was reached in antlions receiving the Random treatment, even by the end of the experiment on Day 70. In addition, we demonstrate a novel manifestation of antlions' learned response to cues predicting prey arrival, behavior that does not match the typical “learning curve” but which is well-adapted to their sedentary predation strategy. Finally, we suggest that what has long appeared to be instinctive predatory behavior is likely to be highly modified and shaped by learning