Generalization of navigation memory in honeybees

Flying insects like the honeybee learn multiple features of the environment for efficient navigation. Here we introduce a novel paradigm in the natural habitat, and ask whether the memory of such features is generalized to novel test conditions. Foraging bees from colonies located in 5 different home areas were tested in a common area for their search flights. The home areas differed in the arrangements of rising natural objects or their lack, and in the existence or lack of elongated ground structures. The test area resembled partly or not at all the layout of landmarks in the respective home areas. In particular, the test area lacked rising objects. The search flights were tracked with harmonic radar and quantified by multiples procedures, extracting their differences on an individual basis. Random search as the only guide for searching was excluded by two model calculations. The frequencies of directions of flight sectors differed from both model calculations and between the home areas in a graded fashion. Densities of search flight fixes were used to create heat maps and classified by a partial least squares regression analysis. Classification was performed with a support vector machine in order to account for optimal hyperplanes. A rank order of well separated clusters was found that partly resemble the graded differences between the ground structures of the home areas and the test area. The guiding effect of elongated ground structures was quantified with respect to the sequence, angle and distance from these ground structures. We conclude that foragers generalize their specific landscape memory in a graded way to the landscape features in the test area, and argue that both the existence and absences of landmarks are taken into account. The conclusion is discussed in the context of the learning and generalization process in an insect, the honeybee, with an emphasis on exploratory learning in the context of navigation

Detrimental effects of clothianidin on foraging and dance communication in honey bees

Ongoing losses of pollinators are of significant international concern because of the essential role they have in our ecosystem, agriculture, and economy. Both chemical and non-chemical stressors have been implicated as possible contributors to their decline, but the increasing use of neonicotinoid insecticides has recently emerged as particularly concerning. In this study, honey bees were exposed orally to sublethal doses of the neonicotinoid clothianidin in the field in order to assess its effects on the foraging behavior, homing success, and dance communication. The foraging span and foraging activity at the contaminated feeder decreased significantly due to chronic exposure at field-realistic concentrations. Electrostatic field of dancing bees was measured and it was revealed that the number of waggle runs, the fanning time and the number of stop signals were significantly lower in the exposed colony. No difference was found in the homing success and the flight duration between control and treated bees released at a novel location within the explored area. However, a negative effect of the ambient temperature, and an influence of the location of the trained feeder was found. Finally, the residues of clothianidin accumulated in the abdomens of exposed foraging bees over time. These results show the adverse effects of a chronic exposure to sublethal doses of clothianidin on foraging and dance communication in honey bees

Honey bees infer source location from the dances of returning foragers

Honeybees (Apis mellifera carnica) communicate the direction and distance to a food source by means of a waggle dance. We ask whether bees recruited by the dance use it only as a flying instruction, with the technical form of a polar vector, or also translate it into a location vector that enables them to set courses directed toward the food source from arbitrary locations within their familiar territory. The flights of recruits captured on exiting the hive and released at distant sites were tracked by radar. The recruits performed first a straight flight in approximately the compass direction indicated by the dance. However, this “vector” portion of their flights and the ensuing tortuous “search” portion were strongly and differentially affected by the release site. Searches were biased toward the true location of the food and away from the location specified by translating the origin for the danced polar vector to the release site. We conclude that by following the dance recruits get two messages, a polar flying instruction (bearing and range from the hive) and a location vector that enables them to approach the source from anywhere in their familiar territory. The dance communication is much richer than thought so far

Eavesdropping on Honeybee Communication via Electrostatic Field Recordings

As a canary in a coalmine warns of dwindling breathable air, the honeybee can indicate the health of an ecosystem. Honeybees are the most important pollinators of fruit-bearing flowers, and share similar ecological niches with many other pollinators; therefore, the health of a honeybee colony can reflect the conditions of a whole ecosystem. The health of a colony may be mirrored in social signals that bees exchange during their sophisticated body movements such as the waggle dance. To observe these changes, we developed an automatic system that records and quantifies social signals under normal beekeeping conditions. Here, we describe the system and report representative cases of normal social behavior in honeybees. Our approach utilizes the fact that honeybee bodies are electrically charged by friction during flight and inside the colony, and thus they emanate characteristic electrostatic fields when they move their bodies. These signals, together with physical measurements inside and outside the colony (temperature, humidity, weight of the hive, and activity at the hive entrance) will allow quantification of normal and detrimental conditions of the whole colony. The information provided instructs how to setup the recording device, how to install it in a normal bee colony, and how to interpret its data

Guidance of Navigating Honeybees by Learned Elongated Ground Structures

Elongated landscape features like forest edges, rivers, roads or boundaries of fields are particularly salient landmarks for navigating animals. Here, we ask how honeybees learn such structures and how they are used during their homing flights after being released at an unexpected location (catch-and-release paradigm). The experiments were performed in two landscapes that differed with respect to their overall structure: a rather feature-less landscape, and one rich in close and far distant landmarks. We tested three different forms of learning: learning during orientation flights, learning during training to a feeding site, and learning during homing flights after release at an unexpected site within the explored area. We found that bees use elongated ground structures, e.g., a field boundary separating two pastures close to the hive (Experiment 1), an irrigation channel (Experiment 2), a hedgerow along which the bees were trained (Experiment 3), a gravel road close to the hive and the feeder (Experiment 4), a path along an irrigation channel with its vegetation close to the feeder (Experiment 5) and a gravel road along which bees performed their homing flights (Experiment 6). Discrimination and generalization between the learned linear landmarks and similar ones in the test area depend on their object properties (irrigation channel, gravel road, hedgerow) and their compass orientation. We conclude that elongated ground structures are embedded into multiple landscape features indicating that memory of these linear structures is one component of bee navigation. Elongated structures interact and compete with other references. Object identification is an important part of this process. The objects are characterized not only by their appearance but also by their alignment in the compass. Their salience is highest if both components are close to what had been learned. High similarity in appearance can compensate for (partial) compass misalignment, and vice versa

Honeybees Learn Landscape Features during Exploratory Orientation Flights

Degen J, Kirbach A, Reiter L, et al. Honeybees Learn Landscape Features during Exploratory Orientation Flights. Current Biology. 2016;26(20):2800-2804

Massed and Spaced Learning in Honeybees: The Role of CS, US, the Intertrial Interval, and the Test Interval

Conditioning the proboscis extension reflex of harnessed honeybees (Apis mellifera) is used to study the effect temporal spacing between successive conditioning trials has on memory. Retention is monitored at two long-term intervals corresponding to early (1 and 2 d after conditioning) and late long-term memory (3 and 4 d). The acquisition level is varied by using different conditioned stimuli (odors, mechanical stimulation, and temperature increase at the antenna), varying strengths of the unconditioned stimulus (sucrose), and various numbers of conditioning trials. How learning trials are spaced is the dominant factor both for acquisition and retention, and although longer intertrial intervals lead to better acquisition and higher retention, the level of acquisition per se does not determine the spacing effect on retention. Rather, spaced conditioning leads to higher memory consolidation both during acquisition and later, between the early and long-term memory phases. These consolidation processes can be selectively inhibited by blocking protein synthesis during acquisition

Neonicotinoids interfere with specific components of navigation in honeybees

Three neonicotinoids, imidacloprid, clothianidin and thiacloprid, agonists of the nicotinic acetylcholine receptor in the central brain of insects, were applied at non-lethal doses in order to test their effects on honeybee navigation. A catch-and-release experimental design was applied in which feeder trained bees were caught when arriving at the feeder, treated with one of the neonicotinoids, and released 1.5 hours later at a remote site. The flight paths of individual bees were tracked with harmonic radar. The initial flight phase controlled by the recently acquired navigation memory (vector memory) was less compromised than the second phase that leads the animal back to the hive (homing flight). The rate of successful return was significantly lower in treated bees, the probability of a correct turn at a salient landscape structure was reduced, and less directed flights during homing flights were performed. Since the homing phase in catch-and-release experiments documents the ability of a foraging honeybee to activate a remote memory acquired during its exploratory orientation flights, we conclude that non-lethal doses of the three neonicotinoids tested either block the retrieval of exploratory navigation memory or alter this form of navigation memory. These findings are discussed in the context of the application of neonicotinoids in plant protection

Effects of sublethal doses of glyphosate on honeybee navigation

Glyphosate (GLY) is a herbicide that is widely used in agriculture for weed control. Although reports about the impact of GLY in snails, crustaceans and amphibians exist, few studies have investigated its sublethal effects in non-target organisms such as the honeybee Apis mellifera, the main pollen vector in commercial crops. Here, we tested whether exposure to three sublethal concentrations of GLY (2.5, 5 and 10 mg l-1: corresponding to 0.125, 0.250 and 0.500 μg per animal) affects the homeward flight path of honeybees in an open field. We performed an experiment in which forager honeybees were trained to an artificial feeder, and then captured, fed with sugar solution containing traces of GLYand released from a novel site either once or twice. Their homeward trajectories were tracked using harmonic radar technology. We found that honeybees that had been fed with solution containing 10 mg l-1 GLY spent more time performing homeward flights than control bees or bees treated with lower concentrations. They also performed more indirect homing flights. Moreover, the proportion of direct homeward flights performed after a second release from the same site increased in control bees but not in treated bees. These results suggest that, in honeybees, exposure to levels of GLY commonly found in agricultural settings impairs the cognitive capacities needed to retrieve and integrate spatial information for a successful return to the hive. Therefore, honeybee navigation is affected by ingesting traces of the most widely used herbicide worldwide, with potential long-term negative consequences for colony foraging success.Fil: Balbuena, María Sol. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; ArgentinaFil: Tison, Léa. Freie Universitat Berlin; AlemaniaFil: Hahn, Marie-Luise. Freie Universitat Berlin; AlemaniaFil: Greggers, Uwe. Freie Universitat Berlin; AlemaniaFil: Menzel, Randolf. Freie Universitat Berlin; AlemaniaFil: Farina, Walter Marcelo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentin