Andrew B. Barron

A quantitative model of honey bee colony population dynamics.

Since 2006 the rate of honey bee colony failure has increased significantly. As an aid to testing hypotheses for the causes of colony failure we have developed a compartment model of honey bee colony population dynamics to explore the impact of different death rates of forager bees on colony growth and development. The model predicts a critical threshold forager death rate beneath which colonies regulate a stable population size. If death rates are sustained higher than this threshold rapid population decline is predicted and colony failure is inevitable. The model also predicts that high forager death rates draw hive bees into the foraging population at much younger ages than normal, which acts to accelerate colony failure. The model suggests that colony failure can be understood in terms of observed principles of honey bee population dynamics, and provides a theoretical framework for experimental investigation of the problem.

Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera)

Abstract. The biogenic amine neurochemical octopamine is involved in the onset of foraging behaviour in honey bees. We tested the hypothesis that octopamine influences honey bee behavioural development by modulating responsiveness to task-related stimuli. We examined the effect of octopamine treatment on responsiveness to brood pheromone (an activator of foraging) and to the presence of older bees in the colony (an inhibitor of foraging in young bees). Octopamine treatment increased responsiveness to brood pheromone and decreased responsiveness to social inhibition. These results identify octopamine both as an important source of variation in response thresholds and as a modulator of pheromonal communication in insect societies. We speculate that octopamine plays more than one role in the organisation of behavioural development indicating a very high level of integration between the neurochemical system and the generation of complex behaviour.

A Role for Octopamine in Honey Bee Division of Labor

Efficient division of labor is one of the main reasons for the success of the social insects. In honey bees the division of labor is principally achieved by workers changing tasks as they age. Typically, young adult bees perform a series of tasks within the colony before ultimately making the transition to foraging outside the hive for resources. This lifelong behavioral development is a well-characterized example of naturally occurring behavioral plasticity, but its neural bases are not well understood. Two techniques were used to assess the role of biogenic amines in the transition from in-hive work to foraging, which is the most dramatic and obvious transition in honey bee behavioral development. First, associations between amines and tasks were determined by measuring the levels of amines in dissected regions of individual bee brains using HPLC analysis. Second, colonies were orally treated with biogenic amines and effects on the onset of foraging were observed. Octopamine concentration in the antennal lobes of the bee brain was most reliably associated with task: high in foragers and low in nurses regardless of age. In contrast, octopamine in the mushroom bodies, a neighboring neuropil, was associated with age and not behavior, indicating independent modulation of octopamine in these two brain regions. Treating colonies with octopamine resulted in an earlier onset of foraging in young bees. In addition, octopamine levels were not elevated by non-foraging flight, but were already high on return from the first successful foraging trip and subsequently remained high, showing no further change with foraging experience. This observation suggests that octopamine becomes elevated in the antennal lobes in anticipation of foraging and is involved in the release and maintenance of the foraging state. Foraging itself, however, does not modulate octopamine levels. Behaviorally related changes in octopamine are modulated by juvenile hormone, which has also been implicated in the control of honey bee division of labor. Treatment with the juvenile hormone analog methoprene elevated octopamine and octopamine treatment ‘rescued’ the delay in behavioral development caused by experimentally depleting juvenile hormone in bees. Although the pathways linking juvenile hormone and octopamine are presently unknown, it is clear that octopamine acts ‘downstream’ of juvenile hormone to influence behavior and that juvenile hormone modulates brain octopamine levels. A working hypothesis is that octopamine acts as an activator of foraging by modulating responsiveness to foraging-related stimuli. This is supported by the finding that octopamine treatment increased the response of bees to brood pheromone, a stimulator of foraging activity. Establishing a role for octopamine in honey bee behavioral development is a first step in understanding the neural bases of this example of naturally occurring, socially mediated, behavioral plasticity. The next level of analysis will be to determine precisely where and how octopamine acts in the nervous system to coordinate this complex social behavior.

Octopamine modulates honey bee dance behavior

Honey bees communicate the location and desirability of valuable forage sites to their nestmates through an elaborate, symbolic “dance language.” The dance language is a uniquely complex communication system in invertebrates, and the neural mechanisms that generate dances are largely unknown. Here we show that treatments with controlled doses of the biogenic amine neuromodulator octopamine selectively increased the reporting of resource value in dances by forager bees. Oral and topical octopamine treatments modulated aspects of dances related to resource profitability in a dose-dependent manner. Dances for pollen and sucrose responded similarly to octopamine treatment, and these effects were eliminated by treatment with the octopamine antagonist mianserin. We propose that octopamine modulates the representation of floral rewards in dances by changing the processing of reward in the honey bee brain. Octopamine is known to modulate appetitive behavior in a range of solitary insects; the role of octopamine in dance provides an example of how neural substrates can be adapted for new behavioral innovations in the process of social evolution.

Rapid behavioral maturation accelerates failure of stressed honey bee colonies

Significance Honey bee colony death rates are unsustainably high. While many stressors have been identified that contribute to this problem, we do not know why colonies transition so rapidly from a state of apparent health to failure. It is well known that individual bees react to nutritional and pathogen stresses by foraging precociously: our study explains how colony failure arises from the social responses of individual bees to stress. We used radio tracking to monitor performance of bees and found that workers who begin foraging prematurely perform very poorly. This compounds the stresses on the colony and accelerates failure. We suggest how colonies at risk can be identified early, and the most effective interventions to prevent failure. Many complex factors have been linked to the recent marked increase in honey bee colony failure, including pests and pathogens, agrochemicals, and nutritional stressors. It remains unclear, however, why colonies frequently react to stressors by losing almost their entire adult bee population in a short time, resulting in a colony population collapse. Here we examine the social dynamics underlying such dramatic colony failure. Bees respond to many stressors by foraging earlier in life. We manipulated the demography of experimental colonies to induce precocious foraging in bees and used radio tag tracking to examine the consequences of precocious foraging for their performance. Precocious foragers completed far fewer foraging trips in their life, and had a higher risk of death in their first flights. We constructed a demographic model to explore how this individual reaction of bees to stress might impact colony performance. In the model, when forager death rates were chronically elevated, an increasingly younger forager force caused a positive feedback that dramatically accelerated terminal population decline in the colony. This resulted in a breakdown in division of labor and loss of the adult population, leaving only brood, food, and few adults in the hive. This study explains the social processes that drive rapid depopulation of a colony, and we explore possible strategies to prevent colony failure. Understanding the process of colony failure helps identify the most effective strategies to improve colony resilience.

Anaesthetising Drosophila for behavioural studies

The detrimental effect of anaesthesia by chilling or CO(2) on the mating behaviour of Drosophila melanogaster was investigated. Both agents significantly increased copulation latency, even when flies were given 20 h to recover from anaesthesia. CO(2) anaesthesia increased copulation latency more than anaesthesia by chilling. Delivery of a mechanical shock to the flies immediately before testing also increased copulation latency. These experiments demonstrate the sensitivity of insect behaviour to disruption by anaesthesia or rough handling. It is preferable to avoid anaesthetising flies that are to be used in behavioural studies.

The roles of dopamine and related compounds in reward-seeking behavior across animal phyla.

Motile animals actively seek out and gather resources they find rewarding, and this is an extremely powerful organizer and motivator of animal behavior. Mammalian studies have revealed interconnected neurobiological systems for reward learning, reward assessment, reinforcement and reward-seeking; all involving the biogenic amine dopamine. The neurobiology of reward-seeking behavioral systems is less well understood in invertebrates, but in many diverse invertebrate groups, reward learning and responses to food rewards also involve dopamine. The obvious exceptions are the arthropods in which the chemically related biogenic amine octopamine has a greater effect on reward learning and reinforcement than dopamine. Here we review the functions of these biogenic amines in behavioral responses to rewards in different animal groups, and discuss these findings in an evolutionary context.

Visual regulation of ground speed and headwind compensation in freely flying honey bees (Apis mellifera L.)

SUMMARY There is now increasing evidence that honey bees regulate their ground speed in flight by holding constant the speed at which the image of the environment moves across the eye (optic flow). We have investigated the extent to which ground speed is affected by headwinds. Honey bees were trained to enter a tunnel to forage at a sucrose feeder placed at its far end. Ground speeds in the tunnel were recorded while systematically varying the visual texture of the tunnel, and the strength of headwinds experienced by the flying bees. We found that in a flight tunnel bees used visual cues to maintain their ground speed, and adjusted their air speed to maintain a constant rate of optic flow, even against headwinds which were, at their strongest, 50% of a bees maximum recorded forward velocity. Manipulation of the visual texture revealed that headwind is compensated almost fully even when the optic flow cues are very sparse and subtle, demonstrating the robustness of this visual flight control system. We discuss these findings in the context of field observations of flying bees.

What insects can tell us about the origins of consciousness

How, why, and when consciousness evolved remain hotly debated topics. Addressing these issues requires considering the distribution of consciousness across the animal phylogenetic tree. Here we propose that at least one invertebrate clade, the insects, has a capacity for the most basic aspect of consciousness: subjective experience. In vertebrates the capacity for subjective experience is supported by integrated structures in the midbrain that create a neural simulation of the state of the mobile animal in space. This integrated and egocentric representation of the world from the animal’s perspective is sufficient for subjective experience. Structures in the insect brain perform analogous functions. Therefore, we argue the insect brain also supports a capacity for subjective experience. In both vertebrates and insects this form of behavioral control system evolved as an efficient solution to basic problems of sensory reafference and true navigation. The brain structures that support subjective experience in vertebrates and insects are very different from each other, but in both cases they are basal to each clade. Hence we propose the origins of subjective experience can be traced to the Cambrian.

Preimaginal conditioning in Drosophila revisited

During metamorphosis, the nervous system of a holometabolous insect changes significantly. Attempts to demonstrate preimaginal conditioning, here taken to mean the retention of learning through metamorphosis, have given mixed results. We used two behavioural assays (the T maze and trap assay) to see whether a change in adult responsiveness could be induced by exposing Drosophila melanogaster larvae to a conditioning stimulus. There was no evidence for preimaginal conditioning from either assay, but the trap assay demonstrated that menthol contamination from the larval environment on the puparial surface could induce a change in adult behaviour. Exposure of adult insects to this contamination could give the appearance of preimaginal conditioning, when in fact the behavioural induction occurred during the adult stage. Young flies responded less strongly than older flies to the odour cues in both assays. This may explain the apparently contradictory findings of some earlier studies of preimaginal conditioning. Copyright 1999 The Association for the Study of Animal Behaviour.