How to Join a Wave: Decision-Making Processes in Shimmering Behavior of Giant Honeybees (Apis dorsata)

Institute of Zoology, University of Graz, Graz, Austria.
PLoS ONE (Impact Factor: 3.23). 05/2012; 7(5):e36736. DOI: 10.1371/journal.pone.0036736
Source: PubMed


Shimmering is a collective defence behaviour in Giant honeybees (Apis dorsata) whereby individual bees flip their abdomen upwards, producing Mexican wave-like patterns on the nest surface. Bucket bridging has been used to explain the spread of information in a chain of members including three testable concepts: first, linearity assumes that individual "agent bees" that participate in the wave will be affected preferentially from the side of wave origin. The directed-trigger hypothesis addresses the coincidence of the individual property of trigger direction with the collective property of wave direction. Second, continuity describes the transfer of information without being stopped, delayed or re-routed. The active-neighbours hypothesis assumes coincidence between the direction of the majority of shimmering-active neighbours and the trigger direction of the agents. Third, the graduality hypothesis refers to the interaction between an agent and her active neighbours, assuming a proportional relationship in the strength of abdomen flipping of the agent and her previously active neighbours. Shimmering waves provoked by dummy wasps were recorded with high-resolution video cameras. Individual bees were identified by 3D-image analysis, and their strength of abdominal flipping was assessed by pixel-based luminance changes in sequential frames. For each agent, the directedness of wave propagation was based on wave direction, trigger direction, and the direction of the majority of shimmering-active neighbours. The data supported the bucket bridging hypothesis, but only for a small proportion of agents: linearity was confirmed for 2.5%, continuity for 11.3% and graduality for 0.4% of surface bees (but in 2.6% of those agents with high wave-strength levels). The complimentary part of 90% of surface bees did not conform to bucket bridging. This fuzziness is discussed in terms of self-organisation and evolutionary adaptedness in Giant honeybee colonies to respond to rapidly changing threats such as predatory wasps scanning in front of the nest.


Available from: Gerald Kastberger
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    • "The multiple goals of defence of shimmering The wave-like shimmering in giant honeybees (Seeley et al. 1982; Oldroyd and Wongsiri 2006; Woyke et al. 2006; Kastberger et al. 2012, 2013a, b) is a collective action of the bees on the nest surface with the potential to repel predatory wasps (e.g. the autochthon species of Vespa orientalis, V. tropica, Vespa mandarinia). Such wasps usually hover or scan in front of the bees' nest, preying on the stationary curtain bees or ambushing homing or departing forager bees in flight (Kastberger et al. 2008, 2011a). "
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    ABSTRACT: The open nesting behaviour of giant honeybees (Apis dorsata) accounts for the evolution of a series of defence strategies to protect the colonies from predation. In particular, the concerted action of shimmering behaviour is known to effectively confuse and repel predators. In shimmering, bees on the nest surface flip their abdomens in a highly coordinated manner to generate Mexican wave-like patterns. The paper documents a further-going capacity of this kind of collective defence: the visual patterns of shimmering waves align regarding their directional characteristics with the projected flight manoeuvres of the wasps when preying in front of the bees’ nest. The honeybees take here advantage of a threefold asymmetry intrinsic to the prey–predator interaction: (a) the visual patterns of shimmering turn faster than the wasps on their flight path, (b) they “follow” the wasps more persistently (up to 100 ms) than the wasps “follow” the shimmering patterns (up to 40 ms) and (c) the shimmering patterns align with the wasps’ flight in all directions at the same strength, whereas the wasps have some preference for horizontal correspondence. The findings give evidence that shimmering honeybees utilize directional alignment to enforce their repelling power against preying wasps. This phenomenon can be identified as predator driving which is generally associated with mobbing behaviour (particularly known in selfish herds of vertebrate species), which is, until now, not reported in insects. Electronic supplementary material The online version of this article (doi:10.1007/s00114-014-1220-0) contains supplementary material, which is available to authorized users.
    The Science of Nature 08/2014; 101(11). DOI:10.1007/s00114-014-1220-0 · 2.10 Impact Factor
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    • "First, mechanical cues provoked by shimmering may be important for the rapidness of the wave propagation across the nest. Alternative strategies eventually processed by visual cues among adjacent neighbours, utilising stigmergic (Grasse 1959; Kastberger et al. 2013) principles, such as bucket-bridging (Kastberger et al. 2012) or eavesdropping (Peake 2005; Jones et al. 2011), would be much slower by one or two orders of magnitude than those which are actually observed in shimmering (Kastberger et al. 2012, 2013). The saltatoric principle of wave propagation (Kastberger et al. 2013), which may speed up the wave from a basically bucket-bridging process by a factor of 3, is supposed to be associated to the visual input of threatening cues and to the mechanical effects of the shimmering waves in the bee curtain. "
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    ABSTRACT: Giant honeybees (Apis dorsata) nest in the open and have developed a wide array of strategies for colony defence, including the Mexican wave-like shimmering behaviour. In this collective response, the colony members perform upward flipping of their abdomens in coordinated cascades across the nest surface. The time–space properties of these emergent waves are response patterns which have become of adaptive significance for repelling enemies in the visual domain. We report for the first time that the mechanical impulse patterns provoked by these social waves and measured by laser Doppler vibrometry generate vibrations at the central comb of the nest at the basic (=‘natural’) frequency of 2.156 ± 0.042 Hz which is more than double the average repetition rate of the driving shimmering waves. Analysis of the Fourier spectra of the comb vibrations under quiescence and arousal conditions provoked by mass flight activity and shimmering waves gives rise to the proposal of two possible models for the compound physical system of the bee nest: According to the elastic oscillatory plate model, the comb vibrations deliver supra-threshold cues preferentially to those colony members positioned close to the comb. The mechanical pendulum model predicts that the comb vibrations are sensed by the members of the bee curtain in general, enabling mechanoreceptive signalling across the nest, also through the comb itself. The findings show that weak and stochastic forces, such as general quiescence or diffuse mass flight activity, cause a harmonic frequency spectrum of the comb, driving the comb as an elastic plate. However, shimmering waves provide sufficiently strong forces to move the nest as a mechanical pendulum. This vibratory behaviour may support the colony-intrinsic information hypothesis herein that the mechanical vibrations of the comb provoked by shimmering do have the potential to facilitate immediate communication of the momentary defensive state of the honeybee nest to the majority of its members. Electronic supplementary material The online version of this article (doi:10.1007/s00114-013-1056-z) contains supplementary material, which is available to authorized users.
    The Science of Nature 05/2013; 100(7). DOI:10.1007/s00114-013-1056-z · 2.10 Impact Factor
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    ABSTRACT: In Giant Honey Bees, abdomen flipping happens in a variety of contexts. It can be either synchronous or cascaded, such as in the collective defense traits of shimmering and rearing-up, or it can happen as single-agent behavior. Abdomen flipping is also involved in flickering behavior, which occurs regularly under quiescent colony state displaying singular or collective traits, with stochastic, and (semi-) synchronized properties. It presumably acts via visual, mechanoceptive, and pheromonal pathways and its goals are still unknown. This study questions whether flickering is preliminary to shimmering which is subject of the fs (flickering-shimmering)-transition hypothesis? We tested the respective prediction that trigger sites (ts) at the nest surface (where shimmering waves had been generated) show higher flickering activity than the alternative non-trigger sites (nts). We measured the flickering activity of ts- and nts-surface bees from two experimental nests, before and after the colony had been aroused by a dummy wasp. Arousal increased rate and intensity of the flickering activity of both ts- and nts cohorts (P < 0.05), whereby the flickering intensity of ts-bees were higher than that of nts-bees (P < 0.05). Under arousal, the colonies also increased the number of flickering-active ts- and nts-cohorts (P < 0.05). This provides evidence that cohorts which are specialist at launching shimmering waves are found across the quiescent nest zone. It also proves that arousal may reinforce the responsiveness of quiescent curtain bees for participating in shimmering, practically by recruiting additional trigger site bees for expanding repetition of rate and intensity of shimmering waves. This finding confirms the fs-transition hypothesis and constitutes evidence that flickering is part of a basal colony-intrinsic information system. Furthermore, the findings disprove that the muscle activity associated with flickering would heat up the surface bees. Hence, surface bees are not actively contributing to thermoregulation.
    Insects 08/2012; 3(3):833-856. DOI:10.3390/insects3030833
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