Frank Weihmann

Self-Assembly Processes in Honeybees: The Phenomenon of Shimmering

Giant honeybees, Apis dorsata, have evolved a plethora of defence behaviours that enable this lifestyle. Against predatory wasps, they display Mexican wave-like cascades of “shimmering” whereby hundreds of bees flip their abdomens upwards in a split second. Shimmering is a type of social defence that also has relevance for task partitioning, collective decision making and social communication. Shimmering also relies on unexplored principles of information transfer and is a compelling example of self-organisation. It addresses “proximate” questions (how does shimmering work?) and ultimate questions (why has shimmering evolved?) and, therefore, gives rise to the discovery of interdependencies between giant honeybees as prey and its predators as part of a “co-evolutionary arms race”. Here, we review the underlying mechanisms of the phenomenon of shimmering and prove some of its anti-predatory goals.

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

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.

Complex social waves of giant honeybees provoked by a dummy wasp support the special-agent hypothesis

The social waves in Giant honeybees termed as shimmering are more complex than Mexican waves. It has been demonstrated1 that shimmering is triggered by special agents at the nest surface. In this paper, we have used a nest that originated by amalgamation of two previously separated nests and stimulated waves by a dummy wasp moved on a miniature cable car. We illustrate the plausibility of the special-agent hypothesis1 also for complex shimmering processes.

Speeding Up Social Waves. Propagation Mechanisms of Shimmering in Giant Honeybees

Shimmering is a defence behaviour in giant honeybees (Apis dorsata), whereby bees on the nest surface flip their abdomen upwards in a Mexican wave-like process. However, information spreads faster than can be ascribed to bucket bridging, which is the transfer of information from one individual to an adjacent one. We identified a saltatoric process that speeds up shimmering by the generation of daughter waves, which subsequently merge with the parental wave, producing a new wave front. Motion patterns of individual “focus” bees (n = 10,894) and their shimmering-active neighbours (n = 459,558) were measured with high-resolution video recording and stereoscopic imaging. Three types of shimmering-active surface bees were distinguished by their communication status, termed “agents”: “Bucket-bridging” agents comprised 74.98% of all agents, affected 88.17% of their neighbours, and transferred information at a velocity of v = 0.317±0.015 m/s. “Chain-tail” agents comprised 9.20% of the agents, were activated by 6.35% of their neighbours, but did not motivate others to participate in the wave. “Generator agents” comprised 15.82% of agents, showed abdominal flipping before the arrival of the main wave front, and initiated daughter waves. They affected 6.75% of their neighbourhood and speeded up the compound shimmering process compared to bucket bridging alone by 41.5% to v = 0.514±0.019 m/s. The main direction of shimmering was reinforced by 35.82% of agents, whereas the contribution of the complementing agents was fuzzy. We discuss that the saltatoric process could enable the bees to instantly recruit larger cohorts to participate in shimmering and to respond rapidly to changes in flight direction of preying wasps. A third, non-exclusive explanation is that at a distance of up to three metres from the nest the acceleration of shimmering could notably contribute to the startle response in mammals and birds.

Evidence for Ventilation through Collective Respiratory Movements in Giant Honeybee (Apis dorsata) Nests

The Asian giant honeybees (Apis dorsata) build single-comb nests in the open, which makes this species particularly susceptible to environmental strains. Long-term infrared (IR) records documented cool nest regions (CNR) at the bee curtain (nCNR = 207, nnests > 20) distinguished by marked negative gradients (ΔTCNR/d < -3°C / 5 cm) at their margins. CNRs develop and recede within minutes, predominantly at higher ambient temperatures in the early afternoon. The differential size (ΔACNR) and temperature (ΔTCNR) values per time unit correlated mostly positively (RAT > 0) displaying the Venturi effect, which evidences funnel properties of CNRs. The air flows inwards through CNRs, which is verified by the negative spatial gradient ΔTCNR/d, by the positive grading of TCNR with Tamb and lastly by fanners which have directed their abdomens towards CNRs. Rare cases of RAT < 0 (< 3%) document closing processes (for ΔACNR/Δt < -0.4 cm2/s) but also suggest ventilation of the bee curtain (for ΔACNR/Δt > +0.4 cm2/s) displaying “inhalation” and “exhalation” cycling. “Inhalation” could be boosted by bees at the inner curtain layers, which stretch their extremities against the comb enlarging the inner nest lumen and thus causing a pressure fall which drives ambient air inwards through CNR funnels. The relaxing of the formerly “activated” bees could then trigger the “exhalation” process, which brings the bee curtain, passively by gravity, close to the comb again. That way, warm, CO2-enriched nest-borne air is pressed outwards through the leaking mesh of the bee curtain. This ventilation hypothesis is supported by IR imaging and laser vibrometry depicting CNRs in at least four aspects as low-resistance convection funnels for maintaining thermoregulation and restoring fresh air in the nest.

Intraspecific Aggression in Giant Honey Bees (Apis dorsata).

We investigated intraspecific aggression in experimental nests (expN1, expN2) of the giant honey bee Apis dorsata in Chitwan (Nepal), focusing on interactions between surface bees and two other groups of bees approaching the nest: (1) homing “nestmate” foragers landing on the bee curtain remained unmolested by guards; and (2) supposed “non-nestmate” bees, which were identified by their erratic flight patterns in front of the nest, such as hovering or sideways scanning and splaying their legs from their body, and were promptly attacked by the surface bees after landing. These supposed non-nestmate bees only occurred immediately before and after migration swarms, which had arrived in close vicinity (and were most likely scouting for a nesting site). In total, 231 of the “nestmate” foragers (fb) and 102 approaches of such purported “non-nestmate” scouts (sc) were analysed (total observation time expN1: 5.43 min) regarding the evocation of shimmering waves (sh). During their landing the “nestmate” foragers provoked less shimmering waves (relnsh[fb] = 23/231 = 0.0996, relnsh[sc] = 75/102 = 0.7353; p <0.001, χ2-test) with shorter duration (Dsh[fb] = 197 ± 17 ms, Dsh[sc] = 488 ± 16 ms; p <0.001; t-test) than “non-nestmates”. Moreover, after having landed on the nest surface, the “non-nestmates” were attacked by the surface bees (expN1, expN2: observation time >18 min) quite similarly to the defensive response against predatory wasps. Hence, the surface members of settled colonies respond differently to individual giant honey bees approaching the nest, depending on whether erratic flight patterns are displayed or not.

Training for Defense? From Stochastic Traits to Synchrony in Giant Honey Bees (Apis dorsata)

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.