1. Introduction
Giant Honey Bees (
Apis dorsata) are famous for being the most dangerous stinging insect on earth [
1,
2,
3,
4,
5]. However, they are also known for traditional honey hunting and they generate fascination in the scientific community for the multifaceted collective behaviors of their colonies [
4,
6,
7]. Giant Honey Bees are social insects with open-nesting behavior [
8,
9,
10]; they attach their nest with single central semicircular combs beneath tree branches, rock spurs or house balconies [
6,
10] and orient one of their nest planes to the direction of the sun [
9]. They provide unique opportunities to investigate sophisticated collective behaviors which are otherwise, in particular in cave-nesting honeybees (for example in the Western Honey Bee,
A. mellifera), cryptic for the observer. Giant Honey Bees display swarm behavior in migration [
11,
12,
13,
14], reproduction [
15], and defense [
4,
5,
16]. A striking example of collective defense in Giant Honey Bees is shimmering [
1,
2,
3,
7,
10,
17; movie 1]. Shimmering is accomplished mostly by mid-aged Giant Honey Bees at the quiescent zones of the nest surface [
18] and may therefore constitute a prominent example of division of labor in honeybees [
19,
20]. Its seemingly wave-like visual pattern repels predators such as wasps, which are the major threat of Giant Honey Bees [
7,
10].
In addition to this highly coordinated shimmering, Giant Honey Bees also display flickering [
4,
7,
21,
22] in various behavioral contexts, which represent a collective trait associated with abdomen flipping movements or the movements being singular actions. Flickering displays a diffuse stochastic activity, which can evolve into transient quiescence or shimmering [
4]. It seems from visual observation that flickering surface bees flip their abdomens independently, each bee with a different and unsynchronized flickering rate and intensity compared to its neighbor. Up to now, the phenomenon has only been observed in Giant Honey Bees (
Apis dorsata,
A. laboriosa) and is only roughly described and termed in literature as
dorso-ventral abdomen flipping [
21,
22]. We prefer the term
flickering over the use of (
dorso-ventral)
abdominal flipping since the latter also encompasses a series of other activities in Giant Honey Bees. For instance, Giant Honey Bees use abdominal flipping to divert water droplets away from the nest after exposure to rain [
4], to fan the nest [
7,
9,
23,
24,
25], and to perform waggle and tremble dances [
26,
27]. It is also the main behavioral component of shimmering [
28], and is observed in rearing up [
16,
29]. Rearing up behaviors typically occur following arousal by either mechanical vibrations of the nest or by sudden approaches of birds, big game, and humans in proximity of the nest.
Visual observations suggest that flickering does not occur strictly stochastically. Rather, it appears that some areas of the nest surface display activities with higher rates and intensities, which suggests a semi-stochastic or semi-synchronous aspect to flickering. However, we do not know the extent to which the flipping movements in flickering are controlled by random processes or carried over the nest surface in a certain order. It is also unknown whether flickering is affected by the ability of Giant Honey Bees to either modify the rate and strength of their collective behaviors in response to a rising threat, as documented for shimmering waves [
30], or to recruit defenders [
7,
31].
In this contribution, we aim to determine under which conditions and to which extent flickering shows random distribution over a patterning that is more lumped in space and time. A deeper understanding of the flickering behavior should come from simultaneously studying properties of the nest surface associated with the generation of shimmering waves. We already know that shimmering waves are initiated by cohorts of bees at specific trigger sites at the nest surface, which also control the propagation of shimmering in response to threatening cues in a wavelike pattern [
28]. Parental shimmering waves are generated or triggered (or re-triggered, producing daughter waves) primarily through visual pathways [
10,
17] while wave propagation is predominantly mechanoceptively controlled [
30] and mediated by bucket-bridging strategies from one surface bee to the adjacent one [
17].
It seems that both modes of social coordination of a Giant Honey Bee colony,
i.e., flickering and shimmering, are subject to modification under threat [
7]. In particular, the control of intensity and rate of flickering and shimmering often coincide, which allow us to propose that while the colony shifts from the flickering mode to shimmering, it brings the colony’s intrinsic coordination from stochasticity to synchrony. This is subject of the
flickering-shimmering transition hypothesis. Consequently, we monitored Giant Honey Bee colonies over longer intervals under two arousal conditions, (a) when the colony was quiescent or only occasionally disturbed by natural cues, and (b) when the colony was repetitively exposed to a dummy wasp. We then focused on one of the main potential aspects of the interrelationship between flickering and shimmering and compared the expression of flickering patterns with respect to the trigger sites (
ts) and non-trigger sites (
nts) which are, per definition, associated with shimmering. The
flickering-shimmering transition hypothesis could be accepted under the following two conditions: (a) if the flickering activity of
ts would be significantly more strongly affected by an external threat than those of
nts. This would mean that the flickering activity correlates with the arousal state of the surface bees positioned at the
ts, which is the key condition for generating shimmering waves; furthermore (b), if the flickering activity of
nts also grades, although less, with the arousal state of the colony. This would mean that
nts switch to trigger mode. This would increase the numbers of
ts recruiting generator agents for intensifying strength and rate of shimmering which finally lowers the threshold levels for defensiveness.
Movie 1. Shimmering behavior in Giant Honey Bees. The movie shows the expN1, which was attached to the roof of a residential house in Chitwan, Nepal. The movie was recorded with a HD camera at a frame rate of 25 Hz. Above the nest was a black-and-white striped computer controlled dummy wasp, itself mounted on a cable-car device. The dummy wasp provoked shimmering waves. The mouth zone is still at a nascent stage.
Movie 2. Flickering behavior in Giant Honey Bees. The movie shows expN1 during the non-arousal phase, i.e., before the stimulation started. The nest, including the mouth zone, was quiescent and mostly undisturbed, with only a few small shimmering waves provoked by natural cues (not shown). The spatial distribution of flickering behavior is clearly visible. The higher flickering rates are observed in the upper and concave region to the left side of the nest.
Movie 3. Infrared movie of shimmering behavior in Giant Honey Bees. Detailed illustration of abdominal flipping bees at the expN2 during shimmering. Left, HD-image; right, infrared image (in color palette rain900) in temperature range of 20 °C – 40 °C. Infrared recordings convincingly showed that abdominal movements do not alter the body temperature of the surface of the bees during shimmering. Due to the disparity in frame rate (50 Hz and 9 Hz for HD and IR, respectively) the frames are neither congruent nor warp-free. The conversion factor is 9:1. The thorax of a highly flickering active bee was marked by yellow full circle. During the wave episodes, the dot is displaced by a yellow rectangle because thorax detection was difficult. Red patches reflect movements of single bees at the nest surface which were identified by image analysis (see Methods). The dark shadow in some IR frames originates from the cable car dummy. Numbers refer to frame and time (in s) information.
Movie 4. Infrared movie of flickering behavior in Giant Honey Bees. Detailed illustration of abdominal flipping of bees at the expN2 during flickering. Left, HD-image; right, infrared image. The same bee is marked as in movie 3. Infrared recordings showed that flickering movements do not alter the body temperature of surface bees. During the flickering episodes, the flickering active bee was marked by a yellow rectangle. More details are shown in additional movie 3.