Direct and Indirect Messaging Within the Hive
Signals are a form of communication that directly alter the behaviour of the receiver, whereas a cue is a feature of the environment that guides an organism’s behaviour. In the honey bee colony, signals range from the waggle dance to pheromones, whereas cues are more complex. An example cue is that the more rejections a water-foraging bee gets from the receiving bees, the less likely the colony needs water, and so the forager interprets it as a cue to stop gathering water.
Signals are derived by evolution. One signal gives one outcome, every time. Cues are coincidental information that has been wired in as a byproduct of the signal and environment. Cues are subjective – the same cue can be interpreted differently by two different organisms on the basis of context and prior experience. In the water forager example above, if she instead unloaded the water right at the hive entrance, then the cue is reinterpreted as “the colony is desperate, I must gather more water”.
Mechanical Communication Through Vibrational Signals
Mechanical communication transmits information through physical interactions (e.g. “shaking” the queen for weightloss) or vibrations (“dances”). These signals coordinate the complex behaviours within the hive, such as foraging and swarming.
The Shaking Signal – Time to Work
The shaking signal is when one worker bee grasps another and rapidly shakes their body from side to side (Nieh, 1998). Foragers are the one who do most of the shaking, delivering a general message of “we need workers elsewhere”, or “time to do even more work”. During dearths, these shakes are correlated with its duration – the longer the dearth, the longer the shaking; triggering bees to move faster and “prepare for greater foraging activity”.
When foragers shake other foragers, they are priming their nestmates for additional trips. Biesmeijer notes that the successful foragers perform this signal, and it is more common after times of poor conditions, like dearths or bad weather (Biesmeijer, 2003). Most shakes occurred early morning – inside, near the hive entrance (“the waggle dance dance floor”). Nieh suggests that they are reporting the foraging status of the previous day – very similar to the dorsoventral vibrations covered below (Nieh, 1998).
In the afternoon, most shaking occurred on combs above the dance floor, as there were less foragers at on that floor. These happened in the absence of forage, and are assumed to signal the “end of the work day”, directing nectar receivers to reduce their activity. “If they are typically unable to gather food after time X on each day, then on subsequent days they could save energy by reallocating resources to other activities after time X” (Nieh, 1998).
Dorsoventral Abdominal Vibration (DVAV) – Prepare for Takeoff, or, More Foraging
Both the shaking signal and DVAV are similar. I will paraphrase Nieh’s words to distinguish between the two: the shaking signal moves her entire body, whereas the DVAV is as the name implies, only shaking the abdomen up and down (Nieh, 1998). DVAV is more relevant to swarming, whereas the shaking is more about foraging.
Scout bees perform DVAVs. The signalling bee grasps onto other bees and rapidly vibrates their abdomen, signalling an upcoming action for a swarm. Visscher and colleagues’ research showed that the signal can “activate bees for takeoff”, as in a departing swarm, or trigger scout bees to search for a new hive site (Visscher et al., 1999).
DVAVs are constantly produced, from when the cluster first forms, until it departs. The peak of vibration activities occurred between 30-60 minutes prior to swarm flight, ceasing after takeoff. This is the basis of Tom Seely’s “piping hot bees” and “boisterous buzz runners” – these bees use DVAVs to signal the stages of swarming, from first landing to first (and final) departure. Without DVAVs, swarm departure times significantly increases, and depending on the vibration intensity, it can cause the swarm to abandon their takeoff attempt altogether (Donahoe et al., 2003).
Dorsoventral Vibrations & Foraging
DVAVs can adjust worker activity in response to the colony’s needs, such as increasing foraging or labour reallocation (Reviewed in Schneider & Lewis, 2004). When bees receive a DVAV, in 10-25% cases they are prompted to gather more food. Five aspects are suggested for DVAV function:
Resuming foraging activities after a period of dearth,
Following along with waggle dancers,
Signalling a need for new sources of nutrition (likely in times of monofloral diets or in diseased states),
Looking for higher quality food (not always restricted to monofloral diets), and
Indicating a change in forage availability over time.
Like the shaking signal, DVAVs are at their highest during the morning, and low during the afternoon (Reviewed in Schneider & Lewis, 2004). It keeps a colony’s foragers informed and prepared for the day ahead. The bees performing DVAVs are those who were successful in the previous day, and the more DVAVs in the morning, the more waggle dancing to follow. Seeing this from an observational hive can informed whether the colony is on a nectar flow or when a large number of flowers are in bloom.
The Waggle Dance – Locating Forage
Books have been written about the waggle dance, and I refer you to them for further reading. In short, the waggle dance is how foragers convey information about the location, distance, and quality of a food source. It is a series of movements performed on the comb in a “dance floor”, or designated section of the hive, consisting of:
The straight run, in which the dancer waggles her abdomen while moving in a straight line. The angle of this run indicates the direction of the forage relative to the sun.
The duration of this round dance conveys the forage’s distance. The longer it is, the further away the forage (Wario et al., 2017).
The return, in which the dancer loops back to the starting point, creating a figure-eight pattern.
When a forager discovers a profitable food source, she returns and performs the waggle dance to recruit other foragers to that location. The intensity and duration of the dance is determined by the resource’s quality. A higher nectar or pollen concentration will lead to more intensive dancing than your 25L bucket of sugar syrup… unless it’s a dearth (Reviewed in Dong et al., 2023).
Primarily, the waggle dance is about recruiting foraging bees to gather more food at that indicated location. This communication helps the colony allocate foraging efforts, so that workers collect food from the most profitable locations, rather than a free-for-all foraging spree. Social learning plays a role in the dance: Workers who observe experienced dancers prior to performing their first dance produced more accurate dances compared to those without such an opportunity (Reviewed in Dong et al., 2023).
Beyond the visual, further signals in the form of chemical substances are released by the dancing bee (Thom et al., 2007). Thom & colleagues found that the tergal glands of waggle-dancing bees release four cuticular hydrocarbons: tricosane, pentacosane, Z-(9)-tricosene and Z-(9)-pentacosene. Non-dancing bees do not release this, and when researchers artificially injected the dance floor with these compounds, more bees left the hive compared to controls, searching for forage that does not exist.
Finally, the dance language is used in the swarm decision making. A scout bee will advertise potential nesting sites to the swarm and recruit bees to that location. Should the home be suitable, then more workers will dance in favour of that location, until a quorum1 is reached, and the bees fly to that location.
The Tremble Dance as a Stop Signal
When the colony is overwhelmed with nectar deposits, returning foragers produce a “stop signal” – a short vibration from flight muscle contraction while butting against a waggle-dancing bee (Nieh, 1993). This is the colony’s negative feedback loop, informing the advertising foragers that “we have too much to handle”, reducing the number of foraging bee and enabling the nectar-receivers to manage their workload.
Most stop signals came from the tremble dancers, who moved throughout the hive in a disorganised manner in shaking and trembling movements; The tremble-dancing bee aims to stop the waggle dancer. Nieh reports that a sufficiently large number of tremble dancers must be present for the waggle dance to stop (Nieh, 1993).
Further, he noted that stop signals are also conducted by foragers returning from crowded sugar feeders. Overcrowding leads to bees fighting bees from other colonies, and the defeated ones return to signal the end of forager recruitment to that particular sugar feeder (Nieh, 2010). The tremble dance as a defensive measure for foragers is also observed by the aggressor hive when they engage in robbing behaviour. If robber bees are repelled by the defending hive, they return with tremble rather than waggle dances against this “dangerous” location.
Cues: an Individualised Response to the Environment
Cues are subjective. They are a byproduct of the environment and past experiences. Several cues in bees and hymenopterans are discussed below.
Colony Thirst and Water Foraging
Water is always available to foragers, unlike nectar, which changes throughout the day. When bees experience a hot day and the demand for water increases, water-collectors gather water and readily offload to receiving bees. How does the water collector know when to stop? No signal is given to her from the receiving bees, rather it is the “disinterest” of those in-hive bees to her water loads that cues her as to when less water is required.
Each time a water collector returns to her hive, she gets an update on the colony’s thirst status via her offloading speed. However Kuhnholz & Seeley found that it was the number of rejections from the receivers that cued foragers to stop gathering more water (Kuhnholz & Seeley, 1997). It was not the time it took her to unload, nor the number of receiving bees, nor the time it takes her to find a water receiver. The forager could not sense that the hive temperature had decreased – instead she relied on a sizeable number of rejections2 by receiver bees (>10) to cease her water collection.
Sensing a Nectar Flow
Flowers bloom and go, sugar syrup stays. How do foragers know when a nectar flow is on, and when to stop gathering syrup? Initially, it was thought that when syrup foragers experienced a delay in unloading their nectar, it suggested “a higher quality nectar is available” (plain sugar syrup is worse than junk food). However Seeley showed that it is the quantity, not quality of nectar that tells a colony when it’s a nectar flow (Seeley, 1989 & Seeley et al., 1991).
The authors experimented with two feeders. One feeder had there times as many foragers visiting than the other (North 90 vs South 30). They found that when the bees at the north feeder were “jailed” (in ziplock bags), more foragers began dancing in support of the south feeder – their logic being “less nectar is coming from the north, therefore the south must be a nectar flow). The south source did not change at all, only the number of foragers returning from the north; it was enough information for the colony to conclude a “nectar flow is on”.
Responses to Carbon Dioxide
Seeley reports that air quality in weak hives is worse than strong ones (Seeley, 1974). Smaller hives have less workers available for fanning and air circulation, leading to an increase in carbon dioxide levels – up to 4.25% (by contrast, fresh air is 0.04%). Bees are tolerant of high CO2 levels, and what cues them to start fanning is a certain threshold of CO2, rather than the loss of oxygen.
When nitrogen gas was added to displace the oxygen, the bees did nothing – went about their business until they dropped. They did not sense the drop in oxygen nor the introduction of a foreign gas, as a need for fanning. However, when CO2 was introduced, it recruited more fanning at the hive entrance. The increase in CO2 cued bees to ventilate. By contrast, if it were a signal, any foreign gas that displaced oxygen (i.e the nitrogen above), would have triggered fanning (Seely, 1974).
Bumble Bees Communicate Cues Using Footprint Pheromones
Saleh & colleagues who found that bumble bees leave footprint pheromones everywhere they go, providing a cue for other forager bees (Saleh et al., 2007). The contents of each footprint secretion was unchanged between foraging sites, the nest entrance or neutral sites (empty plastic containers). The authors conclude that the individual bee will assign different meanings to each footprint and location based on context and experience.
The Importance of Cues in Locating the Nest Entrance
Scent-based cues for wild-nesting species have been suggested as an alternative method for locating nests. Consider that bumble bees nest in the ground, a landscape that changes throughout the weeks. Returning forager bees cannot rely on visual cues every time, and thus use chemical substances to determine nest location (Foster and Gamboa 1989). The bees can distinguish between pheromones produced by nestmates, other bees in the same species, or even insects other species.
Vespine wasps also deposit chemical substances to mark their nest entrance. What distinguishes a cue from a signal is that if the wasps deliberately secreted these pheromones as markers, then only the scent of a few individuals is required to indicate the entrance, hence a signal. By contrast, the German wasp Vespa germanica, required hundreds of worker trails are in order to mark a site as the colony entrance (Jandt et al., 2005)3.
Pheromones as Chemical Signalling
Adapted from Honey bee pheromones
Pheromones are a chemical signal secreted by a nestmate to trigger a specific reaction to the colony members. In honey bees, there are “primer” and “releaser” pheromones. Primer pheromones are compounds that impact the bee’s physiology (e.g. suppression of worker egg laying), whereas releaser pheromones influence their behaviour (e.g. increased pollen forage). Each caste produces pheromones, including the brood.
By contrast, the absence of chemicals (cuticular hydrocarbons) from a dead bee’s body signals that this is a corpse. In life, these carbon-based compounds are constantly being produced and as part of the chemical signatures used in nestmate recognition.
Brood Pheromones to Signal Hunger & Suppress Worker Ovaries
“Brood pheromone” is a blend of 10 fatty-acid esters, with each compound being individually capable of triggering a degree of brood pheromone effects on adult bees (Le Conte et al. 2001). One signal of brood pheromone is “hunger”. Upon detection, nurse bees are prompted to feed the larvae (bee bread or nectar), and foragers begin gathering pollen (Pankiw et al., 1998 & Pankiw, 2004). A combination of brood and queen pheromones contributes to the inhibition of worker bee ovary development. This prevents the emergence of egg-laying workers and maintains order in the hive; the colony’s resources are dedicated to rearing bees from queen-laid eggs.
Queen Pheromones for Colony Cohesion
Most of the queen’s pheromones overlap in signalling her presence and suppress the workers (her daughters) from laying eggs.
The major colony pheromone is the queen mandibular pheromone, which maintains colony cohesion and signals Her Majesty’s presence. During mating flights, the virgin queen relies on queen mandibular pheromone (specifically its component 9-ODA) to signal her location for the drones. The presence of both brood and queen pheromone concentrations help suppress worker ovaries.
Queen retinue pheromone combines with queen mandibular pheromone to form the queen’s attendees – those worker bees who groom and feed her. Her Dufour’s gland is a marker of fertility, tied to the strength of her ovarian development was.
The queen’s abdominal tergal glands are thought to be complementary to queen mandibular pheromone, assisting in worker bee attraction. Likewise, her tarsal gland (foot) also secrets compounds that signal her presence to the hive, and stops the construction of queen cups (Lensky & Slabezki, 1981).
Worker Bee Pheromones: Foraging, Swarming, Defence…
Worker bees communicate A LOT, and pheromones are one half of the equation. Books have been written about their Nasonov gland and its roles in swarming, hive entrance marking, identifying foraging sources, and helping the queen find her way back home. Unlike their long-distance Nasonov gland, forager bees use their tarsal glands to mark high-yielding flowers to other foragers. Their mandibular gland produces 2-heptanone, used to immobilise invaders that are too small to sting (Varroa mites, wax moth larvae).
The scent of 2-heptanone is part of the alarm pheromone, along with their sting & Koschevnikov glands. Alarm pheromones are produced by the Koschevnikov gland and gland-containing areas around the sting sheath. During defence, guard bees appear at the hive entrance, raising their abdomen and exposing the sting chamber to release alarm pheromones. They fan their wings simultaneously, dispersing the volatile components and signalling actual or perceived dangers to the colony.
Evolutionary Signals and Cues in Bee Life
Insect communication is a mix of pheromones, vibrations and the environment. Signal are shaped by evolution in response to an unchanging environment- each signal gives an expected outcome. Once the environment changes, then it becomes a matter of context and experience to determine a bee’s new role in the hive.
A high number of footprint pheromones at a grassy patch suggests a hive nest entrance, whereas the same footprint pheromone on a flower patch tells other bees that another bee was here. The honey bee dance language signals profitable forage, whereas the associated vibrations tell colony members to prepare themselves for the day ahead, or the end of business.
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Footnotes
- Unlike consensus, quorum is when a threshold is reached by certain number bees, triggering the swarming reaction. In contrast, a consensus would require the vote of every single bee before moving out. You can see the inefficiency of getting a verdict out of 10,000 bees – so bee swarms evolved to find their new home via quorum – if a certain number of workers vote “yes”, then it’s good enough for everyone! ↩︎
- Even when water is required, some receiving bees reject the water forager if they are allocated to the task of nectar receiving. Nectar processing does not stop, for there is never enough honey for the bees. ↩︎
- Think of it this way – if only a few wasp markings triggered the cue, then it would be indistinguishable from a rich foraging site or a source of water. When hundreds of wasp imprints are present, it must mean the nest entrance, as no foraging site would be able to accommodate for such a large amount of foragers within a small area. ↩︎