Guard Bees and the Hive Entrance

Guarding as a Specialisation of Middle-Aged Worker Bees

In beekeeping circles, we speak highly of the nurse bees (less than 7 days of age) and foragers (over 21 days of age), rarely of the multi-specialist middle-aged bees. These workers are undertaker bees and corpse cleaners, store & process forage, aid in ventilation, produce wax, build comb and guard the hive, amongst other specialisations within their age bracket.

Once the colony meets its basic survival, it turns to expansion and defence. Guard bees patrol at the hive entrance and surrounds to inspect incoming bees. If a forager bears the colony’s “scent” (pheromones), she is allowed entry, and denied if she does not (with exceptions). If an intruder tries forcing their way in, guards expose their sting chamber to release the alarm pheromones, priming their nestmates for defence.

Several defensive tactics exist, depending on the situation. How do bees know which method is right? Moreover, how does the colony know when to assign guards? Are these guards a special caste of bees who are adapted to the frontlines? This article focuses on guarding in European honey bee subspecies. Guarding in African bees has some overlaps, but these colonies guard for longer and are more aggressive in their response to intruders (Breed et al., 2004).

What are Guard Bees Doing at the Hive Entrance?

To the untrained eye, guard bees appear to lounge around. The literature describes it as “commonly seen sitting at the hive entrance in a characteristic stance, their forelegs off the ground and their antennae pointing forward… When very excited, their mandibles open and their wings are held away from their body, ready to fly towards any intruder” (reviewed in Nouvian et al., 2016). Guards are there to check on the incoming worker bees – are these friends or foes?

Nestmate Recognition: You Shall Not Pass…

Pheromones on the bee exoskeleton are used in nestmate recognition, and this signature distinguishes nestmates from non-nestmates. Nestmates will have the same cuticular hydrocarbon “smell” as the hive, informing the guards that she is a friendly bee. Signorotti and colleagues describe this as a “label” and “template”– the scent of incoming bee (“label”) is matched against the colony odour (“template”; reviewed in Signorotti et al., 2015). Guards develop their template from the wax comb (which is an extension of the queen and brood pheromones), and compare incoming workers against it.

Newly-emergent bees produce their own cuticular hydrocarbons based on their genetics (Signorotti et al., 2015). As they spend time in the hive, they pick up the “hive scent”; by the time they commence foraging, they can recognise and be recognised by guard bees.

…But You Can Pass if you Beg Hard Enough

A foreign bee that acts submissive is more likely to be accepted (observed by Butler & Free, 1952). These bees will stop at the entrance and allow guards to thoroughly inspect her with their antennae and mouthparts. If a foreigner had nectar loads, she would prove it to the inspectors, signalling “usefulness” and increasing her chance of being accepted. I have seen cases where the bee is accepted but was “carded” by the guards – having the golden hairs on her body removed. According to my beekeeping club, this is a returning robber, and the act of removing its hairs is a “atonement for her sins”.

When might this begging situation happen? One example is a crowded apiary – a forager may find herself landing at the wrong hive and has to make amends in order to be allowed in¹. Another scenario is during a beekeeping inspection- suppose some bees fall off the frame and outside the hive. Odds are these workers are nurses or middle-aged bees who had not been outside for their orientation flights. Lost and disoriented, they would walk back to the nearest hive, and if it is a stranger’s hive, would beg their way in, rather than remain exposed in the landscape. They are not harmed by the guard bees, as they treat their low-levels of “foreign” cuticular hydrocarbons as harmless (Signorotti et al., 2015).

What if Guards Make Mistakes?

The scents of nestmates and non-nestmates can overlap, leading to an acceptance error by the guard bees. This is not an issue, as the occasional drifter can be adopted into a new hive.

Modelling work by Reeve labelled two types of errors: rejection errors, where nestmates are classified as intruders, and acceptance errors, where intruders are classified as nestmates (Reeve, 1989). Of those, acceptance errors are the most common. It’s not the guards who make mistakes, rather the intruder who tricks them into thinking they’re one of them.

One such example are the cuckoo bumble bees (subgenus Psithyrus; reviewed in Lhomme & Hines, 2019). These parasites invade the nests of other bumble bees to lay eggs, whereby the host colony unknowingly rears the bee’s offspring. The larvae grow and consumes the host’s resource, including the larvae, leading to eventual colony collapse.

Likewise, Varroa jacobsoni, the less destructive cousin of V. destructor, has a cuticular hydrocarbon profile similar to its host Apis mellifera bees (Nation et al., 1992). These mites obtain chemical camouflage either passively from close contact with adults and larvae, or actively via feeding on bee fat body tissue (Ramsey et al., 2019). A total of 91 compounds were shared between V. jacobsoni and A. mellifera, with mites having slight differences in their proportions (Martin et al., 2001). This imperfection could be why bees can detect and remove V. jacobsoni more readily, and why it is (relatively) less harmful than V. destructor.

When Does a Worker Bee Become a Guard?

In other insects like ants and termites, the defensive (“guard”) members are distinct – solider castes are physically larger and can have specialised features like larger heads. Honey bees show no such thing, and throughout a worker’s life it can be a nurse, a guard, an undertaker, and a forager. This does not make bees less effective at hive defence, for the colony’s strength is in its coordination and communication.

Guarding is performed by middle aged bees around 7-22 days of age (Moore et al., 1987). Workers below that age range are the cleaners and nurses, whereas those above are foragers. When bees performed guarding, they did so for a few days, rather than the entire the duration of their middle-aged life. The longest guard period by a single bee was six days, and even then, the behaviour of this bee was no different than her nestmates (in other words, it did not act any different or “specialised”).

Moore and colleagues used Seely’s hypothesis (“complex tasks that require learning will be performed for longer periods of time by fewer bees”; Seeley 1983) to assume that a small group of workers would perform guarding activities due to its complexity, and were proven wrong (Moore et al., 1987). What we consider as a “complex task” not the case for bees – each colony’s guard count was determined by its aggressiveness; more aggressive bees meant more guards at the hive entrance.

The number of bees assigned to guarding has been contested- Moore and colleague suggest only 10-15% of middle aged bees become workers at any given time, and this is based on the genetic makeup of the colony (Moore et al., 1987). However, Unger & Guzman-Novoa suggest that guarding isn’t as rare as we think it to be (Unger & Guzman-Novoa, 2012). Over the ~10-day period of observation, they found 42% of middle-aged bees to engage in guarding.

What Cause Colonies to Assign Guard Bees?

Two major factors drive guard bee assignment, genetics and environmental conditions:

• “Genetics”, in that more aggressive colonies will assign more guards.
  • In European bees, aggression did not influence guarding duration, rather its frequency.
• “Environmental”, as in during periods of dearth or when there is an increased risk of robbing
  • Not just from honey bees- there are other insect predators (hornets) who raid hives for their stores when other food is scarce

In times of abundance, a colony reduces the number of guard bees, reassigning them to other tasks like nectar processing or water receiving (reviewed in Nouvian et al., 2016).

Can a Colony’s Guarding Behaviour Increase Over Time?

We already know that hives engaged in robbing have more guards and foragers, to the point where the guards become aggressive to their returning nestmates (Grume et al., 2021). When a colony becomes a robber, it is also more likely to be robbed- while its workers are raiding elsewhere, it puts at itself at risk of being robbed by another colony, leading to the downward spiral of robbing one another to death. In the aforementioned paper of Grume and colleagues,, there is a “switch” in the worker bees’ brains, increasing the expression of genes associated with aggressive behaviour.

In the short term (i.e. late summer/autumn dearths), a colony may go from “docile” to “highly aggressive” when engaged in robbing. By winter, they would probably return to normal behaviours, assuming that the robbers are not themselves destroyed. Likewise, after disturbances (for example, a rough hive inspection), the number of guards increases for a short time, returning to normal levels after a few hours.

I wonder if guarding behaviour can be learnt? Supposed colony A received frequent (but not destructive) predatory attacks and colony B received none. By the same time next season, would colony A show increased guarding behaviour? Maybe. Alas, I could not find a literary reference.

Honey bees have been shown to be capable of associative learning at the individual level (Gould & Towne 1988). What at the colony level though? Unlikely, for it would require genetic changes in the queen that would then be passed onto her eggs. Over many generations, these adaptations would give rise to that new behaviour…  basically evolution via natural selection at work.

Nest Defence: Alarm Pheromones and Preparation for Stinging

During hive defence, guard bees raise their abdomen and expose the sting chamber along with alarm pheromones- fanning their wings to disperse these volatile components inside the hive. The compounds signal actual or perceived dangers to the colony, and are released not just when exposing the stinger, but also during the act of stinging like a beacon towards the enemy’s location.

Alarm pheromones are produced by the Koschevnikov gland and gland-containing areas around the sting sheath. The active component of the sting alarm pheromone is isopentyl acetate (“IPA”); its release alerts workers to commence defensive behaviours. The concentrations of IPA are negligible in queens, and slowly develop in worker bees, peaking at 2-3 weeks of age when they begin guard duties (Allan et al., 1987). IPA is the main active component, but not the only one – others like 2-heptanol or 2-nonnal can trigger defensive behaviour; the complete alarm pheromone is a blend of over 40 compounds.

Genetics of Guard Bees

It’s no surprise that gene expression is involved in division of labour. Guard bees had a higher number of genes related to stinging and guarding² (Arechavaleta-Velasco et al., 2003). Within the guarding traits, the gene sting-1 was involved in both stinging and guarding, whereas sting-2 and sting-3 where more associated with guarding. A combination of these genes (along with other factors like hormones), contributes to the aggressiveness and guarding behaviours in colonies.

Frontline Workers: Reduced Immune Systems?

For an overview of the individual bee immune system, read here

As guards interact with foragers, they are also exposed to pathogens carried by the returning bees. This suggests that guards would require a heightened immune system to avoid infection. Cappa and colleagues found otherwise: guards had a reduced immune response relative to their nurse bee counterparts (Cappa et al., 2020). The authors provided two hypothesises:

• Since guard bees are actively patrolling and have altered aggression-associated hormone levels (higher juvenile hormone & lower vitellogenin; Pearce et al., 2001), then energy is allocated away from the immune system as guarding is physiologically demanding, or
• Guarding is not a risk to overall hive health, and most bees guard for 1-3 days (as covered above), so it does not require an enhanced immune system. Further, these guards do not return to in-hive duties after guarding (Moore et al., 1987).

In preparation for guarding, the worker bee’s immune system transitions into a midpoint between nurse and forager bee (Cappa et al., 2020). Consider that nurse bees need a heightened immune system³ as tending to the queen and brood is a delicate task – should one a member of the queen’s retinue be infected, then Her Majesty would succumb to it. Likewise, should a brood be infected and transfer the disease to the adult nurse, then she would spread it to her hivemates.

These results are in line with the “social immunity” phenomenon (Cremer et al., 2018) – individuals working at the centre “core” of the colony have the most efficient immune systems (nurses), and this progressively lowers as they work outside of it (foragers).

Bonus: Guard Formations in Apis cerana– Arms and Tails

Swarms of A. cerana are often attacked by hornets in their native Asian range. Predators approach as the swarm rests on a tree and attempt to hunt the worker bee. In response to the siege, the swarm begins “shaking”, and exposing the Nasonov gland (Robinson 2013). This alerts the rest of the colony into defensive formation, such as the “tail”, (whereby 20 to 200 bees hang below the cluster), or an “arm”, where that same number of workers stretches along the branch. At these extensions, the bees shake and snap at the predator in unison in an attempt to protect the main cluster. Tails form when the hornets hover, and arms when the hornet walks up the branch and onto the swarm.

Arm and tail formation is constant during hornet attacks, and hornets prefer engaging these “decoy” extensions; perceiving the fewer bees to be an easier target. As such, the colony achieves its purpose drawing attention away from the queen and scout bees as they continue searching for a new home.

Why Aren’t There Guard Bees Inside the Hive?

Guarding the hive entrance evolved in response to the environment. When an intruder seeks to attack a beehive, they do so from the entrance. Honey bees did not evolve around beekeepers, and do not post guards in the event someone decides to remove a chunk out of their “hollow cavity”. Predatory exceptions exist, such as species woodpeckers drill into the hives and eat bees from the outside, yet the majority of predators approach from the front, and that is where evolution worked to establish guards.

When you’re attacked by bees during an inspection, it is from the foragers acting either in “self defence” or after being alerted by their guard bees. This is partly why we smoke the hive entrance – it stops guards from alerting the rest of the hive to the intrusion. Want to avoid getting stung during inspections? Wear the right gear. Want to avoid aggressive bees? Requeen your hive with a gentler stock and inspect carefully. Use a smoker, and make sure the weather is right for it.

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Footnotes

1. For those wondering why the bees doesn’t take off and relocate her proper home, that is a mystery to me to… is she too heavy/tired to fly again? Has she forgotten where she belongs or gotten the scents mixed up? Perhaps she accepted her fate? ↩︎
2. Quantitative trait locus (“QTL”) are measurable regions of DNA associated with a specific trait and influenced by multiple genes and environmental factors. QTLs determine the genetic basis of complex traits like guarding or undertaking or honey production, comparing the how much of the variation is due to genetic factors vs environmental influences. ↩︎
3. This doesn’t mean that foragers have a “weak” immune system– it’s all relative. For example, if nurse bees had a 9/10 immune system, then foragers be a 7/10. Not “low” by any standards, only “lower” than the nurse bees. Maintaining an immune system is energy-intensive, and the forager would receive greater benefits by allocating that energy elsewhere (e.g. flight muscles). ↩︎