By: Edward Balogh
Maybe the nurse bees start it all.
Dr. Tom Seeley (46) acknowledged and restated that “he would love to know how the bees decide when they are going to swarm”(3). The question has obviously been the subject of inquisitive beekeepers for many years, but as E.F. Phillips (17) notes in his 1915 Treatise on Beekeeping, “A discussion of the life of the honey bee and of the production of honey”: The simplest way to account for this phenomenon is to attribute it to “instinct” but…instincts are called into action only by definite conditions in the environment. There have been many hypotheses presented regarding the pre-swarm conditions that usually are singularly or in combination linked to the swarming process that follows. They still don’t identify the bee caste that by action starts the swarming process. Dr. Grozinger et al, (21) suggest that continued investigation at the genomic and physiological levels can help us to understand why only a small handful of individuals produce the key signals that coordinate the swarming process. Research supports an hypothesis that a quorum of nurse bees have a “distinct neurogenomic state” unique to them created by the multiple pre-swarm conditions in the hive similar to the genomic changes pointed out regarding scout versus nonscouts (28, 42) bees producing vibration signals versus those that do not (1), and bees departing with the swarm versus those staying in the hive (21). This quorum of nurse bees serves to establish a colony consensus that initiates the swarming process.
Narrative
In the Biology of the Honey Bee (66), swarming specifically describes a particular activity or event where a large number of bees leave a hive with the queen to establish a new colony. Fundamental to establishing a new colony is the rearing of a queen and consequently all swarming hypotheses describe conditions which result in queen rearing. The swarming phenomena has been an important topic of discussion for many years. The concept of splitting a colony was noted in a pamphlet “A description of the bar-and-frame hive” published in 1844 (34). Since the invention of the Langstroth hive design in 1851, and the associated wooden ware and frames, the ability to manipulate hives to avoid swarms became more feasible. Consequently, the management of swarms in turn led to more research to identify those conditions that precede swarming. This supports the goal of beekeepers to utilize this banked knowledge to take appropriate action to intercept and stop the swarming process. By doing so, the beekeeper’s investment in his hives is preserved. While a variety of techniques to inhibit swarming have been employed, none have been found to be unambiguously reliable (18, 10, 56, 58). As is discussed in Swarm Essentials (41) there are some general conditions that effect swarming which include abundance of resources, genetic strain, environmental conditions and the age of the queen. Abundance of resources includes a high number of young bees, large amounts of nectar and pollen, the presence of sealed virgin queen cells or actual virgin queens. Genetic race or strain of the honey bee is a factor. Some races have differing tendencies to swarm. Environmental conditions are determinant depending on local seasonal weather conditions. The age of the queen is a determinant in how much queen substance she produces because research suggests that older queens are more likely to swarm than younger queens (41).
In addition to the general conditions that correlate to a hive swarming, there are more specific hypotheses that suggest that these conditions, singularly or in concert, increase a hive’s propensity to swarm. In early research, as noted in “The Biology of the Honey bee”(59), was focused on explaining the initiation of queen rearing prior to a swarming. The nurse bee, or brood, food hypotheses (20, 32), states that a surplus of young nurse bees develops in pre-swarming colonies, resulting in an excess amount of brood food for which queen rearing is an outlet. Another, the colony congestion or crowding hypothesis (25,16) points out that crowding of adult workers and limited space for brood rearing results in the initiation of queen rearing. Neither of these hypotheses provided adequate proof to fully explain the initiation of queen rearing. Subsequent to these hypotheses, additional ones were developed. The following list, which while not inclusive, forms a representative sample: colony size, brood comb congestion, worker age distribution, reduced transmission of queen pheromones (18) and brood pheromone (60). The following is a synopsis of each of these hypotheses:
Colony size: Three aspects of colony size are important for the initiation of queen rearing: comb area, colony volume, and worker population. The area/volume threshold is 40L and 23,000 cm2 for European bees. Honey bees have an accelerated population growth following the Winter clustering period in the cold temperate climates. The critical threshold is at 12,000 bees, at which time queen rearing begins and the colonies swarm when the population reaches 20,000 workers. The most important aspect of the colony size is not the physical size of the nest, but the size of the active colony. European bees may construct enough to fill their cavities before swarming, although only 54-76% of that comb is used when the queen rearing begins (61). The first visible sign that a colony may be preparing to swarm is the production of queen cups – the first step in the queen rearing process. It is also possible for colonies to become congested, yet show no preparation to swarm, demonstrating that worker density and colony size are not sole deciding factors (53).
Brood comb congestion: There are two aspects of brood nest congestion which may be important stimuli to queen rearing: congestion of brood and crowding of adult workers. The effective brood nest is not the entire area of the drawn foundation in a hive, but only that area with the maximum number of cells occupied during a swarm cycle. Queen rearing is initiated coincidental with congestion in that area. At that time, 90-95% of all cells in the brood nest contain some stage of brood, and there are few empty cells in the brood nest for the queen to lay eggs (61). This necessitates an increase in nurse bees tending to the brood. In addition to the cells being occupied with brood, there may be a situation where foraging bees have started to store nectar and/or pollen in these same brood cells creating what is referred to as a “honey bound” hive. Interestingly and noteworthy, in colonies preparing to swarm, adult workers appear to crowd together in the brood area, even if additional space is available in the nest (53,65). This is because of the accelerated population growth and the effect of foragers pheromone that retards the normal temporal polytheism of nurse bees into foragers (22, 24) – thus creating a sub-caste imbalance adding to the brood area congestion.
Worker age distribution: A skewed worker age distribution is also associated with swarming: colonies preparing to swarm tend to have a large proportion of young bees (65). This phenomenon is likely caused by the emergence of large quantities of young workers from brood cells (19). In addition, the forager pheromone that retards the normal temporal polytheism of nurse bees into foragers increases the proportion of nurse bees (22, 24) compounding the problem. At the beginning of the growing season, the age distribution of a colony is greatly skewed towards older (≥24days old) workers. Gradually, as the older workers die and increasing numbers of eggs are laid develop into adults, and eclose to take their place, the proportion of younger (≤ seven days old) workers increases (18). However, adding a large amount of young workers to colonies does not reliably trigger swarming (52).
Reduced transmission of queen pheromones: The presence of a healthy queen is signaled throughout a colony by a combination of pheromones unique to the queen . . . the queen mandibular pheromone (QMP) and footprint pheromone. There is no difference in the production of one queen pheromone, (QMP) or 9-ODA, between queens in colonies preparing to swarm and those that are not (48) which suggest that it is the transmission of queen pheromones which is reduced rather than the queen’s pheromones output prior to queen rearing (62). There is a difference in the amount of QMP produced by young queens and older queens and this may explain the tendency for older queens to swarm more readily than young queens. In addition, the congestion in the hive from an unusually large mix of nurse bees, particularly crowding the brood area, limits the queens mobility within the hive and thus is another factor interfering with the transmission of her QMP pheromone. In addition to the QMP pheromone influencing the swarming process, the queen has what has been labeled her “footprint” pheromone which is produced in the queen’s tarsal glands and may be involved in the suppression of the first stage of queen rearing associated with swarming, cup construction (64) in a congested state, the queen’s mobility is limited and in turn the footprint pheromones distribution. When a combination of mandibular and tarsal gland extracts were applied to the bottom edges of comb in overcrowded colonies, the construction of queen cups was inhibited (27). Neither of these secretions affected queen cup construction when applied separately. It should be noted that the presence of the queen and her QMP message slows the ontogeny from hive tasks to foraging (37). This could be traced by the QMP acting to inhibit the juvenile hormone production to regulate the rate at which workers progress from within-nest to outside tasks (43) thus increasing the disproportionate mix of nurse bees to worker bees.
Brood pheromone shift: A “two-way primer” model (7,35) hypothesizes that brood pheromone may both accelerate and decelerate the transition to foraging depending on the physiological state of the individual worker bee. Additional studies suggest that young and old brood release different chemicals which have opposing effects on the behavioral maturation (29). Furthermore, bees reared in the presence of low levels of BEP (Brood Ester Pheromone) behaved more like foragers in a sucrose response assay, while bees reared with higher levels behaved more like nurses (36). Consequently, the nurse bees inhibited behavioral maturation adds to the nurse bee imbalance and/or the earlier maturing of foragers are added without effectively being able to add a proportionate amount of nectar or pollen to the hive because of its honey bound state.
All of the above hypotheses have established virtual thresholds which probabilistically correlates with the commencement of swarming. An alternative explanation for the inability to these hypothesis to support a single mechanism suggests that instead of being causal triggers, the hypothesized mechanisms are simultaneous artifacts (i.e. correlates) of the actual mechanistic cause of swarming. That is, there may be a single underlying mechanism coincident with the above mentioned factors (18). Lengefelder (26) summed up several of the already known theories of the origin of the swarming fever and concluded none of the theories was quite complete and formulated a new theory, i.e. the so-called theory of latent swarm workers that are formed in the colony a few weeks before swarming. What he considered important was the ratio of the brood, house bees and foraging bees. None of them, however, offer to identify the bee caste that would most likely take the lead in orchestrating the swarming process. This hypothesis suggests that it is a worker bee and that it is a quorum of nurse bees that act to initiate the swarm.
Consideration must be given to all three bee castes – the drone, queen and worker. Very few pheromones are known in the drone and most are linked to sexual features. This reflects the minor role of males in honey bee society, almost entirely limited to the mating function (33). Since the drone does not demonstrate any active role in sustaining the colony, the drones’ involvement in swarming would be inconsequential.
The queen is most typically identified by beekeepers as being responsible for starting the swarming process. It is understandable because the queen is involved in several functional or pheromonal-influenced actions during the pre-swarm process. Consideration has to be given specifically to her involvement in the proposed pre-swarm hypotheses previously noted.
Colony size: The queen must be capable of producing brood at a rate that will sustain the hive. The success will result in producing enough worker bees to gather and store sufficient quantities of both nectar and pollen to sustain the hive’s continued rejuvenation during the temperate climate as well as through the following cold weather when the hive will cluster. As noted above, the consequences of a large population correlates with a swarming event when populations reach prescribed historical thresholds. Exceeding the swarming population threshold of bees is an unintended consequence, and not necessarily an intent of the queen to promote a swarm. The size of the population also does affect the transmission of the QMP throughout the hive and this in turn, adds to the pre-swarm inclination of the bees – they are no longer inhibited by the QMP from queen rearing.
Brood comb congestion: The situation directly affects the egg laying rate of the queen. The diminished brood area that can effectively be employed by the queen to lay eggs has been reduced significantly by the ramping up of her egg laying during the Spring buildup and the fact that during the nectar flow, the foragers are starting to utilize the loosely defined brood area to store nectar in addition to the increased level of pollen necessary for the increasing number of brood. Again, the queen must throttle back her egg laying rate, and contend with the honey bound state that the hive is in. In addition, the increased number of worker bees, both foragers that have stopped foraging because of limited storage space and nurse bees that have disproportionately increased in numbers as a function of the increased egg laying rate of the queen and the maturation to foragers being delayed by both brood pheromone (36) and forager pheromone effect (43). The queen’s mobility is affected by the crowding and her egg laying diminished considerably. Other queen related swarming consequences, describe the queen’s subordinate role during the swarming process. It has been observed that the queen does not lead the swarm from its parental but is instead pushed out of it by workers(53). Furthermore, the queen is evaluated and if the consensus decides she cannot reproduce in a swarm hive, she will be superseded during swarm preparation(67). Frustrated swarms (those that cannot “coerce” their queen to swarm because she is clipped) often kill the queen in an attempt to rear one that can fly (14).
Worker age distribution: There is a disproportionate mix favoring young/nurse bees developing during the pre-swarm process. The nurse bees are the primary distributor of the QMP. It is done on a worker-worker contact. QMP influence is dependent on direct contact with the worker bees and is not transmitted by sight, scent or sound (25). Because the nurse bees are not as mobile because of congestion, the transmission of the QMP and the footprint pheromone of the queen is reduced and sporadic, which results in a significant pre-swarm condition conducive to queen rearing.
Reduced transmission of queen pheromone: As noted above, the dosage and transmission of the QMP and the footprint pheromone are a consequence of hive conditions, which the queen cannot control at this point in the pre-swarm state.
Brood pheromone shift: Brood comb congestion is a consequence. The decreasing percentage of eggs and in turn young brood, shifts the effect of the pheromone to produce workers with behavioral tendencies like nurse bees. This would increase the proportion of nurse bees in the hive to foster a swarming mix which is composed of a large contingent of nurse bees. The queen has no role in this shifting population mix until she can resume her full rate of egg laying.
Based on the above, the queen is not at any point starting the swarming process. The regulation of queen activity during colony reproduction may, therefore be controlled largely by workers that normally have little contact with queens, but help to formulate colony reproductive and movement decisions(44). The worker bee cast, and the nurse bee sub-cast specifically, is in a convergent position in all of the hypothesis to take action. Again, consider the pre-swarm condition hypotheses.
Colony size: The colony size must be populated with enough bees to support both the primary and swarm hives. Worker age is the major factor determining which workers will remain in the nest and which will issue with the prime swarm (8, 31, 57). Young workers have a higher probability issuing with swarms than older workers, and up to 70% of workers less than 10 days old leave with swarms of temperate-evolved bee races (63). This would correlate with the excess of nurse bees proportionately in the primary hive prior to the swarm lift off. Evidence supports the nurse bee cast as being in the best position to access the proper colony size and caste mix for swarming.
Brood comb congestion: Obviously, the nurse bees are focused on the brood nest area and can best respond when unusual conditions are present. The fact that the queen’s egg laying has slowed down, the proportion of capped brood to egg/larval state and the shifting of brood ester pheromone from the young brood dosage to the higher old brood dosage are cues that a shift from a preferred state had taken place (22). In addition, workers may be able to assess the queen’s egg laying rate directly (30).
Worker age distribution: Nurse bees have established a large proportion of the colony population as compared to foragers. With this large nurse sub caste and the resultant diminished transmission of the QMP, the number of nurse bees uninhibited to queen rearing grows quickly, and the further increase in nurse bee population induces a rapid shift from high to low in the equilibrium proportion of the inhibited nurses (4). The mix of nurse bees and their distinctive physiological JH factor between nurse bees that swarm and those that stay supports a genetic shift theory of “swarm bees” (2). Nurse bees tend to crowd themselves on the combs (15). Taranov (55) concluded and Butler (8) and Simpson (52) agreed that as pre-swarm conditions advance, nurse bees become displaced from the brood nest in ever increasing numbers and become differentiated from the colony as “swarm bees” i.e the bees which form 70% the swarm when it departs (63).
Reduced transmission of queen pheromone: The diluted effect of the queen pheromone, both QMP and Footprint, liberates worker bees on the periphery of the hive to produce queen cups. The nurse bee proportion of the population is significant and being dispersed throughout the hive, can best assess the multiple pre-swarm conditions and take action to initiate the swarm.
Brood pheromone shift: As noted above, the mix of brood, when egg laying by the queen has been reduced because of brood comb congestion, results in the brood pheromone concentration promoting the worker bee behavior with nurse bee sub-caste tendencies increasing the nurse bee proportion of the worker bee population predicted in pre-swarming hive conditions.
Consistent with the above observations, Fefferman and Starks (18) considers, “It is likely that honey bees use pheromones to determine whether their colony is large, congested, or has a skewed worker age distribution.” It is clear that worker behavioral development, which leads to the typical honey bee age polyethism, is a complex and flexible process, involving more than one stimulus. The combined effect of queen signals, worker pheromones (ethyl oleate), and brood pheromones results in a plastic modulation of worker activity that is able to adapt worker response to the needs of the colony, which vary depending on colony developmental stage and environmental factors( 7,11).
There are several sub-castes which are formed during the swarming process. The swarm hive site search scouts – a sub-caste of forgers, the worker bees that put the queen on a diet and exercise her – a sub-caste of house bees, the bees that vibrate her prior to hive departure and of course the division of the population into those that swarm and those that stay – both sub-casts of house bees. This supports the formation of a sub-cast of nurse bees proposition. It is likely that the regulation of worker behavioral development is primarily modulated by the workers themselves, since the artificial alteration of worker demography is effective in changing age polyethism development even with constant presence of the queen (22, 23). It is by now well known that such group-level decisions are the result of the individual insects acting mainly on local information obtained from the interactions with their peers and their immediate environment (5, 6, 9) – a decentralized decision model. In the context of collective decision-making, positive feedback allows the selection of a particular option to cascade through the group, as the growing number of adherents to an option increases its attractiveness to undecided members. Moreover, this initiative behavior often takes a step-like form, with an individual’s probability of selecting an option changing sharply when the number of like-minded conspecifics crosses a threshold. Here we refer to this functional form as a quorum response, following well-studied cases in which threshold group sizes trigger key changes in behavior (39,49). Empirical evidence, at least in the case of honey bees Dr. Seeley (50,51) concludes that unanimity is not what triggers a consensus choice, instead, a final choice is made once the number of agents in favor of a particular option reaches a quorum (12,54). As the dilution of the QMP liberates worker bees from the inhibiting influence, the nurse bees also are liberated at a distance from the queen. A group or quorum of nurse bees could undergo a physiological shift in neurogenomic state which is the precursor to initiating the swarming process (21). The worker bees in various sub-cast tasks can assess the “abnormal” conditions present in the hive and colony ontology. Dr. Seeley (47) notes that when a worker bee processes the information in a signal, she often integrates the signal information with a large amount of contextual information. The conditions noted above are evaluated by the nurse bees and process the pre-swarm conditions. They integrate this information with a large amount of contextual information and a quorum starts to build throughout the hive. The formation of the swarm queen cups, which is the first sign of swarming and is a genetically programmed response to the diminished effect of the reduction in QMP throughout the hive (38), is the last pre-swarm cue that a quorum of the sub-cast of nurse bees assesses and conclude that the conditions are appropriate to swarm. The quorum threshold having been reached, a consensus choice follows, and the colony now moves forward and initiates the swarm preparation. Exactly how bees sense a quorum remains an enigma. They may use visual, olfactory or even tactile information. This remains a subject for future study (45).
The direct preparations for swarming begins two to four weeks before the swarm issues (64). The preparations are described in detail in Honey Bee Democracy (51), Swarm Essentials (40) and The Hive and The Honey Bee (13).
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