Division of labour in a colony: Who does what?

Kayla deJong, TTP Summer Technician

Early Life and the Teenage Days

Honey bees have long had an industrious reputation, as their colonies are very complex with an overwhelming number of different activities being carried out simultaneously. The ease of which the thousands of bees in any single colony synergistically cooperate and contribute to each other’s needs has led to the perspective of honey bees as a “superorganism,” wherein individual bees and their colony contributions are comparable to those of cells or organs within a larger organism (Seeley 1989). Indeed, individual honey bees are not self-sufficient and instead exhibit a high level of task-specialization and interdependence. But rather than viewing a colony as “one organism”, let’s break down the many moving parts within the hive and look at the role of individual bees….

 

Division of labour between castes:

A normal colony consists of one queen, 300-500 drones, and 10,000-60,000 workers (Gruszka 1998). All three castes are necessary for the functioning of a colony, but the labour is definitely not divided evenly! Reproductive activities are the responsibility of the queen and the drones, while nearly all other tasks are the responsibility of the many workers.

The Queen – ruling the colony, but only kind of

A queen typically lives for about two years but can live up to five years (Gruszka 1998). Although not genetically different from female workers, the royal jelly diet provided by workers leads queens to develop into reproductive individuals. In natural succession, multiple queen cells are usually built and a newly-emerged queen’s first responsibility will be to eliminate potential competitors for the “throne” – the earliest emerged queen stings other queen cells. From days 5-10, a virgin queen will go out on one or more mating flights and mate with several (on average 7-17) drones (Winston 1987). Eggs will be first seen around 12-21 days following a queen’s emergence and thus begins a lifetime of egg-laying – up to 2000 eggs are laid every day, although a break in brood production occurs in winter (Page & Peng 2001).

It is easy to view the queen as a ruler of the hive as similar to a human head of state – after all she is the queen. However, honey bees are a little more complex. Outside her reproductive role, a queen also plays a highly important part in regulating the colony t

 

Through her pheromone scents, which prevent construction of new queen cells, suppress worker ovary development and stimulate foraging (Gruszka 1998). Through these measures a queen practices some level of control over her hive’s environment, but workers in turn also influence a queen’s behaviour. For example, when a queen’s pheromone no longer reaches all workers in a crowded colony, workers will initiate swarming behaviour: building queen cells for the queen to lay in, seeking out new homes, and lessening queen feeding in preparation for departure. Another example: the queen is able to selectively fertilize her eggs and thus controls the sex ratio of her offspring (with unfertilized eggs becoming drones and fertilized eggs resulting in workers), but this decision is made on the basis of the cell size that a queen lays into, which is determined by workers who will only construct drone comb at seasonally appropriate times.  Of course, workers also have the final say in a queen’s acceptance – a queen of poor quality will be killed and replaced.

The Drones: One Job

A drone’s sole purpose in life is to mate with a queen, which is most common in the spring when drones leave the colony in large groups and congregate, attracted by a queen’s mating pheromone. Drones are reproductively mature around 7 days of age and can live to thirty days or longer, but die immediately after mating (Rangel & Fisher 2019). Drones do not contribute to the colony in any other way and must even be fed by worker bees. As winter approaches, worker bees will push drones out of the colony – resources are no longer abundant enough to feed the free loaders!

The Workers: It’s in the name

 

Every other task in the busy hive falls to the workers. In other social insects, such as ants and termites, physical differences between workers establish which task an individual carries out – this type of division of labour is known as morphological polytheism (Johnson 2010). For example, leaf-cutting ant workers are born into three distinct size classes which determines their role in the colony – the smallest care for the young, the largest harvest plant material, and the medium-sized build and defend the nest (Boulogne 2014). However, honey bee exhibit temporal polytheism, wherein workers graduate to different functional tasks as they age, according to a set developmental pattern (Johnson 2010). Changes in a worker’s behaviour throughout their lifespan are most evident, but important temporary physical changes (such as development of certain glands) do occur and are highly important, even if they are not evident externally.

In the summer, there are four different age categories of workers:

1. Cell cleaners
2. Nurses
3. Middle-aged bees
4. Foragers

In this issue we will discuss the roles of the first two age groups: cell cleaners and nurses. We will dive into the tasks carried out by the older bees next month, and also briefly touch on winter bees and the importance of healthy age structures for colony wellbeing. But for now, the baby bees!

Cell cleaners – days 0-4

A bee’s first task after emerging is to clean the cells immediately in the area she just emerged from (Winston 1987). For the first 3-4 days of their lives these “baby bees”, recognisable by their pale, fluffy hair, continue to clean out cells and remain in the brood nest. This may not be a highly specialized task, as bees of other age groups can and do clean out cells (Johnson 2010), but it remains an important one – brood comb is reused for years and general cleanliness is important for reducing disease transmission across generations (Wagoner et al. 2021). Fifteen or more workers will contribute to the clearing of a single cell and all together it takes about 40 minutes for the average cell to be fully cleaned (Winston 1987). These clean brood cells that are ready for the queen to lay in have a distinctive polished and shiny look that is particularly visible in older comb held to sunlight.

Like most insects, wings must dry and harden before flight is possible. Bees carrying out in-hive tasks will rarely fly, but an individual’s earliest orientation/defecation flights may occur in the first 9 days her life (Herold & Borei 1963). Such early flights are “short-range” – bees remain in the immediate vicinity of the hive and fly slowly, memorizing the appearance and location of their home (Degen et al. 2015).

Bees also cannot effectively sting at emergence – it takes 1-2 days for the exoskeleton, including the skeletal area around the sting glands to harden (Winston 1987). However, young bees will begin to accumulate the compound promellitin in their venom sacs during the cell cleaning life stage (Bachmayer et al. 1972). After day 3, conversion of promellitin to millitin, the primary poisonous component of bee venom, will begin to occur Bachmayer et al. 1972) – now they are able sting and hit you with venom!

Newly emerged bees do not begin their lives with the hive-specific pheromone scent that honey bees use to distinguish nestmates from intruders but will obtain this pheromone through interactions with the older bees that feed, groom and brush by them (Breed 2004). Contact with the food-provisioning nurse bees is also important for early physiological development – newly emerged bees reared without nurse companionship have been shown to have smaller hypopharyngeal glands (important for future brood feeding) and lower protein content throughout their bodies, demonstrating the continued importance of worker jelly after emergence (Naiem et al. 1999).

Nurse bees – days 4-12

The nursing stage of a bee’s life lasts about a week and revolves around brood care. The most important physiological attribute of nurses are the developed hypopharyngeal glands, which are located in the head and are responsible for the addition of protein to the brood food that nurses produce (Corby-Harris and Snyder 2018). A diet of pollen (stored and fermented in the hive comb into “bee bread”) is critical for young bees to promote the growth and activity of these glands (Herbert et al. 1970). Newly emerged bees will start nibbling on small amounts of pollen, but it is in the nursing stage that pollen consumption reaches a lifetime high (Crailsheim et al. 1992). Nurses are physiologically equipped for such a diet as they produce special enzymes to efficiently digest large amounts of pollen (Crailsheim et al. 1992). The pollen diet of nurses is why healthy colonies will store pollen on or near to brood comb in the spring and summer. Colonies with insufficient pollen availability will have poorly fed nurses and poorly fed brood, which will affect the overall colony health as malnourished bees have greater susceptibility to diseases and reduced ability to grow and develop as they age (Di Pasquale et al. 2013).

The nursing temporal caste can be farther divided into two stages. From days 4 to 6 of their adult lives, nurse bees feed the colony’s older larvae with worker jelly – a mixture of honey and pollen, with some glandular secretions added in for good measure (Winston 1987). By day 7, a worker’s hypopharyngeal glands are fully developed and at their peak size, and she now transitions to feeding highly proteinaceous royal jelly secretions to worker and drone eggs (up to 3 days post laying) or to queen larvae if present (Melliou & Chinou 2014).

Nurse bees are receptive to many chemical and pheromonal signals emitted from the brood, including the brood’s age, whether a larva “feels” hungry, and whether food levels have diminished in a cell (Huang & Otis 1991). Brood cells are inspected regularly by nurses according to these stimuli, but nurses appear not to immediately respond to individual signals, instead continuing inspections to ensure efficient allocation of resources (Huang & Otis 1991). An interesting study from the 50s found that over the course of 272 hours, an individual larva is inspected an average 1926 times, but fed only 143 times (Lindauer 1953). Nurses cap the brood cells with papery substance (created from remnants of old pupal cocoons mixed with wax) as individual brood reach the appropriate age (Winston 1987).

In addition to caring for the brood, nurses also do the lion’s share of feeding the adult bees in the colony. Although older worker bees do feed honey or nectar to one another, their hypopharyngeal glands have shrunk and no longer produce worker or royal jelly (Crailsheim 1998, Corby-Harris and Snyder 2018). Foragers are also not able to digest pollen as efficiently as nurses because the necessary enzymes are no longer be produced in high amounts (Crailsheim et al. 1992), so the easily digestible worker jelly provisioned by nurses is a better way for older bees to obtain much-needed protein (Crailsheim et al. 1992). The worker jelly also spreads fast as recipient workers go on to share it with other bees! Additionally, the quality and quantity of worker jelly spread throughout the hive informs foragers about the colony’s pollen needs (Crailsheim 1998).

 

Care for the queen falls to the nurse bees as well. The queen’s retinue (or “court”) is largely composed of early-stage nurses (days 3-9) and is not a set group, but rather consists of up to 12 bees in her vicinity attracted to pheromones secreted from her mandibular glands (Seely 1979, Naumann et al. 1991). The retinue is responsible for feeding and grooming the queen and is also largely responsible for redistributing her pheromone throughout the colony, which inhibits queen cell production and worker ovary development. Part of the “retinue response” to the queen’s pheromone signals is to lick and touch antennae to her (collecting pheromone from her body), followed by immediate self-grooming (spreading pheromone over one’s own body) and an approximate 30 minute “messenger” period of movement and frequent contact with nestmates (spreading pheromone over colony) (Naumann et al. 1991, Seely 1979). This is a highly effective game of “telephone”: bees already start to perform behaviours associated with queenlessness 30 min after a queen’s removal and the inhibition against building queen cells has worn off by the tenth hour (Velthuis 1972, Seely 1979).

The retinue is also eager to offer food to the queen, who will be fed as frequently as five times an hour in peak egg laying times (Velthuis 1972, Crailsheim 1998). When preparing to swarm, nurses and other workers will no longer feed her – she needs to become slimmer to fly!

Adulthood and Old Age

Middle-aged bees (MABs) – days 12-21

”]Middle-aged bees (MABs) are the final age group to carry out in-hive tasks. Although MABs frequently overlap nurse bees in distribution and also interact with foragers far more than nurses do, the tasks they do are distinctly different – and also make up quite the long list!

Younger MABs (days 12-17) carry out comb building and general colony maintenance tasks (Johnson 2010). At this age, the four wax glands that workers have on the underside of their abdomen have matured and are at their peak size. These glands secrete liquid wax, which hardens when exposed to air (Winston 1987). Workers scrape the wax scales they have produced off their abdomen with their hind legs and pass it forwards along their pairs of legs before placing the wax in their mouth (Winston 1987). After chewing the wax until pliable, the MABs carefully craft the distinctive hexagonal cells that honey bee colonies are known for.

The plastic frame foundation commonly provided in managed colonies provides bees with head start in their building activities. However, natural comb built in feral colonies (or in pesky open spaces in your boxes) requires more planning on the part of the bees – this can be seen in bees’ abilities to festoon into long chains to measure spaces or provide “scaffolding”, the fact that comb is often started in multiple places and later joined, and the construction of gradual gradients of cell sizes to allow for a seamless transition between worker and drone comb (Smith et al. 2021). Construction of new honey comb is dependent on the rate of nectar flow into the colony (evaluated through the number of nestmates offering nectar food) as well as the fullness of existing honey comb (evaluated through cell inspections); comb construction is energetically costly and if both above conditions are not met, bees will shift their efforts to other tasks (Pratt 2004). If needed, food in the brood nest can be relocated to provide a queen with more cells to lay in, and the building of drone comb is seasonal and dependent on the amount of existing drone comb (Pratt 2004).

As bees age, they begin to do tasks nearer to the hive entrance. Slightly older MABs are occupied with nectar reception from foragers and the production of honey. Returned foragers will pass their loads of nectar to MABs around the hive entrance. If there are not enough nectar receivers, impatient foragers will recruit more through the tremble dance (Seeley 1992). Nectar laden MABs will either immediately feed nestmates, or travel to the hive’s combs to deposit into a cell. The fast-walking bees seen on brood or honey frames can be assumed to be MABs making the long trek (in bee terms) to the honey supers – no other task specialization sees movement through the entrance area, brood nest and honey combs. Once choosing a cell, the worker bee manipulates the liquid drop in her mouth for about 20 minutes – repeatedly swallowing and regurgitating the droplet while exposing it to air and adding glandular secretions (Seeley 1995). Her hypopharyngeal glands have atrophied since the nursing stage of her life, but they are now put to a new use: creating enzymes that break down sugars and produce hydrogen peroxide, which prevents the honey from spoiling (Corby-Harris & Snyder 2018, Seeley 1995). Multiple bees will deposit nectar in a single cell, where it continues to ripen as the moisture content is reduced – fanning behaviour also speeds up evaporation. It the responsibly of the slightly younger, wax-producing MABs to cap honey cells, which they do in batches.

Older MABs (middle-aged bees) also play an important role in regulating hive temperature. When clustered together, bees are very good at keeping each other warm. But during high temperatures, a sort of air conditioning system must be employed. MABs will partake in organized fanning throughout the hive, but especially the at the entrance – rapidly flapping their wings while standing still to circulate the air (Southwick & Heldmaier 1987). You can see this yourself on hot summer days! Foragers will also bring back water and pass it on to the receiver bees, who then distribute drops throughout the brood nest and the rest of the colony, which cools the hive through evaporation and prevents brood from drying out (Southwick & Heldmaier 1987).

Thermoregulation is most important in the brood nest, where brood survival requires temperatures of 33-36°C (Seeley 1985). Although all bees contribute to colony heating by having thorax temperatures above 35°C, some “heater” bees specialize in transferring body heat to brood, generating heat by vibrating their flight muscles and repeatedly pressing their warm thorax against capped pupal cells while standing still (Bujock et al. 2002). Therefore, while some bees you see standing still on your brood comb may indeed be taking a break, many may still be hard at work! Bees of any age group can practice this behaviour, but MABs frequently carry it out, often while making circuits to deliver nectar obtained from foragers or honey cells to other bees on the brood comb (Basile et al. 2008).

Other MABs may specialize in hygienic behaviour – the removal of dead or diseased pupae (Arathi et al. 2003). One subset of bees is responsible for detecting and uncapping diseased pupal cells, while another pulls out the pupa and drops them to the colony floor, and yet another (older) category specializes in undertaking – carrying corpses outside for disposal (Arathi et al. 2003, Trumbo et al. 1997). Such behaviour is important for reducing disease transmission and keeping the hive sanitary (Wagoner et al. 2021). Certain genetic lines have been demonstrated to better respond to unhealthy brood odours and are considered to be especially hygienic (Wagoner et al. 2021).

Defense of the colony falls to the oldest MABs which are nearing the transition to foragers. The guard bees’ job is to identify and exclude any foreign intruders. The number of bees patrolling the hive entrance, ready to attack suspicious-smelling individuals, is estimated to be about 75 at any one time (Moore et al. 1987). This is a relatively low number considering the thousands of bees residing in the colony behind them, but this force is effective against robbing bees from other colonies, or other insects with nefarious agendas (Moore et al. 1987, Breed et al. 1990). However, when exposed to greater disturbances, such as those performed by bears, skunks or other animals, another group emerges – the defender bees! These bees fly in larger groups and seek to sting, or at least intimidate, any giant-sized offenders (Breed et al. 1990). Defender bees are forager-aged but have low levels of wing wear, leading some researchers to believe that this a specialized behavioural caste rather than ordinary bees recruited by alarm pheromone (Breed et al. 1990).

Considering the number of different tasks that the MABs (middle-aged bees) are responsible for, how is the labour allocated among the bees of this age cohort? It is known that juvenile hormone (JH) plays a large role in the transition between age groups – JH increases as bees ages, therefore low levels are associated with in-hive tasks and high levels with foraging (Robinson 1985, Jaycox et al. 1974). If a scientist injects a young bee with an artificial mimic of JH, she exhibits an earlier start to foraging behaviour (Jaycox et al. 1974). However, studies carried out by Robinson (1992) suggest that JH is also important for task allocation within age groups, as individual variation of the hormone within similar aged bees leads to variability in individual bee’s abilities to notice and respond to environmental triggers in the hive (such as food availability or amount of brood). Thus, every worker will do every task in her lifetime, as this depends on environmental and hive conditions during her life, and inherent genetic variation in hormonal levels.

Foragers (days 21 onwards)

Only about 60% of workers will make it to the final life stage (Prado et al. 2020). As these surviving in-hive bees transition to foragers they lose about 40% of their body mass due to changes in their abdomen and digestive tract, which will make flight more efficient and provide more storage room for nectar (Harrison 1986). Glycogen stores in the thorax will double, allowing for a quick source of energy for flight muscles (Harrison 1986). Although younger bees may perform shorter orientation flights, as bees approach the age of foraging they will begin to perform the longer orientation flights which are important practice for way-finding and calibration of the internal bee compass, which is oriented around the sun (Degen et al. 2015). The bees are now better equipped for flight than at any other point in their life – and they are about to do a lot of flying!

There are four resources which foragers collect: nectar, pollen, water, and resin. Generally, foragers seem to specialize in the collection of one substance (Winston 1987). Nectar and water are sucked up through a forager’s straw-like proboscis (tongue) and stored in her honey stomach for later regurgitation (Winston 1987). Upon returning to the hive entrance, nectar and water foragers seek out a receiving worker whom they transfer the sugary liquid to. Foragers specializing in pollen collection pack their loads on the enlarged, hairy portions of their hind legs – the pollen baskets. Unlike nectar foragers, pollen foragers are responsible for depositing their own load in the hive, which is typically done on or near brood frames, where the nurse bees and their charges require high protein diet. Tree resin (propolis) is gathered much less frequently but is important for filling cracks and holes in the hive walls and for its antibacterial properties (Simone-Finstrom et al. 2017). Propolis is also carried on pollen baskets but is so sticky that another bee must pull it off!

While some bees participate in the foraging itself, others play the role of scout and fly beyond the range of known food sources in search of new resources. Returning scouts report new findings to other foragers via the waggle dance, which informs other bees of the direction of the resource (oriented around the sun) and the distance (or energy spent getting there) (Liang et al. 2012, von Frisch & Lindauer 1956). Generally, forager-aged bees are either scouts or foragers, and only shift roles if necessary (Liang et al. 2012). Scouts will make up 5-25% of a colony’s forager-aged bees, and are also tasked with seeking out a new home when a colony swarms (Liang et al. 2012).

Foraging is a dangerous activity and individual foragers have a 36% chance of dying each day spent foraging (Prado et al. 2020). High flight speeds (25 km/hr) wear down a bee’s body and older foragers can be recognised by their tattered wings and thinning hair (Seeley 1995). The average summer lifespan of a worker is 38 days and bees that are not prematurely killed during their foraging trips will die of exhaustion – after flying about 800 km the ability to covert carbohydrates to glycogen as an energy source is significantly reduced and bees are no longer above to recover from physical exertion in the same way as when they were younger (Winston 1987).

A Note on the Separate System of Winter Bees:

Winter bees cannot be sorted into the four temporal castes that define the lifecycle of summer bees, instead they are considered a separate “generalist state” (Johnson 2010). The queen will not continue to produce brood over the cold months, but the winter bees that result from eggs laid in late fall can survive the full winter. The average winter bee lifespan ranges from 100 to over 200 days – partly because it takes much longer for a winter bee stuck in a hive to reach the lifetime flight distance that is associated with natural death in workers (Mattila et al. 2001, Winston 1987). Unlike their summer counterparts, the tasks that these bees are engaged in (thermoregulation, feeding, queen care, brood care in early spring) are not divided according to age – any bee can practice these tasks (Johnson 2010). Indeed, winter bees are physiologically different from summer bees as their levels of juvenile hormone (associated with performing different in-hive tasks) are comparatively low throughout their lifetime (Mattila et al. 2001). Additionally, winter bees have hypopharyngeal glands that do not degrade as they age which results in continued ability to create royal and worker jellies, as well as enlarged fat bodies which act as enhanced energy reserves for many months of heat-generating vibration (Brejcha et al. 2023).

Importance of Healthy Age Distribution:

Clearly this detailed partitioning of labour is necessary for the synergistic functioning of a healthy colony – but what if the age distribution of a colony is not even?

The transition between temporal castes is environmentally regulated (e.g., bees will not take up foraging activities if there is an already existing/sufficient foraging force), so if there are less-than-ideal environmental conditions, such a past break in the brood pattern leading to no nurse-aged bees, or mass loss of foragers, the bees can adjust their caste transitions according to their perception of the colony’s needs. Younger bees can accelerate their development and begin to take on later tasks at an earlier age (Perry et al. 2015). Bees are also capable of doing the reverse – should a colony lack young workers, older bees can revert back to doing tasks they previously did when younger (Robinson et al. 1992). These are not seamless transitions as in both instances the bee carrying out the task is not physiologically optimized to do so. For example, precocious foragers are heavier and less efficient flyers than regular-aged foragers and are also more likely to fail to return from foraging trips (Rueppell 2007, Perry et al. 2015). Similarly, the hypopharyngeal glands of a forager that reverts back to performing nursing duties have reduced in size and now produce secretions other than brood food, although there is evidence that reversal of this aging process can occur to some degree (Robinson et al. 1992). Environmental conditions are not the only reason bees may speed up development; some diseases, such as infection with Nosema ceranae, are known to accelerate aging, causing premature foraging, reduced harvest efficiency and early death (Goblirsch et al. 2013). Exposure to neonicotinoid pesticides may also have similar effects (Colin et al. 2019).

Another problem with foragers reverting back to in-hive tasks is the potential to bring diseases or contaminants from the outside world into the brood chamber. The colony is structured such that there is a separation between bees that perform in-hive tasks and those that travel out of the hive, and as bees age they begin to do tasks associated with the hive entrance (see figure at right). By this mechanism, the queen, the brood, and the bees that attend to them are somewhat sheltered from diseases and pathogens (Laomettachit et al. 2021). So, although colonies can cope with disruptions in age structure, healthy age distribution is desired. As this article has shown, the task division performed by honey bees is very complex and allows for the bees to contribute to each other’s welfare and overall colony wellbeing in detailed and amazing ways!

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