Division of Labour in Workers

Francis L. W. Ratnieks

Department of Biological & Environmental Science

University of Sussex

Laboratory of Apiculture & Social Insects

Social Insects: C1139

Aims & Objectives Aims 1. To provide information on the tasks performed by workers and how these may be divided among the workers in a colony according to age and size. The primary focus will be on the honey bee Apis mellifera, in which workers of different ages do different talks (age polyethism), and Atta ants, in which workers of different size do different tasks. 2. To become aware of possible advantages of division of labour, the kinds of tasks that need to be performed, and how this varies among species; control of age polyethism. 3. To show how diversity in the sizes and shapes of ant workers may arise from some simple underlying relationships concerning the overall range of sizes of workers, and allometric differences between workers of different body size. Objectives 1. Learn the main features of division of labour in honey bee and Atta. 2. Be aware of some hypotheses for the adaptive significance of division of labour at both colony and individual levels. 3. Understand the basics of allometry/isometry in worker ants.

Some Tasks Carried Out by Worker Honey Bees

The previous slide shows 4 of the many tasks carried out by workers. Top left. The queen is in the centre laying an egg. She is surrounded by a court of workers who feed her and touch her with their antennae. These workers pick up queen pheromone and distribute it round the colony, partly by touching other workers. In this way the colony knows the queen is alive. If the queen dies or is lost, the colony knows within hours because the pheromone level drops. The colony then rears several emergency queens from larvae in worker cells, which are fed royal jelly. Top right. Guards at the entrance intercept a robber bee (centre) from another colony. Guard to bottom right is in typical posture with forelegs raised. Guard below robber is biting intruder. Robber is trying to placate guard above by regurgitating food to guard’s outstretched tongue. Bottom left. Forager African honey bee in Brazil collecting propolis (tree resin) seeping out from tree trunk where damaged by insects. Bottom right. Nectar forager. Foragers often collect both pollen and nectar from the same flower. This forager has an empty pollen basket suggesting that it is collecting only nectar, or possibly has only just begun its foraging trip. Some flowers (e.g., kiwi fruit, some poppies) only provide pollen as a reward to bees. Some foragers collect water.

Some Tasks Carried Out by Worker Honey Bees Pheidole Ants

male

queen

These Pheidole ants show allometry in worker head size. In the largest workers, the head is half the ant.

In most Pheidole there is a very clear bimodal distribution of worker sizes with many minor workers and few major workers. Foraging is by minors, but majors may help in retrieving large prey items near the entrance. Majors are mainly involved in defence.

Division of Labour: Big Picture Reproductive division of labour: reproducing & working individuals

The key feature of eusociality

Division of labour among working individuals Individual workers specialize on specific tasks For a few days to their whole life DoL = workers/tasks

Behavioural specializations Workers do different tasks as they age: "age polyethism" initially work inside nest foraging (dangerous) is last

Morphological specializations Body size and shape affect tasks performed by a worker Size and shape affect task performance effectiveness Colony needs (e.g., Atta: big defenders, small gardeners)

Hypothesized Advantages of Division

of Labour

Hypothesized Advantages of Division of Labour DoL occurs so is presumably advantageous But for whom? Colony or Individual? Most hypotheses stress benefits to colony

That is, DoL makes workers better at working Various ways this may occur

Benefits to self may also be relevant in species without distinct queens and workers an adult worker may, in principle, replace queen

by delay foraging, worker increases chance of reproducing

DoL Between In-Nest & Forager Workers On any day, each worker could both forage and work in-nest

DoL not present Or there might be specialist forager and in-nest workers

DoL present

The DoL situation increases lifetime work output per worker but only if foraging comes last

as normally happens

DoL Between In-Nest & Forager Workers The DoL situation increases lifetime work output per worker, but only if foraging comes last. The diagram below shows why. You could make a more formal model. The key is that the mortality rate of in-nest workers is lower than that of foragers. The area represents the expected total amount of work per worker lifetime. Clearly, it is greater for forage last.

Foraging

Foraging

In-nest

Prob

abili

ty of

surv

ival

Age In-nest

1. Forage last

2. Forage first

Other Possible Colony Advantages of DoL Specialization may increase an individual’s task performance

Big Atta workers: guarding Small Atta workers: tending fungus garden

Smaller workers are cheaper to rear and sustain Don’t use a big worker where a little one will do

Specialization may reduce time wasted moving between tasks Do tasks located together spatially honey bee Apis mellifera, ant Pheidole dentata

Colobopsis Ants These ants live in tunnels in tree trunks. The larger workers have flattened heads to block the entrance holes. Colonies without these larger workers are unable to survive so well. The large workers also act to store food. In this situation, a different morphology leads to superior task performance and colony survival. However, the colony does not benefit if all the workers are larger. They are more expensive to rear and sustain, and just a few are enough to block the entrance.

Hon

ey b

ee, A

pis m

ellif

era Pheidole dentata ants

NEAR EGGS

NEAR LARVAE

NEAR ENTR-ANCE & OUT-SIDE

Discretization & Spatial Location of Tasks

In both species workers do different tasks as they age. The tasks that they do at the same time are also located in the same place.

Parallel With Human Organizations Human hospitals, factories etc. Improved efficiency via DoL

Many tasks to be done Employees do what they are good at Employees work on one/few tasks each (nurse, cleaner, surgeon) Tasks are grouped spatially

Surgeons (expensive to train, to employ) don’t clean the floors What Work Needs Doing?

Guarding the Nest Almost all insect colonies guard the nest in one way or another. Frequently, this involves guards who are stationed at the entrance or who can rapidly come out of the nest. In some ants and most termites the guards are morphologically specialized. In honey bees the guards are middle-aged workers, who have not yet begun to forage but who have a full venom reservoir and abundant alarm pheromone. The previous slide has photos from Fazenda Aretuzina, S ão Simão, São Paulo State, Brazil. Top left. Unidentified mound building termite (Termitidae). Soldiers come out of hole made in the mound. Small-headed workers also seen. Top right. Nest of Polybia paulista wasps under palm leaf. Normally, dozens of workers sit on the outside of the nest. Slight disturbance brings hundreds more out. More disturbance causes them to fly & sting. Bottom left. Nest of stingless bee Melipona scutellaris. The entrance always has a single guard who checks incomers. This species has sharp mandibles. The guard can kill intuder bees who attempt to enter. Bottom right. Part of surface of nest of the silk weaving ant Camponotus senex. Normally, dozens of workers patrol the surface. Vibrations or CO2 cause a rapid alarm reaction. Workers drum their abdomen on the nest surface, causing more to do the same making a loud rustling noise. Within seconds, hundreds of workers come out of the nest onto the surface through one of dozens of small holes in the silk (one at lower centre). They will run onto an intruder, biting and releasing formic acid.

Guarding the Nest What Work Needs Doing? In-nest v Outside nest: main distinction Inside/At nest

cleaning nest, cells; removing waste from nest nursing (feeding brood); feeding queen & nestmates nest building & maintenance, excavation food handling, processing storage grooming self or nestmate guarding nest & nest entrance

Outside nest foraging for food & building materials scouting maintaining trails (clearing debris, laying pheromone) defending foragers

Differences in Among Species Work that needs doing differs according to way of life

Some examples of tasks specific to certain groups

Inside nest Atta: tending fungus garden & processing leaves Soil living species: excavating to enlarge nest

Outside nest: foraging Honey bee: nectar, pollen, water, propolis (= plant resin)

note: pollen & nectar usually collected together at same flowers Stingless bees: as above + soil (for building) Vespinae wasps: prey, nectar, plant fibres, water Polyergus (slave making ants): forage for slave pupae

Pheidole dentata A list of tasks for the ant Pheidole dentata, and the frequency (= proportion time) spent on these tasks by minor workers (left) and major workers (right).

Here the researcher is interested in comparing the overall work profiles of the two sizes of workers, and so has a complete list of acts that workers are seen to perform. The major workers (big heads) don’t do much! But once in a while they are needed to defend the nest.

Age Polyethism in the Honey Bee, Apis

mellifera

Age & Task in the Honey Bee

Data collected from a group of worker honey bees shows clearly how the work tasks performed change with age. Some clear patterns are: 1. Cleaning cells is the first task 2. Tending brood (nursing) and eating pollen by young bees)

3. Somewhat older bees handle food, shape comb 4. Foraging by oldest bees 5. A lot of time spent by bees of all ages in walking round nest (patrolling) and resting

Age & Task in the Honey Bee

Ages at which Apis mellifera workers do different things.

A Day in the Life of a Worker Bee

A day in the life of worker honey bee 107. Lindauer M. 1961. Communication among social bees. Harvard UP.

Idiosyncratic Tasks in the Honey Bee xxx

Some tasks, such as undertaking (above: removing worker corpse from nest) are not performed by all workers because there is little work to do.

Physiology: Honey Bee Worker Age & Glands Wax glands in abdomen

A. Honey bee workers have well-developed mandibular glands in their head when young and nursing larvae. They eat pollen and convert this into a white liquid that is fed to larvae. B. When older the mandibular glands are less active, and the four pairs of wax glands on the ventral surface of the abdomen are active. C. In older workers that are foraging both sets of glands are inactive.

A

Age, days

B

C

Worker with scales in wax glands

Food glands in head

Morphological Worker Castes in Atta ants

Worker Leafcutter Ants, Atta Atta have probably the most sophisticated division of labour among workers of any social insect. There is a 100-fold variation in worker weight within a colony. The workers also vary in shape, spininess, behaviour, and gland activation. This complexity is linked to their way of life, which requires then to collect and process leaves for their fungus garden, which is tended by small ants inside the nest.

Fungus Garden of Acromyrmex

Part of fungus garden of Acromyrmex sp. (Acro. Have smaller colonies that Atta, and lack the very largest guard workers.) A range of ant sizes can be seen. The large ants are not the gardeners but guards & foragers.

Tasks Performed by Different-Sized Atta Workers

Smaller workers mainly work in the nest, caring for the fungus garden and chopping leaves into small pieces. Larger workers work outside cutting and retrieving leaf pieces. Even larger workers (not shown) act as guards, help to keep foraging trails clear, and may also help to cut up fruit and dung for smaller workers to take to the nest.

Tasks Performed by Different-Sized Atta Workers Atta Leaf Cutting Efficiency Atta Leaf Cutting Efficiency

Workers of intermediate head sizes are most efficient at cutting leaves, in terms of oxygen consumed per unit of leaf. Foragers are this size.

Tasks Performed by Majors

Tasks Performed By Atta laevigata Majors

The massive heads on these major Atta laevigata workers from Fazenda Aretuzina, Brazil are full of muscles to operate the jaws. They have several roles. They may defend the colony and the foraging trails (left, biting finger of F. Ratnieks), cut up difficult food items like fallen fruit (right, cutting up mango) or horse dung into smaller pieces for others to carry home, and help clear foraging trails of debris (not shown).

Honey pot ants have evolved several times in desert ants.One honey pot species is Myrmecocystus mimicus from Arizona. Workers use their bodies to store liquid food, including sugar solutions. (Many ants collect sugars from aphids and other honeydew secreting insects.) The ants that do this are known as “repletes”. Food storage is one of the tasks done by the major workers.

Tasks Performed By Honey Pot Ant Majors

Tasks Performed By S. geminata Majors

In the fire ant Solenopsis geminata, majors mill seeds. They are much larger than the main peak of worker size (head width 2.34 v 0.66mm).

Underlying Simplicity in Worker Size

Distributions in Ants In isometric growth the relative sizes of body parts remain in the same proportion as an organism grows, or in workers of different sizes. Here by 1.5 for the head and rest of the body.

x 1.5 x 1.5

Isometric Growth

x 1.5 x 1.5

Allometric Growth

In allometric growth the relative sizes of body parts is not the same in different sized individuals. Here, the head doubles in linear dimension as the rest increases by 1.5. In ants, the head is usually relatively larger in larger individuals. Soldiers can appear to be almost all head.

x 2.0 x 1.5

x 2.0 x 1.5

Allometric Growth

x 1.25 x 1.5

x 1.25 x 1.5

Here, the head only increases 1.25 in linear dimension as the rest increases by 1.5. This does not often happen in ants, but does in humans.

As a human matures, all parts of the body become larger. But not at the same rate. The adult head is relatively smaller.

Allometric Growth in Humans

Isometric & Allometric Growth

Thorax width, mm

Hea

d w

idth

, mm

1 2 4 0.5 1.5 0.75 3 0.5

1

2

4

1.5

0.75

3

Isometric, y = x1

Allometric, y = x0.55

Allometric, y = x1.71

This figures plots the head width and thorax width of the examples on the previous slides. The upper line is for (x2 head, x1.5 rest of body). The lower line is for (x1.25, x1.5). Note that the axes are logarithmic. This linearizes things.

Isometric & Allometric Growth If you are mathematically inclined this may interest you. The previous slide shows that if you plot head width against thorax width the relationship is linear when logarithmic axes are used. You can see how this follows from the general equation for allometric growth. Y = aXb Where Y is the linear dimension of one body part (e.g., head), and X is the linear size of another part (e.g., thorax); a & b are constants. In one example, the head increases by 2 as the thorax increases by 1.5, to give 2 = a(1.5)b a = 1 because when x = 1, y =1, to give 2 = 1.(1.5)b Now take logarithms of both sides to give log(2) = log (1) + b(log (1.5)) log (2)/log (1.5) – log(1) = b b = 0.301/0.176 – 0 = 1.71 Note that [log(2) = log (1) + b(log (1.5))] is the equation of a straight line, y = a + bx. That is, log(headwith) = log(a) + b(log(thoraxwidth)) is a straight line if growth is allometric or isometric.

Isometric & Allometric Growth. 1

Thorax width, mm

Hea

d w

idth

, mm

1 2 4 0.5 1.5 0.75 3 0.5

1

2

4

1.5

0.75

3 Line of isometry

In this hypothetical example, the colony produces workers all of which are very much the same size and shape.

Isometric & Allometric Growth. 2

Thorax width, mm

Hea

d w

idth

, mm

1 2 4 0.5 1.5 0.75 3 0.5

1

2

4

1.5

0.75

3 In this hypothetical example, the colony produces workers of a wide range of sizes, but all of the same shape, that is relative size of head to thorax. This is because the worker dimensions fall on the line of isometry.

Line of isometry

Isometric & Allometric Growth. 3

Thorax width, mm

Hea

d w

idth

, mm

1 2 4 0.5 1.5 0.75 3 0.5

1

2

4

1.5

0.75

3 In this hypothetical example, the colony produces workers of a wide range of sizes. However, there is a clear bimodal distribution of sizes. All workers are of a very similar shape because they fall on the line of isometry.

Line of isometry

Isometric & Allometric Growth. 4

Thorax width, mm

Hea

d w

idth

, mm

1 2 4 0.5 1.5 0.75 3 0.5

1

2

4

1.5

0.75

3

Line of isometry

In this hypothetical example, the colony produces workers of a wide range of sizes. The workers are also of different shapes. This is because the worker dimensions do not fall on the line of isometry. The larger workers will have relatively larger heads.

Isometric & Allometric Growth. 5

Thorax width, mm

Hea

d w

idth

, mm

1 2 4 0.5 1.5 0.75 3 0.5

1

2

4

1.5

0.75

3 In this hypothetical example, the colony produces workers of a wide range of sizes. However, there is a clear bimodal distribution of sizes. The workers are also of different shapes. This is because the worker dimensions do not fall on the line of isometry. The larger workers will have relatively larger heads.

Line of isometry

Isometric & Allometric Growth. 6

Thorax width, mm

Hea

d w

idth

, mm

1 2 4 0.5 1.5 0.75 3 0.5

1

2

4

1.5

0.75

3 In this hypothetical example, the colony produces workers of a wide range of sizes. The workers are also of different shapes, and also vary in the shape/size relationships. The smaller workers all have the same shape although they vary in size. The larger workers have relatively larger heads.

Line of isometry

Monomorphism Workers of wood ant Formica exsectoides. Monomorphism is the simplest situation. The workers of a mature colony have a unimodal size distribution, and isometry. Examples are found in most ant genera. In most ant genera and species. May be both an ancestral and a derived condition. Compare to examples 1, 2.

isometry

Monophasic Allometry

Hea

d w

idth

acr

oss e

yes,

mm

Allometry with a unimodal distribition of sizes in wood ant Formica obscuripes (also occurs in many other ants such as the army ant Neivamyrmex army ant, the British ant Lasius fuliginosus). Example 4. There is a trend towards bimodality in Camponotus, Azteca, Megaponera. Example 5. Max. pronotal (thorax) width, mm

isometry

Head width across eyes, mm

Hea

d w

idth

abo

ve e

yes,

mm

allometric

allometric the other way

isometric

Diphasic Allometry Diphasic allometry in Atta texana. The relationship is allo-metric in both smaller and larger ants but in the oppo-site way. In the smaller ants, larger heads are relatively more narrow (compare A, B). In larger ants, larger heads are relatively broader (compare, B, C). If the allometry of the small ants applied to all sizes, the largest ants would have heads like X. The top part of the head is where the jaw muscles are. Compare example 6.

Sizes & Shapes of Workers The preceding slides show that there can be an underlying simplicity in the sizes and shapes of workers. A few simple processes can give rise to considerable variation, and different types of variation. Presumably, this variation in size and shape variation is caused in large part by tuning developmental pathways. But it will also have a component of worker behaviour, as it is the workers who feed the larvae. Different species of ants show different patterns. These different patterns can presumably evolve one from another, with monomorphism being the ancestral condition and still the must common situation in number of species. Thus, a bimodal size distribution may evolve from a continuous size distribution. And diphasic allometry from monophasic. Why don’t bees and wasps show similar size and shape differences? Bumble bees normally have a range of worker sizes, but in honey bees, stingless bees, and Vespidae wasps workers are almost exactly the same size as each other. This may be because in these species brood are reared in individual cells that are normally arranged in a comb, resulting in similar-sized cells. Bumble bees rear brood in communal cells that are not arranged regularly into combs.

Fruit Cutting by Atta Workers

Fruit Cutting by Major Workers Fruit Cutting by Major Workers

Fruit Carrying by Media Workers Why Do Big Workers Cut Soft Fruit? Geometry Hypothesis

Long mandibles needed to cut piece from 3-D object (fruit)

Long mandibles not needed to cut piece from 2-D object (leaf)

Testing Geometry Hypothesis

Measure sizes of ants cutting leaves and fruit

Measure sizes of pieces cut

Investigate relationship (allometry)

Measuring Head Width Measured with Fuji S7000 camera in super macro against 1mm graph paper.

Results Almost no effect of ant size on leaf piece size Significant effect of ant size on fruit piece size

cubic allometry (fruit weight, y, to mandible length, x) y = axb

“Optimal” to have larger ants cut fruit

But major ants are not actually designed to cut fruit not many of them head allometry results in strong but not long mandibles

Results

-0.25 0.00 0.250.0

0.5

1.0

1.5

2.0

-0.25 0.00 0.25

-0.25 0.00 0.250.0

0.5

1.0

1.5

2.0

-0.25 0.00 0.25

Mango pieces Leaf pieces

Worker mass (mg, log)

Item

mas

s (m

g, lo

g)

Colony 1 Slope = 3.91 (3.10 – 4.72)

Colony 2 Slope = 4.33 (3.17 – 5.49)

Colony 1 Slope = -0.02 (-1.18– 1.23)

Colony 2 Slope = 2.02 (1.10 – 2.94)

Head Shape Media ants: oval head

Maximum headwidth 1.9 mm

Apical tip

Basal angle

Major workers: heart-shaped head Maximum headwidth 6.6 mm

Apical tip

Basal angle

Fruit Cutting by Atta Majors Many ant species have morphologically distinct worker sub-castes. This presumably increases colony efficiency and is thought to be optimized by natural selection. Optimality arguments are, however, often lacking in detail. In ants, the benefits of having workers in a range of sizes have rarely been explained mechanistically. In Atta leafcutter ants, large workers specialize in defence and also cut fruit. Fruit is soft and can be cut by smaller workers. Why, therefore, are large workers involved? According to the geometry hypothesis, cutting large pieces from three-dimensional objects like fruit is enhanced by longer mandibles. By contrast, long mandibles are not needed to cut leaves that are effectively two-dimensional. Our results from Atta laevigata support three predictions from the geometry hypothesis. First, larger workers cut larger fruit pieces. Second, the effect of large size is greater in cutting fruit than leaves. Third, the size of fruit pieces cut increases approximately in proportion to the cube of mandible length. Our results are a novel mechanistic example of how size variation among worker ants enhances division of labour.

Helanterä, H., Ratnieks, F. L. W. 2008. Geometry explains the benefits of division of labour in a leafcutter ant. Proceedings of the Royal Society B 275: 1255-1260.

Evison, S., Ratnieks, F. L. W. 2007. New role for majors in Atta leafcutter ants. Ecological Entomology 32: 451-454.