Why are there “Lazy” ants?Explaining the occurrence of seemingly unproductive workers in social insects

D Charbonneau ▪ A Dornhaus

Most animals are “lazy”

“All cold-blooded animals and a large number of warm-blooded ones spend an unexpectedly large proportion of their time doing nothing at all, or at any rate, nothing in particular.”

-Elton 1927

Solitary animals

>50%Harvestmen

(Williams 1962)

85%Hummingbirds

(Wolf et al. 1975)

Social animals

60%Temnothorax ants

(Dornhaus et al. 2009)

Eusocial insects

Animals across a wide range of taxa, life histories and ecologies have been reported of spending >50% of their time resting

80%Honey bees

(Schmid-Hempel 1990)

70%Howling monkeys

(Smith 1977)

75%Lions

(Schaller 1972)

Most animals are “lazy”

“Laziness” in social animals

Inactivity in social animals is further complicated by social behaviors, such as division of labor and specialization

In groups, the amount of work required for the survival of an individual is dependent upon the amount of work done by others in the group.

division of labor

“Laziness” in social insects

Inactivity in social animals is particularly interesting because the colony can regulate the number of workers it produces

If >50% of the colony is inactive at any time, why would the colony produce so many apparently extraneous workers?

Workers are expensive to produce and maintain, so

there is a real cost to having “too many”

Why are there “Lazy” ants?

Model system used to answer this question:

The ant: Temnothorax rugatulus

Worker ant

Queen ant

Recording ant behavior

AntsWater

Food “Stone” wall

Sample unit: 5 minute HD videos

Behaviors and activity

BuildingForaging

Wandering outside nestBrood care

Self-GroomingGroom otherBe groomedTrophallaxis

EatingMoving but not active

Stationary and not active

Active

Wandering InsideInactive

Similar to: Cole, BES 1986

Observable task Activity category

Breaking down observable behavior into categories of activity

Defining “inactivity”

Colony-level inactivity:

Individual-level inactivity:

Mean proportion of time an individual worker spends inactive during one video

Mean individual-level inactivity within a colony

∑ time spent inactive by all ants in colony∑ of individual observation times

or

= % of colony time inactive

i.e. % of worker time inactive

Inactivity variesAt the individual-level

And at the colony-level

Colony 2 Colony 3

Inactivity variesMy work focuses on individual-level variation

And at the colony-level

Colony 2 Colony 3

Main question: How can we explain high levels of worker

inactivity?

Consistency of worker inactivity / Shift-workCan apparent individual-level variation in inactivity be explained by a bias in observation timescale?

Selfish worker reproductionIs worker ovary development positively correlated to individual-level inactivity?

Inactive workers as a reserve labor forceDo highly inactive workers become more active when the colony is presented with more work?

Inactivity in the field / Lab artifactDoes colony-level inactivity occur in the field at levels comparable to those observed in the lab?

Inactive workers facilitate communicationAre highly inactive workers actually performing a communication task?

Consistency of worker inactivity / Shift-workCan apparent individual-level variation in inactivity be explained by a bias in observation timescale?

Selfish worker reproductionIs worker ovary development positively correlated to individual-level inactivity?

Inactive workers as a reserve labor forceDo highly inactive workers become more active when the colony is presented with more work?

Inactivity in the field / Lab artifactDoes colony-level inactivity occur in the field at levels comparable to those observed in the lab?

Inactive workers facilitate communicationAre highly inactive workers actually performing a communication task?

Ecologically non-relevant explanati

ons

Main question: How can we explain high levels of worker

inactivity?

Consistency of worker inactivity / Shift-workCan apparent individual-level variation in inactivity be explained by a bias in observation timescale?

Selfish worker reproductionIs worker ovary development positively correlated to individual-level inactivity?

Inactive workers as a reserve labor forceDo highly inactive workers become more active when the colony is presented with more work?

Inactivity in the field / Lab artifactDoes colony-level inactivity occur in the field at levels comparable to those observed in the lab?

Inactive workers facilitate communicationAre highly inactive workers actually performing a communication task?

Functions of individual inactivity that are

detrimental to colony

fitness

Main question: How can we explain high levels of worker

inactivity?

Consistency of worker inactivity / Shift-workCan apparent individual-level variation in inactivity be explained by a bias in observation timescale?

Selfish worker reproductionIs worker ovary development positively correlated to individual-level inactivity?

Inactive workers as a reserve labor forceDo highly inactive workers become more active when the colony is presented with more work?

Inactivity in the field / Lab artifactDoes colony-level inactivity occur in the field at levels comparable to those observed in the lab?

Inactive workers facilitate communicationAre highly inactive workers actually performing a communication task?

Functions of individual inactivity that are

beneficial to colony fitness

Main question: How can we explain high levels of worker

inactivity?

Inactivity in the field / Lab artifactDoes colony-level inactivity occur in the field at levels

comparable to those observed in the lab?

We recorded behavior in the field and in the lab and compared overall

inactivity levels

p=0.38

Linear Mixed-Effects Model - Fixed-effects: Treatment (lab or field); Random effects: Colony/Date/Timepoint

There were no significant differences in inactivity between observations in the field and in the lab

Consistency of worker inactivity

Observations of variation in individual inactivity are just a snapshot in time

It’s possible that over longer timescales,

individual variation would

disappear

Can apparent individual-level variation in inactivity be explained by a bias in observation timescale?

Snapshot (large

variation)

Multiple observations

(little variation)

Theoretical frequency distributions

Consistency of worker inactivityCan apparent individual-level variation in inactivity

be explained by a bias in observation timescale?

8 am – 08:00h12 pm – 12:00h

4 pm – 16:00h8 pm – 20:00h

12 am – 24:00h 4 am – 28:00h

5 minute HD videos,every 4 hours,over 24 hours

Day

Night

Individually marked ants (Temnothorax rugatulus)

Individual marking allows workers to be tracked across multiple time points and days

Recording schedule

5 Colonies recordedon 3 separate days,within a 2 week period

p-valueAnt <0.0001Time period 0.24Ant x Time period 0.66

Linear Mixed-Effects Model - Fixed-effects: Time Step, Unique Ant ID, Time Step x Unique Ant ID; Random effects: Colony/Date/Timepoint

Consistency of worker inactivityCan apparent individual-level variation in inactivity

be explained by a bias in observation timescale?

there are consistent

differences in individual

inactivity levels

Even when observed over longer time periods and at different times of the day,

Overall freq. distributions of inactivity for each colony

Consistency of worker inactivity / Shift-workCan apparent individual-level variation in inactivity be explained by a bias in observation timescale?

Selfish worker reproductionIs worker ovary development positively correlated to individual-level inactivity?

Inactive workers as a reserve labor forceDo highly inactive workers become more active when the colony is presented with more work?

Inactivity in the field / Lab artifactDoes colony-level inactivity occur in the field at levels comparable to those observed in the lab?

Inactive workers facilitate communicationAre highly inactive workers actually performing a communication task?

Ecologically non-relevant explanati

ons

Inactivity can’t be explained by

Consistency of worker inactivity / Shift-workCan apparent individual-level variation in inactivity be explained by a bias in observation timescale?

Selfish worker reproductionIs worker ovary development positively correlated to individual-level inactivity?

Inactive workers as a reserve labor forceDo highly inactive workers become more active when the colony is presented with more work?

Inactivity in the field / Lab artifactDoes colony-level inactivity occur in the field at levels comparable to those observed in the lab?

Inactive workers facilitate communicationAre highly inactive workers actually performing a communication task?

Functions of individual inactivity that are

detrimental to colony

fitness

Future work will look at:

Functions of individual inactivity that are

beneficial to colony fitness

- and -

Selfish worker reproductionIs worker ovary development positively correlated

to individual-level inactivity?

Oocyte diam.In

activ

ity

Ovary dissections by undergraduate student Neil Hillis

To test this hypothesis, we will measure individual inactivity and then dissect

worker ovaries.

A positive relationship between inactivity and measures of ovary development (e.g. number of ovarioles, ovary length, diameter of largest oocyte) would suggest a reproductive conflict where highly inactive workers are conserving energy by avoiding work and putting that energy toward their own reproduction

Inactive workers as a reserve labor force

Can apparent individual-level variation in inactivity be explained by a bias in observation timescale?

We have preliminary evidence that inactivity might be linked to the amount of work

There is an apparent relationship between

colonies, their brood/worker ratios,

and colony-level inactivity.

Future work will involve manipulating “available work”:- Starvation - Increased brood- Predator- Wall destruction- Emigration

Linear Model - Fixed-effects: Brood/Worker ratio, Season of observation, and Colony

Inactive workers facilitate communication

Are highly inactive workers actually performing a communication task?

Deg. centrality

Inac

tivity

Info

rmat

ion

flow

20% laziest removed

20% randomremoved

Looking at network topology, we can determine whether highly inactive workers hold a highly central position

We will also do a removal experiment where the 20% laziest workers and 20% random workers are removed from colonies and measure whether information flow (Blonder & Dornhaus 2011) is lower in colonies with fewer inactive workers

Automated tracking developed by Dr. Shin at UNCC

Broader impacts

Emerging technologiesAutomated tracking allows us to gather large amounts of network data quickly. These can be used to investigate network topologies of social insect interaction networks. We can also look beyond interaction networks and answer novel questions, by creating innovative network types such as time-ordered and bipartite task networks (Charbonneau et al. 2013)

Knowledge about how animals allocate their time between inactivity, or rest, and other more active tasks provides insight into ecological trade-offs

Social insect colonies are evolved (and thus optimized) and highly successful organized complex systems. Our findings will be applicable to improving management strategies and information flow in human-made and biological networks (e.g. the internet, traffic, social groups, and neural networks).

Division of labor / work allocation

Ecological trade-offs

Thank you!

IOS-0841756IOS-1045239

GIDP-EIS

University of Arizona

Center for Insect Science

Undergraduate helpers (Andrew Scott, Alex Down, Matt Velazquez, Nicole Fischer, and Mary Levandowski)

Nicole Fischer, Mary Levandowski

Folks at UNCC (Min Shin, Corey Poff and Hoan Nguyen)

Dornhaus Lab