Journal of Asia-Pacific Entomology 13 (2010) 45–49
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Journal of Asia-Pacific Entomology
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j a p e
Behavioral variation among tunnelers in the Formosan subterranean termite
Paul Bardunias ⁎, Nan-Yao Su, Rou-Ling Yang
Department of Entomology and Nematology, Fort Lauderdale Research and Education Center, Institute of Food and Agricultural Sciences, 3205 College Avenue,
Fort Lauderdale, FL 33314, USA
a r t i c l e
i n f o
Article history:
Received 27 July 2009
Revised 30 October 2009
Accepted 4 November 2009
Keywords:
Key individual
Excavation
Tunnel
Division of labor
Coptotermes formosanus
a b s t r a c t
Division of labor is a common feature of insect societies and has been theorized to account for much of their
success. Asymmetries in the work of individuals, whose aggregate labor results in the completion of a task,
can lead to the emergence of key individuals that dominate or govern the task. Coptotermes formosanus
Shiraki excavate in a series of alternating workers whose efforts combine not only to elongate tunnels, but
also to guide the direction of propagation. When groups of 100 termites were presented with a single tunnel,
only ∼ 16% of termites entered. Of those that entered, the level of excavation was not uniform, with 20.6% of
termites responsible for over half of the total excavation. These termites, a small percentage of the total
available workforce, act as key individuals, producing the majority of labor and possibly guiding the efforts of
others. An examination of the excavation patterns of individuals shows that some individuals excavate
sporadically, but at a very high rate (number of excavation events per time). By focusing their effort over a
short period, these highly active individuals may influence the orientation of a tunnel and the formation of
branches to a degree out of proportion to the total amount of digging they engage in.
© Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection
Society, 2009 Published by Elsevier B.V. All rights reserved.
The benefit of task specialization and division of labor was perhaps
best described by Xenophon, a student of Socrates, in one of the
earliest descriptions of the process, “…he who devotes himself to a
very highly specialized line of work is bound to do it in the best
possible manner.” Division of labor is a major factor in the success of
social insects, thought to increase the efficiency of the large workforces
of colonies (Oster and Wilson, 1978). Often this division of labor is
reflected in worker polymorphism or temporal polyethism, but a more
fluid system of task specialization among less specialized individuals is
seen as well (Robinson, 1992). Most studies emphasized the
differences between task-groups, while minimizing or ignoring
variation within them (Robson and Traniello, 1999). Groups may not
be uniform in their task performance, and many individuals that could
partake in tasks appear to do no work (Herbers, 1983; Evans, 2006;
Dornhaus et al., 2008). Conversely, elite individuals (Hölldobler and
Wilson, 1990) or key individuals (Robson and Traniello, 1999) perform
a disproportionate amount of labor. Robson and Traniello (1999)
proposed three types of key individuals: catalysts, performers, and
organizers. Performers are simply individuals who are highly active
and account for a disproportionate amount of labor on any task.
Catalysts stimulate others to activity through their actions, and
organizers serve to initiate labor and maintain group cohesion
throughout the task. The presence of key individuals results in their
⁎ Corresponding author.
E-mail address: paulmb@ufl.edu (P. Bardunias).
behavioral idiosyncrasies being over-represented in the final work
product.
One task that termites carry out as groups is the excavation of
tunnels. Coptotermes formosanus Shiraki excavate tunnels by combining their efforts as members of a group which removes soil from the
tunnel in rotation (Bardunias and Su, 2009a, 2010). Recently, Yang et
al. (2009) demonstrated that termites in excavation groups that were
introduced to experimental arenas did not perform equal amounts of
work. Understanding how termites apportion the total work on a task
among individuals is important to our understanding of the evolution
of division of labor (Robson and Traniello, 1999). Alternatively, if our
goal is to understand the mechanics of tunnel excavation, then the
manner in which individuals combine their efforts over a limited
time-frame, their place and frequency of occurrence in the rotation of
excavators is more important than the overall duration of labor.
In situations where a key individual is responsible for choosing a
prey item (Robson and Traniello, 1998) or a new nest site (Möglich
and Hölldobler, 1975), the ability for a single key individual's actions
to shape the outcome of task is obvious. Termites in a tunneling-group
alternate their labor at a digging site, each individual working as part
of a rotation of individuals who work in series (Bardunias and Su,
2009a, 2010). This will tend to dampen the influence of any single
termite's idiosyncratic behavior. For example, termites tunnel along
internally generated vectors and tunnel headings reflect a consensus
of the orientation vectors of the working group (Bardunias and Su,
2009a). The reliance on multiple individuals to work together to
generate tunnel headings may act to mitigate individual errors in path
1226-8615/$ – see front matter © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2009 Published by Elsevier B.V.
All rights reserved.
doi:10.1016/j.aspen.2009.11.002
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P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
integration through the “many wrongs principle” (Walraff, 1978,
Simons, 2004). The orientation vectors on individuals may drift away
from their initial movement vector, but they will not all err in the
same direction or by the same magnitude. Thus, if many individuals
work in union, the resulting vector is more likely to correspond to the
original vector. If key individuals dominate excavation, then the
homogenizing effect of sampling the orientation vectors of many
excavators is reduced. Termites are also known to respond to
depressions in tunnel walls by excavating at the site (Lee et al.,
2008; Bardunias and Su, 2009b). Repeated excavation by an individual
at a preferred site along the tunnel wall may be enough to stimulate
others to dig there as well, leading to branch formation.
In order to characterize the workforce that is responsible for
tunnel excavation we re-examined the asymmetry in excavation
shown by Yang et al. (2009) by counting the actual occurrence of
excavation events rather than the time on task. We sought to
determine if all termites with access to a tunnel opening take the first
step in tunneling by entering the tunnel. Of those termites that did
enter the tunnel, we determined if they shared equally in the
excavation process. Most importantly, we gauged the potential for any
single excavator's behavior to disproportionately shape the resultant
tunnel's form or heading by determining if termites excavate at a
uniform rate (excavation/time).
between a pair of plastic spacers forming a tunnel 2 cm directly away
from the introduction point, then the spacers forced the termites to
turn 90° and travel another 2 cm (Fig. 1c). Termites respond to this
forced turn by excavating a curved tunnel (Fig. 1d) in the opposite
direction when they were free of the spacers and allowed to tunnel
freely once more (Bardunias and Su, 2009a). A curved tunnel allows
the maximum length of tunnel to fit into a video frame and the
termites to be filmed at maximum magnification.
Upon debouching from this guided channel, termites then
tunneled freely. Once the tunnel tip advanced beyond the guided
channel, tunneling activity was recorded at room temperature (26 °C)
and room lighting for 1 h with a video camcorder (Sony DVHandycam, Tokyo, Japan) mounted above the arena.
Entering the tunnel
Methods
The first step in an individual termite's joining the group of
excavators in an existing tunnel is simply entering the tunnel from the
introduction chamber. In each trial the identity of every termite
entering the tunnel over the 1 h period was recorded. The average of
the percentages of termites entering the tunnel among trials was
determined. The number of termites entering the tunnel in ten trials
was compared with the expectation that all 90 potential excavators
would enter the tunnel in each trial via chi-square analysis at α = 0.05
(SAS Institute, 1985).
Study subjects
Excavation
Individuals of C. formosanus were collected from two field colonies
in Broward County, FL, by using the methodology of Su and Scheffrahn
(1986). They were stored at 27 ± 2 °C in plastic boxes with thin, moist
wood chips. Ten groups, five from each colony, of 100 termites, made
up of 90 potential excavators of at least 3rd instar and 10 soldiers,
were created for 10 experimental trials. All 100 termites were
individually marked with a unique one- and two-dot color scheme
of 12 colors of enamel paint (Testor Corp., Rockford, IL) on their dorsal
abdomen.
Horizontal arenas consisted of two sheets of transparent Plexiglas
(24 by 24 cm2), with four Plexiglas spacers (2 × 24 by 4 by 0.2 cm3, and
2 × 20 by 4 by 0.2 cm3) between the outer margins. Sifted sand (150–
500 μm sieves, Play Sand Bonsal, Miami, FL) was moistened with
deionized water ≈ 7% by weight. A 15 ml cryogenic vial (Nalge Nunc
International, Rochester, NY) was used as an introduction chamber
(Fig. 1a, 3 cm diameter by 4 cm height). This was connected to the
arena via a 6 cm, 3 mm diameter, tunnel bored through a Plexiglas
coupling (Fig. 1b). Termites were initially constrained to excavate
The contribution of each termite that entered a tunnel to the total
labor that went into tunnel excavation was determined. Over the 1 h
experimental period, all of the excavation events performed by each
termite in a trial were tallied. In order to determine if all termites
contributed equally to the tunnel excavation, the number of
excavation events performed by each individual within a trial was
compared to the mean number of excavations performed by all
termites within that trial via chi-square analysis at α = 0.05 (SAS
Institute 1985).
The proportion of the tunnel excavation performed by each
participant within a trial was calculated by dividing the number of
excavation events performed by the individual by the total number of
excavation in the trial. The result was converted to a percentage and
these were binned in 5% intervals from 0% to 35%. The mean
percentage of individuals whose contribution to overall excavation
of the tunnel in their trial fell into each of these 5% intervals was
compared via Kruskal–Wallis test (SAS Institute 1985). Significant
differences among the mean percentages of individuals whose
proportion of excavation fell within each of the binned intervals
from 0% to 35% were separated by a Dunn's post-hoc test at an
adjusted α of 0.001 (0.05/42).
Temporal pattern of excavation
Fig. 1. The experimental arenas consisted of sifted sand between two sheets of
transparent Plexiglas (24 by 24 cm2). (a) 15 ml cryogenic vial was used as an
introduction chamber. (b) A 4 cm, 3 mm diameter Plexiglas coupling connected the
introduction chamber to the arena. (c) Termites were initially constrained to excavate
between a pair of plastic spacers forming a tunnel 3 cm directly away from the
introduction point, then the spacers forced the termites to turn 90° and travel another
3 cm. (d) The forced turn results in the excavation of a curved tunnel.
To examine the temporal pattern of an individual's excavation we
plotted each individual termite's excavation over the total time of the
trial. Even if termites contributed an equal number of excavation
events over the course of the trial, the rate (number of excavations/
time) at which they work may be different. The time of the initiation
of excavation was recorded when a termite initiated excavation by
grasping sand with its maxilla. The number of excavation events that
occurred within a 1 min period was recorded over the 1 h duration of
the trial for each excavator in the 10 trials. Plotting the number of
excavation events carried out by each individual in a trial results in a
graph that is too cluttered to be easily understood. For the sake of
clarity, we plotted the excavation for 1 min intervals from 0 to 60 min
of only the top excavators in each trial: the minimum number of
individuals whose labor accounted for at least 50% of the total
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
47
excavation. In addition, because there could be long periods of
inactivity, we calculated a rate of excavation for these top excavators
as the number of excavation events occurring in any 1 min period in
which they performed an excavation. By examining the pattern of
every individual's excavation each trial we determined if termites
ever performed an uninterrupted series of excavation events rather
than excavating in alternation with other termites.
Results
Entering the tunnel
Not all of the 90 potential excavators with access to the tunnel
entered it. The number of potential excavators that entered over
the 1 h period of recording ranged among trials from 21 to 9, with
an average of 14.5 ± 3.7 (mean ± SD). That is a mean percentage of
15.7 ± 4% of all potential excavators entering the tunnels, which
differed significantly from the expectation that all termites would
enter the tunnel (χ2 = 634.71, df = 9, P b 0.0001).
Excavation
The termites entering the tunnel did not contribute equally to the
excavation of the tunnel (Table 1). In each trial some individuals
performed at a much higher level than did others, their efforts ranging
from 0 to 56 excavation events in any trial during the 1 h period.
The percentage of individuals whose labor fell into each of the 5%
excavation intervals from 0% to 35% within their trial was significantly
different according to a Kruskal–Wallis test (χ2 = 45.276, df = 6,
P b 0.0001). The mean percentages of termites in the 5%, 10%, 15%, and
20% excavation intervals were all significantly different from the other
intervals (Fig. 2), but the 25% excavation interval did not differ
significantly from the 30%, or the 30% from the 35%.
Few termites (5.5%) entered the tunnel, yet failed to excavate any
soil. Of those termites that entered the tunnel, 57.9% performed 5% or
less and 84.8% performed 15% or less of the excavation in their
tunnels. The effort of top excavators in any tunnel still accounted for
less than a third of the total tunnel excavation. Small groups of
individuals, 3 ± 0.9 (mean ± SD), in each tunnel whose aggregate
excavation accounted for at least 50% of the total work on that tunnel
represented 20.6% of all of the termites which entered tunnels. This
drops to only 3.3% of the total number of termites if we include the
majority that never entered the tunnels.
Temporal pattern of excavation
The number of excavation events in each 1 min interval, from 0 to
60 min, for each of the top excavators in a trial is plotted for all ten
Table 1
A comparison of the number of excavation events performed by each of the termites
that entered a tunnel within a trial compared with the mean number of excavation
events for all termites in that trial.
Trial
n
Mean ± SE
1
2
3
4
5
6
7
8
9
10
21
13
18
17
10
13
9
17
13
14
6.714 ± 1.313a
9.846 ± 2.991a
7.556 ± 1.873a
10.529 ± 2.749a
17.5 ± 6.32a
12.307 ± 3.663a
12.444 ± 3.44a
12.764 ± 3.804a
11.153 ± 4.102a
12.857 ± 4.192a
a
Means that are significantly different at α = 0.05 (chi-square analysis, SAS Institute
1985).
Fig. 2. The percentage of total tunnel excavation in trials, binned in 5% increments, and
the mean percentage of termites (± SE) whose relative excavation effort falls within
each. Bars bearing different letters are significantly different at α = 0.001 (Kruskal–
Wallis test; Dunn's post-hoc test).
trials in Fig. 3. The temporal pattern of excavation for highly active
individuals varied between individuals. Some termites excavated
steadily over time (Fig. 3I, b and c), while others excavated in short
bursts of activity followed by an extended absence from the tunnel
(Fig. 3I, a). The mean rate (number of excavations/time) of excavation
for the 876 excavation events that were recorded in any minute
during the 10 trials was 1.3 ± 0.8 excavation events (mean ± SD)
varying from a minimum mean of 1 event in any minute where
excavation occurred (Fig. 3A, a) to a mean of 3.4 ± 2.1 per minute
(Fig. 3I, a). The maximum number of excavation events in any minute
was 7, one every 8.57 s. Looking at all of the excavation events carried
out by all workers in a trial shows that at a high excavation rate
(number of excavations/time) an individual may perform a series of
uninterrupted excavations, whereas when the excavation rate is as
low as once per minute, excavation always occurred as a part of a
group of termites alternating their digging among them.
Discussion
Tunnel excavation in termites is a group effort, but not all
individuals contribute equally to the creation of tunnels. Without
knowledge of the full repertoire of behaviors that can be conducted by
termites in the introduction chamber, we cannot know if they were
simply not motivated to enter the tunnel to excavate or if instead they
were performing another task. Even among termites that did enter the
tunnel excavation was not uniform, with a small minority of termites
responsible for most of the excavation.
The few termites that dominated excavation in each trial may be
considered key individuals, but defining their role in the organization
of labor within the three categories (organizer, catalyst, and
performer) defined by Robson and Traniello (1999) will require
further research. They clearly performed the task of excavation at high
rate relative to the other termites. In this way they are similar to
“performers” because, within the period of their peak excavation, they
are carrying out the majority of excavation. Their presence could be
inhibiting other excavators by physically blocking access to the tunnel
end, but, through their rapid excavation, they may be acting as
“catalysts,” leading others to greater effort. Similarities between the
group excavation process in termites and ants (Chen, 1937, but see
Sudd, 1972) suggest that this may occur. Future studies should
include the removal of these highly active individuals to determine if
the overall rate of excavation decreases in their absence, as it would
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P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
Fig. 3. Excavation schedules over the 1 h experimental period for the top excavators, defined as the minimum number whose labor accounted for at least 50% of total excavation. Each
point represents the number of excavation events occurring within a 1 min period. The symbols for each line correspond to individuals a through e, assigned in no particular order.
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
were they true “performers,” or if the excavation effort of other
termites decreases in their absence, indicating a catalytic function.
An intriguing possibility is that the highly active excavators are
also acting in an organizational capacity akin to the “organizers” of
Robson and Traniello (1999). The sporadic excavation at a high rate
(number of excavations/time) seen for some termite excavators
reflects a breakdown in the rotation system that results in the efforts
of the key individuals dominating the course and shape of the tunnel
over the short period of their labor. Because of the fidelity of termites
in following the tunnel to its tip to excavate (Bardunias and Su, 2009a)
and the ability of small irregularities in tunnel wall profile to release
excavation behavior (Bardunias and Su, 2010), rapid excavation over
a short period by a termite oriented along an idiosyncratic vector can
change the course of tunnels away from the previous consensus
direction or induce branching which may be followed by subsequent
excavators long after the termite has left the tunnel. This excavation
would display an organizing effect out of proportion with their
contribution to the total excavation effort of the group of termites
digging in rotation.
The breakdown of the rotation system at first seems maladaptive,
but the sinuosity that will emerge in tunnel heading as they drift
around a specific vector due to idiosyncratic excavation and
subsequent corrections may be adaptive. Such tunnels may cover a
broader search area than tunnels that are straighter and more faithful
to a vector heading. Imprecision may lead to a more efficient spread of
search area in a manner similar to the imprecision in honeybee dances
(Weidenmüller and Seeley, 1999). The ability of key individuals to
alter tunnel heading or branch in a given direction may also enable
tunnels to respond to environmental stimuli, such as moisture (Su and
Puche, 2003) or olfactory gradients (Su, 2005) more rapidly because if
an individual exists with a low threshold for detection, it can of itself
facilitate a change.
It remains to be determined why so few termites were excavating
the tunnel at any given time. The queuing described by Bardunias and
Su (2009a, 2010) by termites awaiting access to excavate at the tunnel
tip implies a role of interference between individuals in organizing
labor. Because excavation is focused at the tips of elongating tunnels,
the width of tunnels at the tip and the number of tunnel tips may be
more important in determining the size of the excavation force than
the total number of available termites outside of the tunnel. Surplus
termites would have no access to tunnel tips and would be relegated
to excavating along the tunnel walls after a period of delay (Bardunias
and Su, 2010).
Acknowledgments
We thank R. Pepin and P. Ban, (University of Florida) and S. Koi
and E. Helmick for technical assistance. This research was supported
49
by the Florida Agricultural Experiment Station and a grant from
USDA-ARS under the grant 58-6435-8-276.
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