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First published online January 30, 2009
Journal of Experimental Biology 212, 499-505 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.022988
Priority rules govern the organization of traffic on foraging trails under crowding conditions in the leaf-cutting ant Atta colombica
1 Centre de Recherches sur la Cognition animale, UMR CNRS 5169,
Université Paul Sabatier, 118 route de Narbonne, 31062 Toulouse Cedex
4, France
2 Unit of Social Ecology, Université Libre de Bruxelles, Boulevard du
Triomphe, B-1050 Bruxelles, Belgium
3 Department of Entomology, 320 Morrill Hall, University of Illinois at
Urbana-Champaign, 505 S. Goodwin Avenue, Urbana, IL 61801, USA
Author for correspondence (e-mail:
dussutou{at}cict.fr)
Accepted 25 November 2008
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Summary |
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Key words: leaf-cutting ant, traffic, priority rule, cooperation
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INTRODUCTION |
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)
(reviewed by Helbing et al.,
2007). Traffic flows could be improved if all drivers adhered to
the strict priority rules devised by traffic-engineers. Admittedly, however,
this is not always the case, and the tireless effort of the traffic police to
enforce these rules testifies to the immense difficulty of the task... When
moving on trails, social insects such as ants or termites provide one of the
best examples of a smooth and ordered traffic flow in the animal world. In
many social insect species, collective motion is organized along well-defined
recruitment trails. These trails are initially created by pheromone
deposition, but, in case of sustained traffic over a long period of time, they
can turn into long-lasting trunk-trails through the physical modification of
the environment (Hölldobler and
Wilson, 1990; Anderson and
McShea, 2001). Because social insects are central-place foragers,
the movements on these trails, unlike most collective movements that take
place in a migration context, are bi-directional. This adds to the difficulty
in the maintenance of a smooth traffic flow
(John et al., 2004) and makes
these insects an excellent model for the study of traffic dynamics and
traffic-related problems – for biologists (reviewed by
Burd, 2006) and
traffic-engineers alike (reviewed by
Chowdhury et al., 2004;
Chowdhury et al., 2005).
As ants are social insects, the behavior of individual workers is
subordinated to the interest of all the members of the colony. One should thus
expect natural selection to have selected for organizational rules that can
maximize the traffic flow on the trails in order to ensure a high rate of food
return to the nest. This is generally the case
(Burd et al., 2002). However,
the question of the robustness of these organizational rules arises. For
example, bottlenecks can be created if some of the trail sections are too
narrow, as occurs for example when ants are moving on liana or small branches.
Overcrowding can occur, and this can slow down the progression along the
trails (Burd et al., 2002;
Burd and Aranwela, 2003;
Dussutour et al., 2005).
However, solutions exist to prevent overcrowding. In the black garden ant
Lasius niger, for example, overcrowding is avoided by a temporal
organization of the flow as a sequence of alternating clusters of inbound and
outbound ants (Dussutour et al.,
2005). This organization emerges through the implementation of
priority rules between ants, and it allows the minimization of head-on
encounters. It explains why a narrow trail can sustain the same flow intensity
as a wide trail, thus ensuring the same rate of food return to the nest. In
Lasius niger, however, ants carrying internal loads (i.e. within
their bodies) coming from the food source do not behave differently than
emptied ants coming from the nest. The priority rules generating the ant
clusters are the same in both directions: the ant that gives way is always the
one that has the possibility to do it, by moving aside and waiting before
entering a narrow passageway. Moreover, nestbound loaded ants and outbound
emptied ants do not have a significantly different locomotory rate
(Mailleux et al., 2000). In
species carrying external loads, by contrast, laden individuals returning to
the nest are always given way by those going to the food source [army ants:
Dorylus sp. and Eciton burchelli (Gottwald, 1995;
Couzin and Franks, 2003);
termites: Longipeditermes longipes and Hospitalotermes
(Miura and Matsumoto, 1998a;
Miura and Matsumoto, 1998b)]
and they progress more slowly than unloaded individuals [Atta
cephalotes (Rudolph and Loudon,
1986); A. colombica
(Lighton et al., 1987);
Eciton hamatum (Bartholomew et
al., 1988); Eciton burchelli (Gottwald, 1995;
Couzin and Franks, 2003);
Pogonomyrmex rugosus (Lighton et
al., 1993); P. maricopa
(Weier and Feener, 1995);
Dorymyrmex goetschi
(Torres-Contreras and Vasquez,
2004)]. This difference in speed could potentially have a great
impact on the organization of traffic. For example, differences in speed
between vehicles are known to generate a temporal organization of traffic
whereby fast vehicles adjust their speed to that of slower ones. This
phenomenon creates clusters of vehicles moving in the same direction and leads
to a reduction in the overall flow of vehicles on a road
(Helbing and Huberman, 1998;
Nagatani, 2000) (reviewed by
Chowdhury et al., 2000;
Helbing, 2001;
Helbing et al., 2007).
Here, we examine the effect of trail width on traffic organization in ants
carrying external loads. We chose leaf-cutting ants for our study because, in
these species, the relation between speed and load mass is well documented
[Atta cephalotes (Rudolph and
Loudon, 1986; Burd,
2000; Burd and Aranwela,
2003); A. colombica
(Lighton et al., 1987;
Shutler and Mullie, 1991;
Burd, 1996); Atta
vollenweideri (Röschard and
Roces, 2002); Acromyrmex lundi
(Roces and Nuñez,
1993)]. Moreover, although they have never been precisely
quantified, the existence of priority rules has been reported
(Burd et al., 2002). Our
experiment involved forcing ants going from their nest to a food source to
cross a narrow bridge whose width allowed the passage of a maximum of two ants
at a time. We show that, in this condition, a temporal organization of traffic
through a cooperative behavior between ants can emerge. This organization
facilitates minimization of head-on encounters between unloaded ants traveling
in opposite directions and promotes head-on encounters between outbound ants
traveling away from the nest and those returning from the food source loaded
with food. These contacts could potentially stimulate outbound ants to cut and
retrieve leaf fragments to the nest and thus increase the colony foraging
efficiency (Dussutour et al.,
2007).
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MATERIALS AND METHODS |
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). In this species, small colonies less than one year old have
103–104 workers, whereas established colonies can
contain 105–106 workers
(Hart and Ratnieks, 2001). We
used an experimental colony that consisted of one queen, brood, approximately
20,000 workers and 
11,000 cm3 of fungus distributed in four
clear plastic nest boxes (WxLxH: 12x23x10 cm). The
nest boxes were kept in a plastic tray (WxLxH:
40x60x15 cm) whose walls were coated with Fluon to prevent ants
from escaping. The nests were regularly moistened, and the colony was kept at
room temperature (30±1°C) with a 12 h:12 h light:dark photoperiod.
We supplied the colony with leaves of Malus coccinela four times a
day (08:00 h, 12:00 h, 16:00 h and 20:00 h). The leaves were placed in a
plastic tray (WxLxH: 40x60x15 cm), which was used as a
foraging area and was linked to the colony by a plastic bridge 300 cm long and
5 cm wide. The bridge length we used is consistent with the foraging distance
measured for small colonies in the field
(Kost et al., 2005). In the
experiments, the bridge was removed and replaced by a new unmarked bridge of
the same width (50 mm: `wide bridge') or of a reduced width (5 mm: `narrow
bridge').
Experimental procedure
Because the removal of the marked bridge and its replacement by a new
unmarked one was generally followed by a sharp decrease in ant traffic, a
period of 24 h was allowed before starting an experiment and measuring the
effect of bridge change on the characteristics of the traffic. One hour and a
half before the start of an experiment, the colony was deprived of foraging
material by removal of all leaves remaining in the foraging area. Foraging
material was then placed again in the foraging area at the start of the
experiment [see Dussutour and colleagues
(Dussutour et al., 2007) for
details on the experimental procedure].
Twelve replicates of the experiment were achieved with each type of bridge (wide bridge and narrow bridge). In all replicates, the traffic on the bridge was filmed from above at the center of the bridge for 60 min with a Sony Digital Handycam DCR VX 2000E camera.
Data collection
Temporal organization of the flow of ants
We first analyzed the temporal organization of the flow as a function of
bridge width. For five replicates chosen randomly for each bridge, we noted
during one hour the travel direction of the sequence of successive ants (+1
for inbound ants, –1 for outbound ants) crossing a line in the middle of
the bridge. The number of individuals in each sequence was: N=3836,
N=5627, N=6317, N=5622, N=5692 ants for
the narrow bridge and N=8822, N=8224, N=9556,
N=7590, N=9821 ants for the wide bridge. In addition, we
also noted whether each inbound ant was laden.
In order to investigate whether the sequences of inbound and outbound ants
were random or consisted of an alternation of groups of ants traveling in
opposite directions, we used a one-sample runs test of randomness
(Siegel and Castellan, 1988).
This test is based on the number of runs in a sequence of categorical data. A
run is defined as a succession of data belonging to the same category (in our
case +1 or –1) and is delimited at both ends by data belonging to the
other category. The total number of runs in a sequence gives an indication of
whether or not the sequence is random. The occurrence of very few runs
suggests a time trend or some bunching owing to a lack of independence between
data. Conversely, the occurrence of many runs indicates systematic cyclical
fluctuations of a short time period. We tested with a Kolmogorov–Smirnov
two-sample test whether the distribution of the size of the groups of ants
traveling in the same direction was random by comparing it with that given by
a theoretical sequence of same size generated on a basis of equal probability
of occurrence of nestbound and outbound ants.
Travel duration
We investigated how travel duration was affected by the direction of
travel, the load carried and the position occupied by an ant within a group.
We measured on a single replicate of the experiment with a narrow bridge the
travel duration of a sample of ants traveling on a 15 cm section at the centre
of the bridge. We defined four categories of ants: outbound ants, inbound
laden ants, inbound unladen ants following a laden ant and inbound unladen
ants preceding a laden ant. We followed 110 ants of each category. We
considered only the individuals that did not encounter other ants while
traveling the bridge section. The durations were measured from the time stamp
of the video frames, allowing a precision of 1/25=0.04 s. The measures began
15 min after the beginning of the experiment, when the outbound and nestbound
flow of ants were at equilibrium.
Interaction probability and time loss per contact
In order to assess the probability for an inbound unladen ant to contact an
outbound unladen ant, we counted in a single replicate with the narrow bridge
the number of encounters occurring per ant for a sample of 100 unladen ants
preceding a laden ant and traveling to the nest on a 15 cm section at the
center of the bridge. An encounter was considered each time an ant passes
another one traveling in the opposite direction, whether a physical contact
occurred or not between the ants. Encounters with or without physical contact
were distinguished. A contact was always the result of a head-on collision.
The probability of being contacted during an encounter was estimated by
regressing the number of encounters with physical contact on the total number
of encounters with or without contact.
The net travel duration (i.e. including the time spent in contact) for each ant was also measured. The time lost per encounter with contact was estimated by regressing the net travel duration on the number of encounters in which a contact occurred. The measurements began 15 min after the beginning of the experiment, when the outbound and nestbound flow of ants were at dynamic equilibrium.
Priority and cooperative rules between ants
To investigate the mechanisms allowing the formation of alternating groups
of ants traveling in opposite directions on the narrow bridge, we analyzed on
a single replicate the outcome of head-on collisions between outbound ants and
inbound laden ants (N=300), and that between outbound ants and
inbound unladen ants (N=400). Typically, after a collision occurred,
one ant moves to the bridge side to allow the passage of the oncoming ant
(Fig. 1). We noted for each
collision which of the inbound or outbound ant moved to the side of the bridge
in order to give way and how many ants benefited from this behavior by
following the ant that was given way. This latter effect corresponds to a
cooperative behavior between ants because the subsequent ants benefit from the
passage of the leading ant (the ant that was given way)
(Fig. 1).
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RESULTS |
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2=6.06,
d.f.=4, P=0.195, mean proportion ±s.d.: 0.24±0.01). The
proportion of laden ants in each group varied according to group size
(Fig. 3). For groups of less
than five workers, the proportion of laden ants was significantly lower than
the expected proportion – that is, the mean proportion of laden ants in
the inbound flow (0.24). This means that laden ants were overrepresented in
inbound groups whose size was greater than five individuals. Moreover, laden
ants were not randomly distributed within the groups. They were significantly
more likely to occupy the first and second position within the groups than any
other positions (Fig. 4).
Moreover, when the size of the group was higher than three individuals, the
proportion of groups led by a laden ant was significantly higher than the
expected value – that is, the proportion of laden ants in each group
size (Fig. 5). Thus, the size
of a group led by a laden ant was significantly higher than the size of a
group led by an unladen ant (Mann–Whitney test, U=502 228,
P<0.001, mean ±s.d., 6.58±5.29 and 4.49±4.08,
respectively).
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Interaction probability and time loss per contact
The regression model of the number of encounters with physical contacts on
the number of encounters per ant yielded a significant linear relationship
(ANOVA for the model: F1,99=198.94, P<0.001)
and accounted for 67% of the variance. As expected, the number of contacts
increased significantly with the number of encounters (t=14.10,
P<0.001). The slope of the regression line describing the
relationship between the number of encounters with contact and the number of
encounters indicates that the probability to physically contact another ant
during an encounter was 0.30. An inbound unladen ant contacted on average four
ants per 15 cm (mean ± s.d.: 3.9±2.4). The regression model of
the net travel duration on the number of contacts was also significant (ANOVA:
F1,99=297.77, P<0.001) and accounted for 75.2%
of the variance. Travel duration increased significantly with the number of
contacts (t=16.38, P<0.001). The time lost per contact
was on average 0.80 s.
Priority and cooperative rules between ants
Close observations of the head-on encounters occurring on the bridge
between ants traveling in opposite directions show that the majority of
outbound ants stopped and gave way to the laden ants (in 294 out of 300
head-on encounters) but were mostly given way by unladen ants traveling away
from the food source (in 301 out of 400 head-on encounters). When an ant gave
way to another, it generally moved to the side of the bridge and allowed the
passage of the oncoming ants before returning to the top of the bridge. The
probability for an ant to benefit from the passage of the leading ant depended
both on its position as a follower and on the category of the leading ant
(Fig. 6). When an outbound ant
gave way to an inbound ant, the number of individuals that benefited from its
behaviour was significantly higher when the inbound ant was laden than when it
was not (mean ±s.d.: 5.40±3.16 and 1.18±1.40 ants,
respectively) (one-way ANOVA F2,693=62.53,
P<0.001, followed by a Bonferroni post-hoc test)
(Fig. 6, inset). Moreover, the
number of individuals that benefited from the passage of the leading ant was
significantly lower when an outbound ant gave way to an inbound unladen one
than when an inbound unladen ant gave way to an outbound one (1.18±1.40
and 3.68±3.90 ants, respectively).
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DISCUSSION |
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), avoid crowding on recruitment trails by changing the
temporal organization of the flows of inbound and outbound individuals. On
wide bridges, the sequence of outbound and inbound ants was not different from
random, whereas alternating groups of inbound and outbound ants were observed
on narrow bridges.
We found that laden workers moved more slowly on a recruitment trail than
unladen workers. This confirms the results obtained by others authors
(Lighton et al., 1987;
Burd, 1996;
Burd, 2000;
Shutler and Mullie, 1991;
Couzin and Franks, 2003). We
observed in addition that inbound unladen ants generally never attempted to
overtake the laden ants in front of them and instead preferred to slow down
their pace and stay behind. This speed adjustment passively induces an
accumulation of ants behind laden ants and generates inbound groups led by
laden ants. Similar phenomena are also observed in vehicular traffic when a
mixture of trucks and cars are present on a highway
(Peeta et al., 2005) and in
pedestrians when individuals prefer to follow a person ahead than move against
an opposing stream (reviewed by Helbing et
al., 2007).
When an outbound ant encounters a group led by a laden ant, it first stops
and gives way to the laden ant. This phenomenon has also been reported in army
ants [Dorylus sp. (Gottwald, 1995); Eciton burchelli
(Couzin and Franks, 2003)] and
in the termites Longipeditermes longipes and Hospitalotermes
(Miura and Matsumoto, 1998a;
Miura and Matsumoto, 1998b).
The outbound ant generally moves to the side of the bridge, allows the passage
of the incoming ants and returns to the top of the bridge. This behavior
prevents the fission of the incoming group of ants. In addition, as the
outbound ant moving to the side is frequently followed by other ants, this
produces an accumulation of outbound ants on the side of the bridge. As soon
as the path is free, these ants return to the top of the bridge to move as a
cluster. The priority rules followed by outbound ants might therefore help to
maintain the inbound groups led by laden ants along the recruitment trail. At
the same time, it also generates groups of outbound ants. The temporal
organization of the flow can therefore be described as a self-organized
process emerging from the simple rules of priority between individuals moving
in opposite directions.
What is the advantage for an inbound unladen ant to move slower by staying
behind a laden ant instead of progressing more rapidly by moving at its
desired speed? The most likely explanation is that the ants that follow a
laden ant gain benefit of the right of way it is given by other ants. These
ants avoid head-on collisions with outbound ants and thus spare the time they
would waste by moving to the side of the bridge as they do most of the times
when they face an outbound ant. On a 15 cm section of the bridge, an inbound
unladen ant contacts on average four outbound ants and wastes on average 0.8 s
per contact. Therefore, compared with an inbound unladen ant that does not
make any contacts and moves at its desired speed (travel duration: 6.57 s), an
unladen ant preceding a laden ant wastes on average 3.2 s in frontal contacts,
whereas an unladen ant following a laden ant wastes 1.6 s by adjusting its
speed to that of the laden ant it is following. An unladen ant traveling on a
300 cm bridge would thus waste 32 s by staying behind a laden ant and not
overtaking it while an unladen ant overtaking a laden ant would waste 64 s. In
leaf-cutting ants, unladen ants, in the same way as laden ants, take part in
the recruitment process by laying a chemical trail
(Evison et al., 2008).
Therefore, returning earlier to the colony allows acceleration of the build-up
of the recruitment trail, which in turn allows a faster recruitment to the
food source (Roces and Hölldobler,
1994).
Another advantage generated by the temporal organization of the flow is
that head-on encounters between laden ants traveling away from the food and
outbound ants traveling to the food are facilitated. Contacts between workers
in our experiments were not simple accidents occurring at random. Unladen
returning ants avoided outbound foragers by moving to the side, whereas laden
returning ants never attempted to do so, possibly because their loads hindered
their capacity to maneuver (Zollikofer,
1994). An outbound ant encountering an inbound group led by a
laden ant generally moves to the side of the bridge, allows the passage of
incoming ants, returns to the top of the bridge and there encounters again
another group led by a laden ant. As a result of these priority rules, an
outbound ant on its way to the food source contacts mostly laden ants. These
contacts might increase information transfer on the availability of food at
the end of the trail and stimulate outbound workers to cut and transport leaf
fragments, leading to an increase in foraging efficiency
(Dussutour et al., 2007). This
phenomenon might be particularly important when leaf-cutting ants are
traveling on narrow branches to reach leaves because it could be a cue as to
continue or not on a particular branch.
It remains to be seen whether, in the natural environment, trail widths are
adjusted to optimize the net benefit of the trail, given the traffic demand,
the cost of clearing (Howard,
2001) and the effect of traffic density on contact rates and
information exchange. Indeed, according to our results, building wider
foraging trails not only could be more costly but could also result in a lower
foraging efficiency. This might also explain why leaf-cutting ants in their
natural environment often prefer to settle their trails along small fallen
logs or branches instead of building a wider trail by clearing the leaf
litter.
Leaf-cutting ants present an interesting comparison with vehicles moving on
highways or with pedestrians crossing a corridor
(Helbing et al., 2007). Like a
mixture of cars, trucks and other vehicles with a range of desired speeds,
leaf-cutting ant foragers are highly polymorphic and vary widely in the
locomotion speed they can attain (Burd,
2000). The mechanisms leading to the formation of clusters of ants
on a foraging trail are analogous to those leading to clusters of cars on a
highway. The temporal organization of the flow of ants we observed is also
reminiscent of that observed in bidirectional pedestrian traffic through a
narrow passageway (Helbing et al.,
2005). If opposing flows of pedestrians interrupt at a narrow
passageway, oscillations in passing direction are observed – that is, a
temporal organization of the flow (Helbing
et al., 2005). Typically, groups of individuals rather than single
individuals go through the passage before individuals located on the other
side have a chance to do the same. This occurs because it is easier to follow
someone than to move against an opposing stream. The resulting stream of
individuals going through the passage releases the pressure in the pedestrian
crowd on one side, while the pressure on the other side increases. When the
pressure difference reaches a certain threshold, the stream of people is
stopped and individuals on the other side in turn are allowed through the
passage (Helbing et al.2005).
In other ways, however, ant traffic is distinct from either pedestrian or
vehicular traffic. Human pedestrians anticipate potential interactions, such
as collisions, and act to avoid them in order to maintain high velocities and
flows in the face of rising concentrations
(Helbing et al., 2007). This
is not the case of ants that, with their small mass, are not damaged by
collisions and do not seem to employ particular means to avoid incoming
workers in traffic streams. Ants have much lower inertia than humans: they can
rapidly come to a halt and then accelerate to regain their former speed.
Moreover, ants from the same colony presumably act with a unity of purpose
very different to the multiplicity of individual interests pursued by
pedestrians or drivers moving in a traffic stream.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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  K. Knight ANTS OBEY ROAD RULES TO KEEP TRAFFIC FLOWING J. Exp. Biol., February 15, 2009; 212(4): i - i. [Full Text] [PDF]
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(i+1). Laden ants were significantly
overrepresented in the first and second position and were significantly
underrepresented in position >6th. *P<0.05,
**P<0.01, ***P<0.001.
