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Memory span for heterospecific individuals’ odors in an ant, Cataglyphis cursor

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  • Université Sorbonne Paris Nord

Abstract and Figures

Only recently have researchers studied the ability of ants to learn and remember individual heterospecific odors. Cataglyphis cursor adults have the capacity to learn these odors, but the duration of their memory and the factors that affect its formation remain unknown. We used a habituation/discrimination paradigm to study some of these issues. C. cursor adult workers were familiarized to an anesthetized Camponotus aethiops on four successive encounters. Then they were either isolated or placed with 20 nestmates for a certain length of time before undergoing a discrimination test that consisted of reintroducing the familiar C. aethiops, as well as introducing an unknown member of the same colony. The results showed that adult C. cursor ants can retain in memory a complex individual odor for at least 30 min, as well as differentiate it from the odor of another closely related individual. However, when ants were replaced in a rich social background between the habituation and the discrimination trials, we did not observe a significant discrimination between the known and unknown C. aethiops ants. Our study shows, for the first time, the existence of long-term memory for individual odors in mature ant workers.
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Learning abilities in insects are well documented, es-
pecially for navigation and foraging activities. Bees and
ants are able to learn visual pattern sequences and to reuse
them to orient themselves (Chameron, Schatz, Pastergue-
Ruiz, Beugnon, & Collett, 1998; Horridge, 2006; Mac-
quart & Beugnon, 2004; Zhang, Mizutani, & Srinivasan,
2000). Bees are also well known for their notable olfactory
learning and memory abilities (Horridge, 2006; Zhang
et al., 2000). These olfactory abilities have been studied in
other models such as fruit flies (Drosophila melanogaster;
Davis, 2005), crickets (Gryllus bimaculatus; Matsumoto
& Mizunami, 2000, 2005), and cockroaches (Periplaneta
americana; Sakura & Mizunami, 2001; Sakura, Okada, &
Mizunami, 2002; Watanabe, Kobayashi, Sakura, Matsu-
moto, & Mizunami, 2003).
Among social insects, olfactory abilities are essential in
kin and colonial recognition. In a colony, every individual
carries a “gestalt odor” across the surface of the body.
This mixture comprises the odors of all of the colony’s
individuals and is spread through trophallaxis and licking
(Errard, Hefetz, & Jaisson, 2006; Lahav, Soroker, Hefetz,
& Vander Meer, 1999; Lenoir, Fresneau, Errard, & Hefetz,
1999). Early in adult life, each colony member must learn
these cues, which, when encoded as a template, serve not
only to determine the colonial membership of other indi-
vidual ants, but also to discriminate among them (Crozier
& Pamilo, 1996).
The learning of colonial odor in Cataglyphis cursor
takes place during the first larval stage (Isingrini, Lenoir,
& Jaisson, 1985). This learning is predicted to be stable;
information acquired during the larval stage is known to
persist through the metamorphosis into adulthood. How-
ever, there is another learning period after adult emer-
gence (Isingrini et al., 1985; Jaisson, 1974). Moreover, the
colonial visa is flexible because it depends on each indi-
vidual odor, the colony’s demographic fluctuations (Breed
& Bennett, 1987), the season, and resources (Nielsen,
Boomsma, Oldham, Petersen, & Morgan, 1999; Provost,
Bonavita-Cougourdan, & Rivière, 1994; Vander Meer &
Morel, 1998; Vander Meer, Saliwanchik, & Lavine, 1989).
That is why the template must be constantly updated and
requires cerebral plasticity—in particular, efficient learn-
ing and memory abilities.
Crozier (1987) proposed another model for both primi-
tive ant societies and other insect societies that have rela-
tively few individuals. In this model, there is no gestalt odor
process; each individual keeps its own chemical character-
istics. Recognition of each of the members of the colony
occurs via individual recognition. In typical ant societies, in
which individuals live in colonies of hundreds or thousands
of individuals, this kind of recognition system was assumed
to be improbable. However, contrary to this assumption, re-
cent studies have shown homospecific individual discrimi-
nation and recognition among social insects, such as wasps
(Polistes fuscatus; Tibbetts, 2002) and founding queen ants
(Pachycondyla villosa; D’Ettore & Heinze, 2005). Both
systems are characterized by long-term, stable dominance
hierarchies enforced by individual aggression.
Among Cataglyphis ants, discrimination of heterospe-
cific individuals and nonnestmate homospecific individu-
als occurs in a nonhierarchical context, and the learning
of each individual odor was observed using a habituation
319 Copyright 2008 Psychonomic Society, Inc.
Memory span for heterospecific individuals’
odors in an ant, Cataglyphis cursor
Em m E l i n E Fo u b E r t a n d El i s E no w b a h a r i
LEEC CNRS UMR 7153, Université Paris 13, Villetaneuse, France
Only recently have researchers studied the ability of ants to learn and remember individual heterospecific
odors. Cataglyphis cursor adults have the capacity to learn these odors, but the duration of their memory and the
factors that affect its formation remain unknown. We used a habituation/discrimination paradigm to study some
of these issues. C. cursor adult workers were familiarized to an anesthetized Camponotus aethiops on four suc-
cessive encounters. Then they were either isolated or placed with 20 nestmates for a certain length of time before
undergoing a discrimination test that consisted of reintroducing the familiar C. aethiops, as well as introducing an
unknown member of the same colony. The results showed that adult C. cursor ants can retain in memory a complex
individual odor for at least 30 min, as well as differentiate it from the odor of another closely related individual.
However, when ants were replaced in a rich social background between the habituation and the discrimination tri-
als, we did not observe a significant discrimination between the known and unknown C. aethiops ants. Our study
shows, for the first time, the existence of long-term memory for individual odors in mature ant workers.
Learning & Behavior
2008, 36 (4), 319-326
doi: 10.3758/LB.36.4.319
E. Nowbahari, elise.nowbahari@leec.univ-paris13.fr
320 Fo u b e r t a n d no w b a h a r i
series, 16 C. cursor workers (4 from each colony) were removed
from the foraging area near the nest entrance and individually
marked on the abdomen by a distinct spot of odorless, indelible paint
(Uni Paint Marker PX 20, Mitsubishi Pencil Co.). The ants were
placed in a box with other test members from their colony, apple–
honey mixture, and moisturized cotton, until the beginning of the
tests the following day.
Encounters occurred in a circular box that was 3.5 cm in diam-
eter. Two individuals were tested in parallel for the purpose of mak-
ing crossed encounters (Figure 1). C. cursor workers were set in the
encounter area at least 1 min before the presentation of the stimulus
in order to reduce their excitability following the manipulation. The
test area surface was covered with filter paper and changed after
each encounter to avoid chemical markings. During the 10 min
between encounters, the ant was gently placed in an individual box
with wet cotton, allowing it to drink. Stimulus C. aethi ops were
anesthetized with CO2 to prevent their behavior from biasing the
response of C. cursor. The stimulus ants were kept under an an-
esthetic between encounters. This procedure (using CO2) allowed
us to keep stimulus ants alive and avoid chemical alterations that
would induce behavioral modifications (necrophoric behavior) in
individuals perceiving it (Ataya & Lenoir, 1984; Wilson, Durlach,
& Roth, 1958). CO2 anesthesia is more reliable than cooling, which
can lead to substantial mortality rates. Moreover, the immobility
duration acheived by cooling is shorter than that achieved by using
CO2 anesthesia. Cold also restricts molecular volatility from the
cuticle. In both experiments, stimuli ants (C. aethi ops) were placed
in a box with their nestmates during the rest period.
Two experiments were conducted. In Experiment 1, we tested
the memory span for learned odors belonging to heterospecif ic
individuals. Experiment 2 was carried out to determine whether
the social exposure with the nestmate group would interfere with
the heterospecific memory. In addition, a control test was carried
out to ensure that olfactory marks had not been deposited on the
stimulus ant.
All encounters were videotaped, and the occurrence of behavior
patterns listed in Table 1 was blind counted. The sum of these occur-
rences determined the number of agonistic behaviors, which were
analyzed using nonparametric inference with permutation tests (also
called randomization tests) for paired samples and for independent
process without reinforcement (Nowbahari, 2007). These
heterospecific and homospecific individual discrimina-
tion abilities in workers can be understood in terms of the
“dear enemy” phenomenon with regard to allocolonial or
heterospecific individuals and in the context of the prefer-
ence networks among members of the same colony (Delat-
tre & Nowbahari, 2007). Individual recognition in a hier-
archical context seems to require long-term memory and
is robust enough not to be erased by several encounters
(Dreier, van Zweden, & D’Ettorre, 2007). In this study,
we tested whether the memory of the odor of a worker
ant from a different species (i.e., Camponotus aethiops)
would be retained by C. cursor ants in long-term memory,
as well as whether this learning would be imperturbable.
GENERAL METHOD
Ants and Rearing Conditions
Two ant species were used for these experiments: C. cursor and
C. aethiops. For each test series, we tested 16 C. cursor from four
monogynous colonies, each of which included one reproductive
queen. Three of these colonies were sampled at Menerbes, and the
fourth was sampled at Bonnieux (Vaucluse, France) in April 2006.
These colonies were reared in the laboratory in a cylindrical, closed
nest connected with a foraging area. Ants were fed on mealworm
larvae and apple –honey mixture twice a week. The temperature of
the breeding room was kept at 28º 6 2ºC, with a humidity level of
20% to 40% and a 12:12-h light:dark cycle.
C. aethiops ants were used as stimuli. This species is sympatric
with C. cursor. The two colonies used for these experiments were
collected in Touraine, France, in 2006, and were reared in the same
laboratory, in the same room, and under the same conditions as the
C. cursor colonies.
Procedure
We used the habituation/discrimination test method usually ap-
plied in studies of vertebrates (see, e.g., Todrank & Heth, 2003) and
adapted for use with ants (Nowbahari, 2007). For each experimental
Habituation (Tests 1 to 4) Discrimination (Test 5)
= Cataglyphis cursor = Camponotus aethiops
Figure 1. Schematic setup of the habituation/discrimination experimental
procedure.
Me M o r y F o r in d i v i d u a l s ’ od o r s in a n t s 321
unfamiliar individual after at least 30 min, which is con-
sidered long-term memory for an insect. The rare studies
of long-term memory using habituation and stimuli that
possess a particular social valence include those from our
laboratory, using Cataglyphis niger (Nowbahari, 2007),
and a recent study by Dreier et al. (2007), which showed
that unrelated founding queens of P. villosa and Pa c h y-
chondyla inversa retain information about the individual
identities of other founding queens as long as 24 h after
separation. However, Dreier et al. focused on a homospe-
cific hierarchical context, in which individual recognition
facilitates a stable linear dominance hierarchy between
queens and workers. In this small-group context, the im-
portance of individual recognition is obvious.
EXPERIMENT 2
The Effect of Social Environment on Lifetime
Retention of Individual Learned Odors
Method
This experiment was conducted to determine whether the social
environment influenced the memory span. We proceeded as in Ex-
periment 1, except that during the 10- or 30-min rest period, which
followed immediately after the four habituation trials, each subject
was placed in a small homocolonial group of 20 individuals taken
directly from the nest.
Results
Habituation trials
. As in Experiment 1, we observed
habituation to the encountered C. aethiops. C. cursor ants
were more aggressive against the stimulus C. aethiops dur-
ing the f irst encounter than during the fourth (permutation
test for paired samples: for the 10-min rest period, n 5 14,
p 5 .02; for the 30-min rest period, n 5 14, p 5 .05; for
the two delays together, n 5 28, p 5 .0016) (Figure 3).
Discrimination test
. Unlike the behavior we observed
in Experiment 1, C. cursor ants did not show a signif icant
discrimination between the 2 C. aethiops stimulus ants, ei-
ther after a 10-min (n 5 14, p 5 .30) or 30-min (n 5 14,
p 5 .19) rest period (see Figure 3). Although a comparison
of the data in Experiments 1 and 2 might suggest that ants
were simply less aggressive in Experiment 2, a statistical
analysis of the interaction between the two experiments and
the test stimuli revealed no differences in aggressive behav-
ior between the two experiments (permutation test for two
independent samples: for the 10-min rest period, p 5 .18;
for the 30-min rest period, p 5 .30; for these two delays
together, p 5 .092). As in Experiment 1, the occurrence of
agonistic behavior of C. cursor toward 2 stimulus C. aethi-
ops was not significantly different when we compared the
10-min rest period test with the 30-min rest period test (per-
mutation test for two independent samples, p 5 .92). In the
same way, the sum of these occurrences was not signifi-
cantly different when we compared Experiments 1 and 2
(permutation test for two independent samples, p 5 .30).
As in Experiment 1, the sum of occurrences of agonistic
behaviors of C. cursor toward 2 stimulus C. aethiops was
not significantly different when we compared the 10-min
rest period test with the 30-min rest period test (permuta-
tion test for two independent samples, p 5 .92). In the
samples with StatXact 7 (Cytel, 2005). The statistics were consid-
ered significant at p # .05.
EXPERIMENT 1
Memory Span for
Heterospecific Individuals’ Odors
Method
In this experiment, we tested the memory span for the learned
odors belonging to heterospecif ic individuals. Each C. cursor
worker was habituated to a C. aethiops anesthetized by CO2, in four
successive encounters of 3 min each, separated by 10-min inter-
vals (habituation trials). After the four habituation trials, C. cursor
ants were isolated from C. aethiops stimuli for a 10-, 30-, or 60-min
interval (rest period). During this rest period, C. cursor ants were
socially isolated. After the rest/isolation period, we proceeded with
a discrimination test: For each C. cursor, we presented both the fa-
miliar and a homocolonial unknown C. aethiops.
Results
Habituation trials
. During the four successive en-
counters, we observed habituation on agonistic behavior.
C. cursor adult ants were more aggressive toward the
stimulus C. aethiops during the first encounter than dur-
ing the fourth (permutation test for paired samples signifi-
cant in each situation: For 10 min of isolation, n 5 16, p 5
.03; for 30 min of isolation, n 5 15, p 5 .0009; For these
two situations together, n 5 31, p 5 .0003; for 60 min of
isolation, n 5 14, p 5 .04) (Figure 2).
Discrimination test
. When the rest period was either
10 min (a time period that was identical to that between
the habituation trials) or 30 min in duration, C. cursor ants
were able to discriminate between familiar and unfamiliar
C. aethiops. More agonistic behaviors were exhibited to-
ward the unfamiliar ant than toward the familiar one (per-
mutation test for paired samples: For 10 min, n 5 16, p 5
.0056; for 30 min, n 5 15, p 5 .029) (Figure 2). The sum
of occurrences of agonistic behaviors of C. cursor toward
the 2 stimulus C. aethiops was not signif icantly differ-
ent during the discrimination test when we compared the
10-min rest period test with the 30-min rest period test
(permutation test for two independent samples, p 5 .80).
However, when the rest period was 60 min, C. cursor
ants did not respond differently to the familiar and unfa-
miliar C. aethiops ants (n 5 14, p 5 .34; Figure 2).
Discussion
Our results from Experiment 1 showed that C. cursor
adult ants are able to learn the individual odor of a het-
erospecific ant and discriminate it from the odor of an
Table 1
Observed Behaviors During Trials
Behavior Description
Opening of mandibles Opening of mandibles near the stimulus,
often after an antennal contact
Biting Seizing the stimulus body with mandibles
Gaster flexion
Folding abdomen toward the stimulus,
frequently seizing it with mandibles, and
spraying formic acid
322 Fo u b e r t a n d no w b a h a r i
A
34
29
24
19
14
9
4
–1
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 10-min Isolated
Familiar Unfamiliar
Discrimination 10-min Isolated
***
24
19
14
9
4
–1
B
34
29
24
19
14
9
4
–1
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 30-min Isolated
Familiar Unfamiliar
Discrimination 30-min Isolated
24
19
14
9
4
–1
*** *
C
34
29
24
19
14
9
4
–1
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 60-min Isolated
Familiar Unfamiliar
Discrimination 60-min Isolated
24
19
14
9
4
–1
*NS
Figure 2. Number of agonistic behaviors expressed by a C. cursor ant toward a Camponotus ant in 3 min during the habituation/
discrimination procedure for three experimental conditions: (A) 10 min, (B) 30 min, or (C) 60 min of rest period, during which C. cur-
sor ants were isolated. Horizontal lines represent the 10th, 25th, 50th (median), 75th, and 90th percentiles. Scores above the 90th and
below the 10th percentiles are plotted as individual points.
*
p # .05.
**
p # .01.
***
p # .001.
Me M o r y F o r in d i v i d u a l s ’ od o r s in a n t s 323
that the ants did not actively delete “old” individual odor
memories; rather, we suggest that the information may not
have been recalled correctly, which is why the ant was not
able to discriminate a familiar from an unfamiliar indi-
vidual. This inhibitor effect may be due to the interference
caused by the perception of its sisters’ odors and/or by the
update of the colonial template via contact with conge-
ners. This effect is immediate, because C. cursor did not
discriminate significantly between 2 C. aethiops ants after
10 min with its sisters.
Ichikawa and Sasaki (2003) showed, in honeybees, that
the development of learning abilities requires social ex-
perience. Indeed, those abilities deteriorate when honey-
bees are socially deprived. Acquisition and maintenance
of learning abilities require continual input of appropriate
stimulation. The results of our study show that C. cursor
ants are able to maintain the new individual information
after being socially deprived, but returning to their nest-
mates perturbs or prevents individuals from discriminating
same way, the sum of these occurrences was not signifi-
cantly different when we compared Experiments 1 and 2
(permutation test for two independent samples, p 5 .30).
Discussion
If C. cursor regains a rich social background of 20 nest-
mates after the habituation, as if returning to the nest, we
descriptively observe a differentiation between two odor
stimuli. The ants discriminate between the familiar and
unfamiliar heterospecific individual odors, but the differ-
ence of intensity of agonistic behaviors toward unfamiliar
individuals in comparison with that toward the familiar
individual is less evident than in the individual condition
(Experiment 1) and is nonsignificant. It seems that the
ants were uncertain about how to choose and react toward
known and unknown strangers. Simulation of a return to
the nest may disturb access to memorized information,
but it does not necessarily block it. That is, no certain evi-
dence for memory loss is at hand. We propose tentatively
A
34
29
24
19
14
9
4
–1
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 10-min Social
Familiar Unfamiliar
Discrimination 10-min Social
24
19
14
9
4
–1
*NS
B
34
29
24
19
14
9
4
–1
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 30-min Social
Familiar Unfamiliar
Discrimination 30-min Social
24
19
14
9
4
–1
*NS
Figure 3. Number of agonistic behaviors expressed by a C. cursor ant toward a Camponotus ant in 3 min during the habituation/
discrimination procedure for a rest period of (A) 10 min and (B) 30 min, during which C. cursor ants were set back with 20 nestmates.
Horizontal lines represent the 10th, 25th, 50th (median), 75th, and 90th percentiles. Scores above the 90th and below the 10th percen-
tiles are plotted as individual points.
*
p # .05.
324 Fo u b e r t a n d no w b a h a r i
familiar pellet and a clean, unfamiliar one that had been molded at
the same time as the familiar one.
Results
Habituation trials
. During four successive trials, as in
Experiment 1, C. cursor ants exhibited agonistic behavior
in the first encounter with fixative gum pellets, and it de-
creased during the four successive trials (permutation test
for linked data, n 5 20, p 5 .03).
Discrimination test
. No difference in agonistic be-
havior was observed between encounters with the familiar
and the unfamiliar fixative gum pellets (n 5 20, p 5 1;
Figure 4).
Discussion
The control experiment with f ixative gum pellets sug-
gests that C. cursor does not mark—that is, does not deposit
a chemical substance on—the stimulus and does not, there-
fore, recognize it on subsequent encounters. Even though
the tested ants decreased their agonistic behavior over suc-
cessive encounters with the gum pellet (and thus habitu-
ated to this odor), they did not respond differently between
the previously encountered pellet and another, novel pellet
in the discrimination test. This absence of marking is not
surprising: Marking could occur only through the deposi-
tion of alarm pheromones—which are very volatile—or
through the deposition of cuticular hydro carbons that are
produced during allogrooming, which was absent here.
Ants readily discriminate between novel objects, partic-
ularly those possessing a novel color and odor, and show
some reactions to them. In this experiment, for example,
ants behaved aggressively toward the gum pellets, which
were yellow and had a special odor. Indeed, the color
and odor of the gum pellets were particularly effective
in releasing aggressive behavior, even if the level of ag-
gression was lower than that toward the anesthetized ants
and decreased more rapidly. Moreover, the interpretation
perfectly between the two similar odors. However, Ichikawa
and Sasaki studied social privation in young adults. In our
study, we used mature individuals (older than 15 days).
The fact that C. cursor ants reintroduced into their so-
cial environment do not discriminate between two C. aethi
ops does not mean that they cannot distinguish between
the two individuals. Our statistical analysis shows that re-
turning to the social environment does not decrease ants’
aggressiveness, but causes a lapse of memory. Cheng and
Wignall’s (2006) experiments on honeybees showed how
the learning of a second task interfered with what had
been previously learned. Their results implicated response
competition as a major contributor to the retroactive in-
terference effect. The honeybees, like our C. cursor ants,
seemed to hold on to memories of the learned task. In
C. cursor, we suggest that returning to nestmates did not
fully eliminate the ants’ memory of learned odors.
CONTROL EXPERIMENT
Controlling for Olfactory Marking of
C. aethiops Stimulus Ants
Method
The control experiment was conducted to determine whether
C. cursor deposited olfactory marks on the C. aethiops stimulus. To
distinguish between two stimuli—a familiar individual and an unfa-
miliar individual—individuals may learn idiosyncratic particularities
of the familiar one, or simply mark it, actively or not, with a recog-
nition label. To control for this possibility, we used a procedure in
which C. aethiops stimuli were substituted with a neutral stimulus.
We chose pellets of a fixative gum (UHU Patafix) as a neutral
stimulus, not only because it has no alimentary or social valence
(since it is a nonliving stimulus), but also because it causes aggres-
siveness in C. cursor ants. The only way for the ants to discriminate
between two identical gum pellets would be to mark the familiar one
with an olfactory label.
We proceeded as in Experiment 1, with a rest period of 10 min.
In each habituation trial, we presented a pellet of fixative gum to
the C. cursor subject. In the discrimination test, we presented the
17
15
13
11
9
7
5
3
1
–1
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation
Familiar Gum Pellet Unfamiliar Gum Pellet
Discrimination
6
5
4
3
2
1
0
–1
*NS
Figure 4. Number of agonistic behaviors expressed by a C. cursor ant toward a fixative gum pellet in 3 min during the habituation/
discrimination procedure with a rest period of 10 min, during which the C. cursor ants were isolated. Horizontal lines represent the
10th, 25th, 50th (median), 75th, and 90th percentiles. Scores above the 90th and below the 10th percentiles are plotted as individual
points.
*
p # .05.
Me M o r y F o r in d i v i d u a l s ’ od o r s in a n t s 325
learning a global colonial odor, or gestalt odor learning,
rather than individual discrimination ability. For example,
Errard (1994) showed that when Formica selysi (Formici-
nae) and Manica rubida (Myrmicinae) ants were placed
5 h after emergence in a mixed heterospecific group, and
then, after 3 months, separated and placed in homospecific
groups, they recognized familiar heterospecific ants after
up to 1 year of separation. Because cuticular hydrocarbon
profiles have only traces of heterospecific hydrocarbons,
self-reference is not a reliable recognition process (Errard,
1994). Learning that occurs shortly after emergence and
is related to the colony—even an artificial colony—and
to the nest is very stable. Our study shows that in mature
ants, learning that occurs in the context of competitive
interactions is stored for a shorter time in memory and is,
therefore, more sensitive to external stimulation. Main-
taining that information is possible only if the ant is likely
to be confronted again with the same stimulus. In our
study, we simulated an encounter in a foraging area with
the forager ants. The probability of encountering the same
heterospecific individual multiple times over a long time
interval is low, even if we imagine that both individuals
have overlapping foraging roads. Thus, it is not surprising
to see the disappearance of individual discrimination of a
familiar individual, especially after returning to the nest.
In Errard’s experiments, heterospecific individual recog-
nition is linked to the mixed nature of the nest. Heterospe-
cific individual odors are then closely associated with the
nest and the colony as a whole.
The memory of individual identities is advantageous
when contacts are repeated among a small number of indi-
viduals. This is obvious in hierarchical conflicts (D’Ettorre
& Heinze, 2005; Dreier et al., 2007; Tibbetts, 2002). This
advantage is not yet known in heterospecific encounters,
but our study reveals substantive cognitive and mnemonic
abilities in a biological model, the ant, until then largely
ignored in such research. We show that adult workers are
able to learn and maintain in memory complex chemi-
cal information for heterospecific individual odors for at
least 30 min, without reinforcement, in a neutral context,
in which the ant experiences no hierarchical conflict over
food or colony defense. Moreover, this information is
available for a discrimination task between two very close
odors after a relatively long duration of at least 30 min,
but less than 60 min.
Neurological processes linked to our observations are
still unknown. Understanding them may allow us to con-
duct a comparative study with models such as honeybees
and fruit flies, which are relatively well known neuro-
anatomically, molecularly, and genetically (see Davis,
2005, on Drosophila).
AUTHOR NOTE
We are grateful to A. Lenoir, P. Gouat, and R. Fénéron for helpful dis-
cussion and suggestions; J.-L. Durand for helping in statistics analysis;
K. Hollis and three anonymous referees for comments; M. C. Malherbe
for rearing the ants; and L. Baltenneck for revising the first version of this
article in English. E.F. is now affiliated with UMR CNRS 5558–LBBE,
Université Claude Bernard–Lyon 1. Correspondence concerning this ar-
ticle should be addressed to E. Nowbahari, Laboratoire d’Ethologie Ex-
that ants do not recognize individuals by marking them is
supported by two additional arguments. First, because we
employed a crossed design (see Figure 1), the unfamiliar
C. aethiops ant used in the discrimination test would have
been the same individual used in the habituation trials of a
different C. cursor subject. Thus, if our C. cursor subjects
had marked individuals with an odor—which would nec-
essarily have been very similar, because the subjects were
nestmates—then this mark should have interfered with
the ants’ ability to discriminate the familiar self-marked
C. aethiops from the unfamiliar nestmate-marked stimu-
lus ant. Second, unpublished data from our lab show that
when anesthetized stimulus ants are returned to their own
C. aethiops nestmates, those nestmates do not respond
aggressively to them. If, in those experiments, a C. cur-
sor subject ant had deposited any chemical marks on a
C. aethiops stimulus ant, the stimulus ant would have been
attacked immediately by her nestmates on her return to
the nest.
Another way to discriminate the stimulus subjects with-
out using mnemonic abilities would be by obtaining the
stimuli’s odorant cues, which they carry away with them
and then use as a template. However, we excluded this
possibility, because this does not require learning pro-
cesses highlighted by the habituation phenomena.
GENERAL DISCUSSION
These results confirm and extend previous studies in
Cataglyphis ants (Nowbahari, 2007) and show that C. cur-
sor adult ants are able to learn a heterospecific individual’s
odor and discriminate it spontaneously, without reinforce-
ment, from the odor of another close individual. We show
here for the first time that the retention interval of the
learned odor is at least 30 min. After a 60-min interval,
however, C. cursor ants are not able to discriminate be-
tween the familiar and unfamiliar stimuli.
Dupuy, Sandoz, Giurfa, and Josens (2006) showed that
two Camponotus species, C. mus and C. fellah, were able
to learn simple odors (limonene and octanal, heptanal and
2-heptanone) in both positive and negative reinforcement
tasks, using sucrose and quinine, respectively. Their tests
demonstrated a retention time of at least 5 min. Matsumoto
and Mizunami (2000) showed that G. bimaculatus crickets
have long-lasting olfactory learning abilities: They are able
to remember a simple odor up to 7 days after three operant
conditioning sessions. Others studies have demonstrated
long-term memory abilities in other adult insects, such as
honeybees, but those studies employed operant condition-
ing tasks using simple nutritive valence odorants (Hammer
& Menzel, 1995), whereas we used complex social odor-
ants in a nonoperant conditioning task.
Our results complement the work of Dreier et al. (2007)
by demonstrating analogous findings in a worker recogni-
tion abilities paradigm. In all other studies of heterospe-
cific recognition (which has been explored extensively),
the emphasis was placed on the role of cuticular hydrocar-
bons, especially in the early period of adult life. However,
those studies focused on the imprint-like phenomenon of
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... Individuals that are not familiar (not encountered before) will not be accepted, irrespective of whether they are related or not. In ants, there are very few examples of individual recognition, which could be based on this mechanism (d'Ettorre and Heinze, 2005; Foubert and Nowbahari, 2008). Ant queens of Pachycondyla villosa are able to recognize each others individually (d'Ettorre and Heinze, 2005). ...
... Long-term memory would not necessarily be adaptive, as an ant generally leaves the nest only for relatively short foraging trips. Cataglyphis niger ants, repeatedly encountering a non-nestmate are less aggressive against this specific individual in subsequent encounters than against non-familiar non-nestmates (Nowbahari, 2007; Foubert and Nowbahari, 2008 ). The authors rule out deposition of hydrocarbons as an explanation, and suggest that learning plays a role in this process (Foubert and Nowbahari, 2008 ). ...
... Cataglyphis niger ants, repeatedly encountering a non-nestmate are less aggressive against this specific individual in subsequent encounters than against non-familiar non-nestmates (Nowbahari, 2007; Foubert and Nowbahari, 2008 ). The authors rule out deposition of hydrocarbons as an explanation, and suggest that learning plays a role in this process (Foubert and Nowbahari, 2008 ). Nevertheless , the reduction in aggression is less pronounced when, between encounters, the discriminating ant is placed back into its own colony instead of being isolated. ...
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