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

  • 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,
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.
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.
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
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.
The Effect of Social Environment on Lifetime
Retention of Individual Learned Odors
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.
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.
Memory Span for
Heterospecific Individuals’ Odors
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.
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).
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
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 10-min Isolated
Familiar Unfamiliar
Discrimination 10-min Isolated
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 30-min Isolated
Familiar Unfamiliar
Discrimination 30-min Isolated
*** *
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 60-min Isolated
Familiar Unfamiliar
Discrimination 60-min Isolated
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).
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
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 10-min Social
Familiar Unfamiliar
Discrimination 10-min Social
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Habituation 30-min Social
Familiar Unfamiliar
Discrimination 30-min Social
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.
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).
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.
Controlling for Olfactory Marking of
C. aethiops Stimulus Ants
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
Number of Agonistic
Behaviors/3 min
H1 H2 H3 H4
Familiar Gum Pellet Unfamiliar Gum Pellet
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
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).
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.
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
326 Fo u b e r t a n d no w b a h a r i
Lenoir, A., Fresneau, D., Errard, C., & Hefetz, A. (1999). Individu-
ality and colonial identity in ants: The emergence of the social repre-
sentation concept. In C. Detrain, J. L. Deneubourg, & J. M. Pasteels
(Eds.), Information processing in social insects (pp. 219-223). Basel:
Macquart, D., & Beugnon, G. (2004). L’apprentissage de routes
familières chez la fourmi néotropicale Gigantiops destructor. Actes
des Colloques Insectes Sociaux, 16, 70-74.
Matsumoto, Y., & Mizunami, M. (2000). Olfactory lear ning in the
cricket Gryllus bimaculatus. Journal of Experimental Biology, 203,
Matsumoto, Y., & Mizunami, M. (2005). Formation of long-term ol-
factory memory in the cricket Gryllus bimaculatus. Chemical Senses,
30, 1299-1300.
Nielsen, J., Boomsma, J. J., Oldham, N. J., Petersen, H. C., & Mor-
gan, E. D. (1999). Colony-level and season-specific variation in cu-
ticular hydrocarbon profiles of individual workers in the ant Formica
truncorum. Insectes Sociaux, 46, 58-65.
Nowbahari, E. (2007). Learning of colonial odor in the ant Cataglyphis
niger (Hymenoptera; Formicidae). Learning & Behavior, 35, 87-94.
Provost, E., Bonavita-Cougourdan, A., & Rivière, G. (1994). Plas-
ticité du profil cuticulaire spécifique des hydrocarbures chez les four-
mis: Facteurs physiologiques et environnementaux. Actes des Col-
loques Insectes Sociaux, 9, 1-10.
Sakura, M., & Mizunami, M. (2001). Olfactory learning and memory in
the cockroach Periplaneta americana. Zoological Science, 18, 21-28.
Sakura, M., Okada, R., & Mizunami, M. (2002). Olfactory discrim-
ination of structurally similar alcohols by cockroaches. Journal of
Comparative Physiology, 188, 787-797.
Tibbetts, E. A. (2002). Visual signals of individual identity in the wasp
Polistes fuscatus. Proceedings of the Royal Society of London B, 269,
Todrank, J., & Heth, G. (2003). Odor–genes covariance and genetic
relatedness assessments: Rethinking odor-based “recognition” mech-
anisms in rodents. In P. J. B. Slater, J. S. Rosenblatt, C. T. Snowdon,
& T. J. Roper (Eds.), Advances in the study of behavior (Vol. 32,
pp. 77-130). San Diego: Academic Press.
Vander Meer, R. K., & Morel, L. (1998). Nestmate recognition in
ants. In R. K. Vander Meer, M. D. Breed, M. Winston, & C. Espelie
(Eds.), Pheromone communication in social insects: Ants, wasps, bees
and termites (pp. 79-103). Boulder, CO: Westview.
Vander Meer, R. K., Saliwanchik, D., & Lavine, B. (1989). Tem-
poral changes in colony cuticular hydrocarbon patterns of Solenopsis
invicta: Implications for nestmate recognition. Journal of Chemical
Ecology, 15, 2115-2125.
Watanabe, H., Kobayashi, Y., Sakura, M., Matsumoto, Y., & Mizu-
nami, M. (2003). Classical olfactory conditioning in the cockroach
Periplaneta americana. Zoological Science, 20, 1447-1454.
Wilson, E. O., Durlach, N. I., & Roth, L. M. (1958). Chemical releas-
ers of necrophoric behavior in ants. Psyche, 65, 108-114.
Zhang, S., Mizutani, A., & Srinivasan, M. V. (2000). Maze naviga-
tion by honeybees: Learning path regularity. Learning & Memory,
7, 363-374.
(Manuscript received April 8, 2008;
revision accepted for publication April 24, 2008.)
périmentale et Comparée UMR CNRS 7153, Université Paris 13, 99 Ave-
nue J.-B. Clément, 93430 Villetaneuse, France (e-mail: elise.nowbahari@
Ataya, H., & Lenoir, A. (1984). Le comportement nécrophorique chez
la fourmi Lasius niger L. [Necrophoric behavior of Lasius niger L.].
Insectes Sociaux, 31, 20-33.
Breed, M. D., & Bennett, B. (1987). Kin recognition in highly euso-
cial insects. In D. J. C. Fletcher & C. D. Michener (Eds.), Kin recogni-
tion in animals (pp. 243-286). New York: Wiley.
Chameron, S., Schatz, B., Pastergue-Ruiz, I., Beugnon, G., &
Collett, T. S. (1998). The learning of a sequence of visual patterns
by the ant Cataglyphis cursor. Proceedings of the Royal Society of
London B, 265, 2309-2313.
Cheng, K., & Wignall, A. E. (2006). Honeybees (Apis mellifera) hold-
ing on to memories: Response competition causes retroactive interfer-
ence effects. Animal Cognition, 9, 141-150.
Crozier, R. H. (1987). Genetic aspects of kin recognition: Concepts,
models, and synthesis. In D. J. C. Fletcher & C. D. Michener (Eds.),
Kin recognition in animals (pp. 55-73). New York: Wiley.
Crozier, R. H., & Pamilo, P. (1996). Evolution of social insect colonies:
Sex allocation and kin selection. Oxford: Oxford University Press.
Davis, R. L. (2005). Olfactory memory formation in Drosophila: From
molecular to systems neuroscience. Annual Review of Neuroscience,
28, 275-302.
Delattre, O., & Nowbahari, E. (2007). [Individual discrimination
among sisters in the ant Cataglyphis cursor]. Unpublished raw data.
D’Ettorre, P., & Heinze, J. (2005). Individual recognition in ant
queens. Current Biology, 15, 2170-2174.
Dreier, S., van Zweden, J. S., & D’Ettorre, P. (2007). Long-term mem-
ory of individual identity in ant queens. Biology Letters, 3, 459-462.
Dupuy, F., Sandoz, J.-C., Giurfa, M., & Josens, R. (2006). Individ-
ual olfactory learning in Camponotus ants. Animal Behaviour, 72,
Errard, C. (1994). Long-term memory involved in nestmate recogni-
tion in ants. Animal Behaviour, 48, 263-271.
Errard, C., Hefetz, A., & Jaisson, P. (2006). Social discrimination
tuning in ants: Template formation and chemical similarity. Behav-
ioral Ecology & Sociobiology, 59, 353-363.
Hammer, M., & Menzel, R. (1995). Learning and memory in the hon-
eybee. Journal of Neuroscience, 15, 1617-1630.
Horridge, A. (2006). Visual discriminations of spokes, sectors, and
circles by the honeybee (Apis mellifera). Journal of Insect Physiol-
ogy, 52, 984-1003.
Ichikawa, N., & Sasaki, M. (2003). Importance of social stimuli for the
development of learning capability in honeybees. Applied Entomol-
ogy & Zoology, 38, 203-209.
Isingrini, M., Lenoir, A., & Jaisson, P. (1985). Preimaginal learning
as a basis of colony-brood recognition in the ant Cataglyphis cursor.
Proceedings of the National Academy of Sciences, 82, 8545-8547.
Jaisson, P. (1974). L’imprégnation dans l’ontogenèse des comportements
de soins aux cocons chez la jeune fourmi rousse (Formica polyctena
Först). Behaviour, 52, 1-37.
Lahav, S., Soroker, V., Hefetz, A., & Vander Meer, R. K. (1999).
Direct behavioral evidence for hydrocarbons as ant recognition dis-
criminators. Naturwissenschaften, 86, 246-249.
... 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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Recognizing the identity of others, from the individual to the group level, is a hallmark of society. Ants, and other social insects, have evolved advanced societies characterized by efficient social recognition systems. Colony identity is mediated by colony specific signature mixtures, a blend of hydrocarbons present on the cuticle of every individual (the "label"). Recognition occurs when an ant encounters another individual, and compares the label it perceives to an internal representation of its own colony odor (the "template"). A mismatch between label and template leads to rejection of the encountered individual. Although advances have been made in our understanding of how the label is produced and acquired, contradictory evidence exists about information processing of recognition cues. Here, we review the literature on template acquisition in ants and address how and when the template is formed, where in the nervous system it is localized, and the possible role of learning. We combine seemingly contradictory evidence in to a novel, parsimonious theory for the information processing of nestmate recognition cues.
... The day following the phase of social status determination, we tested the ability of low-ranking workers to discriminate other lowranking nestmates individually and/or their nestmates on the basis of their status within the group. To do this, we used and video recorded a procedure of habituation/discrimination commonly used for vertebrates (see for example : Johnston 1993) and adapted for ants (Nowbahari 2007;Foubert & Nowbahari 2008). During the habituation phase, the tested ant (taken randomly from the group of low-ranking workers) was exposed to a nestmate previously anaesthetized with CO 2 . ...
... Habituation/discrimination procedures thus offer an easy method to assess the ability of animals to discriminate signals. This method has usually been used in vertebrates (see for example Johnston 1993) but recent studies have demonstrated the validity of its use in ants (Nowbahari 2007;Foubert & Nowbahari 2008). In our study, the reinstatement of investigation towards the novel ant in the discrimination test shows that some information allowing workers to differentiate the two ants had been learned during the habituation tests and then remembered. ...
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In group-living animals where dominance hierarchies occur, aggression can be reduced if individuals are able to recognize each other. To do this, and to adapt their behaviour suitably when faced with a rival, individuals may rely on two nonmutually exclusive recognition means: they could recognize group members individually and/or their social status. Within insect societies, although conflicts over reproduction resulting in hierarchy establishment are widespread, relatively little is known about the cognitive abilities involved in the regulation of agonistic interactions. We tested whether low-ranking workers of Pachycondyla apicalis ants are able to discriminate each other individually and/or if they can discriminate the status of their nestmates. We found no evidence of individual discrimination among subordinates whereas they were able to discriminate their nestmates on the basis of their social and reproductive status. Such a skill may allow them to regulate worker reproduction in queenright colonies efficiently. By considering the structure of the hierarchy and the nature of the dominance relationships in P. apicalis societies, we discuss the existence of a more accurate recognition system among the high-ranking workers.
... Learning abilities and their impact on behavior in ants may be much more developed than considered to date. Using the habituation/discrimination paradigm (decrease of response towards the same stimulus; individual/high response towards a new stimulus, if it is discriminated), it has been shown that C. niger workers are able to recognize previously encountered individuals, whether conspecific or heterospecific (Nowbahari, 2007; Foubert and Nowbahari, 2008). ...
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Cataglyphis ants comprise one of the most characteristic groups of insects in arid regions around the Mediterranean basin and have been intensively studied over the last 30 years. These ants are central-place foragers and scavengers, single-prey loaders that have become a model for insect navigation using sophisticated visual orientation, having lost pheromone orientation. They are highly heat-tolerant ants that forage close to their critical thermal limit during the hottest hours of the day, with their long-chain cuticular hydrocarbons protecting them from desiccation. This is exemplified in two Cataglyphis species, each of which developed different mechanisms for counteracting extreme heat when foraging: polymorphism of workers vs. physiological and behavioral adaptations. Several species in this genus have also become a model for studying nestmate recognition mechanisms. The role of cuticular hydrocarbons and the postpharyngeal gland as a reservoir of hydrocarbons in nestmate recognition was initially discovered mainly in Cataglyphis, including the first experimental demonstration of the Gestalt model of nestmate recognition. These ants possess very acute discrimination capacities, down to individual recognition. Such fine discrimination is seemingly used by ants that rescue from ant-lion traps only those individuals that are their nestmates. Two main reproductive strategies are exhibited by species of this genus: some reproduce classically, by independent colony foundation following nuptial flight, whereas others reproduce by colony fission. Limited dispersion increases competition for access to resources, and local resource competitionhas been demonstrated. Multiple mating, which had been considered to be rare in ants, has also been reported in all species studied. Finally, the most important discovery in recent years with regard to reproduction strategies in Cataglyphis is probably the occurrence of thelytokous parthenogenesis in both workers and queens. In Cataglyphis cursor, queens are able to produce new queens by thelytoky, a phenomenon that was later found in four other ant species. This ability does not exist in any other Cataglyphis species, attesting to the great variety of reproductive strategies in this genus.
Social insects have an efficient recognition system that guarantees social cohesion and protection against intruders in their colonies and territories. However, the energy costs in constant conflicts with neighboring colonies could promote a reduction in the fitness of colonies. Here, we evaluated the effect of previous exposure to allocolonial odor and the consumption of similar food resources on aggressive behavior and choice of allocolonial cues in Nasutitermes aff. coxipoensis (Termitidae: Nasutitermitinae). Our results showed that intercolonial aggressiveness was not affected by previous exposure to allocolonial odor and by the consumption of similar food resources. However, individuals previously exposed to allocolonial odor were more attracted to these odors than individuals who had no prior exposure to allocolonial odor. In addition, individuals from colonies of N. aff. coxipoensis that use similar food resources increased alertness via a greater number of vibration than individuals who consumed different food resources. In general, our results indicate that colonies of N. aff coxipoensis perceive allocolonial cues that have been previously exposed and that the consumption of similar resources triggers an alert signal between individuals. Additional studies are necessary to assess how widespread this capacity of perception is present among the different Isoptera groups and the consequences of colony recognition odor cues on termite space use.
Ants are among the most advanced social insects and are characterized by a very efficient recognition system allowing discrimination between group members and strangers, thus protecting colonies from competitors and parasites. Nestmate recognition cues are encoded in the complex hydrocarbon profile present on the cuticle of each ant. The neural mechanisms allowing ants to distinguish between friends and enemies are still not completely understood, and it is unclear whether learning plays a crucial role in this process. However, learning does play an important role when distinguishing individual identity is beneficial, as in the case of co-founding associations of ant queens that establish a dominance hierarchy. Recently, a set of experimental tools has been developed to study learning and memory in ants. This will allow exploring cognitive abilities and their underlying mechanisms in this very diverse taxon.
The ability to discriminate between friends and foes is a central feature of social life. In social insects, nestmate recognition is mediated by colony specific cuticular hydrocarbons (CHCs) (label) that are perceived by an individual and compared with its neural representation of the colony odour (template). Although numerous advances have been made in understanding the identity, origin and production of recognition cues in social hymenoptera, relatively little is known about the ontogeny of nestmate recognition, and the learning processes that might be involved. It appears that wasps and bees learn the recognition cues required for template formation from their nest/comb odour, while ants learn principally from their nestmates. In general, the referent template is learned during the early stages of adult life, although pre-imaginal learning might play a role. The CHC blend can change over time; cue-exchange among nestmates is therefore needed to reduce chemical variability among individuals and to integrate environmental compounds into the colony odour. As a result of this process, the referent template is updated during life. This relative plasticity of the recognition system can be exploited by insect social parasites to integrate themselves within the host colonies and to fool host workers about their real identity. By studying the chemical integration strategies of social parasites new insights on the ontogeny of nestmate recognition could be acquired. However, further studies are needed to reveal the neural substrates implicated in learning and memory at different stages of social insect life to better understand how and when template formation occurs.
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Nestmate recognition is the process by which individuals discriminate between nestmates and con- and hetero-specifics. Nestmate recognition is based on recognition cues, which include cuticular hydrocarbons (CHCs). Models of nestmate recognition predict that recognition decisions are based on the overlap of recognition cues. Colony recipients assess cue differences by comparing an individual's CHC profile to an internal template, which is based on the colony-specific cues. The behavioral response to this assessment depends on cue similarities or differences with the template. Ants show graded responses to cue differences. More recent models of nestmate recognition include adjustable thresholds that account for graded responses and intra-colony individual variation in behavioral responses towards non-nestmates. Ants display differing levels of aggression towards conspecifics under different contexts, which suggests that nestmate recognition is context-dependent. Here, we review models of decision rules and the role of CHCs in nestmate recognition. We discuss the role of ecological and social context in nestmate recognition, and explore future directions of research for the field.
Many herbivorous arthropods use defensive chemistry to discourage predators from attacking. This chemistry relies on the ability of predators to rapidly learn to recognize and avoid offensive stimuli. Western corn rootworm (WCR), Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae), employs multifaceted chemical defences in its haemolymph, which may contribute significantly to its success as a major economic pest. Here, we test the hypothesis that agrobiont predators can rapidly learn to recognize and avoid WCR larvae, and will thereby reduce their contribution to WCR suppression. In controlled feeding assays, the effectiveness of WCR haemolymph defences varied across three predator taxa (crickets, centipedes, and ants). Centipedes (Chilopoda: Lithobiidae) were minimally affected by WCR defences, but crickets [Gryllus pennsylvanicus Burmeister (Orthoptera: Gryllidae)] spent less time feeding on WCR than on an undefended control prey, house fly maggots. However, we uncovered no evidence indicating that experienced crickets rapidly learn to avoid WCR larvae, indicating that haemolymph defences offer few, if any, survival benefits for WCR. Colonies of ants [Lasius neoniger Emery (Hymenoptera: Formicidae)] switched from low worker participation in initial attacks on WCR to higher worker participation in subsequent attacks, indicating an attempt to overcome, rather than avoid, WCR haemolymph defences. These results suggest that a diverse assemblage of natural enemies will show a diverse array of behavioural responses to toxic pest prey, and highlight the importance of behavioural diversity in driving the function of natural enemy assemblages.
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Individual Camponotus fellah ants perceive and learn odours in a Y-maze in which one odour is paired with sugar (CS+) while a different odour (CS-) is paired with quinine (differential conditioning). We studied olfactory retention in C. fellah to determine whether olfactory learning leads to long-term memory retrievable 24 h and 72 h after training. One and 3 days after training, ants exhibited robust olfactory memory through a series of five successive retention tests in which they preferred the CS+ and stayed longer in the arm presenting it. In order to determine the nature of the associations memorized, we asked whether choices within the Y-maze were driven by excitatory memory based on choosing the CS+ and/or inhibitory memory based on avoiding the CS-. By confronting ants with a novel odour vs either the CS+ or the CS- we found that learning led to the formation of excitatory memory driving the choice of the CS+ but no inhibitory memory based on the CS- was apparent. Ants even preferred the CS- to the novel odour, thus suggesting that they used the CS- as a contextual cue in which the CS+ was embedded, or as a second-order cue predicting the CS+ and thus the sugar reward. Our results constitute the first controlled account of olfactory long-term memory in individual ants for which the nature of associations could be precisely characterized.
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We investigated the ability of honeybees to learn mazes of four types: constant-turn mazes, in which the appropriate turn is always in the same direction in each decision chamber; zig-zag mazes, in which the appropriate turn is alternately left and right in successive decision chambers; irregular mazes, in which there is no readily apparent pattern to the turns; and variable irregular mazes, in which the bees were trained to learn several irregular mazes simultaneously. The bees were able to learn to navigate all four types of maze. Performance was best in the constant-turn mazes, somewhat poorer in the zig-zag mazes, poorer still in the irregular mazes, and poorest in the variable irregular mazes. These results demonstrate that bees do not navigate such mazes simply by memorizing the entire sequence of appropriate turns. Rather, performance in the various configurations depends on the existence of regularity in the structure of the maze and on the ease with which this regularity is recognized and learned.
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Heritable cuticular hydrocarbon patterns ofSolenopsis invicta workers are consistent within colonies for a given sampling time but vary sufficiently from colony to colony to distinguish the colonies from each other. In addition, cuticular hydrocarbon patterns change within colonies over time. Nestmate recognition cues found on the individual's cuticle, can be from heritable or environmental sources, and are a subset of colony odor. The cuticular hydrocarbons can be used as a model for heritable nestmate recognition cues. We propose that because potential nestmate recognition cues, both environmental and genetic, are dynamic in nature rather than static, during its lifetime a worker must continually update its perception (template) of colony odor and nestmate recognition cues.
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The understanding of the physiology of learning is dominated by two basically different hypotheses. The deterministic view, following Hebb’s (1949) concept of the memory engram, presupposes a memory groove which is built during memory formation by the adaptive change of a relatively small number of reacting sites or switch points. These so-called ’switchpoint theories’ or ‘place theories’ assume that memory involves a discrete set of cells reserved for the special function of information storage (Young 1964; Eccles 1964; Ungar 1970). The non-deterministic or statistical theory is based on Lashley’s (1950) findings which suggest that all, or nearly all, stored information is distributed throughout the whole association cortex rather than by distinct association paths or centres. The individual neuronal switch points may then be involved in the storage of many different memory traces (John 1967, 1972). The two views are similar in that they take the adaptivity of single synapses between neurones as the basic modifiable component of the nervous system (Eccles and McIntyre 1953; Eccles 1964; Ungar 1970; John 1972). They differ, however, in their conception of the gross structure of the memory system. The crucial problem, then, is to locate the stored information. The spatio-temporal pattern of activity during memory formation produces a localised change in the excitability of specific neurones. It should be possible to find such neurones using the same techniques as have been employed for the location of units in the sensory integration centres.
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The learning ability of the European honeybee, Apis mellifera, is well known. However, in a proboscis-extension reflex (PER) assay, newly emerged and very young worker bees could not associate a given odor (conditioned stimulus, CS) with a sucrose reward (unconditioned stimulus, US): This ability was acquired 5 to 9 days after emergence in workers, while it was accomplished 2 to 5 days after emergence in drones, probably reflecting the earlier onset of flight in drones. When workers are reared individually in a confined condition deprived of colony odor and other social stimuli, they do not develop the ability even after 9 days after emergence. In a series of experiments subjecting the bees to the confined condition for various lengths and timings, the important period for acquiring the learning ability was from day 2 to 6 after emergence. However, even bees that acquired the ability lost it when exposed to the confined (stimuli-deprived) condition for the next 15 days, meaning that the continuous input of appropriate sensory stimuli is essential for both acquiring and maintaining the learning capability.
Cuticular hydrocarbon profiles of individual workers of the ant Formica truncorum were measured and found to contain relatively few hydrocarbons. Pentacosane, heptacosane, nonacosane and hentriacontane dominated the mixture, but small amounts of the corresponding alkenes were also present. Principal component analysis and nested analysis of variance showed that workers from different colonies varied significantly in quantitative aspects of their cuticular hydrocarbon profiles. Furthermore, differences between habitat-patches within populations and (to some extent) between populations were also detected. Finally, workers from the same colony, sampled only a few months apart, were found to be different in the quantitative composition of their cuticular hydrocarbon profiles, emphasising the importance of collecting samples from a colony at a single point in time.
Theoretical distinctions among proposed kin recognition mechanisms in rodents are difficult to reconcile with some available data. Ambiguity remains because research on recognition mechanisms was originally driven by kin selection theory but never adequately grounded in behavioral data that could inspire principles to explain observed responses. There is a tendency to design experiments in terms of categorical distinctions, such as kin vs nonkin or conspecifics vs heterospecifics, which may be more useful for researchers than meaningful to the animals. Serendipitous findings helped clarify practical aspects of odor-based mechanisms underlying differential responses to individuals of varying degrees of genetic relatedness and their individual odors. In experiments using habituation-generalization techniques, subjects from multiple species of hamsters, mole rats, and mice consistently, across degrees of relatedness from siblings to different close species, treated the individual odors of two more closely related individuals as similar in quality in comparison with the odor of less closely related individuals. The process by which particular genes are manifest in particular proportions of compounds in individual odors remains unknown, but the genotype of each individual is clearly evident in the odor of that individual. This predictable relationship between genotypes and individual odors, namely, the greater the proportion of genes that two individuals share, the greater the similarity between their individual odors, is termed "odor-genes covariance." There were two important consequences of these studies for understanding recognition mechanisms. First, differential responses to odors of familiar and unfamiliar individuals indicated that rodents learn to associate particular individuals with their individual odors and can recognize the odors of familiar individuals irrespective of genetic relatedness. Thus "individual recognition" is a mechanism for responding both to kin and nonkin rather than a "kin recognition" process. Second, in conjunction with evidence for self-referencing in graded responses based on degrees of genetic relatedness to odors of kin, populations, and species, the odor-genes covariance findings raised the intriguing possibility that such self-referencing would be the most practical means of assessing degrees of genetic relatedness to any other individual. Differential responses could occur throughout the spectrum from siblings to across species by comparing the degree of similarity between the odor of the other individual and one's own odor, that is, "genetic relatedness assessments through individual odor similarities" or G-ratios. Individual odors are individually distinctive composites that also share common qualities with other genetically similar individuals from the same kin group, population, and species. These shared qualities in the odor gestalt enable relatedness assessments rather than specific odor markers of each group. Particular preferences for individuals with similar odors and genotypes that emerge with genetic divergence could serve as a premating ethological isolating mechanism during rodent speciation. Such a mechanism may help incipient rodent species remain genetically distinct without the necessity of species- specific odor signals. Future studies should determine the breadth of these mechanisms, the neurophysiological basis of differential responses, the extent to which they are innate or learned, and their robustness in the face of transient factors, such as diet and motivational state, that may alter the qualities of individual odors.
The role of long-term memory in nestmate recognition in ants was investigated. Workers of Formica selysi (Formicinae) and Manica rubida (Myrmicinae) were reared in single-species groups or in artificial mixed-species groups, created 5 h after their emergence. In mixed groups, hydrocarbon profiles of both species acquire at least some of the components characteristic of each other. After 3 months, the species reared in mixed groups were separated and each single-species group was divided into two groups for 8, 15, 30, 60 or 90 days, 6 months or 1 year. After the separation period, 'nestmate' recognition was evaluated for individuals of different species previously reared together ('familiar'), and for allospecific individuals from single-species and mixed groups ('unfamiliar'). Even after 1 year of separation, the workers reared in mixed groups recognized familiar allospecific ants, even though their cuticular profiles possessed only trace amounts of allospecific hydrocarbons. Moreover, they were not aggressive towards unfamiliar allospecifics reared in single-species groups. These results suggest that individuals recognized the allospecific cues borne on each individual's body surface, even when they were present in only trace amounts, and/or each individual learned and memorized allospecific recognition cues during its early life. They suggest also that each individual possesses a template encoding the allospecific and the conspecific cues to characterize nestmates.