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Significance of chemical recognition cues is context dependent in ants



Recognition of group members is of fundamental importance in social animals, allowing individuals to protect resources against intruders and parasites, as well as ensuring social cohesion within the group. In ants and other social insects, social recognition relies on multicomponent chemical signatures, composed primarily of long-chain cuticular hydrocarbons. These signatures are colony specific and allow discrimination between nestmates and non-nestmates. Nevertheless, the mechanisms underlying detection, perception and information processing of chemical signatures are poorly understood. It has been suggested that associative learning might play a role in nestmate recognition. We investigated whether Camponotus aethiops ants can associate a complete cuticular hydrocarbon profile, consisting of about 40 compounds, with a food reward and whether the new association, developed in an appetitive context, affects aggression against non-nestmates carrying the hydrocarbon profile associated with food. Individual ant workers were able to associate the non-nestmate chemical profile with food. However, conditioned ants were still aggressive when encountering a non-nestmate carrying the odour profile used as training odour in our experiments. This suggests that ants, like some, but not all other insects, show interactions between different modalities (i.e. olfactory and visual), and can treat complex chemical cues differently, according to the context in which they are perceived. This plasticity ensures that learning in an appetitive context does not interfere with the crucial task of colony defence.
Signicance of chemical recognition cues is context dependent in ants
Nick Bos
, Fernando J. Guerrieri
, Patrizia dEttorre
Centre for Social Evolution, Department of Biology, University of Copenhagen
Max Planck Institute for Chemical Ecology, Department of Evolutionary Neuroethology, Germany
Laboratoire dEthologie Expérimentale et Comparée (LEEC), Université Paris 13, France
article info
Article history:
Received 10 March 2010
Initial acceptance 7 May 2010
Final acceptance 2 August 2010
Available online 9 September 2010
associative learning
Camponotus aethiops
cuticular hydrocarbon
Recognition of group members is of fundamental importance in social animals, allowing individuals to
protect resources against intruders and parasites, as well as ensuring social cohesion within the group. In
ants and other social insects, social recognition relies on multicomponent chemical signatures, composed
primarily of long-chain cuticular hydrocarbons. These signatures are colony specic and allow discrimi-
nation between nestmates and non-nestmates. Nevertheless, the mechanisms underlying detection,
perception and information processing of chemical signatures are poorly understood. It has been suggested
that associative learning might play a role in nestmate recognition. We investigated whether Camponotus
aethiops ants can associate a complete cuticular hydrocarbon prole, consisting of about 40 compounds,
with a food reward and whether the new association, developed in anappetitive context, affects aggression
against non-nestmates carrying the hydrocarbon prole associated with food. Individual ant workers were
able to associate the non-nestmate chemical prole with food. However, conditioned ants were still
aggressive when encountering a non-nestmate carrying the odour prole used as training odour in our
experiments. This suggests that ants, like some, but not all other insects, show interactions between
different modalities (i.e. olfactoryand visual), and can treat complex chemical cues differently, according to
the context in which they are perceived. This plasticity ensures that learning in an appetitive context does
not interfere with the crucial task of colony defence.
Ó2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Associative learning is a widespread phenomenon in the animal
kingdom (Giurfa 2007), allowing individuals to extract important
information from their environment by establishing predictive
relationships between different stimuli (i.e. honeybees, Apis melli-
fera:Bitterman et al. 1983;cuttlesh, Sepia ofcinalis:Cole & Adamo
2005;housemice,Mus domesticus:Watkins et al. 19 98). Although
insects have been generally neglected in studies addressing higher-
order cognitive processes, during the last three decades the
honeybee has become a model organism for the study of learning
and memory (Giurfa 2007; de Brito-Sánchez et al. 2008), since they
live in organized complex societies and show an amazing capacity
for learning.
All ants are eusocial, having cooperative brood care, reproductive
division of labour and overlapping generations. Ants often live in
very complex societies, and can learn to solve a variety of problems,
such as navigating in complex environments (Cataglyphis:Wehner
2009), visiting feeding places at specic times during the day
(Paraponera:Harrison & Breed 1987) or learning to avoid plants that
are detrimental for their fungus garden (Atta:Saverschek et al. 2010).
Some ants can learn and remember individual recognition cues
(dEttorre & Heinze 2005; Dreier et al. 2007) and selectively police or
punish colony members (e.g. Monnin et al. 2002; Van Zweden et al.
2007). However, ants have been largely ignored in studies on
learning, memory and cognition other than studies on spatial
memories (reviewed in Collett et al. 2006). A pioneering work by
Dupuy et al. (2006) showed that individual Camponotus ants can
learn to associate volatile substances with either a positive stimulus
(sucrose solution) or an aversive stimulus (quinine). In their study,
foraging ants had to make a choice between an odour associated
with sucrose solution (appetitive conditioned stimulus) and another
odour associated with quinine (aversive conditioned stimulus) in
a Y-maze. Individual Camponotus aethiops ants can be trained to
associate single synthetic long-chain hydrocarbons with a sucrose
reward (S. Dreier et al., unpublished data). These hydrocarbons have
a low volatility, are present on the ant cuticle and thus not usually
found in a foraging context. Instead, cuticular hydrocarbons (CHCs),
especially some classes of hydrocarbons, such as methyl-branched
alkanes, are important for nestmate recognition (e.g. Guerrieri et al.
2009; reviewed in dEttorre & Lenoir 2010). Ant colonies are good
targets for predators and parasites, since they contain many worker
*Correspondence: N. Bos, Centre for Social Evolution, Department of Biology,
University of Copenhagen, Universitetsparken 15, bygning 12, DK-2100 Copenha-
gen, Denmark.
E-mail address: (N. Bos).
Contents lists available at ScienceDirect
Animal Behaviour
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0003-3472/$38.00 Ó2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Animal Behaviour 80 (2010) 839e844
ants, eggs, larvae, pupae and stored food. To maintain these valuable
resources, ants need to defend theircolonies from potential invaders.
Also, because ant workers usually do not reproduce, tness benets
are gained only if cooperative acts are directed towards nestmates,
which are usually related, and not towards alien individuals. This
requires an effective recognition system, allowing reliable discrimi-
nation of nestmates from non-nestmates.
Nestmate recognition is therefore essential for the stability and
success of insect societies. Because ant nests are usually dark,
a nonvisual recognition system is needed. Recognition cues are
chemical in nature and, as mentioned above, CHCs appear to be
important substances for chemical recognition in social insects
(i.e. bees: Breed 1998; wasps: Dani 2006; termites: Dronnet et al.
2006; ants: Hefetz 2007; dEttorre & Lenoir 2010). One of the rst
studies showing the role of CHCs in ant recognition was performed
by Bonavita-Cougourdan et al. (1987), who removed the chemical
prole of freshly killed workers of Camponotus vagus and replaced
it with a chemical cuticular extract of a different colony. Workers
were signicantly more aggressive against these treated nestmates
than against nontreated ones. In a subsequent study, a single
synthetic hydrocarbon was added to the cuticle of individual
C. vagus ants, which were then attacked by their nestmates
(Meskali et al. 1995); however, a recent study showed that this
might not be the case for all classes of hydrocarbons, although it is
the presence and not the absence of specic hydrocarbons on the
cuticle that promotes aggression (Guerrieri et al. 2009).
According to the currently accepted hypothesis, which has
recently been questioned (Ozaki et al. 2005; Guerrieri et al. 2009),
nestmate recognition occurs following a labeletemplate matching
model: each worker carries a set of recognition cues (the label) and
when an individual detects this label, it compares the label and its
inner template (a neural representation of the colony odour, stored
in the long-term memory). If the label is dissimilar to the template,
the worker will reject the encountered individual (Vander Meer &
Morel 1998; Lenoir et al. 1999). Previous studies specically
showed that ants behave aggressively against the CHC extracts
from non-nestmates (Lahav et al. 1999; Lucas et al. 2005; Ozaki
et al. 2005). Guerrieri & dEttorre (2008) recently introduced
a controlled protocol for recording a clear binary response, named
the mandible opening response (MOR): harnessed ants (genus
Camponotus and Formica) will immediately open their mandibles,
as a sign of aggression, when presented with a glass rod coated with
the cuticular extracts of non-nestmates. Conversely, ants keep their
mandibles closed when presented with the cuticular extract of
nestmates. These studies demonstrate that the chemical stimulus
itself, that is, the CHC extract of non-nestmates, is sufcient to elicit
aggression in several ant species.
Knowing that ants behave aggressively against CHC extracts of
non-nestmates, and also that ants can be conditioned to associate
asynthetic chemical compound, including long-chain hydrocarbons,
with food (Dupuy et al. 2006; S. Dreier et al., unpublished data), we
investigated whether individual focal ants were able to associate the
chemical extract of the CHC prole of a non-nestmate with food, thus
transforming this non-nestmate cuticular hydrocarbon prole from
an aversive stimulus (see Guerrieri & dEttorre 2008)intoanappe-
titive stimulus. The question then arises, how would an ant that
previously associated a non-nestmate CHC prole with food react to
a real non-nestmate individual bearing the same CHC prole? We
predicted two mutually exclusive scenarios: (1) the non-nestmate
CHC prole changes its meaning, now indicating the presence of
food and not of a potential enemy, and thus the focal ant will not
behave aggressively towards the non-nestmate individual; (2) even
if in a foraging context the CHC prole indicated the presence of
a food source, the focal ant will still behave aggressively against
a non-nestmate bearing the food-associated CHC prole. Our
experimental design allowed us to distinguish between these two
predictions, although it remains to be investigated whether the ants
learn the entire cuticular hydrocarbon mixture or a subset of it.
Study Organism
Twelve queenright colonies of C. aethiops (Latr.) were collected in
April 2008 in the Italian Apennines. Six colonies were collected in
Castel del Rio (44
N, 11
E) and six in Moraduccio
N, 11
E). Each colony was housed in a plastic
box (27 17 cm and 9.5 cm high) with a plaster oor, serving as
a nest. This was connected to another plastic box of the same size,
serving as a foraging arena. The ants were fed twice a week with
diluted honey and mealworms, Tenebrio molitor; water was provided
ad libitum. The nests were kept in a climate room, at 25 2
C, and
a 12:12 h light:dark regime. Ants were deprived of honey at least 1
week before the experiment to increase motivation for foraging on
sucrose food sources.
Preparation of CHC Extracts
To condition individual ants to the chemical prole of non-
nestmates, we used cuticular extracts in pentane as a solvent
(SigmaeAldrich); this was the training odour. For each colony
source of training odour, we prepared ve extracts in the
following way: 11 foragers (six major and ve media workers)
were frozen and after 30 min their abdomen was cut off to prevent
any possible extraction of pheromones produced by glands. The
remaining parts of the bodies were inserted into a glass vial and
covered with 1 ml of pentane. After 10 min, the extract was
transferred to a new vial and the solvent allowed to evaporate;
chemical extracts were then redissolved in 50 0
before use in the following experiments.
Conditioning Set-up and Procedure
The ant nests used in conditioning trials were provided with
a vertical wooden stick in their foraging arena for the ants to climb
on. For each ant to be tested, seven petri dishes (100 mm diame-
ter 15 mm high) were prepared bycoating their walls with Fluon
and covering their oor with clean lter paper. Two microscope
cover slips (18 18 mm) were placed on each lter paper. One
cover slip was treated with 20
l of non-nestmate extract
(the training odour, as described above) deposited on its borders
and the solvent was allowed to evaporate completely. In the centre
of the cover slip, a droplet of sucrose solution (1
l, 30% w/w) was
deposited. On the other cover slip, we put 1
l of water, so that the
two slips looked exactly alike. The slips were positioned on oppo-
site sides of the petri dish (see Fig. 1a).
At the start of the rst conditioning trial, a medium foraging
worker climbing on the verticalstick was gently allowed to walk onto
a small piece of paper, whichwasthen transferred into the petri dish
where theant was allowed toget off the paper at approximately equal
distance from both cover slips (see Fig. 1a). We then recorded the
time the ant required to nd the sucrose reward. After the ant
nished drinking the sugar reward, it was picked up withsoft forceps,
and marked with a dot of enamel paint on its abdomen. The ant was
then allowed to walk on the piece of paper again, and transferred
back to the vertical stick inits colony of origin. Once back in the nest,
the ants usually transferred the food to their nestmates by trophal-
laxis and returned to the stick. After a minimum of 1 min, the same
ant was picked up again from thestick and transferred to a new petri
dish for a subsequent conditioning trial. A total of six conditioning
N. Bos et al. / Animal Behaviour 80 (2010) 839e844840
trials were performed per ant. The location of the slide with the
sucrose reward was randomized in each trial, but the cover slip was
never in the same quadrant for more than two consecutive trials to
prevent the ant from associating a given spatial direction with the
Following conditioning, a choice test was conducted to see
whether the ant had developed a positive association between
non-nestmate CHC extract and the sucrose reward. This choice test
consisted of presenting the focal ant, in a new petri dish, with one
cover slip coated with the CHC extract used as training odour, and
another one treated with solvent only (pentane, P). In this test
neither sucrose nor water was provided. The cover slips represent
the contextual stimulus in these tests. The petri dish was divided
into four quadrants by drawing a light cross in the middle of the
lter paper with a pencil, and the two slips were placed randomly
in two opposite quadrants (see Fig. 1b). The ant was transferred
from the stick to the petri dish, analogously to the conditioning
procedure, and was allowed to search for the expected reward for
2 min (although only the chemical stimulus, and not the reward,
was present during this time). The time spent by the focal ant in
each quadrant was recorded using the software EthoLog (Ottoni
2000). Afterwards, 1
l of sucrose solution was provided on the
CHC-coated cover slip to avoid any possible extinction effect. The
ant was then transferred back to the vertical stick in the foraging
arena of the colony.
As a control, naïve ants were subjected directly to the choice
test, without conditioning. Ten naïve ants were tested from each
colony used for conditioning (40 control ants in total).
Aggression Tests
Once the choice test was completed, the conditioned ant was left
in its colony for 10 min and then underwent an aggression test. We
measured aggression by placing the focal ant from the stick into
a neutral arena (50 mm diameter 60 mm height), where she was
allowed to habituate to the new environment for 1 min. After this,
a dead ant (freshly killed by freezing), from its own colony (nestmate
control), the colony carrying the CHC prole used as the training
odour or a novel colony (non-nestmate control), was placed in the
centre of the arena. In these tests, the dead ant represents the
contextual stimulus. The small size of the arena allowed for rapid
contact between the focal ant and the freshly killed ant (average
delay for rst contact SE ¼7. 2 1.4 s). The behaviour of the focal
ant towards the dead ant was recorded continuously for 3 min using
the software EthoLog (Ottoni 2000). We evaluated any possible
aggression elicited by the target (dead ant) by recording six cate-
gorical behaviours: (1) no contact between the focal ant and the
target; (2) antennation; (3) grooming; (4) mandible opening;
(5) biting; and (6) gaster exing (attempting to spread formic acid).
We established a baseline of aggression before starting the
conditioning experiments. Ten unconditioned focal ants and 10
target ants were used for each set of dyadic encounters (with an ant
from the focal ants own colony, the colony carrying the CHC prole
used as the training odour or a novel colony), giving a total of 30
aggression tests. This was replicated four times, using three new
colonies for each replicate, for a total of 12 colonies and 120
aggression tests.
In summary, 15 ants were conditioned. The aggression tests
involving these conditioned focal ants were repeated ve times with
target nestmate ants, ve times with target ants originating from the
colony whose cuticular extracts were used as the training odour and
ve times with target ants from a novel non-nestmate colony. This
was replicated four times, involving a total of 12 colonies and 60
conditioned ants. As a control for the conditioning experiment, 40
additional naïve ants were used in choice tests, and to establish the
baseline of aggression,120 additional unconditioned ants were used.
Data Analysis
There were no signicant differences in searching time between
colonies (KruskaleWallis ANOVA:
<9.49, P>0.05), so the data
could be pooled. Searching time in the course of the six condi-
tioning trials (1e6) were analysed using a Friedman ANOVA
followed by multiple comparisons (Siegel & Castellan 1988).
For the choice tests, a preference index (PI) was calculated using
the following formula, where t
and t
is the time spent in quad-
rant TO (training odour) and P (pentane), respectively.
PI ¼t
PI data were normally distributed (KolmogoroveSmirnov test:
P>0.2 in all cases). There was no colony effect on PI (ANOVA:
conditioned ants: F
¼1.47, P¼0.23; naïve ants: F
P¼0.37); hence the data were pooled. If ants preferred one
quadrant over the other, the PI would differ signicantly from zero.
This was analysed using a ttest for single means. Preference for
quadrants was also compared between conditioned and uncondi-
tioned (naïve) ants using a ttest for independent samples.
The different behaviours observed during aggression tests were
scored so that the most aggressive behaviour was assigned the
highest score: 0 ¼antennation and grooming; 1 ¼mandible
opening; 2 ¼biting; 3 ¼gaster exing. The maximum level of
aggression was recorded, giving a value between 0 and 3 for every
ant tested.
Since there was no colony effect on overall aggression
(KruskaleWallis ANOVA: P>0.05), data could be pooled. The
difference in baseline aggression of unconditioned workers
towards nestmates, non-nestmate ants bearing the CHC prole
used for conditioning and novel non-nestmate ants was analysed
with a Wilcoxon signed-ranks tests.
The data were not normally distributed (KolmogoroveSmirnov
test: P<0.05) and thus a generalized linear model (GLM; Poisson
CHC profile
CHC profile
Focal ant
Focal ant
Figure 1. (a) Set-up for conditioning. (b) Set-up for choice test. For (a) the time the
focal ant spent nding the reward was recorded. For (b) the time the focal ant spent in
each of the four quadrants was recorded for 2 min.
N. Bos et al. / Animal Behaviour 80 (2010) 839e844 841
distribution, log link function) was used for analysing aggression
levels among naïve ants (the baseline of aggression) and condi-
tioned ants.
All analyses were performed using Statistica 7.1 (StatSoft, Tulsa,
OK, U.S.A.).
The searching time decreased signicantly in the course of the
six conditioning trials (Friedman ANOVA:
¼97.17, N¼60,
P<0.05; Fig. 2). In particular, searching time decreased markedly
from the second trial on, showing that ants directed their search
more promptly towards the training odour.
In the control group (naïve ants), the PI did not differ signi-
cantly from zero (one-sample ttest: t
¼0.27, P¼0.79), meaning
that ants had no spontaneous preference for a particular quadrant
during the choice test. However, for the conditioned ants, the PI
differed signicantly from zero (one-sample ttest: t
P<0.001). During the choice test, conditioned ants spent signi-
cantly more time in the quadrant containing the training odour
than control (naïve) ants (ttest: t
¼10.60, P<0.001; Fig. 3).
When the baseline of aggression was established, aggression of
unconditioned ant workers was signicantly higher towards non-
nestmate ants bearing the CHC prole used for conditioning (b) or
novel non-nestmate ants (c) than towards nestmates (a; Wilcoxon
signed-ranks test: aaeab: T¼0.00, P<0.01; aaeac: T¼8.00,
P<0.01; abeac: T¼7. 50 , P>0.05; Bonferroni correction, adjusted
signicance level
¼0.025). The results of the aggression tests are
shown in Fig. 4. Aggression levels of conditioned ants against either
ants from their own colony, non-nestmate ants bearing the CHC
prole used for conditioning or novel non-nestmate ants did not
differ signicantly from the baseline of aggression of unconditioned
ants (GLM: Wald
¼2.783, P¼0.249), showing that conditioning
did not interfere with recognition abilities and expression of
aggressive behaviour.
We investigated whether ants are able to associate a cuticular
hydrocarbon mixture with food, and whether this association,
developed in an appetitive context, might affect nestmate discrimi-
nation, which is usually expressed in an aggressive context. We
conditioned freely walkingindividual C. aethiops workers to asso ciate
a cuticularextract of a non-nestmate with a sucrose reward,showing
that stimuli that originally elicit aggression in ants can be associated
with food. This suggests plasticity in the signicance of cues/signals
that are typically important in the modulation of social interactions.
The fact that the conditioned ant kept coming back to the stick, and
that during the trials more ants were present on the stick, shows
clearlythat our set-up wasappropriate to simulate a foraging context.
Ants formed the association between the chemical blend and reward
very rapidly; right after the rst training trial, the searching time
needed by the ant to nd the reward decreased signicantly.
A subsequent choice test showed that the association between the
Searching time (s)
Figure 2. Average searching time for each conditioning trial (N¼60) showing median,
quartiles and range.
Preference index
Figure 3. Preference index of conditioned and unconditioned (naïve) ants (meanSE).
0Nestmate Familiar Novel
Aggression index
Figure 4. Aggression index of conditioned and unconditioned ants versus nestmates,
familiar non-nestmates and novel non-nestmates, respectively (mean SE). Note that
the familiar non-nestmatesare novel non-nestmates for the unconditioned ants, since
they have not been familiarized by conditioning.
N. Bos et al. / Animal Behaviour 80 (2010) 839e844842
food and the non-nestmate CHC prole was robustly established,
although we do not know whether the ants learned the entire CHC
prole or a subset of it (see below).
Individual olfactory learning in ants was shown for the rst time
only recently (Dupuy et al. 2006), by conditioning individual ants to
pure volatile substances using a Y-maze. Although the substances
tested were present in either owers or honeybee pheromones
(see Balderrama et al. 2002), they were not potential cues involved
in nestmate recognition. In addition, (S. Dreier et al., unpublished
data) showed that individual Camponotus ants can be conditioned
to associate single synthetic long-chain hydrocarbons with a sugar
reward. Unlike these two studies, in which only pure synthetic
chemical substances were used as conditioned stimuli, we used
a multicomponent blend, namely the cuticular extract of C. aethiops
workers, consisting of about 40 different hydrocarbons
(Van Zweden et al. 2009), as training odour. The extracted cuticular
hydrocarbons have the same properties as the natural mix on the
ants cuticle, as shown by Bonavita-Cougourdan et al. (1987), Morel
et al. (1988) and Nowbahari et al. (1990). These authors washed
ants in solvent to remove the cuticular hydrocarbons, and then
applied on these washed ants the cuticular extract of a nestmate or
non-nestmate. This restored the expected levelof aggression, while
washed ants did not elicit an aggressive response. In addition,
Ozaki et al. (2005) and Guerrieri & dEttorre (2008) showed that
a non-nestmate cuticular extract, when applied to a glass bead (or
rod), elicits aggression, proving that the CHC extract alone is
sufcient to promote aggression.
It remains to be determined whether the ants indeed learned the
entire CHC prole or only some specic compounds within the
prole. If the ants learned the entire CHC mixture of the prole, or
a large part of it, learning could have happened in various ways.
According to the elemental theory of learning (i.e. Rescorla & Wagner
1972), a mixture is processed as the sum of its components
(AB ¼AþB), while the congural theory (i.e. Pearce 1987) suggests
that the properties of a mixture are different from the properties of
the components (AB ¼XsAþB; Giurfa 2003). In honeybees,
a new model has been suggested: the key odorant hypothesis, which
encompasses features of both elemental and congural learning
(Reinhard et al. 2010). Even though honeybees were able to learn all
individual odorants used in the experiments; when conditioned to
a complex mixture, only certain key compounds were learned,
suggesting that some odorants are more representative of the
mixture than others.
In our experiment, we cannot distinguish between these
models. However, recent evidence indicates that methyl-branched
alkanes are more important in nestmate recognition than linear
alkanes (i.e. Guerrieri et al. 2009), suggesting that only key
compounds of the cuticular hydrocarbon blend present on the ant
might be used in recognition. Future studies should focus on which
classes of hydrocarbons are learned when a mixture is used as the
training odour.
In our experiments, the association of the CHC prole with food
did not affect the social meaning of the non-nestmate cuticular
prole. Indeed, after conditioning, the focal ants were as aggressive
towards an individual bearing the familiar odour (the cuticular
prole associated with food) as towards an individual bearing
a novel non-nestmate cuticular hydrocarbon prole.
Context-dependent learning in the visual modality has been
shown in a variety of organisms (e.g. ants: Chameron et al. 1998;
honeybees: Collett et al. 1993; humans: Smith & Vela 2001;for
a review on insects, see Collett et al. 2003). However, context-
dependent olfactory learning in insects has only been shown in the
cricket Gryllus bimaculatus (Matsumoto & Mizunami 2004) and the
cockroach Periplaneta americana (Sato et al. 2006). For instance,
individual crickets were conditioned to select one odour and to avoid
another odour in one context (darkness), and to do the opposite in
anothercontext (light). In thisexperiment, neitherthe light condition
nor the odour could predict a reward (water) or non-reward
(saline solution); only a combination of the two could. In contrast,
Drosophila melanogaster is not capable of solving a similar task (Yara li
et al. 2008). Groups of ies were conditioned in a biconditional
discriminationdesign. One odour was paired with an electric shock
in darkness, but not in light;another odour waspaired with a shock in
light, but not darkness. Flies failed to show any preference for the
right odour in the specic light conditions. Therefore, interactions
between different modalities (i.e. visual and olfactory), which are
necessary for context-dependent learning, are not a general feature
of all insects. Two explanations of context-dependent learning have
been proposed (Pearce & Bouton 2001). In the occasion-setting
theory, the contextual stimulus (in our case, the cover slip or the
target ant) sets the occasionfor responding to another conditioned
stimulus (in our case, the training odour: the non-nestmate CHC
prole), without forming an association with the unconditioned
stimulus (the food reward) itself. In the congural theory, an indi-
vidual perceives different CSecontext combinations as different
stimuli. Although learning in our experimental design was clearly
context dependent, further studies will be needed to distinguish
between these two theories.
Living in a complex and changing environment requires being
aware that the same cues/signals might have different signicance
according to context and the role of individual experience is
extremely important. This learning capability and exibility is an
adaptive trait for the ants, as it maximizes their tness and survival:
on the one hand, ants can eventually nd food by following the
smell of non-nestmates, but still avoid or attack enemies that they
encounter. Our study shows that ants have complex cognitive
abilities and are capable of distinguishing the meaning of identical
cues according to the context in which they are perceived.
This work was supported by the Marie Curie Excellence grant
CODICES (MEXT-CT-2004-014202) and a Freia grant from the
Faculty of Science, University of Copenhagen, both assigned to P.dE.
We are grateful to all members of the Copenhagen Centre for Social
Evolution for a stimulating work environment. We thank three
anonymous referees for useful comments and suggestions.
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... Past studies provide evidence for visual and olfactory learning by ants (Roces, 1994;Harris et al., 2005;Dupuy et al., 2006;Narendra et al., 2007;Bos et al., 2010) but, to our knowledge, no studies have tested whether associative learning of natural blends of plant chemicals by ants mediates their associations with plants in the field. Associative learning has only been studied in a few ant species (Acromyrmex lundi, Camponotus spp. ...
... and Cataglyphis fortis) (Roces, 1994;Helmy & Jander, 2003;Huber & Knaden, 2018), thus making it unclear whether learning is widespread across ants. Most of these studies have been conducted in the laboratory, in which ants have been shown to form positive and negative associations with pure chemical compounds (Dupuy et al., 2006;Josens et al., 2009), artificial odours (Roces, 1990(Roces, , 1994 and the cuticular hydrocarbon profiles of other ants (Bos et al., 2010). Such experiments provide opportunity for controlled tests of ant associative learning and its underlying mechanisms (e.g. ...
... Nonetheless, we found evidence for associative learning of natural blends of plant chemicals by both ant species (2018 only), as well as by all ant taxa present in the community combined (2017 and 2018). Thus, our results contribute to a growing number of studies of associative odour-learning in ants (Roces, 1990(Roces, , 1994Helmy & Jander, 2003;Dupuy et al., 2006;Bos et al., 2010;Huber & Knaden, 2018), which together show that associative learning of plant chemicals may be widespread across ant species. ...
1. Although associative learning is widespread across animals, its ecological importance is difficult to assess because learning is rarely studied in the field, where informative cues are juxtaposed against complex backgrounds of uninformative noise. 2. Ants rely heavily on chemical cues for foraging and engage in many ecologically important interactions with plants. Nevertheless, little is known about the role of associative learning of plant chemicals in ant foraging for carbohydrates. 3. In a field setting, the present study investigated whether the distantly related ant species Formica podzolica (Formicinae subfamily) and Tapinoma sessile (Dolichoderinae subfamily) exhibited associative learning of the chemical cues from two co-occurring plant species that are taxonomically and chemically distinct (Asteraceae: Helianthella quinquenervis and Apiaceae: Ligusticum porteri). 4. For two consecutive summers, ants were trained to forage from artificial sugar-rich baits associated with the leaf chemicals from either H. quinquenervis or L. porteri for 24 h, after which a two-choice test was deployed to assess whether ants would be more likely to select baits associated with the same (versus different) plant chemicals on which they had been trained. 5. The present study demonstrates associative learning of chemicals from both plant species, and these effects were consistent between ant species and years; training increased bait occupancy from 42% on the untrained scent to 66% on the trained scent. These results indicate that associative odour-learning may be widespread across ants and serve as an important mechanism mediating ant selection of resources.
... Just like honey bees, ants are social insects for whom learning is important in many contexts (Bos et al., 2010). Ants can learn odours of rewarding food sources and also have to learn the specific odour of their own colony (Neupert et al., 2018). ...
... Ants can learn odours of rewarding food sources and also have to learn the specific odour of their own colony (Neupert et al., 2018). Indeed, ants can perform similar learning tasks to bees and other insects (Bos et al., 2010;Guerrieri and d'Ettorre, 2010;Fernandes et al., 2018;Piqueret et al., 2019). In addition to floral odours that might signal food sources, ants were successfully conditioned to respond to hydrocarbons that play an important role in social interactions (Bos et al., 2012;Sharma et al., 2015). ...
... We directly compared whether the ants spent more time on one of the two odour mixtures using paired Wilcoxon tests (all statistical tests are two-tailed). In addition, we calculated and visualized (ggplot2; Wickham, 2016) a preference index (PI) as an intuitive measurement of preference and hence learning performance based on the time (t) spent on the different odours (Bos et al., 2010(Bos et al., , 2012: ...
Associative learning relies on the detection of coincidence between a stimulus and a reward or punishment. In the insect brain, this process is carried out in the mushroom bodies under control of octopaminergic and dopaminergic neurons. It was assumed that appetitive learning is governed by octopaminergic neurons, while dopamine is required for aversive learning. This view has been recently challenged: Both neurotransmitters are involved in both types of learning in bees and flies. Here, we test which neurotransmitters are required for appetitive learning in ants. We trained Lasius niger workers to discriminate two mixtures of linear hydrocarbons and to associate one of them with a sucrose reward. We analysed the walking paths of the ants using machine learning and found that the ants spent more time near the rewarded odour than the other, a preference that was stable for at least 24 hours. We then treated the ants before learning with either epinastine, an octopamine receptor blocker, or with flupentixol, a dopamine receptor blocker. Ants with blocked octopamine receptors did not prefer the rewarded odour. Octopamine signalling is thus necessary for appetitive learning of olfactory cues, likely because it signals information about odours or reward to the mushroom body. In contrast, ants with blocked dopamine receptors initially learned the rewarded odour but failed to retrieve this memory 24 hours later. Dopamine is thus likely required for long-term memory consolidation, independent of short-term memory formation. Our results show that appetitive olfactory learning depends on both octopamine and dopamine signalling in ants.
... basiconica form glomeruli in a cluster called T6, suggesting this region plays a role in nestmate recognition (Ozaki et al., 2005;Nakanishi et al., 2009;D'Ettorre et al., 2017) and may be subject to selection on social communication. On the other hand, while some ants have elaborate visual systems used in navigation, foraging, and learning and memory (Jaffé et al., 1990;Narendra et al., 2011;Yilmaz et al., 2017Yilmaz et al., , 2019Fernandes et al., 2018;Wehner, 2020), and may rely on multiple modalities for nestmate recognition (Bos et al., 2010), there are no documented examples of visually based nestmate recognition systems in ants (Hölldobler, 1999). ...
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In social insects colony fitness is determined in part by individual worker phenotypes. Across ant species, colony size varies greatly and is thought to affect worker trait variation in both proximate and ultimate ways. Little is known about the relationship between colony size and worker trait evolution, but hypotheses addressing the role of social structure in brain evolution suggest workers of small-colony species may have larger brains or larger brain regions necessary for complex behaviors. In previous work on odorous ants (Formicidae: Dolichoderinae) we found no correlation between colony size and these brain properties, but found that relative antennal lobe size scaled negatively with colony size. Therefore, we now test whether sensory systems scale with colony size, with particular attention to olfactory components thought to be involved in nestmate recognition. Across three species of odorous ants, Forelius mccooki , Dorymyrmex insanus , and D. bicolor , which overlap in habitat and foraging ecology but vary in colony size, we compare olfactory sensory structures, comparing those thought to be involved in nestmate recognition. We use the visual system, a sensory modality not as important in social communication in ants, as a control comparison. We find that body size scaling largely explains differences in eye size, antennal length, antennal sensilla density, and total number of olfactory glomeruli across these species. However, sensilla basiconica and olfactory glomeruli in the T6 cluster of the antennal lobe, structures known to be involved in nestmate recognition, do not follow body size scaling observed for other structures. Instead, we find evidence from the closely related Dorymyrmex species that the larger colony species, D. bicolor , invests more in structures implicated in nestmate recognition. To test for functional consequences, we compare nestmate and non-nestmate interactions between these two species and find D. bicolor pairs of either type engage in more interactions than D. insaus pairs. Thus, we do not find evidence supporting a universal pattern of sensory system scaling associated with changes in colony size, but hypothesize that observed differences in the olfactory components in two closely related Dorymyrmex species are evidence of a link between colony size and sensory trait evolution.
... In the present study, we not only investigated the ants' abilities to learn a switch in valence of social signals (compare Bos et al., 2010;Roussel et al., 2012), but we asked our subjects to express the exact opposite of their innate behaviour, making the present experiments, to our knowledge, one of the first assessments of such learning ability in insects. ...
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Learning allows animals to respond to changes in their environment within their lifespan. However, many responses to the environment are innate, and need not be learned. Depending on the level of cognitive flexibility an animal shows, such responses can either be modified by learning or not. Many ants deposit pheromone trails to resources, and innately follow such trails. Here, we investigated cognitive flexibility in the ant Lasius niger by asking whether ants can overcome their innate tendency and learn to avoid conspecific pheromone trails when these predict a negative stimulus. Ants were allowed to repeatedly visit a Y-maze, one arm of which was marked with a strong but realistic pheromone trail and led to a punishment (electroshock and/or quinine solution), and the other arm of which was unmarked and led to a 1 M sucrose reward. After circa 10 trials ants stopped relying on the pheromone trail, but even after 25 exposures they failed to improve beyond chance levels. However, the ants did not choose randomly: rather, most ants begun to favour just one side of the Y-maze, a strategy which resulted in more efficient food retrieval over time, when compared to the first visits. Even when trained in a go/no-go paradigm which precludes side bias development, ants failed to learn to avoid a pheromone trail. These results show rapid learning flexibility towards an innate social signal, but also demonstrate a rarely seen hard limit to this flexibility.
... Typically, snails What can we teach Lymnaea? trained in one context only showed memory if memory testing was performed in the same context, similar to results obtained for other invertebrate models such as Aplysia, C. elegans, honeybees, Drosophila and ants, and in studies on mammals (Ardiel & Rankin, 2010;Bos, Guerrieri & d'Ettorre, 2010;Kahsai & Zars, 2011;Fujinaka et al., 2016;Panoz-Brown et al., 2016;Giurfa, 2017). However, context generalization was reported in predator-experienced Lymnaea. ...
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This review describes the advantages of adopting a molluscan complementary model, the freshwater snail Lymnaea stagnalis, to study the neural basis of learning and memory in appetitive and avoidance classical conditioning; as well as operant conditioning of its aerial respiratory and escape behaviour. We firstly explored ‘what we can teach Lymnaea’ by discussing a variety of sensitive, solid, easily reproducible and simple behavioural tests that have been used to uncover the memory abilities of this model system. Answering this question will allow us to open new frontiers in neuroscience and behavioural research to enhance our understanding of how the nervous system mediates learning and memory. In fact, from a translational perspective, Lymnaea and its nervous system can help to understand the neural transformation pathways from behavioural output to sensory coding in more complex systems like the mammalian brain. Moving on to the second question: ‘what can Lymnaea teach us?’, it is now known that Lymnaea shares important associative learning characteristics with vertebrates, including stimulus generalization, generalization of extinction and discriminative learning, opening the possibility to use snails as animal models for neuroscience translational research.
... It is likely that queens may sense the shortage of workers due to a decrease in contact with workers. Studies have shown that ants typically communicate by cuticle hydrocarbons which are perceived by the olfactory organs (Vander Meer et al., 1989;Saïd et al., 2005;Ichinose and Lenoir, 2009;Bos et al., 2010), hence a decrease in the amount of cuticle hydrocarbons perceived might be an indicator to queens that the worker population has decreased. Maximum worker behavior frequencies were observed on the 8th day of the experiment, coinciding with minimum egg laying frequencies. ...
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Many species of social Hymenoptera demonstrate behavioral flexibility, where older workers that typically forage can revert to younger worker tasks, such as nursing, when these are absent. This flexibility is typical of the sterile worker class, yet rare in queens. In the little fire ant (Wasmannia auropunctata), queens have been reported to perform only egg laying. We examined behavior of queens of W. auropunctata after demographic manipulation. When half of the workers were removed from the colony, queens were observed caring for eggs, larvae and pupae as well as eating outside of the nest, like forager workers. We examined the relationship between these atypical queen behaviors and their juvenile hormone binding protein (JHbp) and vitellogenin (Vg) expression via QRT-PCR method. JHbp and Vg expression decreased when queens were performing worker tasks, resembling the expected expression pattern of typical sterile workers. Flexibility in queen behaviors in the little fire ant may be an important adaptation to changing environments. As a significant invasive species, such adaptation may increase the probability of colony survival during propagation. Our results not only present new insights in behavioral flexibility in social insects, but also increases our understanding of the success of this significant invasive species.
... In A. mellifera, workers only react to isopentyl acetate, the main component in the alarm pheromone, when they are in groups, and they are most sensitive when they are close to the colony entrance [110]. In Camponotus aethiops, an odor presented on nonnestmate ant elicited aggression even though the same odor was previously associated with a reward and learned as a positive stimulus [111]. Temnothorax rugatulus reject a new nest marked with 2,5-dimethylpyrazine, their alarm pheromone, but move towards it near their home nest [112]. ...
Pheromones mediating social behavior are critical components in the cohesion and function of the colony and are instrumental in the evolution of eusocial insect species. However, different aspects of colony function, such as reproductive division of labor and colony maintenance (e.g. foraging, brood care, and defense), pose different challenges for the optimal function of pheromones. While reproductive communication is shaped by forces of conflict and competition, colony maintenance calls for enhanced cooperation and self-organization. Mechanisms that ensure efficacy, adaptivity and evolutionary stability of signals such as structure-to-function suitability, honesty and context are important to all chemical signals but vary to different degrees between pheromones regulating reproductive division of labor and colony maintenance. In this review, we will discuss these differences along with the mechanisms that have evolved to ensure pheromone adaptivity in reproductive and non-reproductive context.
... Individual recognition, familiarity and kinship play key roles in the modulation of social behaviour, particularly competition and mate choice [30]. The majority of mammals are small-brained (e.g. they have a high ratio of limbic to cortical structures), with the regulation of social relationships requiring individual recognition by olfactory cues [31]. ...
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Olfaction is the primary sensory communication mode for most mammals; social, sexual, maternal and feeding behaviours are four basic and fundamental aspects directly related to olfaction. Herein we consider these four main aspects of olfaction in a variety of mammals from the families Ungulata and Carnivora. Firstly, we provide a brief explanation on the anatomy and how olfaction is modulated. In particular, we discuss the literature in the context of recent trends in main olfactory epithelium and vomeronasal organ functions, briefly explaining the main differences between the anatomical olfactory structures of various domestic animals. Subsequently, examples of animal welfare implications of diet selection, predation, aversion, breeding and mother–young bonding behaviours are described. An ethological view of olfaction in addition to the brain structure and olfaction morphology aspects has been covered, as it offers a promising approach in the welfare of mammalian species under our care. We conclude that the knowledge of the roles played by olfaction in chemical communication may help improving housing conditions, fulfilment of feeding requirements, handling and breeding of companion, farm and zoo mammals, and promote the development of appropriate social, sexual, parental and feeding behaviours thus enhancing animal welfare.
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In this opinion piece, we briefly review our knowledge of the mechanisms underlying auditory individual recognition in birds and chemical nest-mate recognition in social Hymenoptera. We argue that even though detection and perception of recognition cues are well studied in social Hymenoptera, the neural mechanisms remain a black box. We compare our knowledge of these insect systems with that of the well-studied avian ‘song control system’. We suggest that future studies on recognition should focus on the hypothesis of a distributed template instead of trying to locate the seat of the template as recent results do not seem to point in that direction. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.
Events typically occur in a specific context and the ability to assign importance to this occurrence plays a significant role in memory formation and recall. When the scent of a crayfish predator (CE) is encountered in Lymnaea stagnalis strains known to be predator experienced (e.g. the W-strain), enhancement of memory formation and depression of feeding occur, which are part of a suite of anti-predator behaviours. We hypothesized that Lymnaea possess a form of higher-order conditioning, namely configural learning. We tested this by simultaneously exposing W-strain Lymnaea to a carrot food odour (CO) and predator scent (CE). Two hours later, we operantly conditioned these snails with a single 0.5 h training session in CO to determine whether training in CO results in long-term memory (LTM) formation. A series of control experiments followed and demonstrated that only the CO+CE snails trained in CO had acquired enhanced memory-forming ability. Additionally, following CE+CO pairing, CO no longer elicited an increased feeding response. Hence, snails have the ability to undergo configural learning. Following configural learning, CO becomes a risk signal and evokes behavioural responses phenotypically similar to those elicited by exposure to CE.
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Strong evidence indicates that in Polistes wasps, as in other social insects, epicuticular lipids are involved in several aspects of recognition, such as nest-, nestmate- and fertility recognition. This evidence is based both on the study of differences in composition between groups of conspecific individuals (members of different colonies; age groups; dominants and subordinates; fertile and infertile individuals), and on bioassays. The first part of this review considers the general characteristics of Polistes epicuticular hydrocarbons and summarises what is currently known about the non-hydrocarbon articular lipids. The second part concerns the most relevant contributions of the work on Polistes towards an understanding of the role of epicuticular hydrocarbons as semiochemicals in social insects. Four aspects, highlighted in 1993 by Howard, as future directions for the study of epicuticular hydrocarbons will be considered: (i) the need for a complete determination of epicuticular hydrocarbon structures (in particular chirality); (ii) the role of individual hydrocarbons as semiochemicals, or of classes of hydrocarbons in the epicuticular mixtures; (iii) the intraspecific variability in epicuticular lipid composition; and, (iv) current knowledge about cuticular hydrocarbon perception by insects.
Both behavioral and chemical analyses demonstrated that in the ant Camponotus vagus the colony recognition signal is strongly correlated with the composition of cuticular hydrocarbons. Variation of relative proportions of dimethylalkanes characterize the chemical signatures in different colonies.
In the last decades North African desert ants of the genus Cataglyphis FOERSTER, 1850 - and more recently their eco logical equivalents in the Namib desert (Ocymyrinex EMERY, 1886) and Australia (Melophorus LUBBOCK, 1883) - have become model organisms for the study of insect navigation. While foraging individually over distances of many thousand times their body lengths in featureless as well as cluttered terrain, they navigate predominantly by visual means using vector navigation (path integration) and landmark-guidance mechanisms as well as systematic-search and target-expansion strategies as their main navigational tools. In vector navigation they employ several ways of acquiring information about directions steered (compass information) and distances covered (odometer information). In landmark guidance they rely on view-based information about visual scenes obtained at certain vantage points and combined with certain steering (motor) commands of what to do next. By exploring how these various navigational routines interact, the current position paper provides a hypothesis of what the architecture of the ant's navigational toolkit might look like. The hypothesis is built on the assumption that the toolkit consists of a number of domain-specific routines. Even though these routines are quite rigidly preordained (and get modified during the ant's lifetime by strictly task-dependent, rapid learning processes), they interact quite flexibly in various, largely context-dependent ways. However, they are not suited to provide the ant with cartographic information about the locations of places within the animal's foraging environment. The navigational toolkit does not seem to contain a central integration state in which local landmark memories are embedded in a global system of metric coordinates.
Abstract Hydrocarbons are the main lipid constituents on the insect cuticle, and generally provide the insect with a waterproof layer to prevent desiccation. In many insects this class ofchemicals,has been coopted to serve as pheromones. In so- cial insects, in particular in ants cuticular hydrocarbons (CHCs) have at least two pheromonal functions. They act as recognition cues that facilitate colony insularity, protecting it from parasites or conspecific invasions. Supporting evi- dence for this function are their extreme complexity, their colony specific composition, and in a few cases also de- monstrating elevated or reduced,aggression between,encountering ants as a function of the label (alien or nestmate) they were painted with. The second function of CHCs is in signaling fertility. In many ant species it was demonstrated that fertile individuals (queens, gamergates, or egg laying workers) have CHC profiles that are distinct from that of their sterile nestmates. This can be expressed as the augmentation of a single or a small subset of the blend components, or differences in the entire blend. The fact that these signals have an abundance of branched alkanes, which lower the break point of cuticular impermeability thus imposing cost on the individual, indicates that these may constitute honest signals. This dual function seems contradictory since nestmate recognition necessitates a uniform colony odor, i.e., uniform CHC composition, whereas fertility signal requires idiosyncrasy since the fertile individual needs to be singled out among the colony members,rather than conform to colony odor. A possible resolution is that species that use CHCs for nestmate recognition do not use them as fertility signals and vice versa. I propose an alternative solution whereby,workers have variable discrimination thresholds and response to differences in the pheromone blend, large or small, in a context- dependent manner. Key words:Cuticular hydrocarbons, nestmate recognition, fertility signals, pheromones, reproductive skew. Myrmecol. News 10: 59-68 Prof. Dr. Abraham Hefetz, Department of Zoology, George S. Wise Faculty of LifeScience, Tel Aviv University, Ramat Aviv 69978, Israel. E-mail:
The ability to recognize group members is a key characteristic of social life. Ants are typically very efficient in recognizing non-group members and they aggressively reject them in order to protect their colonies. There are a range of different recognition mechanisms including prior association, phenotype matching, and recognition alleles. The concept of kin recognition should be considered different from that of nestmate recognition. Most of the available studies address the nestmate recognition level, namely the discrimination of nestmates from non-nestmates, independently of actual relatedness. Indirect and direct evidence identify long-chain cuticular hydrocarbons as the best candidates to act as recognition cues in ants, even if other chemical substances could also play a role, at least in some ant species. The relative importance of genetic and environmental factors on the expression and variation of the cuticular hydrocarbon profile vary among species and is linked to life history strategies.