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Sucrose responsiveness, learning success, and task specialization in ants

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Social insects possess remarkable learning capabilities, which are crucial for their ecological success. They also exhibit interindividual differences in responsiveness to environmental stimuli, which underlie task specialization and division of labor. Here we investigated for the first time the relationships between sucrose responsiveness, behavioral specialization, and appetitive olfactory learning in ants, including reproductive castes. We show that castes of the ant Camponotus aethiops differ in their responsiveness to sucrose and in their learning success in olfactory conditioning experiments in which sucrose is used as reward. Olfactory learning was better in foragers than in nurses, in agreement with their higher sucrose responsiveness. Interindividual variation in stimulus responsiveness and in learning may be, therefore, a crucial factor for division of labor in social insects.
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10.1101/lm.031427.113Access the most recent version at doi:
2013 20: 417-420 Learn. Mem.
Margot Perez, Uther Rolland, Martin Giurfa, et al.
in ants
Sucrose responsiveness, learning success, and task specialization
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Brief Communication
Sucrose responsiveness, learning success, and task
specialization in ants
Margot Perez,
Uther Rolland,
Martin Giurfa,
and Patrizia d’Ettorre
Research Center on Animal Cognition, University of Toulouse, UPS, F-31062 Toulouse Cedex 9, France;
Research Center on Animal
Cognition, CNRS, F-31062 Toulouse Cedex 9, France;
Laboratory of Experimental and Comparative Ethology, University Paris 13,
Sorbonne Paris Cite
, F-93430 Villetaneuse, France
Social insects possess remarkable learning capabilities, which are crucial for their ecological success. They also exhibit inter-
individual differences in responsiveness to environmental stimuli, which underlie task specialization and division of labor.
Here we investigated for the first time the relationships between sucrose responsiveness, behavioral specialization, and ap-
petitive olfactory learning in ants, including reproductive castes. We show that castes of the ant Camponotus aethiops differ in
their responsiveness to sucrose and in their learning success in olfactory conditioning experiments in which sucrose is used
as reward. Olfactory learning was better in foragers than in nurses, in agreement with their higher sucrose responsiveness.
Interindividual variation in stimulus responsiveness and in learning may be, therefore, a crucial factor for division of labor
in social insects.
[Supplemental material is available for this article.]
The capacity to learn and form robust memories about events in
the environment is a distinctive trait of social insects (Giurfa
2007, 2013; Avargue
s-Weber et al. 2011). It allows them to master
changing environments and contributes to their ecological
success. Social insects are mainly known for their sophisticated co-
lonial organization, which relies on division of labor—the special-
ization of individuals in reproduction or in colony maintenance
tasks such as brood care, foraging, nest defense, or storage of
food resources (Wilson 1971). Task specialization is typically en-
sured by individuals of different morphological castes and/or ages.
Different models have been proposed to explain division of
labor and its relation to colony organization (Beshers and Fewell
2001). The response threshold model, which has been extremely
influential in this framework, posits that individuals differ in their
sensitivity (and therefore in their responsiveness) to biologically
relevant stimuli associated with specific tasks, thus leading to
the emergence of division of labor (Robinson 1992; Bonabeau et
al. 1996). Differential responsiveness to stimuli that act as positive
(e.g., food) or negative (e.g., noxious events) reinforcements re-
sults also in variable learning performances, in which individuals
learn better about reinforcements to which they are more sensi-
tive (Scheiner et al. 2005).
These behavioral traits have been studied in the honeybee
Apis mellifera where individual differences in sucrose responsive-
ness correlate with individual tendencies to forage either for pol-
len or nectar (Page et al. 1998; Pankiw and Page 1999; Pankiw et al.
2001; Scheiner et al. 2003). Pollen foragers, for instance, are more
responsive to a broad spectrum of sucrose concentrations than
nectar foragers, which respond mainly to higher sucrose concen-
trations (Pankiw and Page 1999). In these experiments, sucrose re-
sponsiveness was quantified by stimulating the antennae of
restrained bees with increasing sucrose concentrations and deter-
mining if proboscis extension reflex (PER) occurred (Pankiw and
Page 1999). Interindividual differences are established either via
a sucrose response threshold (SRT), i.e., the sucrose concentration
at which the response to sucrose differs from that to water (Page
et al. 1998), or a sucrose response score (SRS), which is the total
number of PER to a series of sucrose concentrations (Pankiw
et al. 2001). Sucrose responsiveness not only correlates with the
task performed by a bee, but also with its learning success: The
lower the SRT (i.e., the higher the SRS), the higher the bee’s ability
to learn in appetitive conditioning tasks (Scheiner et al. 1999,
2001a,b, 2003; Scheiner and Arnold 2010). These correlations re-
main so far unique as the interplay between learning, reinforce-
ment responsiveness, and social organization has not been
studied in any other social insect.
Ants constitute a remarkable example of eusocial lifestyle
lldobler and Wilson 1990). Despite their sophisticated social
organization and division of labor, little is known about the deter-
minants of these specializations. Responses to food are flexible and
may change among individuals in several ant species (e.g., Josens
et al. 1998; Falibene et al. 2009; Schilman 2011). Interindividual
differences in sucrose responsiveness were found in immobilized
workers of various ant species, which were stimulated with differ-
ent concentrations of sucrose solution (Falibene and Josens
2012). The possible relationship between these differences, learn-
ing success, and behavioral specializations within the colony
remains, however, unknown. Yet, relating these variables is possi-
ble because, besides the possibility of testing sucrose respon-
siveness, controlled learning protocols have been recently
established for ants (Dupuy et al. 2006; Guerrieri and d’Ettorre
2010; Guerrieri et al. 2011).
Here we provide the first comprehensive study investigating
the interplay between learning success, sucrose responsiveness,
and task specialization in ants. We focused on the carpenter ant
Camponotus aethiops, which feeds to some extent on nectar (most-
ly from extra-floral nectaries); this species can also be subjected
to appetitive olfactory conditioning in harnessing conditions in
the laboratory (Guerrieri and d’Ettorre 2010). We determined
whether different castes differ in their SRS and analyzed how
SRS levels relate to task specialization. We further studied if nurses
and foragers differ in appetitive olfactory learning and if these dif-
ferences relate to their respective SRS levels.
Corresponding authors
Article is online at
2013, Published by Cold Spring Harbor Laboratory Press
ISSN 1549-5485/13;
417 Learning & Memory
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Nine queenright colonies of C. aethiops were collected at
Pompertuzat (Midi-Pyre
es, France, latitude 43.5
, longitude
) and keptin the laboratory (24
C, 12-h lightdark cycle,
60% humidity), each in two Fluon-coated plastic boxes connected
by a plastic hose. One box was provided with plaster floor and cov-
ered by cardboard (nest); the other was exposed to light (foraging
arena). Colonies were deprived of sucrose 3 wk before the experi-
ments. Mealworms and water were provided ad libitum.
For the experiments, each ant was immobilized by cooling it
on ice for 10 min and then harnessed in a holder (Eppendorf of 0.2
mL for workers and males, and 1.5 mL for gynes from which the
tip was removed). The ant’s head was then passed through the api-
cal hole and strips of adhesive tape were placed between the head
and the thorax to prevent body movements except those of the
antennae and mouthparts (Supplemental Fig. S1; Guerrieri and
d’Ettorre 2010). Ants were then kept in a humid box over 3 h for
recovery and habituation to the harness.
Individual responsiveness scores were quantified via the max-
illalabium extension response (MaLER) (Guerrieri and d’Ettorre
2010) upon stimulation with a series of linear logarithmic ascend-
ing concentrations of sucrose solution (0.1%, 0.3%, 1%, 3%, 10%,
and 30% w/w) (Page et al. 1998). Each stimulation lasted 2 sec.
Prior to each sucrose stimulation water was delivered to control
for sensitization or habituation to increasing sucrose concentra-
tion. Groups of 15 ants were tested, one ant at a time, with an in-
terstimulus interval of 7 min. A 10-sec interval was established
before and after stimulus presentation to avoid contextual effects.
MaLER was scored as 1 when visible, 0 otherwise. Individuals that
did not respond to concentrations that were higher than those
eliciting prior to responding were discarded (7% of ants in
both experiments). Individual sucrose and water responsiveness
scores (SRS and WRS, respectively), were quantified as the sum of
the ant’s response to either stimulus. These scores varied between
0 (no response at any sucrose/water stimulation) and 6 (response
to all sucrose/water stimulations) (Scheiner et al. 2003).
In Experiment 1, we compared the sucrose responsiveness of
five castes performing different tasks: gynes, males, nurses, inac-
tive workers, and foragers. Gynes and males were collected from
three colonies 2 wk after they showed activity in the foraging are-
na; minor workers were collected from two different colonies and
assigned to one of three behavioral castes (marked with different
color paint) after 2 wk of behavioral observations (1 h, twice a
day):foragers, if theycollected food or water;nurses, if they werein-
volved in brood care, or “inactive,” if they
displayed reduced locomotor activity and
a distended (full) abdomen at the begin-
ning of sucrose deprivation. The SRS of
eachcaste wasthen determined (for work-
ers, assays were performed blind with re-
spect to individual behavioral task).
In Experiment 2, nurses and for-
agers were tested for their SRS and then
subjected to a differential conditioning
procedure with two odors, a rewarding
one and a nonrewarding one. Nurses
and foragers were collected from four col-
onies and their SRTs were determined.
Individuals that responded to the highest
sucrose concentration assay (30%) were
used 1 h later for differential condition-
ing experiments in which the uncondi-
tioned stimulus (US) was 30% sucrose
solution. We trained ants to respond
with MaLER to a CS+ odor paired with
the US and not to a CS2 odor that was
not paired with the US. Octanal and hex-
anol (floral scents, Sigma Aldrich) were used as CS+ and CS2 in a
balanced way. Six microliters of pure odorant were applied onto a
piece of filter paper that was inserted in a plastic 10-mL syringe.
Ants responding to the first presentation of the CS+ or the CS2
were discarded. The acquisition phase consisted of 12 trials (six
CS+ presentations and six CS2 presentations in pseudo-random
order, i.e., no more than two trials of the same CS type were al-
lowed [Guerrieri and d’Ettorre 2010]). Each trial lasted 1 min. In
CS+ trials, odor stimulation lasted 5 sec and preceded sucrose
stimulation by 3 sec, which also lasted 5 sec. In CS2 trials, only
the 5-sec odorant stimulation was delivered. In both cases, 25 sec
and 30 sec elapsed before and after stimulus delivery, respectively.
Intertrial interval was 10 min. An air extractor was placed behind
the ant to remove undesired odorant stimulations. Only individu-
als that responded at least five times to the US were included in the
statistical analyses. Individual acquisition scores to CS+ (AS+)
and CS2 (AS
were calculated as the sum of an ant’s conditioned
responses (CR) to CS+ and CS2, respectively. These scores vary be-
tween 0 (no CR to CS+/CS2) and 5 (CR to CS+/CS2 in trials 26).
Statistical analyses were performed with R environment (ver-
sion 2.15.0, Two-tailed Kruskal
Wallis tests were used to test variation in SRS and WRS between
worker and sexual castes (package pgirmess; see CRAN.R-project.
org/package¼ pgirmess). Multiple WilcoxonMannWhitney
rank sum tests were applied for pairwise comparisons between
castes (with sequential Bonferroni corrections) and for testing dif-
ferences in SRS, WRS, AS+, and AS2 between nurses and foragers.
Spearman rank correlation test was used to study correlations be-
tween SRS and AS+ (Rcorr function, package Hmisc; http:// For further details about
statistics see Supplemental Material.
In Experiment 1, sucrose and water responsiveness scores
(SRS and WRS, respectively) differed significantly between castes
(SRS, KruskalWallis, x
¼ 69.58, df ¼ 4, P , 0.001 [Fig. 1A];
WRS, x
¼ 57.21, df ¼ 4, P , 0.001 [Fig. 1B]; see Supplemental
Fig. S2 for sucrose and water responsiveness curves). Although for-
agers and males exhibited higher SRS and WRS values, inactive
workers and gynes showed lower SRS and WRS values. Nurses
showed intermediate SRS values and WRS values similar to those
of foragers (Table 1).
In Experiment 2, we quantified sucrose responsiveness of
nurses and foragers (Supplemental Fig. S3) and kept only those
ants (83.87% and 50.81%, respectively, of foragers and nurses
Figure 1. Sucrose and water responsiveness scores of the five castes. (A) Box plots of sucrose respon-
siveness score of nurses (n ¼ 37), inactive workers (n ¼ 34), foragers (n ¼ 44), gynes (n ¼ 23), and
males (n ¼ 26). (B) Boxplots of water responsiveness scores of the same individuals. SRS and WRS
vary between 0 (no response to sucrose/water stimulation) and 6 (response to all six stimulations).
Boxes show median (line and dot), 1st and 3rd quartiles, 5th and 95th percentiles (whiskers).
Groups that are statistically different have different letters.
Sucrose responsiveness and learning in ants 418 Learning & Memory
Cold Spring Harbor Laboratory Press on July 19, 2013 - Published by learnmem.cshlp.orgDownloaded from
assayed) that responded to the highest sucrose concentration
(30%), used as US in the subsequent conditioning procedure. As
in the previous experiment, SRS values were significantly higher
in foragers than in nurses, but WRS values were not statistically
different (SRS, WilcoxonMannWhitney rank sum test, W ¼
890.5, P , 0.05; WRS, W ¼ 1028.5, P ¼ 0.25).
Both castes learned the discrimination between rewarded
and unrewarded odors (see Supplemental Fig. S4 for learning
curves), but foragers learned the olfactory discrimination better
than nurses. Indeed, foragers exhibited higher AS+ values than
nurses (W ¼ 888, P , 0.05) (Fig. 2), although AS2 values did not
differ (W ¼ 1077.5, P ¼ 0.31). Thus, AS+ values are a reliable indi-
cator of individual learning success. AS+ values were positively
correlated with SRS values for nurses (n ¼ 35, rs ¼ 0.62, P ,
0.0001) and approached significance for foragers (n ¼ 68, rs ¼
0.23, P ¼ 0.055). AS2 values also correlated positively with SRS
values both for nurses (n ¼ 35, rs ¼ 0.54, P , 0.0001) and foragers
(n ¼ 68, rs ¼ 0.28, P ¼ 0.05), thus indicating that the excitatory
strength from the CS+ generalized in part to the CS2.
Our results show for the first time that different castes of an
ant species exhibit a significant variation in their sucrose respon-
siveness, which is ecologically relevant since these ants feed on
extra-floral nectaries. This inter-caste variation in sucrose re-
sponse scores (SRS) found in C. aethiops is in line with the response
threshold model of division of labor
(Beshers and Fewell 2001): Foragers, for
instance, proved to be highly sensitive
both to sucrose (high SRS) and to water
(high WRS). Higher WRS and SRS endow
ants with the capacity to collect water
and to sample food sources of variable
quality, thus increasing information
gathering about potential food sources.
Inactive workers, in contrast, exhibited
low WRS and SRS as they did not practi-
cally respond to water and responded
to the highest sucrose concentra-
tions. This high selectivity for sucrose is
adaptive in a scenario in which inactive
workers serve as sucrose storers for the
colony. The low SRS found in these ants
could relate to the fact that crop filling
induces a decrease in sucrose responsive-
ness (Falibene and Josens 2012). Nurses,
which are younger than foragers and in-
active workers (Ho
lldobler and Wilson
1990), responded to intermediate sucrose concentrations. They
could, therefore, modulate their responsiveness and specialize in
different tasks as they age. Gynes responded only to highest
sucrose concentrations probably because they need to store ener-
gy for solitary colony founding and egg laying. By contrast, males,
which die quickly after swarming and do not need to store energy,
may afford high responsiveness to water and low sucrose concen-
trations. This scenario thus proposes that both sucrose and water
responsiveness are adaptive traits related to the specific biological
constraints of each caste. Variations in water responsiveness
would reflect such biological differences and a general state of re-
sponsiveness to appetitive stimuli rather than being the mere re-
sult of sucrose sensitization.
The superior learning performance of foragers compared to
that of nurses is relevant for quickly acquiring local environmen-
tal cues (e.g., olfactory ones) predicting food, thus increasing for-
aging efficiency. Their higher level of acquisition likely results
from their higher responsiveness to sucrose reward (i.e., their
high SRS), similarly to honeybees, where pollen foragers show
better acquisition performances than nectar foragers due to their
higher responsiveness to sucrose (Scheiner et al. 2005).
The picture emerging from these experiments is one in
which castes within an ant colony differ in terms of their respon-
siveness to food reward and therefore in their learning capabilities
in conditioning experiments in which this food reward is used as
US. Although learning was only evaluated in foragers and nurses,
the sucrose scores found for the other castes allow predicting their
learning success. Males, like foragers, had higher SRS and are thus
expected to have a learning success as high as that of foragers.
Inactive workers and gynes, which showed SRS lower than those
of nurses, should be the less efficient learners.
In conclusion, C. aethiops exhibit interindividual variability
in sucrose and water responsiveness, thereby supporting the re-
sponse threshold model of division of labor. Differences in appe-
titive learning are thus likely mediated by sucrose responsiveness
and relate to behavioral tasks.
We thank A. Dussutour and S. Teseo for comments on previous
versions of the manuscript and H. Ro
del for help with statistical
analyses. M.G. was supported by the Institut Universitaire de
France, the French Research Council (CNRS) and the University
Paul Sabatier and P.dE. by a Marie Curie Reintegration Grant.
Figure 2. Learning success of nurses and foragers. Box plots of acquisition score to (A)CS+ (AS+)
and (B)CS2 (AS2) of nurses (n ¼ 35) and foragers (n ¼ 68). AS+ and AS2 vary between 0 (no re-
sponse to CS+ and CS2, respectively, during all successive trials) and 5 (positive responses to CS+
and CS2, respectively, after the first trial). Boxes show median (line and dot), 1st and 3rd quartiles,
5th and 95th percentiles (whiskers). (
) P , 0.05.
Table 1. Comparison of SRS and WRS between castes
Caste 1 Caste 2
SRS (adjusted
WRS (adjusted
Foragers Nurses ,0.05 0.052
,0.001 ,0.001
Gynes ,0.001 ,0.001
Males NS NS
Nurses Inactive
,0.001 ,0.05
Gynes ,0.01 ,0.05
Males ,0.01 ,0.001
Gynes NS NS
Males ,0.001 ,0.001
Gynes Males ,0.001 ,0.001
Adjusted P-values correspond to pairwise comparisons of scores between
each caste (sequential Bonferroni corrections after multiple Wilcoxon
MannWhitney rank sum tests). (NS) not significant.
Sucrose responsiveness and learning in ants 419 Learning & Memory
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This work was supported by the CNRS research network GDR 2822
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... The model posits that individuals differ in their sensitivity (and therefore in their responsiveness) to a biologically relevant stimuli associated with specific tasks, thus leading to the emergence of division of labor (Robinson, 1992;Bonabeau et al., 1997;Beshers & Fewell, 2001). In this sense, it has been shown that in honeybees and ants, responsiveness to sucrose varies with age, experience, and subcaste (Pankiw & Page, 1999;Falibene & Josens, 2012;Perez et al., 2013). For example, in Camponotus aethiops ants, a significant variation in the sucrose responsiveness between nurse and foraging workers has been observed (Perez et al., 2013). ...
... In this sense, it has been shown that in honeybees and ants, responsiveness to sucrose varies with age, experience, and subcaste (Pankiw & Page, 1999;Falibene & Josens, 2012;Perez et al., 2013). For example, in Camponotus aethiops ants, a significant variation in the sucrose responsiveness between nurse and foraging workers has been observed (Perez et al., 2013). In our work, age and long-term experience effects are difficult to separate due to the experimental design deployed; nevertheless, our results suggest that variation in responsiveness between subcastes does not seem to occur in V. germanica wasps. ...
Decisions made by foraging animals conform a complex process based on the integration of information from multiple external environmental stimuli and internal physiological signals, which in turn are modulated by individual experience and a detection threshold of each individual. For social insects in which foraging is limited to given age sub-castes, individual foraging decisions may also be affected by ontogenetic shifts and colony requirements. We studied the short-term changes in foraging preferences of the generalist wasp Vespula germanica, focusing on whether the individual response to different resources could be influenced by the ontogenetic shifts and/or by social interaction with nestmates. We carried both laboratory and field experiments to confront worker wasps to a short-term resource switch between either protein or carbohydrate-based foods. We tested the response of (1) Pre-forager workers (no foraging experience nor interaction with other wasps), (2) Forager workers (experience in foraging and no colony feedback), and (3) Wild forager workers (foraging naturally and exposed to free interactions with nestmates). We evaluated the maxilla-labium extension response (MaLER) for laboratory assays or the landing response for field assays. We observed that for wasps deprived of colony feedback (either pre-foragers or foragers), the protein-rich foods acceptance threshold increased (and thus a lower level of foraging on that item was observed) if they had foraged on carbohydrates previously, whereas carbohydrates were accepted in all assays. However, wasps immersed in a natural foraging context did accept protein foods regardless of their first foraging experience and reduced the carbohydrates collected when trained on protein foods. We provide evidence that short-term changes in foraging preferences depend on the type of resource foraged and on the social interactions, but not on ontogenetic shifts. This article is protected by copyright. All rights reserved
... ; Beshers and Fewell, 2001;Perez et al., 2013;Mattiacci, 2019;Balbuena and Farina, 2020). Individuals with a relatively low threshold for a given task tend to respond to lower stimulus intensities and, consequently, to learn better if the stimulus acts as reinforcement (e.g. ...
... Individuals with a relatively low threshold for a given task tend to respond to lower stimulus intensities and, consequently, to learn better if the stimulus acts as reinforcement (e.g. food) (Scheiner et al., 2005;Perez et al., 2013). On the contrary, individuals with higher thresholds learn worse about reinforcements to which they are less sensitive. ...
Searching for reward motivates and drives behaviour. In honey bees, Apis mellifera, specialized pollen foragers are attracted to and learn odours with pollen. However, pollen's role as a reward remains poorly understood. Unlike nectar, pollen is not ingested during collection. We hypothesized that pollen (but not nectar) foragers could learn pollen by the sole antennal or tarsal stimulation. Then, we tested how pairing of pollen (either hand- or bee-collected) and a neutral odour during a pre-conditioning affects performance of both pollen and nectar foragers during the classical conditioning of the proboscis extension response. Secondly, we tested whether nectar and pollen foragers perceive the simultaneous presentation of pollen (on the tarsi) and sugar (on the antennae) as a better reinforcement than sucrose alone. Finally, we searched for differences in learning of the pollen and nectar foragers when they were prevented from ingesting the reward during the conditioning. Differences in pollen reinforced learning correlate with division of labour between pollen and nectar foragers. Results show that pollen foragers performed better than nectar foragers during the conditioning phase after being pre-conditioned with pollen. Pollen foragers also performed better than nectar foragers in both the acquisition and extinction phases of the conditioning, when reinforced with the dual reward. Consistently, pollen foragers showed improved abilities to learn cues reinforced without sugar ingestion. We discussed that differences in how pollen and nectar foragers respond to a cue associated with pollen greatly contribute to the physiological mechanism that underlies foraging specialization in the honeybee.
... A study in honeybees found evidence for life-long personality differences in workers and suggested that the response thresholds to some stimuli could be related to personality type, thus contributing to more robust inter-individual behavioural differences leading to division of labour even when individuals age together or share similar experiences (Walton and Toth, 2016). In carpenter ants, there is evidence for inter-individual variability in sucrose responsiveness and learning success in different behavioural groups of workers performing different tasks (Perez et al., 2013). In the ant Myrmica rubra, individual personality differences are connected to spatial fidelity (the position in the nest) and ants located in a given position show low thresholds to perform tasks associated with that position, thus generating division of labour (Pamminger et al., 2014). ...
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Ants use debris as tools to collect and transport liquid food to the nest. Previous studies showed that this behaviour is flexible whereby ants learn to use artificial material that is novel to them and select tools with optimal soaking properties. However, the process of tool use has not been studied at the individual level. We investigated whether workers specialise in tool use and whether there is a link between individual personality traits and tool use in the ant Aphaenogaster senilis. Only a small number of workers performed tool use and they did it repeatedly, although they also collected solid food. Personality predicted the probability to perform tool use: ants that showed higher exploratory activity and were more attracted to a prey in the personality tests became the new tool users when previous tool users were removed from the group. This suggests that, instead of extreme task specialisation, variation in personality traits within the colony may improve division of labour.
... Indeed, social insect behavioral specialists demonstrate increased efficiency in nest emigration (Langridge et al. 2008), nest excavation (Jeanson et al. 2008), undertaking (Trumbo and Robinson 1997;Julian and Cahan 1999), and response to sucrose (Perez et al. 2013). ...
Collective behavior is widespread in nature and examples include schools of fish and nest building in social insects. Although collective behavior and other group-level phenotypes are assumed to be shaped by selection, we do not know to what degree they are heritable and how selection acts on them. Furthermore, we have identified relatively few genes underlying variation in group-level phenotypes, hindering our understanding of the molecular mechanisms by which genes influence these traits and how they evolve. Elucidating the genetic architecture underlying group-level phenotypes is especially diffuclt because it depends on the genotypes of multiple interacting individuals. In this thesis, we use a new pharaoh ant (Monomorium pharaonis) laboratory mapping population to investigate the genetic architecture underlying a number of group-level phenotypes. These group-level phenotypes include collective behaviors (foraging, aggression, and exploration) and cuticular hydrocarbons, which play a vital role in chemical communication within social insect colonies. We demomonstrate that these phenotypes are heritable and have fitness consequences – the two prerequites for evolution via natural selection. Next, we perform genome-wide association studies to identify many interesting candidate genes associated with variation in group-level phenotypes, including genes associated with variation in collective behavior that have been implicated in neurological disorders or in the development of the visual system. Next, we explore how the genetic makeup of groups affects collective behavior and find that the specific combinations of genotypes within a group influence group-level outputs. Finally, we focus on the important social interactions between nurse workers and larvae. We first explore the evolutionary origin of sibling care and find that it likely shares a genetic basis with maternal care. Next, we demonstare that some nurse workers are behaviorally specicialized to care for larvae of different development stages and identify genes differentially expressed between nurses caring for different larval types. These specialized nurse workers likely play a large role in regulating divion of labor within social insect colonies. Overall, this work begins to identify the genetic architecture underlying group-level phenotypes, highlights the importance of within-group genetic composition on group-level output, and demonstrates the important role of nurse workers in modulating group-level phenotypes.
... In Myrmica rubra, foragers are more active, exploratory, aggressive and attracted to light than workers who worked inside the nest (Pamminger et al., 2014). Foragers of Camponotus aethiops show better learning abilities and higher sucrose responsiveness than the nurses (Perez et al., 2013). However, it is not clear from these studies whether personality is related to the age of workers which determines which tasks they will perform. ...
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Animals live in heterogeneous environments where food resources are transient and have to be exploited rapidly. Ants show a wide range of foraging strategies and this activity is tightly regulated irrespective of the mode of recruitment used. Individual foragers base their decision to forage on information received from nestmates (social information). Transmission of information can be in the form of direct physical interactions such as antennation or indirect exchange of information such as laying of pheromone trails. Foragers also rely on information from their internal states or experience (personal information). The interaction between these two sources of information gives rise to plasticity in foraging behavior. Recent studies have examined the role of personality (consistent inter-individual variation in behavioral traits) during ant foraging. Since colonies differ from each other in the distribution of personalities of their members, colonies may consistently differ in behavioral traits, giving rise to colony level personality. However, the interaction between information use and personality, especially at the individual level, remains unexplored. Here, we briefly summarize the literature on the effect of social and personal information on the regulation of ant foraging and the effect of personality on this behavior. We point out that a more focused examination of the interplay between personality and information use will help us understand how behavioral plasticity in the context of foraging is shaped at the colony and individual levels.
... This proboscis extension response (PER) first reflects the integration of gustatory perception and motivation for sugar and then allows feeding. Sucrose-elicited PER has been described and involved in associative learning in restrained insects including moths (Hartlieb, 1996;Fan et al., 1997;Hartlieb et al., 1999a,b;Fan and Hansson, 2001;Skiri et al., 2005;Jorgensen et al., 2007), butterflies ( Kroutov et al., 1999), bees (Menzel, 1999(Menzel, , 2012Page and Erber, 2002;Sandoz, 2011;Giurfa and Sandoz, 2012;Giurfa, 2015) and flies (Fresquet, 1999;Chabaud et al., 2006); similar feeding-related responses exist in ants (Guerrieri and d'Ettorre, 2010;Perez et al., 2013), crickets ( Matsumoto et al., 2015), and bugs (Vinauger et al., 2013;Labrousse et al., 2017). PER has been used by Scheiner and her colleagues to assess responsiveness to sucrose in bees and flies (Scheiner et al., 2004a(Scheiner et al., ,b, 2013Mujagic et al., 2010). ...
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Adult moths need energy and nutrients for reproducing and obtain them mainly by consuming flower nectar (a solution of sugars and other compounds). Gustatory perception gives them information on the plants they feed on. Feeding and food perception are integrated in the proboscis extension response, which occurs when their antennae touch a sugar solution. We took advantage of this reflex to explore moth sugar responsiveness depending on different parameters (i.e., sex, age, satiety, site of presentation, and composition of the solution). We observed that starvation but not age induced higher response rates to sucrose. Presentation of sucrose solutions in a randomized order confirmed that repeated sugar stimulations did not affect the response rate; however, animals were sometimes sensitized to water, indicating sucrose presentation might induce non-associative plasticity. Leg stimulation was much less efficient than antennal stimulation to elicit a response. Quinine prevented and terminated sucrose-elicited proboscis extension. Males but not females responded slightly more to sucrose than to fructose. Animals of either sex rarely reacted to glucose, but curiously, mixtures in which half sucrose or fructose were replaced by glucose elicited the same response rate than sucrose or fructose alone. Fructose synergized the response when mixed with sucrose in male but not female moths. This is consistent with the fact that nectars consumed by moths in nature are mixtures of these three sugars, which suggests an adaptation to nectar perception.
Division of labor is central to the ecological success of social insects. Among honeybees foragers, specialization for collecting nectar or pollen correlates with their sensitivity to gustatory stimuli (e.g. sugars). We hypothesize that pollen and nectar foragers also differ in their sensitivity to odors, and therefore in their likelihood to show odor-mediated responses. To assess foragerś sensitivity to natural odors, we quantified the conditioning of the proboscis extension reflex (PER) to increasing concentrations (0.001; 0.01; 0.1; 1M) of linalool or nonanal. Furthermore, we compared electroantennogram (EAG) recordings to correlate bees’ conditioned responses with the electrophysiological responses of their antennae. To further explore differences of the antennal response of foragers in relation to task-related odors, we registered EAG signals for two behaviorally ‘‘meaningful’’ odors that mediate pollen collection: fresh pollen odors and the brood pheromone (E)-β-ocimene. Pollen foragers performed better than nectar foragers in PER conditioning trials when linalool and nonanal were presented at low concentrations (0.001, 0.01M). Consistently, their antennae showed stronger EAG signals (higher amplitudes) to these odors, suggesting that differences in sensitivity can be explained at the periphery of the olfactory system. Pollen and nectar foragers detect pollen odors differently, but not (E)-β-ocimene. Pollen volatiles evoked EAG signals with hyper and depolarization components. In pollen foragers, the contribution of the hyperpolarization component was higher than in nectar foragers. We discuss our findings in terms of adaptive advantages to learn subtle olfactory cues that influence the ability to better identify/discriminate food sources.
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Division of labor within and between the worker and queen castes is thought to underlie the tremendous success of social insects. Colonies might benefit if subsets of nurse workers specialize further in caring for larvae of a certain stage or caste, given that larval nutritional requirements depend on stage and caste. We used short- (<1 hr) and long-term (ten days) behavioral observations to determine whether nurses of the pharaoh ant ( Monomorium pharaonis ) exhibit such specialization. We found that nurses were behaviorally specialized based on larval instar but not on larval caste. This specialization was widespread, with 56% of nurses in the short-term and between 22-27% in the long-term showing significant specialization. Additionally, we identified ∼200 genes that were differentially expressed in nurse head and abdominal tissues between nurses feeding young versus old larvae. These included 18 genes predicted to code for secreted proteins, which may be passed from nurses to larvae via trophallaxis, as well as vitellogenin and major royal jelly protein-1, which have previously been implicated in the transfer of nutrition from nurse to larvae and the regulation of larval development and caste in social insects. Altogether, our results provide the first evidence in any social insect for a division of labor among nurse workers based on larval stage, and our study begins to elucidate the molecular mechanisms underlying this specialization.
The Argentine ant, Linepithema humile, is native from South America but has become one of the most invasive species in the world. These ants heavily rely on trail pheromones for foraging and previous studies have focused on this signal to develop a strategy of chemical control. Here, we studied the effect of pre-exposure to the trail pheromone on sugar acceptance and olfactory learning in Argentine ants. We used the synthetic trail pheromone component (Z)-9-hexadecenal, which triggers the same attraction and trail following behavior than the natural trail pheromone. We found that pre-exposure to (Z)-9-hexadecenal increases the acceptance of sucrose solutions of different concentrations, thus changing the antś subjective evaluation of a food reward. On the other hand, although ants learned to associate an odor with a sucrose reward, pheromone pre-exposure did neither affect the learning nor the mid-term memory of the odor-reward association. Taking into account the importance of the Argentine ant as a pest and invasive organism, our results highlight the importance of pheromonal cues in resource evaluation, a fact that could be useful in control strategies implemented for this species.
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Foraging exposes organisms to rewarding and aversive events, providing a selective advantage for maximizing the former while minimizing the latter. Honey bees (Apis mellifera) associate environmental stimuli with appetitive or aversive experiences, forming preferences for scents, locations, and visual cues. Preference formation is influenced by inter-individual variation in sensitivity to rewarding and aversive stimuli, which can be modulated by pharmacological manipulation of biogenic amines. We propose that foraging experiences act on biogenic amine pathways to induce enduring changes to stimulus responsiveness. To simulate varied foraging conditions, freely-moving bees were housed in cages where feeders offered combinations of sucrose solution, floral scents, and aversive electric shock. Transient effects were excluded by providing bees with neutral conditions for three days prior to all subsequent assays. Sucrose responsiveness was reduced in bees that had foraged for scented rather than unscented sucrose under benign conditions. This was not the case under aversive foraging conditions, suggesting an adaptive tuning process which maximizes preference for high quality, non-aversive floral sites. Foraging conditions also influenced antennal lobe octopamine and serotonin, neuromodulators involved in stimulus responsiveness and foraging site evaluation. Our results suggest that individuals’ foraging experiences durably modify neurochemistry and shape future foraging behaviour.
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In independent assays, workers of the ant Camponotus mus were conditioned to visit an arena where they found a large drop of sucrose solution of different concentrations, from 5 to 70% weight on weight (w/w). Single ants were allowed to collect the sucrose solution ad libitum, and feeding time, feeding interruptions, crop load, and intake rates were recorded. Feeding time increased exponentially with sucrose concentration, and this relationship was quantitatively described by the increase in viscosity with concen-tration corresponding to pure sucrose solutions. Ants collecting dilute solutions (5 to 15% w/w) returned to the nest with partial crop loads. Crop filling increased with increasing sucrose concentration, and reached a maximum at 42.6% w/w. Workers collecting highly concentrated solutions (70% w/w) also returned to the nest with a partially-filled crop, as observed for dilute solutions. Nectar intake rate was observed to increase with increasing sucrose concentration in the range 5 to 30% sucrose. It reached a maximum at 30.8%, and declined with increasing sucrose concentration. Results suggest that both sucrose concentration and viscosity of the ingested solution modulate feeding mechanics as well as the worker's decision about the load size to be collected before leaving the source.
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Insects possess miniature brains but exhibit a sophisticated behavioral repertoire. Recent studies have reported the existence of unsuspected cognitive capabilities in various insect species that go beyond the traditionally studied framework of simple associative learning. Here, I focus on capabilities such as attentional modulation and concept learning and discuss their mechanistic bases. I analyze whether these behaviors, which appear particularly complex, can be explained on the basis of elemental associative learning and specific neural circuitries or, by contrast, require an explanatory level that goes beyond simple associative links. In doing this, I highlight experimental challenges and suggest future directions for investigating the neurobiology of higher-order learning in insects, with the goal of uncovering the basic neural architectures underlying cognitive processing.
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Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact SUMMARY A simple model of regulation of division of labour in insect societies is introduced and studied. Individuals are assumed to respond to task-related stimuli with response thresholds. When the intensity of a particular stimulus exceeds an individual's response threshold, the individual engages in task performance with high probability, and successful task performance reduces the intensity of the stimulus. If individuals belonging to different (physical or behavioural) castes have different response thresholds, and if thresholds are assumed to remain fixed over the timescales of experiments, this model can account for some observations on ant species of Pheidole (Wilson 1984).
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Chemical trails have been shown to act as an orientation cue in some ant species. Here, I report that the trail-laying behaviour in the nectar-feeding ant, Camponotus rufipes , varies with the concentration of the sucrose solutions collected. Single workers collected solutions of different sucrose concentrations (5%, 20%, and 40% in weight) during 4 consecutive visits to the resource, and their trail-marking behaviour was recorded on soot-coated slides during their first and last visits. Results suggest that these chemical trails provide both an orientation cue between the nest and the food source, as previously suggested for Camponotus ants, as well as information about food quality.
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Associative proboscis extension learning differs widely among bees of a colony. This variety of performances is often related to differences in sucrose responsiveness, which determines learning performance. Sucrose responsiveness is partly determined genetically. We studied for the first time effects of paternal genes on associative learning independent of sucrose responsiveness. To do this, we used wild-type workers stemming from five unrelated patrilines. Bees of the patrilines were first tested for sucrose responsiveness. Only bees with equal sucrose responsiveness were analysed for associative olfactory learning, memory and discrimination. The bees of different patrilines did not differ in their acquisition, memory or discrimination of odours when they had similar sucrose responsiveness. But patrilines differed significantly in their sucrose responsiveness. This shows genetic effects on sensory responsiveness but no independent effects on associative learning.
Bees derived from artificially selected high-and low-pollen-hoarding strains were tested for their proboscis extension reflex response to water and varying sucrose concentrations. High-strain bees had a lower response threshold to sucrose than low-strain bees among pre-foragers, foragers, queens and drones. Preforaging low-strain workers showed ontogenetic changes in their response threshold to sucrose which was inversely related to age. High-strain foragers were more likely to return with loads of water compared to low-strain foragers. Whereas low-strain foragers were more likely to return with loads of nectar. Low-strain nectar foragers collected nectar with significantly higher sucrose concentrations than did the high-strain nectar foragers. Alternatively, low-strain foragers were more likely to return empty compared to high-strain foragers. These studies demonstrate how a genotypically varied sensory-physiological process, the perception of sucrose, are associated with a division of labor for foraging.
Honey bee foragers often show a variation in laboratory proboscis extension learning during the foraging season, making comparisons between experiments difficult. We analysed whether the seasonal variation in learning performance was related to a variation in sucrose responsiveness in pollen and non-pollen foragers. Pollen foragers were very responsive to water and sucrose throughout the season. Non-pollen foragers were overall less responsive and showed more variation. Sucrose responsiveness strongly correlated with tactile and olfactory learning performance in pollen and non-pollen foragers throughout the season. Learning performance was significantly better when sucrose responsiveness was high than when it was low. We suggest conditioning bees that have uniform sucrose responsiveness throughout the season to reduce experimental variance.