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Sucrose responsiveness, learning success, and task specialization in ants

July 2013
Learning & memory (Cold Spring Harbor, N.Y.) 20(8):417-20

DOI:10.1101/lm.031427.113

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PubMed

Authors:

Uther Rolland

University of Burgundy

Martin Giurfa

Sorbonne University

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.

. Comparison of SRS and WRS between castes

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2013 20: 417-420 Learn. Mem.

Margot Perez, Uther Rolland, Martin Giurfa, et al.

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Sucrose responsiveness, learning success, and task specialization

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Brief Communication

Sucrose responsiveness, learning success, and task

specialization in ants

Margot Perez,

1,2,3

Uther Rolland,

Martin Giurfa,

1,2,4

and Patrizia d’Ettorre

3,4

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

(Ho

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

E-mail martin.giurfa@univ-tlse3.fr

E-mail dettorre@leec.univ-paris13.fr

Article is online at http://www.learnmem.org/cgi/doi/10.1101/lm.031427.113.

20:417–420

2013, Published by Cold Spring Harbor Laboratory Press

ISSN 1549-5485/13; www.learnmem.org

417 Learning & Memory

Cold Spring Harbor Laboratory Press on July 19, 2013 - Published by learnmem.cshlp.orgDownloaded from

Nine queenright colonies of C. aethiops were collected at

Pompertuzat (Midi-Pyre

es, France, latitude 43.5

, longitude

1.516667

) and keptin the laboratory (24

C, 12-h light–dark 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-

illa–labium 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 2–6).

Statistical analyses were performed with R environment (ver-

sion 2.15.0, http://www.R-project.org/). 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 Wilcoxon–Mann–Whitney

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://

CRAN.R-project.org/package=Hmisc). 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, Kruskal–Wallis, 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

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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, Wilcoxon–Mann–Whitney 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

only

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.

Acknowledgments

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

P-value)

WRS (adjusted

P-value)

Foragers Nurses ,0.05 0.052

Inactive

workers

,0.001 ,0.001

Gynes ,0.001 ,0.001

Males NS NS

Nurses Inactive

workers

,0.001 ,0.05

Gynes ,0.01 ,0.05

Males ,0.01 ,0.001

Inactive

workers

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–

Mann–Whitney rank sum tests). (NS) not signiﬁcant.

Sucrose responsiveness and learning in ants

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Cold Spring Harbor Laboratory Press on July 19, 2013 - Published by learnmem.cshlp.orgDownloaded from

This work was supported by the CNRS research network GDR 2822

Ethologie.

References

Avargue

s-Weber A, Deisig N, Giurfa M. 2011. Visual cognition in social

insects. Annu Rev Entomol 56: 423 – 443.

Beshers SN, Fewell JH. 2001. Models of division of labor in social insects.

Annu Rev Entomol 46: 413 – 440.

Bonabeau E, Theraulaz G, Deneubourg JL. 1996. Quantitative study of the

ﬁxed threshold model for the regulation of division of labour in insect

societies. Proc R Soc B 263: 1565–1569.

Dupuy F, Sandoz J-C, Giurfa M, Josens R. 2006. Individual olfactory

learning in Camponotus ants. Anim Behav 72: 1081 – 1091.

Falibene A, Josens R. 2012. Sucrose acceptance threshold: A way to measure

sugar perception in ants. Insect Soc 59: 75–80.

Falibene A, de Figueiredo Gontijo A, Josens R. 2009. Sucking pump activity

in feeding behavior regulation in carpenter ants. J Insect Physiol 55:

518–524.

Giurfa M. 2007. Behavioral and neural analysis of associative learning in

the honeybee: A taste from the magic well. J Comp Physiol A 193:

801–824.

Giurfa M. 2013. Cognition with few neurons: Higher-order learning in

insects. Trends Neurosci 363: 285–294.

Guerrieri FJ, d’Ettorre P. 2010. Associative learning in ants: Conditioning of

the maxilla-labium extension response in Camponotus aethiops. J Insect

Physiol 56: 88–92.

Guerrieri FJ, d’Ettorre P, Devaud J-M, Giurfa M. 2011. Long-term olfactory

memories are stabilized via protein synthesis in Camponotus fellah ants.

J Exp Biol 214: 3300 –3304.

lldobler B, Wilson EO. 1990. The ants. Springer-Verlag, Berlin.

Josens R, Farina WM, Roces F. 1998. Nectar feeding by the ant Camponotus

mus: Intake rate and crop ﬁlling as a function of sucrose concentration.

J Insect Physiol 44: 579 – 585.

Page RE Jr, Erber J, Fondrk MK. 1998. The effect of genotype on response

thresholds to sucrose and foraging behavior of honey bees (Apis

mellifera L.). J Comp Physiol A 182: 489–500.

Pankiw T, Page RE Jr. 1999. The effect of genotype, age, sex, and caste on

response thresholds to sucrose and foraging behavior of honey bees

(Apis mellifera L.). J Comp Physiol A 185: 207–213.

Pankiw T, Waddington K, Page RE Jr. 2001. Modulation of sucrose response

thresholds in honey bees (Apis mellifera L.): Inﬂuence of genotype,

feeding, and foraging experience. J Comp Physiol A 187: 293– 301.

Robinson GE. 1992. Regulation of division of labor in insect societies. Annu

Rev Entomol 37: 637– 665.

Scheiner R, Arnold G. 2010. Effects of patriline on gustatory responsiveness

and olfactory learning in honey bees. Apidologie 41:

29–37.

Scheiner

R, Erber J, Page RE Jr. 1999. Tactile learning and the individual

evaluation of the reward in honey bees (Apis mellifera L.). J Comp Physiol

A 185: 1– 10.

Scheiner R, Page RE Jr, Erber J. 2001a. Responsiveness to sucrose affects

tactile and olfactory learning in preforaging honey bees of two genetic

strains. Behav Brain Res 120: 67–73.

Scheiner R, Page RE Jr, Erber J. 2001b. The effects of genotype, foraging

role, and sucrose responsiveness on the tactile learning

performance of honey bees (Apis mellifera L.). Neurobiol Learn Mem

76: 138–150.

Scheiner R, Barnert M, Erber J. 2003. Variation in water and sucrose

responsiveness during the foraging season affects proboscis extension

learning in honey bees. Apidologie 34: 67 – 72.

Scheiner R, Kuritz-Kaiser A, Menzel R, Erber J. 2005. Sensory responsiveness

and the effects of equal subjective rewards on tactile learning and

memory of honeybees. Learn Mem 12: 626 – 635.

Schilman PE. 2011. Trail-laying behavior as a function of resource quality

in the ant Camponotus ruﬁpes. Psyche. doi: 10.1155/2011/139385.

Wilson EO. 1971. The insect societies. Harvard University Press, Cambridge,

MA.

Received April 15, 2013; accepted in revised form June 4, 2013.

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Perez et al - Supplementary Material

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October 2013

Margot Perez · Uther Rolland · Martin Giurfa · Patrizia d'Ettorre

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Aug 2023
INSECT SCI

Workers' task specialization and division of labor are critical features of social insects' ecological success. It has been proposed that the division of labor relies on response threshold models: individuals varying their sensitivity (and responsiveness) to biologically relevant stimuli and performing a specific task when a stimulus exceeds an internal threshold. In this work, we study carbohydrate and protein responsiveness and their relation to worker task specialization in Vespula germanica, an invasive social wasp. The sucrose and peptone responsiveness of two different subcastes, preforagers and foragers, was determined by stimulating the antenna of the wasps with increasing concentrations of the solution and quantifying whether each concentration elicited a licking response. We studied responsiveness in five different ways: (1) response threshold, (2) concentration 50 (concentration to which at least 50% of wasps responded), (3) maximum response, (4) mean scores and (5) median scores. Our results suggest that V. germanica foragers are more sensitive to sucrose (lower thresholds) than preforager workers. However, we found no differences for peptone thresholds (i.e., a protein resource). Nonetheless, this is the first study to investigate response thresholds for protein resources. The intercaste variation in sucrose responsiveness shown in our work contributes to the existing knowledge about response threshold theory as a mechanism for task specialization observed in V. germanica.

Changes in resource perception throughout the foraging visit contribute to task specialization in the honeybee Apis mellifera

Preprint

Full-text available

Nov 2022

Division of labor is central to the ecological success of social insects. Among foragers of the honeybee specialization for collecting nectar or pollen correlates with their sensitivity to sucrose. So far, differences in gustatory perception have been mostly studied in bees returning to the hive, but not during foraging. Here, we showed that the phase of the foraging visit (i.e. beginning or end) interacts with foraging specialization (i.e. predisposition to collect pollen or nectar) to modulate sucrose and pollen sensitivity in foragers. In concordance with previous studies, pollen foragers presented higher sucrose responsiveness than nectar foragers at the end of the foraging visit. On the contrary, pollen foragers were less responsive than nectar foragers at the beginning of the visit. Consistently, free-flying foragers accepted less concentrated sucrose solution during pollen gathering than immediately after entering the hive. Pollen perception also changes throughout foraging, as pollen foragers captured at the beginning of the visit learned and retained memories better when they were conditioned with pollen + sucrose as reward than when we used sucrose alone. Altogether, our results support the idea that changes in foragers' perception throughout the foraging visit contributes to task specialization.

Intraspecific variation in invertebrate cognition: a review

Article

Full-text available

Dec 2023
BEHAV ECOL SOCIOBIOL

A well-established field of research in vertebrates focuses on the variability of cognitive abilities within species. From mammals to fish, numerous studies have revealed remarkable differences in the cognitive phenotype among individuals, particularly in terms of sex or personality. However, many aspects of the mechanisms, genetics, and selective pressures that underlie individual cognitive variation remain unclear. Surprisingly, intraspecific variability in cognition has received much less attention in invertebrates, despite the increasing evidence of remarkable cognitive abilities in this group and the insights that could be gained from examining simultaneously two distinct taxa, namely vertebrates and invertebrates. In this review, we provide evidence that certain invertebrate species exhibit all the key features of cognitive variation observed in vertebrates, including differences related to sex and personality. In many cases, invertebrate studies have provided insights into the genetic basis, evolvability and response to selection of cognitive variability. Moreover, we highlight evidence for caste differences in eusocial insects, which are linked to task specialisation within the colony. This makes insect eusociality a valuable system for understanding how selection influences cognitive variation. We propose that cognitive variation in invertebrates may be more widespread than currently thought, and that selection may operate in a similar manner on two distantly related cognitive systems (vertebrates and invertebrates). Finally, we suggest that invertebrates hold the potential to serve both as alternative and complementary models to vertebrates, contributing to a deeper understanding of cognitive evolution.

Using pupae as appetitive reinforcement to study visual and tactile associative learning in the Ponerine ant Diacamma indicum

Article

Full-text available

Sep 2023

Associative learning is of great importance to animals, as it enhances their ability to navigate, forage, evade predation and improve fitness. Even though associative learning abilities of Hymenopterans have been explored, many of these studies offered food as appetitive reinforcement. In the current study, we focus on tactile and visual cue learning in an ant Diacamma indicum using a Y-maze setup with pupa as a positive reinforcement. Using pupa as a reward resulted in a significantly higher proportion of ants completing the training in a shorter time as compared to using food as reinforcement. Ants spent significantly more time in the conditioned arm for both visual cues (white dots or black dots) and tactile cues (rough or smooth surfaces) presented on the floor when associated with pupa, thus showing that they were capable of associative learning. On encountering a conflict between visual and tactile cues during the test, ants chose to spend significantly more time on the arm with the tactile cues indicating that they had made a stronger association between pupa and the tactile cue as compared to the visual cue during training. Using pupa as an ecologically relevant reward, we show that these solitary foraging ants living in small colonies are capable of visual and tactile associative learning and are likely to learn tactile cues over visual cues in association with pupa.

Changes in resource perception throughout the foraging visit contribute to task specialization in the honey bee Apis mellifera

Article

Full-text available

May 2023

Division of labor is central to the ecological success of social insects. Among foragers of the honey bee, specialization for collecting nectar or pollen correlates with their sensitivity to sucrose. So far, differences in gustatory perception have been mostly studied in bees returning to the hive, but not during foraging. Here, we showed that the phase of the foraging visit (i.e. beginning or end) interacts with foraging specialization (i.e. predisposition to collect pollen or nectar) to modulate sucrose and pollen sensitivity in foragers. In concordance with previous studies, pollen foragers presented higher sucrose responsiveness than nectar foragers at the end of the foraging visit. On the contrary, pollen foragers were less responsive than nectar foragers at the beginning of the visit. Consistently, free-flying foragers accepted less concentrated sucrose solution during pollen gathering than immediately after entering the hive. Pollen perception also changes throughout foraging, as pollen foragers captured at the beginning of the visit learned and retained memories better when they were conditioned with pollen + sucrose as reward than when we used sucrose alone. Altogether, our results support the idea that changes in foragers' perception throughout the foraging visit contributes to task specialization.

Sex and Lifestyle Dictate Learning Performance in a Neotropical Wasp

Article

Full-text available

Mar 2023

In contrast to extensive investigations on bee cognition, the cognitive capacities of wasps remain largely unexplored despite their key role as pollinators and predators of insect pests. Here we studied learning and memory in the neotropical wasp Mischocyttarus cerberus using a Pavlovian conditioning in which harnessed wasps respond with conditioned movements of their mouthparts to a learned odorant. We focused on the different castes, sexes and ages coexisting within a nest and found that adults of M. cerberus learned and memorized efficiently the odor-sugar associations. In contrast, newly emerged females, but not males, were unable to learn odorants. This difference concurs with their different lifestyle as young males perform regular excursions outside the nest while young females remain in it until older age. Our results thus highlight the importance of socio-ecological constraints on wasp cognition and set the basis for mechanistic studies on learning differences across ages and castes.

Differences in Olfactory Sensitivity and Odor Detection Correlate with Foraging Task Specialization in Honeybees Apis Mellifera

Article

Jan 2022

Part I - Evolution of Learning Processes

Book

May 2022

Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.

Nectar feeding by the ant Camponotus mus: Intake rate and crop filling as a function of sucrose concentration

Article

Full-text available

Jan 1998

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.

Cognition with few neurons: Higher-order learning in insects

Article

Full-text available

Jan 2013

Martin Giurfa

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.

Quantitative Study of the Fixed Response Threshold Model for the Regulation of Division of Labour in Insect Societies

Article

Full-text available

Dec 1996

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 support@jstor.org. 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).

Trail-Laying Behaviour as a Function of Resource Quality in the Ant Camponotus rufipes

Article

Full-text available

Jan 2011
Psyche

P. E. Schilman

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.

Effects of patriline on gustatory responsiveness and olfactory learning in honey bees

Article

Full-text available

Jan 2010

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.

The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.)

Article

Aug 1999

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.

The ants

Book

Jan 1990

The Insect Societies

Book

Jan 1971

Wilson Edward O.

The Insect Societies

Book

Jan 1971

Edward O. Wilson

Variation in water and sucrose responsiveness during the foraging season affects proboscis extension learning in honey bees

Article

Jan 2003

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.