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Decision-making processes face the dilemma of being accurate or faster, a phenomenon that has been described as speed-accuracy trade-off in numerous studies on animal behaviour. In social insects, discriminating between colony members and aliens is subject to this trade-off as rapid and accurate rejection of enemies is of primary importance for the maintenance and ecological success of insect societies. Recognition cues distinguishing aliens from nestmates are embedded in the cuticular hydrocarbon (CHC) layer and vary among colonies. In walking carpenter ants, exposure to formic acid (FA), an alarm pheromone, improves the accuracy of nestmate recognition by decreasing both alien acceptance and nestmate rejection. Here, we studied the effect of FA exposure on the spontaneous aggressive mandible opening response (MOR) of harnessed Camponotus aethiops ants presented with either nestmate or alien CHCs. FA modulated both MOR accuracy and the latency to respond to odours of conspecifics. In particular, FA decreased the MOR towards nestmates but increased it towards aliens. Furthermore, FA decreased MOR latency towards aliens but not towards nestmates. As response latency can be used as a proxy of response speed, we conclude that contrary to the prediction of the speed-accuracy trade-off theory, ants did not trade off speed against accuracy in the process of nestmate recognition., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

Biogenic amines play an important role in the regulation of appetitive responses in insects. Among them, serotonin (5-HT) regulates feeding-related processes in numerous insect species. In carpenter ants, 5-HT administration has been shown to depress feeding behavior, thus opening the possibility of using 5-HT modulation in control strategies against those species considered as pest. Here we studied if administration of a 5-HT antagonist, ketanserin, promotes feeding of a sucrose solution and a toxic bait in carpenter ants Camponotus mus. We found that 3 h after a single oral administration of ketanserin, the mass of sucrose solution consumed by carpenter ants increased significantly. A similar effect was found after a chronic administration that lasted 5 days. Yet, ketanserin did neither affect the intake rates nor the activity of the pharyngeal pump that mediates feeding dynamics. In addition, ketanserin promoted the consumption of a toxic bait based on boric acid. Our results thus show that feeding motivation and consumption of both sucrose solution and a toxic bait can be enhanced via prior administration of ketanserin. We discuss the possible mechanisms underlying these effects and conclude that understanding basic physiological and neural principles that underlie feeding motivation allows establishing more efficient control strategies for pest insects., (© 2021. The Author(s).)

The Argentine ant, Linepithema humile , is native to 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 such signals to develop a strategy for chemical control. Here, we studied the effects 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 as 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 ants' subjective evaluation of a food reward. However, although ants learned to associate an odor with a sucrose reward, pheromone pre-exposure affected neither 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., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2020. Published by The Company of Biologists Ltd.)

The ecological and evolutionary success of social insects relies on their ability to efficiently discriminate between group members and aliens. Nestmate recognition occurs by phenotype matching, the comparison of the referent (colony) phenotype to the one of an encountered individual. Based on the level of dissimilarity between the two, the discriminator accepts or rejects the target. The tolerated degree of mismatch is predicted by the acceptance threshold model, which assumes adaptive threshold shifts depending on the costs of discrimination errors. Inherent in the model is that rejection (type I) and acceptance (type II) errors are reciprocally related: if one type decreases, the other increases. We studied whether alarm pheromones modulate the acceptance threshold. We exposed Camponotus aethiops ants to formic acid and subsequently measured aggression toward nestmates and nonnestmates. Formic acid induced both more nonnestmate rejection and more nestmate acceptance than a control treatment, thus uncovering an unexpected effect of an alarm pheromone on responses to nestmates. Nestmate discrimination accuracy was improved via a decrease in both types of errors, a result that cannot be explained by a shift in the acceptance threshold. We propose that formic acid increases the amount of information available to the ants, thus decreasing the perceived phenotypic overlap between nestmate and nonnestmate recognition cues. This mechanism for improved discrimination reveals a novel function of alarm pheromones in recognition processes and may have far-reaching implications in our understanding of the modus operandi of recognition systems in general.

Ants have recently emerged as useful models for the study of olfactory learning. In this framework, the development of a protocol for the appetitive conditioning of the maxilla-labium extension response (MaLER) provided the possibility of studying Pavlovian odor-food learning in a controlled environment. Here we extend these studies by introducing the first Pavlovian aversive learning protocol for harnessed ants in the laboratory. We worked with carpenter ants Camponotus aethiops and first determined the capacity of different temperatures applied to the body surface to elicit the typical aversive mandible opening response (MOR). We determined that 75°C is the optimal temperature to induce MOR and chose the hind legs as the stimulated body region because of their high sensitivity. We then studied the ability of ants to learn and remember odor-heat associations using 75°C as the unconditioned stimulus. We studied learning and short-term retention after absolute (one odor paired with heat) and differential conditioning (a punished odor versus an unpunished odor). Our results show that ants successfully learn the odor-heat association under a differential-conditioning regime and thus exhibit a conditioned MOR to the punished odor. Yet, their performance under an absolute-conditioning regime is poor. These results demonstrate that ants are capable of aversive learning and confirm previous findings about the different attentional resources solicited by differential and absolute conditioning in general., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2017. Published by The Company of Biologists Ltd.)

Perceptual similarity between stimuli is often assessed via generalization, the response to stimuli that are similar to the one which was previously conditioned. Although conditioning procedures are variable, studies on how this variation may affect perceptual similarity remain scarce. Here, we use a combination of behavioural and computational analyses to investigate the influence of olfactory conditioning procedures on odour generalization in ants. Insects were trained following either absolute conditioning, in which a single odour (an aldehyde) was rewarded with sucrose, or differential conditioning, in which one odour (the same aldehyde) was similarly rewarded and another odour (an aldehyde differing in carbon-chain length) was punished with quinine. The response to the trained odours and generalization to other aldehydes were assessed. We show that olfactory similarity, rather than being immutable, varies with the conditioning procedure. Compared with absolute conditioning, differential conditioning enhances olfactory discrimination. This improvement is best described by a multiplicative interaction between two independent processes, the excitatory and inhibitory generalization gradients induced by the rewarded and the punished odour, respectively. We show that olfactory similarity is dramatically shaped by an individual's perceptual experience and suggest a new hypothesis for the nature of stimulus interactions underlying experience-dependent changes in perceptual similarity., (© 2016 The Authors.)

Natural odours are complex blends of numerous components. Understanding how animals perceive odour mixtures is central to multiple disciplines. Here we focused on carpenter ants, which rely on odours in various behavioural contexts. We studied overshadowing, a phenomenon that occurs when animals having learnt a binary mixture respond less to one component than to the other, and less than when this component was learnt alone. Ants were trained individually with alcohols and aldehydes varying in carbon-chain length, either as single odours or binary mixtures. They were then tested with the mixture and the components. Overshadowing resulted from the interaction between chain length and functional group: alcohols overshadowed aldehydes, and longer chain lengths overshadowed shorter ones; yet, combinations of these factors could cancel each other and suppress overshadowing. Our results show how ants treat binary olfactory mixtures and set the basis for predictive analyses of odour perception in insects.

The ability of animals to adjust their behaviour according to seasonal changes in their ecology is crucial for their fitness. Eusocial insects display strong collective behavioural seasonality, yet the mechanisms underlying such changes are poorly understood. We show that nest preference by emigrating Temnothorax albipennis ant colonies is influenced by a season-specific modulatory pheromone that may help tune decision-making according to seasonal constraints. The modulatory pheromone triggers aversion towards low-quality nests and enhances colony cohesion in summer and autumn, but not after overwintering-in agreement with reports that field colonies split in spring and reunite in summer. Interestingly, we show that the pheromone acts by downgrading the perceived value of marked nests by informed and naive individuals. This contrasts with theories of collective intelligence, stating that accurate collective decision-making requires independent evaluation of options by individuals. The violation of independence highlighted here was accordingly shown to increase error rate during emigrations. However, this is counterbalanced by enhanced cohesion and the transmission of valuable information through the colony. Our results support recent claims that optimal decisions are not necessarily those that maximize accuracy. Other criteria-such as cohesion or reward rate-may be more relevant in animal decision-making.

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.

Ants exhibit impressive olfactory learning abilities. Operant protocols in which ants freely choose between rewarded and non-rewarded odours have been used to characterise associative olfactory learning and memory. Yet, this approach precludes the use of invasive methods allowing the dissection of molecular bases of learning and memory. An open question is whether the memories formed upon olfactory learning that are retrievable several days after training are indeed based on de novo protein synthesis. Here, we addressed this question in the ant Camponotus fellah using a conditioning protocol in which individually harnessed ants learn an association between odour and reward. When the antennae of an ant are stimulated with sucrose solution, the insect extends its maxilla-labium to absorb the solution (maxilla-labium extension response). We differentially conditioned ants to discriminate between two long-chain hydrocarbons, one paired with sucrose and the other with quinine solution. Differential conditioning leads to the formation of a long-term memory retrievable at least 72 h after training. Long-term memory consolidation was impaired by the ingestion of cycloheximide, a protein synthesis blocker, prior to conditioning. Cycloheximide did not impair acquisition of either short-term memory (10 min) or early and late mid-term memories (1 or 12 h). These results show that, upon olfactory learning, ants form different memories with variable molecular bases. While short- and mid-term memories do not require protein synthesis, long-term memories are stabilised via protein synthesis. Our behavioural protocol opens interesting research avenues to explore the cellular and molecular bases of olfactory learning and memory in ants.

Self-organisation underlies many collective processes in large animal groups, where coordinated patterns and activities emerge at the group level from local interactions among its members. Although the importance of key individuals acting as effective leaders has recently been recognised in certain collective processes, it is widely believed that self-organised decisions are evenly shared among all or a subset of individuals acting as decision-makers, unless there are significant conflicts of interests among group members. Here, we show that certain individuals are disproportionately influential in self-organised decisions in a system where all individuals share the same interests: nest site selection by the ant Temnothorax albipennis. Workers that visited a good available nest site prior to emigration (the familiar nest) memorised its location, and later used this memory to navigate efficiently and find that nest faster than through random exploration. Additionally, these workers relied on their private information to expedite individual decisions about the familiar nest. This conferred a bias in favour of familiar nests over novel nests during emigrations. Informed workers were shown to have a significantly greater share in both recruitment and transport to the familiar nest than naïve workers. This suggests that they were the main determinants of the collective preference for familiar nests, and thus contributed greatly to enhance collective performance. Overall, these results indicate that self-organised decisions are not always evenly shared among decision-makers, even in systems where there are no conflicts of interest. Animal groups may instead benefit from well-informed, knowledgeable individuals acting as leaders in decisions.

Background: Successful collective decision-making depends on groups of animals being able to make accurate choices while maintaining group cohesion. However, increasing accuracy and/or cohesion usually decreases decision speed and vice-versa. Such trade-offs are widespread in animal decision-making and result in various decision-making strategies that emphasize either speed or accuracy, depending on the context. Speed-accuracy trade-offs have been the object of many theoretical investigations, but these studies did not consider the possible effects of previous experience and/or knowledge of individuals on such trade-offs. In this study, we investigated how previous knowledge of their environment may affect emigration speed, nest choice and colony cohesion in emigrations of the house-hunting ant Temnothorax albipennis, a collective decision-making process subject to a classical speed-accuracy trade-off., Methodology/principal Findings: Colonies allowed to explore a high quality nest site for one week before they were forced to emigrate found that nest and accepted it faster than emigrating naïve colonies. This resulted in increased speed in single choice emigrations and higher colony cohesion in binary choice emigrations. Additionally, colonies allowed to explore both high and low quality nest sites for one week prior to emigration remained more cohesive, made more accurate decisions and emigrated faster than emigrating naïve colonies., Conclusions/significance: These results show that colonies gather and store information about available nest sites while their nest is still intact, and later retrieve and use this information when they need to emigrate. This improves colony performance. Early gathering of information for later use is therefore an effective strategy allowing T. albipennis colonies to improve simultaneously all aspects of the decision-making process--i.e. speed, accuracy and cohesion--and partly circumvent the speed-accuracy trade-off classically observed during emigrations. These findings should be taken into account in future studies on speed-accuracy trade-offs.

Background: Olfactory systems create representations of the chemical world in the animal brain. Recordings of odour-evoked activity in the primary olfactory centres of vertebrates and insects have suggested similar rules for odour processing, in particular through spatial organization of chemical information in their functional units, the glomeruli. Similarity between odour representations can be extracted from across-glomerulus patterns in a wide range of species, from insects to vertebrates, but comparison of odour similarity in such diverse taxa has not been addressed. In the present study, we asked how 11 aliphatic odorants previously tested in honeybees and rats are represented in the antennal lobe of the ant Camponotus fellah, a social insect that relies on olfaction for food search and social communication., Results: Using calcium imaging of specifically-stained second-order neurons, we show that these odours induce specific activity patterns in the ant antennal lobe. Using multidimensional analysis, we show that clustering of odours is similar in ants, bees and rats. Moreover, odour similarity is highly correlated in all three species., Conclusion: This suggests the existence of similar coding rules in the neural olfactory spaces of species among which evolutionary divergence happened hundreds of million years ago.

Individual Camponotus fellah ants perceive and learn odours in a Y-maze in which one odour is paired with sugar (CS+) while a different odour (CS-) is paired with quinine (differential conditioning). We studied olfactory retention in C. fellah to determine whether olfactory learning leads to long-term memory retrievable 24 h and 72 h after training. One and 3 days after training, ants exhibited robust olfactory memory through a series of five successive retention tests in which they preferred the CS+ and stayed longer in the arm presenting it. In order to determine the nature of the associations memorized, we asked whether choices within the Y-maze were driven by excitatory memory based on choosing the CS+ and/or inhibitory memory based on avoiding the CS-. By confronting ants with a novel odour vs either the CS+ or the CS- we found that learning led to the formation of excitatory memory driving the choice of the CS+ but no inhibitory memory based on the CS- was apparent. Ants even preferred the CS- to the novel odour, thus suggesting that they used the CS- as a contextual cue in which the CS+ was embedded, or as a second-order cue predicting the CS+ and thus the sugar reward. Our results constitute the first controlled account of olfactory long-term memory in individual ants for which the nature of associations could be precisely characterized.