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Social isolation in ants: Evidence of its impact on survivorship and behavior in Camponotus fellah (Hymenoptera, Formicidae).
Abstract
We investigated the effect of social isolation on survivorship, body weight, and readiness to engage in allogrooming and trophallaxis in the ant Camponotus fellah. Life duration of the workers caged singly with access to food was significantly lower than if they were caged with another nestmate, which implies that the stressful effects of social isolation cannot be reduced to the effects of food deprivation, Three day social isolation and food deprivation led to about 15% weight loss in the ants caged singly, but did not result in significant weight loss in the ants caged by tens. Social isolation also led to significant increase in the readiness to engage in trophallaxis. In the ants isolated with access to food, increased rate of trophallaxis between dyads of workers reunited after the period of social isolation (24 - 480 hours) might have been triggered by possible divergence of their cuticular profiles acting as colony recognition cues: trophallactic exchanges are known to play a crucial role in the exchange of recognition labels among the members of ant colonies.
... Experiments on ants are done at the colony level (Cook et al. 2010;Greenwald et al. 2018;Lesne et al. 2022), on colony fragments or even at the individual level. For example, several studies have investigated small groups of workers, with or without brood, or isolated individuals to test the effect of limited social interactions on behavior, development, gene expression, and lifespan (Boulay et al. 1999;Koto et al. 2015;Scharf et al. 2021). Isolation of individuals has also been used for testing treatment effects on workers' survival (Arganda et al. 2017) and disease resistance (Hughes et al. 2002;Konrad et al. 2012). ...
... Humidity and water access are also a matter of concern. Ants usually have ad libitum access to water by moistened pieces of cotton, sponge, or plaster, or even drops of water directly deposited on the ground (Chang 1985;Boulay et al. 1999;Arganda et al. 2017). Nevertheless, water may dry out quickly, which necessitates daily inspection. ...
... As expected, both species survived significantly longer in the feeding treatment followed by the starvation and the desiccation treatments (Bonferroni corrected post-hoc pairwise comparisons, for both species: all comparisons: P < 0.001 except for F/NSU versus F/SSU, and S/NSU versus S/SSU). Similar results were observed in the ant species Camponotus fellah, where workers survived longer when they had access to food than under starvation (Boulay et al. 1999;Koto et al. 2015). The social environment also influenced workers' survival: isolated individuals died faster than workers kept in groups (Boulay et al. 1999;Koto et al. 2015). ...
Laboratory studies on insects face the dual challenge of maintaining organisms under artificial conditions, and in reduced spaces while mimicking the species’ ecological requirements as much as possible. Over decades, myrmecologists have developed and continuously improved laboratory methods and artificial nests for rearing ants. However, the setups commonly used to house colony fragments of few individuals or even isolated individuals present disadvantages such as insufficient ventilation, difficult access to specific workers, and problems with water delivery. Here, we developed and tested a new setup for keeping ants or similar sized insects in small groups. The setup consisted of a Petri dish containing a piece of plaster connected underneath to a water tank by a sponge. The sponge is immersed in the water on one side and embedded in the plaster on the other side, maintaining the plaster permanently moist and thus offering a water source to the ants. We tested the setup with two ant species of different sizes, Platythyrea punctata and Cardiocondyla obscurior in feeding, starvation, and desiccation conditions. Our results showed that our new setup worked equally well for both species in all conditions in comparison to a more conventional setup with the advantage of reducing maintenance costs and ant manipulation, but also preventing death by drowning and offering water ad libitum . The setup was quick to build, with cheap and reusable materials for further experiments. Therefore, we are confident that it will facilitate future studies on isolated or small groups of individuals and that such a standardized setup will make future studies more comparable.
... The social environment has also been well documented to reduce immune function and alter digestive processes through mating, which is the most common process being social interaction (McKean and Nunney, 2001;Rolff and Siva-Jothy, 2002;White et al., 2021). Social interaction, one of the most important biotic factors, is now well known for its tremendous influence on many aspects of animals' fitness (Boulay et al., 1999;Koto et al., 2015). ...
The social-sexual environment is well known for its influence on the survival of organisms by modulating their reproductive output. However, whether it affects survival indirectly through a variety of cues without physical contact and its influence relative to direct interaction remain largely unknown. In this study, we investigated both the indirect and direct influences of the social-sexual environment on the survival and reproduction of the mite Tyrophagus curvipenis (Acari: Acaridae). The results demonstrated no apparent influence of conspecific cues on the survival of mites, but the survival and reproduction of mated female mites significantly changed, with the females mated with males having a significantly shortened lifespan and increased lifetime fecundity. For males, no significant difference was observed across treatments in their survival and lifespan. These findings indicate that direct interaction with the opposite sex has a much more profound influence on mites than indirect interaction and highlight the urgent need to expand research on how conspecific cues modulate the performance of organisms with more species to clarify their impacts across taxa.
... One way to measure whether and how individuals respond to changes in their social environment is to examine discrete shifts in phenotype that accompany those changes. In ants, for example, such changes occur after the removal of the queen in the form of increased reproduction and lifespan of workers (Almond et al., 2019;Choppin et al., 2021;Heinze et al., 1997;Kohlmeier et al., 2017;Majoe et al., 2021;Negroni et al., 2021) and, in isolated ants, in the form of altered behaviour (Boulay, 1999;Scharf et al., 2021;Seid & Junge, 2016). Over the past decade, with advances in omics technologies, studies were able to not only investigate the molecular basis of discrete phenotypes but also to discover even subtle changes on the molecular level, even with no apparent phenotypic changes. ...
Insect social parasites are characterized by exploiting the hosts' social behaviour. Why exactly hosts direct their caring behaviour towards these parasites and their offspring remains largely unstudied. One hypothesis is that hosts do not perceive their social environment as altered and accept the parasitic colony as their own. We used the ant Leptothorax acervorum, host of the dulotic, obligate social parasite Harpagoxenus sublaevis, to shed light on molecular mechanisms underlying behavioural exploitation by contrasting tissue-specific transcriptomes in young host workers. Host pupae were experimentally (re-)introduced into fragments of their original, another conspecific, heterospecific or parasitic colony. Brain and antennal mRNA was extracted and sequenced from adult ants after they had lived in the experimental colony for at least 50 days after eclosion. The resulting transcriptomes of L. acervorum revealed that ants were indeed affected by their social environment. Host brain transcriptomes were altered by the presence of social parasites, suggesting that the parasitic environment influences brain activity, which may be linked to behavioural changes. Transcriptional activity in the antennae changed most with the presence of unrelated individuals, regardless of whether they were conspecifics or parasites. This suggests early priming of odour perception, which was further supported by sensory perception of odour as an enriched function of differentially expressed genes. Furthermore, gene expression in the antennae, but not in the brain corresponded to ant worker behaviour before sampling. Our study demonstrated that the exploitation of social behaviours by brood parasites correlates with transcriptomic alterations in the central and peripheral nervous systems.
... Each desiccation chamber held five nestmate workers, such that we had two treatment chambers per colony to hold 10 workers. We chose to maintain workers in groups to mitigate the confounding negative effects of social isolation on ant survival and energy consumption (Boulay et al. 1999;Koto et al. 2015).To control for other possible causes of death over the experimental period, we additionally established a high-humidity control in the same design as our desiccation chambers, but replacing Drierite with water. We used Hygrochron humiditylogging iButtons® (DS1923, Maxim Integrated, San Jose, CA, USA) to confirm that desiccation chambers consistently provided 0% relative humidity conditions. ...
As small-bodied terrestrial organisms, insects face severe desiccation risks in arid environments, and these risks are increasing under climate change. Here, we investigate the physiological, chemical, and behavioral mechanisms by which harvester ants, one of the most abundant arid-adapted insect groups, cope with desiccating environmental conditions. We aimed to understand how body size, cuticular hydrocarbon profiles, and queen number impact worker desiccation resistance in the facultatively polygynous harvester ant, Pogonomyrmex californicus. We measured survival at 0% humidity of field-collected worker ants sourced from three closely situated populations within a semi-arid region of southern California. These populations vary in queen number, with one population dominated by multi-queen colonies (primary polygyny), one population dominated by single-queen colonies, and one containing an even mix of single- and multi-queen colonies. We found no effect of population on worker survival in desiccation assays, suggesting that queen number does not influence colony desiccation resistance. Across populations, however, body mass and cuticular hydrocarbon profiles significantly predicted desiccation resistance. Larger-bodied workers survived longer in desiccation assays, emphasizing the importance of reduced surface area-to-volume ratios in maintaining water balance. Additionally, we observed a positive relationship between desiccation resistance and the abundance of n-alkanes, supporting previous work that has linked these high-melting point compounds to improved body water conservation. Together, these results contribute to an emerging model explaining the physiological mechanisms of desiccation resistance in insects.
... Wheeler (1926) avançait déjà l'idée que les animaux sociaux possèdent un besoin social au même titre que les besoins alimentaires ou sexuels. Ce besoin est démontré chez les insectes par les modifications du comportement et de la physiologie suite à l'isolation sociale (Sitbon 1967;Arnold 1978;Boulay et al. 1999;Boulay & Lenoir 2001;Koto et al. 2015;Seid & Junge 2016). La mise en place de cette valeur appétitive devra être déterminée dans les travaux futurs. ...
Les interactions entre individus sont un socle vital pour l’organisation des colonies d’abeilles, en particulier lors du recrutement pour le butinage. Outre la communication de la localisation d’une source de nourriture par la fameuse danse, les abeilles recrutées apprennent les caractéristiques de l’odeur des fleurs butinées au cours de transferts de nectar (trophallaxie). Les mécanismes de cet apprentissage ne sont pas encore éclaircis car il est parfois effectif sans aucun transfert de nectar, suggérant que d’autres mécanismes, comme par exemple d’apprentissage social, sont impliqués. Nous avons reproduit cette interaction en laboratoire, suivant un protocole basé sur le conditionnement olfactif appétitif de la réponse d’extension du proboscis (REP). Ici, un composé odorant initialement neutre (Stimulus conditionnel) était associé à un contact avec une congénère (Stimulus Inconditionnel social), sans récompense sucrée. Nos expériences montrent que ce simple contact social entre congénères peut constituer un renforcement pour les abeilles. A la suite de cette association, celles-ci montrent donc des REP à l’odeur préalablement associée au contact social. Nos expériences montrent de plus que des contacts antennaires entre les abeilles sont indispensables à l’efficacité de cet apprentissage social, représentant un indice social tactile. Nous avons alors développé un dispositif permettant d’enregistrer les mouvements des antennes de manière précise et à haute vitesse (90 hz) et étudié les différents facteurs modulant les mouvements antennaires des abeilles. Les abeilles montrent des réponses contrastées et reproductibles à des odeurs de valeurs biologiques différentes. De plus, le couplage de ces enregistrements à des expériences de conditionnement associatif montre que ces réponses antennaires sont plastiques et modifiées par l’expérience des individus. Ce travail a permis de mettre en lumière un nouveau type d’apprentissage social chez les insectes et d’approfondir l’étude des mouvements antennaires comme indicateurs de l’état motivationnel, attentionnel et physiologique des abeilles ainsi que de la valence des stimuli perçus.
... Camponotus fellah has evolved a polymorphic worker caste with subcastes of minor and major workers (Boulay et al., 1999;Laciny et al., 2019) and a spectrum of transitions, often called media workers (medias) (Boulay et al., 2000;Lenoir et al., 2001). The worker subcastes differ significantly in their morphometry (Laciny et al., 2019), showing considerable distinction in mesosoma and head shapes (Fig. 1). ...
Worker polymorphism in ants has evolved repeatedly, with considerable differences in the morphometry of worker subcastes. Such body size differences and especially caste- and subcaste-specific characteristics might significantly influence locomotion. Therefore, we performed a comprehensive locomotion analysis along gradients in both body size and walking speed of Camponotus fellah worker subcastes, and of males, which have rarely been studied to date due to short life spans associated with mating flights. We provide a detailed description of the morphometry and size differences of C. fellah castes and subcastes and analyse locomotion in the different polymorphic groups in terms of absolute and relative walking speeds (mesosoma lengths per second). Our results reveal that body size and shape affect locomotion behaviour to different extents in the worker subcastes (minor workers, medias, major workers) and in males. Nevertheless, C. fellah ants use the same overall locomotion strategy, with males and major workers reaching considerably lower walking speeds than minors and medias. Body size thus mainly affects walking speed. Minor workers reach the highest relative velocities by high relative stride lengths in combination with large vertical and lateral COM oscillations and clearly higher stride frequencies of up to 25 Hz. Locomotion of males was characterised by clearly lower walking speeds, wider footprint positions, significant phase shifts and a notable dragging of the shorter hind legs. However, general walking parameters of males differed less from those of the female workers than expected due to division of labour in the colony.
Social isolation negatively affects health, induces detrimental behaviors, and shortens lifespan in social species. Little is known about the mechanisms underpinning these effects because model species are typically short-lived and non-social. Using colonies of the carpenter ant Camponotus fellah, we show that social isolation induces hyperactivity, alters space-use, and reduces lifespan via changes in the expression of genes with key roles in oxidation-reduction and an associated accumulation of reactive oxygen species. These physiological effects are localized to the fat body and oenocytes, which perform liver-like functions in insects. We use pharmacological manipulations to demonstrate that the oxidation-reduction pathway causally underpins the detrimental effects of social isolation on behavior and lifespan. These findings have important implications for our understanding of how social isolation affects behavior and lifespan in general.
Social isolation, particularly in early life, leads to deleterious physiological and behavioral outcomes. Here, we leverage new high-throughput tools to comprehensively investigate the impact of isolation in the bumblebee, Bombus impatiens, from behavioral, molecular, and neuroanatomical perspectives. We reared newly emerged bumblebees in complete isolation, in small groups, or in their natal colony, and then analyzed their behaviors while alone or paired with another bee. We find that when alone, individuals of each rearing condition show distinct behavioral signatures. When paired with a conspecific, bees reared in small groups or in the natal colony express similar behavioral profiles. Isolated bees, however, showed increased social interactions. To identify the neurobiological correlates of these differences, we quantified brain gene expression and measured the volumes of key brain regions for a subset of individuals from each rearing condition. Overall, we find that isolation increases social interactions and disrupts gene expression and brain development. Limited social experience in small groups is sufficient to preserve typical patterns of brain development and social behavior.
Social isolation, particularly in early life, leads to deleterious physiological and behavioral outcomes. Few studies, if any, have been able to capture the behavioral and neurogenomic consequences of early life social isolation together in a single social animal system. Here, we leverage new high-throughput tools to comprehensively investigate the impact of isolation in the bumblebee (Bombus impatiens) from behavioral, molecular, and neuroanatomical perspectives. We reared newly emerged bumblebees either in complete isolation, small groups, or in their natal colony, and then analyzed their behaviors while alone or paired with another bee. We find that when alone, individuals of each rearing condition show distinct behavioral signatures. When paired with a conspecific, bees reared in small groups or in the natal colony express similar behavioral profiles. Isolated bees, however, showed increased social interactions. To identify the neurobiological correlates of these differences, we quantified brain gene expression and measured the volumes of key brain regions for a subset of individuals from each rearing condition. Overall, we find that isolation increases social interactions and disrupts gene expression and brain development. Limited social experience in small groups is sufficient to preserve typical patterns of brain development and social behavior.
Heritable cuticular hydrocarbon patterns ofSolenopsis invicta workers are consistent within colonies for a given sampling time but vary sufficiently from colony to colony to distinguish the colonies from each other. In addition, cuticular hydrocarbon patterns change within colonies over time. Nestmate recognition cues found on the individual's cuticle, can be from heritable or environmental sources, and are a subset of colony odor. The cuticular hydrocarbons can be used as a model for heritable nestmate recognition cues. We propose that because potential nestmate recognition cues, both environmental and genetic, are dynamic in nature rather than static, during its lifetime a worker must continually update its perception (template) of colony odor and nestmate recognition cues.
Activity levels within ant colonies are monitored by using a solid-state automatically digitizing camera. The movement-activity levels of whole colonies and of isolated groups of workers are studied. Whole colonies of Leptothorax allardycei show rhythmic changes in movement-activity level. Fourier and autocorrelation analyses indicate that the activity levels of colonies are periodic, with an average period of 26 min. Single, isolated workers do not show the pattern of periodic changes in activity level. Single workers become active spontaneously, but at no particular interval. Pairs of workers, confined together, also do not show periodicity in activity level. One worker can stimulate another worker to become active, thus coupling their movement-activity patterns. As ants are placed in larger groups, the variation in the interval between activity peaks declines in a manner predicted by coupled-oscillator theory. It is argued that the colony can be regarded as a population of excitable subunits, and it is shown that the results of this paper can be explained in this light. The formal similarity between movement-activity patterns in ant colonies and the dynamics of epidemics is noted. It is further argued that periodicity in the movement-activity levels of the colony is probably an epiphenomenon rather than an adaptation. Selection at the colonial level probably acts on the spontaneity of activity and coupling strength to produce changes in the overall activity level of the colony. One of the patterns that can result is periodicity in the colony's activity level, but it is not the only possible outcome.
Detailed observation of 60 individually labelled young workers of the ponerine ant Ectatomma tuberculatum during the first 45 days after emergence indicated that behavioural specializations appear progressively according to an individual's age. A comparison of control ants and isolated young workers, deprived of early social contact for a fixed interval at different post-emergence ages, revealed the existence of a sensitive period during which social stimuli affect the establishment of behaviour related to brood care. This sensitive period may involve two phases: a ‘permissive’ period, during the first 2 days of social contact, and a ‘stabilization’ period, during the subsequent 2 days.
Food exchange occurred as an appeasement response in distant ant colonies ofSolenopsis invicta, S. geminata, andPheidole dentata. More regurgitated radioactive fluid was given to major workers than to minors by the donors from the alien colonies of these species.
(1) Resting workers emitted 0.50+-0.024 mu l carbon dioxide/mg/h at 19 degrees C, whether alone or in groups of ten; single queens emitted 0.40+-0.017 mu l of carbon dioxide/mg/h, significantly less. (2) Groups of workers with or without queens or larvae were cultured at 20 degrees C and 98% R.H. and their use of prey, water and sugar measured. Prey residues were collected and an estimate of ingestion made; production was measured as larval growth, eggs laid and storage in adults. (3) Both active spring larvae and queens increased the flies eaten, the water drunk and the sugar consumed. Queens made all larvae grow faster (except the big, queen-generating ones). (4) With sugar available fewer flies were eaten (except when no larvae or queens were present); dilute sugar reduced the amount of water taken independently. Strong solutions (40%) were deleterious and were avoided but moderate solutions (10 and 20%) were attractive and could compensate for the absence of queens. Frequently no more sugar was taken than the workers alone needed for their basal metabolism. (5) Queen influence was complex because of their caste-control function which suppresses the growth of big spring larvae, encourages that of small ones, and reduces the incidence of diapause in summer larvae. They reduced the supply of prey to big spring larvae without reducing their water consumption. (6) Overabundant prey (without sugar) reduced the water drunk, the degree of extraction of prey and larval growth. The feeding drive of workers was thus affected, not only by queens, larval type and dilute sugar solutions but by prey availability. (7) The ratio production/ingestion was virtually constant in one experiment with spring larvae at a value 0.49+-0.01 but varied more with summer larvae (due to a diapause tendency). Sugar supplied in increasing quantity reduced the ratio progressively but improved the assimilation of protein. Queens had no effect except where the incidence of diapause in summer larvae was involved.
The objective of the present study was to evaluate the interrelationship between the cuticular and postpharyngeal glands' hydrocarbons, both in the individual ant and during its interaction with nestmates. In vivo radiochemical assays were employed to monitor the de novo hydrocarbon biosynthesis from acetate in the ant's body. The newly synthesized hydrocarbons appeared first internally and after 24 hr they accumulated in the postpharyngeal gland and on the cuticular surface. Blocking the possibility of external transfer of hydrocarbons between cuticle and postpharyngeal gland led to a significant decrease of labeled hydrocarbons in the postpharyngeal gland. In addition, during encounters between labeled and unlabeled ants, newly synthesized hydrocarbons were transferred, mainly via trophallaxis, but also by allo-grooming and physical contact. In view of these results, we propose as a model for their dynamics that hydrocarbons are synthesized in tissues associated with the integument. Through self-grooming, there is a constant exchange of hydrocarbons between the cuticular surface and the postpharyngeal gland. Furthermore, in encounters between nestmates, hydrocarbons are exchanged among them mostly by trophallaxis, with the mediation of the postpharyngeal gland. Thus, this gland acts as a pool for mixing colonial hydrocarbons and may serve to attain a unified colony odor.
Societies of the ant Cataglyphis iberica (Hymenoptera, Formicidae) comprise several satellite queenless nests around a queenright nest. During spring, at the end of hibernation, the incidence of adult transport between these nests is high, but it decreases during summer. Quantitative analyses of the contents of postpharyngeal glands of transporter and transportee ants reveal the amounts of hydrocarbons to be lower in the latter, indicating that these ants are generally younger. Moreover, the more diverse composition of the transportees' secretion may reflect their individual makeup. Transporters, in contrast, maintained a uniform colony odour uirough trophallactic exchanges before entering hibernation. The odour disparity between the transportees and the general colony odour may stimulate the transporters to bear them to the nest containing the queen where they can obtain the colony odour via trophallaxis. The intense traffic between satellite nests in the spring may thus be the means by which a uniform colonial odour is regained after hibernation. Adult transport seems also to be necessary since the young transportee ants are not able to orient themselves and find the other nests.
The postpharyngeal gland of Cataglyphis niger (André, 1881) workers is characterized, at the ultrastructural level, by a well-developed smooth endoplasmic reticulum, Golgi apparatus, and numerous mitochondria and lamellar inclusions suggesting an involvement in lipid metabolism. In addition, the microvillar differentiation of the apical membrane and basal invaginations of the cell imply a transportation process.
The gland shows a clear structural as well as chemical age-dependent development. Epithelial thickness increases with age, reaching its maximum within the first week after emergence. Concurrently there is a progressive development of microvilli and appearance of the lamellar inclusions. The gland's secretion consists mainly of hydrocarbons, with a predominance of monomethyl and dimethyl alkanes. Congruency was found between the hydrocarbon composition of glandular exudates and those of the epicuticular washes. An age-dependent increase in the total amount of hydrocarbons was found to correlate with the ultrastructural development and gross morphology (thickness of epicuticular lining) of the gland.
In homospecific groups of ants, each species has its own hydrocarbon profile, on the epicuticle and in the postpharyngeal gland (PPG). When reared together in bispecific groups, workers of both species possess each other's hydrocarbons in both locations. The present study investigated two alternative mechanisms by which a mixed odour in artificial groups ofFormica selysi/Manica rubida can be created. Using [1-14C] sodium acetate as a precursor,de novo biosynthesis of hydrocarbons was demonstrated for both species whether reared in homospecific or mixed-species groups. The newly synthesized hydrocarbons occurred on the epicuticle, internally, and in particularly large amounts in the PPG. As expected from their PPG and epicuticular hydrocarbons composition, workersF. selysi synthesized alkanes and alkenes in comparable amounts irrespective of their rearing scheme. Likewise,M. rubida reared in bispecific groups synthesized mostly alkanes with only negligible amounts of alkenes, according to a ratio characteristic toM. rubida workers from homospecific groups and not toF. selysi workers. During dyadic encounters, a transfer of labeled hydrocarbons between nestmates (conspecific in homospecific groups and allospecific in mixed groups) was observed. These results suggest that the formation of the mixed hydrocarbon profile in artificial groups of ants is the result of a transfer of these chemicals between nestmates rather thande novo biosynthesis of the allospecific hydrocarbons. Behaviours like trophallaxis, grooming and body contact that occurred during the encounters mediated such a transfer.