Hydration state does not affect selected body temperature during gravidity or gravidity duration in pythons (Antaresia childreni).

The embryonic development of many ectothermic species are highly sensitive to temperature and typically have a higher thermal optima than do most other physiological processes. Thus, female ectotherms often maintain a higher and more carefully controlled body temperature when she is supporting developing embryos (early development in oviparous species, throughout development in viviparous species). Considering the positive correlation between body temperature and evaporative water loss, this response could potentially exacerbate female water imbalance in water-limited environments, suggesting that female water balance and egg development may be in conflict. Using Children's pythons (Antaresia childreni), we hypothesized that water deprivation reduces thermophily during gravidity. We split reproductive females into two thermal treatments: those provided with a continuously available thermal gradient of 25-45 °C and those kept at a constant 31 °C. We also had seven non-reproductive females that were provided a thermal gradient. Within each thermal treatment group, we alternatingly assigned females to either have or not have water throughout gravidity. We found that reproduction increased female body temperature, but this increase was not affected by water regime. Reproduction also increased plasma osmolality, and lack of water during gravidity exacerbated this effect. We also found that thermal treatment, but not water regime, significantly influenced gravidity duration, with females given a thermogradient having a shorter gravidity duration, likely as a result of having a higher average body temperature than did the females provided constant heat. Finally, we found that females provided water throughout gravidity had greater clutch masses than did females without water. Further research is needed to improve scientific understanding of the interactions among water balance, body temperature, and various physiological performances.

Protocol to obtain long movement trajectories of leaders and followers in ant tandem runs.

Tandem running in ants is a sophisticated form of communication. Precise measurement of movement coordination by the tandem pair can shed light on social interactions. Here, we describe an integrative approach to obtain long movement trajectories of a specific tandem pair within a crowd of ants. We describe a maze-like arena, video recording and editing, and movement tracking. We integrate two pieces of image-based tracking software that have distinct individual assignment strategies. This protocol aids comparative studies of recruitment communication across species. For complete details on the use and execution of this protocol, please refer to Mizumoto et al. (2023)1 and Valentini et al. (2020).2.

Weaver ants regulate the rate of prey delivery during collective vertical transport.

The collective transport of massive food items by ant teams is a striking example of biological cooperation, but it remains unclear how these decentralized teams coordinate to overcome the various challenges associated with transport. Previous research has focused on transport across horizontal surfaces and very shallow inclines, disregarding the complexity of natural foraging environments. In the ant Oecophylla smaragdina, prey are routinely carried up tree trunks to arboreal nests. Using this species, we induced collective transport over a variety of angled surfaces with varying prey masses to investigate how ants respond to inclines. We found that weight and incline pose qualitatively different challenges during transport. Prey were carried over vertical and inclined surfaces faster than across horizontal surfaces, even though inclines were associated with longer routes and a higher probability of dropping the load. This additional speed was associated with more transporters being allocated to loads on steeper inclines and not with the persistence of individual ants. Ant teams also regulated a stable prey delivery rate (rate of return per transporter) across all treatments. Our proposed constrained optimization model suggests a possible explanation for these results; theoretically, prey intake rate at the colony level is maximized when the allocation of transporters yields a similar prey delivery rate across loads.

Functional and mechanistic diversity in ant tandem communication.

Communication is fundamental to the organization of animal societies, often resulting in the convergent evolution of similar social behavior across lineages. However, this similarity may conceal underlying functional and mechanistic differences. Here we combined network and information-theoretic analysis to quantify how tandem recruitment is distinguishable between two ant genera, Temnothorax and Diacamma. We show that Temnothorax uses tandem running to recruit additional recruiters, while Diacamma uses it principally to move the passive majority of their colony, a task that Temnothorax accomplishes with a different behavior, social carrying. Accordingly, the network structure of Diacamma tandems was dissimilar to that of Temnothorax, instead resembling the social-carrying networks in Temnothorax. Furthermore, our information-theoretical analysis on movement trajectories revealed that Diacamma tandem runs lack bidirectional information transfer, the signature of route learning in Temnothorax. By quantifying the diversity of similar communication systems, this study increases the resolution of our understanding of animal societies.

Is collective nest site selection in ants influenced by the anchoring effect?

Evolutionary theory predicts that animals make decisions that maximize fitness. If so, they are expected to adhere to principles of rational choice, which a decision-maker must follow to reliably maximize net benefit. For example, evaluation of an option should not be influenced by the quality of other unchosen options. However, humans and other animals are known to evaluate a mediocre option more favorably after encountering poor options than after encountering no options, a phenomenon known as the 'anchoring effect'. Rationality is also expected in the consensus decisions of animal societies, but the anchoring effect has not previously been tested in that context. Here we show that colonies of the rock ant, Temnothorax rugatulus, demonstrate the anchoring effect during nest site selection - colonies moved more readily from a mediocre nest to a good nest when exposed to poor nests than when exposed to mediocre nests. This effect depended on both current conditions and past experience; movement probability was affected only when colonies were exposed to surrounding nests before and during the emigration. The effect was small, reaching statistical significance in only one of two experimental replicates. We discuss possible mechanisms and ultimate explanations for why colonies show this seemingly suboptimal behavior.

The Power of Population Effect in Temnothorax Ant House-Hunting: A Computational Modeling Approach.

The decentralized cognition of animal groups is both a challenging biological problem and a potential basis for bioinspired design. In this study, we investigated the house-hunting algorithm used by emigrating colonies of Temnothorax ants to reach consensus on a new nest. We developed a tractable model that encodes accurate individual behavior rules, and estimated our parameter values by matching simulated behaviors with observed ones on both the individual and group levels. We then used our model to explore a potential, but yet untested, component of the ants' decision algorithm. Specifically, we examined the hypothesis that incorporating site population (the number of adult ants at each potential nest site) into individual perceptions of nest quality can improve emigration performance. Our results showed that attending to site population accelerates emigration and reduces the incidence of split decisions. This result suggests the value of testing empirically whether nest site scouts use site population in this way, in addition to the well-demonstrated quorum rule. We also used our model to make other predictions with varying degrees of empirical support, including the high cognitive capacity of colonies and their rational time investment during decision-making. In addition, we provide a versatile and easy-to-use Python simulator that can be used to explore other hypotheses or make testable predictions. It is our hope that the insights and the modeling tools can inspire further research from both the biology and computer science community.

Naïve individuals promote collective exploration in homing pigeons.

Group-living animals that rely on stable foraging or migratory routes can develop behavioural traditions to pass route information down to inexperienced individuals. Striking a balance between exploitation of social information and exploration for better alternatives is essential to prevent the spread of maladaptive traditions. We investigated this balance during cumulative route development in the homing pigeon Columba livia. We quantified information transfer within pairs of birds in a transmission-chain experiment and determined how birds with different levels of experience contributed to the exploration-exploitation trade-off. Newly introduced naïve individuals were initially more likely to initiate exploration than experienced birds, but the pair soon settled into a pattern of alternating leadership with both birds contributing equally. Experimental pairs showed an oscillating pattern of exploration over generations that might facilitate the discovery of more efficient routes. Our results introduce a new perspective on the roles of leadership and information pooling in the context of collective learning.

Coordination of movement via complementary interactions of leaders and followers in termite mating pairs.

In collective animal motion, coordination is often achieved by feedback between leaders and followers. For stable coordination, a leader's signals and a follower's responses are hypothesized to be attuned to each other. However, their roles are difficult to disentangle in species with highly coordinated movements, hiding potential diversity of behavioural mechanisms for collective behaviour. Here, we show that two Coptotermes termite species achieve a similar level of coordination via distinct sets of complementary leader-follower interactions. Even though C. gestroi females produce less pheromone than C. formosanus, tandem runs of both species were stable. Heterospecific pairs with C. gestroi males were also stable, but not those with C. formosanus males. We attributed this to the males' adaptation to the conspecific females; C. gestroi males have a unique capacity to follow females with small amounts of pheromone, while C. formosanus males reject C. gestroi females as unsuitable but are competitive over females with large amounts of pheromone. An information-theoretic analysis supported this conclusion by detecting information flow from female to male only in stable tandems. Our study highlights cryptic interspecific variation in movement coordination, a source of novelty for the evolution of social interactions.

Complex Relationship between Tunneling Patterns and Individual Behaviors in Termites.

AbstractThe nests built by social insects are complex group-level structures that emerge from interactions among individuals following simple behavioral rules. Nest patterns vary among species, and the theory of complex systems predicts that there is no simple one-to-one relationship between variation in collective patterns and variation in individual behaviors. Therefore, a species-by-species comparison of the actual building process is essential to understand the mechanism producing diverse nest patterns. Here, we compare tunnel formation of three termite sp ecies and reveal two mechanisms producing interspecific variation: in one, a common behavioral rule yields distinct patterns via parameter tuning, and in the other, distinct rules produce similar patterns. We found that two related species transport sand in the same way using mandibles but build tunnels with different degrees of branching. The variation arises from different probabilities of choosing between two behavioral options at crowded tunnel faces: excavating the sidewall to make a new branch or waiting for clearance to extend the current tunnel. We further discovered that a third species independently evolved low-branched patterns using different building rules, namely, a bucket brigade that can excavate a crowded tunnel. Our findings emphasize the importance of direct comparative study of collective behaviors at both individual and group levels.

Termite males enhance mating encounters by changing speed according to density.

Search theory predicts that animals evolve efficient movement patterns to enhance encounter rates with specific targets. The optimal movements vary with the surrounding environments, which may explain the observation that animals often switch their movement patterns depending on conditions. However, the effectiveness of behavioural change during search is rarely evaluated because it is difficult to examine the actual encounter dynamics. Here we studied how partner-seeking termites update their search strategies depending on the local densities of potential mates. After a dispersal flight, termites drop their wings and walk to search for a mate; when a female and a male meet, they form a female-led tandem pair and search for a favourable nesting site. If a pair is separated, they have two search options-reunite with their stray partner, or seek a new partner. We hypothesized that the density of individuals affects separation-reunion dynamics and thus the optimal search strategy. We observed the searching process across different densities and found that termite pairs were often separated but obtained a new partner quickly at high mate density. After separation, while females consistently slowed down, males increased their speed according to the density. Under high mate density, separated males obtained a partner earlier than females, who do not change movement with density. Our data-based simulations confirmed that the observed behavioural change by males contributes to enhancing encounters. Males at very low mate densities did best to move slowly and thereby reduce the risk of missing their stray partner, who is the only available mate. On the other hand, males that experienced high mate densities did better in mating encounters by moving fast because the risk of isolation is low, and they must compete with other males to find a partner. These results demonstrate that termite males adaptively update their search strategy depending on conditions. Understanding the encounter dynamics experienced by animals is key to connecting the empirical work to the idealized search processes of theoretical studies.

Revealing the structure of information flows discriminates similar animal social behaviors.

Behavioral correlations stretching over time are an essential but often neglected aspect of interactions among animals. These correlations pose a challenge to current behavioral-analysis methods that lack effective means to analyze complex series of interactions. Here we show that non-invasive information-theoretic tools can be used to reveal communication protocols that guide complex social interactions by measuring simultaneous flows of different types of information between subjects. We demonstrate this approach by showing that the tandem-running behavior of the ant Temnothorax rugatulus and that of the termites Coptotermes formosanus and Reticulitermes speratus are governed by different communication protocols. Our discovery reconciles the diverse ultimate causes of tandem running across these two taxa with their apparently similar signaling mechanisms. We show that bidirectional flow of information is present only in ants and is consistent with the use of acknowledgement signals to regulate the flow of directional information.

Social animals continuously influence each other's behavior. Most of these interactions simply consist in an individual immediately responding to the behavior of another in a predictable way. Still, when the same individuals interact over long periods, complex social interactions can arise. These can be difficult for scientists to study, because how animals behave at a given moment depends on their shared history. Certain species of ants and termites use smell and touch to do 'tandem runs' and move in pairs through the environment. Only ants, however, can learn a new route from their running partner. Understanding how this difference arises means examining how the animals interact and communicate over longer time scales. This requires new approaches to capture how information flows between the insects. Here, Valentini et al. used a scientific methodology known as information theory to study tandem running in one species of ants and two species of termites. Information theory provides a framework to quantify how information is shared, processed and stored. The flow of information between individuals was measured separately for different aspects of tandem running. At small time scales, ant and termite behavior appeared identical, but over longer periods, it was possible to distinguish between the two types of insects. In termites, only one individual in a pair sent information to the other to instruct the second termite where to go. By contrast, in ants, both members of the tandem communicated with each other in a way that was consistent with how humans acknowledge information they receive from other individuals. The approach used by Valentini et al. will be useful to researchers who study how complex and often cryptic social interactions develop over extended periods in social animals. This framework could also be applied in other systems such as groups of cells, or economic networks.

Route learning during tandem running in the rock ant Temnothorax albipennis.

Many animals use information from conspecifics to change their behavior in adaptive ways. When a rock ant, Temnothorax albipennis, finds food, she returns to her colony and uses a method called tandem running to lead nestmates, one at a time, from the nest to the food. In this way, naive ants can learn the location of a food source. Less clear is whether they also learn navigational cues that guide them from nest to food, although this is often assumed. We tested this idea by tracing the routes of individually marked ants as they followed tandem runs to a feeder, returned to the nest, and later traveled independently back to the food. Our results show, for the first time, that tandem run followers learn specific routes from their leaders. Independent journeys back to the food source were significantly more similar to the routes on which the ants had been led, compared with the routes taken by other tandem runs. In contrast, the homeward journey did not resemble the tandem run route. These results are consistent with followers memorizing visual cues during the tandem run that are useful for recapitulating the outward journey, but not as effective when facing in the opposite direction on the homeward journey. We further showed that foraging routes improved through individual experience over multiple trips but not through the social transfer of route information via tandem running. We discuss our findings in relation to social learning and integration of individual and social information in ants.

Division of labour promotes the spread of information in colony emigrations by the ant Temnothorax rugatulus.

The fitness of group-living animals often depends on how well members share information needed for collective decision-making. Theoretical studies have shown that collective choices can emerge in a homogeneous group of individuals following identical rules, but real animals show much evidence for heterogeneity in the degree and nature of their contribution to group decisions. In social insects, for example, the transmission and processing of information is influenced by a well-organized division of labour. Studies that accurately quantify how this behavioural heterogeneity affects the spread of information among group members are still lacking. In this paper, we look at nest choices during colony emigrations of the ant Temnothorax rugatulus and quantify the degree of behavioural heterogeneity of workers. Using clustering methods and network analysis, we identify and characterize four behavioural castes of workers-primary, secondary, passive and wandering-covering distinct roles in the spread of information during an emigration. This detailed characterization of the contribution of each worker can improve models of collective decision-making in this species and promises a deeper understanding of behavioural variation at the colony level.

Rational time investment during collective decision making in Temnothorax ants.

The study of rational choice in humans and other animals typically focuses on decision outcomes, but rationality also applies to decision latencies, especially when time is scarce and valuable. For example, the smaller the difference in quality between two options, the faster a rational actor should decide between them. This is because the consequences of choosing the inferior option are less severe if the options are similar. Experiments have shown, however, that humans irrationally spend more time choosing between similar options. In this study, we assessed the rationality of time investment during nest-site choice by the rock ant, Temnothorax albipennis. Previous studies have shown that collective decision-making allows ant colonies to avoid certain irrational errors. Here we show that the same is true for time investment. Individual ants, like humans, irrationally took more time to complete an emigration when choosing between two similar nests than when choosing between two less similar nests. Whole colonies, by contrast, rationally made faster decisions when the options were more similar. We discuss the underlying mechanisms of decision-making in individuals and colonies and how they lead to irrational and rational time investment, respectively.

Inferring collective behaviour from a fossilized fish shoal.

Collective motion by animal groups can emerge from simple rules that govern each individual's interactions with its neighbours. Studies of extant species have shown how such rules yield coordinated group behaviour, but little is known of their evolutionary origins or whether extinct group-living organisms used similar rules. Here, we report evidence consistent with coordinated collective motion in a fossilized group of the extinct fish Erismatopterus levatus, and we infer possible behavioural rules that underlie it. We found traces of two rules for social interaction similar to those used by extant fishes: repulsion from close individuals and attraction towards neighbours at a distance. Moreover, the fossilized fish showed group-level structures in the form of oblong shape and high polarization, both of which we successfully reproduced in simulations incorporating the inferred behavioural rules. Although it remains unclear how the fish shoal's structure was preserved in the fossil, these findings suggest that fishes have been forming shoals by combining sets of simple behavioural rules since at least the Eocene. Our study highlights the possibility of exploring the social communication of extinct animals, which has been thought to leave no fossil record.

Symmetry breaking and pivotal individuals during the reunification of ant colonies.

Maintenance of a social group requires the ability to reach consensus when faced with divisive choices. Thus, when migrating colonies of the ant Temnothorax rugatulus split among multiple sites, they can later reunify on the basis of queen location or differences in site quality. In this study, we found that colonies can reunify even without obvious cues to break the symmetry between sites. To learn how they do so, we observed both symmetric reunifications (between identical nests) and asymmetric reunifications (between nests of unequal quality) by colonies of individually marked ants. Both reunification types were accomplished by a tiny minority that carried nestmates from the 'losing' to the 'winning' site. Reunification effort was highly skewed in asymmetric splits, where the majority of the work was done by the first ant to transport, which nearly always came from the winning site. This contrasted with symmetric splits, where the initiator did not play an outsize role and was just as likely to come from the losing site. Symmetric reunifications were also characterized by high transporter attrition, which may help to prevent deadlocks. Tandem runs were abundant in both types and were typically led by transporters as they returned to the losing site to fetch another nestmate. Few tandem followers joined the transport effort, suggesting that tandem runs do not serve to recruit transporters but may have another, as yet unidentified role. Our results underscore the potentially large contribution of highly active individuals to group behaviour, even in decentralized societies such as ant colonies.

Ant-plant sociometry in the Azteca-Cecropia mutualism.

A holistic understanding of superorganism biology requires study of colony sociometry, or the quantitative relationships among growth, nest architecture, morphology, and behavior. For ant colonies that obligately nest within plant hosts, their sociometry is likely intertwined with the plant, which has implications for the evolution, strength, and stability of the mutualism. In the Azteca-Cecropia mutualism, plants provide ants with food rewards and hollow stems for nesting in return for protection from herbivores. Several interesting questions arise when considering ant-plant sociometry: are colony growth and plant growth synchronized? How do colonies distribute themselves within the stem of their host plant? How do plant traits influence worker morphology? How is collective personality related to tree structure, nest organization, and worker morphology? To address these questions, we investigated patterns within and relationships among five major sociometric categories of colonies in the field - plant traits, colony size, nest organization, worker morphology, and collective personality. We found that colony sociometry was intimately intertwined with host plant traits. Colony and plant growth rates were synchronized, suggesting that positive feedback between plant and colony growth stabilizes the mutualism. The colony's distribution inside the host tree tended to follow leaf growth, with most workers, brood, and the queen in the top half of the tree. Worker morphology correlated with plant size instead of colony size or age, which suggests that plant traits influence worker development. Colony personality was independent of colony distribution and tree structure but may correlate with worker size such that colonies with smaller, less variable workers had more aggressive personalities. This study provides insights into how ant-plant structural relationships may contribute to plant protection and the strength of mutualisms.

Multi-robot replication of ant collective towing behaviours.

In this work, teams of small mobile robots are used to test hypotheses about cooperative transport by ants. This study attempts to explain a decrease in steady-state transport speed with increasing team size that was previously observed in the ant Novomessor cockerelli. Two models of one-dimensional collective towing are compared: one in which transporters with different maximum speeds pull the payload with continuous, variable forces and another in which transporters with identical speeds pull with intermittent, unsynchronized forces. A statistical analysis of ant data supports the hypothesis that ants behave according to the first model, in which the steady-state transport speed is the maximum speed of the slowest teammate. By contrast, the ant data are not consistent with the second model, which predicts constant speed regardless of team size. To verify these predictions, the ant behaviours in each model are translated into decentralized controllers and implemented on teams of two to four robots. The controller for the first model incorporates a real-time reinforcement learning algorithm that successfully reproduces the observed relationship between ant team size and transport speed. The controller for the second model yields the predicted invariance of transport speed with team size. These results show the value of robotic swarms for testing mechanistic hypotheses about biological collectives.

Scaling of speed with group size in cooperative transport by the ant Novomessor cockerelli.

Working together allows social animals to accomplish tasks beyond the abilities of solitary individuals, but the benefits of cooperation must be balanced with the costs of coordination. Many ant species form cooperative groups to transport items too large for a single ant. However, transport by groups is often slower and less efficient than that of lone ants, for reasons that remain poorly understood. We tested the hypothesis that groups are slower when porters must encircle the load to carry it, because this arrangement places ants in a variety of postures relative to the load and the direction of travel. Porters may therefore have difficulty maximizing individual forces and aligning them with those of other group members. Experiments on the desert ant Novomessor cockerelli, an adept cooperative transporter, did not support this hypothesis. Groups ranging in size from one to four ants were induced to carry loads such that all porters were aligned with one another. Load weight was adjusted so that all porters pulled the same per capita weight, but lone porters were nonetheless faster than groups of any size. As group size increased, porters persisted in carrying the load for longer periods before letting go. We used simulations to explore a scenario in which ants vary in their intrinsic speed and the group's speed is limited by that of its slowest member. This proposed mechanism is analogous to other social groups where group efficiency is determined by the weakest link. We discuss how interactions among porters, mediated by the load itself, might explain such a constraint.

Parallel vs. comparative evaluation of alternative options by colonies and individuals of the ant Temnothorax rugatulus.

Both a single ant and the colony to which it belongs can make decisions, but the underlying mechanisms may differ. Colonies are known to be less susceptible than lone ants to "choice overload", whereby decision quality deteriorates with increasing number of options. We probed the basis of this difference, using the model system of nest-site selection by the ant Temnothorax rugatulus. We tested the applicability of two competing models originally developed to explain information-processing mechanisms in vertebrates. The Tug of War model states that concurrent alternatives are directly compared, so that choosing between two alternatives takes longer than accepting a single one. In contrast, the Sequential Choice Model assumes that options are examined in parallel, and action takes place once any option reaches a decision criterion, so that adding more options shortens time to act. We found that single ants matched the Tug of War model while colonies fitted the Sequential Choice model. Our study shows that algorithmic models for decision-making can serve to investigate vastly different domains, from vertebrate individuals to both individuals and colonies of social insects.