Collective search in ants: Movement determines footprints, and footprints influence movement.

Collectively searching animals might be expected to coordinate with their groupmates to cover ground more evenly or efficiently than uncoordinated groups. Communication can lead to coordination in many ways. Previous work in ants suggests that chemical 'footprints', left behind by individuals as they walk, might serve this function by modulating the movement patterns of following ants. Here, we test this hypothesis by considering the two predictions that, first, ants may turn away from sites with higher footprint concentrations (klinotaxis), or, second, that they may change their turning patterns depending on the presence of footprints (klinokinesis). We tracked 5 whole colonies of Temnothorax rugatulus ants in a large arena over 5h. We approximated the footprint concentration by summing ant visitations for each point in the arena and calculated the speed and local path straightness for each point of the ant trajectories. We counterintuitively find that ants walk slightly faster and straighter in areas with fewer footprints. This is partially explained by the effect that ants who start out from the nest walking straighter move on average further away from the nest, where there are naturally fewer footprints, leading to an apparent relationship between footprint density and straightness However, ants walk slightly faster and straighter off footprints even when controlling for this effect. We tested for klinotaxis by calculating the footprint concentrations perceived by the left and right antennae of ants and found no evidence for a turning-away (nor turning-towards) behavior. Instead, we found noticeable effects of environmental idiosyncrasies on the behavior of ants which are likely to overpower any reactions to pheromones. Our results indicate that search density around an ant colony is affected by several independent processes, including individual differences in movement pattern, local spatial heterogeneities, and ants' reactions to chemical footprints. The multitude of effects illustrates that non-communicative coordination, individual biases and interactions with the environment might have a greater impact on group search efficiency and exploratory movements than pheromone communication.

Ants combine systematic meandering and correlated random walks when searching for unknown resources.

Animal search movements are typically assumed to be mostly random walks, although non-random elements may be widespread. We tracked ants (Temnothorax rugatulus) in a large empty arena, resulting in almost 5 km of trajectories. We tested for meandering by comparing the turn autocorrelations for empirical ant tracks and simulated, realistic Correlated Random Walks. We found that 78% of ants show significant negative autocorrelation around 10 mm (3 body lengths). This means that turns in one direction are likely followed by turns in the opposite direction after this distance. This meandering likely makes the search more efficient, as it allows ants to avoid crossing their own paths while staying close to the nest, avoiding return-travel time. Combining systematic search with stochastic elements may make the strategy less vulnerable to directional inaccuracies. This study is the first to find evidence for efficient search by regular meandering in a freely searching animal.

Injected serotonin decreases foraging aggression in black widow spiders (Latrodectus hesperus), but dopamine has no effect.

A fundamental goal of animal behavior research is to discover the proximate mechanisms driving individual behavioral differences. Biogenic amines are known to mediate various aspects of behavior across many species, including aggression, one of the most commonly measured behavioral traits in animals. Arthropods provide an excellent system to manipulate biogenic amines and quantify subsequent behavioral changes. Here, we investigated the role of dopamine (DA) and serotonin (5-HT) on foraging aggression in western black widow spiders (Latrodectus hesperus), as measured by the number of attacks on a simulated prey animal in the web. We injected spiders with DA or 5-HT and then quantified subsequent changes in behavior over 48 h. Based on previous work on insects and spiders, we hypothesized that increasing DA levels would increase aggression, while increasing 5-HT would decrease aggression. We found that injection of 5-HT did decrease black widow foraging aggression, but DA had no effect. This could indicate that the relationship between DA and aggression is complex, or that DA may not play as important a role in driving aggressive behavior as previously thought, at least in black widow spiders. Aggressive behavior is likely also influenced by other factors, such as inter-individual differences in genetics, metabolic rates, environment, and other neurohormonal controls.

Distributing Defenses: How Resource Defendability Shapes the Optimal Response to Risk.

AbstractMany organisms divide limited defenses among heterogeneous assets. Plants allocate defensive chemicals among tissues differing in value, cost of defense, and risk of herbivory. Some ant colonies allocate specialized defenders among multiple nests differing in volume, entrance size, and risk of attack. We develop a general mathematical model to determine the optimal strategy for dividing defenses among assets depending on their value, defendability, and risk of attack. We build on plant defense theory by focusing on defendability, which we define as the functional relationship between defensive investment and successful defense. We show that if hard-to-defend assets cost more to defend, as assumed in resource defense theory, the optimal strategy allocates more defenses to those assets, regardless of risk. Inspired by cavity-nesting ants, we also consider the possibility that hard-to-defend assets have a lower chance to be successfully defended, even when defensive investment is high. Under this assumption, the optimal response to elevated risk is to reduce defensive allocation to hard-to-defend assets, a conservative strategy previously observed in turtle ants (Cephalotes). This new perspective on defendability suggests that in systems where assets differ in the chance of successful defense, defensive strategies may evolve to be sensitive to risk in surprising ways.

How Can We Fully Realize the Potential of Mathematical and Biological Models to Reintegrate Biology?

Both mathematical models and biological model systems stand as tractable representations of complex biological systems or behaviors. They facilitate research and provide insights, and they can describe general rules. Models that represent biological processes or formalize general hypotheses are essential to any broad understanding. Mathematical or biological models necessarily omit details of the natural systems and thus may ultimately be "incorrect" representations. A key challenge is that tractability requires relatively simple models but simplification can result in models that are incorrect in their qualitative, broad implications if the abstracted details matter. Our paper discusses this tension, and how we can improve our inferences from models. We advocate for further efforts dedicated to model development, improvement, and acceptance by the scientific community, all of which may necessitate a more explicit discussion of the purpose and power of models. We argue that models should play a central role in reintegrating biology as a way to test our integrated understanding of how molecules, cells, organs, organisms, populations, and ecosystems function.

Juvenile social experience generates differences in behavioral variation but not averages.

Developmental plasticity is known to influence the mean behavioral phenotype of a population. Yet, studies on how developmental plasticity shapes patterns of variation within populations are comparatively rare and often focus on a subset of developmental cues (e.g., nutrition). One potentially important but understudied developmental experience is social experience, as it is explicitly hypothesized to increase variation among individuals as a way to promote "social niches." To test this, we exposed juvenile black widow spiders (Latrodectus hesperus) to the silk of conspecifics by transplanting them onto conspecific webs for 48 h once a week until adulthood. We also utilized an untouched control group as well as a disturbed group. This latter group was removed from their web at the same time points as the social treatment, but was immediately placed back on their own web. After repeatedly measuring adult behavior and web structure, we found that social rearing drove higher or significant levels of repeatability relative to the other treatments. Repeatability in the social treatment also decreased in some traits, paralleling the decreases observed in the disturbed treatments. Thus, repeated juvenile disturbance may decrease among-individual differences in adult spiders. Yet, social rearing appeared to override the effect of disturbance in some traits, suggesting a prioritization effect. The resulting individual differences were maintained over at least one-third of the adult lifespan and thus appear to represent stable, canalized developmental effects and not temporal state differences. These results provide proximate insight into how a broader range of developmental experiences shape trait variation.

Signal categorization by foraging animals depends on ecological diversity.

Warning signals displayed by defended prey are mimicked by both mutualistic (Müllerian) and parasitic (Batesian) species. Yet mimicry is often imperfect: why does selection not improve mimicry? Predators create selection on warning signals, so predator psychology is crucial to understanding mimicry. We conducted experiments where humans acted as predators in a virtual ecosystem to ask how prey diversity affects the way that predators categorize prey phenotypes as profitable or unprofitable. The phenotypic diversity of prey communities strongly affected predator categorization. Higher diversity increased the likelihood that predators would use a 'key' trait to form broad categories, even if it meant committing errors. Broad categorization favors the evolution of mimicry. Both species richness and evenness contributed significantly to this effect. This lets us view the behavioral and evolutionary processes leading to mimicry in light of classical community ecology. Broad categorization by receivers is also likely to affect other forms of signaling.

Peripheral sensory organs vary among ant workers but variation does not predict division of labor.

The neural mechanisms underlying behavioral variation among individuals are not well understood. Differences among individuals in sensory sensitivity could limit the environmental stimuli to which an individual is capable of responding and have, indeed, been shown to relate to behavioral differences in different species. Here, we show that ant workers in Temnothorax rugatulus differ considerably in the number of antennal sensory structures, or sensilla (by 45% in density and over 100% in estimated total number). A larger quantity of sensilla may reflect a larger quantity of underlying sensory neurons. This would increase the probability that a given set of neurons in the antenna detects an environmental stimulus and becomes excited, thereby eliciting the expression of a behavior downstream at lower stimulus levels than an individual with comparatively fewer sensilla. Individual differences in antennal sensilla density, however, did not predict worker activity level or performance of any task, suggesting either that variation in sensilla density does not, in fact, reflect variation in sensory sensitivity or that individual sensory response thresholds to task-associated stimuli do not determine task allocation as is commonly assumed, at least in this social insect. More broadly, our finding that even closely related individuals can differ strongly in peripheral sensory organ elaboration suggests that such variation in sensory organs could underlie other cases of intraspecific behavioral variation.

How cognitive biases select for imperfect mimicry: a study of asymmetry in learning with bumblebees.

Imperfect mimicry presents a paradox of incomplete adaptation - intuitively, closer resemblance should improve performance. Receiver psychology can often explain why mimetic signals do not always evolve to match those of their models. Here, we explored the influence of a pervasive and powerful cognitive bias where associative learning depends upon an asymmetric interaction between the cue (stimulus) and consequence (reinforcer), such as in rats, which will associate light and tone with shock, and taste with nausea, but not the converse. Can such biases alter selection for mimicry? We designed an artificial mimicry system where bees foraged on artificial flowers, so that colours could be switched between rewarding or aversive. We found that when the colour blue was paired with a sucrose reward, other cues were ignored, but not when blue was paired with aversive compounds. We also tested the hypothesis that costs of errors affect how receivers sample imperfect mimics. However, costs of errors did not affect bee visits to imperfect mimics in our study. We propose a novel hypothesis for imperfect mimicry, in which the pairing between specific cues and reinforcers allows an imperfect mimic to resemble multiple models simultaneously. Generally, our results emphasize the importance of receiver psychology for the evolution of signal complexity and specificity.

Costs of task allocation with local feedback: Effects of colony size and extra workers in social insects and other multi-agent systems.

Adaptive collective systems are common in biology and beyond. Typically, such systems require a task allocation algorithm: a mechanism or rule-set by which individuals select particular roles. Here we study the performance of such task allocation mechanisms measured in terms of the time for individuals to allocate to tasks. We ask: (1) Is task allocation fundamentally difficult, and thus costly? (2) Does the performance of task allocation mechanisms depend on the number of individuals? And (3) what other parameters may affect their efficiency? We use techniques from distributed computing theory to develop a model of a social insect colony, where workers have to be allocated to a set of tasks; however, our model is generalizable to other systems. We show, first, that the ability of workers to quickly assess demand for work in tasks they are not currently engaged in crucially affects whether task allocation is quickly achieved or not. This indicates that in social insect tasks such as thermoregulation, where temperature may provide a global and near instantaneous stimulus to measure the need for cooling, for example, it should be easy to match the number of workers to the need for work. In other tasks, such as nest repair, it may be impossible for workers not directly at the work site to know that this task needs more workers. We argue that this affects whether task allocation mechanisms are under strong selection. Second, we show that colony size does not affect task allocation performance under our assumptions. This implies that when effects of colony size are found, they are not inherent in the process of task allocation itself, but due to processes not modeled here, such as higher variation in task demand for smaller colonies, benefits of specialized workers, or constant overhead costs. Third, we show that the ratio of the number of available workers to the workload crucially affects performance. Thus, workers in excess of those needed to complete all tasks improve task allocation performance. This provides a potential explanation for the phenomenon that social insect colonies commonly contain inactive workers: these may be a 'surplus' set of workers that improves colony function by speeding up optimal allocation of workers to tasks. Overall our study shows how limitations at the individual level can affect group level outcomes, and suggests new hypotheses that can be explored empirically.

Who Are the "Lazy" Ants? The Function of Inactivity in Social Insects and a Possible Role of Constraint: Inactive Ants Are Corpulent and May Be Young and/or Selfish.

Social insect colonies are commonly thought of as highly organized and efficient complex systems, yet high levels of worker inactivity are common. Although consistently inactive workers have been documented across many species, very little is known about the potential function or costs associated with this behavior. Here we ask what distinguishes these "lazy" individuals from their nestmates. We obtained a large set of behavioral and morphological data about individuals, and tested for consistency with the following evolutionary hypotheses: that inactivity results from constraint caused by worker (a) immaturity or (b) senescence; that (c) inactive workers are reproducing; that inactive workers perform a cryptic task such as (d) acting as communication hubs or (e) food stores; and that (f) inactive workers represent the "slow-paced" end of inter-worker variation in "pace-of-life." We show that inactive workers walk more slowly, have small spatial fidelity zones near the nest center, are more corpulent, are isolated in colony interaction networks, have the smallest behavioral repertoires, and are more likely to have oocytes than other workers. These results are consistent with the hypotheses that inactive workers are immature and/or storing food for the colony; they suggest that workers are not inactive as a consequence of senescence, and that they are not acting as communication hubs. The hypotheses listed above are not mutually exclusive, and likely form a "syndrome" of behaviors common to inactive social insect workers. Their simultaneous contribution to inactivity may explain the difficulty in finding a simple answer to this deceptively simple question.

Who needs 'lazy' workers? Inactive workers act as a 'reserve' labor force replacing active workers, but inactive workers are not replaced when they are removed.

Social insect colonies are highly successful, self-organized complex systems. Surprisingly however, most social insect colonies contain large numbers of highly inactive workers. Although this may seem inefficient, it may be that inactive workers actually contribute to colony function. Indeed, the most commonly proposed explanation for inactive workers is that they form a 'reserve' labor force that becomes active when needed, thus helping mitigate the effects of colony workload fluctuations or worker loss. Thus, it may be that inactive workers facilitate colony flexibility and resilience. However, this idea has not been empirically confirmed. Here we test whether colonies of Temnothorax rugatulus ants replace highly active (spending large proportions of time on specific tasks) or highly inactive (spending large proportions of time completely immobile) workers when they are experimentally removed. We show that colonies maintained pre-removal activity levels even after active workers were removed, and that previously inactive workers became active subsequent to the removal of active workers. Conversely, when inactive workers were removed, inactivity levels decreased and remained lower post-removal. Thus, colonies seem to have mechanisms for maintaining a certain number of active workers, but not a set number of inactive workers. The rapid replacement (within 1 week) of active workers suggests that the tasks they perform, mainly foraging and brood care, are necessary for colony function on short timescales. Conversely, the lack of replacement of inactive workers even 2 weeks after their removal suggests that any potential functions they have, including being a 'reserve', are less important, or auxiliary, and do not need immediate recovery. Thus, inactive workers act as a reserve labor force and may still play a role as food stores for the colony, but a role in facilitating colony-wide communication is unlikely. Our results are consistent with the often cited, but never yet empirically supported hypothesis that inactive workers act as a pool of 'reserve' labor that may allow colonies to quickly take advantage of novel resources and to mitigate worker loss.

Temnothorax rugatulus ant colonies consistently vary in nest structure across time and context.

A host of animals build architectural constructions. Such constructions frequently vary with environmental and individual/colony conditions, and their architecture directly influences behavior and fitness. The nests of ant colonies drive and enable many of their collective behaviors, and as such are part of their 'extended phenotype'. Since ant colonies have been recently shown to differ in behavior and life history strategy, we ask whether colonies differ in another trait: the architecture of the constructions they create. We allowed Temnothorax rugatulus rock ants, who create nests by building walls within narrow rock gaps, to repeatedly build nest walls in a fixed crevice but under two environmental conditions. We find that colonies consistently differ in their architecture across environments and over nest building events. Colony identity explained 12-40% of the variation in nest architecture, while colony properties and environmental conditions explained 5-20%, as indicated by the condition and marginal R2 values. When their nest boxes were covered, which produced higher humidity and lower airflow, colonies built thicker, longer, and heavier walls. Colonies also built more robust walls when they had more brood, suggesting a protective function of wall thickness. This is, to our knowledge, the first study to explicitly investigate the repeatability of nestbuilding behavior in a controlled environment. Our results suggest that colonies may face tradeoffs, perhaps between factors such as active vs. passive nest defense, and that selection may act on individual construction rules as a mechanisms to mediate colony-level behavior.

Sampling and tracking a changing environment: persistence and reward in the foraging decisions of bumblebees.

The question of when to collect new information and how to apply that information is central to much of behaviour. Theory suggests that the value of collecting information, or sampling, depends on environmental persistence and on the relative costs of making wrong decisions. However, empirical tests of how these variables interact are lacking. We tested whether bumblebee foraging decisions are indeed influenced by these two factors. We gave bees repeated choices between a resource providing a steady, mediocre reward and a resource fluctuating between a low reward and a high reward. In this paradigm, we manipulated environmental persistence by changing how long the quality of a fluctuating resource remained stable at one reward level. We manipulated the costs of decision errors by changing the relative values of the available rewards. Bees sampled the fluctuating resource more frequently when it changed quality more frequently, indicating that they measured environmental persistence and reacted to it as predicted by theory. Bees showed surprisingly suboptimal tracking, not reliably choosing the currently best resource except when the fluctuating resource was very persistent and the potential rewards high. While bees modify their choices in response to different levels of change and potential rewards, they do not always do so according to optimality predictions.

Task switching is associated with temporal delays in Temnothorax rugatulus ants.

The major evolutionary transitions often result in reorganization of biological systems, and a component of such reorganization is that individuals within the system specialize on performing certain tasks, resulting in a division of labor. Although the traditional benefit of division of labor is thought to be a gain in work efficiency, one alternative benefit of specialization is avoiding temporal delays associated with switching tasks. While models have demonstrated that costs of task switching can drive the evolution of division of labor, little empirical support exists for this hypothesis. We tested whether there were task-switching costs in Temnothorax rugatulus. We recorded the behavior of every individual in 44 colonies and used this dataset to identify each instance where an individual performed a task, spent time in the interval (i.e., inactive, wandering inside, and self-grooming), and then performed a task again. We compared the interval time where an individual switched task type between that first and second bout of work to instances where an individual performed the same type of work in both bouts. In certain cases, we find that the interval time was significantly shorter if individuals repeated the same task. We find this time cost for switching to a new behavior in all active worker groups, that is, independently of worker specialization. These results suggest that task-switching costs may select for behavioral specialization.

Foraging Bumble Bees Weigh the Reliability of Personal and Social Information.

Many animals, including insects, make decisions using both personally gathered information and social information derived from the behavior of other, usually conspecific, individuals [1]. Moreover, animals adjust use of social versus personal information appropriately under a variety of experimental conditions [2-5]. An important factor in how information is used is the information's reliability, that is, how consistently the information is correlated with something of relevance in the environment [6]. The reliability of information determines which signals should be attended to during communication [6-9], which types of stimuli animals should learn about, and even whether learning should evolve [10, 11]. Here, we show that bumble bees (Bombus impatiens) account for the reliability of personally acquired information (which flower color was previously associated with reward) and social information (which flowers are chosen by other bees) in making foraging decisions; however, the two types of information are not treated equally. Bees prefer to use social information if it predicts a reward at all, but if social information becomes entirely unreliable, flower color will be used instead. This greater sensitivity to the reliability of social information, and avoidance of conspecifics in some cases, may reflect the specific ecological circumstances of bee foraging. Overall, the bees' ability to make decisions based on both personally acquired and socially derived information, and the relative reliability of both, demonstrates a new level of sophistication and flexibility in animal, particularly insect, decision-making.

Dance communication affects consistency, but not breadth, of resource use in pollen-foraging honey bees.

In groups of cooperatively foraging individuals, communication may improve the group's performance by directing foraging effort to where it is most useful. Honey bees (Apis mellifera) use a specialized dance to communicate the location of floral resources. Because honey bees dance longer for more rewarding resources, communication may shift the colony's foraging effort towards higher quality resources, and thus narrow the spectrum of resource types used. To test the hypothesis that dance communication changes how much honey bee colonies specialize on particular resources, we manipulated their ability to communicate location, and assessed the relative abundance of different pollen taxa they collected. This was repeated across five natural habitats that differed in floral species richness and spatial distribution. Contrary to expectation, impairing communication did not change the number or diversity of pollen (resource) types used by individual colonies per day. However, colonies with intact dance communication were more consistent in their resource use, while those with impaired communication were more likely to collect rare, novel pollen types. This suggests that communication plays an important role in shaping how much colonies invest in exploring new resources versus exploiting known ones. Furthermore, colonies that did more exploration also tended to collect less pollen overall, but only in environments with greater floral abundance per patch. In such environments, the ability to effectively exploit highly rewarding resources may be especially important-and dance communication may help colonies do just that. This could help explain how communication benefits honey bee colonies, and also why it does so only under certain environmental conditions.

Behavioural syndromes and social insects: personality at multiple levels.

Animal personalities or behavioural syndromes are consistent and/or correlated behaviours across two or more situations within a population. Social insect biologists have measured consistent individual variation in behaviour within and across colonies for decades. The goal of this review is to illustrate the ways in which both the study of social insects and of behavioural syndromes has overlapped, and to highlight ways in which both fields can move forward through the synergy of knowledge from each. Here we, (i) review work to date on behavioural syndromes (though not always referred to as such) in social insects, and discuss mechanisms and fitness effects of maintaining individual behavioural variation within and between colonies; (ii) summarise approaches and principles from studies of behavioural syndromes, such as trade-offs, feedback, and statistical methods developed specifically to study behavioural consistencies and correlations, and discuss how they might be applied specifically to the study of social insects; (iii) discuss how the study of social insects can enhance our understanding of behavioural syndromes-research in behavioural syndromes is beginning to explore the role of sociality in maintaining or developing behavioural types, and work on social insects can provide new insights in this area; and (iv) suggest future directions for study, with an emphasis on examining behavioural types at multiple levels of organisation (genes, individuals, colonies, or groups of individuals).

Floral nectar guide patterns discourage nectar robbing by bumble bees.

Floral displays are under selection to both attract pollinators and deter antagonists. Here we show that a common floral trait, a nectar guide pattern, alters the behavior of bees that can act opportunistically as both pollinators and as antagonists. Generally, bees access nectar via the floral limb, transporting pollen through contact with the plant's reproductive structures; however bees sometimes extract nectar from a hole in the side of the flower that they or other floral visitors create. This behavior is called "nectar robbing" because bees may acquire the nectar without transporting pollen. We asked whether the presence of a symmetric floral nectar guide pattern on artificial flowers affected bumble bees' (Bombus impatiens) propensity to rob or access nectar "legitimately." We discovered that nectar guides made legitimate visits more efficient for bees than robbing, and increased the relative frequency of legitimate visits, compared to flowers lacking nectar guides. This study is the first to show that beyond speeding nectar discovery, a nectar guide pattern can influence bees' flower handling in a way that could benefit the plant.

Bigger is better: honeybee colonies as distributed information-gathering systems.

In collectively foraging groups, communication about food resources can play an important role in the organization of the group's activity. For example, the honeybee dance communication system allows colonies to selectively allocate foragers among different floral resources according to their quality. Because larger groups can potentially collect more information than smaller groups, they might benefit more from communication because it allows them to integrate and use that information to coordinate forager activity. Larger groups might also benefit more from communication because it allows them to dominate high-value resources by recruiting large numbers of foragers. By manipulating both colony size and the ability to communicate location information in the dance, we show that larger colonies of honeybees benefit more from communication than do smaller colonies. In fact, colony size and dance communication worked together to improve foraging performance; the estimated net gain per foraging trip was highest in larger colonies with unimpaired communication. These colonies also had the earliest peaks in foraging activity, but not the highest ones. This suggests they may find and recruit to resources more quickly, but not more heavily. The benefits of communication we observed in larger colonies are thus likely a result of more effective informationgathering due to massive parallel search rather than increased competitive ability due to heavy recruitment.