Chelsea N. Cook

Cleptobiosis in Social Insects

In this review of cleptobiosis, we not only focus on social insects, but also consider broader issues and concepts relating to the theft of food among animals. Cleptobiosis occurs when members of a species steal food, or sometimes nesting materials or other items of value, either from members of the same or a different species. This simple definition is not universally used, and there is some terminological confusion among cleptobiosis, cleptoparasitism, brood parasitism, and inquilinism. We first discuss the definitions of these terms and the confusion that arises from varying usage of the words. We consider that cleptobiosis usually is derived evolutionarily from established foraging behaviors. Cleptobionts can succeed by deception or by force, and we review the literature on cleptobiosis by deception or force in social insects. We focus on the best known examples of cleptobiosis, the ectatommine ant Ectatomma ruidum, the harvester ant Messor capitatus, and the stingless bee Lestrimellita limão. Cleptobiosis is facilitated either by deception or physical force, and we discuss both mechanisms. Part of this discussion is an analysis of the ecological implications (competition by interference) and the evolutionary effects of cleptobiosis. We conclude with a comment on how cleptobiosis can increase the risk of disease or parasite spread among colonies of social insects.

Social context influences the initiation and threshold of thermoregulatory behaviour in honeybees

Interactions between individuals in a society are the basis of effective task allocation. Division of labour plays a critical role in the ecological efficiency of social insect societies. In this study we tested whether social context, specifically the number of workers present, affects thermoregulatory task performance in honeybees, Apis mellifera. We report here that worker bees assayed singly were significantly less likely to initiate fanning behaviour in response to elevated temperature than bees assayed in small groups of three or 10 workers. Bees assayed in groups also showed lower response thresholds than those assayed alone. The likelihood for fanning behaviour varied significantly among behavioural castes, while thermal response thresholds did not. These results suggest that worker task performance depends on the presence of other workers and offer another method by which division of labour in societies is organized.

Rapidly changing environment modulates the thermoregulatory fanning response in honeybee groups

Social insect societies maintain homeostasis through decentralized collective effort. In quickly changing environments, homeostasis can be difficult, as information may promptly become outdated. How do decentralized social insect groups respond to rapid environmental changes? Honeybee (Apis mellifera L.) workers use thermoregulatory fanning behaviour as part of their repertoire to maintain nest temperatures below 36xa0°C, as larvae can develop malformations and die if temperatures surpass this threshold. Here, we determine whether honeybees alter their fanning behaviour when experiencing different rates of thermal change. We found that honeybee fanners were significantly more likely to fan when experiencing rapidly increasing temperatures, but this response was only seen in larger groups of bees. Additionally, fanners responded at significantly lower temperatures when temperatures were increased quickly, but again, only when they were in larger groups. Our results show a statistically significant interaction between fanning response and group size. These findings illustrate the importance of exploring both response thresholds and probability of response of animals in social groups experiencing changing environments, as both factors affect homeostatic responses. Understanding how self-organized animal societies maintain homeostasis provides insight into decentralized organization across many biological systems.

Larvae influence thermoregulatory fanning behavior in honeybees (Apis mellifera L.)

For many animals, maintaining a specific range of temperatures during offspring development is critical for the survival of the young. While this is most studied in birds and mammals, some insects regulate nest temperatures to create an ideal environment for larval development. Here, we explore the thermoregulatory fanning behavior in honeybees performed to maintain colony temperatures in the presence of larvae. We found that honeybees are more likely to fan when larvae are present, but need direct contact with larvae to fan. We found no evidence that exposure to brood pheromone plays a role in stimulating fanning behavior. Finally, we saw a shift in the fanning response seasonally. These results show that the presence of developing offspring influences the fanning response in honeybees and help us to understand how honeybee colonies achieve the fine thermoregulation necessary for healthy larval development.

Nestmate Recognition in Eusocial Insects: The Honeybee as a Model System

This review summarizes and evaluates the available information on honeybee nestmate recognition. Nestmate recognition is the ability of members of a colony to discriminate members of their own colony from others, particularly conspecifics, trying to enter the nest. Honeybee nestmate recognition is mediated by chemical cues that bees gain after emergence as adults. The comb wax in the nest is an important intermediary for transfer of cues among bees in the colony, resulting in a relatively uniform recognition profile which is carried by workers in the colony. Alkenes and free fatty acids are the primary chemical cues in the recognition profile. The ability of honeybees to discriminate nestmates from non-nestmates has raised the question of whether recognition mechanisms might exist to support nepotism within colonies. A variety of experimental approaches have failed to generate support for preferential behavior among highly related subgroups of bees in honeybee colonies. Other questions addressed in this review include queen recognition, response thresholds for expression of recognition, and sensory and information gathering aspects of the recognition system of honeybees. Nestmate recognition in honeybees is a valuable model system for the study of social recognition in animals.

Individual differences in learning and biogenic amine levels influence the behavioural division between foraging honey bee scouts and recruits

Animals must effectively balance the time they spend exploring the environment for new resources and exploiting them. One way that social animals accomplish this balance is by allocating these two tasks to different individuals. In honeybees, foraging is divided between scouts, which tend to explore the landscape for novel resources, and recruits, which tend to exploit these resources. Exploring the variation in cognitive and physiological mechanisms of foraging behaviour will provide a deeper understanding of how the division of labour is regulated in social insect societies. Here, we uncover how honeybee foraging behaviour may be shaped by predispositions in performance of latent inhibition (LI), which is a form of non-associative learning by which individuals learn to ignore familiar information. We compared LI between scouts and recruits, hypothesizing that differences in learning would correlate with differences in foraging behaviour. Scouts seek out and encounter many new odours while locating novel resources, while recruits continuously forage from the same resource, even as its quality degrades. We found that scouts show stronger LI than recruits, possibly reflecting their need to discriminate forage quality. We also found that scouts have significantly elevated tyramine compared to recruits. Furthermore, after associative odour training, recruits have significantly diminished octopamine in their brains compared to scouts. These results suggest that individual variation in learning behaviour shapes the phenotypic behavioural differences between different types of honeybee foragers. These differences in turn have important consequences for how honeybee colonies interact with their environment. Uncovering the proximate mechanisms that influence individual variation in foraging behaviour is crucial for understanding the ecological context in which societies evolve.

Octopamine and tyramine modulate the thermoregulatory fanning response in honey bees (Apis mellifera)

ABSTRACT Biogenic amines regulate the proximate mechanisms underlying most behavior, including those that contribute to the overall success of complex societies. For honey bees, one crucial set of behaviors contributing to the welfare of a colony is involved with nest thermoregulation. Worker honeybees cool the colony by performing a fanning behavior, the expression of which is largely influenced by response thresholds modulated by the social environment. Here, we examined how changes in biogenic amines affect this group-performed thermoregulatory fanning behavior in honeybees. Concentrations of two biogenic amines, octopamine and tyramine, are significantly lower in active fanners than in non-fanners, but there is no difference in dopamine and serotonin concentrations. Direct feeding of octopamine and tyramine induced a decrease in fanning responses, but only when both amines were included in the treatment. This is the first evidence that fanning behavior is influenced by these two biogenic amines, and this result is consistent with the typical role of these neurotransmitters in regulating locomotor activity in other insects. Individual variation in amine expression also provides a mechanistic link that helps to explain how this group behavior might be coordinated within a colony. Summary: Two biogenic amines, octopamine and tyramine, influence the thermoregulatory fanning behavior in honeybees, highlighting the importance of physiological mechanisms in the organization of social insect societies.

Task allocation and site fidelity jointly influence foraging regulation in honeybee colonies

Variation in behaviour among group members often impacts collective outcomes. Individuals may vary both in the task that they perform and in the persistence with which they perform each task. Although both the distribution of individuals among tasks and differences among individuals in behavioural persistence can each impact collective behaviour, we do not know if and how they jointly affect collective outcomes. Here, we use a detailed computational model to examine the joint impact of colony-level distribution among tasks and behavioural persistence of individuals, specifically their fidelity to particular resource sites, on the collective trade-off between exploring for new resources and exploiting familiar ones. We developed an agent-based model of foraging honeybees, parametrized by data from five colonies, in which we simulated scouts, who search the environment for new resources, and individuals who are recruited by the scouts to the newly found resources, i.e. recruits. We varied the persistence of returning to a particular food source of both scouts and recruits and found that, for each value of persistence, there is a different optimal ratio of scouts to recruits that maximizes resource collection by the colony. Furthermore, changes to the persistence of scouts induced opposite effects from changes to the persistence of recruits on the collective foraging of the colony. The proportion of scouts that resulted in the most resources collected by the colony decreased as the persistence of recruits increased. However, this optimal proportion of scouts increased as the persistence of scouts increased. Thus, behavioural persistence and task participation can interact to impact a colonys collective behaviour in orthogonal directions. Our work provides new insights and generates new hypotheses into how variations in behaviour at both the individual and colony levels jointly impact the trade-off between exploring for new resources and exploiting familiar ones.

Social Behavior and Interactions: Behavioral Ecology

Social animals are ubiquitous on Earth. Here we present reasons for why animals may or may not live in groups and review hypotheses explaining how social behavior evolved. There are many benefits to living in groups with other individuals, including protection from predators or collectively foraging for food that would be unattainable by individuals. While there are many reasons to live in a group there are also associated costs. Living in a group can result in competition for limited resources, such as food and mates. The extent of each benefit and cost in any given environment will determine which species form social groups. The evolution of cooperative behavior, which underlies group living, has been attributed to high genetic relatedness among group members or the benefits it provides one group over others. Uncovering why animals live in groups and how social behavior has evolved are active research questions that are addressed in a range of species from microbes to the largest mammals.