How honeybees respond to heat stress from the individual to colony level.

A honey bee colony functions as an integrated collective, with individuals coordinating their behaviour to adapt and respond to unexpected disturbances. Nest homeostasis is critical for colony function; when ambient temperatures increase, individuals switch to thermoregulatory roles to cool the nest, such as fanning and water collection. While prior work has focused on bees engaged in specific behaviours, less is known about how responses are coordinated at the colony level, and how previous tasks predict behavioural changes during a heat stress. Using BeesBook automated tracking, we follow thousands of individuals during an experimentally induced heat stress, and analyse their behavioural changes from the individual to colony level. We show that heat stress causes an overall increase in activity levels and a spatial reorganization of bees away from the brood area. Using a generalized framework to analyse individual behaviour, we find that individuals differ in their response to heat stress, which depends on their prior behaviour and correlates with age. Examining the correlation of behavioural metrics over time suggests that heat stress perturbation does not have a long-lasting effect on an individual's future behaviour. These results demonstrate how thousands of individuals within a colony change their behaviour to achieve a coordinated response to an environmental disturbance.

Sub-lethal but potentially devastating - The novel insecticide flupyradifurone impairs collective brood care in bumblebees.

The worldwide decline in pollinating insects is alarming. One of the main anthropogenic drivers is the massive use of pesticides in agriculture. Risk assessment procedures test pesticides for mortality rates of well-fed, parasite free individuals of a few non-target species. Sublethal and synergistic effects of co-occurring stressors are usually not addressed. Here, we present a simple, wildly applicable bio-essay to assess such effects. Using brood thermoregulation in bumblebee microcolonies as readout, we investigate how this collective ability is affected by long-term feeding exposure to the herbicide glyphosate (5 mg/l), the insecticide flupyradifurone (0.4 mg/l) and the combination of both, when co-occurring with the natural stressor of resource limitation. Documenting brood temperature and development in 53 microcolonies we find no significant effect of glyphosate, while flupyradifurone significantly impaired the collective ability to maintain the necessary brood temperatures, resulting in prolonged developmental times and a decrease in colony growth by over 50 %. This reduction in colony growth has the potential to significantly curtail the reproductive chances of colonies in the field. Our findings highlight the potentially devastating consequences of flupyradifurone use in agriculture even at sub-lethal doses and underline the urgent need for improved risk assessment procedures.

Glyphosate impairs aversive learning in bumblebees.

Agrochemicals represent prominent anthropogenic stressors contributing to the ongoing global insect decline. While their impact is generally assessed in terms of mortality rates, non-lethal effects on fitness are equally important to insect conservation. Glyphosate, a commonly used herbicide, is toxic to many animal species, and thought to impact a range of physiological functions. In this study, we investigate the impact of long-term exposure to glyphosate on locomotion, phototaxis and learning abilities in bumblebees, using a fully automated high-throughput assay. We find that glyphosate exposure had a very slight and transient impact on locomotion, while leaving the phototactic drive unaffected. Glyphosate exposure also reduced attraction towards UV light when blue was given as an alternative and, most strikingly, impaired learning of aversive stimuli. Thus, glyphosate had specific actions on sensory and cognitive processes. These non-lethal perceptual and cognitive impairments likely represent a significant obstacle to foraging and predator avoidance for wild bumblebees exposed to glyphosate. Similar effects in other species could contribute to a widespread reduction in foraging efficiency across ecosystems, driven by the large-scale application of this herbicide. The high-throughput paradigm presented in this study can be adapted to investigate sublethal effects of other agrochemicals on bumblebees or other important pollinator species, opening up a critical new avenue for the study of anthropogenic stressors.

Glyphosate impairs collective thermoregulation in bumblebees.

Insects are facing a multitude of anthropogenic stressors, and the recent decline in their biodiversity is threatening ecosystems and economies across the globe. We investigated the impact of glyphosate, the most commonly used herbicide worldwide, on bumblebees. Bumblebee colonies maintain their brood at high temperatures via active thermogenesis, a prerequisite for colony growth and reproduction. Using a within-colony comparative approach to examine the effects of long-term glyphosate exposure on both individual and collective thermoregulation, we found that whereas effects are weak at the level of the individual, the collective ability to maintain the necessary high brood temperatures is decreased by more than 25% during periods of resource limitation. For pollinators in our heavily stressed ecosystems, glyphosate exposure carries hidden costs that have so far been largely overlooked.

Behavioral flexibility promotes collective consistency in a social insect.

Deciphering the mechanisms that integrate individuals and their behavior into a functional unit is crucial for our understanding of collective behaviors. We here present empirical evidence for the impressive strength of social processes in this integration. We investigated collective temperature homeostasis in bumblebee (Bombus terrestris) colonies and found that bees are less likely to engage in thermoregulatory fanning and do so with less time investment when confronted with heat stress in a group setting than when facing the same challenge alone and that this down-regulation of individual stimulus-response behavior resulted in a consistent proportion of workers in a group engaged in the task of fanning. Furthermore, the bees that comprised the subset of fanning individuals changed from trial to trial and participation in the task was predominately unpredictable based on previous response behavior. Our results challenge basic assumptions in the most commonly used class of models for task allocation and contrast numerous collective behavior studies that emphasize the importance of fixed inter-individual variation for the functioning of animal groups. We demonstrate that bumblebee colonies maintain within-group behavioral heterogeneity and a consistent collective response pattern based on social responsiveness and behavioral flexibility at the individual level.

Interindividual variability in social insects - proximate causes and ultimate consequences.

Individuals within social groups often show consistent differences in behaviour across time and context. Such interindividual differences and the evolutionary challenge they present have recently generated considerable interest. Social insects provide some of the most familiar and spectacular examples of social groups with large interindividual differences. Investigating these within-group differences has a long research tradition, and behavioural variability among the workers of a colony is increasingly regarded as fundamental for a key feature of social insects: division of labour. The goal of this review is to illustrate what we know about both the proximate mechanisms underlying behavioural variability among the workers of a colony and its ultimate consequences; and to highlight the many open questions in this research field. We begin by reviewing the literature on mechanisms that potentially introduce, maintain, and adjust the behavioural differentiation among workers. We highlight the fact that so far, most studies have focused on behavioural variability based on genetic variability, provided by e.g. multiple mating of the queen, while other mechanisms that may be responsible for the behavioural differentiation among workers have been largely neglected. These include maturational, nutritional and environmental influences. We further discuss how feedback provided by the social environment and learning and experience of adult workers provides potent and little-explored sources of differentiation. In a second part, we address what is known about the potential benefits and costs of increased behavioural variability within the workers of a colony. We argue that all studies documenting a benefit of variability so far have done so by manipulating genetic variability, and that a direct test of the effect of behavioural variability on colony productivity has yet to be provided. We emphasize that the costs associated with interindividual variability have been largely overlooked, and that a better knowledge of the cost/benefit balance of behavioural variability is crucial for our understanding of the evolution of the mechanisms underlying the social organization of insect societies. We conclude by highlighting what we believe to be promising but little-explored avenues for future research on how within-colony variability has evolved and is maintained. We emphasize the need for comparative studies and point out that, so far, most studies on interindividual variability have focused on variability in individual response thresholds, while the significance of variability in other parameters of individual response, such as probability and intensity of the response, has been largely overlooked. We propose that these parameters have important consequences for the colony response. Much more research is needed to understand if and how interindividual variability is modulated in order to benefit division of labour, homeostasis and ultimately colony fitness in social insects.

Preimaginal and adult experience modulates the thermal response behavior of ants.

Colonies of social insects display an amazing degree of flexibility in dealing with long-term and short-term perturbations in their environment. The key organizational element of insect societies is division of labor. Recent literature suggests that interindividual variability in response thresholds plays an important role in the emergence of division of labor among workers (reviewed in [1, 2]). Genetic variation can only partly explain the variability among workers. Here we document the effects of both preimaginal and adult thermal experience on the behavioral differentiation of Camponotus rufipes ant workers. We show that preimaginal temperature (22 degrees C or 32 degrees C during pupal stage) affects temperature-response thresholds and temperature preferences of adult brood-tending workers. We further show that brood-carrying experience gathered as adult during several repeated temperature increases modifies thermal behavior. Experienced workers showed a faster transition from first sensing the temperature stimulus to responding with brood translocation. Developmental plasticity of workers provides a colony with flexibility in dealing with thermal variations and constitutes an important mechanism underlying interindividual variability. Adult thermal experience further fine tunes the behavioral response thresholds and reinforces behavioral differentiation among workers.