Nigel E. Raine

Combined pesticide exposure severely affects individual- and colony-level traits in bees

Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production. Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations . Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour and reductions in colony queen production. However, the key link between changes in individual behaviour and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concentrations can have subtle or sublethal effects at the individual level, it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging, yet the possible combinatorial effects of pesticide exposure have rarely been investigated. Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.

Speed–accuracy tradeoffs in animal decision making

The traditional emphasis when measuring performance in animal cognition has been overwhelmingly on accuracy, independent of decision time. However, more recently, it has become clear that tradeoffs exist between decision speed and accuracy in many ecologically relevant tasks, for example, prey and predator detection and identification; pollinators choosing between flower species; and spatial exploration strategies. Obtaining high-quality information often increases sampling time, especially under noisy conditions. Here we discuss the mechanisms generating such speed-accuracy tradeoffs, their implications for animal decision making (including signalling, communication and mate choice) and the significance of differences in decision strategies among species, populations and individuals. The ecological relevance of such tradeoffs can be better understood by considering the neuronal mechanisms underlying decision-making processes.

A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators

There is evidence that in Europe and North America many species of pollinators are in decline, both in abundance and distribution. Although there is a long list of potential causes of this decline, there is concern that neonicotinoid insecticides, in particular through their use as seed treatments are, at least in part, responsible. This paper describes a project that set out to summarize the natural science evidence base relevant to neonicotinoid insecticides and insect pollinators in as policy-neutral terms as possible. A series of evidence statements are listed and categorized according to the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

The correlation of learning speed and natural foraging success in bumble-bees

Despite the widespread assumption that the learning abilities of animals are adapted to the particular environments in which they operate, the quantitative effects of learning performance on fitness remain virtually unknown. Here, we evaluate the learning performance of bumble-bees (Bombus terrestris) from multiple colonies in an ecologically relevant associative learning task under laboratory conditions, before testing the foraging performance of the same colonies under the field conditions. We demonstrate that variation in learning speed among bumble-bee colonies is directly correlated with the foraging performance, a robust fitness measure, under natural conditions. Colonies vary in learning speed by a factor of nearly five, with the slowest learning colonies collecting 40% less nectar than the fastest learning colonies. Such a steep fitness function is suggestive of strong selection for higher learning speed. Partial correlation analysis reveals that other factors such as forager body size or colour preference appear to be negligible in our study. Although our study does not directly prove causality of learning on foraging success, our approach of correlating natural within-species variation in these two factors represents a major advance over traditional between-species correlative analyses where comparability can be compromised by the fact that species vary along multiple dimensions.

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).

The Adaptive Significance of Sensory Bias in a Foraging Context: Floral Colour Preferences in the Bumblebee Bombus terrestris

Innate sensory biases could play an important role in helping naïve animals to find food. As inexperienced bees are known to have strong innate colour biases we investigated whether bumblebee (Bombus terrestris) colonies with stronger biases for the most rewarding flower colour (violet) foraged more successfully in their local flora. To test the adaptive significance of variation in innate colour bias, we compared the performance of colour-naïve bees, from nine bumblebee colonies raised from local wild-caught queens, in a laboratory colour bias paradigm using violet (bee UV-blue) and blue (bee blue) artificial flowers. The foraging performance of the same colonies was assessed under field conditions. Colonies with a stronger innate bias for violet over blue flowers in the laboratory harvested more nectar per unit time under field conditions. In fact, the colony with the strongest bias for violet (over blue) brought in 41% more nectar than the colony with the least strong bias. As violet flowers in the local area produce more nectar than blue flowers (the next most rewarding flower colour), these data are consistent with the hypothesis that local variation in flower traits could drive selection for innate colour biases.

Adaptation, Genetic Drift, Pleiotropy, and History in the Evolution of Bee Foraging Behavior

Publisher Summary This chapter focuses on the following traits: flower constancy, floral color preference, learning behavior, traplining, and communication about food sources. Aristotle observed, ‘‘During each flight the bee does not settle on flowers of different kinds, but flies, as it were, from violet to violet, and touches no other till it returns to the hive’’. This phenomenon, now termed “flower constancy”, is defined as “An individual insect is flower constant if it visits only a restricted number of flower species, even if other species are available and equally rewarding, and if the insect has no innate or imprinted predisposition to visit only flowers of a restricted plant taxon, which must be confirmed by the observation that other individuals of the same insect species visit other plant species within the same array.” Comparisons between species can be more rewarding when we compare many closely related species of known phylogeny. Comparisons between populations of the same species are attractive because they reveal the patterns of adaptation among very closely related individuals operating under divergent ecological conditions. A rarely used but potentially powerful method of testing the adaptiveness of a (foraging) behavior is by testing an animals (foraging) performance under natural conditions in its native habitat and then transplanting this animal into a second animals native environment and re-testing its performance. One possible approach to studying the adaptive significance of a foraging strategy is to manipulate the environment in such a way that the foraging strategy cannot be used. In behavioral ecology, two types of models have traditionally been used to study adaptation. The chapter illustrates the value of a number of approaches taken from the toolbox of the modern evolutionary biologist, which can be used to study the adaptive nature of foraging behavior.

Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure

Summary 1. Insect pollination is a vital ecosystem service that maintains biodiversity and sustains agricultural crop yields. Social bees are essential insect pollinators, so it is concerning that their populations are in global decline. 2. Although pesticide exposure has been implicated as a possible cause for bee declines, we currently have a limited understanding of the risk these chemicals pose. Whilst environmental exposure to pesticides typically has non-lethal effects on individual bees, recent reports suggest that sublethal exposure can affect important behavioural traits such as foraging. However, at present, we know comparatively little about how natural foraging behaviour is impaired and the relative impacts of acute and chronic effects. 3. Using Radio-Frequency Identification (RFID) tagging technology, we examined how the day-to-day foraging patterns of bumblebees (Bombus terrestris) were affected when exposed to either a neonicotinoid (imidacloprid) and/or a pyrethroid (k-cyhalothrin) independently and in combination over a four-week period. This is the first study to provide data on the impacts of combined and individual pesticide exposure on the temporal dynamics of foraging behaviour in the field over a prolonged period of time. 4. Our results show that neonicotinoid exposure has both acute and chronic effects on overall foraging activity. Whilst foragers from control colonies improved their pollen foraging performance as they gained experience, the performance of bees exposed to imidacloprid became worse: chronic behavioural impairment. We also found evidence, suggesting that pesticide exposure can change forager preferences for the flower types from which they collect pollen. 5. Our findings highlight the importance of considering prolonged exposure (which happens in the field) when assessing the risk that pesticides pose to bees. The effects of chronic pesticide exposure could have serious detrimental consequences for both colony survival and also the pollination services provided by these essential insect pollinators.

Chronic sublethal stress causes bee colony failure

Current bee population declines and colony failures are well documented yet poorly understood and no single factor has been identified as a leading cause. The evidence is equivocal and puzzling: for instance, many pathogens and parasites can be found in both failing and surviving colonies and field pesticide exposure is typically sublethal. Here, we investigate how these results can be due to sublethal stress impairing colony function. We mathematically modelled stress on individual bees which impairs colony function and found how positive density dependence can cause multiple dynamic outcomes: some colonies fail while others thrive. We then exposed bumblebee colonies to sublethal levels of a neonicotinoid pesticide. The dynamics of colony failure, which we observed, were most accurately described by our model. We argue that our model can explain the enigmatic aspects of bee colony failures, highlighting an important role for sublethal stress in colony declines.

Pollination ecology of acacias (Fabaceae, Mimosoideae)

We review the pollination ecology of acacias worldwide, discussing (1) the rewards provided to flower visitors, (2) the temporal patterns of flowering and reward provision and (3) the taxonomic composition of flower visitor assemblages. The flowers of most acacias (including all members of the subgenus Phyllodineae) offer only pollen to flower visitors and floral nectar is limited to a minority of species in the subgenera Acacia and Aculeiferum. The most important pollinators of acacias are social and solitary bees, although other insects and nectar-feeding birds are important in specific cases. Acacias that secrete nectar attract far more species-rich assemblages of flower visitors, although many of these are probably not important as pollinators. Most acacias in the subgenus Phyllodineae have long-lived protogynous flowers, without clear daily patterns in reward provision and visitation. In contrast, most members of the other two subgenera have flowers that last for a single day, appear to be protandrous and have clear daily patterning in reward provision and visitation. The generality of these patterns should not be assumed until the pollination ecology of many more phyllodinous acacias has been studied, particularly in arid environments. The accessibility of the floral rewards in acacia flowers makes them important examples of two general issues in plant communities—the partitioning of shared pollinators and the evolution of floral ant repellents. SBogy as G. N.