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Summary: A new study shows that bumblebees learn socially, and this resulted in a novel behavior becoming dominant across a group. These findings highlight the opportunity going forward to use social insects to address how simple cognitive mechanisms can underpin the development of complex behavioral phenomena. [ABSTRACT FROM AUTHOR]

Octopamine has broad roles within invertebrate nervous systems as a neurohormone, neurotransmitter, and neuromodulator. It orchestrates foraging behavior in many insect taxa via effects on feeding, gustatory responsiveness, and appetitive learning. Knowledge of how this biogenic amine regulates bee physiology and behavior is based largely on study of a single species, the honey bee, Apis mellifera. Until recently, its role in the foraging ecology and social organization of diverse bee taxa had been unexplored. Bumble bees (Bombus spp.) are a model for research into the neural basis of foraging and learning, but whether octopamine similarly affects sensory and cognitive performance in this genus is not known. To address this gap, we explored the effects of octopamine on gustatory responsiveness and associative learning in Bombus impatiens via conditioning of the proboscis extension reflex (PER) using a visual (color) cue. We found that octopamine had similar effects on bumble bee behavior as previously reported in honey bees; however, higher doses were required to induce these effects. At this higher dose, octopamine lowered bees’ gustatory responsiveness and appeared to enhance associative learning performance during the early phase of our experiment. Adding to recent studies on stingless bees (Meliponini), these findings support the idea that octopamine’s role in reward perception and processing is broadly conserved across Apidae, while pointing towards some differences across systems worth exploring further. [ABSTRACT FROM AUTHOR]

Animals develop food preferences based on taste, nutritional quality and to avoid environmental toxins. Yet, measuring preferences in an experimental setting can be challenging since ecologically realistic assays can be time consuming, while simplified assays may not capture natural sampling behavior. Field realism is a particular challenge when studying behavioral responses to environmental toxins in lab-based assays, given that toxins can themselves impact sampling behavior, masking our ability to detect preferences. We address these challenges by comparing different experimental methods for measuring sucrose concentration preference in bumble bees (Bombus impatiens), evaluating the utility of two preference chamber-based methods (ad libitum versus a novel restricted-sampling assay) in replicating bees' preferences when they fly freely between artificial flowers in a foraging arena. We find that the restricted-sampling method matched a free-flying scenario more closely than the ad libitum protocol, and we advocate for expanded use of this approach, given its ease of implementation. We then performed a second experiment using the new protocol to ask whether consuming the neonicotinoid pesticide imidacloprid, known to suppress feeding motivation, interfered with the expression of sucrose preferences. After consuming imidacloprid, bees were less likely to choose the higher-quality sucrose even as they gained experience with both options. Thus, we provide evidence that pesticides interfere with bees' ability to discriminate between floral rewards that differ in value. This work highlights a simple protocol for assessing realistic foraging preferences in bees and provides an efficient way for researchers to measure the impacts of anthropogenic factors on preference expression. [ABSTRACT FROM AUTHOR]

Females and males often face different sources of selection, resulting in dimorphism in morphological, physiological, and even cognitive traits. Sex differences are often studied in respect to spatial cognition, yet the different ecological roles of males and females might shape cognition in multiple ways. For example, in dietary generalist bumblebees (Bombus), the ability to learn associations is critical to female workers, who face informationally rich foraging scenarios as they collect nectar and pollen from thousands of flowers over a period of weeks to months to feed the colony. While male bumblebees likely need to learn associations as well, they only forage for themselves while searching for potential mates. It is thus less clear whether foraging males would benefit from the same associative learning performance as foraging females. In this system, as in others, cognitive performance is typically studied in lab-reared animals under captive conditions, which may not be representative of patterns in the wild. In the first test of sex and species differences in cognition using wild bumblebees, we compared the performance of Bombus vancouverensis nearcticus (formerly bifarius) and Bombus vosnesenskii of both sexes on an associative learning task at Sierra Nevada (CA) field sites. Across both species, we found that males and females did not differ in their ability to learn, although males were slower to respond to the sucrose reward. These results offer the first evidence from natural populations that male bumblebees may be equally as able to learn associations as females, supporting findings from captive colonies of commercial bees. The observed interspecific variation in learning ability opens the door to using the Bombus system to test hypotheses about comparative cognition. [ABSTRACT FROM AUTHOR]

Systemic insecticides, such as neonicotinoids, are a major contributor towards beneficial insect declines. This has led to bans and restrictions on neonicotinoid use globally, most noticeably in the European Union, where four commonly used neonicotinoids (imidacloprid, thiamethoxam, clothianidin and thiacloprid) are banned from outside agricultural use. While this might seem like a victory for conservation, restrictions on neonicotinoid use will only benefit insect populations if newly emerging insecticides do not have similar negative impacts on beneficial insects. Flupyradifurone and sulfoxaflor are two novel insecticides that have been registered for use globally, including within the European Union. These novel insecticides differ in their chemical class, but share the same mode of action as neonicotinoids, raising the question as to whether they have similar sub-lethal impacts on beneficial insects. Here, we conducted a systematic literature search of the potential sub-lethal impacts of these novel insecticides on beneficial insects, quantifying these effects with a meta-analysis. We demonstrate that both flupyradifurone and sulfoxaflor have significant sub-lethal impacts on beneficial insects at field-realistic levels of exposure. These results confirm that bans on neonicotinoid use will only protect beneficial insects if paired with significant changes to the agrochemical regulatory process. A failure to modify the regulatory process will result in a continued decline of beneficial insects and the ecosystem services on which global food production relies. [ABSTRACT FROM AUTHOR]

Foraging theory assumes that animals assess value based on objective payoffs; however, animals often evaluate rewards comparatively, forming expectations based on recent experience. This form of evaluation may be particularly relevant for nectar foragers such as bumblebees, where individuals can visit thousands of flowers daily that vary in nectar quality. While many animals, including bees, demonstrate reference-based evaluation in experimental contexts, it is unclear whether this occurs in the wild. Here, we asked how daily experience with wildflower nectar influenced wild bumblebees' reward evaluation. We measured the daily nectar concentration of bee-visited wildflowers (Penstemon spp.), before presenting foragers with conspecific flowers filled with a range of artificial nectar concentrations. We recorded bees' acceptance of artificial nectar, the probability of subsequent visits to flowers on the same plant, and residence time. While bees had a minimum threshold of nectar acceptability that was unaffected by experience, when there was higher-concentration environmental nectar, they were less likely to accept lower-quality rewards on manipulated plants. Bees also visited more flowers and stayed longer on plants with higher-concentration nectar. This study shows evidence for both absolute and reference-based evaluation in wild bees and points towards differences between bees' behavior in lab- and wild-foraging contexts. [ABSTRACT FROM AUTHOR]

Learning associations between food-related stimuli and nutrients allows foragers to collect resources efficiently. In turn, the nutrients that foragers consume can themselves affect learning performance, through innate preferences for pre-ingestive stimuli, as well as post-ingestive reinforcement. Bees are insect models of learning and memory, yet the vast majority of this research concerns nectar (carbohydrate) rather than pollen (protein/lipid) rewards, despite the fact that many bees collect both simultaneously. We asked how one component of pollen surface chemistry, a free fatty acid (oleic acid), affected bees' performance in a nectar-learning task. We found that ingestion of oleic acid enhanced visual learning, likely through positive post-ingestive reinforcement. This was supported by our finding that although bees did not prefer to consume the oleic acid solution, its ingestion both decreased motor activity and increased survival. These results are a step towards understanding how nutritionally complex floral rewards may affect cognitive processes that underlie pollination mutualisms. [ABSTRACT FROM AUTHOR]

In their natural environments, most animals must learn about multiple kinds of rewards, both within and across contexts. Despite this, the majority of research on animal learning involves a single reward type. For example, bees are an important model system for the study of cognition and its ecological consequences, but nearly all research to date on their learning concerns a single reward, nectar (carbohydrates), even though foragers often simultaneously collect pollen (protein). Features of learning under more ecologically realistic conditions involving multiple reward types are thus largely unexplored. To address this gap, we compared performance on a colour-learning task when floral surrogates offered bumblebees, Bombus impatiens , a single type of floral reward versus multiple, nutritionally distinct rewards. In one experiment, bees learned a floral association with nectar either alone or while simultaneously collecting pollen. In a reciprocal experiment, bees learned a floral association with pollen either alone or while simultaneously collecting nectar. Bees that collected pollen while learning about nectar did not suffer any detriment to learning which flower colour offered nectar. However, this was not the case for the reciprocal task: collecting nectar impaired bees' ability to learn and remember associations between floral colour and pollen. Our findings offer new insight into how bees learn in relation to ecologically realistic rewards and how cognitive constraints may shape their behaviour under ecologically realistic foraging scenarios. [ABSTRACT FROM AUTHOR]

How foragers cope with complexity in both needs and resources is a major question in behavioral ecology. When faced with nutritionally diverse resources, or when foraging for offspring with divergent nutritional needs, animals must meet the challenge of how to structure their foraging bouts, including what resources to forage for and in what order (how) to collect them. We investigated how nutritional variation in resources and requirements shapes the structure of bumble bee foraging bouts. Bumble bee workers collect 2 nutritionally distinct resources for consumers with different nutritional needs, floral nectar (largely carbohydrates) for their own needs and that of larvae, and pollen (largely protein) that is used primarily by larvae. We maintained colonies of the Eastern Bumble Bee (Bombus impatiens) in the laboratory on either protein-rich or protein-limited diets and assessed bees' foraging bout structure on artificial flowers that offered low, medium, or high ratios of pollen to nectar. We analyzed bout structure using both traditional floral constancy metrics as well as hierarchical Bayesian analyses. Bees from pollen-satiated colonies responded to variation in floral pollen:nectar ratios, tending to collect pollen consecutively when nectar volumes were high. In contrast, foragers from pollen-limited colonies were relatively insensitive to floral reward ratio, tending to collect pollen in long runs regardless of nectar volume. We discuss the implications of these findings for the pollination services that bees provide plants. [ABSTRACT FROM AUTHOR]

Ever since Karl von Frisch's Nobel Prize-winning work in the early 1900s, bees have served as an important model system for the study of learning, memory and foraging behaviour. Bees can learn about floral features including colour, scent, texture and electrostatic charge, and show surprisingly sophisticated forms of learning. However, nearly every study of bee cognition and foraging to date has used a sole reward: nectar, most often in the form of a simple sucrose solution. Plants also offer a number of other rewards to pollinators, the most prevalent being pollen that bees collect as their primary source of protein. Indeed, a significant proportion of angiosperm species are nectarless, rewarding bees with pollen alone. Surprisingly, whether free-flying bees can learn visual features based solely on floral pollen rewards is unknown. Here we show that bees can learn to associate multiple floral features with a pure pollen reward. Furthermore, these associations are remembered long term, comparable to bees' memory for nectar associations. These findings raise new questions about bee learning and the evolutionary history between plants and bee pollinators. [ABSTRACT FROM AUTHOR]

Stress has complex effects on learning and memory, depending on both the type of stress and when the animal experiences it. Honeybees and bumblebees are agriculturally important pollinators for whom the effects of stress are extremely relevant. These pollinators are often transported long distances during which colonies experience severe physical disturbance, causing stress to individuals prior to their release for pollination. Under natural foraging conditions, bees are excellent at learning about the flowers they forage from, including associations between floral stimuli and rewards. However, it is not clear how stress might affect bees’ abilities to learn and remember floral features. Here we address the effects of acute stress on learning and memory in the bumble bee, Bombus impatiens . Using the Proboscis Extension Response (PER) protocol, we look at stress effects on learning and memory in three experiments. After being trained to a conditioned stimulus, we addressed: (1) the effect of 24 h and (2) 30 min of stress on the recall of this learned association and (3) the effect of stress on subsequently learning an association. We found that 24 h of stress after learning appeared to improve memory recall, and there was a trend in the same direction for 30 min of stress. However, bees that were stressed prior to learning an association did not differ from unstressed bees in their ability to learn or remember an association. Our finding that stress has effects on memory in the bumblebee could have implications for their use in behavioral experiments and for promoting the success of both managed and wild populations. [ABSTRACT FROM AUTHOR]

It is assumed that many birds attempt to conceal their nests by using camouflage. To our knowledge, however, no previous experimental studies have explicitly tested this assumption. To explore whether birds choose materials that match the background colors of nest sites to reduce the conspicuousness of their nests, we offered nest-building male Zebra Finches (Taeniopygia guttata) a choice of nest materials that either matched or did not match the color of their nest cup and the surrounding cage walls. Males chose to nest predominantly with material that matched the background color of the cage. To our knowledge, this is the first experimental evidence that birds actively select materials that camouflage their nests. [ABSTRACT FROM AUTHOR]

Across the animal kingdom, many animals build structures. One especially diverse example is that of nest building by birds. It remains unclear, however, what birds know or whether they learn about the structural aspects of the material with which they build a nest. Here we tested whether nest-building male zebra finches would choose the appropriate type of material when building in a novel situation. They did do this: males provided with a nestbox with either a small or a large entrance hole and with nest material of two types (‘long’ and ‘short’) chose the type of material that was appropriate for the box in which they built. Additionally, the birds' material use improved with experience: males building in nestboxes with small entrances became less choosy in their material choice as they became more skilled at inserting material of either length into their nestbox. The birds, therefore, first chose the appropriate materials for the nestbox in which they were building but then modified their handling skills so as to make use of all of the available material. How the cognitive abilities used in this nest-building context compare with those used in solving other physical problems such as tool use tasks is not yet clear. [Copyright &y& Elsevier]

Highlights: [•] It is not always clear why nest-building birds choose the materials they do. [•] We compared nest and food colour preferences in male zebra finches. [•] Birds preferred blue nest material, but had no food colour preferences. [•] It appears that nest material colour preferences are specific to that context. [Copyright &y& Elsevier]

Nests are built by nearly all bird species and can be extremely varied in their structural characteristics, both within and among species. As with a number of other avian behaviours, it seems plausible that early learning might be important in producing adult nest-building behaviour. To examine whether preferences that adults have for nest materials are related to their early-life experience, we experimentally manipulated the colour of the nest in which Zebra Finch pairs built and raised chicks. We then tested these chicks at maturity to determine whether they preferred the colour of the nest from which they had fledged or preferred the same colour as their father. We also examined the overall structure of nests that fathers and their sons built to determine whether the nest a male builds resembles that from which he hatched. When males and females naïve to building were paired as adults and tested for their nest material preferences, they did not prefer the colour of their natal nest. When these males were re-paired and their preference tested a second time, the majority then preferred the colour that their father had preferred (which was also the colour preferred by most of the males). The structural components of a male's nest did not resemble the nest built by his father, but neither did his father's nests resemble each other. We found no evidence that the experience of the nest from which a bird fledges influences his preferences for the colour of nest material or the structure of his first nest. [ABSTRACT FROM AUTHOR]

Whether learning plays a role in nest building in birds is largely unknown. Here we investigated whether the colour of nest materials used to build a first nest affected the subsequent nest material choices made by male zebra finches when building a second nest. Males were tested for their preference for green or brown nest material and then were provided with either their preferred or nonpreferred colour with which to build their first nest. The success of this nesting attempt was manipulated such that half of the breeding pairs had their eggs removed, while the other half were allowed to keep their eggs and fledge chicks. Males were then retested to determine which colour of nest material they now preferred. Males had strong initial preferences for one or other of the two colours of nest material. Males that built a nest with their preferred colour of nest material continued to prefer that colour after nesting, regardless of their breeding success in that nest. However, of the males that built a nest with material of their nonpreferred colour, those that raised and fledged chicks from it subsequently preferred that colour of material for their second nest, while males that suffered a failed breeding attempt did not. Thus breeding experience can influence decisions relating to nest material choice in nest construction in the zebra finch. [Copyright &y& Elsevier]

Novel insecticides are continuously being developed for application in response to increased legal restriction of previously developed insecticides and resistance in target insects. These novel insecticides, such as flupyradifurone (FPF), remain relatively untested on non‐target organisms, including bumblebees. Further, existing tests on honeybees tend to focus on adult mortality and thus sub‐lethal effects, such as impacts on reproductive output, are neglected, despite their importance for population‐level impacts. To address if the novel insecticide FPF has sub‐lethal effects on bumblebee reproduction and behaviour, we established microcolonies and chronically exposed them to field‐realistic concentrations over a 14‐day period. We found that exposure to FPF reduced the bumblebees' reproductive output in terms of the number of larvae produced and the mean mass of each larval instar. FPF‐treated bees also stored less sucrose and constructed fewer honeypots. However, adult bumblebee mortality was similar between control and FPF‐exposed microcolonies. Our results show that field‐realistic FPF exposure leads to increased larval mortality and/or delayed larval development, as well as reduced nectar storage, without affecting adult mortality. Policy implications. Insecticides that impair bumblebee reproduction can have long‐term population‐level consequences, even if adult bees do not experience increased mortality. Despite this fact, sub‐lethal effects, such as impacts on reproduction, are not mandatorily assessed within the regulatory process. Our findings highlight the importance of determining sub‐lethal effects of pesticides across developmental stages, as well as using pollinator species other than honeybees within the regulatory process. [ABSTRACT FROM AUTHOR]

Agricultural intensification has been identified as one of the key causes of global insect biodiversity losses. These losses have been further linked to the widespread use of agrochemicals associated with modern agricultural practices. Many of these chemicals are known to have negative sublethal effects on commercial pollinators, such as managed honeybees and bumblebees, but less is known about the impacts on wild bees. Laboratory‐based studies with commercial pollinators have consistently shown that pesticide exposure can impact bee behavior, with cascading effects on foraging performance, reproductive success, and pollination services. However, these studies typically assess only one chemical, neglecting the complexity of real‐world exposure to multiple agrochemicals and other stressors. In the summer of 2020, we collected wild‐foraging workers of the common eastern bumblebee, Bombus impatiens, from five squash (Cucurbita) agricultural sites (organic and conventional farms), selected to represent a range of agrochemical, including neonicotinoid insecticide, use. For each bee, we measured two behaviors relevant to foraging success and previously shown to be impacted by pesticide exposure: sucrose responsiveness and locomotor activity. Following behavioral testing, we used liquid chromatography–tandem mass spectrometry (LC–MS/MS) chemical analysis to detect and quantify the presence of 92 agrochemicals in each bumblebee. Bees collected from our sites did not vary in pesticide exposure as expected. While we found a limited occurrence of neonicotinoids, two fungicides (azoxystrobin and difenoconazole) were detected at all sites, and the pesticide synergist piperonyl butoxide (PBO) was present in all 123 bees. We found that bumblebees that contained higher levels of PBO were less active, and this effect was stronger for larger bumblebee workers. While PBO is unlikely to be the direct cause of the reduction in bee activity, it could be an indicator of exposure to pyrethroids and/or other insecticides that we were unable to directly quantify, but which PBO is frequently tank‐mixed with during pesticide applications on crops. We did not find a relationship between agrochemical exposure and bumblebee sucrose responsiveness. To our knowledge, this is the first evidence of a sublethal behavioral impact of agrochemical exposure on wild‐foraging bees. [ABSTRACT FROM AUTHOR]

Neonicotinoid insecticides can have sub‐lethal effects on bees which has led to calls from conservationists for a global ban. In contrast, agrochemical companies argue that neonicotinoids do not harm honeybees at field‐realistic levels. However, the focus on honeybees neglects the potential impact on other bee species. We conducted a meta‐analysis to assess whether field‐realistic neonicotinoid exposure has sub‐lethal effects on non‐Apis bees. We extracted data from 53 papers (212 effects sizes) and found that it largely consisted of two genera: bumblebees (Bombus) and mason bees (Osmia), highlighting a substantial taxonomic knowledge gap. Neonicotinoid exposure negatively affected reproductive output across all bees and impaired bumblebee colony growth and foraging. Neonicotinoids also reduced Bombus, but not Osmia, individual development (growth and body size). Our results suggest that restrictions on neonicotinoids should benefit bee populations and highlight that the current regulatory process does not safeguard pollinators from the unwanted consequences of insecticide use. [ABSTRACT FROM AUTHOR]

Over decades, pesticide regulations have cycled between approval and implementation, followed by the discovery of negative effects on nontarget organisms that result in new regulations, pesticides, and harmful effects. This relentless pattern undermines the capacity to protect the environment from pesticide hazards and frustrates end users that need pest management tools. Wild pollinating insects are in decline, and managed pollinators such as honey bees are experiencing excessive losses, which threatens sustainable food security and ecosystem function. An increasing number of studies demonstrate the negative effects of field-realistic exposure to pesticides on pollinator health and fitness, which contribute to pollinator declines. Current pesticide approval processes, although they are superior to past practices, clearly continue to fail to protect pollinator health. In the present article, we provide a conceptual framework to reform cyclical pesticide approval processes and better protect pollinators. [ABSTRACT FROM AUTHOR]

Intensive agriculture is reliant on pesticides to control crop pests, but these chemicals can have negative environmental consequences. This has resulted in repeated calls for pesticide risk assessments to be modified to better protect ecosystem services such as pollination. However, the pesticide licensing process is complex, and consequently there is often confusion between risk assessments where the environmental impact of pesticide use is considered, and risk management where licensing decisions are made. Using bees as a case study, we provide a roadmap for how pesticides are licensed for use in the European Union. By outlining the regulatory process, we highlight key data gaps that need to be addressed to generate a holistic approach to environmental risk assessment. Such an approach is vital to protect pollinators and wildlife more broadly from the unintended consequences of pesticide use. Siviter et al. outline the regulatory process by which pesticides are licenced in the European Union, and highlight gaps that need to be addressed to generate a holistic approach to environmental risk assessment. [ABSTRACT FROM AUTHOR]