Field agrochemical exposure impacts locomotor activity in wild bumblebees.

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.

The sign effect in temporal discounting does not require the hippocampus.

When considering future outcomes, humans tend to discount gains more than losses. This phenomenon, referred to as the temporal discounting sign effect, is thought to result from the greater anticipated emotional impact of waiting for a negative outcome (dread) compared to waiting for a positive outcome (mixture of savoring and impatience). The impact of such anticipatory emotions has been proposed to rely on episodic future thinking. We evaluated this proposal by examining the presence and magnitude of a sign effect in the intertemporal decisions of individuals with hippocampal amnesia, who are severely impaired in their ability to engage in episodic mental simulation, and by comparing their patterns of choices to those of healthy controls. We also measured loss aversion, the tendency to assign greater value to losses compared to equivalent gains, to verify that any reduction in the sign effect in the hippocampal lesion group could not be explained by a group difference in loss aversion. Results showed that participants with hippocampal amnesia exhibited a sign effect, with less discounting of monetary losses compared to gains, that was similar in magnitude to that of controls. Loss aversion, albeit greater in the hippocampal compared to the control group, did not account for the sign effect. These results indicate that the sign effect does not depend on the integrity of hippocampally mediated episodic processes. They suggest instead that the impact of anticipatory emotions can be factored into decisions via semantic future thinking, drawing on non-contextual knowledge about oneself.

Future thinking in PTSD: Preliminary evidence for altered event construction.

Using a future event fluency task, the current study sought to examine future event construction in PTSD and to identify clinical profiles associated with altered event construction. Thirty-eight trauma exposed war-zone veterans with (n=25) and without (n=13) PTSD generated within one minute as many positive and negative future events as possible in the near and distant future. The PTSD group generated fewer specific, but not generic, events than the no-PTSD group, a difference that was amplified for positive events as a result of comorbid depression. Clinical correlates of event construction varied as a function of event valence.

Pollen carryover, pollinator movement, and spatial context impact the delivery of pollination services in apple orchards.

Assessing the relative contributions of different pollinator taxa to pollination services is a central task in both basic eco-evolutionary research and applied conservation and agriculture. To that end, many studies have quantified single-visit pollen deposition and visitation frequency, which together determine a pollinator species' rate of conspecific pollen delivery. However, for plant species that require or benefit from outcrossing, pollination service quality further depends upon the ratio of outcross to self-pollen deposited, which is determined by two additional pollinator traits: pollen carryover and movement patterns among genetically compatible plant individuals. Here, we compare the pollination capacities of managed honey bees, native bumble bees, and native mining bees in apple-a varietally self-incompatible commercial crop-when pollen carryover and pollinator movement patterns are considered. We constructed simulation models of outcross pollen deposition parameterized using empirically measured single-visit pollen deposition, visitation frequency, and probabilities of intertree movement exhibited by each pollinator type, as well as pollen carryover patterns simulated based on parameters reported in the literature. In these models, we also explicitly specified the spatial relationships among cross-compatible trees based on field-realistic orchard layout schemes. We found that estimated pollination service delivery was considerably reduced for all pollinator types when pollen carryover and pollinator movement patterns were considered, as compared to when only single-visit pollen deposition and visitation frequency were considered. We also found that the performance of different pollinator types varied greatly across simulated orchard layout schemes and pollen carryover scenarios, including one instance where bumble and mining bees reversed their relative rankings. In all simulations, native bumble and mining bees outperformed managed honey bees in terms of both outcross pollen delivery per unit time and per flower visited, with disparities being greatest under scenarios of low pollen carryover. We demonstrate the degree to which pollination studies may reach inaccurate conclusions regarding pollination service delivery when pollen carryover and pollinator movement patterns are ignored. Our finding of the strong context dependence of pollination efficiency, even within a single plant-pollinator taxon pair, cautions that future studies in both basic and applied pollination biology should explicitly consider the ecological context in which pollination interactions take place.

Judgement bias may be explained by shifts in stimulus response curves.

Judgement bias, or 'optimism' and 'pessimism', has been demonstrated across many taxa, yet the cognitive mechanisms underlying this behaviour remain unclear. In an optimism paradigm, animals are trained to an association, and, if given a positive experience, behave more favourably towards 'ambiguous' stimuli. We tested whether this effect could be explained by changes to stimulus response gradients by giving bees a task where their response was tested across a wider gradient of stimuli than typically tested. In line with previous work, we found that bees given a positive experience demonstrated judgement bias, being more likely to visit ambiguous stimuli. However, bees were also less likely to visit a stimulus on the other side of the rewarded stimulus (S+), and as such had a shifted stimulus response curve, showing a diminished peak shift response. In two follow-up experiments we tested the hypothesis that our manipulation altered bees' stimulus response curves via changes to the peak shift response by reducing peak shift in controls. We found that, in support of our hypothesis, elimination of peak shift also eliminated differences between treatments. Our results point towards a cognitive explanation of 'optimistic' behaviour in non-human animals and offer a new paradigm for considering emotion-like states.

Verbal recall in amnesia: Does scene construction matter?

The hippocampus plays a critical role in episodic memory and imagination. One theoretical model posits that the hippocampus is important for scene construction, namely, the ability to conjure and maintain a scene-based representation in one's mind. To test one idea put forth by this view, we examined whether amnesia is associated with more severe impairment in memory when the to-be-remembered content places high demands on scene construction. To do so, we examined free recall performance for abstract (i.e., low scene imagery) and concrete, high scene-imagery single words in seven amnesic patients with hippocampal lesions and concomitant scene-construction deficits, and compared their performance to demographically matched healthy controls. As expected, amnesic patients were severely impaired in their free recall performance; however, their impairment did not differ as a function of word type. That is, their impairment was equally severe for words that evoke high versus low scene imagery. These findings suggest that the role of the hippocampus in verbal memory extends to content that does not place high demands on scene construction. Theoretical implications of these findings are discussed.

Peak frequency of the sensorimotor mu rhythm varies with autism-spectrum traits.

Autism spectrum disorder (ASD) is a neurodevelopmental syndrome characterized by impairments in social perception and communication. Growing evidence suggests that the relationship between deficits in social perception and ASD may extend into the neurotypical population. In electroencephalography (EEG), high autism-spectrum traits in both ASD and neurotypical samples are associated with changes to the mu rhythm, an alpha-band (8-12 Hz) oscillation measured over sensorimotor cortex which typically shows reductions in spectral power during both one's own movements and observation of others' actions. This mu suppression is thought to reflect integration of perceptual and motor representations for understanding of others' mental states, which may be disrupted in individuals with autism-spectrum traits. However, because spectral power is usually quantified at the group level, it has limited usefulness for characterizing individual variation in the mu rhythm, particularly with respect to autism-spectrum traits. Instead, individual peak frequency may provide a better measure of mu rhythm variability across participants. Previous developmental studies have linked ASD to slowing of individual peak frequency in the alpha band, or peak alpha frequency (PAF), predominantly associated with selective attention. Yet individual variability in the peak mu frequency (PMF) remains largely unexplored, particularly with respect to autism-spectrum traits. Here we quantified peak frequency of occipitoparietal alpha and sensorimotor mu rhythms across neurotypical individuals as a function of autism-spectrum traits. High-density 128-channel EEG data were collected from 60 participants while they completed two tasks previously reported to reliably index the sensorimotor mu rhythm: motor execution (bimanual finger tapping) and action observation (viewing of whole-body human movements). We found that individual measurement in the peak oscillatory frequency of the mu rhythm was highly reliable within participants, was not driven by resting vs. task states, and showed good correlation across action execution and observation tasks. Within our neurotypical sample, higher autism-spectrum traits were associated with slowing of the PMF, as predicted. This effect was not likely explained by volume conduction of the occipitoparietal PAF associated with attention. Together, these data support individual peak oscillatory alpha-band frequency as a correlate of autism-spectrum traits, warranting further research with larger samples and clinical populations.

Interaction of memory systems is controlled by context in both food-storing and non-storing birds.

Animals and humans have multiple memory systems. While both black-capped chickadees (Poecile atricapillus) and dark-eyed juncos (Junco hyemalis) are under selective pressure to remember reliable long-term spatial locations (habit memory), chickadees must additionally quickly form and rapidly update spatial memory for unique cache sites (one-trial memory). We conducted a series of three experiments in which we assessed the degree to which habit and one-trial memory were expressed in both species as a function of training context. In Experiment 1, birds failed to demonstrate habits on probe trials after being trained in the context of a biased Match-to-Sample task in which the same high-frequency target was always correct. In Experiment 2, habit strongly controlled performance when habits were learned as Discriminations, defining a specific training context. In Experiment 3, context no longer defined when to express habits and habit and one-trial memory competed for control of behavior. Across all experiments, birds preferentially used the memory system at test that was consistent with the context in which it was acquired. Although the memory adaptations that allow chickadees to successfully recover cached food might predispose them to favor one-trial memory, we found no species differences in the weighting of habit and one-trial memory. In the experiments here, context was a powerful factor controlling the interaction of memory systems.

Imidacloprid impairs performance on a model flower handling task in bumblebees (Bombus impatiens).

Bumblebees exposed to neonicotinoid pesticides collect less pollen on foraging trips. Exposed bumblebees are also slower to learn to handle flowers, which may account for reduced pollen collection. It is unclear, however, why neonicotinoid exposure slows learning to handle flowers. We investigated the effect of imidacloprid, a neonicotinoid pesticide, on bumblebee motor learning using a lab model of flower handling. Bumblebees learned to invert inside a narrow tube and lift a petal-shaped barrier to reach a reward chamber. Imidacloprid-exposed bumblebees showed a dose-dependent delay to solve the task, which resulted from reduced switching between behavioural strategies and a subsequent delay in use of the successful strategy. This effect was consistent in colonies exposed at 10 but not 2.6 ppb, suggesting a variable effect on individuals at lower doses. These results help to explain why exposed bumblebees are slow to learn to handle flowers and collect less pollen on foraging trips.

Imidacloprid slows the development of preference for rewarding food sources in bumblebees (Bombus impatiens).

Bee pollination is economically and ecologically vital and recent declines in bee populations are therefore a concern. One possible cause of bee declines is pesticide use. Bumblebees exposed to imidacloprid, a neonicotinoid pesticide, have been shown to be less efficient foragers and collect less pollen on foraging trips than unexposed bees. We investigated whether bumblebees (Bombus impatiens) chronically exposed to imidacloprid at field-realistic levels of 2.6 and 10 ppb showed learning deficits that could affect foraging. Bumblebees were tested for their ability to associate flower colour with reward value in a simulated foraging environment. Bumblebees completed 10 foraging trips in which they collected sucrose solution from artificial flowers that varied in sucrose concentration. The reward quality of each artificial flower was predicted by corolla colour. Unexposed bumblebees acquired a preference for feeding on the most rewarding flower colour on the second foraging trip, while bumblebees exposed at 2.6 and 10 ppb did not until their third and fifth trip, respectively. The delay in preference acquisition in exposed bumblebees may be due to reduced flower sampling and shorter foraging trips. These results show that bumblebees exposed to imidacloprid are slow to learn the reward value of flowers and this may explain previously observed foraging inefficiencies associated with pesticide exposure.

Context controls access to working and reference memory in the pigeon (Columba livia).

The interaction between working and reference memory systems was examined under conditions in which salient contextual cues were presented during memory retrieval. Ambient colored lights (red or green) bathed the operant chamber during the presentation of comparison stimuli in delayed matching-to-sample training (working memory) and during the presentation of the comparison stimuli as S+ and S- cues in discrimination training (reference memory). Strong competition between memory systems appeared when the same contextual cue appeared during working and reference memory training. When different contextual cues were used, however, working memory was completely protected from reference memory interference.

Memory systems interaction in the pigeon: working and reference memory.

Pigeons' performance on a working memory task, symbolic delayed matching-to-sample, was used to examine the interaction between working memory and reference memory. Reference memory was established by training pigeons to discriminate between the comparison cues used in delayed matching as S+ and S- stimuli. Delayed matching retention tests then measured accuracy when working and reference memory were congruent and incongruent. In 4 experiments, it was shown that the interaction between working and reference memory is reciprocal: Strengthening either type of memory leads to a decrease in the influence of the other type of memory. A process dissociation procedure analysis of the data from Experiment 4 showed independence of working and reference memory, and a model of working memory and reference memory interaction was shown to predict the findings reported in the 4 experiments. (PsycINFO Database Record

Contrasting styles in cognition and behaviour in bumblebees and honeybees.

Bumblebees and honeybees have been the subjects of a great deal of recent research in animal cognition. Many of the major topics in cognition, including memory, attention, concept learning, numerosity, spatial cognition, timing, social learning, and metacognition have been examined in bumblebees, honeybees, or both. Although bumblebees and honeybees are very closely related, they also differ in important ways, including social organization, development, and foraging behaviour. We examine whether differences between bumblebees and honeybees in cognitive processes are related to differences in their natural history and behaviour. There are differences in some cognitive traits, such as serial reversal learning and matching-to-sample, that appear related to differences between bumblebees and honeybees in foraging and social behaviour. Other cognitive processes, such as numerosity, appear to be very similar. Despite the wealth of information that is available on some aspects of bumblebee and honeybee cognition and behaviour, there are relatively few instances, however, in which adequate data exist to make direct comparisons. We highlight a number of phenomena, including concept learning, spatial cognition, timing, and metacognition, for which targeted comparative research may reveal unexpected adaptive variation in cognitive processes in these complex animals. This article is part of a Special Issue entitled: In Honor of Jerry Hogan.

Serial reversal learning in bumblebees (Bombus impatiens).

Bumblebees are capable of rapidly learning discriminations, but flexibility in bumblebee learning is less well understood. We tested bumblebees (Bombus impatiens) on a serial reversal learning task. A serial reversal task requires learning of an initial discrimination between two differentially rewarded stimuli, followed by multiple reversals of the reward contingency between stimuli. A reduction in errors with repeated reversals in a serial reversal task is an indicator of behavioural flexibility. Bees were housed in a large indoor environment and tested during foraging flights. Testing free-flying bees allowed for large numbers of trials and reversals. All bees were trained to perform a simultaneous discrimination between two colours for a nectar reward, followed by nine reversals of this discrimination. Results showed that bumblebees reduced errors and improved their performance across successive reversals. A reduction in perseverative errors was the major cause of the improvement in performance. Bees showed a slight increase in error rate in their final trials, perhaps as a consequence of increasing proactive interference, but proactive interference may also have contributed to the overall improvement in performance across reversals. Bumblebees are thus capable of behavioural flexibility comparable to that of other animals and may use proactive interference as a mechanism of behavioural flexibility in varying environments.