Multimodal processing of noisy cues in bumblebees.

Multimodal cues can improve behavioral responses by enhancing the detection and localization of sensory cues and reducing response times. Across species, studies have shown that multisensory integration of visual and olfactory cues can improve response accuracy. However, in real-world settings, sensory cues are often noisy; visual and olfactory cues can be deteriorated, masked, or mixed, making the target cue less clear to the receiver. In this study, we use an associative learning paradigm (Free Moving Proboscis Extension Reflex, FMPER) to show that having multimodal cues may improve the accuracy of bees' responses to noisy cues. Adding a noisy visual cue improves the accuracy of response to a noisy olfactory cue, despite neither the clear nor noisy visual cue being sufficient when paired with a novel olfactory cue. This may provide insight into the neural mechanisms underlying multimodal processing and the effects of environmental change on pollination services.

Compounds without borders: A mechanism for quantifying complex odors and responses to scent-pollution in bumblebees.

AUTHOR SUMMARY: Recent work has indicated that anthropogenic pollution of floral-scent may have negative impacts on bumblebee foraging behavior. We need quantitative tools to both measure how much pollution of a learned floral-odor bumblebees can tolerate and identify which scent-pollutants are problematic. This study used encoding characteristics of insect olfactory systems to develop a new paradigm for quantifying complex odors. This 'Compounds Without Borders' method builds multidimensional vectors of scents based on physiologically relevant physical characteristics of component odorant-compounds. The angular distance between CWB-vectors then provides a single quantitative variable describing how similar (or dissimilar) two complex odors are. This angular representation of odor similarity is predictive of bumblebees' behavior in an associative odor learning task.

The prevalence of olfactory- versus visual-signal encounter by searching bumblebees.

While the phrase 'foraging bumblebee' brings to mind a bumbling bee flying flower to flower in a sunny meadow, foraging is a complicated series of behaviors such as: locating a floral patch; selecting a flower-type; learning handling skills for pollen and nectar extraction; determining when to move-on from a patch; learning within-patch paths (traplining); and learning efficient hive-to-patch routes (spatial navigation). Thus the term 'forager' encompasses multiple distinct behaviors that rely on different sensory modalities. Despite a robust literature on bumblebee foraging behavior, few studies are directly relevant to sensory-guided search; i.e. how workers locate novel patches. The first step in answering this question is to determine what sensory information is available to searching bumblebees. This manuscript presents a computational model that elucidates the relative frequency of visual and olfactory cues that are available to workers searching for floral resources under a range of ecologically relevant scenarios. Model results indicate that odor is the most common sensory cue encountered during search flights. When the likelihood of odor-plume contact is higher, odor-encounter is ubiquitous. While integrative (visual + olfactory) cues are common when foragers are searching for larger flowers (e.g. Echinacea), they become rare when foragers are searching for small flowers (e.g. Penstemon). Visual cues are only encountered in isolation when foragers are seeking large flowers with a low odor-plume contact probability. These results indicate that despite the multisensory nature of floral signals, different modalities may be encountered in isolation during search-behavior, as opposed to the reliably multimodal signals encountered during patch-exploitation or nectar/ pollen acquisition.

The effect of olfactory exposure to non-insecticidal agrochemicals on bumblebee foraging behavior.

Declines in bumblebee populations have led to investigations into potential causes - including agrochemical effects on bumblebee physiology. The indirect effects of agrochemicals (i.e. behavior modulation) have been postulated, but rarely directly tested. Olfactory information is critical in mediating bumblebee-floral interactions. As agrochemicals emit volatiles, they may indirectly modify foraging behavior. We tested the effects of olfactory contamination of floral odor by agrochemical scent on foraging activity of Bombus impatiens using two behavioral paradigms: localization of food within a maze and forced-choice preference. The presence of a fungicide decreased bumblebees' ability to locate food within a maze. Additionally, bumblebees preferred to forage in non-contaminated feeding chambers when offered a choice between control and either fertilizer- or fungicide-scented chambers.

Responses of descending visually-sensitive neurons in the hawkmoth, Manduca sexta, to three-dimensional flower-like stimuli.

Hawkmoths rely on vision to track moving flowers during hovering-feeding bouts. Visually guided flight behaviors require a sensorimotor transformation, where motion information processed by the optic ganglia ultimately modifies motor axon activity. While a great deal is known about motion processing in the optic lobes of insects, there has been far less exploration into the visual information available to flight motor axons. Visual information recorded at this stage has likely arisen from multiple visual pathways, and has potentially been modified by outside sensory information. As a first step, understanding the sensorimotor transformation from transduction of moving flower signals to active flower tracking behavior requires that the visual information available to the thoracic flight control centers be assayed. This paper investigated the response of descending visually sensitive neurons in the cervical connectives of the hawkmoth, Manduca sexta L. (Lepidoptera: Sphingidae), to flower-like stimuli. Because flower structure lends itself to oscillatory (vibratory) motion, the stimuli used in these experiments were discs oscillating in each axis of motion (horizontal, vertical, and looming). Object-sensitive descending-neurons (OSDNs) respond to multiple directions of object motion and do not clearly sort into classes of directional tuning. The broad spatial distribution of directional sensitivities exhibited by OSDNs indicates that the direction of object motion may be encoded on a population scale. Although OSDNs exhibit broad frequency response curves, over the range of frequencies that M. sexta are able to track (0-2 Hz) OSDNs exhibit monotonically increasing response. Additionally, OSDNs respond to discs oscillating at frequencies as high at 6 Hz, indicating that the visual information being sent to thoracic motor control centers is not likely the limiting factor in flower tracking ability.

Neural mechanisms underlying target detection in a dragonfly centrifugal neuron.

Visual identification of targets is an important task for many animals searching for prey or conspecifics. Dragonflies utilize specialized optics in the dorsal acute zone, accompanied by higher-order visual neurons in the lobula complex, and descending neural pathways tuned to the motion of small targets. While recent studies describe the physiology of insect small target motion detector (STMD) neurons, little is known about the mechanisms that underlie their exquisite sensitivity to target motion. Lobula plate tangential cells (LPTCs), a group of neurons in dipteran flies selective for wide-field motion, have been shown to take input from local motion detectors consistent with the classic correlation model developed by Hassenstein and Reichardt in the 1950s. We have tested the hypothesis that similar mechanisms underlie the response of dragonfly STMDs. We show that an anatomically characterized centrifugal STMD neuron (CSTMD1) gives responses that depend strongly on target contrast, a clear prediction of the correlation model. Target stimuli are more complex in spatiotemporal terms than the sinusoidal grating patterns used to study LPTCs, so we used a correlation-based computer model to predict response tuning to velocity and width of moving targets. We show that increasing target width in the direction of travel causes a shift in response tuning to higher velocities, consistent with our model. Finally, we show how the morphology of CSTMD1 allows for impressive spatial interactions when more than one target is present in the visual field.

Flower tracking in hawkmoths: behavior and energetics.

As hovering feeders, hawkmoths cope with flower motions by tracking those motions to maintain contact with the nectary. This study examined the tracking, feeding and energetic performance of Manduca sexta feeding from flowers moving at varied frequencies and in different directions. In general we found that tracking performance decreased as frequency increased; M. sexta tracked flowers moving at 1 Hz best. While feeding rates were highest for stationary flowers, they remained relatively constant for all tested frequencies of flower motion. Calculations of net energy gain showed that energy expenditure to track flowers is minimal compared to energy intake; therefore, patterns of net energy gain mimicked patterns of feeding rate. The direction effects of flower motion were greater than the frequency effects. While M. sexta appeared equally capable of tracking flowers moving in the horizontal and vertical motion axes, they demonstrated poor ability to track flowers moving in the looming axis. Additionally, both feeding rates and net energy gain were lower for looming axis flower motions.