James Jonathan Foster

Skylight polarisation patterns provide a critical navigational cue for many insects. Bees perceive these patterns through specialised ommatidia in the dorsal rim area of their compound eyes, enabling them to estimate the sun’s direction and navigate between food sources and the hive. Although polarisation-based navigation has been extensively studied behaviourally, computational models that link DRA anatomy with navigational performance are lacking. Here, we simulate polarisation vision in honeybees ( Apis mellifera ) and bumblebees ( Bombus terrestris ) using real sky polarisation images to capture biologically relevant skylight properties. Our biologically grounded simulation incorporates species-specific DRA anatomy, including ommatidial optical axis directions, photoreceptor receptive fields, and microvillar orientations. We evaluate navigational accuracy and consistency across sun elevations under two distinct, potentially complementary navigational models: the matched filter, which requires scanning across body orientations to identify the solar axis, and the vector-sum model, which generates instantaneous sun azimuth estimates from a single body orientation, making it independent of active scanning. Matched filter errors in estimating solar axis are below 5° across most sun elevations and in both species. Absolute errors in the vector-sum model are lower for honeybees than bumblebees (median ∼10° and ∼30°, respectively), reflecting differences in DRA anatomy, particularly viewing direction and microvillar arrangement. Both models allow stable course control across most sun elevations in both species, yet the matched filter, being limited to solar axis alignment, only enables positive or negative phototaxis. Overall, this work provides a mechanistic and comparative framework based on realistic DRA anatomy to study polarisation-based navigation, generating testable predictions for insect navigation under natural sky conditions. Author Summary: Many insects, including bees, navigate with the help of skylight polarisation patterns which hold information about the sun’s position even when it is not visible. Bees detect these patterns through the dorsal rim area (DRA) of their complex eyes. How differences in DRA anatomy between bee species translate into differences in navigational ability has remained unclear. Here, we built a biologically realistic simulation of polarisation vision in honeybees and bumblebees. We used real sky images to examine what polarisation information is available to each species. We then tested two models of sun position estimation based on the polarisation pattern: one that requires the bee to actively scan the sky, and one that generates an instantaneous estimate from a single body orientation. In both species, both models show that accurate sun position estimation and stable navigation are possible using just polarisation information under a wide range of sun elevations. Differences in navigational performance between honeybees and bumblebees arise because the two DRAs look at different parts of the sky. Our results provide a robust framework for understanding how DRA anatomy shapes polarisation-based navigation in bees.

When making decisions, animals often rely on multiple cues simultaneously. These provide complementary sources of information, which can increase the accuracy of decisions. In this study, we tested the decision and learning strategies of insects faced with multiple cues in a foraging task, using the bumblebee Bombus terrestris . We presented combinations of visual-only features, as found in natural flowers: colors of varying discriminability, paired with shapes or patterns. We found that the bees relied exclusively on colors when these were easy to discriminate, and did not learn pattern or shape features simultaneously. With harder to discriminate colors, the bees learned both color and shape or pattern features. Our results demonstrate that bumblebees flexibly adjust their learning strategies when presented with visual features of varying discriminability, to balance the investment in learning time and accuracy during multicue learning and decision making. A difference in learning dynamics suggests that blocking could serve as a mechanism to implement this strategy switch.

Artificial light at night (ALAN) is altering nocturnal ecosystems. While the effects of direct light sources on insect behavior are well studied, the influence of large-scale skyglow on migratory orientation remains unclear. Here, we tested how skyglow-induced luminance gradients influence the flight orientation of the fall armyworm, Spodoptera frugiperda, a globally invasive nocturnal migrant that performs seasonal migration in China, using controlled indoor simulations and field assays. Surprisingly, individuals consistently oriented toward darker regions, suggesting that luminance gradients may influence their heading away from the expected seasonal migratory direction. This response was highly consistent across both settings, indicating that skyglow-generated luminance gradients can function as directional cues and potentially interfere with seasonal orientation processes. Such gradients may thus function as ecological traps and represent an underrecognized factor in nocturnal insect navigation. Our findings point to a previously overlooked pathway through which skyglow may affect long-distance orientation in nocturnal migrants, underscoring the need for further work to evaluate its ecological significance within light-polluted environments.

Many insects rely on skylight polarization patterns to navigate their habitats. To perform this vital task, most insect species have evolved specialized ommatidia in the dorsal rim area (DRA) of their compound eyes, which are adapted to detect linearly polarized light in large patches of the sky. In this study, we conducted electrophysiological recordings of ultraviolet-sensitive photoreceptors in the DRA and other regions of the compound eyes in honeybees ( Apis mellifera ) and bumblebees ( Bombus terrestris ) to map their receptive fields (RFs). For both species, we report novel evidence for photoreceptor coupling, i.e. spatial summation, recorded in the retinal layer of the DRA. We explore spatial summation as a possible mechanism to increase the effective size of DRA ommatidia RFs, a crucial functional feature of the polarization compass.

Many insects rely on skylight polarization patterns to navigate their habitats. To perform this vital task, most insect species have evolved specialized ommatidia in the dorsal rim area (DRA) of their compound eyes that are adapted to detect linearly polarized light in large patches of sky. In this study, we conducted electrophysiological recordings of honeybee ( Apis mellifera ) and bumblebee ( Bombus terrestris ) photoreceptors in the DRA and other regions of the compound eye to map their receptive fields. For both species, we report novel evidence for photoreceptor coupling, i.e., spatial summation, present in the retinal layer of the DRA. We explore spatial summation as a possible, eye-region-specific mechanism to increase the effective size of DRA ommatidia receptive fields; a crucial functional feature of the polarization compass.

Like many insects, bumblebees use polarized light (PL) to orient and navigate. The celestial PL pattern is strongest when the sun is close to the horizon, during the dim light of dawn and dusk. In the dim light, the sensitivity of the compound eyes may not be sufficient for detecting PL or landmarks, and it has previously been hypothesized that bumblebees rely on PL from their more sensitive ocelli to navigate at dawn and dusk. Here, we tested this hypothesis using a combination of electrophysiological and behavioural tests. Specifically, we investigate whether bumblebee ocelli can detect PL and explore how the PL contribution from the ocelli and compound eyes is affected by light intensity. We find that bumblebee ocelli do indeed have PL sensitivity and that PL information can be used to guide behaviour in dim light. In bright light, however, both the compound eyes and ocelli are important for the detection of PL. Our results support the hypothesis that bumblebees use PL information from the ocelli at the low light levels that occur around dawn and dusk, and this may support their ability to forage during these periods.

Colourful patterns on flowers are thought to benefit both pollinators and the plants they visit, by increasing the plants' pollination success via an increased foraging efficiency of the pollinators. This increased efficiency is assumed to result from a guidance effect of the flower patterns, correspondingly termed ‘nectar guides’, which indicate the position of the nectary to visiting pollinators, thus reducing their flower handling time. Although it is well established that flower patterns play an important role in flower choice, the mechanisms by which they improve the foraging efficiency of flower‐visiting insects remain poorly understood. In this study, we quantified the contributions of patterns to all phases of flower interaction in the buff‐tailed bumblebee Bombus terrestris. We analysed the bees' flight paths, as well as landing positions and walking tracks on artificial flowers with different pattern types. We reveal that flower patterns reduced the overall flower handling time of the bees by up to 30%, by guiding their approach flight, landing positions and departure decisions. Surprisingly, we observed no improvement in nectary discovery time after the bees landed on the flower. Since we tested experienced foragers, which represent the majority of insect pollinators active in nature, the newly described nectary‐independent guidance effects of flower patterns are of high ecological relevance. Read the free Plain Language Summary for this article on the Journal blog.

The sun is the most prominent source of directional information in the heading direction network of the diurnal, ball-rolling dung beetle Kheper lamarcki. If this celestial body is occluded from the beetle's field of view, the distribution of the relative weight between the directional cues that remain shifts in favour of the celestial pattern of polarised light. In this study, we continue to explore the interplay of the sun and polarisation pattern as directional cues in the heading direction network of K. lamarcki. By systematically altering the intensity and degree of the two cues, we effectively change the relative reliability as they appear to the dung beetle. The response of the beetle to these modifications allows us to closely examine how the weighting relationship of these two sources of directional information is influenced and altered in the heading direction network of the beetle. We conclude that the process by which K. lamarcki relies on directional information is very likely done based on Bayesian reasoning, where directional information conveying the highest certainty at a particular moment is afforded the greatest weight.