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The corneal projection (CP) of compound eyes. (A) The CP of each bee's left eye shown on a sphere representing the world. (B) A sinusoidal projection and analysis of the CPs (iii). Profiles of integrated CP are shown across elevation (panel Bi, the integral of all azimuth points in the CP as a function of elevation) and azimuth (panel Bii, the integral of all elevation points in the CP as a function of azimuth) and are expressed as a percentage Figure 4 continued on next page
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The quality of visual information that is available to an animal is limited by the size of its eyes. Differences in eye size can be observed even between closely related individuals, yet we understand little about how this affects vision. Insects are good models for exploring the effects of size on visual systems because many insect species exhibit...
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... CP increases with bumblebee eye size ( Figure 2C), but it appears that this increase does not result from simply enlarging the CP in all directions ( Figure 4A,B). The dorsolateral limit of the CP of each eye is relatively consistent (between 30˚to30˚30˚to 60˚elevation60˚60˚elevation (el.) and À90˚toÀ90˚À90˚to À60åzimuthÀ60åzimuth (az. - Azimuth), Figure 4B), while bigger bees appear to enlarge their CP dorsofrontally (between 0 ˚ to 90˚el90˚90˚el. ...
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... CP increases with bumblebee eye size ( Figure 2C), but it appears that this increase does not result from simply enlarging the CP in all directions ( Figure 4A,B). The dorsolateral limit of the CP of each eye is relatively consistent (between 30˚to30˚30˚to 60˚elevation60˚60˚elevation (el.) and À90˚toÀ90˚À90˚to À60åzimuthÀ60åzimuth (az. - Azimuth), Figure 4B), while bigger bees appear to enlarge their CP dorsofrontally (between 0 ˚ to 90˚el90˚90˚el. and À15˚toÀ15˚À15˚to 75˚(75˚75˚(az. ...
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... When the CP of each bee's right eye is also considered, it is apparent that all bees have regions of binocular CP overlap ( Figure 4C) that increase in angular area with eye size ( Figure 2C). Increasing binocularity is primarily observed dorsofrontally (between 30˚to30˚ 30˚to 90˚el90˚90˚el. ...
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... À75˚toÀ75˚À75˚to 75˚(75˚75˚(az. -Azimuth), Figure 4C), but a wedge of binocularity is also observed facing directly forwards (between À30˚toÀ30˚À30˚to 30˚el30˚30˚el. and À15˚toÀ15˚À15˚to 15˚(15˚15˚(az. ...
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... As for panel B but showing the topology (indicated by the blue-black color gradient bar) and profiles of average facet diameter. Squares denote bumblebees and circles denote honeybees in panels A and C, and a power function was fitted to the Bombus measurements for the parameters in these panels (Supplementary file 1- Table S1) Figure 4C). Arguably, maps of scaling exponents provide a clearer of the total number of points. ...
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... of honeybee eyes are that their values for corneal lens thickness are distinctly lower than those for all bumblebees ( Figure 3- figure supplement 2A), and that the extent of their binocular overlap is also smaller than that for to medium-sized Bombus ( Figure 2C). The CPs of honeybees were also shifted dorsoposteriorly relative to those of bumblebees ( Figure 4A,B), while their binocular CP overlap is limited to their dorsal visual field and does not extend frontally ( Figure 4C). After account- ing for the differences in their visual fields, the projected topologies of the honeybees are similar to those of medium-sized bumblebees but with two differences: first, honeybees have an obvious increase in retinal thickness in their lateral visual field (Figure 5Bii, À120˚toÀ120˚À120˚to À75˚(À75˚À75˚(az. ...
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... of honeybee eyes are that their values for corneal lens thickness are distinctly lower than those for all bumblebees ( Figure 3- figure supplement 2A), and that the extent of their binocular overlap is also smaller than that for to medium-sized Bombus ( Figure 2C). The CPs of honeybees were also shifted dorsoposteriorly relative to those of bumblebees ( Figure 4A,B), while their binocular CP overlap is limited to their dorsal visual field and does not extend frontally ( Figure 4C). After account- ing for the differences in their visual fields, the projected topologies of the honeybees are similar to those of medium-sized bumblebees but with two differences: first, honeybees have an obvious increase in retinal thickness in their lateral visual field (Figure 5Bii, À120˚toÀ120˚À120˚to À75˚(À75˚À75˚(az. ...
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... also identified an area of binocular overlap not previously reported in bumblebees. The extent of this corneal binocular overlap, directed both fron- tally and dorsofrontally ( Figure 4C), increased rapidly with body size. Bumblebee workers have been found to approach artificial ( Reber et al., 2016) and natural flowers (Orth and Waddington, 1997) from below, which would place the visual target dorsofrontally, in a region where we also found that IF angle decreases with eye size ( Figure 6A). ...
Citations
... Like most insects, they guide their flight visually with apposition eyes that are typically adapted for vision under bright light [1]. Activity in low light is limited by the sensitivity and capacity of their eyes and visual system [2,3]. While natural dim-light behaviour has previously been described in solitary bees [4][5][6] and honeybees [2], until recently there was no more than qualitative evidence of bumblebee activity in such conditions. ...
... A larger body size correlates with larger eyes [23] and greater visual sensitivity [3], therefore the size of a forager determines its experience of lower light conditions [24]. Alongside other factors relating to size including temperature regulation [25] and memory [22], differing visual sensitivities may result in foragers making different decisions in similar light conditions. ...
Only a few diurnal animals, such as bumblebees, extend their activity into the time around sunrise and sunset when illumination levels are low. Low light impairs viewing conditions and increases sensory costs, but whether diurnal insects use low light as a cue to make behavioural decisions is uncertain. To investigate how they decide to initiate foraging at these times of day, we observed bumblebee nest-departure behaviours inside a flight net, under naturally changing light conditions. In brighter light bees did not attempt to return to the nest and departed with minimal delay, as expected. In low light the probability of non-departures increased, as a small number of bees attempted to return after spending time on the departure platform. Additionally, in lower illumination bees spent more time on the platform before flying away, up to 68 s. Our results suggest that bees may assess light conditions once outside the colony to inform the decision to depart. These findings give novel insights into how behavioural decisions are made at the start and the end of a foraging day in diurnal animals when the limits of their vision impose additional costs on foraging efficiency.
... The μCT method has recently been used to measure angles and other eye parameters in bees (Taylor et al., 2019) and ommatidial diameters in other compound eyes (Currea et al., 2023), but our method using the 32-ID beamline achieves ~18× or ~ 170× greater resolution respectively, and imaging speeds of ~1 mm 3 /30 min. This enhanced resolution combined with our novel embedding method allows for greater automated throughput. ...
Comparative anatomy is an important tool for investigating evolutionary relationships among species, but the lack of scalable imaging tools and stains for rapidly mapping the microscale anatomies of related species poses a major impediment to using comparative anatomy approaches for identifying evolutionary adaptations. We describe a method using synchrotron source micro‐x‐ray computed tomography (syn‐μXCT) combined with machine learning algorithms for high‐throughput imaging of Lepidoptera (i.e., butterfly and moth) eyes. Our pipeline allows for imaging at rates of ~15 min/mm³ at 600 nm³ resolution. Image contrast is generated using standard electron microscopy labeling approaches (e.g., osmium tetroxide) that unbiasedly labels all cellular membranes in a species‐independent manner thus removing any barrier to imaging any species of interest. To demonstrate the power of the method, we analyzed the 3D morphologies of butterfly crystalline cones, a part of the visual system associated with acuity and sensitivity and found significant variation within six butterfly individuals. Despite this variation, a classic measure of optimization, the ratio of interommatidial angle to resolving power of ommatidia, largely agrees with early work on eye geometry across species. We show that this method can successfully be used to determine compound eye organization and crystalline cone morphology. Our novel pipeline provides for fast, scalable visualization and analysis of eye anatomies that can be applied to any arthropod species, enabling new questions about evolutionary adaptations of compound eyes and beyond.
... Besides acting as a heat source, the light from the sun is necessary for bee navigation (Reber et al., 2015). Eye size allometry is established in honeybees (Streinzer et al., 2013;Taylor et al., 2019): the larger eye of bumblebees allows them to see in lower light conditions, which could explain the larger effect of solar radiation on honeybee activity and the lack of an effect on bumblebees. Reduced honeybee activity observed at lower solar radiation could be due to low sunlight in the morning or reduced visibility in cloudy conditions. ...
Migratory beekeeping increases honey production and reduces the feeding costs of stationary beekeeping during longer dearth periods. This study discerns the influence of environmental conditions on the foraging behavior of the Indian honey bee, Apis cerana indica F., at different migratory sites in Southern India. The total number of foraging bees, pollen foraging efficiency, and nectar foraging efficiency were estimated. Furthermore, the influence of environmental factors, including temperature, relative humidity, rainfall, and solar radiation, was recorded to identify its impact on the foraging behavior of honey bees. Among the climatic factors, maximum temperature (>30 °C) was the most crucial, negatively affecting bee activity with correlation coefficients of -0.83, -0.34, and -0.33 for outgoing bees, nectar, and pollen collectors, respectively. The relative humidity showed a positive impact on the frequency of worker bees moving out of the hive (r = 0.79), those coming in with nectar (r = 0.27), and pollen (r = 0.29). Rainfall hampered foraging activity, while solar radiation was found to have no significant effect on bee activity. Diurnal variations showed peak activity of bee foragers between 6.00 and 10.00 am. The visits by honey bees were significantly higher at low temperatures, solar radiation, precipitation, and high relative humidity. They made about 90% of their flower visits in the early morning, although plenty of bee flora was available throughout the day. Also, the environmental conditions at different sites strongly influenced the foraging behavior. However, the honey bees still focused their activities on favorable conditions depending on their biology and fixed their daily foraging patterns, improving beekeeping and honey production throughout the year.
... If the wing was slightly rolled up at the tip or slightly wrinkled, it was flattened carefully and taped to the paper. The left half of the head (including the compound eye) was dissected and placed in 75% ethanol before being stained with 0.5% phosphotungstic acid (PTA), dehydrated in an ethanol series and embedded in epoxy resin, following the methods described in Taylor et al. (2019). The head samples were scanned at the TOMCAT beamline of the Swiss Light Source, Paul Scherrer Institute, Villigen (Switzerland) (beamtime number 20190641) with monochromatic X-ray beam set to 20 keV energy. ...
... Spatial acuity and contrast sensitivity can be measured using many methods. In compound eyes (the most common eye type in arthropods) spatial acuity is often calculated from anatomical information such as the distribution and density of photoreceptors ( particularly inter-ommatidial angle; Land, 1997;Snyder et al., 1977;Stavenga, 2003), using the pseudopupil analytical approach (Horridge, 1978;Land, 1997;Rigosi et al., 2021;Stavenga, 1979) or (more recently) by using micro-computed tomography (microCT)-based 3D reconstruction techniques (Bagheri et al., 2020;Taylor et al., 2019). Anatomical methods can provide a detailed estimation of visual acuity across the full visual field of animals. ...
Most animals rely on visual information for a variety of everyday tasks. The information available to a visual system depends in part on its spatial resolving power and contrast sensitivity. Due to their competing demands for physical space within an eye, these traits cannot simultaneously be improved without increasing overall eye size. The contrast sensitivity function is an integrated measure of visual performance that measures both resolution and contrast sensitivity. Its measurements helps us identify how different species have made a trade-off between contrast sensitivity and spatial resolution. It further allows us to identify the evolutionary drivers of sensory processing and visually mediated behaviour. Here, we measured the contrast sensitivity function of the fiddler crab Gelasimus dampieri using their optokinetic responses to wide-field, moving, sinusoidal intensity gratings of different orientations, spatial frequencies, contrasts, and speeds. We further tested whether the behavioural state of the crabs (i.e. whether crabs are actively walking or not) affects their optokinetic gain and contrast sensitivity. Our results from a group of five crabs suggest a minimum perceived contrast of 6%, and a horizontal and vertical visual acuity of 0.4 cyc/deg and 0.28 cyc/deg respectively in the crabs’ region of maximum optomotor sensitivity. Optokinetic gain increased in moving crabs compared to restrained crabs, adding another example of the importance of naturalistic approaches when studying the performance of animals.
... ThermoFisher Scientific, Waltham, MA, USA) using a combination of segmenting tools that included thresholding, brush, fill, shrink, and grow. The surface area of the compound eye was obtained by generating a surface from its segmented label [72]. ...
... The compound eye also correlated positively with body size (t 12 = 7.137, p < 0.001, n = 20, regression analysis). This result is consistent with the findings of Taylor et al. [72] and suggests that the variation of eye size with body size likely affects visual capabilities such as resolution and sensitivity in B. terrestris. This, in turn, is likely to affect visually guided behavior, such as the timing of activity [74,75]. ...
... related positively with body size (t12 = 7.137, p < 0.001, n = 20, regression analysis). This result is consistent with the findings of Taylor et al. [72] and suggests that the variation of eye size with body size likely affects visual capabilities such as resolution and sensitivity in B. terrestris. This, in turn, is likely to affect visually guided behavior, such as the timing of activity [74,75]. ...
Polarized light-based navigation in insects is facilitated by a polarization-sensitive part of the eye, the dorsal rim area (DRA). Existing methods to study the anatomy of the DRA are destructive and time-consuming. We presented a novel method for DRA localization, dissection, and measurement using 3D volumetric images from X-ray micro-computed tomography in combination with 2D photographs. Applying the method on size-polymorphic buff-tailed bumblebees, Bombus terrestris, we found that the DRA was easily obtainable from photographs of the dorsal eye region. Allometric analysis of the DRA in relation to body size in B. terrestris showed that it increased with the body size but not at the same rate. By localizing the DRA of individual bumblebees, we could also perform individual-level descriptions and inter-individual comparisons between the ommatidial structures (lens, crystalline cones, rhabdoms) of three different eye regions (DRA, non-DRA, proximate to DRA). One feature distinct to the bumblebee DRA was the smaller dimension of the crystalline cones in comparison to other regions of the eye. Using our novel methodology, we provide the first individual-level description of DRA ommatidial features and a comparison of how the DRA varies with body size in bumblebees.
... Insects perform sinuous movements when exploring their environments, such arcs, loops, and zigzags. During these movements, the insects turn back and look at the goal (Lehrer 1991(Lehrer , 1993 or surrounding structure, such as objects (Lobecke et al. 2018), placing the goal or surrounding structure at the highest acuity zone of their visual field (Taylor et al. 2019). We will explore how these movements might support the learning of two duos: path integration and local homing, and path integration and route-following. ...
Hymenopterans, such as bees and wasps, have long fascinated researchers with their sinuous movements at novel locations. These movements, such as loops, arcs, or zigzags, serve to help insects learn their surroundings at important locations. They also allow the insects to explore and orient themselves in their environment. After they gained experience with their environment, the insects fly along optimized paths guided by several guidance strategies, such as path integration, local homing, and route-following, forming a navigational toolkit. Whereas the experienced insects combine these strategies efficiently, the naive insects need to learn about their surroundings and tune the navigational toolkit. We will see that the structure of the movements performed during the learning flights leverages the robustness of certain strategies within a given scale to tune other strategies which are more efficient at a larger scale. Thus, an insect can explore its environment incrementally without risking not finding back essential locations.
... With each bee observation, we included measurements of light and temperature to assess the potential association of these variables with species identity and traits [27,28]. We related our observations to key morphological traits including body size, which relates to both bees' eye size [22,29,30] and thermoregulatory ability [31,32]. In addition, we related observations to the eye parameter trait, which relates to the trade-off between light sensitivity and resolution that comes with facetted eyes [33]. ...
... Body size, measured as inter-tegular distance (ITD, in mm), was assumed to be related to bumblebee thermoregulatory ability, with larger individuals being more cold tolerant [31,32]. Body size relates allometrically to eye size (on a log-log scale, R 2 = 0.91 for eye area and 0.95 for eye volume, respectively; [30]; figure 1b) (1) Body size can serve as a proxy for both eye size (as eye and body size are allometrically related) and thermoregulatory ability (surface-to-volume relationship). ...
... This choice was supported by a fourth-corner analysis, where the eye parameter was significantly correlated to light intensity, while the inter-ommatidial angle and the facet area were not. To obtain the eye parameter for different species [2], we used measurements taken on bumblebee specimens from the Biological Museum at Lund University collected in Scania and Abisko (Sweden), as well as from specimens previously analysed in Taylor et al. [30]. For each specimen, the left eye was prepared as described in Taylor et al. [30]. ...
Local coexistence of bees has been explained by flower resource partitioning, but coexisting bumblebee species often have strongly overlapping diets. We investigated if light microhabitat niche separation, underpinned by visual traits, could serve as an alternative mechanism underlying local coexistence of bumblebee species. To this end, we focused on a homogeneous flower resource-bilberry-in a heterogeneous light environment-hemi-boreal forests. We found that bumblebee communities segregated along a gradient of light intensity. The community-weighted mean of the eye parameter-a metric measuring the compromise between light sensitivity and visual resolution decreased with light intensity, showing a higher investment in light sensitivity of communities observed in darker conditions. This pattern was consistent at the species level. In general, species with higher eye parameter (larger investment in light sensitivity) foraged in dimmer light than those with a lower eye parameter (higher investment in visual resolution). Moreover , species realized niche optimum was linearly related to their eye parameter. These results suggest microhabitat niche partitioning to be a potential mechanism underpinning bumblebee species coexistence. This study highlights the importance of considering sensory traits when studying pollinator habitat use and their ability to cope with changing environments.
... Thermo Fisher Scientific, Waltham. MA, USA) [17]. The lengths (L) of 38 rhabdoms in 5 regions were measured using ImageJ (1.8.0, USA). ...
... Visual heterogeneity and the trade-off between resolution and sensitivity are necessary for behavioral requirements of small insects [23]. In general, larger insects have better visual acuity [17,24], but the "bright areas" and "love spots" formed by compound eye specialization can satisfy the trade-off of the distribution of visual resolution and optical sensitivity among different areas of the compound eye [25,26], which is a fine-tuned mechanism of compound eyes shaped by long-term evolution. In predatory insects such as Holcocephala fusca (∆φ = 0.28 • ), which have a small body size, the nearly planar region of the anterior part of the compound eye provides high-resolution recognition of flying prey, and their vision in specialized regions is comparable to that of the dragonfly (Anax junius), which has compound eyes that are several times larger (∆φ = 0.24 • ) [27,28]. ...
Empoasca onukii is a common tea plant pest with a preference for the color yellow. Past work has shown that host leaf color is a key cue for habitat location for E. onukii. Before studying the effect of foliage shape, size, or texture on habitat localization, it is necessary to determine the visual acuity and effective viewing distance of E. onukii. In this study, a combination of 3D microscopy and X-ray microtomography showed that visual acuity did not significantly differ between females and males, but there were significant differences in the visual acuity and optical sensitivity among five regions of E. onukii’s compound eyes. The dorsal ommatidia had the highest visual acuity at 0.28 cycles per degree (cpd) but the lowest optical sensitivity (0.02 μm2sr), which indicated a trade-off between visual resolution and optical sensitivity for E. onukii. The visual acuity determined from the behavioral experiment was 0.14 cpd; E. onukii exhibited low-resolution vision and could only distinguish the units in a yellow/red pattern within 30 cm. Therefore, visual acuity contributes to the limited ability of E. onukii to distinguish the visual details of a distant target, which might be perceived as a lump of blurred color of intermediate brightness.
... The shaded areas indicate 95% confidence intervals for the regression lines Besides acting as a heat source, the light of the sun is necessary for bee navigation (Reber et al. 2015). Eye size allometry is established in both honeybees and bumblebees (Streinzer et al. 2013;Taylor et al. 2019): the larger eyes of bumblebees allow them to see in lower light conditions, which could explain the larger effect of solar radiation on honeybee activity and the lack of an effect on bumblebees. Reduced honeybee activity observed at lower solar radiation could be due to low sunlight in the morning or reduced visibility in cloudy conditions. ...
Insect pollination, and in particular pollination by bees, is a highly valued ecosystem service that ensures plant reproduction and the production of high-quality crops. Bee activity is known to be influenced by the weather, and as the global climate continues to change, the flying frequency and foraging behaviour of bees may also change. To maximise the benefits of pollination in a changing world, we must first understand how current weather conditions influence the activity of different bee species. This is of particular interest in a country such as Ireland where inclement weather conditions are nominally sub-optimal for foraging. We observed honeybee (Apis mellifera) and buff-tailed bumblebee (Bombus terrestris) activity across a variety of weather conditions at seven apple orchards to determine how four weather variables (temperature, relative humidity, solar radiation, wind) influenced the flight activity of each species. Each orchard contained three honeybee and three bumblebee colonies, and so we were able to observe a colony of each species concurrently in the same weather conditions. Overall, honeybees were more sensitive to changes in weather than bumblebees and could be more predisposed to future changes in within-day weather conditions. Our results indicate bumblebees could compensate for low honeybee activity in inclement conditions, which supports the theory that pollinator diversity provides resilience. This may be particularly important in management of pollinators in crops that flower in the spring when weather is more variable, and to allow varied responses to global climate change.
