Bumblebee visual allometry results in locally improved resolution and globally improved sensitivity

Abstract

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 but we understand little about how this affects visual quality. Insects are good models for exploring the effects of size on visual systems because many species exhibit size polymorphism, which modifies both the size and shape of their eyes. Previous work in this area has been limited, however, due to the challenge of determining the 3D structure of eyes. To address this, we have developed a novel method based on x-ray tomography to measure the 3D structure of insect eyes and calculate their visual capabilities. We investigated visual allometry in the bumblebee Bombus terrestris and found that size affects specific aspects of visual quality including binocular overlap, optical sensitivity across the field of view, and visual resolution in the dorsofrontal visual field. This holistic study on eye allometry reveals that differential scaling between different eye areas provides substantial flexibility for larger bumblebees to have improved visual capabilities. List of abbreviations:az. -Azimuth CC -Crystalline cone el. -Elevation EV -Eye volume FOV -Field of view ITW -Inter-tegula width IO -Inter-ommatidial microCT -micro-computed tomography NV -Normal vector

Measuring Compound Eye Optics with Microscope and MicroCT Images

“…Ultimately, anatomical measurements cannot replace optical techniques in measuring compound eye optics (Stavenga 1979;Taylor et al 2018). When light passes through the eye optics, the angle of refraction is determined by both the incident angle and the index of refraction of the image space (Stavenga 1979).…”

“…The effect of this skewness on adjusted lens diameter was a reduction of 3.30±3.92µm or 12.7±15.4%, which is substantial and consistent with a non-spherical eye. The ommatidia were separated by an anatomical IO angle of 2.29±1.65°, which is greater than the spherical approximation of 0.74±.27°, the previous measurement of 1.6±0.6° using orthogonal ommatidial axes on the same scan (Taylor et al 2018), and the previous measurement of 1.9° using the pseudopupil technique on a similarly sized conspecific (Spaethe 2003).…”

“…Our second proposed method, the µCT pipeline, extracts crystalline cones from a µCT image stack (using the ODA) to measure the size, orientation, and spatial distribution of ommatidia. As mentioned above, we validate it on µCT scans of the spherical eyes of two moth species (M. sexta and D. elpenor) collected by us and an open access scan of a non-spherical, oval bumblebee eye (B. terrestris) used in Taylor et al (2018). For the bumblebee eye, we further demonstrate how the µCT pipeline can test for features of an oval eye; measure regional changes in skewness, spatial acuity, and sensitivity; and project onto world-referenced coordinates to more accurately measure FOV.…”

InSegtCone: Interactive Segmentation of crystalline Cones in compound eyes

“…Micro-CT image stacks of eye samples of adult workers (females) of Apis mellifera (specimen: LU:3_14:AM_F_5) and Bombus terrestris (specimen: LU:4_16_: BT_F_CE_10) were the same as those previously analysed in Taylor et al (2019b), where the sample preparation and data acquisition method are described in detail. An adult female of Pieris napi was obtained from laboratory stock at the Department of Zoology, Stockholm University, Sweden.…”

The neuroplasticity of division of labor: worker polymorphism, compound eye structure and brain organization in the leafcutter ant Atta cephalotes

“…2009; Palavalli-Nettimi and Narendra 2018; Taylor et al 2019). Ants are an ideal model system 56 to examine relationships among behavior, body size, and neuroanatomy because workers have 57 evolved as task specialists in several clades (Hölldobler and Wilson 1990).…”