Abstract
Honeybees have a visual system composed of three ocelli (simple eyes) located on the top of the head, in addition to two large compound eyes. Although experiments have been conducted to investigate the role of the ocelli within the visual system, their optical characteristics, and function remain controversial. In this study, we created three-dimensional (3-D) reconstructions of the honeybee ocelli, conducted optical measurements and filled ocellar descending neurons to assist in determining the role of ocelli in honeybees. In both the median and lateral ocelli, the ocellar retinas can be divided into dorsal and ventral parts. Using the 3-D model we were able to assess the viewing angles of the retinas. The dorsal retinas view the horizon while the ventral retinas view the sky, suggesting quite different roles in attitude control. We used the hanging drop technique to assess the spatial resolution of the retinas. The lateral ocelli have significantly higher spatial resolution compared to the median ocellus. In addition, we established which ocellar retinas provide the input to five pairs of large ocellar descending neurons. We found that four of the neuron pairs have their dendritic fields in the dorsal retinas of the lateral ocelli, while the fifth has fine dendrites in the ventral retina. One of the neuron pairs also sends very fine dendrites into the border region between the dorsal and ventral retinas of the median ocellus.
Highlights
Honeybees (Apis mellifera), like most of the flying insects possess two visual systems: the compound eyes and a set of simple lens eyes
We show for the first time that four of these neurons have their primary dendritic fields in the dorsal retinas of the lateral ocelli, while the fifth sends fine dendrites into the ventral retina
Combining the results from the 3-D reconstructions and the 2-D sections, we provide a complete visualization of the retinal structures and their relation to the lenses. In both the median and lateral ocelli of honeybee we identified two retinas, the dorsal and ventral retinas
Summary
Honeybees (Apis mellifera), like most of the flying insects possess two visual systems: the compound eyes and a set of simple lens eyes (ocelli). The same feature was subsequently found in other species (e.g., locust: Parry, 1947; Cornwell, 1955; Wilson, 1978; Berry et al, 2007c; blowfly: Cornwell, 1955; Schuppe and Hengstenberg, 1993; nocturnal bee and diurnal wasp: Warrant et al, 2006) The function of these under-focused lenses is not yet entirely clear, speculation about their role began over 100 years ago (Müller, 1826; Lowne, 1870). Wilson (1978) proposed a convincing hypothesis of ocellar function based on locust ocelli, referred to as the “single-sensor” hypothesis (Stange et al, 2002) It suggests that the ocelli do not resolve spatial details of the environment: instead, each ocellus functions as a highly sensitive light detector of illumination levels from a wide region of visual space. Their large aperture and field of view suggest that they are designed to detect overall brightness while minimizing the effect of small objects in the visual field (Wilson, 1978)
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