Three‐dimensional visualization of ocellar interneurons of the orchid bee Euglossa imperialis using micro X‐ray computed tomography
Neither the function of insect ocelli nor the adaptive significance of their design is fully understood. The three simple lens eyes that are carried dorsally or frontally on the head between the compound eyes have been shown to supply information for the control of roll and pitch orientation of the head in dragonflies, locusts, and flies (e.g., Hengstenberg, 1993; Stange, 1981; Stange & Howard, 1979; Taylor, 1981a; Wilson, 1978), but also celestial compass information in ants (Fent & Wehner, 1985; Schwarz, Albert, Wystrach, & Cheng, 2011). Ocellar photoreceptors are UV and green sensitive (in dragonflies: van Kleef, James, & Stange, 2005) and in addition polarization sensitive, at least in hymenopteran insects (honeybees: Geiser & Labhart, 1982; Ogawa, Ribi, Zeil, & Hemmi, 2017; reviewed in Zeil, Ribi, & Narendra, 2014). In the case of orchid bees, ocellar photoreceptors have distinctly aligned rhabdom cross‐sections in the lateral and the median ocelli (Taylor et al., 2016).
Recent comparative work of ocellar systems has sparked a renewed interest in their functional design: (a) Although ocelli are generally not focused, in some cases, such as in the ocelli of dragonflies (Berry, Stange, Olberg, & Kleef, 2006; Berry, Stange, & Warrant, 2007; Berry, van Kleef, & Stange, 2007; Stange, Stowe, Chahl, & Massro, 2002; van Kleef et al., 2005) and in the equatorial region of the honeybee ocelli, ocellar retinae appear to be close to the focal plane of the lens (Hung & Ibbotson, 2014; Ribi, Warrant, & Zeil, 2011); (b) Ocellar retinae are very diverse, in particular with respect to the arrangement and shape of rhabdoms (e.g., Zeil et al., 2014); (c) The retinae of most ocellar systems are divided into a dorsal and a ventral part which differ in their distance from the ocellar lens surface, in the sizes and arrangements of rhabdoms and in the properties of screening pigments (e.g., Ribi et al., 2011; Zeil et al., 2014); (d) The organization of rhabdoms in many hymenopteran ocellar retinae suggests that ocellar photoreceptors are polarization sensitive (Geiser & Labhart, 1982; Ribi et al., 2011; Taylor et al., 2016; Zeil et al., 2014) as shown by electrophysiological recordings (Geiser and Labhart, 1982; Ogawa et al., 2017); (e) In insects that are active at low light, ocellar optics and rhabdoms are enlarged, compared to diurnal insects and thus show the usual adaptations to dim‐light vision (e.g., Berry, Wcislo, & Warrant, 2011; Greiner, 2006; Narendra et al., 2011; Somanathan, Kelber, Borges, Wallen, & Warrant, 2009; Streinzer, Brockmann, Nagaraja, & Spaethe, 2013; Warrant, Kelber, Wallen, & Wcislo, 2006); (f) In ants, ocellar systems also depend on the mode of locomotion, being larger in flying, compared to walking castes (Narendra, Ramirez‐Esquivel, & Ribi, 2016).
The functional importance of ocelli, in particular in flying insects, is also reflected in the fact that some of the ocellar interneurons (L‐neurons) that collect information from the ocellar retinae belong to the largest neurons in the insect brain (reviewed in Mizunami, 1995a). Recent electrophysiological evidence shows that these neurons contribute fast signals to roll and pitch sensitive motion pathways (blowflies: Parsons, Krapp, & Laughlin, 2006; honeybee: Hung, van Kleef, Stange, & Ibbotson, 2013).