Adaptations for nocturnal and diurnal vision in the hawkmoth lamina

Abstract

Animals use vision over a wide range of light intensities, from dim starlight to bright sunshine. For animals active in very dim light the visual system is challenged by several sources of visual noise. Adaptations in the eyes, as well as in the neural circuitry, have evolved to suppress the noise and enhance the visual signal, thereby improving vision in dim light. Among neural adaptations, spatial summation of visual signals from neighboring processing units is suggested to increase the reliability of signal detection and thus visual sensitivity. In insects, the likely neural candidates for carrying out spatial summation are the lamina monopolar cells (LMCs) of the first visual processing area of the insect brain (the lamina). We have classified LMCs in three species of hawkmoths with considerably different activity periods but very similar ecology-the diurnal Macroglossum stellatarum, the nocturnal Deilephila elpenor and the crepuscular-nocturnal Manduca sexta. Using this classification, we investigated the anatomical adaptations of hawkmoth LMCs suited for spatial summation. We found that specific types of LMCs have dendrites extending to significantly more neighboring cartridges in the two nocturnal and crepuscular species than in the diurnal species, making these LMC types strong candidates for spatial summation. Moreover, while the absolute number of cartridges visited by the LMCs differed between the two dim-light species, their dendritic extents were very similar in terms of visual angle, possibly indicating a limiting spatial acuity. The overall size of the lamina neuropil did not correlate with the size of its LMCs.

Anatomical organization of the brain of a diurnal and a nocturnal dung beetle

“…The network in the primary visual integration centers in the brain, the optic lobes, have also been demonstrated to support a higher sensitivity for dimlight vision (Greiner, Ribi, Wcislo, & Warrant, 2004;St€ ockl, Ribi, & Warrant, 2016). This difference in eye design is obvious among the dung beetles .…”

Differential investment in brain regions for a diurnal and nocturnal lifestyle in Australian Myrmecia ants

“…Insects may thus engage in spatial and temporal integration of receptor signals to improve the visual signal‐to‐noise ratio at low light levels (Greiner, Ribi, & Warrant, ; Stöckl, O'Carroll, & Warrant, ; Warrant, ). Spatial summation is thought to occur in the first optic neuropil, the lamina, via extensive lateral branching of laminar monopolar cell dendrites into neighboring cartridges, which receive input from single ommatidia (Greiner, Ribi, Wcislo, & Warrant, ; Ribi, ; Stöckl, Ribi, & Warrant, ). Apart from these adaptations found in the peripheral sensory system, it is unclear whether and how the size of distinct brain regions changes between visually oriented day‐ and night‐active animals.…”

Connecting spectral radiometry of anthropogenic light sources to the visual ecology of organisms

“…The Wolf has dichromatic color vision comprised of a short wavelength cone and a long wavelength cone, and the same rod as humans (Jacobs et al ., ). Lastly, the elephant hawk moth has trichromatic color vision and is currently the record holder for lowest light level color vision in the animal kingdom ((Schlecht, ; Kelber, Balkenius & Warrant, ; Stöckl, Ribi & Warrant, ; Stöckl, O'Carroll & Warrant, )). All photoreceptor sensitivities were calculated using published lambda max values, the peak sensitivity of the photoreceptor, for each visual system and then a Govardovskii template to calculate the complete spectral sensitivity, Table for lambda max values and citations for each visual system (Govardovskii et al ., ).…”