Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles

Abstract

Most bees are diurnal, with behaviour that is largely visually mediated, but several groups have made evolutionary shifts to nocturnality, despite having apposition compound eyes unsuited to vision in dim light. We compared the anatomy and optics of the apposition eyes and the ocelli of the nocturnal carpenter bee, Xylocopa tranquebarica, with two sympatric species, the strictly diurnal X. leucothorax and the occasionally crepuscular X. tenuiscapa. The ocelli of the nocturnal X. tranquebarica are unusually large (diameter ca. 1 mm) and poorly focussed. Moreover, their apposition eyes show specific visual adaptations for vision in dim light, including large size, large facets and very wide rhabdoms, which together make these eyes 9 times more sensitive than those of X. tenuiscapa and 27 times more sensitive than those of X. leucothorax. These differences in optical sensitivity are surprisingly small considering that X. tranquebarica can fly on moonless nights when background luminance is as low as 10(-5) cd m(-2), implying that this bee must employ additional visual strategies to forage and find its way back to the nest. These strategies may include photoreceptors with longer integration times and higher contrast gains as well as higher neural summation mechanisms for increasing visual reliability in dim light.

Resolution and sensitivity of the eyes of the Asian honeybees Apis florea, Apis cerana and Apis dorsata

“…However, unlike X. tranquebarica, X. tenuiscapa can only fly on full-moon nights. Accordingly, Somanathan et al found that the eyes of this species lack some adaptations for nocturnal vision that are found in X. tranquebarica (Somanathan et al, 2009). We expected that A. dorsata and A. m. adansonii may be similar cases because they extend foraging activity into the night if at least a half-moon is present in the sky (Fletcher, 1978) and if favourable food sources can be exploited at such times.…”

“…While Kerfoot (Kerfoot, 1967) has recognised that nocturnal bees have unusually large ocelli, the adaptations of the eyes and the visual system for a nocturnal lifestyle have only recently been the focus of research. Warrant et al (Warrant et al, 2004) gave a detailed report of the visual activity of the halictid bee Megalopta genalis, and Somanathan et al (Somanathan et al, 2009) have described the eyes of X. tranquebarica and compared them with the eyes of sympatric diurnal congeners. Common features of nocturnal bees -and other nocturnal hymenopterans -are their huge ocelli and relatively large eyes with reasonably large facets and, most importantly, their unusually wide rhabdoms (Kerfoot, 1967;Menzi, 1987;Greiner et al, 2004a;Warrant et al, 2004;Greiner, 2006;Kelber et al, 2006;Greiner et al, 2007;Somanathan et al, 2009) (for a review, see Warrant, 2008).…”

Light and dark adaptation mechanisms in the compound eyes of Myrmecia ants that occupy discrete temporal niches

“…Nilsson, 1989Nilsson, , 1990) -typically limits vision to bright daylight conditions because each photoreceptor receives light through one small facet lens only (Greiner, 2006;Schwarz et al, 2011;Warrant et al, 2004). However, several hymenopteran insects are active in dim light conditions (Greiner, 2006;Greiner et al, 2007;Kelber et al, 2006Kelber et al, , 2003Klotz and Reid, 1993;Narendra et al, 2010;Somanathan et al, 2008Somanathan et al, , 2009Wolda and Roubik, 1986) and have modified apposition compound eyes to increase photon capture: larger lenses, wider and longer rhabdoms and spatial and temporal pooling of photoreceptor signals across neighbouring ommatidia (Stöckl et al, 2016;Warrant and Dacke, 2011). Such highly sensitive eyes have then to be protected against bright light.…”

Ultrastructure of dorsal rim area of compound eyes of the male the red palm weevil, Rhynchophorus ferrugineus (Olivier) (Curculionidae: Rhynchophorinae): in relation to habitat

“…SEM observations revealed that the facets size of the dorsal rim area assumed that wide facets sizes were related to their functional importance correlated with the amount of light received by each facet at this region. Somanathan et al (2009) andWarrant (1999) previously reported the correlation between polarization vision, behavior and time of day, so that interpreted the diurnal relatives and polarization vision may play an important role in the long-distance homing flights of the diurnal-crepuscular male of R. ferrugineus. Dark/light adaption is also presumably because after the pupation and larval stages they spend long periods inside the palm trunk, where they complete their remaining life cycle, some of the males started has been emerging from of the palm trunk.…”