Visual Adaptations for Mate Detection in the Male Carpenter Bee Xylocopa tenuiscapa

Abstract

Sexual dimorphism in eye structure is attributed to sexual selection in animals that employ vision for locating mates. In many male insects, large eyes and eye regions of higher acuity are believed to facilitate the location of females. Here, we compare various features of male and female eyes in three sympatric carpenter bee species, which include two diurnal species (Xylocopa tenuiscapa and X. leucothorax) as well as a nocturnal species (X. tranquebarica). In X. tenuiscapa, males have larger eyes than females, while in the nocturnal X. tranquebarica, males have slightly smaller eyes and in X. leucothorax, the eyes are of similar size in both sexes. X. tenuiscapa males detect females by perching near nest sites (resource defence) or along fly-ways and other open areas with good visibility. Males of the other two species search for females by patrolling. We postulate that the larger eyes of male X. tenuiscapa are beneficial to their mode of mate detection since perching males may benefit from a larger visual area of high resolution detecting moving stimuli across the sky, and which may be germane to the more social and gregarious nesting behaviour of this species, compared to the other solitary bees. We tested the performance of the eyes of male X. tenuiscapa behaviourally and find that a perching male can detect a flying female at a distance of 20 m, which darkens the visual field of a single ommatidium by just 2%. This, together with the bee’s high spatial resolution permits detection of moving stimuli at least as well or even better than achieved by honey bee drones.

Spatial Vision and Visually Guided Behavior in Apidae

“…In carpenter bees, sexual dimorphism of eye size is correlated with mating strategy [36]. Males, which defend resources, tend to have dorsal acute zones with more and larger facets and smaller interommatidial angles than females, as described in X. tenuiscapa [14], while no obvious sexual dimorphism is seen in species with other mating strategies. A similar pattern can be seen in bumblebees: males of species, which adopt a perching strategy, for instance B. confusus, B. melaleucus, and B. niveatus, have larger eyes and facets than workers, while those using a patrolling strategy have similarly sized eyes ( [13]; and see Table 2).…”

“…Given the same visual field (but see [15]), this results in higher resolution, higher sensitivity, or a combination of both. Because each pixel is served by its own optical apparatus, sensitivity and resolution can vary widely within an eye, leading to acute and bright zones, the most extreme forms of which are found in the eyes of male bees [10][11][12][13][14]. When comparing different species, we mostly focus on the eye regions with highest resolution and sensitivity (Table 1).…”

“…The degree of sexual dimorphism depends partly on the mating system of a species. In bumblebee and carpenter bee species, which rely to a large degree on chemical cues, male and female eyes are more similar than in species that use visual mate detection [13,14,36].…”

“…Where sexual dimorphism is found, the eye region of highest spatial resolution in the drone eye, the acute zone, is often found in the dorsal part of the eye [10][11][12][13][14]. In A. mellifera drones, the upper third of the eye builds a large upwards-looking acute zone with larger facet diameters (30-40 µm), smaller inter-ommatidial angles (1-2 • ), and larger, and thus more sensitive, rhabdoms (2-3 µm 2 ), than the remaining two-thirds of the eye (20-30 µm; 2-4 • ; 0.8-2 µm 2 ) [10,11].…”

“…While most bees are active during daytime, few species have extended their activity into the night, which requires high absolute sensitivity of their eyes. Males may have different demands than females, and thus, dimorphic eyes occur amongst bees [10][11][12][13][14]. We will review properties of the eyes and vision first, and then discuss visually guided behaviors.…”