Fig 8 - uploaded by Srdjan Maksimovic
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Geometrical interpretations of sample bases. (A) Geometry of standing and lying hexagonal arrays. (B) Hypothetical organization of sampling units in three neighboring eyelets. The retina of one eyelet has up to four sampling units in the horizontal plane, subsuming a total of about 30-35°. The smaller sampling base around 10° occurs within an eyelet, for instance between units 1-2, 2-3, 3-4 in the middle eyelet. One possibility for the larger sample base around 20° is that neighboring eyelets span, for instance between units 1-1, 2-2, etc. (C) Irregularities in the organization of eyelets indicated by the number of nearest neighbors for several specific eyelets. (D) A horizontal section of X. peckii illustrates an alternative explanation for the larger sample base, connecting only nearest optical neighbors. The angles of two such connections are indicated. Variation results because some eyelets lie in the same horizontal plane as their neighbors, such as those in which the same number of sampling units are visible (their optical axes in 2D indicated with straight lines), while other neighbors lie outside the horizontal plane, such as those in which different numbers of units are visible. Scale bars, 50·m.
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Compound eyes are typically composed of hundreds to thousands of ommatidia, each containing 8-10 receptors. The maximal spatial frequency at which a compound eye can sample the environment is determined by the inter-ommatidial angle. Males of the insect order Strepsiptera are different: their eyes are composed of a smaller number of relatively larg...
Citations
... Visual stereopsis of apposition or superposition compound eyes mostly found in nature offers relatively inaccurate depth information because a small number of photoreceptor cells in a single facet lens generate a simple point image [13][14][15][16] . However, the unusual design of Xenos peckii eyes exhibits multi-view stereopsis with high visual acuity through chunk sampled images, which is created by multiple photoreceptors on a single facet lens [17][18][19] . ...
Insects exhibit intriguing vision capability using fragmented information from arrays of lenses. Visual disparity between lenses or eyelets (also known as stereopsis) helps insects to locate their prey or find landing spots. Here we report a multi-functional imaging system inspired by insect stereopsis using a single ultrathin microlens array camera. Individual channels through tens of microlenses capture distinct images with visual disparities. We demonstrate that reconstruction of these images can provide diverse capabilities, such as simultaneous near-distance microscopic imaging, high speed imaging at far distances and 3D depth imaging at intermediate distances. Our findings offer clues to further understand the vision capability of insects as well as insights for advanced compact functional imaging tools.
... Furthermore, compound eyes have superior visual functions, such as large depth-of-field (DOF), wide field-ofview (FOV), high motion sensitivity, and low aberration 6,7 . In particular, the eye structures of an adult Xenos peckii, exhibiting hundreds of photoreceptors on an individual eyelet, offer engineering inspiration for ultrathin camera or imaging applications because they have higher visual acuity than other compound eyes [8][9][10] . For instance, Xenos peckii's eye-inspired cameras provide an~50 times higher spatial resolution than those from arthropod eyes, i.e., compound eyes with ommatidia 1,10,11 . ...
Compound eyes found in insects provide intriguing sources of biological inspiration for miniaturised imaging systems. Here, we report an ultrathin arrayed camera inspired by insect eye structures for high-contrast and super-resolution imaging. The ultrathin camera features micro-optical elements (MOEs), i.e., inverted microlenses, multilayered pinhole arrays, and gap spacers on an image sensor. The MOE was fabricated by using repeated photolithography and thermal reflow. The fully packaged camera shows a total track length of 740 μm and a field-of-view (FOV) of 73°. The experimental results demonstrate that the multilayered pinhole of the MOE allows high-contrast imaging by eliminating the optical crosstalk between microlenses. The integral image reconstructed from array images clearly increases the modulation transfer function (MTF) by ~1.57 times compared to that of a single channel image in the ultrathin camera. This ultrathin arrayed camera provides a novel and practical direction for diverse mobile, surveillance or medical applications.
... The individual optical unit consists of a relatively large convex facet lens and multiple photoreceptor cells, whereas that of the apposition compound eye has one to several photoreceptor cells in a single unit. Each optical unit, called an eyelet, detects part of the overall FOV, with improved spatial resolution and sensitivity compared to other compound eyes [5][6][7] . ...
... Figure 1c shows fluorescently stained optical units (called eyelets) superimposed onto an SEM image of a Xenos peckii eye, which illustrates in detail a relatively large lens and underlying receptor arrays. Each eyelet detects a partial image within the total FOV (Fig. 1d), thus improving the spatial resolution and the sensitivity [5][6][7] . Figure 1e shows a schematic illustration of a biologically inspired ultrathin digital camera. ...
Increased demand for compact devices leads to rapid development of miniaturized digital cameras. However, conventional camera modules contain multiple lenses along the optical axis to compensate for optical aberrations that introduce technical challenges in reducing the total thickness of the camera module. Here, we report an ultrathin digital camera inspired by the vision principle of Xenos peckii, an endoparasite of paper wasps. The male Xenos peckii has an unusual visual system that exhibits distinct benefits for high resolution and high sensitivity, unlike the compound eyes found in most insects and some crustaceans. The biologically inspired camera features a sandwiched configuration of concave microprisms, microlenses, and pinhole arrays on a flat image sensor. The camera shows a field-of-view (FOV) of 68 degrees with a diameter of 3.4 mm and a total track length of 1.4 mm. The biologically inspired camera offers a new opportunity for developing ultrathin cameras in medical, industrial, and military fields.
... There is discrepancy over whether Strepsiptera see well with so few facets, which some expect to effectively act as pixels (Pix et al. 2000), while others hold that each 'ommatidia' should behave as a separate image-forming eyelet (Buschbeck et al. 1999;Maksimovic et al. 2007). The capture of large numbers of eclosed males below the grass canopy at Wakulla Beach suggests that E. koebelei can fly between grass blades before sunrise, and therefore must see well enough to do so. ...
Strepsiptera are a small order of obligately endoparasitic insects. Adult females are neotenic and never leave their host, instead bearing motile young that seek out their own insect hosts to infect. Males eclose without killing their hosts. In their 4-h adult lifespan, they fly off to search for mating opportunities, assisted by unconventional eyes with few, but large, ommatidia. Such distinctive features make Strepsiptera interesting in their own right, but also offer an opportunity to better understand evolutionary innovation. Unfortunately, Strepsiptera also are minute, reclusive, and difficult to obtain, severely reducing the study thereof, especially species not infecting solitary bees or social wasps. Here we describe methods for the successful capture of a strepsipteran species. We placed an ultraviolet light trap among Spartina alterniflora Loisel (Poaceae) shoots to attract adult male Elenchus koebelei Pierce (Strepsiptera: Elenchidae) in salt marshes in the southeastern United States. In 72 d of sampling, 488 adult males were captured between 30 min before and 15 min after sunrise. None arrived more than 63 min before or 36 min after sunrise. The majority of E. koebelei were caught at wind speeds ranging from 0 to 10 km/h; however, a light breeze of about 1.5 km/h appears to be preferred. The highest daily catches occurred when the temperature was between 23 and 26 °C. No Strepsiptera were caught at temperatures below 17 °C. With 521 adult male E. koebelei caught in a single light trap, our results show this little-known parasite may be reliably obtained, enhancing opportunities for further study.
... Because of the characteristics of lenses, the image is inverted within each eyelet. However, in X. peckii, the original orientation of each image is restored via downstream wiring (Buschbeck et al., 2003), allowing the eye as a whole to produce a combined image of higher acuity (Maksimovic et al., 2007) than the 50 or so pixels that X. peckii would be able to represent if each of the eyelets only resolved a single point in space (as is typical for compound eye ommatidia). ...
The highly specialized evolution of Strepsiptera has produced one of the most unusual eyes among mature insects, perhaps in line with their extremely complex and challenging life cycle. This relatively rare insect order is one of the few for which it has been unclear what spectral classes of photoreceptors any of its members may possess, an even more apt question given the nocturnal evolution of the group. To address this question, we performed electroretinograms on adult male Xenos peckii: we measured spectral responses to equi-quantal monochromatic light flashes of different wavelengths, and established VlogI relationships to calculate spectral sensitivities. Based on opsin template fits, we found maximal spectral sensitivity (λmax) in the green domain at 539 nm. Application of a green light to 'bleach' green receptors revealed that a UV peak was contributed to by an independent UV opsin with a λmax of 346 nm. Transcriptomics and a phylogenetic analysis including 50 other opsin sequences further confirmed the presence of these two opsin classes. While these findings do not necessarily indicate that these unorthodox insects have color vision, they raise the possibility that UV vision plays an important role in the ability of X. peckii males to find the very cryptic strepsipteran females that are situated within their wasp hosts.
... Moreover, a departure from the compound eye, although relatively uncommon, is possible. Indeed, while many insect larvae evolved chambered eyes from compound ones, adults of the same species did not [43], and a parasitic insect harbors an intermediate form between a compound and chambered type eye [44]. ...
Motion vision provides important cues for many tasks. Flying insects, for example, may pursue small, fast moving targets for mating or feeding purposes, even when these are detected against self-generated optic flow. Since insects are small, with size-constrained eyes and brains, they have evolved to optimize their optical, neural and behavioral target visualization solutions. Indeed, even if evolutionarily distant insects display different pursuit strategies, target neuron physiology is strikingly similar. Furthermore, the coarse spatial resolution of the insect compound eye might actually be beneficial when it comes to detection of moving targets. In conclusion, tiny insects show higher than expected performance in target visualization tasks.
... Moreover, a departure from the compound eye, although relatively uncommon, is possible. Indeed, while many insect larvae evolved chambered eyes from compound ones, adults of the same species did not [43], and a parasitic insect harbors an intermediate form between a compound and chambered type eye [44]. ...
Motion vision provides important cues for many tasks. Flying insects, for example, may pursue small, fast moving targets for mating or feeding purposes, even when these are detected against self-generated optic flow. Since insects are small, with size-constrained eyes and brains, they have evolved to optimize their optical, neural and behavioral target visualization solutions. Indeed, even if evolutionarily distant insects display different pursuit strategies, target neuron physiology is strikingly similar. Furthermore, the coarse spatial resolution of the insect compound eye might actually be beneficial when it comes to detection of moving targets. In conclusion, tiny insects show higher than expected performance in target visualization tasks.
... The co-occurrence of the males' emergence period (Fig. 5, bottom) and the females' calling period (Fig. 5, top) may be an adaptation that mitigates this challenge. This does not exclude other potential adaptations including acute vision and olfaction of mateseeking males (Strohm 1910; Rösch 1913; Wachmann 1972; Bushbeck et al. 1999 Bushbeck et al. , 2003 Beutel et al. 2005; Srdjan et al. 2007), the males' extraordinary flight ability and apparatus (Kinzelbach 1971; Pohl and Beutel 2008), as well as behavioural manipulation of the host wasp (Salt 1927Salt , 1931, and references therein; Hughes et al. 2004; Beani 2006; Dapporto et al. 2007; Beani et al. 2011). In light of reports (Brues 1905; Bohart 1941; Kinzelbach 1971; Beani et al. 2005 , and references therein; P.W.S., personal observation) that male Xenos species in general, and male X. peckii in particular (Hubbard 1892; Schrader 1924), emerge early in the morning (but see Kathirithamby and Hughes 2006), we expected X. peckii males in this study to emerge and mate in the morning. ...
We studied life history traits of Xenos peckii Kirby (Strepsiptera: Xenidae), a little-known parasite of the paper wasp Polistes fuscatus (Fabricus) (Hymenoptera: Vespidae) in North America. We field-collected 24 wasp nests in early July 2012, isolated parasitised wasps, tracked life history events of X. peckii, and recorded such behaviour as emergence of males and mating by normal-speed and high-speed cinematography. To emerge, males first cut the puparium with their mandibles along an ecdysial suture line, and then push aside the pupal cap during emergence. The endoparasitic females engage in active calling (pheromone release) behaviour by slowly inflating their cephalothorax, and then extruding it even farther out of, and tilting it away from, the host wasp abdomen. Seasonal and diel (afternoon) emergence periods of males coincide with seasonal and diel receptivity and calling periods of females. Males approach calling females in a swaying flight with smooth turns. They typically land on the anterior portion of the host wasp's abdomen, and then step backward until they make contact with the cephalothorax of the female. As soon as their mesothoracic legs contact the female's cephalothorax, they curl around it, and the male initiates mating. Thereafter, the female fully retreats and never re-mates.
... Although gaze stabilization has been studied in great detail using tethered insects (e.g. Goodman 1965;Land 1973;Stange 1981;Hengstenberg 1988;Gilbert et al. 1995;Pix et al. 2000;Maksimovic et al. 2007), only a few studies have done so in freely flying insects (Wehner & Flatt 1977;van Hateren & Schilstra 1999). Because insects cannot move their eyes within the head capsule, their gaze is determined by the orientation of the head relative to the external world. ...
As animals travel through the environment, powerful reflexes help stabilize their gaze by actively maintaining head and eyes in a level orientation. Gaze stabilization reduces motion blur and prevents image rotations. It also assists in depth perception based on translational optic flow. Here we describe side-to-side flight manoeuvres in honeybees and investigate how the bees' gaze is stabilized against rotations during these movements. We used high-speed video equipment to record flight paths and head movements in honeybees visiting a feeder. We show that during their approach, bees generate lateral movements with a median amplitude of about 20 mm. These movements occur with a frequency of up to 7 Hz and are generated by periodic roll movements of the thorax with amplitudes of up to + or - 60 degrees . During such thorax roll oscillations, the head is held close to horizontal, thereby minimizing rotational optic flow. By having bees fly through an oscillating, patterned drum, we show that head stabilization is based mainly on visual motion cues. Bees exposed to a continuously rotating drum, however, hold their head fixed at an oblique angle. This result shows that although gaze stabilization is driven by visual motion cues, it is limited by other mechanisms, such as the dorsal light response or gravity reception.
... The same is true for stemmata (the eyes of holometabolous insect larvae), which have likely evolved from the most posterior facets of their hemimetabolous ancestors (Paulus 1979(Paulus , 2000Liu and Friedrich 2004;Friedrich 2006;Liu et al. 2006;Sbita et al. 2007). Other examples are the telescopic eye of the mysid shrimp (Nilsson and Modlin 1994) and the eyes of male Strepsiptera (Buschbeck et al. 1999(Buschbeck et al. , 2003, which recently have been demonstrated to be capable of resolving multiple image points within each unit (Maksimovic et al. 2007). While in these examples the transition must have occurred a relatively long time ago, margarodids may represent a living transitional form that can be investigated. ...
... All specimens were stored in 70% ethanol for several months or years. In order to evaluate the structural organization of the eye, comparisons are made with (1) wild-type Drosophila melanogaster (Oregon R strain), (2) a Cincinnati Brood X cicada (Magicicada sp.), and (3) with lab-reared male Strepsiptera of the species Xenos peckii (see Maksimovic et al. 2007 for details on husbandry). ...
... One insect in which ommatidia have evolved into small image-forming eyes are Strepsiptera (Fig. 6d). In Xenos peckii, each of the eyelets are thought to function as a small camera eye, resolving a partial image (Buschbeck et al. 1999(Buschbeck et al. , 2003Maksimovic et al. 2007). ...
Animal eyes generally fall into two categories: (1) their photoreceptive array is convex, as is typical for camera eyes, including the human eye, or (2) their photoreceptive array is concave, as is typical for the compound eye of insects. There are a few rare examples of the latter eye type having secondarily evolved into the former one. When viewed in a phylogenetic framework, the head morphology of a variety of male scale insects suggests that this group could be one such example. In the Margarodidae (Hemiptera, Coccoidea), males have been described as having compound eyes, while males of some more derived groups only have two single-chamber eyes on each side of the head. Those eyes are situated in the place occupied by the compound eye of other insects. Since male scale insects tend to be rare, little is known about how their visual systems are organized, and what anatomical traits are associated with this evolutionary transition. In adult male Margarodidae, one single-chamber eye (stemmateran ocellus) is present in addition to a compound eye-like region. Our histological investigation reveals that the stemmateran ocellus has an extended retina which is formed by concrete clusters of receptor cells that connect to its own first-order neuropil. In addition, we find that the ommatidia of the compound eyes also share several anatomical characteristics with simple camera eyes. These include shallow units with extended retinas, each of which is connected by its own small nerve to the lamina. These anatomical changes suggest that the margarodid compound eye represents a transitional form to the giant unicornal eyes that have been described in more derived species.
