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Functional anatomy and ultrastructure of photoreceptors

Goal: To investigate structural and functional adaptations of photoreceptive sensors of organisms under a variety of conditions.

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Victor Benno Meyer-Rochow
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Summary: The invasive polydesmid millipede Chamberlinius hualienensis Wang 1956 has been known to occur on the Japanese Izu Island of Hachijojima since 2002. Several mass outbreaks of the species have been reported and during the 2015 outbreak all the specimens that were examined had deutonymphsofanunidentifiedHistiostomaspeciesontheirbodies.Thespecieswasmorphologically compared with deutonymphs of related Histiostoma species of the ‘Feroniarum-group’. ThespeciesH.abietisandH.formosana sharethelargestnumberoftraitswith the Hachijojima species. However, H. abietes occurs only in Europe and its hosts are beetles, while H.formosana does occur in Taiwan, but has an association with the termite Coptotermes formosanusand is considerably smaller than the Hachijojima Histiostoma species. Since the latter was not present on any C. hualienensis millipedes collected in Taiwan, the possibility exists that it is a species new to Japan (or not described from anywhere else) and that it occurred on Hachijojima prior to the Taiwanese millipede’s arrival and then switched its host or added a new one, namely C. hualienensis. A detailed description combined with a molecular characterization of the Hachijojima species is planned.
Victor Benno Meyer-Rochow
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Male and female individuals of the Baltic Sea, stalk‐inhabiting amphipod Dulichia porrecta posses eyes that differ in size and organization. Ommatidial numbers also vary, and in adult male and female specimens amount to approximately 80 and 90, respectively. Ommatidial diameters are larger in males (40–45) μm) than in females (approx. 30 μ.m). Externally, female eyes are covered with a dense pelt of approximately 3–4 μm long and 0.01–0.15 μm thick cuticular hairs, interspersed by up to 8 μm long, filament‐containing sensilla of unknown function. An identical structure occurs in males, but there it is less frequent. Eyes of male individuals also have considerably fewer and shorter (0.5 μm) cuticular hairs. Internally, the main difference is the somewhat broader (2.7 versus 2.4 μm) and longer (40–50 versus 32–40 μm) rhabdom in male animals and the significantly greater amount of screening pigment granules in the eyes of females. Anatomical features shared between males and females consist of bipartite crystalline cones, five equally‐contributing retinula cells and their rhabdomeres per ommatidium, a perirhabdomal space and two kinds of screening pigment granules. Ultrastructural derangements of rhabdom or microvilli following several hours of exposure to very bright spotlights are not apparent. The rhabdom length/width ratio for both male and female individuals is very high and, despite their essentially sedentary biology, allies D. porrecta most closely with pelagic amphipod species such as Hyperia and Phronima. It is concluded that from a sensory‐ecological viewpoint D. porrecta is a species that does not require vision for most of its vital functions, but that it does make use of vision in shallower water to evade predators. Males are likely to have more sensitive eyes than females, but those of the latter may posses greater resolution.
Victor Benno Meyer-Rochow
added a research item
The unusual case of a male Cryptotympana atrata cicada from China attempting to mate with a dead male conspecific is described and illustrated. Although hitherto unreported, necrophilic behaviour in the form of an attempted necrocoitus, involving dead male or female corpses, may not be as isolated a case as has been previously assumed, but it does not seem to have been mentioned earlier in the entomological literature. Although the described behaviour could have been an expression of a lack of opportunity to locate a cooperative female, several other possibilities, referred to in the Discussion, exist and should not be dismissed.
David Stella
added 3 research items
It has been suggested that structural ultraviolet (UV) patches on the wings of butterflies play a role in sexual selection. UV patches may be condition-dependent signals of mate quality. In the current study, we investigated associations between the morphological properties of two male wing patterns (one signalling and one non-signalling trait) and between these patterns and various environmental variables in seven species of the genus Gonepteryx (G. rhamni, G. nepalensis, G. maxima, G. amintha, G. aspasia, G. niphonica and G. cleopatra). We collected UV photographs of a total of 320 male specimens and analysed them using geometric morphometrics. Our results show that the shape of UV patches (a signalling trait) is more asymmetric than the wing venation (a non-signalling trait). In both examined traits, however, relationship between the environment and fluctuating asymmetry is significant only in a minority of species. Our results thus do not support the hypothesis that fluctuating asymmetry is a reliable indicator of an individual’s quality, in other words, that UV patches are condition-dependent trait. Examination of correlations between the two investigated shapes and the environment yielded similar results, and while the shape of UV patterns tended to be more strongly associated with the environment than the venation patterns, the correlation reached a level of significance only in a minority of cases. Due to the ambiguity of our findings, we cannot corroborate the hypothesis that UV patches act as biological signals of male quality in Gonepteryx butterflies, which is the case in various other related butterfly species. Finally, we found that UV patches discriminate among various Gonepteryx species better than the venation patterns do, which indicates that UV patches play a role in species recognition. It also suggests that UV patterns could be a useful taxonomic trait.
Ultraviolet patterns in butterflies have been recognized and studied for many years. They are frequently involved in both intraspecific and interspecific interactions. Only a handful of studies, however, have investigated possible links between ultraviolet (UV) reflectance and ecological properties in some genera of the Lepidoptera as a whole. This study examines the impact of habitat and distribution on UV reflectance patterns on the wings of 106 species and subspecies of Colias butterflies. Based on standardized digital photographs, we performed a multivariate analysis of relations between UV reflectance, preferred habitat (alpine, arctic, dry grasslands, humid, forest, and ubiquitous), and distribution area (Afrotropical, Nearctic, Neotropical, European, Caucaso-Anatolian, boreal Eurasian, Central Asian mountains, northern China and Japan, and northern Oriental region). UV patterns occur more frequently in the male (60 taxa) than in female (25 taxa) Coliads. This difference in presence of UV patterns is used for differentiating between the males and females of a given species or subspecies. Further possible explanations of this phenomenon are also discussed. This study also shows that particular configurations of UV patterns are significantly associated with particular distribution areas. This relation is relatively strong but overall trends remain unclear. Based on the results of this study, it can be concluded that there exists a significant difference in the configuration of UV reflectance between the sexes, and that the configuration of UV reflectance significantly interacts with the geographical distribution of Colias species and subspecies.
Victor Benno Meyer-Rochow
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ENTOMOLOGIE HEUTE Vol. 30: 45-53 Ultrastructure of the compound eye of a 0.65 mm long "three-eyed" gall midge 57 Entomologie heute 31 (2019) Entomologie heute 31 (2019): 57-72 Consequences of Extreme Miniaturization: The Ultrastructure of the Compound Eyes of a 0.65 mm Long "Three-Eyed" Gall Midge (Diptera; Cecidomyiidae) Folgen einer extremen Miniaturisierung: die Ultrastruktur des Facettenauges einer 0,65 mm langen "dreiäugigen" Gallmücke (Diptera; Cecidomyiidae) VICTOR BENNO MEYER-ROCHOW & YUMI YAMAHAMA Summary: Cecidomyiid midges of the genera Trisopsis and Lestodiplosis possess three compound eyes. The single dorsal compound eye of our only 0.65 mm long cecidomyiid specimen contained 90 omma-tidia and represented the fusion product of left and right dorsal moieties jointly covering an area at the top of the head of 70 00 μm 2. Each of the two latero-ventral compound eyes on either side of the head consisted of approximately 35 ommatidia that did not differ anatomically from those of the dorsal eye (with the exception of the interommatidial angles, which measured 10-12° and were thus much smaller than those of the dorsal eye). The retinal layers of both the dorsal and the two lateral eyes were extraordinarily thin, only measuring approximately 12 μm, but all ommatidia were capped by 8 μm thick and 8-10 μm wide corneal lenses with a dense and regular coverage of 160 nm high corneal nipples. Despite being a species of the order Diptera, for which open rhabdoms with non-connected rhabdomeres are characteristic, our tiny cecidomyiid possessed the fused type of rhabdom. The microvilli were of usual width for insect eyes, i.e. 65 nm in diameter. It is postulated that despite the reduction in body and eye size, microvilli could not be scaled down and rhabdomeres, too, had already reached their functional cross sectional limit of 1.5-2.0 μm in Diptera the size of Drosophila. A further reduction would have rendered the rhabdom ineffective as a waveguide. As the tiny insect was a swift fl yer and on the basis of the eye's anatomy it is discussed what the insect could possibly see with its tiny eyes. Zusammenfassung: Cecidomyiiden der Gattungen Trisopsis und Lestodiplosis besitzen drei Facettenaugen. Das unpaare dorsale Auge einer nur 0,65 mm lange n Cecidomyiide mit 90 Ommatidien stellt das Fusions-produkt der dorsalen Hälften der Augen auf beiden Seiten des Kopfes dar und bedeckt eine Fläche von 7000 μm 2. Jedes der latero-ventralen Facettenaugen besteht aus 35 Ommatidien, die sich anatomisch nicht von denen des Dorsalauges unterscheiden (außer dass ihre Interommatidialwinkel mit 10-12° viel schmaler als die des Dorsalauges sind). In beiden Fällen sind die Retinae nur 12 μm dick, aber alle Ommatidien besitzen 8 μm dicke corneale Linsen mit Durchmessern von 8-10 μm und einer dichten Beschichtung mit 160 nm hohen "Nippeln". Trotz ihrer Zugehörigkeit zur Ordnung der Diptera, deren Charakteristika sogenannte "offene Rhabdome" sind, besitzt unsere winzige Cecidomyiide ein geschlossenes Rhabdom mit den für Insektenaugen typischen 65 nm Mikrovillositäten. Es ist anzunehmen, dass eine Reduktion der Mikrovilli und Rhabdomere trotz Habitus-und Augenminiaturisierung nicht hat stattfi nden können, weil mit einem Durchmesser von 1,5-2,0 μm der Rhabdomere ein Grenzwert schon für Dipteren wie Drosophila erreicht wurde; dünnere Rhabdome können nicht als Lichtleiter fungieren. Der schnelle Flug des kleinen Insekts macht ein Sehvermögen wahrscheinlich; auf Basis der anatomischen Daten wird diskutiert, wozu die Augen dieses Insekts visuell in der Lage sein sollten.
Victor Benno Meyer-Rochow
added 2 research items
Amber contains numerous well-preserved adult aquatic insects (e.g., aquatic beetles – Coleoptera, water bugs – Heteroptera, dragonflies – Odonata, caddisflies – Trichoptera, mayflies – Ephemeroptera, stone flies – Plecoptera). Since amber is fossilised resin of terrestrial conifer trees, it is an enigma how aquatic insects have ended up in the resin. Based on field studies in a Hungarian forest along a freshwater creek we suggest that tree resin traps water-seeking flying polarotactic aquatic insects because of its property to polarise reflected light. The sticky tree resin was modelled by a water-proof, transparent, colourless insect-monitoring glue laid on vertical and horizontal fallen tree trunks next to the creek. Adults of various polarotactic aquatic insect species were trapped only by the horizontal sticky trunk. In earlier field experiments we showed that these insects find water by means of the horizontal polarisation of water-reflected light, and therefore are attracted to and land on all surfaces which reflect horizontally polarised light. Using imaging polarimetry, we revealed the criterion of polarisation-based trapping by resiny tree trunks. According to our observations, flying aquatic insects can be trapped by sticky (resiny) regions of fallen tree trunks that reflect horizontally polarised light and thus attract polarotactic species. The resin continues to flow out of the trees even when fallen over or fractured in a storm. Our findings support and complement an earlier hypothesis, according to which amber-preserved adult aquatic insects have been trapped by resiny bark when they dispersed over land.
Bumblebees have apposition compound eyes (one on either side of the head) and three small single-lens ocelli on the frons of their head capsule. The surface of the eye is smooth and interommatidial hairs, present in the honeybee, are not developed. Each ommatidium (approx. 26 µm in diameter) is capped by a hexagonal facet and contains in its centre a 3 µm wide, columnar light-perceiving structure known as the rhabdom. Rhabdoms consist of thousands of regularly aligned, fingerlike microvilli, which in their membranes contain the photopigment molecules. Axons from each ommatidium transmit the information of their photic environment to the visual centres of the brain, where behavioural reactions may be initiated. Since bumblebee eyes possess three classes of spectrally different sensitivity peaks in a ratio of 1:1:6 (UV = 353 nm, blue = 430 nm and green = 548 nm) per ommatidium, they use colour vision to find and select flower types that yield pollen and nectar. Ommatidial acceptance angles of at least 3° are used by the bumblebees to discriminate between different flower shapes and sizes, but their ability to detect polarized light appears to be used only for navigational purposes. A flicker fusion frequency of around 110 Hz helps the fast flying bumblebee to avoid obstacles. The small ocelli are strongly sen-sitive to ultraviolet radiation and green wavelengths and appear to act as sensors for light levels akin to a photometer. Unlike the bumblebee’s compound eyes, the ocelli would, however, be in-capable of forming a useful image.
Victor Benno Meyer-Rochow
added a research item
The coleopteran family Ptiliidae (featherwing beetles) includes some of the smallest insects known with most of the representatives of this family measuring less than 1 mm in body length. A small body size largely determines the morphology, physiology, and biology of an organism and affects the organization of complex sense organs. Information on the organization of the compound eyes of Ptiliidae is scarce. Using scanning electron microscopy we analyzed the eyes of representatives of all subfamilies and tribes and provide a detailed description of the eye ultrastructure of four species (Nephanes titan, Porophila mystacea, Nanosella sp. and Acrotrichis grandicollis) using transmission electron microscopy. The results are compared with available data on larger species of related groups of Staphyliniformia and scale quantitative analyses are performed. The eyes of Ptiliidae consist of 15–50 ommatidia 6–13 μm in diameter and all conform to the apposition acone type of eye with fused rhabdoms of banded organization. Each ommatidium has the typical cellular arrangement present also in the eyes of larger staphyliniform beetles, but strongly curved lenses, short cones, reduced pigment cells, a high density of pigment granules and certain modifications of the rhabdom seem typical of ptiliid eyes. Allometric analyses show that as body size decreases, the number of facets drops more steeply than their average size does.
David Stella
added a research item
The males of the Brimstone butterfly (Gonepteryx rhamni) have ultraviolet pattern on the dorsal surfaces of their wings. Using geometric morphometrics, we have analysed correlations between environmental variables (climate, productivity) and shape variability of the ultraviolet pattern and the forewing in 110 male specimens of G. rhamni collected in the Palaearctic zone. To start with, we subjected the environmental variables to principal component analysis (PCA). The first PCA axis (precipitation, temperature, latitude) significantly correlated with shape variation of the ultraviolet patterns across the Palaearctic. Additionally, we have performed two-block partial least squares (PLS) analysis to assess co-variation between intraspecific shape variation and the variation of 11 environmental variables. The first PLS axis explained 93 % of variability and represented the effect of precipitation, temperature and latitude. Along this axis, we observed a systematic increase in the relative area of ultraviolet colouration with increasing temperature and precipitation and decreasing latitude. We conclude that the shape variation of ultraviolet patterns on the forewings of male Brimstones is correlated with large-scale environmental factors.
Victor Benno Meyer-Rochow
added a research item
Biofoam in spittlebugs has traditionally been seen as a defence against predation and a microclimate that reduces the risks of overheating and drying out. This study addresses the possible role of the foam as a light attenuator. 2. Nymphs exhibit higher mortalities when reared under brighter light (1800–2000 lux) than under less bright light (600–800 lux). At all developmental stages, photoavoidance is strongest when the nymphs are depleted of foam covers. First- and second-instar nymphs appear to be the most vulnerable to exposures by bright light. 3. Smaller bubbles are more effective as light attenuators than are larger ones. As younger instars possess smaller canals from which bubbles are released and, furthermore, exhibit higher concentrations of proteins in bubble liquid, they can produce smaller-sized bubbles and their foams are more effective at reducing light than are those of older nymphs. 4. The findings of this study show that most of the visible and UV radiation is reflected by the foam: transmittance of visible light was 15% at 600 nm and 12% at 350 nm. 5. These results demonstrate that spittlebug foam also possesses properties that render it an effective barrier against potentially damaging solar radiation.
Victor Benno Meyer-Rochow
added a research item
When individuals of the crustacean Mysis relicta are fully dark- adapted and preparations for electroretinogramme recordings are performed in infra-red light of wavelength >730 run, responses to 300 ms flashes of light can be recorded. Though this is the first time that responses to such long wavelengths have ever been reported for any invertebrate photoreceptor, the authors suggest that near infra-red sensitivity in arthropods could be more widespread, and that because of very long adaptation and sensitivity regeneration times preparations should not be carried out in red light, hitherto deemed invisible to most arthropods, but with the aid of an infra-red image converter and a filter at wavelengths >800 run.
Victor Benno Meyer-Rochow
added 3 research items
Evolution need not resemble a tree, but could be a pyramid (Gould 1989) with a tip of a few successful and/or lucky species (extended to cell types in this discussion) and perhaps applicable to pinealocytes. The much greater number of pineal cell types in lamprey pineal organs than in the mammalian pineal, clould be interpreted as a 'pool of hopefuls' from which only one or two kinds of cells (now known as the typical mammalian pinealocytes) were able to 'make it' into the mammalian organ, while the remainder, for whatever reason, were left behind. The mammalian pinealocyte would then not be a regressed or modified photoreceotive cell, but would represent an older cell type from the dawn of vertebrate evolution, neither conductor nor player, but 'obedient follower', marching to the tune that comes from the extra-pineal pacemaker like the SCN, for instance.
Larvae of the weakly blue-luminescent fungus gnat Keroplatus nipponicus possess on either side of their heads a small black stemmatal eye with a plano-convex lens approximately 25 μm in diameter. In total, 12–14 retinula cells give rise to a centrally fused rhabdom of up to 8 μm in diameter. The rhabdom's constituent microvilli, approximately 70 nm in width, are roughly orthogonally oriented, a requirement for polarization sensitivity. Screening pigment granules are abundant in the retinula cells and measure at least 1 μm in diameter. In comparison with the stemmatal eye of the brightly luminescent Arachnocampa luminosa, that of K. nipponicus is considerably smaller with a poorer developed lens and a rhabdom that is less voluminous, but possesses wider microvilli. Although the larval eye of K. nipponicus can be expected to be functional, as the larvae react to light with a behavioural response, the eyes are probably mainly involved in the detection of ambient light levels and not, as in A. luminosa, also in responding to the luminescence of nearby conspecifics.
Victor Benno Meyer-Rochow
added 2 research items
In polarization-sensitive insect species an orthogonal arrangement of photoreceptive microvilli is a characteristic feature. Mosquito eyes had not revealed such feature and polarization sensitivity (PS) was considered to be non-existent in them. Recently, however, gravid Aedes (Stegomyia) aegypti females were found to possess PS, sequels of which could be demonstrated only in the absence of chemicals emitted by conspecifics. Therefore, PS in Ae. aegypti, unlike that of other aquatic insects, apparently does not play a dominant role in locating water bodies and is difficult to demonstrate in situations free of chemical cues. Here, we present behavioural evidence with Ae. aegypti females, exposed to large-field optomotor stimuli based solely on polarization contrast. Under conditions with stripes of alternating orthogonal directions of polarization, clear optomotor responses were elicited, no different from those in response to a rotating drum with vertical black and white stripes. Thus, Ae. aegypti is indeed polarization-sensitive; it reacts to vertically-striped contrast patterns with low spatial frequency on the basis of both intensity and polarization differences between the stripes.
The subject of our investigation was the visual features of wing colour with special focus on the UV reflectance in the green-veined white (Pieris napi). Previous studies had concluded that UV reflectance on dorsal wing surfaces is found only in the female P. napi. Based on UV sensitive photography, we analysed a correlation between 12 geographic and environmental factors and UV reflectance patterns on three patches on the forewings of 407 P. napi specimens from the Palaearctic region. Results had shown that females significantly differ from males: they exhibit a 25% higher UV reflectance. To investigate whether and how UV reflectance levels on the forewings and hindwings of both sexes are influenced by the environment, we performed a PCA with several environmental variables. For several variables (in particular, latitude and longitude, mean annual temperature and precipitation, and temperature annual range and altitude), the Generalized linear model (GLM) model revealed a significant correlation in both sexes. This suggests a link between UV reflectance levels and the environment and distribution of P. napi. We found that stronger UV reflectance is associated with generally more hostile environments and concluded that large-scale environmental factors influence the UV reflectance on the forewings of both male and female green-veined white butterflies. This article is protected by copyright. All rights reserved.
Victor Benno Meyer-Rochow
added a project goal
To investigate structural and functional adaptations of photoreceptive sensors of organisms under a variety of conditions.