夜行性昆虫微光视觉行为及其视觉适应机制

作为昆虫种群的重要组成部分,夜行性昆虫成功进化出了与其生存环境相适应的感觉机制,普遍认为夜行性昆虫主要依靠嗅觉和机械性感受等来探索环境,其视觉器官发生了退化或功能丧失。近年来,随着红外夜视、视网膜电位(electroretinogram, ERG)和视觉神经等生物新技术的应用,昆虫视觉生态学研究出现了突破性进展,自2002年以来陆续发现蛾类、蜜蜂和蜣螂等夜行性昆虫进化出了非凡的微光视觉(dim-light vision)能力,在夜晚(光照强度低于0.3 lx)依然可以如同在明亮的白天一样清晰、准确地感知目标物体特定的视觉特性,如明暗、颜色、形状、大小、对比度、偏振光和运动状态等,展现出视觉调控夜行性昆虫行为活动的巨大潜力。此外,这些夜行性昆虫复眼瞳孔、小眼焦距、视杆和色素颗粒等方面进化出了一些相应的形态生理特征,以提高光学灵敏度适应夜间微光环境。鉴于夜行性昆虫微光视觉行为及其视觉适应机制的研究尚处于起步阶段,仅见于少数访花昆虫或粪食性昆虫,建议加强以下几个方面的研究：(1)重大夜行性农业害虫的微光视觉及其应用的研究;(2)非典型重叠复眼的光学结构特征及其应对微光环境的适应机制研究;(3)夜行性昆虫响应微光环境的视觉适应机制研究;(4)基于夜行性昆虫微光视觉行为研发新型害虫防控技术。     

Vision in the deep sea

The deep sea is the largest habitat on earth. Its three great faunal environments--the twilight mesopelagic zone, the dark bathypelagic zone and the vast flat expanses of the benthic habitat--are home to a rich fauna of vertebrates and invertebrates. In the mesopelagic zone (150-1000 m), the down-welling daylight creates an extended scene that becomes increasingly dimmer and bluer with depth. The available daylight also originates increasingly from vertically above, and bioluminescent point-source flashes, well contrasted against the dim background daylight, become increasingly visible. In the bathypelagic zone below 1000 m no daylight remains, and the scene becomes entirely dominated by point-like bioluminescence. This changing nature of visual scenes with depth--from extended source to point source--has had a profound effect on the designs of deep-sea eyes, both optically and neurally, a fact that until recently was not fully appreciated. Recent measurements of the sensitivity and spatial resolution of deep-sea eyes--particularly from the camera eyes of fishes and cephalopods and the compound eyes of crustaceans--reveal that ocular designs are well matched to the nature of the visual scene at any given depth. This match between eye design and visual scene is the subject of this review. The greatest variation in eye design is found in the mesopelagic zone, where dim down-welling daylight and bio-luminescent point sources may be visible simultaneously. Some mesopelagic eyes rely on spatial and temporal summation to increase sensitivity to a dim extended scene, while others sacrifice this sensitivity to localise pinpoints of bright bioluminescence. Yet other eyes have retinal regions separately specialised for each type of light. In the bathypelagic zone, eyes generally get smaller and therefore less sensitive to point sources with increasing depth. In fishes, this insensitivity, combined with surprisingly high spatial resolution, is very well adapted to the detection and localisation of point-source bioluminescence at ecologically meaningful distances. At all depths, the eyes of animals active on and over the nutrient-rich sea floor are generally larger than the eyes of pelagic species. In fishes, the retinal ganglion cells are also frequently arranged in a horizontal visual streak, an adaptation for viewing the wide flat horizon of the sea floor, and all animals living there. These and many other aspects of light and vision in the deep sea are reviewed in support of the following conclusion: it is not only the intensity of light at different depths, but also its distribution in space, which has been a major force in the evolution of deep-sea vision.     

Visual reliability and information rate in the retina of a nocturnal bee

Nocturnal animals relying on vision typically have eyes that are optically and morphologically adapted for both increased sensitivity and greater information capacity in dim light. Here, we investigate whether adaptations for increased sensitivity also are found in their photoreceptors by using closely related and fast-flying nocturnal and diurnal bees as model animals. The nocturnal bee Megalopta genalis is capable of foraging and homing by using visually discriminated landmarks at starlight intensities. Megalopta's near relative, Lasioglossum leucozonium, performs these tasks only in bright sunshine. By recording intracellular responses to Gaussian white-noise stimuli, we show that photoreceptors in Megalopta actually code less information at most light levels than those in Lasioglossum. However, as in several other nocturnal arthropods, Megalopta's photoreceptors possess a much greater gain of transduction, indicating that nocturnal photoreceptors trade information capacity for sensitivity. By sacrificing photoreceptor signal-to-noise ratio and information capacity in dim light for an increased gain and, thus, an increased sensitivity, this strategy can benefit nocturnal insects that use neural summation to improve visual reliability at night.     

The costs of becoming nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic Salmon

1. Most animals are active by day or by night, but not both; juvenile salmonids are unusual in that they switch from being predominantly diurnal for most of the year to being nocturnal in winter. They are visual foragers, and adaptations for high visual acuity at daytime light intensities are generally incompatible with sensitive night vision. Here we test whether juvenile Atlantic Salmon Salmo salar are able to maintain their efficiency of prey capture when switching between diurnal and nocturnal foraging.
2. By testing the ability of the fish to acquire drifting food items under a range of manipulated light intensities, we show that the foraging efficiency of juvenile salmon is high at light intensities down to those equivalent to dawn or dusk, but drops markedly at lower levels of illumination: even under the best night condition (full moon and clear sky), the feeding efficiency is only 35% of their diurnal efficiency, and fish will usually be feeding at less than 10% (whenever the moon is not full, skies are overcast or when in the shade of bankside trees). Fish were unable to feed on drifting prey when in complete darkness.
3. The ability of juvenile salmon to detect prey under different light intensities is similar to that of other planktivorous or drift-feeding species of fish; they thus appear to have no special adaptations for nocturnal foraging.
4. While winter drift abundance is slightly higher by night than by day, the difference is not enough to compensate for the loss in foraging efficiency. We suggest that juvenile salmon can nonetheless switch to nocturnal foraging in winter because their food requirements are low, many individuals adopting a strategy in which intake is suppressed to the minimum that ensures survival.     

Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer

The common backswimmer, Notonecta glauca, uses vision by day and night for functions such as underwater prey animal capture and flight in search of new habitats. Although previous studies have identified some of the physiological mechanisms facilitating such flexibility in the animal''s vision, neither the biophysics of Notonecta photoreceptors nor possible cellular adaptations are known. Here, we studied Notonecta photoreceptors using patch-clamp and intracellular recording methods. Photoreceptor size (approximated by capacitance) was positively correlated with absolute sensitivity and acceptance angles. Information rate measurements indicated that large and more sensitive photoreceptors performed better than small ones. Our results suggest that backswimmers are adapted for vision in both dim and well-illuminated environments by having open-rhabdom eyes with large intrinsic variation in absolute sensitivity among photoreceptors, exceeding those found in purely diurnal or nocturnal species. Both electrophysiology and microscopic analysis of retinal structure suggest two retinal subsystems: the largest peripheral photoreceptors provide vision in dim light and the smaller peripheral and central photoreceptors function primarily in sunlight, with light-dependent pigment screening further contributing to adaptation in this system by dynamically recruiting photoreceptors with varying sensitivity into the operational pool.     

HOW A HARBOR SEAL SEES THE NIGHT SKY

Astronavigation is a possible mechanism of offshore orientation in marine mammals. However, the basic prerequisite for astronavigation is to see enough stars of the night sky. This cannot be taken for granted in seals as, due to adaptations of their dioptric apparatus to the optical properties of water, seals are supposed to be myopic and astigmatic when out of the water under low light conditions. Using various real and artificial stars in a go/no-go response paradigm we therefore determined the minimum brightness at which a harbor seal ( Phoca vitulina ) can detect stars. The dark-adapted seal was trained to look through an empty tube ("seal telescope") and to retract its head only when a star appeared at the opposite aperture. The seal reliably detected Venus or Sirius becoming suddenly visible when the telescope was moved across the night sky. Detection thresholds were determined using artificial stars (parallel light identical to starlight coming from the universe) of predefined brightness generated by an optical system installed in front of the seal's telescope. The seal detected artificial stars down to 4.4 stellar magnitudes. Although these results cannot present evidence for astronavigation, they imply that seals should see enough stars to allow such orientation mechanisms.     

Dim Light at Night Does Not Disrupt Timing or Quality of Sleep in Mice

Artificial nighttime illumination has recently become commonplace throughout the world; however, in common with other animals, humans have not evolved in the ecological context of chronic light at night. With prevailing evidence linking the circadian, endocrine, immune, and metabolic systems, understanding these relationships is important to understanding the etiology and progression of several diseases. To eliminate the covariate of sleep disruption in light at night studies, researchers often use nocturnal animals. However, the assumption that light at night does not affect sleep in nocturnal animals remains unspecified. To test the effects of light at night on sleep, we maintained Swiss-Webster mice in standard light/dark (LD) or dim light at night (DLAN) conditions for 8–10 wks and then measured electroencephalogram (EEG) and electromyogram (EMG) biopotentials via wireless telemetry over the course of two consecutive days to determine differences in sleep timing and homeostasis. Results show no statistical differences in total percent time, number of episodes, maximum or average episode durations in wake, slow-wave sleep (SWS), or rapid eye movement (REM) sleep. No differences were evident in SWS delta power, an index of sleep drive, between groups. Mice kept in DLAN conditions showed a relative increase in REM sleep during the first few hours after the dark/light transition. Both groups displayed normal 24-h circadian rhythms as measured by voluntary running wheel activity. Groups did not differ in body mass, but a marked negative correlation of body mass with percent time spent awake and a positive correlation of body mass with time spent in SWS was evident. Elevated body mass was also associated with shorter maximum wake episode durations, indicating heavier animals had more trouble remaining in the wake vigilance state for extended periods of time. Body mass did not correlate with activity levels, nor did activity levels correlate with time spent in different sleep states. These data indicate that heavier animals tend to sleep more, potentially contributing to further weight gain. We conclude that chronic DLAN exposure does not significantly affect sleep timing or homeostasis in mice, supporting the use of dim light with nocturnal rodents in chronobiology research to eliminate the possible covariate of sleep disruption.     

The visual ecology of a deep-sea fish,the escolar Lepidocybium flavobrunneum (Smith, 1843)

Escolar (Lepidocybium flavobrunneum, family Gempylidae) are large and darkly coloured deep-sea predatory fish found in the cold depths (more than 200 m) during the day and in warm surface waters at night. They have large eyes and an overall low density of retinal ganglion cells that endow them with a very high optical sensitivity. Escolar have banked retinae comprising six to eight layers of rods to increase the optical path length for maximal absorption of the incoming light. Their retinae possess two main areae of higher ganglion cell density, one in the ventral retina viewing the dorsal world above (with a moderate acuity of 4.6 cycles deg⁻¹), and the second in the temporal retina viewing the frontal world ahead. Electrophysiological recordings of the flicker fusion frequency (FFF) in isolated retinas indicate that escolar have slow vision, with maximal FFF at the highest light levels and temperatures (around 9 Hz at 23°C) which fall to 1–2 Hz in dim light or cooler temperatures. Our results suggest that escolar are slowly moving sit-and-wait predators. In dim, warm surface waters at night, their slow vision, moderate dorsal resolution and highly sensitive eyes may allow them to surprise prey from below that are silhouetted in the downwelling light.     

Nocturnal vision and landmark orientation in a tropical halictid bee

BACKGROUND: Some bees and wasps have evolved nocturnal behavior, presumably to exploit night-flowering plants or avoid predators. Like their day-active relatives, they have apposition compound eyes, a design usually found in diurnal insects. The insensitive optics of apposition eyes are not well suited for nocturnal vision. How well then do nocturnal bees and wasps see? What optical and neural adaptations have they evolved for nocturnal vision? RESULTS: We studied female tropical nocturnal sweat bees (Megalopta genalis) and discovered that they are able to learn landmarks around their nest entrance prior to nocturnal foraging trips and to use them to locate the nest upon return. The morphology and optics of the eye, and the physiological properties of the photoreceptors, have evolved to give Megalopta's eyes almost 30 times greater sensitivity to light than the eyes of diurnal worker honeybees, but this alone does not explain their nocturnal visual behavior. This implies that sensitivity is improved by a strategy of photon summation in time and in space, the latter of which requires the presence of specialized cells that laterally connect ommatidia into groups. First-order interneurons, with significantly wider lateral branching than those found in diurnal bees, have been identified in the first optic ganglion (the lamina ganglionaris) of Megalopta's optic lobe. We believe that these cells have the potential to mediate spatial summation. CONCLUSIONS: Despite the scarcity of photons, Megalopta is able to visually orient to landmarks at night in a dark forest understory, an ability permitted by unusually sensitive apposition eyes and neural photon summation.     

Concentration Units

Most people are familiar with the concept that animals come in all shapes and sizes and that the body plan of some animals can completely transform during their lifetime. Well-known examples of such complex life cycles of terrestrial animals include butterflies and frogs. Many people are unaware, however, that complex life cycles are exceedingly prevalent in marine environments. Marine invertebrates, such as sea urchins, sea stars, and crabs, all have a microscopic pelagic larval stage that looks nothing at all like the familiar adult form. The authors have developed a lesson to teach students about complex life cycles using crab larvae and adult crabs. This lesson allows 3rd- to 6th-grade students to compare and contrast body plans while learning about adaptations the larvae and adults have made to their respective habitats. Throughout the lesson, students practice skills important for scientific inquiry: making observations, drawing what they see, asking and answering questions, and learning to use scientific tools such as microscopes.     

Eye shape and the nocturnal bottleneck of mammals

Most vertebrate groups exhibit eye shapes that vary predictably with activity pattern. Nocturnal vertebrates typically have large corneas relative to eye size as an adaptation for increased visual sensitivity. Conversely, diurnal vertebrates generally demonstrate smaller corneas relative to eye size as an adaptation for increased visual acuity. By contrast, several studies have concluded that many mammals exhibit typical nocturnal eye shapes, regardless of activity pattern. However, a recent study has argued that new statistical methods allow eye shape to accurately predict activity patterns of mammals, including cathemeral species (animals that are equally likely to be awake and active at any time of day or night). Here, we conduct a detailed analysis of eye shape and activity pattern in mammals, using a broad comparative sample of 266 species. We find that the eye shapes of cathemeral mammals completely overlap with nocturnal and diurnal species. Additionally, most diurnal and cathemeral mammals have eye shapes that are most similar to those of nocturnal birds and lizards. The only mammalian clade that diverges from this pattern is anthropoids, which have convergently evolved eye shapes similar to those of diurnal birds and lizards. Our results provide additional evidence for a nocturnal ‘bottleneck’ in the early evolution of crown mammals.     

Repeated eye reduction events reveal multiple pathways to degeneration in a family of marine snails

Eye reduction occurs in many troglobitic, fossorial, and deep‐sea animals but there is no clear consensus on its evolutionary mechanism. Given the highly conserved and pleiotropic nature of many genes instrumental to eye development, degeneration might be expected to follow consistent evolutionary trajectories in closely related animals. We tested this in a comparative study of ocular anatomy in solariellid snails from deep and shallow marine habitats using morphological, histological, and tomographic techniques, contextualized phylogenetically. Of 67 species studied, 15 lack retinal pigmentation and at least seven have eyes enveloped by surrounding epithelium. Independent instances of reduction follow numerous different morphological trajectories. We estimate eye loss has evolved at least seven times within Solariellidae, in at least three different ways: characters such as pigmentation loss, obstruction of eye aperture, and “lens” degeneration can occur in any order. In one instance, two morphologically distinct reduction pathways appear within a single genus, Bathymophila. Even amongst closely related animals living at similar depths and presumably with similar selective pressures, the processes leading to eye loss have more evolutionary plasticity than previously realized. Although there is selective pressure driving eye reduction, it is clearly not morphologically or developmentally constrained as has been suggested by previous studies.     

Hornets Can Fly at Night without Obvious Adaptations of Eyes and Ocelli

Hornets, the largest social wasps, have a reputation of being facultatively nocturnal. Here we confirm flight activity of hornet workers in dim twilight. We studied the eyes and ocelli of European hornets (Vespa crabro) and common wasps (Vespula vulgaris) with the goal to find the optical and anatomical adaptations that enable them to fly in dim light. Adaptations described for obligately nocturnal hymenoptera such as the bees Xylocopa tranquebarica and Megalopta genalis and the wasp Apoica pallens include large ocelli and compound eyes with wide rhabdoms and large facet lenses. Interestingly, we did not find any such adaptations in hornet eyes or ocelli. On the contrary, their eyes are even less sensitive than those of the obligately diurnal common wasps. Therefore we conclude that hornets, like several facultatively nocturnal bee species such as Apis mellifera adansonii, A. dorsata and X. tenuiscapa are capable of seeing in dim light simply due to the large body and thus eye size. We propose that neural pooling strategies and behavioural adaptations precede anatomical adaptations in the eyes and ocelli when insects with apposition compound eyes turn to dim light activity.     

Elephants and human color-blind deuteranopes have identical sets of visual pigments

Being the largest land mammals, elephants have very few natural enemies and are active during both day and night. Compared with those of diurnal and nocturnal animals, the eyes of elephants and other arrhythmic species, such as many ungulates and large carnivores, must function in both the bright light of day and dim light of night. Despite their fundamental importance, the roles of photosensitive molecules, visual pigments, in arrhythmic vision are not well understood. Here we report that elephants (Loxodonta africana and Elephas maximus) use RH1, SWS1, and LWS pigments, which are maximally sensitive to 496, 419, and 552 nm, respectively. These light sensitivities are virtually identical to those of certain "color-blind" people who lack MWS pigments, which are maximally sensitive to 530 nm. During the day, therefore, elephants seem to have the dichromatic color vision of deuteranopes. During the night, however, they are likely to use RH1 and SWS1 pigments and detect light at 420-490 nm.     

Retinal and optical adaptations for nocturnal vision in the halictid bee<Emphasis Type="Italic"> Megalopta genalis</Emphasis>

The apposition compound eye of a nocturnal bee, the halictid Megalopta genalis, is described for the first time. Compared to the compound eye of the worker honeybee Apis mellifera and the diurnal halictid bee Lasioglossum leucozonium, the eye of M. genalis shows specific retinal and optical adaptations for vision in dim light. The major anatomical adaptations within the eye of the nocturnal bee are (1) nearly twofold larger ommatidial facets and (2) a 4–5 times wider rhabdom diameter than found in the diurnal bees studied. Optically, the apposition eye of M. genalis is 27 times more sensitive to light than the eyes of the diurnal bees. This increased optical sensitivity represents a clear optical adaptation to low light intensities. Although this unique nocturnal apposition eye has a greatly improved ability to catch light, a 27-fold increase in sensitivity alone cannot account for nocturnal vision at light intensities that are 8 log units dimmer than during daytime. New evidence suggests that additional neuronal spatial summation within the first optic ganglion, the lamina, is involved.B.G. is thankful for travel awards from the Royal Physiographic Society, the Per Westlings Fond, the Foundation of Dagny and Eilert Ekvall and the Royal Swedish Academy of Sciences. E.J.W. is grateful for the support of a Smithsonian Short-Term Research Fellowship, the Swedish Research Council, the Crafoord Foundation, the Wenner-Gren Foundation and the Royal Physiographic Society of Lund for their ongoing support     

Nocturnal insects use optic flow for flight control

To avoid collisions when navigating through cluttered environments, flying insects must control their flight so that their sensory systems have time to detect obstacles and avoid them. To do this, day-active insects rely primarily on the pattern of apparent motion generated on the retina during flight (optic flow). However, many flying insects are active at night, when obtaining reliable visual information for flight control presents much more of a challenge. To assess whether nocturnal flying insects also rely on optic flow cues to control flight in dim light, we recorded flights of the nocturnal neotropical sweat bee, Megalopta genalis, flying along an experimental tunnel when: (i) the visual texture on each wall generated strong horizontal (front-to-back) optic flow cues, (ii) the texture on only one wall generated these cues, and (iii) horizontal optic flow cues were removed from both walls. We find that Megalopta increase their groundspeed when horizontal motion cues in the tunnel are reduced (conditions (ii) and (iii)). However, differences in the amount of horizontal optic flow on each wall of the tunnel (condition (ii)) do not affect the centred position of the bee within the flight tunnel. To better understand the behavioural response of Megalopta, we repeated the experiments on day-active bumble-bees (Bombus terrestris). Overall, our findings demonstrate that despite the limitations imposed by dim light, Megalopta-like their day-active relatives-rely heavily on vision to control flight, but that they use visual cues in a different manner from diurnal insects.     

Scotopic illumination enhances entrainment of circadian rhythms to lengthening light:dark cycles

Endogenously generated circadian rhythms are synchronized with the environment through phase-resetting actions of light. Starlight and dim moonlight are of insufficient intensity to reset the phase of the clock directly, but recent studies have indicated that dim nocturnal illumination may otherwise substantially alter entrainment to bright lighting regimes. In this article, the authors demonstrate that, compared to total darkness, dim illumination at night (< 0.010 lux) alters the entrainment of male Syrian hamsters to bright-light T cycles, gradually increasing in cycle length (T) from 24 h to 30 h. Only 1 of 18 hamsters exposed to complete darkness at night entrained to cycles of T > 26 h. In the presence of dim nocturnal illumination, however, a majority of hamsters entrained to Ts of 28 h or longer. The presence or absence of a running wheel had only minor effects on entrainment to lengthening light cycles. The results further establish the potent effects of scotopic illumination on circadian entrainment and suggest that naturalistic ambient lighting at night may enhance the plasticity of the circadian pacemaker.     

Illuminance preferences of nocturnal primates

Laboratory tests reveal a preference for illuminances in a broad range of night light by individuals belonging to four species of nocturnal primates (Aotus trivirgatus, Galago crassicaudatus, Galago senegalensis, andNycticebus coucang). In volitional tests the animals altered the light level very frequently, in one case as often as every 7 sec. In these tests the animals tended to avoid total darkness and extremely dim light as well as moderately bright light. These avoided levels, particularly extremely dim light and darkness, inhibited locomotor activity. The greater bush babies preferred dimmer light for manipulative activities than for locomotion. Nocturnal primates differ from nocturnal rodents in being much more highly motivated to seek variety and frequent stimulus change when in deprivation conditions, and in their avoiding and being markedly inhibited by darkness.     

Structural variation in the inner ears of four deep-sea elopomorph fishes

Deep-sea fishes have evolved in dark or dimly lit environments devoid of the visual cues available to shallow-water species. Because of the limited opportunity for visual scene analysis by deep-sea fishes, it is reasonable to hypothesize that the inner ears of at least some such species may have evolved structural adaptations to enhance hearing capabilities in lieu of vision. As an initial test of this hypothesis, scanning electron microscopy was used to examine the structure of the inner ears of four deep-sea elopomorph species inhabiting different depths: Synaphobranchus kaupii, Synaphobranchus bathybius, Polyacanthonotus challengeri, and Halosauropsis macrochir. The shape of the sensory epithelia and hair cell ciliary bundle orientation of the saccule, lagena, and utricle, the three otolithic organs associated with audition and vestibular function, are described. The saccules of all four species have a common, alternating ciliary bundle orientation pattern. In contrast, the lagena exhibits more interspecific diversity in shape and ciliary bundle orientation, suggesting that it has special adaptations in these species. The macula neglecta, a sensory epithelium of unknown function, is present in all four species.