Higher-order neural processing tunes motion neurons to visual ecology in three species of hawkmoths.

To sample information optimally, sensory systems must adapt to the ecological demands of each animal species. These adaptations can occur peripherally, in the anatomical structures of sensory organs and their receptors; and centrally, as higher-order neural processing in the brain. While a rich body of investigations has focused on peripheral adaptations, our understanding is sparse when it comes to central mechanisms. We quantified how peripheral adaptations in the eyes, and central adaptations in the wide-field motion vision system, set the trade-off between resolution and sensitivity in three species of hawkmoths active at very different light levels: nocturnal Deilephila elpenor, crepuscular Manduca sexta, and diurnal Macroglossum stellatarum. Using optical measurements and physiological recordings from the photoreceptors and wide-field motion neurons in the lobula complex, we demonstrate that all three species use spatial and temporal summation to improve visual performance in dim light. The diurnal Macroglossum relies least on summation, but can only see at brighter intensities. Manduca, with large sensitive eyes, relies less on neural summation than the smaller eyed Deilephila, but both species attain similar visual performance at nocturnal light levels. Our results reveal how the visual systems of these three hawkmoth species are intimately matched to their visual ecologies.

How dim is dim? Precision of the celestial compass in moonlight and sunlight.

Prominent in the sky, but not visible to humans, is a pattern of polarized skylight formed around both the Sun and the Moon. Dung beetles are, at present, the only animal group known to use the much dimmer polarization pattern formed around the Moon as a compass cue for maintaining travel direction. However, the Moon is not visible every night and the intensity of the celestial polarization pattern gradually declines as the Moon wanes. Therefore, for nocturnal orientation on all moonlit nights, the absolute sensitivity of the dung beetle's polarization detector may limit the precision of this behaviour. To test this, we studied the straight-line foraging behaviour of the nocturnal ball-rolling dung beetle Scarabaeus satyrus to establish when the Moon is too dim--and the polarization pattern too weak--to provide a reliable cue for orientation. Our results show that celestial orientation is as accurate during crescent Moon as it is during full Moon. Moreover, this orientation accuracy is equal to that measured for diurnal species that orient under the 100 million times brighter polarization pattern formed around the Sun. This indicates that, in nocturnal species, the sensitivity of the optical polarization compass can be greatly increased without any loss of precision.

Light scattering by selected zooplankton from the Gulf of Aqaba.

Light scattering by zooplankton was investigated as a major factor undermining transparency camouflage in these pelagic animals. Zooplankton of differing transparencies--including the hyperiid amphipod Anchylomera blossevillei, an unknown gammarid amphipod species, the brine shrimp Artemia salina, the euphausiid shrimp Euphausia diomedeae, the isopod Gnathia sp., the copepods Pontella karachiensis, Rhincalanus sp. and Sapphirina sp., the chaetognath Sagitta elegans and an enteropneust tornaria larva--were illuminated dorsally with white light (400-700 nm). Spectral measurements of direct transmittance as well as relative scattered radiances at angles of 30 degrees , 90 degrees , 150 degrees and 180 degrees from the light source were taken. The animals sampled had transparencies between 1.5% and 75%. For all species, the highest recorded relative scattered radiance was at 30 degrees , with radiances reaching 38% of the incident radiance for the amphipod A. blossevillei. Scattering patterns were also found to be species-specific for most animals. Relative scattered radiances were used to estimate sighting distances at different depths. These calculations predict that all of the examined zooplankton are brighter than the background radiance when viewed horizontally, or from diagonally above or below at shallow depths. Thus, in contrast to greater depths, the best strategy for detecting transparent zooplankton in the epipelagic environment may be to search for them from above while looking diagonally downwards, looking horizontally or looking from below diagonally upwards. Looking directly upwards proved to be more beneficial than the other viewing angles only when the viewed animal was at depths greater than 40 m.

A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum.

Many animals have been shown to use the pattern of polarized light in the sky as an optical compass. Specialised photoreceptors are used to analyse this pattern. We here present evidence for an eye design suitable for polarized skylight navigation in the flightless desert scarab Pachysoma striatum. Morphological and electrophysiological studies show that an extensive part of the dorsal eye is equivalent to the dorsal rim area used for polarized light navigation in other insects. A polarization-sensitivity of 12.8 (average) can be recorded from cells sensitive to the ultraviolet spectrum of light. Features commonly known to increase the visual fields of polarization-sensitive photoreceptors, or to decrease their spatial resolution, are not found in the eye of this beetle. We argue that in this insect an optically unspecialised area for polarized light detection allows it not be used exclusively for polarized light navigation.

Temperature-induced pupil movements in insect superposition eyes.

In this paper, we describe the hitherto largely overlooked effect of temperature on the pupil of insect compound eyes. In the turnip moth Agrotis segetum and in two other nocturnal insects with superposition eyes, the lacewing Euroleon nostras and the codling moth Cydia pomonella, the pupil not only opens and closes with changes in the ambient light level, as expected, but also with changes in temperature in the absence of light. In complete darkness, the pupil of A. segetum responds over a wide range of temperatures, with the pupillary pigments migrating to a light-adapted position when the animal is exposed to either low or high temperatures. At temperatures between 21.0 and 22.7 C, the pigments migrate to the fully dark-adapted position, resulting in an open pupil and maximal eye glow. Pupil closure at high temperatures shows two distinct thresholds: the first at 23.8+/-0.7 C and a second some degrees higher at 25.7+/-1.2 C (means +/- s.d., N=10). Temperatures exceeding the first threshold (the activation temperature, T(a)) initiate a closure of the pupil that is completed when the temperature exceeds the second threshold (the closure temperature, T(c)), which causes rapid and complete migration of pigment to the light-adapted position. All temperatures above T(a) affect the pupil, but only temperatures exceeding T(c) result in complete closure. Temperatures between T(a) and T(c) cause a slow, partial and rather unpredictable closure. The lacewing and the codling moth both show very similar responses to those of A. segetum, suggesting that this response to temperature is widespread in superposition eyes. The possibility that the ambient temperature could be used to pre-adapt the eye to different light intensities is discussed.

Visual discrimination: Seeing the third quality of light.

Objects can differ in brightness and colour. At least that is what our own visual system tells us. It now seems that stomatopod shrimps, and possibly also cephalopod molluscs, can see the direction of the electric vector of light, in much the same way we see colour.

Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation.

Animals which need to see well at night generally have eyes with wide pupils. This optical strategy to improve photon capture may be improved neurally by summing the outputs of neighbouring visual channels (spatial summation) or by increasing the length of time a sample of photons is counted by the eye (temporal summation). These summation strategies only come at the cost of spatial and temporal resolution. A simple analytical model is developed to investigate whether the improved photon catch afforded by summation really improves vision in dim light, or whether the losses in resolution actually make vision worse. The model, developed for both vertebrate camera eyes and arthropod compound eyes, calculates the finest spatial detail perceivable by a given eye design at a specified light intensity and image velocity. Visual performance is calculated for the apposition compound eye of the locust, the superposition compound eye of the dung beetle and the camera eye of the nocturnal toad. The results reveal that spatial and temporal summation is extremely beneficial to vision in dim light, especially in small eyes (e.g. compound eyes), which have a restricted ability to collect photons optically. The model predicts that using optimum spatiotemporal summation the locust can extend its vision to light intensities more than 100,000 times dimmer than if it relied on its optics alone. The relative amounts of spatial and temporal summation predicted to be optimal in dim light depend on the image velocity. Animals which are sedentary and rely on seeing small, slow images (such as the toad) are predicted to rely more on temporal summation and less on spatial summation. The opposite strategy is predicted for animals which need to see large, fast images. The predictions of the model agree very well with the known visual behaviours of nocturnal animals.

Absorption of white light in photoreceptors.

The fraction F of incident light absorbed by a photoreceptor of length l has traditionally been given by F = 1 - e-kl, where k is the absorption coefficient of the photoreceptor. Unfortunately, this widely-used expression is incorrect for absorption of the type of light most common in natural scenes--broad spectrum "white" light--and significantly over-estimates absorption. This is because the measured values of k are only valid at the absorbance peak wavelength of rhodopsin, whereas at other wavelengths (which the eye may also see) k is lower. We have accounted for the wavelength dependence of k and calculated the absorption of white light from four different natural radiant sources: the quantal irradiances of natural daylight and a patch of very blue sky, and the quantal reflections of soil and green foliage irradiated by natural daylight. Based on these results, a simple averaged correction for white light stimulation is derived, F = kl/(2.3 + kl), which is valid for a wide range of k and l, and therefore applicable to both vertebrate and invertebrate photoreceptors.

Insect motion detectors matched to visual ecology.

To detect motion, primates, birds and insects all use local detectors to correlate signals sampled at one location in the image with those sampled after a delay at adjacent locations. These detectors can adapt to high image velocities by shortening the delay. To investigate whether they use long delays for detecting low velocities, we compared motion-sensitive neurons in ten species of fast-flying insects, some of which encounter low velocities while hovering. Neurons of bee-flies and hawkmoths, which hover, are tuned to lower temporal frequencies than those of butterflies and bumblebees, which do not. Tuning to low frequencies indicates longer delays and extends sensitivity to lower velocities. Hoverflies retain fast temporal tuning but use their high spatial acuity for sensing low-velocity motion. Thus an unexpectedly wide range of spatio-temporal tuning matches motion detection to visual ecology.