György Kriska

Polarized light pollution: a new kind of ecological photopollution

The alteration of natural cycles of light and dark by artificial light sources has deleterious impacts on animals and ecosystems. Many animals can also exploit a unique characteristic of light – its direction of polarization –as a source of information. We introduce the term “polarized light pollution” (PLP) to focus attention on the ecological consequences of light that has been polarized through interaction with human-made objects. Unnatural polarized light sources can trigger maladaptive behaviors in polarization-sensitive taxa and alter ecological interactions. PLP is an increasingly common byproduct of human technology, and mitigating its effects through selective use of building materials is a realistic solution. Our understanding of how most species use polarization vision is limited, but the capacity of PLP to drastically increase mortality and reproductive failure in animal populations suggests that PLP should become a focus for conservation biologists and resource managers alike.

Ventral polarization vision in tabanids: Horseflies and deerflies (Diptera: Tabanidae) are attracted to horizontally polarized light

Adult tabanid flies (horseflies and deerflies) are terrestrial and lay their eggs onto marsh plants near bodies of fresh water because the larvae develop in water or mud. To know how tabanids locate their host animals, terrestrial rendezvous sites and egg-laying places would be very useful for control measures against them, because the hematophagous females are primary/secondary vectors of some severe animal/human diseases/parasites. Thus, in choice experiments performed in the field we studied the behavior of tabanids governed by linearly polarized light. We present here evidence for positive polarotaxis, i.e., attraction to horizontally polarized light stimulating the ventral eye region, in both males and females of 27 tabanid species. The novelty of our findings is that positive polarotaxis has been described earlier only in connection with the water detection of some aquatic insects ovipositing directly into water. A further particularity of our discovery is that in the order Diptera and among blood-sucking insects the studied tabanids are the first known species possessing ventral polarization vision and definite polarization-sensitive behavior with known functions. The polarotaxis in tabanid flies makes it possible to develop new optically luring traps being more efficient than the existing ones based on the attraction of tabanids by the intensity and/or color of reflected light.

Why do red and dark-coloured cars lure aquatic insects? The attraction of water insects to car paintwork explained by reflection-polarization signals

We reveal here the visual ecological reasons for the phenomenon that aquatic insects often land on red, black and dark-coloured cars. Monitoring the numbers of aquatic beetles and bugs attracted to shiny black, white, red and yellow horizontal plastic sheets, we found that red and black reflectors are equally highly attractive to water insects, while yellow and white reflectors are unattractive. The reflection–polarization patterns of black, white, red and yellow cars were measured in the red, green and blue parts of the spectrum. In the blue and green, the degree of linear polarization p of light reflected from red and black cars is high and the direction of polarization of light reflected from red and black car roofs, bonnets and boots is nearly horizontal. Thus, the horizontal surfaces of red and black cars are highly attractive to red-blind polarotactic water insects. The p of light reflected from the horizontal surfaces of yellow and white cars is low and its direction of polarization is usually not horizontal. Consequently, yellow and white cars are unattractive to polarotactic water insects. The visual deception of aquatic insects by cars can be explained solely by the reflection–polarizational characteristics of the car paintwork.

Degrees of polarization of reflected light eliciting polarotaxis in dragonflies (Odonata), mayflies (Ephemeroptera) and tabanid flies (Tabanidae).

With few exceptions insects whose larvae develop in freshwater possess positive polarotaxis, i.e., are attracted to sources of horizontally polarized light, because they detect water by means of the horizontal polarization of light reflected from the water surface. These insects can be deceived by artificial surfaces (e.g. oil lakes, asphalt roads, black plastic sheets, dark-coloured cars, black gravestones, dark glass surfaces, solar panels) reflecting highly and horizontally polarized light. Apart from the surface characteristics, the extent of such a polarized light pollution depends on the illumination conditions, direction of view, and the threshold p* of polarization sensitivity of a given aquatic insect species. p* means the minimum degree of linear polarization p of reflected light that can elicit positive polarotaxis from a given insect species. Earlier there were no quantitative data on p* in aquatic insects. The aim of this work is to provide such data. Using imaging polarimetry in the red, green and blue parts of the spectrum, in multiple-choice field experiments we measured the threshold p* of ventral polarization sensitivity in mayflies, dragonflies and tabanid flies, the positive polarotaxis of which has been shown earlier. In the blue (450nm) spectral range, for example, we obtained the following thresholds: dragonflies: Enallagma cyathigerum (0%<p*< or =17%), Ischnura elegans (17%< or =p*< or =24%). Mayflies: Baetis rhodani (32%< or =p*< or =55%), Ephemera danica, Epeorus silvicola, Rhithrogena semicolorata (55%< or =p*< or =92%). Tabanids: Tabanus bovinus, Tabanus tergestinus (32%< or =p*< or =55%), Tabanus maculicornis (55%< or =p*< or =92%).

An unexpected advantage of whiteness in horses: the most horsefly-proof horse has a depolarizing white coat

White horses frequently suffer from malign skin cancer and visual deficiencies owing to their high sensitivity to the ultraviolet solar radiation. Furthermore, in the wild, white horses suffer a larger predation risk than dark individuals because they can more easily be detected. In spite of their greater vulnerability, white horses have been highly appreciated for centuries owing to their natural rarity. Here, we show that blood-sucking tabanid flies, known to transmit disease agents to mammals, are less attracted to white than dark horses. We also demonstrate that tabanids use reflected polarized light from the coat as a signal to find a host. The attraction of tabanids to mainly black and brown fur coats is explained by positive polarotaxis. As the hosts colour determines its attractiveness to tabanids, this parameter has a strong influence on the parasite load of the host. Although we have studied only the tabanid–horse interaction, our results can probably be extrapolated to other host animals of polarotactic tabanids, as the reflection–polarization characteristics of the hosts body surface are physically the same, and thus not species-dependent.

Reducing the Maladaptive Attractiveness of Solar Panels to Polarotactic Insects

Human-made objects (e.g., buildings with glass surfaces) can reflect horizontally polarized light so strongly that they appear to aquatic insects to be bodies of water. Insects that lay eggs in water are especially attracted to such structures because these insects use horizontal polarization of light off bodies of water to find egg-laying sites. Thus, these sources of polarized light can become ecological traps associated with reproductive failure and mortality in organisms that are attracted to them and by extension with rapid population declines or collapse. Solar panels are a new source of polarized light pollution. Using imaging polarimetry, we measured the reflection-polarization characteristics of different solar panels and in multiple-choice experiments in the field we tested their attractiveness to mayflies, caddis flies, dolichopodids, and tabanids. At the Brewster angle, solar panels polarized reflected light almost completely (degree of polarization d ≈ 100%) and substantially exceeded typical polarization values for water (d ≈ 30-70%). Mayflies (Ephemeroptera), stoneflies (Trichoptera), dolichopodid dipterans, and tabanid flies (Tabanidae) were the most attracted to solar panels and exhibited oviposition behavior above solar panels more often than above surfaces with lower degrees of polarization (including water), but in general they avoided solar cells with nonpolarizing white borders and white grates. The highly and horizontally polarizing surfaces that had nonpolarizing, white cell borders were 10- to 26-fold less attractive to insects than the same panels without white partitions. Although solar panels can act as ecological traps, fragmenting their solar-active area does lessen their attractiveness to polarotactic insects. The design of solar panels and collectors and their placement relative to aquatic habitats will likely affect populations of aquatic insects that use polarized light as a behavioral cue.

Glass buildings on river banks as “polarized light traps” for mass-swarming polarotactic caddis flies

The caddis flies Hydropsyche pellucidula emerge at dusk from the river Danube and swarm around trees and bushes on the river bank. We document here that these aquatic insects can also be attracted en masse to the vertical glass surfaces of buildings on the river bank. The individuals lured to dark, vertical glass panes land, copulate, and remain on the glass for hours. Many of them are trapped by the partly open, tiltable windows. In laboratory choice experiments, we showed that ovipositing H. pellucidula are attracted to highly and horizontally polarized light stimulating their ventral eye region and, thus, have positive polarotaxis. In the field, we documented that highly polarizing vertical black glass surfaces are significantly more attractive to both female and male H. pellucidula than weakly polarizing white ones. Using video polarimetry, we measured the reflection-polarization characteristics of vertical glass surfaces of buildings where caddis flies swarmed. We propose that after its emergence from the river, H. pellucidula is attracted to buildings by their dark silhouettes and the glass-reflected, horizontally polarized light. After sunset, this attraction may be strengthened by positive phototaxis elicited by the buildings’ lights. The novelty of this visual–ecological phenomenon is that the attraction of caddis flies to vertical glass surfaces has not been expected because vertical glass panes do not resemble the horizontal surface of waters from which these insects emerge and to which they must return to oviposit.

Positive polarotaxis in a mayfly that never leaves the water surface: polarotactic water detection in Palingenia longicauda (Ephemeroptera)

Tisza mayflies, Palingenia longicauda (Olivier 1791), swarm exclusively over the river Tisza (from which the name of the mayfly was derived). This river is bordered by a high vertical wall of trees and bushes, which hinder P. longicauda to move away horizontally from the water. During swarming, Tisza mayflies fly immediately above the river in such a way that their cerci touch the water frequently or sweep its surface. This continuous close connection with water and the vertical wall of the shore and riparian vegetation result in that Tisza mayflies never leave the water surface; consequently, they need not search for water. Several Ephemeroptera species move away far from water and return to it guided by the horizontal polarization of water-reflected light. To reveal whether also P. longicauda is or is not polarotactic, we performed a field experiment during the very short swarming period of Tisza mayflies. We show here that also P. longicauda has positive polarotaxis, which, however, can be observed only under unnatural conditions, when the animals are displaced from the water and then released above artificial test surfaces. P. longicauda is the first species in which polarotactic water detection is demonstrated albeit it never leaves the water surface, and thus, a polarotactic water detection seems unnecessary for it. The polarotactic behaviour of Tisza mayflies explains the earlier observation that these insects swarm above wet asphalt roads running next to river Tisza.

Polarization vision in aquatic insects and ecological traps for polarotactic insects

We review the polarization vision of aquatic insects, which detect water from a distance by the horizontally polarized light refl ected from the water surface. Refl ection–polarization characteristics of different water bodies, as functions of sky conditions and solar elevation, are examined in relation to how they infl uence the detection of water bodies by polarotactic aquatic insects. Examples are given showing how aquatic insects can be deceived by, attracted to and trapped by highly and horizontally polarizing artifi cial refl ectors, such as oil surfaces, horizontal black plastic sheets, asphalt roads, red or black car-bodies and black gravestones. We explain why mirages and polarizing black burnt stubble-fi elds do not attract polarotactic aquatic insects. The existence of a polarization sun-dial, which dictates the optimal time of day for dispersal by fl ying aquatic insects, is demonstrated. We fi nish by examining some unexpected aspects of polarization vision in insects: a polarotactic mayfl y that never leaves the water surface and thus does not need polarotaxis, and polarotactic vision of several tabanid fl ies. Polarization Vision in Aquatic Insects Human observers can detect the presence of a distant water body by means of learned visual cues associated with water, such as mirroring of landmarks on the water surface, rippling of the surface or aquatic plants on the shore. These water-specifi c visual cues arise from the spatiotemporal distribution of the intensity and colour of light originating from water and the surrounding objects. As all these cues must be learned, a completely inexperienced human being (who has never encountered an open water surface) would be unable to recognize water. The inexperienced person’s lack of knowledge about water is similar to the situation when an aquatic insect leaves the water for the fi rst time, driven by Polarization Vision in Aquatic Insects 205 resource shortages or unsuitable environmental conditions. Larval and many adult aquatic insects live in water where they can gather information only about their aquatic environment. When adults leave the water for the fi rst time, they face the task of detecting water while dispersing in order to return to water to avoid dehydration, oviposit, or simply return to the aquatic environment. As they have no opportunity to learn the visual cues associated with water, they need a genetically fi xed and reliable method to detect water visually and from a distance. This sensory capability is polarization vision. In the early 1980s, Rudolf Schwind (1983a,b, 1984a,b, 1985a,b) discovered that the backswimmer, Notonecta glauca, detects water by means of the horizontally polarized light refl ected from the water surface, rather than by the intensity or colour of water-refl ected light, or by the glittering or mirroring of the water surface. In the ventral eye region of Notonecta, Schwind et al. (1984) found ultraviolet-sensitive photoreceptors with horizontal and vertical microvilli that are highly sensitive to horizontally and vertically polarized light (Schwind, 1983b). This eye region is called the ‘ventral polarization-sensitive area’. These photoreceptors can determine whether the direction of polarization of light from the optical environment is horizontal or not. In Notonecta, exactly or nearly horizontally polarized light stimulus elicits a typical plunge reaction, whereby the insect stops fl ying and attempts to re-enter the water (Schwind, 1984b). This attraction to horizontally polarized light is called positive polarotaxis. Following from these initial studies, positive polarotaxis has been discovered in over 250 species of aquatic insects and from many different groups, including bugs, beetles, dragonfl ies, mayfl ies, tabanid fl ies and caddisfl ies (Schwind, 1985a,b, 1989, 1991, 1995; Kriska et al., 1998, 2006a, 2007; Wildermuth, 1998; Horváth et al., 1998; Bernáth et al., 2001; Wildermuth and Horváth, 2005; Csabai et al., 2006). The eyes of many aquatic insects are sensitive to the polarization of light in the visible or ultraviolet spectral ranges (Schwind, 1989, 1991, 1995). These insects fi nd water using horizontally polarized light refl ected from the water surface (Schwind and Horváth, 1993; Horváth, 1995). The spectral sensitivity of the polarization-sensitive photoreceptors of insects living in water is generally matched to the spectral composition of underwater light, which is quite diverse in different types of aquatic habitats (Lythgoe, 1979). Aquatic insects detect polarization in that region of the spectrum that is characteristic of their preferred habitat (Schwind, 1995). Depth, turbidity, transparency, colour, surface roughness of the water and substratum composition, as well as illumination, strongly infl uence the refl ection–polarization characteristics of water bodies. These polarization patterns provide important information on the quality of freshwater habitats for polarotactic insects and can aid the orientation of these insects from a distance. The Optomotor Response to Polarization Patterns in Aquatic Insects The optomotor response is a turning reaction displayed in response to a cylindrical pattern of vertical black and white stripes being rotated around an animal. 206 G. Horváth and G. Kriska This behaviour demonstrates the ability of an animal to detect movement of the optical environment on the basis of brightness cues; it helps to stabilize the animal’s orientation in its environment and to maintain a straight course during locomotion (Varjú, 1959). If the underlying visual subsystem is sensitive to linear polarization, an optomotor response is likely to be elicited also by a rotating pattern of alternating direction of polarization. Both the aboveand underwater optical environments of backswimmers (Notonectidae) and waterstriders (Gerridae) (composed of the underwater world, the water surface, the riparian vegetation and the sky) are rich in polarized light. To test whether this polarization cue can be exploited for motion detection, in behavioural laboratory experiments Horváth and Varjú (2003, pp. 276–292) investigated the optomotor response of the waterstrider Gerris lacustris and the backswimmer Notonecta glauca to overand underwater brightness and polarization patterns. They found that the latero-frontal eye regions in Gerris and Notonecta respond to certain contrasts in the direction of polarization, especially vertical versus horizontal polarization (Fig. 11.1). The function of this polarization-sensitive optomotor response may be a contrast enhancement for motion perception during compensation for passive drift and rotation of the body. They also showed that, in Gerris and Notonecta, the polarization-sensitive optomotoric reaction is mediated by the green receptors. In the aquatic habitat of these insects, brightness and polarization contrasts occur mainly in the visible and especially in the green part of the spectrum (e.g. riparian vegetation, water plants and phytoplankton in water). Refl ection–polarization Characteristics of Different Water Bodies In this and subsequent sections we make a distinction between ‘dark water bodies’ and ‘bright water bodies’. Dark water bodies refl ect little light, because they are deep, the water contains dark suspended particles or the bed sediments are dark. Bright water bodies refl ect a lot of light, because the water is clear and shallow, the water contains bright suspended particles or the bed sediments are bright. Schwind and Horváth (1993) and Horváth (1995) investigated, theoretically, the refl ection–polarization characteristics of fl at water surfaces in relation to the solar elevation. Using different kinds of imaging polarimetry, Horváth and Varjú (1997), Gál et al. (2001a) and Bernáth et al. (2002) measured the refl ection– polarization patterns of various freshwater habitats in the red (650 nm), green (550 nm) and blue (450 nm) spectral ranges, under different meteorological conditions. According to Fig. 11.2D,E, the light refl ected from the so-called Brewster zone (an annular region, the centre line of which is a circle at a nadir angle of 57.5°) of dark water surfaces is highly and always horizontally polarized. Thus, the light refl ected from the Brewster zone is very attractive to polarotactic aquatic insects, even though the refl ectivity R of the Brewster zone is only moderate as R increases nearly exponentially toward the horizon (Fig. 11.2F). What these insects identify as water are only those areas that refl ect light with degrees of linear polarization p higher than the threshold p* of their polarization sensitivity Polarization Vision in Aquatic Insects 207 (p > p*), and with angles of polarization a differing from the horizontal (a = 90° from the vertical) by less than a threshold ∆a > |90° − a|. For example, the black region in Fig. 11.2G shows the area detected as water by a polarotactic insect whose thresholds are p* = 5%, ∆a = 5°. 0.2

Polarotaxis in non-biting midges: female chironomids are attracted to horizontally polarized light.

Non-biting midges (Chironomidae, Diptera) are widely distributed aquatic insects. The short-living chironomid adults swarm in large numbers above water surfaces, and are sometimes considered a nuisance. They are vectors of certain bacteria, and have a key-role in benthic ecosystems. Optical cues, involving reflection-polarization from water, were found to be important in the habitat selection by three Mediterranean freshwater chironomid species. In this work we report on our multiple-choice experiments performed in the field with several other European freshwater chironomid species. We show that the investigated non-biting midges are positively polarotactic and like many other aquatic insects their females are attracted to horizontally polarized light. Our finding is important in the visual ecology of chironomids and useful in the design of traps for these insects.