J Comp Physiol A DOI 10.1007/s00359-014-0895-1
Review
Visual ecology of flies with particular reference to colour vision and colour preferences Klaus Lunau
Received: 2 December 2013 / Revised: 19 February 2014 / Accepted: 25 February 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract The visual ecology of flies is outstanding among insects due to a combination of specific attributes. Flies’ compound eyes possess an open rhabdom and thus separate rhabdomeres in each ommatidium assigned to two visual pathways. The highly sensitive, monovariant neural superposition system is based on the excitation of the peripheral rhabdomeres of the retinula cells R1–6 and controls optomotor reactions. The two forms of central rhabdomeres of R7/8 retinula cells in each ommatidium build up a system with four photoreceptors sensitive in different wavelength ranges and thought to account for colour vision. Evidence from wavelength discrimination tests suggests that all colour stimuli are assigned to one of just four colour categories, but cooperation of the two pathways is also evident. Flies use colour cues for various behavioural reactions such as flower visitation, proboscis extension, host finding, and egg deposition. Direct evidence for colour vision, the ability to discriminate colours according to spectral shape but independent of intensity, has been demonstrated for few fly species only. Indirect evidence for colour vision provided from electrophysiological recordings of the spectral sensitivity of photoreceptors and opsin genes indicates similar requisites in various flies; the flies’ responses to coloured targets, however, are much more diverse. Keywords Colour vision · Colour preference · Flies · Brachycera · Neural superposition
K. Lunau (*) Department of Biology, Institute of Sensory Ecology, Heinrich-Heine-Universität Düsseldorf, Universitätsstr. 1, 40225 Düsseldorf, Germany e-mail: lunau@uni‑duesseldorf.de
Introduction The compound eye of an insect is an assembly of ommatidia, each containing several photoreceptors. Depending on the optics delivering incident light to the photoreceptors, compound eyes are divided into three basic types: apposition, optical superposition, and neural superposition (Land and Nilsson 2002). In apposition eyes, the photoreceptors of each individual ommatidium receive light only via the assigned facet lens, and each facet collects light from one direction in space. In optical superposition eyes, light collected from one direction in space falls through multiple facet lenses onto one set of photoreceptors in one and the same ommatidium. When the ommatidia at the height of the rhabdom are surrounded by a tracheal sheet that functions as a reflective tapetum, spatial resolution in an optical superposition eye can be just as good as in an apposition eye despite the enhanced sensitivity. In cases where a tapetum is lacking, light may reach neighbouring ommatidia, resulting in lower spatial resolution. This difference is directly related to the visual ecology: apposition compound eyes are common in diurnal insects, whereas optical superposition eyes are found mainly in nocturnal insects (Warrant and Dacke 2011). In neural superposition eyes, the photoreceptors have different visual axes, but this is compensated by neural pooling in the lamina, the optical ganglion below the retina. The excitations of those photoreceptors of a limited number of ommatidia that share the same visual axis are pooled in a so-called neuro-ommatidium. Neural superposition eyes are found only in dipterans (Diptera), earwigs (Dermaptera), and true bugs (Heteroptera) (Osorio 2007). Whether and how the light habitat and diurnal or nocturnal activity might have shaped the evolution of the neural superposition eye is unclear. Osorio (2007) hypothesized that the neural superposition eye might have
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evolved from nocturnal ancestors with open rhabdoms, which enhanced sensitivity by pooling signals via receptor axon collaterals that connected neighbouring ommatidia; when they moved from nocturnal to diurnal activity, these neural connections might have been refined in order to avoid compromising spatial acuity. In this review about colour vision and colour preference in flies, the characteristics of compound eyes in flies as compared to other insects’ eyes are compiled as far as they are needed to understand the extraordinary visual system in flies. Some remarkable and spectacular visually guided behavioural reactions of flies are highlighted in order to estimate the involvement of colour vision and colour preferences in the visual ecology of flies. Before introducing current colour vision models of flies, definitions of colour vision and of colour preference are given, because these terms might be used differently depending on context and discipline. The sections about colour vision models will focus on the categorical colour vision and alternative models. The section about colour preferences reviews flower colour preferences of flower-visiting flies, flies as protagonists in visual mimicry systems, and catches of flies by coloured pan traps. In addition, the possible involvement of eye colour caused by screening pigments and corneal colour filters in colour vision of flies is discussed.
General and specific features of compound eyes in flies Just like other insects, flies possess two compound eyes built up by numerous ommatidia, which, although equipped with similar anatomy, may specialize for different tasks. The compound eyes of flies each possess up to several thousands of ommatidia, ranging from 0 in Braula coeca (Herrod-Hempsal 1931) over 780 in Drosophila melanogaster (Böhni et al. 1999) and 3,100 in Musca domestica (Beersma et al. 1977) to 6,400 per eye in Syritta pipiens (Beersma et al. 1977). At first glance, the ommatidia of flies’ compound eyes look rather uniform. However, due to eye regionalization, there is considerable specialization of distinct eye regions for specific tasks (Stavenga 1992; Land and Nilsson 2006). By mapping the density of the visual axes of ommatidia, Land and Eckert (1985) found areas of particularly high density. Areas with small interommatidial angle and thus high spatial resolution are termed ‘acute zones’ in contrast to areas with large facet diameters, termed ‘bright zones’ (Straw et al. 2006). In male houseflies, M. domestica, such an acute and bright zone (including larger facet lenses, higher sampling density, and faster electrical responses), the so-called love spot, is specialized for detecting small, fast flying objects, which could be conspecific females (Burton and Laughlin 2003). In some flies, e.g. Syrphidae and Tabanidae, the dorsal part of males’ eyes
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is specialized for the detection of females (Yuval 2006). Then, the males’ compound eyes are holoptic, i.e. with only small space between the compound eyes at the dorsal side of the head, whereas the females possess clearly separated dichoptic compound eyes (Mc Alpine 1981). Male march flies (Bibionidae) have extremely enlarged dorsal compound eyes as compared to females (Zeil 1983). In contrast to other flies, in which large facets are associated with decreased interommatidial angles to form a dorsal ‘acute zone’ of increased spatial resolution, males of the hoverfly Eristalis tenax possess a dorsal region of large facets forming a ‘bright zone’ of ommatidia with increased light capture without substantially increased spatial resolution (Straw et al. 2006). Male blowflies Chrysomyia megacephala have an extremely prominent ‘bright zone’ (van Hateren et al. 1989). Some flies possess a dorsal rim composed of a few ommatidia in the dorsal periphery of the compound eyes, which is specialized for the detection of polarized sky light by particular ‘marginal’ ommatidia equipped with specific photoreceptor cells and visual pigments (Strausfeld and Wunderer 1985; Tomlinson 2003). In the ommatidia of insects with apposition eyes, the rhabdomeres of all photoreceptor cells are joined tightly together, enhancing optical coupling between each other (Snyder et al. 1973). Although this arrangement is termed ‘fused rhabdom’, the photoreceptor cells are not fused, but grouped closely together and the rhabdom acts as a light guide in each ommatidium (Land and Nilsson 2002). Thus, in apposition eyes, all rhabdomeres of the fused rhabdom share one visual axis. The anatomy of the compound eyes of flies is different and unique, because flies possess—in contrast to most other insects—an open rhabdom. In the ommatidia of flies’ eyes, the rhabdomeres of the photoreceptor cells are not fused. The eight photoreceptor cells have light-sensitive structures, the rhabdomeres, that are optically isolated from each other. The rhabdomeres of the retinula cells R1–6 form six independent light guides situated circumferential as compared to the two central rhabdomeres forming one serial light guide. This rhabdomere–tandem consists of the rhabdomeres of the retinula cells R7 and R8. The central rhabdomere–tandem of cells R7/8 shares the same visual axis of six retinula cells from six different adjacent ommatidia. The eight photoreceptor cells per ommatidium of a fly compound eye are assigned to two visual pathways, which are processed in parallel (Strausfeld and Lee 1991). The neural superposition system is a monovariant system, i.e. based on one receptor type, for motion detection (Yamaguchi et al. 2008). The retinula cells R1–6 of each ommatidium possess different visual axes, but six retinula cells from six different adjacent ommatidia, which share the same visual axis and are arranged in a trapezoid pattern
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(Fig. 6), form a neuro-ommatidium. The excitation of the corresponding retinula cells is neurally pooled by a neuroommatidium in the lamina. For the neuro-ommatidium, the signal in terms of photon captures is thus six times stronger than that in an apposition eye and without reduction in visual acuity, provided the rhabdomeres of the neurally superimposed retinula cells are properly aligned (Land and Nilsson 2002). The axons of such retinula cells (except the central ones, which pass through to the second optic ganglion) converge onto the same cartridge of secondary neurons in the first optic ganglion, the lamina. Thus, each lamina cartridge gets input through six different ommatidia from six retinula cells sharing the same visual axis (Zeil 1983). The spectral sensitivity of the retinula cells R1–6 possesses two major peaks; one peak is caused by the visual pigment exhibiting peak sensitivity in the green wavelength range, and the other, more prominent one is caused by sensitizing pigments with peak sensitivity in the ultraviolet wavelength ranges (Kirschfeld et al. 1977; Minke and Kirschfeld 1979). The absolute spectral sensitivity of single retinula cells R1–6 is similar to that of the retinula cells R7 and R8 (Hardie 1979), which indicates that these visual pathways are unlikely to function under either photopic or scotopic light conditions and fits to their supposed functions as motion-sensitive and colour-sensitive systems. The retinula cells R7 and R8 belong to the tetravariant visual system, i.e. based on four receptor classes, as there are two types of R7/8 rhadomere tandems—named ‘pale’ and ‘yellow’ due to appearance in transmitted light. The compound eyes of flies thus possess four types of central photoreceptors: the retinula cells R7p, R8p, R7y, and R8y. Since the peak sensitivity of the four retinula cells R7p, R8p, R7y, and R8y differs and covers the ultraviolet, blue, and green ranges of wavelength, it offers appropriate preconditions for colour vision (see below). The spectral sensitivity of these four photoreceptors seems to be rather uniform among flies (Fig. 1; Bishop 1974; Horridge et al. 1975; Tsukahara and Horridge 1977a, b; Stark et al. 1979; Hardie and Kirschfeld 1983; Hardie 1985; Yamaguchi et al. 2010). The information delivered by these retinula cells is processed in the second optical ganglion, the medulla, where second-order neurons that contact both R7 and R8 retinula cells from a single ommatidium, or different ommatidia, have been identified (Morante and Desplan 2008). Besides five classes of visual pigments, the ommatidia of flies contain screening pigments located in the pigment cells. The typical red colour of the compound eyes of D. melanogaster, Calliphora vicina, and of many other flies is caused by screening pigments that absorb the light of wavelengths 510 nm as shown in tests with monochromatic light stimuli (Fig. 3; Lunau and Wacht 1994). The admixture of small amounts of ultraviolet and blue light 510 nm and absorbs blue and ultraviolet light (Fig. 3; Lunau 1995, 2000; Wacht et al. 1996). Both female and male imagoes of E. tenax can be trained to land on blue flowers, but cannot be induced to extend the proboscis towards blue colour patches despite prolonged training and differential conditioning sensu Dyer and Chittka (2004) (Lunau 1988; Hohmann, Donda and Lunau, personal communication). By contrast, in houseflies, classical conditioning to visual colour stimuli was successful (Fukushi 1976). Yellow floral guides, mimicking the colour of yellow pollen and anthers (Lunau 2000, 2007), thus bear a large potential to manipulate the movements of pollen-eating hoverflies and flowers (Dinkel and Lunau 2001). When floral guides are present in colour gradients, e.g. comprising red, orange, and yellow dot guides as known from fly-pollinated Saxifraga flowers, E. tenax flies proceed towards the yellow dots (Lunau et al. 2005). Interestingly, the spontaneous proboscis reflex towards yellow colours is shown by other species of the Eristalinae, but is not or less pronounced in more distantly related hoverfly species (Wacht et al. 1996). The relative importance of different visual cues of oviposition sites has been demonstrated for the apple maggot fly, Rhagoletis pomonella (Tephritidae). In behavioural tests, in which the size, shape, and colour of target stimuli were varied, both sexes preferred dark, i.e. red, blue, violet, black, and dark orange objects over light, i.e. green, yellow, white, and light orange ones, if the objects were small and spherical, but preferred yellow objects if they were large and rectangular. Prokopy (1968) interpreted his findings convincingly as follows: the flies are attracted towards a large yellow area as if it was foliage and are attracted to small spherical objects as though they might be developing fruits. The size and shape of the objects thus determined the corresponding colour preference of the apple maggot fly. The reproductive biology of the apple maggot fly elucidates this choice behaviour. Developing fruits are oviposition sites for females and rendezvous sites for males. The response to spherical objects seems to rely on brightness cues only, whereas the response towards a larger object is based on colour vision and colour discrimination (Prokopy 1968). Similar preferences have been demonstrated for the Mediterranean fruit fly Ceratitis capitata (Nakagawa et al. 1978).
In many ecological studies, the research aims at catching a large diversity of fly species (Vrdoljak and Samways 2012) rather than exploring the preferred colour. In most studies, several coloured traps of different colour but similar size and exposure are used. However, the reflection properties of the trap colours are only rarely communicated, and in many cases, the hue of the pan trap colour as viewed by humans is the only colour attribute reported, whereas the ultraviolet wavelength ranges are often not considered, preventing correct interpretations of the colour preferences underlying the trap catches. Colour preferences might cause catches of flies in coloured pan traps (Ssymank 2001; Laubertie et al. 2006), but in many cases it remains unclear whether these preferences relate to flowers of food plants, egg-laying substrates, host organisms, or other relevant objects resting sites for warming up for example. In addition, the array of coloured pan traps used could lead to bias in the catches due to competition between similarly coloured traps. Moreover, in many studies, the spectral reflectance properties of the trap colours are not communicated, particularly the UV-reflectance properties, and thus hamper conclusions on colour preferences of the flies caught. Some studies, however, provide results enabling conclusions regarding colour preferences of distinct fly species (Ssymank 2001; Laubertie et al. 2006). This may permit trap colours to be chosen, in particular circumstances that are ecologically selective for different types of insect (Kirk 1984). Although in field studies with sticky coloured traps a preference for orange over yellow, green, blue, red, black, and white of the Caribbean fruit fly, Anastrepha suspensa (Tephritidae), has been demonstrated, it was noted that fly capture rates were directly related to the proportion of light reflected in the wavelength range between 580 and 590 nm (Greany et al. 1977). Similar results were obtained in a study of the effect of colour hue and brightness of artificial oviposition substrates on the selection of oviposition site by the olive fruit fly, D. oleae. Females preferred yellow and orange over red, blue, black, and white oviposition sites, and ranges of wavelength fostering oviposition (560 and 610 nm) as well as ranges of wavelength inhibiting oviposition (400–480, 520–550, >610 nm) could be identified (Katsoyannos et al. 1985). Despite comprehensive characterization of the colour stimuli, it remained unclear whether the attraction towards the colour stimuli was caused by one colour hue category, by overall brightness or by the brightness in one small wavelength range. Re-evaluation of these studies within the framework of known photoreceptor sensitivities and the colour vision model of Troje (1993) seems promising. However, trap colour design might be precise enough that the dependence of wavelength-specific reflectance intensity for the magnitude of blue colour preference
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in the onion fly Delia antiqua (Anthomyiidae) could be demonstrated under field conditions (Vernon 1986). Field observations of flies targeting coloured substrates and objects and field collections of flies by means of coloured traps are often interpreted as if providing indirect evidence for colour vision or colour preference (Campbell and Hanula 2007), although alternative explanations have not been adequately considered in many cases. Numerous flies of great economic importance have been studied intensively including their response to visual stimuli, e.g. bloodsucking parasites for humans and domestic animals like horse and deer flies (Tabanidae) as well as simuliid flies (Simuliidae), vectors of diseases like tsetse flies (Glossinidae), pathogenic germs like the housefly M. domestica (Muscidae), and pests of field crops like fruit flies (Tephritidae) (Khan 1978; Green 1994; Gibson and Torr 1999; Levinson et al. 2003). The responses of organisms towards objects bearing natural intraspecific or interspecific colour signals, as well as those towards artificial colour signals like coloured traps, provide little reliable indication of an ability of colour vision, because the response is not necessarily caused by colour; intensity and polarization pattern provides visual stimulus components associated with colour without being an attribute of the chromaticity of the stimulus. Non-visual attractants associated with colour cues represent another source of response to colour cues in flies. Within the monophyletic taxon of true flies, Brachycera (Yeates and Wiegmann 1999), there are all kinds of proofs, evidences, and indications of colour vision for various species.
Flies and visual mimicry Flies are well known as mimics of other organisms like bumblebees, wasps, and spiders (Howarth et al. 2000) and copy the conspicuous aposematic colour patterns of their models (Lunau 2011). However, flies are not addressees of these colourful mimic signals, which are mostly directed to animals predaceous on flies. At least, it is unknown whether the mimic colour signals play a role in the mate recognition of flies, too. In a few mimicry systems, flies act as signal receivers responding to visual mimicry, i.e. carrion-mimicking, mushroom-mimicking, and sexually deceptive flowers. Many flowers pollinated by carrion flies and saprophilous flies mimic olfactory and visual cues of carcasses or rotten plants to attract fly pollinators (Angioy et al. 2004; van der Niet et al. 2011). Mimicked olfactory cues of carcasses seem to be far more important than visual cues, which are only important when selecting a final landing site. This has been demonstrated in behavioural tests with the blowfly, L. sericata (Wall and Fisher 2001). The colour of
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carrion-mimicking flowers is rather uniform even in unrelated plant species; the flowers predominantly look fleshy, reddish, or brownish and have a texture that reminds many observers of layers of mould fungi. Since the largest flowers (Rafflesia, Rafflesiacae) of the world attract carrion flies, size of the mimicked cadaver seems to play a role for attraction (Beaman et al. 1988). The sensitivity to red light found by electrophysiological methods in C. erythrocephala (Autrum and Stumpf 1953) seems consistent with this finding, but has not been confirmed by later research. In fact, Goldsmith (1965) showed that sensitivity in the red wavelength range was an artefact due to a recruitment of additional ommatidia during electrophysiological recordings caused by leakage of red wavelengths through the screening pigments. Some mushroom-mimicking flowers that are pollinated by flies mimic not only chemical and tactile cues of mushrooms, but also visual cues including size, shape, and colour pattern. Doing so, the flowers not only attract flies as potential pollinators, but also manipulate the flies to deposit eggs on the flowers. The egg-laying behaviour of flies has been reported for two mushroom-mimicking flowers displaying a striking resemblance to real mushrooms. The flowers of the Mexican tree Aristolochia arborea (Aristolochiaceae) closely resemble mushrooms of the genus Marasmius (Marasmiaceae) and are assumed to be pollinated by small sawflies, but pollination by fungus gnats or flies has not been excluded (Vogel 1978). The females on their search for a suitable place for egg-laying fall into the flytrap. Having been trapped in this way, the flies use positive phototaxis and desperately try to escape through a ‘window’ composed of transparent cells; while doing so, they continuously touch the sticky stigma and deposit some of the pollen grains brought in from previously visited flowers. Not till the next day do the anthers open and shed pollen onto the flies, after which the flower wilts and the flies can escape. Also, some orchids of the genus Dracula are pollinated by mycophilous drosophilid flies of the genus Zygothrica (Endara et al. 2010). The multimodal mimicry of chemical, visual, and tactile cues of mushrooms by fly-pollinated mushroom-mimicking flowers is probably due to the fact that egg-laying in the flowers significantly decreases the fitness for the deceived fly females, because the fly larvae cannot develop in the floral tissues. It can be assumed that those females using more and more complex cues to discriminate between real and mimic mushrooms will gain a net fitness benefit. Interestingly, maculated leaves may play a role in attracting flies by mimicking fungus-infected foliage (Ren et al. 2011). Sexual deception of bombyliid flies (Bombyliidae) occurs in South African daisies, e.g. Gorteria diffusa (Ellis and Johnson 2010; Johnson and Midgley 1997; Thomas et al. 2009). As shown by Ellis and Johnson (2010),
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Gorteria forms eliciting mating behaviour in bombyliid males are less attractive for females and vice versa, suggesting males and females have different preferences and thus select for different floral traits. Paulus (2007) describes the possible deception of male Merodon velox (Syrphidae) by orchids of the species Ophrys regis-ferdinandii (Orchidaceae). The blue and shiny labellum of the orchid resembles the blue-winged males of Merodon velox hoverflies, whereas the females have clear wings; it is thus assumed that not sexual deception but territorial defence is involved in this mimicry system.
Conclusions Flies have evolved one of the most elaborate visual systems among insects. Evidence for colour vision and colour preferences in flies, however, is limited at least as compared to other insect taxa such as bees. Interestingly, only a few flies exhibit a sexual dimorphism of coloured courtship signals, indicating that courtship and mating are based on cues other than colour. The interactions between flies and plants seem to be based on colour cues more frequently than the interactions of flies with conspecifics and with animal hosts. Flies visiting flowers for nectar and pollen as well as flies ovipositing on plant organs like fruits make use of colour vision. In some cases, even distinct colour preferences have been demonstrated. Colour vision and colour preferences at least of selected fly species can be easily studied in laboratory set-ups, because some flies can be bred indoors, some can be collected in large numbers as larvae, and many flies are easy to handle in laboratory conditions. The electrophysiological and genetic data suggest that the equipment of compound eyes in flies is rather uniform, facilitating the assignability of physiological data from model species to particular study species. Future research on colour vision and colour preferences would benefit from developing a model of fly colour vision and provision of software to calculate and illustrate colour loci in an appropriate colour space, as might be predicted from the publication of a colour vision model for bees (Chittka 1992) and publications based thereon. In addition, electrophysiological recordings of the spectral sensitivity of individual photoreceptors in more species could demonstrate specific adaptations to light habitats or ecological specialization in flies. Thus, the interpretation of colour-based behavioural reactions of flies targeting natural colour stimuli like flowers or oviposition substrates or artificial colour stimuli like artificial flowers and pan traps can be thoroughly improved. Acknowledgments I thank Anne Thorson for linguistic improvement, Sarah Papiorek for critical comments on the manuscript and help with the preparation of some figures, and Francismeire Telles for discussion about spectral sensitivity curves for Eristalis tenax. Two
anonymous reviewers commented in a very constructive manner and helped to improve the manuscript.
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Review
Visual ecology of flies with particular reference to colour vision and colour preferences Klaus Lunau
Received: 2 December 2013 / Revised: 19 February 2014 / Accepted: 25 February 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract The visual ecology of flies is outstanding among insects due to a combination of specific attributes. Flies’ compound eyes possess an open rhabdom and thus separate rhabdomeres in each ommatidium assigned to two visual pathways. The highly sensitive, monovariant neural superposition system is based on the excitation of the peripheral rhabdomeres of the retinula cells R1–6 and controls optomotor reactions. The two forms of central rhabdomeres of R7/8 retinula cells in each ommatidium build up a system with four photoreceptors sensitive in different wavelength ranges and thought to account for colour vision. Evidence from wavelength discrimination tests suggests that all colour stimuli are assigned to one of just four colour categories, but cooperation of the two pathways is also evident. Flies use colour cues for various behavioural reactions such as flower visitation, proboscis extension, host finding, and egg deposition. Direct evidence for colour vision, the ability to discriminate colours according to spectral shape but independent of intensity, has been demonstrated for few fly species only. Indirect evidence for colour vision provided from electrophysiological recordings of the spectral sensitivity of photoreceptors and opsin genes indicates similar requisites in various flies; the flies’ responses to coloured targets, however, are much more diverse. Keywords Colour vision · Colour preference · Flies · Brachycera · Neural superposition
K. Lunau (*) Department of Biology, Institute of Sensory Ecology, Heinrich-Heine-Universität Düsseldorf, Universitätsstr. 1, 40225 Düsseldorf, Germany e-mail: lunau@uni‑duesseldorf.de
Introduction The compound eye of an insect is an assembly of ommatidia, each containing several photoreceptors. Depending on the optics delivering incident light to the photoreceptors, compound eyes are divided into three basic types: apposition, optical superposition, and neural superposition (Land and Nilsson 2002). In apposition eyes, the photoreceptors of each individual ommatidium receive light only via the assigned facet lens, and each facet collects light from one direction in space. In optical superposition eyes, light collected from one direction in space falls through multiple facet lenses onto one set of photoreceptors in one and the same ommatidium. When the ommatidia at the height of the rhabdom are surrounded by a tracheal sheet that functions as a reflective tapetum, spatial resolution in an optical superposition eye can be just as good as in an apposition eye despite the enhanced sensitivity. In cases where a tapetum is lacking, light may reach neighbouring ommatidia, resulting in lower spatial resolution. This difference is directly related to the visual ecology: apposition compound eyes are common in diurnal insects, whereas optical superposition eyes are found mainly in nocturnal insects (Warrant and Dacke 2011). In neural superposition eyes, the photoreceptors have different visual axes, but this is compensated by neural pooling in the lamina, the optical ganglion below the retina. The excitations of those photoreceptors of a limited number of ommatidia that share the same visual axis are pooled in a so-called neuro-ommatidium. Neural superposition eyes are found only in dipterans (Diptera), earwigs (Dermaptera), and true bugs (Heteroptera) (Osorio 2007). Whether and how the light habitat and diurnal or nocturnal activity might have shaped the evolution of the neural superposition eye is unclear. Osorio (2007) hypothesized that the neural superposition eye might have
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evolved from nocturnal ancestors with open rhabdoms, which enhanced sensitivity by pooling signals via receptor axon collaterals that connected neighbouring ommatidia; when they moved from nocturnal to diurnal activity, these neural connections might have been refined in order to avoid compromising spatial acuity. In this review about colour vision and colour preference in flies, the characteristics of compound eyes in flies as compared to other insects’ eyes are compiled as far as they are needed to understand the extraordinary visual system in flies. Some remarkable and spectacular visually guided behavioural reactions of flies are highlighted in order to estimate the involvement of colour vision and colour preferences in the visual ecology of flies. Before introducing current colour vision models of flies, definitions of colour vision and of colour preference are given, because these terms might be used differently depending on context and discipline. The sections about colour vision models will focus on the categorical colour vision and alternative models. The section about colour preferences reviews flower colour preferences of flower-visiting flies, flies as protagonists in visual mimicry systems, and catches of flies by coloured pan traps. In addition, the possible involvement of eye colour caused by screening pigments and corneal colour filters in colour vision of flies is discussed.
General and specific features of compound eyes in flies Just like other insects, flies possess two compound eyes built up by numerous ommatidia, which, although equipped with similar anatomy, may specialize for different tasks. The compound eyes of flies each possess up to several thousands of ommatidia, ranging from 0 in Braula coeca (Herrod-Hempsal 1931) over 780 in Drosophila melanogaster (Böhni et al. 1999) and 3,100 in Musca domestica (Beersma et al. 1977) to 6,400 per eye in Syritta pipiens (Beersma et al. 1977). At first glance, the ommatidia of flies’ compound eyes look rather uniform. However, due to eye regionalization, there is considerable specialization of distinct eye regions for specific tasks (Stavenga 1992; Land and Nilsson 2006). By mapping the density of the visual axes of ommatidia, Land and Eckert (1985) found areas of particularly high density. Areas with small interommatidial angle and thus high spatial resolution are termed ‘acute zones’ in contrast to areas with large facet diameters, termed ‘bright zones’ (Straw et al. 2006). In male houseflies, M. domestica, such an acute and bright zone (including larger facet lenses, higher sampling density, and faster electrical responses), the so-called love spot, is specialized for detecting small, fast flying objects, which could be conspecific females (Burton and Laughlin 2003). In some flies, e.g. Syrphidae and Tabanidae, the dorsal part of males’ eyes
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is specialized for the detection of females (Yuval 2006). Then, the males’ compound eyes are holoptic, i.e. with only small space between the compound eyes at the dorsal side of the head, whereas the females possess clearly separated dichoptic compound eyes (Mc Alpine 1981). Male march flies (Bibionidae) have extremely enlarged dorsal compound eyes as compared to females (Zeil 1983). In contrast to other flies, in which large facets are associated with decreased interommatidial angles to form a dorsal ‘acute zone’ of increased spatial resolution, males of the hoverfly Eristalis tenax possess a dorsal region of large facets forming a ‘bright zone’ of ommatidia with increased light capture without substantially increased spatial resolution (Straw et al. 2006). Male blowflies Chrysomyia megacephala have an extremely prominent ‘bright zone’ (van Hateren et al. 1989). Some flies possess a dorsal rim composed of a few ommatidia in the dorsal periphery of the compound eyes, which is specialized for the detection of polarized sky light by particular ‘marginal’ ommatidia equipped with specific photoreceptor cells and visual pigments (Strausfeld and Wunderer 1985; Tomlinson 2003). In the ommatidia of insects with apposition eyes, the rhabdomeres of all photoreceptor cells are joined tightly together, enhancing optical coupling between each other (Snyder et al. 1973). Although this arrangement is termed ‘fused rhabdom’, the photoreceptor cells are not fused, but grouped closely together and the rhabdom acts as a light guide in each ommatidium (Land and Nilsson 2002). Thus, in apposition eyes, all rhabdomeres of the fused rhabdom share one visual axis. The anatomy of the compound eyes of flies is different and unique, because flies possess—in contrast to most other insects—an open rhabdom. In the ommatidia of flies’ eyes, the rhabdomeres of the photoreceptor cells are not fused. The eight photoreceptor cells have light-sensitive structures, the rhabdomeres, that are optically isolated from each other. The rhabdomeres of the retinula cells R1–6 form six independent light guides situated circumferential as compared to the two central rhabdomeres forming one serial light guide. This rhabdomere–tandem consists of the rhabdomeres of the retinula cells R7 and R8. The central rhabdomere–tandem of cells R7/8 shares the same visual axis of six retinula cells from six different adjacent ommatidia. The eight photoreceptor cells per ommatidium of a fly compound eye are assigned to two visual pathways, which are processed in parallel (Strausfeld and Lee 1991). The neural superposition system is a monovariant system, i.e. based on one receptor type, for motion detection (Yamaguchi et al. 2008). The retinula cells R1–6 of each ommatidium possess different visual axes, but six retinula cells from six different adjacent ommatidia, which share the same visual axis and are arranged in a trapezoid pattern
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(Fig. 6), form a neuro-ommatidium. The excitation of the corresponding retinula cells is neurally pooled by a neuroommatidium in the lamina. For the neuro-ommatidium, the signal in terms of photon captures is thus six times stronger than that in an apposition eye and without reduction in visual acuity, provided the rhabdomeres of the neurally superimposed retinula cells are properly aligned (Land and Nilsson 2002). The axons of such retinula cells (except the central ones, which pass through to the second optic ganglion) converge onto the same cartridge of secondary neurons in the first optic ganglion, the lamina. Thus, each lamina cartridge gets input through six different ommatidia from six retinula cells sharing the same visual axis (Zeil 1983). The spectral sensitivity of the retinula cells R1–6 possesses two major peaks; one peak is caused by the visual pigment exhibiting peak sensitivity in the green wavelength range, and the other, more prominent one is caused by sensitizing pigments with peak sensitivity in the ultraviolet wavelength ranges (Kirschfeld et al. 1977; Minke and Kirschfeld 1979). The absolute spectral sensitivity of single retinula cells R1–6 is similar to that of the retinula cells R7 and R8 (Hardie 1979), which indicates that these visual pathways are unlikely to function under either photopic or scotopic light conditions and fits to their supposed functions as motion-sensitive and colour-sensitive systems. The retinula cells R7 and R8 belong to the tetravariant visual system, i.e. based on four receptor classes, as there are two types of R7/8 rhadomere tandems—named ‘pale’ and ‘yellow’ due to appearance in transmitted light. The compound eyes of flies thus possess four types of central photoreceptors: the retinula cells R7p, R8p, R7y, and R8y. Since the peak sensitivity of the four retinula cells R7p, R8p, R7y, and R8y differs and covers the ultraviolet, blue, and green ranges of wavelength, it offers appropriate preconditions for colour vision (see below). The spectral sensitivity of these four photoreceptors seems to be rather uniform among flies (Fig. 1; Bishop 1974; Horridge et al. 1975; Tsukahara and Horridge 1977a, b; Stark et al. 1979; Hardie and Kirschfeld 1983; Hardie 1985; Yamaguchi et al. 2010). The information delivered by these retinula cells is processed in the second optical ganglion, the medulla, where second-order neurons that contact both R7 and R8 retinula cells from a single ommatidium, or different ommatidia, have been identified (Morante and Desplan 2008). Besides five classes of visual pigments, the ommatidia of flies contain screening pigments located in the pigment cells. The typical red colour of the compound eyes of D. melanogaster, Calliphora vicina, and of many other flies is caused by screening pigments that absorb the light of wavelengths 510 nm as shown in tests with monochromatic light stimuli (Fig. 3; Lunau and Wacht 1994). The admixture of small amounts of ultraviolet and blue light 510 nm and absorbs blue and ultraviolet light (Fig. 3; Lunau 1995, 2000; Wacht et al. 1996). Both female and male imagoes of E. tenax can be trained to land on blue flowers, but cannot be induced to extend the proboscis towards blue colour patches despite prolonged training and differential conditioning sensu Dyer and Chittka (2004) (Lunau 1988; Hohmann, Donda and Lunau, personal communication). By contrast, in houseflies, classical conditioning to visual colour stimuli was successful (Fukushi 1976). Yellow floral guides, mimicking the colour of yellow pollen and anthers (Lunau 2000, 2007), thus bear a large potential to manipulate the movements of pollen-eating hoverflies and flowers (Dinkel and Lunau 2001). When floral guides are present in colour gradients, e.g. comprising red, orange, and yellow dot guides as known from fly-pollinated Saxifraga flowers, E. tenax flies proceed towards the yellow dots (Lunau et al. 2005). Interestingly, the spontaneous proboscis reflex towards yellow colours is shown by other species of the Eristalinae, but is not or less pronounced in more distantly related hoverfly species (Wacht et al. 1996). The relative importance of different visual cues of oviposition sites has been demonstrated for the apple maggot fly, Rhagoletis pomonella (Tephritidae). In behavioural tests, in which the size, shape, and colour of target stimuli were varied, both sexes preferred dark, i.e. red, blue, violet, black, and dark orange objects over light, i.e. green, yellow, white, and light orange ones, if the objects were small and spherical, but preferred yellow objects if they were large and rectangular. Prokopy (1968) interpreted his findings convincingly as follows: the flies are attracted towards a large yellow area as if it was foliage and are attracted to small spherical objects as though they might be developing fruits. The size and shape of the objects thus determined the corresponding colour preference of the apple maggot fly. The reproductive biology of the apple maggot fly elucidates this choice behaviour. Developing fruits are oviposition sites for females and rendezvous sites for males. The response to spherical objects seems to rely on brightness cues only, whereas the response towards a larger object is based on colour vision and colour discrimination (Prokopy 1968). Similar preferences have been demonstrated for the Mediterranean fruit fly Ceratitis capitata (Nakagawa et al. 1978).
In many ecological studies, the research aims at catching a large diversity of fly species (Vrdoljak and Samways 2012) rather than exploring the preferred colour. In most studies, several coloured traps of different colour but similar size and exposure are used. However, the reflection properties of the trap colours are only rarely communicated, and in many cases, the hue of the pan trap colour as viewed by humans is the only colour attribute reported, whereas the ultraviolet wavelength ranges are often not considered, preventing correct interpretations of the colour preferences underlying the trap catches. Colour preferences might cause catches of flies in coloured pan traps (Ssymank 2001; Laubertie et al. 2006), but in many cases it remains unclear whether these preferences relate to flowers of food plants, egg-laying substrates, host organisms, or other relevant objects resting sites for warming up for example. In addition, the array of coloured pan traps used could lead to bias in the catches due to competition between similarly coloured traps. Moreover, in many studies, the spectral reflectance properties of the trap colours are not communicated, particularly the UV-reflectance properties, and thus hamper conclusions on colour preferences of the flies caught. Some studies, however, provide results enabling conclusions regarding colour preferences of distinct fly species (Ssymank 2001; Laubertie et al. 2006). This may permit trap colours to be chosen, in particular circumstances that are ecologically selective for different types of insect (Kirk 1984). Although in field studies with sticky coloured traps a preference for orange over yellow, green, blue, red, black, and white of the Caribbean fruit fly, Anastrepha suspensa (Tephritidae), has been demonstrated, it was noted that fly capture rates were directly related to the proportion of light reflected in the wavelength range between 580 and 590 nm (Greany et al. 1977). Similar results were obtained in a study of the effect of colour hue and brightness of artificial oviposition substrates on the selection of oviposition site by the olive fruit fly, D. oleae. Females preferred yellow and orange over red, blue, black, and white oviposition sites, and ranges of wavelength fostering oviposition (560 and 610 nm) as well as ranges of wavelength inhibiting oviposition (400–480, 520–550, >610 nm) could be identified (Katsoyannos et al. 1985). Despite comprehensive characterization of the colour stimuli, it remained unclear whether the attraction towards the colour stimuli was caused by one colour hue category, by overall brightness or by the brightness in one small wavelength range. Re-evaluation of these studies within the framework of known photoreceptor sensitivities and the colour vision model of Troje (1993) seems promising. However, trap colour design might be precise enough that the dependence of wavelength-specific reflectance intensity for the magnitude of blue colour preference
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in the onion fly Delia antiqua (Anthomyiidae) could be demonstrated under field conditions (Vernon 1986). Field observations of flies targeting coloured substrates and objects and field collections of flies by means of coloured traps are often interpreted as if providing indirect evidence for colour vision or colour preference (Campbell and Hanula 2007), although alternative explanations have not been adequately considered in many cases. Numerous flies of great economic importance have been studied intensively including their response to visual stimuli, e.g. bloodsucking parasites for humans and domestic animals like horse and deer flies (Tabanidae) as well as simuliid flies (Simuliidae), vectors of diseases like tsetse flies (Glossinidae), pathogenic germs like the housefly M. domestica (Muscidae), and pests of field crops like fruit flies (Tephritidae) (Khan 1978; Green 1994; Gibson and Torr 1999; Levinson et al. 2003). The responses of organisms towards objects bearing natural intraspecific or interspecific colour signals, as well as those towards artificial colour signals like coloured traps, provide little reliable indication of an ability of colour vision, because the response is not necessarily caused by colour; intensity and polarization pattern provides visual stimulus components associated with colour without being an attribute of the chromaticity of the stimulus. Non-visual attractants associated with colour cues represent another source of response to colour cues in flies. Within the monophyletic taxon of true flies, Brachycera (Yeates and Wiegmann 1999), there are all kinds of proofs, evidences, and indications of colour vision for various species.
Flies and visual mimicry Flies are well known as mimics of other organisms like bumblebees, wasps, and spiders (Howarth et al. 2000) and copy the conspicuous aposematic colour patterns of their models (Lunau 2011). However, flies are not addressees of these colourful mimic signals, which are mostly directed to animals predaceous on flies. At least, it is unknown whether the mimic colour signals play a role in the mate recognition of flies, too. In a few mimicry systems, flies act as signal receivers responding to visual mimicry, i.e. carrion-mimicking, mushroom-mimicking, and sexually deceptive flowers. Many flowers pollinated by carrion flies and saprophilous flies mimic olfactory and visual cues of carcasses or rotten plants to attract fly pollinators (Angioy et al. 2004; van der Niet et al. 2011). Mimicked olfactory cues of carcasses seem to be far more important than visual cues, which are only important when selecting a final landing site. This has been demonstrated in behavioural tests with the blowfly, L. sericata (Wall and Fisher 2001). The colour of
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J Comp Physiol A
carrion-mimicking flowers is rather uniform even in unrelated plant species; the flowers predominantly look fleshy, reddish, or brownish and have a texture that reminds many observers of layers of mould fungi. Since the largest flowers (Rafflesia, Rafflesiacae) of the world attract carrion flies, size of the mimicked cadaver seems to play a role for attraction (Beaman et al. 1988). The sensitivity to red light found by electrophysiological methods in C. erythrocephala (Autrum and Stumpf 1953) seems consistent with this finding, but has not been confirmed by later research. In fact, Goldsmith (1965) showed that sensitivity in the red wavelength range was an artefact due to a recruitment of additional ommatidia during electrophysiological recordings caused by leakage of red wavelengths through the screening pigments. Some mushroom-mimicking flowers that are pollinated by flies mimic not only chemical and tactile cues of mushrooms, but also visual cues including size, shape, and colour pattern. Doing so, the flowers not only attract flies as potential pollinators, but also manipulate the flies to deposit eggs on the flowers. The egg-laying behaviour of flies has been reported for two mushroom-mimicking flowers displaying a striking resemblance to real mushrooms. The flowers of the Mexican tree Aristolochia arborea (Aristolochiaceae) closely resemble mushrooms of the genus Marasmius (Marasmiaceae) and are assumed to be pollinated by small sawflies, but pollination by fungus gnats or flies has not been excluded (Vogel 1978). The females on their search for a suitable place for egg-laying fall into the flytrap. Having been trapped in this way, the flies use positive phototaxis and desperately try to escape through a ‘window’ composed of transparent cells; while doing so, they continuously touch the sticky stigma and deposit some of the pollen grains brought in from previously visited flowers. Not till the next day do the anthers open and shed pollen onto the flies, after which the flower wilts and the flies can escape. Also, some orchids of the genus Dracula are pollinated by mycophilous drosophilid flies of the genus Zygothrica (Endara et al. 2010). The multimodal mimicry of chemical, visual, and tactile cues of mushrooms by fly-pollinated mushroom-mimicking flowers is probably due to the fact that egg-laying in the flowers significantly decreases the fitness for the deceived fly females, because the fly larvae cannot develop in the floral tissues. It can be assumed that those females using more and more complex cues to discriminate between real and mimic mushrooms will gain a net fitness benefit. Interestingly, maculated leaves may play a role in attracting flies by mimicking fungus-infected foliage (Ren et al. 2011). Sexual deception of bombyliid flies (Bombyliidae) occurs in South African daisies, e.g. Gorteria diffusa (Ellis and Johnson 2010; Johnson and Midgley 1997; Thomas et al. 2009). As shown by Ellis and Johnson (2010),
J Comp Physiol A
Gorteria forms eliciting mating behaviour in bombyliid males are less attractive for females and vice versa, suggesting males and females have different preferences and thus select for different floral traits. Paulus (2007) describes the possible deception of male Merodon velox (Syrphidae) by orchids of the species Ophrys regis-ferdinandii (Orchidaceae). The blue and shiny labellum of the orchid resembles the blue-winged males of Merodon velox hoverflies, whereas the females have clear wings; it is thus assumed that not sexual deception but territorial defence is involved in this mimicry system.
Conclusions Flies have evolved one of the most elaborate visual systems among insects. Evidence for colour vision and colour preferences in flies, however, is limited at least as compared to other insect taxa such as bees. Interestingly, only a few flies exhibit a sexual dimorphism of coloured courtship signals, indicating that courtship and mating are based on cues other than colour. The interactions between flies and plants seem to be based on colour cues more frequently than the interactions of flies with conspecifics and with animal hosts. Flies visiting flowers for nectar and pollen as well as flies ovipositing on plant organs like fruits make use of colour vision. In some cases, even distinct colour preferences have been demonstrated. Colour vision and colour preferences at least of selected fly species can be easily studied in laboratory set-ups, because some flies can be bred indoors, some can be collected in large numbers as larvae, and many flies are easy to handle in laboratory conditions. The electrophysiological and genetic data suggest that the equipment of compound eyes in flies is rather uniform, facilitating the assignability of physiological data from model species to particular study species. Future research on colour vision and colour preferences would benefit from developing a model of fly colour vision and provision of software to calculate and illustrate colour loci in an appropriate colour space, as might be predicted from the publication of a colour vision model for bees (Chittka 1992) and publications based thereon. In addition, electrophysiological recordings of the spectral sensitivity of individual photoreceptors in more species could demonstrate specific adaptations to light habitats or ecological specialization in flies. Thus, the interpretation of colour-based behavioural reactions of flies targeting natural colour stimuli like flowers or oviposition substrates or artificial colour stimuli like artificial flowers and pan traps can be thoroughly improved. Acknowledgments I thank Anne Thorson for linguistic improvement, Sarah Papiorek for critical comments on the manuscript and help with the preparation of some figures, and Francismeire Telles for discussion about spectral sensitivity curves for Eristalis tenax. Two
anonymous reviewers commented in a very constructive manner and helped to improve the manuscript.
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