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Zeitschrift/Journal: Entomologie heute

Jahr/Year: 2018

Band/Volume: 30

Autor(en)/Author(s): Neimann Alexander, An Lina, Lunau Klaus

Artikel/Article: The Yellow Specialist: Colour Preferences and Colour Learning of the tenax (Diptera: Syrphidae). Der Gelbspezialist: Farbpräferenzen und Farbenlernen der Schwebfliege (Diptera: Syrphidae) 27-44 Colour preferences and colour learning of the hoverfl y Eristalis tenax 27

Entomologie heute 30 (2018): 27-44

The Yellow Specialist: Colour Preferences and Colour Learning of the Hoverfly Eristalis tenax (Diptera: Syrphidae)

Der Gelbspezialist: Farbpräferenzen und Farbenlernen der Schwebfliege Eristalis tenax (Diptera: Syrphidae)

ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU

Summary: The hoverfl y Eristalis tenax (Syrphidae, Diptera) has a pronounced preference for yel- low fl owers like many other members of the syrphid . Experiments testing landing behaviour and extension indicate that E. tenax has an innate preference for yellow colours. Little is known about colour learning in E. tenax and about colour parameters determining the fl ies’ colour preference. This study focuses on the colour preference and colour learning regarding the role of UV-refl ection properties for visiting yellow fl owers. In multiple choice experiments with artifi cial fl owers inexperienced and naïve E. tenax fl ies showed a clear preference for yellow colours, but no preference in landing behaviour for UV-absorbing or UV-refl ecting yellow artifi cial fl owers. In ad- dition, the fl ies also chose bright UV-absorbing non-yellow artifi cial fl owers for landing. The fl ies extended their proboscis preferably towards dark and UV-absorbing yellow colour patches. These results suggest that brightness has a so far unknown infl uence on colour choice both for landing and proboscis extension. The colour preferences of E. tenax seem to be fi ne-tuned to yellow fl owers displaying an ultraviolet refl ection pattern.

Keywords: Eristalis tenax, dronefl y, colour preference, fl ower visitation

Zusammenfassung: Die Schwebfl iege Eristalis tenax (Syrphidae, Diptera) hat eine ausgesprochene Präferenz für gelbe Blüten wie viele andere Schwebfl iegen auch. Experimente zum Landeverhal- ten und zur Rüsselrektion belegen eine angeborene Präferenz von E. tenax für gelbe Farben. Nur wenig ist bekannt über Farbenlernen bei E. tenax und über die Eigenschaften von Farben, die die Farbpräferenz bestimmen. Diese Studie beschäftigt sich mit Farbpräferenzen und Farbenlernen und den Einfl uss von UV-Refl exion auf den Besuch von gelben Blütenattrappen. In Mehrfachwahlex- perimenten mit unerfahrenen und naiven E. tenax zeigten die Fliegen eine klare Präferenz für gelbe Farben, aber keine Präferenz für UV-refl ektierende oder UV-absorbierende gelbe Blütenattrappen. Zusätzlich wurden helle, UV-absorbierende, nicht-gelbe Blütenattrappen für die Landung gewählt. Die Fliegen zeigten die Rüsselreaktion bevorzugt zu dunklen, UV-absorbierenden Farbfl ecken. Diese Ergebnisse belegen einen bislang unbekannten Einfl uss der Helligkeit auf die Farbwahl bei Landung und Rüsselreaktion. Die Farbpräferenzen von E. tenax scheinen fein abgestimmt zu sein auf den Besuch von gelben Blüten mit einem UV-Muster.

Schlüsselwörter: Eristalis tenax, Mistbiene, Farbpräferenz, Blütenbesuch

1. Introduction plant (VON FRISCH 1914; KELBER & OSORIO 2010; HOPKINS & RAUSHER 2012; LUNAU & Many fl ower visitors use visual colour cues MAIER 1995; VAN DER KOOI et al. 2018). The of fl owers to identify and fi nd their food dronefl y Eristalis tenax (Syrphidae, Diptera)

Entomologie heute 30 (2018) 28 ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU is a Batesian mimic of the Western honeybee of the fl ies (BASTIAN 1986; GILBERT 1986). Apis mellifera (GOLDING & EDMUNDS 2000; The fl ies take from fl owers for energy LUNAU 2011). Honeybees and dronefl ies visit supply (WOODCOCK et al. 2014). fl owers for nectar and (SRINIVASAN Previous studies demonstrated that E. & GUY 1990). The imagines are usually tenax fl ies respond to light stimuli while observed from March to October visiting flying and walking (MAST 1923), have fl owers or laying eggs at manure heaps and colour vision and possess a preference eutrophic waters (GILBERT 1986). The larvae for yellow colours (ILSE 1949). The fl ies exhibit a saprophagous live style in polluted exhibit fl ower constancy also for fl owers waters, muddy pools and liquid manure of other colours than yellow (KUGLER and are considered to be an indicator for 1951). E. tenax exhibits an innate probos- polysaprobic water quality (KOLKWITZ & cis refl ex towards yellow colours (LUNAU MARSSON 1909; CHAPMAN 1996). Because of 1987; STERNKE-HOFFMANN & LUNAU 2015). the extended larval anal breathing tube, the Pollen, anthers and fl ower marks of ma ny larvae of E. tenax are called rat-tailed mag- entomophilous fl owers visited by E. tenax gots. The imagines of E. tenax are consid- refl ect wavelengths longer than 510nm and ered as important in greenhouse absorb UV-light (LUNAU & WACHT 1997a). agriculture (JARLAN et al. 1997). In the wild Yellow and UV-absorbing pollen, anthers the fl ies usually visit yellow and white fl ow- and fl ower marks trigger a spontaneous ers for pollen and nectar (GILBERT 1986; DE proboscis refl ex in newly emerged and BUCK 1990). The freshly hatched imagines inexperienced E. tenax imagines (LUNAU depend on pollen in the fi rst place. The 1988; LUNAU & WACHT 1994, 1997a). This nutrients contained therein are essential for response to yellow colours is innate and the development of the system cannot be modifi ed by training (LUNAU

Fig. 1: Spectral sensitivity of the R8y photoreceptor type of Eristalis tenax (after TSUKAHARA & HORRIDGE 1977; dashed line) and spectral effi ciency function of the innate proboscis extension towards monochromatic test stimuli (solid line). Both functions are normalized at the maximum. Modifi ed from LUNAU & WACHT (1994). Abb. 1: Spektrale Empfi ndlichkeit des R8y-Photorezeptortyps von Eristalis tenax (nach TSUKAHA- RA & HORRIDGE 1977; gestrichelte Linie) und spektrale Reizwirksamkeitskurve der angeborenen Rüsselreaktion auf monochromatische Teststimuli (durchgezogene Linie). Beide Funktionen sind normalisiert auf das Maximum. Modifi ziert nach LUNAU & WACHT (1994). Colour preferences and colour learning of the hoverfl y Eristalis tenax 29

1988; LUNAU et al. 2018). The innate pro- fl ower visiting (LUNAU & MAIER boscis refl ex is triggered by monochro- 1995; VAN DER KOOI et al. 2018) because matic light stimuli in the small range of they need to detect fl owers of potential wavelength between 520nm and 600nm foodplants and to discriminate between (LUNAU & WACHT 1994) and inhibited by fl owers of different plant . Honey- admixed blue and ultraviolet light (LUNAU (A. mellifera) and (Bombus & WACHT 1997b). These results suggest terrestris) are known for their colour prefer- that the stimulation of the retinula cell ence and their abilities of colour learning R8y is involved in this response to green and colour discrimination (ROHDE et al. and yellow monochromatic light (LUNAU 2013). & WACHT 1994; Fig. 1) stimuli similar to Many yellow fl owers display a so-called reactions known as wavelength-specifi c UV bull’s eye, i.e. an ultraviolet refl ection behaviour (CRONIN et al. 2014). pattern with a UV-absorbing centre part The compound eyes of fl ies consist of (LUNAU 2007). From experiments with hundreds to thousands ommatidia. All om- honeybees and bumblebees it is known matidia possess eight photoreceptor cells. that they respond to this kind of fl oral Although colour vision in fl ies is largely colour pattern. Bees do not discriminate understudied, most studies agree to as- between yellow fl owers with or without sume to separate visual subsystems, which a UV-absorbing fl ower centre, but the are a colour-blind neural superposition fi rst physical contact with the fl ower by subsystem and a tetra variant colour vision means of the antennae is targeting to the subsystem (for review see LUNAU 2014). UV-absorbing area (PAPIOREK et al. 2016). The six peripheral receptor cells are labelled Similar studies for hoverfl ies are missing. R1-R6, have identical spectral sensitivity, This study aims to investigate how E. tenax are organized in a neuronal superposition fl ies respond to yellow colours when land- system and are responsible for motion vi- ing and when extending the proboscis with sion (LUNAU & WACHT 1994; LUNAU 2014). particular reference to the UV-refl ection The two interior receptor cells R7 and R8 properties. For this purpose the innate are arranged as a tandem and termed yel- preference for single-coloured artifi cial low (R7y and R8y) or pale (R7p and R8p) fl owers varying in brightness and colour in regard to the appearance of the omma- hue are studied as well as colour learning tidia in orthodromic illumination (HARDIE experiments. The data analysis is based on 1986; HARDIE & KIRSCHFELD 1983) and are the spectral refl ectance properties of the responsible for colour vision (TROJE 1993; tested colours and to a lesser extent based KELBER 2001; KELBER et al. 2003; LUNAU on the colour space of fl ies. The colour 2014). The retinula cell tandems, R7y/P8y, vision model of fl ies (TROJE 1993) that resp. R7p/R8p, are arranged with the R7 predicts that fl ies can discriminate only retinula cell located distal to R8 retinula cell. four colour categories, has been success- It is assumed that E. tenax fl ies thus possess fully applied for understanding of fl ower tetrachromatic colour vision. R7p is most colour choice in Eristalis fl ies (ARNOLD et sensitive to ultraviolet light, whereas R8p is al. 2009; BERGAMO et al. 2018; GRAY et al. sensitive in the blue range of wavelength. 2018). Spontaneous choice experiments R7y is sensitive to ultraviolet and blue light, with yellow artifi cial fl owers displaying a whereas R8y is sensitive to green light (LU- real or, alternatively, an inverse bull’s eye NAU & WACHT 1994). pattern are set up to test the meaning of Colour preference and colour learning are these colour patterns for fl ower choice considered to be important features for and handling.

Entomologie heute 30 (2018) 30 ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU

2. Materials and methods ground in a circle of 60 cm in diameter. By this means the fl ies could choose between 2.1. keeping multiple horizontally oriented artificial when approaching from above The experiments were performed with (Fig. 2A). Additionally, some dummies naive Eristalis tenax that had were covered with UV-absorbing (UV-) or never visited real or artifi cial fl owers be- UV-transmitting (UV+) foil to vary the UV- fore the tests. Pupae and larvae of the refl ection properties. No foils were used if last instar were collected on a farm near the dummies were made of materials that Düsseldorf in 2017 and transferred to exhibited these UV-features on their own. the laboratory of the Institute of Sensory The dummies in the multiple choice land- Ecology of the Heinrich-Heine-Univer- ing experiments were always unrewarded. sity, where they were kept in metal boxes A box with the fl ies was opened within the (length×width×height = 35.5×25.5×19.5 mosquito net so that the fl ies could move cm) with a glass ceiling. Freshly emerged freely within the fl ight cage. imagines were kept in similar boxes in a For the proboscis reaction experiment rec- laboratory at a temperature of 25°C. Two tangular dummies (6.0×1.5 cm) were made fl icker-free Osram Biolux L58W/965, 500lx out of white Whatman No. 1 fi lter paper. lamps above the boxes provided a 12-hour In the middle they had two holes with a day/night cycle. Two sponges, one soaked diameter of 3mm and a distance of 4mm to with a colourless mixture of 1 part honey each other. Under the holes different materi- and 3 parts water served as food source als could be attached, which then served as for the fl ies and the other one with pure fl ower marks (Fig. 2B). In order to increase water in order to provide drinking and motivation for feeding the fl ies were placed keep humidity for fl ies. The experiments on a strip of fi lter paper soaked 30% sugar required hungry fl ies motivated to search water. The contact of the chemoreceptors for food, therefore the fl ies were starved in the foreleg tarsi with the solution stimu- for 48 h before the experiments. To study lated the fl ies to actively search for more the fl ower visiting behaviour of E. tenax the food sources. Following stimulation the fl ies experiments were designed as fi eld tests in were placed on one end of the unrewarded a park near the institute inside a mosquito dummy and then had to walk across the net (length×width×height = 2×1×1 m). dummy towards the holes and decide in The ground of the fl ight cage consisted of favour of one of the two presented fl ower natural green lawn. marks with an aimed dubbing with the pro- boscis. The test was repeated with the fl y 2.2. General description of the test placed on the opposite end of the dummy procedures in order to avoid side preferences. The spectral refl ectance properties of all The experiments consisted of multiple dummies were measured with a spectro- choice tests with naïve and non-trained photometer (USB4000 spectrophotometer, fl ies, dual choice tests following training Ocean Optics, Inc., Ostfi ldern, Germany) and dual choice tests of the spontaneous and the program SpectraSuite (Figs. 3-7). proboscis refl ex. A two-sided Chi-square test was conducted The fl ower dummies for landing behaviour to determine the signifi cant detection level tests varied with each test. In general, the (p<0.05 for signifi cant and p<0.01 for highly fl ower dummies were attached to 20 cm signifi cant values) in the evaluation of the long wooden sticks which were put into the results. Colour preferences and colour learning of the hoverfl y Eristalis tenax 31

Fig. 2: Experimental setups. A Arrangement of the artifi cial fl owers in the multiple choice tests. B Dual choice test of the innate proboscis refl ex. C Y-shape arrangement of artifi cial fl owers in the training experiments. D UV-photo of a Helianthus annuus infl orescence used for the prepara- tion of artifi cial fl owers. Dark areas are UV-absorbing. E Artifi cial fl ower made of ray fl orets of Helianthus annuus. The petals were cut in the middle; in this case the dummy is made from basal UV-absorbing parts of the petals. F UV-photo of an Oenothera biennis fl ower. The dark base of the petals is UV-absorbing. Abb. 2: Experimenteller Versuchsaufbau. A Anordnung der Blütenattrappen in den Mehrfachwahl- versuchen. B Zweifachwahlversuch der angeborenen Rüsselreaktion. C Y-förmige Anordnung der Blütenattrappen in den Dressurversuchen. D UV-Foto eines Blütenstands von Helianthus annuus, der für die Herstellung von Blütenattrappen genutzt wurde. Dunkle Bereiche sind UV-absorbierend. E Blütenattrappe, die aus den Strahlenblüten von Helianthus annuus hergestellt wurde. Die Blütenblätter wurden in der Mitte geteilt; in diesem Fall ist die Attrappe aus den basalen, UV-absorbierenden Bereichen der Blütenblätter hergestellt. F UV-Foto einer Blüte von Oenothera biennis. Die dunklere Basis der Blütenblätter ist UV-absorbierend.

Entomologie heute 30 (2018) 32 ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU

Fig. 3: Spectral refl ectance of bright artifi cial fl owers for multiple choice test with naive imagines of Eristalis tenax. Abb. 3: Spektrale Refl exion der hellen Blütenattrappen für Mehrfachwahlversuche mit naiven Imagines von Eristalis tenax.

Fig. 4: Spectral refl ectance of dark artifi cial fl owers for multiple choice test with naive imagines of Eristalis tenax. Abb. 4: Spektrale Refl exion der dunklen Blütenattrappen für Mehrfachwahlversuche mit naiven Imagines von Eristalis tenax.

Fig. 5: Spectral refl ectance of the four yellow dummies from the multiple choice landing test. Abb. 5: Spektrale Refl exion der vier gelben Blütenattrappen aus dem Mehrfachwahl-Landeversuch. Colour preferences and colour learning of the hoverfl y Eristalis tenax 33

Fig. 6: Spectral refl ectance of different fl ower dummies: ß-carotene, Helianthus annuus, Rudbeckia hirta and Oenothera biennis. Abb. 6: Spektrale Refl exion der verschiedenen Attrappen: ß-Carotin, Helianthus annuus, Rudbeckia hirta und Oenothera biennis.

Fig. 7: Spectral refl ectance of the four green colours used in the training experiments. Abb. 7: Spektrale Refl exion der vier grünen Farben für die Dressurexperimente

2.3. Multiple choice tests of landing each other. Every 30 min during the test the behaviour with naïve fl ies order of the colours was randomly changed. In separate multiple choice tests either the The coloured artifi cial fl owers were discs bright or the dark colours were tested. with a diameter of 3 cm and without fl ower The most preferred yellow colours of the mul- marks and made of fi lter paper Whatman tiple choice tests were also used in a dual choice No. 1 and printed using a Canon MX925 test for the proboscis extension (see below). inkjet printer and original ink in the colours blue, red, yellow, green, pink and white; all 2.4. Dual choice test of landing be- colour were printed either bright or dark. haviour with naïve fl ies and ß-carotene The landing behaviour experiments con- artifi cial fl owers sisted of twelve fl ower dummies arranged in a circle with the artifi cial fl owers covered The ß-carotene fl owers were made of What- with UV+ foil and with UV- foil next to man No. 1 fi lter paper and coloured with ß-

Entomologie heute 30 (2018) 34 ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU carotene solution. ß-carotene was used here rewarded, the test started. In the test one of to closely resemble natural pigmentation of the last two artifi cial fl owers was replaced by fl owers. The procedure for colouring was one unknown to the fl y. The fl y was caught adopted from PAPIOREK et al. (2016). For and released again on the fi rst fl ower. Again this purpose, dummies with a diameter of the fl y had to visit the four fl owers arranged 3 cm made of fi lter paper were immersed in a line, but then to decide for one of the for three seconds in a solution of 1.82 ml fl owers at the fork end, either the trained carotene (an oily solution from Carl Roth one or the unknown artifi cial fl ower. In GmbH & Co. KG, Karlsruhe, Germany) the reciprocal experiment, other fl ies were and 50 ml hexane. After evaporation of the trained on the previously unknown artifi cial solvent hexane either a UV+ foil or a UV- fl ower and were given the same dual choice foil was applied to the dummies, which not in the test. only provided the dummies with different UV-features, but also prevented a possible 2.6. Dual-choice test of landing behav- emission of scents of the ß-carotene solu- iour and proboscis extension with real tion. The dual choice test consisted of six fl ower stimuli artifi cial fl owers arranged in a circle, three of which were covered with UV-transmitting In the landing behaviour and proboscis and three with UV-absorbing foil. The ß- reaction experiment with real fl ower stimuli carotene artifi cial fl owers were used also in petals (ray fl orets) of the Black-Eyed Susan training and proboscis reaction experiments, Rudbeckia hirta and the sunfl ower Helianthus were they served as UV- or UV+ fl ower annuus (Asteraceae) were used. marks. In order to prevent premature bleach- Their ray florets exhibit different UV- ing of the coloured dummies, they were refl ection properties (Fig. 2D) with the kept in the dark and were replaced after 30 base being UV-absorbing and the periph- minutes of exposure to outside conditions. ery being UV-refl ecting (Fig. 2E). The ray fl owers were cut at the border between 2.5. Dual choice test of landing behav- the UV-absorbing base and UV-refl ecting iour with trained fl ies and ß-carotene periphery and then glued (solvent-free artifi cial fl owers paper glue, Stylex Schreibwaren GmbH, Bad Bentheim) on filter paper discs In addition, a training experiment with (Ø 3 cm) resulting in two different varieties similar ß-carotene artifi cial fl owers was set of dummies, one UV-absorbing, the other up. The learning tests were performed with UV-refl ecting. The testing procedure was six artifi cial fl owers. Four of them were similar to that of the ß-carotene experi- arranged in a line with a distance of 10 cm ment without the use of UV-An additional from each other. Two additional fl owers landing experiment was performed with the were arranged at one end of the line at an intact ray fl orets of H. annuus, which were angle of 45° with the same distance to other glued either with the tip or with the base artifi cial fl owers, so that the arrangement pointing to the centre of a white fi lter paper had a Y-shape if seen from above (Fig. 2C). disc (Ø 5 cm) resulting in fl ower dummies The dummies were rewarded with a droplet with either an UV-absorbing centre and an of glucose solution (Biogluc 30%). After be- UV-refl ecting periphery or with the inverse ing placed on the fi rst fl ower, the fl y had to array. Both kinds of semi-natural fl owers accept the reward and to become motivated were presented simultaneously to the fl ies for further food search. After having visited with the objective to document the most all six dummies by the fl y and always being preferred fl ower for landing and to survey Colour preferences and colour learning of the hoverfl y Eristalis tenax 35 the target of the fi rst proboscis reaction if 2.7. Dual-choice following training such would occur. with green artifi cial fl owers varying in The third experiment with real petals was brightness performed with the common evening primrose Oenothera biennis. The petals of this The rationale of these experiments was to fl ower have an UV-absorbing base and a rela- study the impact of the brightness of colour tively strong UV-refl ecting periphery (Fig. stimuli on colour preference. The experi- 2F). Three dummies to test the proboscis ment was performed through the training reaction in dual-choice tests were built, the of the fl ies on four different green artifi cial fi rst with fl ower marks made from the basal fl owers made from HP Advanced glossy and peripheral part of the evening primrose, photo paper and displaying a 2 mm-sized the second made from the peripheral part of yellow spot in the middle. The experimental the evening primrose petal covered with UV- set-up resembled that of the ß-carotene absorbing or UV-transmitting foil and the training experiment with the following dif- third made from the strongly UV-refl ecting ference in the process of training: the train- peripheral part of evening primrose and/or ing and testing were performed in one trial the other from strongly UV-absorbing basal with the fl ies being trained on fi rst four fl ow- part of R. hirta. ers and then offering a dual-choice between

Fig. 8: Colour loci in the fl y colour space (TROJE 1993) of Eristalis tenax of artifi cial fl owers tested in dual choice tests. The spectral line indicates the colour loci of monochromatic light stimuli and mixtures of ultraviolet (350 nm) and yellow (550 nm) light stimuli. The corresponding spectral refl ectance curves are shown in Figure 7. Abb. 8: Farbloci der im Zweifachwahlversuch getesteten Blütenattrappen im Farbraum (TROJE 1993) von Eristalis tenax. Die Spektrallinie zeigt die Farbloci von monochromatischen Stimuli, bzw. einer Mischung von ultravioletten (350 nm) und gelben (550 nm) Lichtstimuli. Die zugehörigen spektralen Refl exionskurven sind in Abbildung 7 dargestellt.

Entomologie heute 30 (2018) 36 ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU the trained and a new colour. The training pendent of UV-refl ection properties over all was repeated for all colour combinations other colours (Fig. 9). resulting in 12 tests. The spectral refl ectance In order to investigate the preference for properties of these colour stimuli as well as the yellow colour in the proboscis refl ex, the respective colour loci in the fl y colour the four yellow dummies from the multiple vision model of TROJE (1993) are shown choice tests were tested against each other (Fig. 7, 8). For details for the calculation of in dual choice tests. In these cases the fl ies colour loci in the categorical colour vision signifi cantly preferred one of the colours model of TROJE (1993) see LUNAU (2014). offered as fl ower marks (Chi-square test, p-values p<0.01). The dark UV-absorbing 3. Results yellow colour was preferred over the dark UV-refl ecting one (n=85, p=1.20*10-16), and The multiple choice tests with artifi cial col- over the bright UV-absorbing yellow one our fl owers resulted in 50 landings on dark (n=83, p=6.79*10-7). The dark UV-refl ecting and 58 landings on bright artifi cial fl owers. yellow was preferred over the bright UV- Naïve Eristalis tenax fl ies given the multiple refl ecting yellow (n=83, p=5.26*10-20), and choice among twelve bright artifi cial fl owers the bright UV-absorbing yellow was pre- visited preferably the yellow colours inde- ferred over the bright UV-refl ecting yellow pendent of UV-refl ection properties and (n=85, p=2.33*10-28)(Fig. 10). the blue UV-absorbing colour, to a lesser Naïve E. tenax fl ies given the dual choice extend the pink and white UV-absorbing between ß-carotene artifi cial fl owers differ- colours, whereas all other colours, i.e. red, ing in UV-refl ection properties did not show green, UV-refl ecting blue, pink and white, any signifi cant landing preference neither for were signifi cantly less attractive (Fig. 9). By UV-refl ecting nor UV-absorbing artifi cial contrast, given the multiple choice among fl owers. The fl ies also did not exhibit any twelve dark artifi cial fl owers, naïve E. tenax preference for landing on artifi cial fl owers fl ies preferred only the yellow colours inde- made of Helianthus annuus and Rudbeckia

Fig. 9: Landing preference of naïve Eristalis tenax on twelve kinds of coloured dummies covered with either UV-absorbing or UV-transmitting foil (n=58 for bright colours and n=50 for dark col- ours). Different letters denote signifi cant differences (p<0.05) due to a two-sided Chi-square test. The corresponding spectral refl ectance curves are shown in Figures 3, 4. Abb. 9: Landepräferenz der naiven Eristalis tenax auf zwölf unterschiedlichen farbigen Blütenattrap- pen, die mit UV-absorbierender oder UV-transmittierender Folie abgedeckt waren (n=58 für helle Farben und n=50 für dunkle Farben). Unterschiedliche Buchstaben zeigen signifi kante Unterschiede (p<0,05) in einem zweiseitigen Chi-Quadrat-Test. Die zugehörigen spektralen Refl exionskurven sind in den Abbildungen 3 und 4 dargestellt. Colour preferences and colour learning of the hoverfl y Eristalis tenax 37

Fig. 10: Frequency of proboscis reactions of Eristalis tenax to the four yellow dummies from the multiple choice landing test. Different letters denote signifi cant differences (p<0.01) due to a two- sided Chi-square test. The corresponding spectral refl ectance curves are shown in Figure 5. Abb. 10: Häufi gkeiten der Rüsselreaktionen von Eristalis tenax auf die vier gelben Blütenattrappen aus dem Mehrfachwahllandeversuch. Unterschiedliche Buchstaben zeigen signifi kante Unterschiede (p<0,05) in einem zweiseitigen Chi-Quadrat-Test. Die zugehörigen spektralen Refl exionskurven sind in Abbildung 5 dargestellt. hirta petals (Fig. 11). The proboscis refl ex to proboscis signifi cantly more often to the ß-carotene fl ower marks was triggered sig- UV-reflecting peripheral part of Oeno- nifi cantly more often by UV-absorbing than thera biennis covered with UV-absorbing UV-refl ecting fl ower marks. The fl ies did foil as compared to that covered with not show any signifi cant differences in the UV-transmitting foil (n=30, p=9.31*10-7, proboscis reaction towards UV-absorbing Chi-square test). The fl ies extended their and UV-refl ecting fl ower marks made of proboscis signifi cantly more often to the the petals of Helianthus and Rudbeckia, both UV-absorbing basal part of Rudbeckia hirta UV-refl ecting and UV-absorbing parts of petals than to the UV-refl ecting periphery the petals (Fig. 11). of O.biennis petals (n=30, p=4.85*10-13, Experienced E. tenax following Chi-square test)(Fig. 13). training given the dual choice between In the experiment testing landing and sub- ß-carotene artifi cial fl owers differing in sequent proboscis reaction with artifi cial UV-reflection properties, did not show fl owers of H. annuus petals the fl ies did not any significant landing preference for prefer one kind of fl ower for landing, but UV-refl ecting or UV-absorbing artifi cial extended its proboscis signifi cantly more fl owers following training to UV-absorbing often towards the basal parts of the ray artificial flowers (n=15, p=0.796, Chi- fl orets independently of their position in the square test), but following training to centre or periphery of the artifi cial fl owers UV-refl ecting artifi cial fl owers signifi cantly (Fig. 14). preferred UV-refl ecting artifi cial fl owers In the dual choice tests with green artifi cial over UV-absorbing ones (n=15, p=0.020, fl owers the trained fl ies exhibited a clear Chi-square test)(Fig. 12). preference for the brighter colour irrespec- The marks made of the UV- tive of training to the brighter or darker absorbing base of Oenothera biennis petals colours in those four cases in which the trigger the proboscis refl ex signifi cantly difference in brightness between the two more often than those made of the UV-re- colours was strong (Fig. 15), whereas learn- fl ecting peripheral part (n=38, p=1.32*10-7, ing of colours that belong to different colour Chi-square test). The fl ies extended their categories was not found.

Entomologie heute 30 (2018) 38 ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU

Fig. 11: Frequency of landings and proboscis ex- tensions of Eristalis tenax on ß-carotene dummies with varying UV-refl ection properties (n=32, resp. n=42), dummies of petals of Helianthus annuus (n=10, resp. n=50) and Rudbeckia hirta n=30, resp. n=55). Signifi cance of results for the fl ies’ preference of UV-absorbing or UV- refl ecting dummies was tested with a two-sided Chi-square test. Non-signifi cant differences are not indicated. The corresponding spectral refl ec- tance curves are shown in Figure 6. Abb. 11: Häufigkeiten der Landungen und Rüsselreaktionen von Eristalis tenax auf Blüten- attrappen aus ß-Carotin mit unterschiedlichen UV-Refl exionseigenschaften (n=32, bzw. n=42), Blütenattrappen aus Petalen von Helianthus annuus (n=10, bzw. n=50) und Rudbeckia hirta (n=30, bzw. n=55). Die Signifi kanz der Ergebnisse für die Präferenz der Fliegen für UV-absorbierende oder UV-refl ektierende Blütenattrappen wurde mit dem zweiseitigen Chi-Quadrat-Test getestet. Nicht signifi kante Unterschiede werden nicht angezeigt. Die zugehörigen spektralen Refl exi- onskurven sind in Abbildung 6 dargestellt.

4. Discussion with artifi cial fl owers (ILSE 1949; DE BUCK 1990; LUNAU 1993). Some related hoverfl y As a fl ower visiting species Erista- species, like , resemble E. lis tenax is expected to have abilities needed tenax in the colour preference for visited for innate recognition of specifi c fl ower fl owers (LUNAU 1988), others are specialists, signals and those needed for learnt fl ower like spp. that collect airborne pollen discrimination. Besides olfactory cues, col- from surfaces of green (SSYMANK & our is one of the most important fl oral at- GILBERT 1993). The preference for yellow tributes used by pollinators to identify fl ow- colours in the landing behaviour seems to ers as potential food sources. The dronefl y be modifi able, since the fl ies have been ob- E. tenax is a worldwide common hoverfl y served on yellow (43%), white (37%) blue species and is known as a generalist being (13%) and different-coloured fl owers (7%) observed visiting many different fl owers (DE BUCK 1990). This fl ower colour prefer- (KORMANN 1988). However, several studies ence is not determined by the accessibility of have reported a preference for yellow fl ow- nectar and pollen alone, since other hover- ers and yellow colour hues in experiments fl ies like bombylans exhibit different Colour preferences and colour learning of the hoverfl y Eristalis tenax 39

Fig. 12: Frequency of landings of Eristalis tenax on ß-carotene dummies with varying UV-refl ection properties following training to UV-refl ecting or UV-absorbing dummies (n=30). Different letters denote signifi cant differences (p<0.05) due to a two-sided Chi-square test. The corresponding spectral refl ectance curves are shown in Figure 6. Abb. 12: Häufi gkeiten der Landungen von Eristalis tenax auf Blütenattrappen aus ß-Carotin mit unterschiedlichen UV-Refl exionseigenschaften nach dem Training auf UV-refl ektierende oder UV- absorbierende Blütenattrappen (n=30). Unterschiedliche Buchstaben zeigen signifi kante Unterschiede (p<0,05) nach einem zweiseitigen Chi-Quadrat-Test. Die zugehörigen spektralen Refl exionskurven sind in Abbildung 6 dargestellt.

Fig. 13: Frequency of proboscis reactions to fl ower marks made of petals from Oenothera biennis and Rudbeckia hirta. Different letters denote signifi cant differences (p<0.05) due to a two-sided Chi-square test. The corresponding spectral refl ectance curves are shown in Figure 6. Abb. 13: Häufi gkeiten der Rüsselreaktionen auf Blütenmalen aus Blütenblättern von Oenothera biennis und Rudbeckia hirta. Unterschiedliche Buchstaben zeigen signifi kante Unterschiede (p<0,05) nach einem zwei- seitigen Chi-Quadrat-Test. Die zugehörigen spektralen Refl exionskurven sind in Abbildung 6 dargestellt. preferences with 18% visits on yellow, 38% Among the twelve artifi cial fl owers with on white, 24% on blue and 20% different- six colour hues and different UV-refl ection coloured fl owers in Belgium (DE BUCK 1990). properties the E. tenax flies preferred The colour preference for yellow fl owers in the yellow colours independent of their Eristalis spp. is also seen if it is controlled UV-refl ection properties. This result un- for availability of fl owers (HASLETT 1989). derlines the preference for yellow colours.

Entomologie heute 30 (2018) 40 ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU

Fig. 14: Frequency of landings (left) on dummies made from entire petal of ray fl orets of Helian- thus annuus and subsequent proboscis reactions (right). Stars indicate signifi cant results as follows: ** ≙ p<0.01; * ≙ p<0.05 due to a Chi-square test (n=39). The corresponding spectral refl ectance curves are shown in Fig. 6. Abb. 14: Häufi gkeiten der Landungen (links) auf Blütenattrappen, die aus ganzen Zungenblüten von Helianthus annuus gemacht waren und anschließenden Rüsselreaktionen (rechts). Die Sterne zeigen folgende Ergebnisse der statistischen Analyse an: ** ≙ p<0,01; * ≙ p<0,05 nach dem Chi- Quadrat-Test (n = 39). Die zugehörigen spektralen Refl exionskurven sind in Abb. 6 dargestellt.

Fig. 15: Dual choice tests of trained Eristalis tenax with artifi cial fl owers displaying different bright- ness. Each left column shows the response to the training colour; each right column shows that to the test colour presented together with the training colour as a dual choice (n=240). * denotes a signifi cant difference at p<0.05, ** at p<0.01, and ns denotes no signifi cant differences due to a one-sided Chi-square test. The corresponding spectral refl ectance curves are shown in Figure 7, the corresponding colour loci in Figure 8. Fig. 15: Zweifachwahlversuche dressierter Eristalis tenax mit künstlichen Blütenattrappen unter- schiedlicher Helligkeit. Jede like Säule zeigt die Reaktion auf die Dressurfarbe; jede rechte Säule zeigt die Reaktion auf die Testfarbe, die zusammen mit der Dressurfarbe als Zweifachwahl präsentiert wurden (n=240). * zeigt signifi kanten Unterschied bei p<0,005, ** bei p<0,01 und ns zeigt nicht signifi kante Unterschiede nach einem zweiseitigen Chi-Quadrat-Test. Die zugehörigen spektralen Refl exionskurven sind in Abbildung 7, die zugehörigen Farbloci in Abbildung 8 dargestellt. Colour preferences and colour learning of the hoverfl y Eristalis tenax 41

It remains unclear why the fl ies landed was visible in most cases. The UV-refl ection mostly on UV-absorbing fl owers among the seems to play a more prominent role, when non-yellow artifi cial fl owers despite their the fl ies are exposed to training. After train- preference for bright over dark colours. ing to UV-refl ecting ß-carotene artifi cial The syrphid fl y balteatus exhibits fl owers the fl ies chose these artifi cial fl owers an olfactory orientation with regards to signifi cantly more often than UV-absorbing non-yellow flowers (PRIMANTE & DÖT- ones, whereas the training to UV-absorbing TERL 2010). For E. tenax it thus cannot be ß-carotene artifi cial fl owers did not result excluded, that they use fl ower scents for in any preference. This is the fi rst time that landing approach on real non-yellow fl ow- a fine-tuned response to yellow colours ers in the wild. depending on UV-refl ection properties is The spontaneous proboscis refl ex towards reported for landing in Eristalis tenax. yellow-UV-absorbing colours, however, can- Many fl owers exhibit a bull’s eye pattern not be altered by conditioning (LUNAU 1987, due to the UV-absorbing centre and the 1988; LUNAU et al. 2018). The results from a UV-refl ecting periphery of the fl ower petals previous study using mixed monochromatic (KOSKI & ASHMAN 2014). The experiments light stimuli (LUNAU & WACHT 1997b) are with the ray fl orets of Helianthus annuus largely confi rmed by this study in which demonstrated that the fl ies landed on artifi - printed colour stimuli and natural fl ower pet- cial fl owers regardless of the real or inverse als were offered. Due to these fi ndings, the bull’s eye pattern, but the landing and the fl ies prefer UV-absorbing over UV-refl ecting fi rst proboscis extension was targeted pref- yellow colour stimuli. It remains open if the erably towards the UV-absorbing part of the fl ies’ preference for darker over brighter yellow fl owers. The experiments with the H. stimuli is triggered by the intensity or the annuus ray fl orets indicate that the proboscis spectral purity of the stimuli, since it is not refl ex in the fl ies is exclusively triggered by known if the fl ies possess a perceptual di- the UV-absorbing fl ower parts irrespective mension for colour saturation. Studies with of its spatial position. The proboscis refl ex mixtures of monochromatic lights showed experiments with yellow spots differing that the fl ies respond to yellow monochro- in brightness and UV-reflection proper- matic light only if the intensity is relatively ties show that also the colour brightness high, but stop responding to these stimuli seems to have an impact on attractiveness if only small amounts of ultraviolet or blue of yellow spots. The dark yellow colours light is admixed (LUNAU & WACHT 1997b). triggered the extension of the proboscis By contrast, the fl ies are able to learn to land signifi cantly more often than bright yellow on distinct fl owers which has been demon- colours, whereas training experiments with strated by KUGLER (1951). However, our green colours indicate that bright colours results suggest that the learning of landing are more attractive for landing than dark behaviour is limited and not corresponding ones. The results of all experiments are in to colour categories, since the fl ies exhib- line with the assumption that E. tenax is ited a preference for bright colours in the adapted to exploit typical yellow fl owers with reciprocal training experiments irrespective easily accessible nectar and pollen displaying of the position of colour loci. a UV-pattern. Previous studies suggested Given the choice between UV-absorbing that further parameters like colour contrast and UV-refl ecting yellow artifi cial fl owers and spot size infl uence the triggering of the for landing the fl ies did not show any prefer- proboscis refl ex (RIEDEL & LUNAU 2015). ence except for a small, yet not signifi cant Besides chemical pollen detection (WACHT preference for UV-refl ecting yellow, which et a1. 1996) the E. tenax has the ability to

Entomologie heute 30 (2018) 42 ALEXANDER NEIMANN, LINA AN & KLAUS LUNAU recognise the yellow and UV-absorbing GILBERT, F.S. (1986): Hoverfl ies. Press Syndicate colour of pollen or anthers by visual cues of the University of Cambridge; New York. (LUNAU 1987; DINKEL & LUNAU 2001). The GOLDING, Y.G., & EDMUNDS, M. (2000): Behav- ability of fl ower-visitors to orientate by ioural of honeybees (Apis mellifera) by dronefl ies (Diptera: Syrphidae: Eristalis spp.). means of odour cues is well known (RAGUSO Proceedings of the Royal Society of London, 2004; YOSHIDA et al. 2015) and has also been B Biological Sciences 267: 903-909. established for hoverfl ies (NORDSTRÖM et GRAY, M., STANSBERRY, M.J., LYNN, J.S., WILLIAMS, al. 2017). C.F., WHITE, T.E., & WHITNEY, K.D. (2018): Consistent shifts in pollinator-relevant fl oral Acknowledgements coloration along Rocky Mountain elevation gradients. Journal of Ecology 2018: 1-15. The authors thank OLIVER KROHN for HARDIE, R.C. (1986): The photoreceptor array of the dipteran retina. Trends in Neuroscience technical assistance, ANDREAS FISCHBACH 9: 419-423. from the Botanical Garden of the Heinrich- HARDIE, R.C., & KIRSCHFELD, K. (1983): Ultra- Heine-University for providing opportuni- violet sensitivity of fl y photoreceptors R7 ties for outdoor experiment and KARL-PETER and R8: evidence for a sensitising function. BERGMEISTER for the permission to collect Biophysics of Structure and Mechanism 9: larvae, pupae and imagines of Eristalis tenax 171-180. on his farm in Düsseldorf Himmelgeist. HASLETT, J.R. (1989): Interpreting patterns of resource utilization: randomness and selec- References tivity in pollen feeding by adult hoverfl ies. Oecologia, 78: 433-442. ARNOLD, S.E.J., SAVOLAINEN, V., & CHITTKA, L. HOPKINS, R., & RAUSHER, M.D. (2012): Pollinator- (2009): Flower colours along an alpine altitude mediated selection on flower color allele gradient, seen through the eyes of fl y and drives reinforcement. Science 335: 1090-1092. pollinators. -Plant Interactions ILSE, D. (1949): Colour discrimination in the 3: 27-43. dronefl y Eristalis tenax. Nature 4137: 255-256. BASTIAN, O. (1986): Schwebfl iegen. A. Ziemsen; JARLAN, A., OLIVEIRA, D.D., & GINGRAS, J. (1997): Wittenberg. by Eristalis tenax (Diptera: Syr- BERGAMO, P.J., TELLES, F.J., ARNOLD, S.E.J., & phidae) and seed set of greenhouse sweet GARCIA DE BRITO, V.L. (2018): Flower colour pepper. Journal of Economic Entomology within communities shifts from overdispersed 90: 1646-1649. to clustered along an alpine altitudinal gradi- KELBER, A. (2001): Receptor based models for ent. Oecologia. DOI: 10.1007/s00442-018- spontaneous color choices in fl ies and but- 4204-5 terflies. Entomologia Experimentalis and CHAPMAN, D. (1996): Water Quality Assessments Applicata 99: 231-244. – A Guide to Use of Biota, Sediments and KELBER, A., & OSORIO, D. (2010): From spec- Water in Environmental Monitoring. 2nd tral information to colour vision: edition. University Press; Cambridge. experiments and concepts. Proceedings of CRONIN, T., JOHNSEN, S., MARSHALL, N., & WAR- the Royal Society B Biological Sciences 277: RANT, E. (2014): Visual Ecology. Princeton 1617-1625. University Press; Princeton. KELBER, A., VOROBYEV, M., & OSORIO, D. (2003): DE BUCK, N. (1990): Bloembezoek en bestui- Animal colour vision – behavioural tests and vingsecologie van zweefvliegen (Diptera, Syr- physiological concepts. Biological Reviews phidae) in het bijzonder voor België. Studie- 78: 81-118. documenten van het K.B.I.N. KOLKWITZ, R., & MARSSON, M. (1909): Ökologie DINKEL, T., & LUNAU, K. (2001): How drone der tierischen Saprobien. Beiträge zur Lehre fl ies (Eristalis tenax L., Syrphidae, Diptera) use von der biologischen Gewässerbeurteilung. fl oral guides to locate food sources. Journal Internationale Revue der gesamten Hydrobio- of Physiology 47: 1111-1118. logie und Hydrographie 2: 126-152. Colour preferences and colour learning of the hoverfl y Eristalis tenax 43

KORMAN, K. (1988): Schwebfl iegen Mitteleuropas, Allgemeine und Angewandte Entomologie ecomed Verlagsgesellschaft mbH, 1. Aufl ., 11: 481-484. Landsberg/München. LUNAU, K., AN, L., DONDA, M., HOHMANN, M., KOSKI, M.H., & ASHMAN, T.-L. (2014): Dissecting SERMON, L., & STEGMANNS, V. (2018): Limita- pollinator responses to a ubiquitous ultraviolet tions of learning in the proboscis refl ex of fl oral pattern in the wild. Functional Ecology the fl ower visiting syrphid fl y Eristalis tenax. 28: 868-877. PLoS ONE 13(3): e0194167. KUGLER, H. (1951): Der Blütenbesuch der MAST, S.O. (1923): Photic orientation in insects Schlammfl iege (Eristalomyia tenax). Zeitschrift with special reference to the drone-fl y, Eristalis für vergleichende Physiologie 32: 328-347. tenax and the robber-fl y, Erax rufi barbis. Jour- LUNAU, K. (1987): Zur Bedeutung optischer nal of Experimental Zoology 38: 109-205. Signale beim Blütenversuch von Schweb- NORDSTRÖM, K., DAHLBOM, J., PRAGADHEESH, V.S., fl iegen – Experimente mit Eristalis pertinax GHOSH, S., OLSSON, A., DYAKOVA, O., SURESH, Scopoli (Diptera, Syrphidae). Mitteilungen der S.K., & OLSSON, S.B. (2017): In situ modeling Deutschen Gesellschaft für Allgemeine und of multimodal fl oral cues attracting wild pol- Angewandte Entomologie 55: 31-35. linators across environments. Proceedings of LUNAU, K. (1988): Angeborenes und erlerntes the National Academy of Sciences U.S.A. 114: Verhalten beim Blütenbesuch von Schwebfl ie- 13218-13223. gen – Attrappenversuche mit Eristalis pertinax PAPIOREK, S., JUNKER, R.R., ALVES-DOS-SANTOS, (Scopoli) (Diptera, Syrphidae). Zoologische I., MELO, G.A.R., AMARAL-NETO, L.P., SAZIMA, Jahrbücher, Abteilung für Zoologie und M. WOLOWSKI, M., FREITAS, L., & LUNAU, Physiologie der Tiere 92: 487-499. K. (2016): Bees, birds and yellow fl owers: LUNAU, K. (1993): Angeborene und erlernte pollinator-dependent of Blütenerkennung bei Insekten. Biologie in UV patterns. Plant Biology 18: 46-55. unserer Zeit 23: 48-54. PRIMANTE, C., & DÖTTERL, S. (2010): A syrphid LUNAU, K. (2007): Stamens and mimic stamens fl y uses olfactory cues to fi nd a non-yellow as components of fl oral colour patterns. flower. Journal of Chemical Ecology 36: Botanische Jahrbücher für Systematik, 1207-1210. Pfl anzengeschichte und Pfl anzengeographie RAGUSO, R.A. (2004): Flowers as sensory bill- 127: 13-41. boards: progress towards an integrated un- LUNAU, K. (2011): Warnen, Tarnen, Täuschen. derstanding of fl oral advertisement. Current Mimikry und Nachahmung bei Pfl anze, Tier Opinion in Plant Biology 7: 434-440. und Mensch. Wissenschaftliche Buchgesell- RIEDEL, L., & LUNAU, K. (2015): Limitations of the schaft, Darmstadt. innate proboscis refl ex in Eristalis tenax L. (Dip- LUNAU, K. (2014): Visual ecology of fl ies with tera: Syrphidae) by the spatial resolution of the particular reference to colour vision and compound eye. Entomologie heute 27: 45-54. colour preferences. Journal of Comparative ROHDE, K., PAPIOREK, S., & LUNAU, K. (2013): Physiology A 200: 497-512. Bumblebees (Bombus terrestris) and honeybees LUNAU, K., & WACHT, S. (1994): Optical releas- (Apis mellifera) prefer similar colours of ers of the innate proboscis extension in the higher spectral purity over trained colours. hoverfl y Eristalis tenax L. (Syrphidae, Diptera). Journal of Comparative Physiology A 199: Journal of Comparative Physiology A 174: 197-210. 575-579. SRINIVASAN, M.V., & GUY, R.G. (1990): Spectral LUNAU, K., & MAIER, E.J. (1995): Innate colour properties of movement perception in the preferences of fl ower visitors. Journal of dronefl y Eristalis. Journal of Comparative Comparative Physiology A 177: 1-19. Physiology A 166: 287-295. LUNAU, K., & WACHT, S. (1997a): Signalfunk- Ssymank, A., & Gilbert, F. (1993): Anemophi- tion von Pollen. Biologie in unserer Zeit 27: lous pollen in the diet of syrphid fl ies with 169-181. special reference to the feeding strategy LUNAU, K., & WACHT, S. (1997b): Innate fl ower occurring in Xylotini (Diptera, Syrphidae). recognition in the hoverfl y Eristalis tenax L. Deutsche Entomologische Zeitschrift 60: Mitteilungen der Deutschen Gesellschaft für 245-258.

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STERNKE-HOFFMANN, R., & LUNAU, K. (2015): Flowers II: Floral Attractants and Rewards. Vergleichende Untersuchungen des Rüs- Journal of Pollination Ecology 12: 63-94. selrefl exes bei blütenbesuchenden Fliegen. YOSHIDA, M., ITOH, Y., OMURA, H., ARIKAWA, K., Entomologie heute 27: 55-71. & KINOSHITA, M. (2015): Plant scents modify VON FRISCH, K. (1915): Der Farbensinn und innate colour preference in foraging swallow- Formensinn der Biene. Zoologische Jahrbü- tail butterfl ies. Biology Letters 11: 20150390. cher Abteilung für allgemeine Zoologie und Physiologie: 35: 1-182. BSc Alexander Neimann TROJE, N. (1993): Spectral categories in the learn- Prof. Dr. Klaus Lunau ing behaviour of blowfl ies. Zeitschrift für Institute of Sensory Ecology Naturforschung 48c: 96-104. Biology Department TSUKAHARA, Y., & HORRIDGE, G.A. (1977): Inter- action between two retinula cell types in the Heinrich-Heine-University Düsseldorf anterior eye of the dronefl y Eristalis. Journal Universitätsstr. 1 of Comparative Physiology A 115: 287-298. D-40225 Düsseldorf (Germany) VAN DER KOOI, C.J., DYER, A.G., KEVAN, P.G., & E-Mail: [email protected] LUNAU, K. (2018) Functional signifi cance of E-Mail: [email protected] the optical properties of fl owers for visual signalling. Annals of Botany mcy119. Doi. MSc Lina An org/10.1093/aob/mcy119 Department of Entomology WACHT, S., LUNAU, K., & HANSEN, K. (1996): College of Plant Protection Optical and chemical stimuli control pollen feeding in the hoverfl y Eristalis tenax. Entomo- Hebei Agricultural University (West Campus) logia Experimentalis et Applicata 80: 50-53. No. 2596 Lekai South Street WOODCOCK, T.S., LARSON, B.M.H., KEVAN, P.G., Baoding (China) INOUYE, D.W., & LUNAU, K. (2014): Flies and E-Mail: [email protected]