REVIEW Eur. J. Entomol. 99: 1-4, 2002 ISSN 1210-5759

Ultraviolet vision in European owlflies (Neuroptera: Ascalaphidae): a critical review

Ka r l KRAL

Institut fur Zoologie, Karl-Franzens-Universitat Graz, A-8010 Graz, Austria; e-mail: [email protected]

Key words.Owlfly, Ascalaphus, Neuroptera, insect vision, ultraviolet sensitivity, visual acuity, visual behaviour, visual pigment

Abstract. This review critically examines the ecological costs and benefits of ultraviolet vision in European owlflies. On the one hand it permits the accurate pursuit of flying prey, but on the other, it limits hunting to sunny periods. First the physics of detecting short wave radiation are presented. Then the advantages and disadvantages of the optical specializations necessary for UV vision are discussed. Finally the question of why several visual pigments are involved in UV vision is addressed.

UV vision in predatory European owlflies of R7 means that the former receives only the longer The European owlflies, like Ascalaphus macaronius, wavelengths, since the short wavelengths are absorbed by A. libelluloides, A. longicornis and Libelloides coccajus the latter. However, intracellular electrophysiological are rapidly-flying neuropteran insects, which hunt in open recordings or microspectrophotometry on these tiny pho­ country for flying insects. These owlflies are only adapted toreceptors have not been done so their spectral sensi­ for daytime activity. They have large double eyes, which tivity is unknown (P. Stušek, personal communication). structurally correspond to optical refracting superposition Advantages of UV vision eyes (Ast, 1920; Gogala & Michieli, 1965; Schneider et What are the advantages of using UV light for locating al., 1978; forreview, seeNilsson, 1989). and capturing prey seen against the sky? The utilization of In the late 1960’s Matija Gogala, of the University of UV light may limit the diffraction of the light providing Ljubljana, combined the results of behavioural observa­ the stimulus. This is critical, since it is the diffraction of tions in the field with electroretinogram recordings on the incident light that determines the resolving power of Ascalaphus macaronius. His electrophysiological studies an eye. Here, resolving power is the ability to detect a revealed that the dorsofrontal part of the eye is sensitive small object, for instance prey, even at great distances. to UV light and he concluded that this might be important The stimulation of an ommatidium by daylight creates a in hunting prey (Gogala, 1967). His finding that the eyes diffraction pattern on the rhabdom layer, which is known of owlflies are sensitive to UV light is interesting and ini­ as the Airy disc. The Airy disc consists of a central spot of tiated a series of studies that led to a better understanding high intensity, surrounded by rings of minima and maxima of UV vision not only in insects, but also in other ani­ of sharply decreasing intensity. The shorter the wave­ mals (Gogala et al., 1970; Hamdorf et al., 1971; length of the stimulating light and the wider the lens aper­ Schwemer et al., 1971; Paulsen & Schwemer, 1972; ture (D), the smaller and sharper the Airy disc and the Hamdorf & Gogala, 1973; for review, see Hamdorf, greater the sharpness of the image. 1979). The half-width of the Airy disc, i.e. the width of the Recent studies on Ascalaphus by Gribakin et al. (1995) brightness distribution at half maximum intensity (see e.g. indicate that the large photoreceptor cells R1-R6 in the Land, 1997) can be calculated at a given ratio of A/D radi­ ventrolateral part of the eye of Ascalaphus macaronius, ans, where A denotes the wavelength of the received light are maximally sensitive in the green region of the spec­ and D represents the facet diameter. This is possible trum (Amax = 520 nm), whereas the small photoreceptor because Ascalaphus has a conventional ommatidial struc­ cells R7 and R8 are maximally sensitive in the ultraviolet ture, i.e. a 1:1 relationship between lenses and rhabdoms. region (Amax = 343 nm). The compound eyes of other neu­ In the dorsofrontal part of the eye of Ascalaphus where ropteran species (e.g. Chrysoperla carnea\ Kral & Stelzl, UV light (Amax= 330 nm) is perceived and D = 31 pm 1998; Mantispa styriaca: Mayer & Kral, 1993) are simi­ which results in a half-width of 0.6°. In contrast, in the larly sensitive. In contrast, the large photoreceptor cells ventrolateral part of the eye, A is the wavelength (520 nm) R1-R6 in the dorsofrontal part of the eye of Ascalaphus, of green light and D = 25 pm, giving a value of 1.2°. are maximally sensitive in the UV region of the spectrum Thus, the width of the Airy disc in the dorsofrontal part of (Amax ~ 330 nm) (Gribakin et al., 1995). Analogous with the eye is half that in the ventrolateral region. This means the situation in other superposition eyes, the small photo­ that the images on the rhabdom layer should be much receptor cell R8 may be sensitive in the blue-green region sharper in the dorsofrontal part of the eye. of the spectrum (Stusek et al., 2000). The proximal posi­ What is the significance of these angular values? They tion of the rhabdomere of R8 relative to the rhabdomere not only indicate image sharpness, but also give a rough

1 estimate of the resolving power of the eye. In conjunction detect small prey (i.e. 5 mm in size) at distances well over with anatomical data, the rhabdom acceptance angle Ap, 1 m. which is a measure of the resolving power, can (also in There is a further possible advantage of UV-vision for superposition eyes) be estimated by means of the formula Ascalaphus. This has already been discussed by Gogala Ap = [V(X/D)2 + (d/f)2], where d is the diameter of the (1967), based on his behavioural observations on the stimulated rhabdom and f is the focal length of the lens hunting territory of Ascalaphus viewed through UV filters system (M. Land, personal communication). In the dor- and UV-blocking filters. In the ultraviolet region of the sofrontal part of the eye, d is approximately 1-10 mm spectrum he found the sky to appear brighter and more (R1-R6) for the light-adapted state, depending on the uniform (homogeneous). Furthermore, the considerable intensity of the light. In the ventrolateral part of the eye, d dispersion of short wavelength light resulted in a quite has a value of 7-10 mm. There are consistent optically hazy view compared to long wavelength light. Ascalaphus determined data on the focal length/, however, estimates may greatly benefit from those background properties may be made based on the principles of superposition when viewing flying insects against the sky (see also optics, where the focal length / is usually about half the Mazokhin-Porshnyakov, 1959). radius of curvature of the eye (Land, 1997; M. Land, per­ How can a high resolution be achieved when the sonal communication). The estimates of the focal lengthf proportion oflight that is UV is so small? based on histological data obtained from longitudinal sec­ Is it not risky for the visual component of the prey­ tions through eyes (Schneider et al., 1978) are 635 pm and capturing system to be restricted to such a very small por­ 350 pm for the dorsofrontal and ventrolateral parts of the tion of the total energy available (Henderson & Hodgkiss, eye, respectively. For the dorsofrontal part of the eye, 1963)? In the case of the dorsofrontal part of the eye of where UV light (Xmax- 330 nm) is received, this results in Ascalaphus, this limitation is particularly extreme. This a very small range of rhabdom acceptance angles Ap, seems to be reflected in the animal’s hunting behaviour. between 0.6-1.10. In contrast, in the ventrolateral part of They only fly on sunny days with clear blue skies, but not the eye the Ap for green light (Xmax = 520 nm) ranges if the sun is obscured, and certainly not if the sky is over­ between 1.6-2.00. However, these angular values need to cast. As soon as a cloud covers the sun, they land and be verified using optical and electrophysiological meas­ wait until the sun is unobscured again (see also Gogala, urements. 1967). What are the implications of the small rhabdom accep­ In the UV-sensitive dorsofrontal part of the eye of tance angles, Ap, of 0.6 -1.10 for the resolving power of Ascalaphus, there is also an iris mechanism, which serves the dorsofrontal part of the eye and prey-capture by Asca­ to maintain the UV-absorbing rhodopsin at a high con­ laphus? This is revealed by observing their hunting behav­ centration level (Schneider et al, 1978; see also Stusek & iour. If the hunting flights of Ascalaphus are observed in Hamdorf, 1999; Stusek et al., 2000). Kirschfeld and the field on a sunny summer’s day, ideally in the boundary Wenk (1976) showed that male simuliid flies may employ between meadow and blue sky looking away from the sun, a similar “iris mechanism”, though in a different behav­ it is immediately noticeable that the flights are very similar ioural context, to maintain a high rhodopsin concentration to those of a dragonfly. Once the dorsofrontal part of the in the UV photoreceptors. In Ascalaphus, this specializa­ eye detects a potential prey, such as a fly,Ascalaphus tion was identified by Schneider et al. (1978) by means of darts toward the prey at very high speed and seizes it from microspectrophotometry using sections of fresh and deep- below. The distances at which Ascalaphus seems to detect frozen eyes. The pupil is composed of primary pigment its prey range up to 1 m and may be greater in some cells containing yellow granules, which function as an iris instances. In his field studies, Stusek observed that Asca­ with respect to UV and violet light, while allowing light laphus can detect flying insects at distances of even a few of longer wavelengths (X - 500-700 nm) to pass. The meters (personal communication). In cases where the prey maximum absorption of these pigment granules lies size ranges between 5-10 mm and is 1 m away the visual approximately at X - 410 nm, which is midway between angle is no greater than about 0.3-0.60. Rhabdom accep­ the values for UV-rhodopsin (Xmax - 330 nm) and the tance angles Ap of 0.6-1.10 in the dorsofrontal part of the related metarhodopsin (Xmax - 475 nm). Thus, the aperture eye would indicate that the pursuit of prey may be trig­ is markedly greater for light oflonger wavelengths, which gered by a brief half-maximum to maximum decrease in is exclusively absorbed by metarhodopsin, than it is for intensity of the UV portion (Xmax - 330 nm) of daylight in UV light. This means that, in accordance with superposi­ rhabdoms (R1-R6). Due to the lack of experimental data, tion optics, light from the blue region of the spectrum is it is currently impossible to estimate how the sensory exci­ captured by several dioptric apparatuses and superposed tation level may be influenced by the blue background on the rhabdoms. For UV light the situation is different, illumination, which depends on the size of the superposi­ as only the incident light rays that are parallel to the tion aperture. optical axis will be received by the receptors. This greatly In summary, it can be concluded that, in conjunction increases the intensity of the rhodopsin-regenerating blue with an enlarged facet diameter D and elongated omma- light in the rhabdoms, which then causes all metarho­ tidia (i.e. a greater radius of curvature of the eye), the dopsin molecules to immediately regenerate rhodopsin. reduction in the rhabdom acceptance angle Ap of UV light Consequently, under natural lighting conditions with to values of between 0.6-1.10 enables Ascalaphus to respect to the blue range of the spectrum, the photo­

2 chemical equilibrium between rhodopsin and metarho­ the chromophore (Gribakin et al., 1995). As a result, the dopsin is almost completely on the side of the intact rho­ resolving power of the dorsal part of the eye may be dopsin. Thus, UV-sensitivity is constantly maintained at a improved by a further few percent (see wavelength high level (see Hamdorf, 1979). This mechanism may theory, cited above; see also Kirschfeld & Vogt, 1986; compensate for the fact that UV makes up a compara­ Vogt, 1989; Seki & Vogt, 1998). tively small proportion of daylight. In addition, a special ACKNOWLEDGEMENTS. Thanks to Mary Ansell for trans­ mechanism of the photo-transductional cascade seems lating the first draft of the manuscript into English. I am grateful also to be responsible for the rapid regeneration of UV- to Drs. Peter Stusek, Michael Land, Dan-E. Nilsson and an sensitive rhodopsin (Stusek et al., 2000; Bentrop et al., anonymous reviewer for many valuable comments on the manu­ 2001). script. This work was supported by research grants from the It is possible that the small photoreceptor cell R7 may Austrian Science Foundation (Grant No. P14697-Bio to K.K.) be involved in this pupil mechanism (Stusek et al., 2000; P. Stusek, personal communication). R7 extends up to the REFERENCES tip of the crystalline cone, where it could easily absorb its Arikawa K., Mizuno S., Schölten D.G.W., Kinoshita M., Seki portion of light. Nevertheless, because of its tiny T., Kitamoto J. & Stavenga D.G. 1999: An ultraviolet diameter, R7 probably does not contribute much to vision absorbing pigment causes a narrow-band violet receptor and a or prey detection against the sky, but may serve a dif­ single-peaked green receptor in the eye of the butterfly ferent function. The function of the other small photore­ Papilio. 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