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How small can small be: The compound eye of the parasitoid wasp Trichogramma evanescens (Westwood, 1833) (Hymenoptera, Hexapoda), an insect of 0.3- to 0.4-mm total body size

Published online by Cambridge University Press:  13 October 2010

STEFAN FISCHER*
Affiliation:
Faculty of Engineering and Science, Jacobs University Bremen, Bremen, Germany
CARSTEN H.G. MÜLLER
Affiliation:
Department Cytology and Evolutionary Biology, Zoological Institute and Museum, Ernst-Moritz-Arndt-University Greifswald, Greifswald, Germany
V. BENNO MEYER-ROCHOW
Affiliation:
Faculty of Engineering and Science, Jacobs University Bremen, Bremen, Germany Department of Biology, Oulu University, Oulu, Finland
*
*Address correspondence and reprint requests to: Stefan Fischer, Faculty of Engineering and Science, Jacobs University Bremen, P.O. Box 750561, D-28725 Bremen, Germany. E-mail: s.fischer@jacobs-university.de

Abstract

With a body length of only 0.3–0.4 mm, the parasitoid wasp Trichogramma evanescens (Westwood) is one of the smallest insects known. Yet, despite its diminutive size, it possesses compound eyes that are of oval shapes, measuring across their long axes in dorsoventral direction 63.39 and 71.11 μm in males and females, respectively. The corresponding facet diameters are 5.90 μm for males and 6.39 μm for females. Owing to the small radii of curvature of the eyes in males (34.59 μm) and females (42.82 μm), individual ommatidia are short with respective lengths of 24.29 and 34.97 μm. The eyes are of the apposition kind, and each ommatidium possesses four cone cells of the eucone type and a centrally fused rhabdom, which throughout its length is formed by no more than eight retinula cells. A ninth cell occupies the place of the eighth retinula cell in the distal third of the rhabdom. The cone is shielded by two primary and six secondary pigment cells, all with no apparent extensions to the basement membrane, unlike the case in larger hymenopterans. The regular and dense packing of the rhabdoms reflects an effective use of space. Calculations on the optics of the eyes of Trichogramma suggest that the eyes need not be diffraction limited, provided they use mostly shorter wavelengths, that is, UV light. Publications on the visual behavior of these wasps confirm Trichogramma’s sensitivity to UV radiation. On the basis of our findings, some general functional conclusions for very small compound eyes are formulated.

Type
Evolution and eye design
Copyright
Copyright © Cambridge University Press 2011

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References

Barlow, H.B. (1952). The size of ommatidia in apposition eyes. The Journal of Experimental Biology 29, 667674.CrossRefGoogle Scholar
Brower, J.H. & Cline, L.D. (1984). Response of Trichogramma pretiosum and T. evanescens to whitelight, blacklight or no-light suction traps. Florida Entomologist 76, 262268.CrossRefGoogle Scholar
Brunnert, A. & Wehner, R. (1971). Fine structure of light- and dark-adapted eyes of desert ants, Cataglyphis bicolor (Formicidae, Hymenoptera). Journal of Morphology 140, 1530.CrossRefGoogle Scholar
Duelli, P. & Wehner, R. (1973). The spectral sensitivity of polarized light orientation in Cataglyphis bicolor. Journal of Comparative Physiology 86, 3753.CrossRefGoogle Scholar
Exner, S. (1891). Die Physiologie der facettirten Augen von Krebsen und Insecten. Leipzig, Germany: Deuticke.CrossRefGoogle Scholar
Eguchi, E. 1999. III. Photoreceptors and photo-environments. III-1 membrane turnover of rhabdom. In Atlas of Arthropod Sensory Receptors. Dynamic Morphology in Relation to Function, ed.Eguchi, E. & Tominaga, Y., pp. 8796. Tokyo, Japan: Springer Verlag.Google Scholar
Gibson, G.A.P. & Huber, J.T. (2000). Review of the family Rotoitidae (Hymenoptera: Chalcidoidea), with description of a new genus and species from Chile. Journal of Natural History 34, 22932314.CrossRefGoogle Scholar
Greiner, B., Ribi, W.A. & Warrant, E.J. (2004). Retinal and optical adaptations for nocturnal vision in the halicit bee Megalopta genalis. Cell and Tissue Research 316, 377390.CrossRefGoogle ScholarPubMed
Grundler, O.J. (1974). EM-Untersuchungen am Auge der Honigbiene (Apis mellifica). 1. Untersuchungen zur Morphologie und Anordnung der neun Retinulazellen in Ommatidien verschiedener Augenbereiche. Cytobiologie 9, 203220.Google Scholar
van Hateren, J.H. (1989). Photoreceptor optics, theory and practice. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 7589. Berlin, Germany: Springer Verlag.Google Scholar
Horvath, G. & Varju, D. (2004). Polarized Light in Animal Vision—Polarization Patterns in Nature. Berlin, Germany: Springer Verlag.CrossRefGoogle Scholar
Jander, U. & Jander, R. (2000). Allometry and resolution of bee eyes (Apoidea). Arthropod Structure & Development 30, 179193.CrossRefGoogle Scholar
Jenkins, F.A. & White, H.E. (1976). Fundamentals of Optics (4th ed.). Auckland, New Zealand: McGraw-Hill.Google Scholar
Karnovsky, M.J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. The Journal of Cell Biology 27, 137138.Google Scholar
Kelber, A., Warrant, E.J., Pfaff, M., Wallen, R., Theobald, J.C., Wcislo, W.T. & Raguso, R.A. (2006). Light intensity limits foraging activity in nocturnal and crepuscular bees. Behavioral Ecology 17, 6372.CrossRefGoogle Scholar
Keskinen, E. & Meyer-Rochow, V.B. (2004) Postembryonic photoreceptor development and dark/light adaptation in the spittle bug Philaenus spumarius (L.) (Homoptera, Cercopidae). Arthropod Structure & Development 33, 405417.CrossRefGoogle ScholarPubMed
Kirschfeld, K. & Snyder, A.W. (1976). Measurement of a photoreceptor’s characteristic waveguide parameter. Vision Research 16, 775778.CrossRefGoogle ScholarPubMed
Land, M.F. (1981). Optics and vision in invertebrates. In Handbook of Sensory Physiology, Vol. VII/6c, ed. Autrum, H., pp. 471592. Berlin, Germany: Springer Verlag.Google Scholar
Land, M.F. (1989). Variations in the structure and design of compound eyes. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 90111. Berlin, Germany: Springer Verlag.CrossRefGoogle Scholar
Land, M.F. & Nilsson, D.-E. (2002). Animal Eyes. Oxford Animal Biology Series. New York: Oxford University Press Inc.Google Scholar
Lewis, W.J., Sparks, A.N. & Redlinger, L.M. (1971). Moth odor: A method of host-finding by Trichogramma evanescens. Journal of Economic Entomology 64, 557558.CrossRefGoogle Scholar
Manning, A. (1956). The effect of honey-guides. Behaviour 9, 114139.CrossRefGoogle Scholar
Martel, V. & Boivin, G. (2004). Premating dispersion in the egg parasitoid Trichogramma (Hymenoptera: Trichogrammatidae). Environmental Entomology 33, 855859.CrossRefGoogle Scholar
Mazokhin-Porshnyakov, G.A. (1969). Insect Vision. New York: Plenum.Google Scholar
Menzel, R. (1971). Über den Farbensinn von Paravespula germanica (Hymenoptera), ERG und selektive Adaptation. Zeitschrift für vergleichende Physiologie 75, 86104.CrossRefGoogle Scholar
Menzel, R. (1972). The fine structure of the compound eye of Formica polyctena—Functional morphology of a hymenopteran eye. In Information Processing in Visual Systems of Arthropods, ed.Wehner, R., pp. 3747. Berlin, Germany: Springer-Verlag.Google Scholar
Menzel, R. & Blakers, M. (1976). Colour receptors in the bee—Morphological and spectral sensitivity. Journal of Comparative Physiology 108, 1133.CrossRefGoogle Scholar
Menzel, R. & Lange, G. (1971). Änderung der Feinstruktur im Komplexauge von Formica polyctena bei Helladaptation. Zeitschrift für Naturforschung 26b, 357359.CrossRefGoogle Scholar
Meyer-Rochow, V.B. (1975). The dioptric system in beetle compound eyes. In The Compound Eye and Vision in Insects, ed. Horridge, G.A., pp. 299314. Oxford, UK: Clarendon Press.Google Scholar
Meyer-Rochow, V.B. (1978). Retina and dioptric apparatus of the dung beetle Euoniticellus africanus. Journal of Insect Physiology 24, 165179.CrossRefGoogle Scholar
Meyer-Rochow, V.B. (1981). Electrophysiology and histology of the eye of the bumblebee Bombus hortorum (L.) (Hymenoptera: Apidae). Journal of the Royal Society of New Zealand 11, 123153.CrossRefGoogle Scholar
Meyer-Rochow, V.B. (1991). Differences in ultraviolet wing patterns in the New Zealand lycaenid butterflies Lycaena salustris, L. rauparaha, and L. faradayi as a likely isolating mechanism. Journal of the Royal Society of New Zealand 21, 169177.CrossRefGoogle Scholar
Meyer-Rochow, V.B. & Keskinen, E. (2003). Post-embryonic photoreceptor development and dark/light adaptation in the stick insect Carausius morosus (Phasmida, Phasmatidae). Applied Entomology and Zoology 38, 281291.CrossRefGoogle Scholar
Meyer-Rochow, V.B. & Nilsson, H.L. (1999). Compound eyes in polar regions, caves, and the deep sea. In Atlas of Arthropod Sensory Receptors, ed. Eguchi, E. & Tominaga, Y., pp. 125142. Tokyo, Japan: Springer Verlag.Google Scholar
Meyer-Rochow, V.B. & Reid, W.A. (1996). An eye for the extreme: Photoreceptor fine-structure in the Antarctic midge Belgica antarctica (Diptera: Chironomidae). Applied Entomology and Zoology 31, 629632.CrossRefGoogle Scholar
Möller, R. (2002). Insects could exploit UV-green contrast for landmark navigation. The Journal of Experimental Biology 214, 619631.Google ScholarPubMed
Müller, C.H.G., Rosenberg, J., Richter, S. & Meyer-Rochow, V.B. (2003). The compound eye of Scutigera coleoptrata (Linnaeus, 1758) (Chilopoda: Notostigmophora): An ultrastructural reinvestigation that adds support to the Mandibulata concept. Zoomorphology 122, 191209.CrossRefGoogle Scholar
Noldus, L.P.J.J. & van Lenteren, J.C. (1985). Kairomones for the egg parasite Trichogramma evanescens Westwood. I. Effect of volatile substances released by two of its hosts, Pieris brassicae L. and Mamestra brassicae L. Journal of Chemical Ecology 11, 781791.CrossRefGoogle Scholar
Paulus, H.F. (1979). Eye structure and the monophyly of the Arthropoda. In Arthropod Phylogeny, ed. Gupta, A.P., pp. 299383. New York: van Nostrand.Google Scholar
Peitsch, D., Fietz, A., Hertel, H., de Souza, J., Fix Ventura, D. & Menzel, R. (1992). The spectral input systems of hymenopteran insects and their receptor-based colour vision. Journal of Comparative Physiology A 170, 2340.CrossRefGoogle ScholarPubMed
Perrelet, A. (1970). The fine structure of the retina of the honey bee drone. An electron microscopial study. Zeitschrift für Zellforschung 108, 530562.CrossRefGoogle Scholar
Quednau, W. (1956). Der vollständige Parasitismus bei Trichogramma als biologisches Phänomen (Hymenoptera Chalcidae). Zeitschrift für Parasitenkunde 17, 360364.CrossRefGoogle Scholar
Quednau, W. (1958). Über einige Orientierungsweisen des Eiparasiten Trichogramma (Hym. Chalcididae) auf Grund von Licht- und Schwerereizen. Anzeiger für Schädlingskunde 31, 8385.Google Scholar
Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron opaque stain in electron microscopy. The Journal of Cell Biology 17, 208.CrossRefGoogle ScholarPubMed
Romeis, J., Brabendreier, D., Wäckers, F.l. & Shanower, T.G. (2005). Habitat and plant specificity of Trichogramma egg parasitoids—Underlying mechanisms and implications. Basic and Applied Ecology 6, 215236.CrossRefGoogle Scholar
Romeis, J., Shanower, T.G. & Zebitz, C.P.W. (1998). Response of Trichogramma egg parasitoids to colored sticky traps. BioControl 43, 1727.CrossRefGoogle Scholar
Rutowski, R.L., Gislen, L. & Warrant, E.J. (2009). Visual acuity and sensitivity increase allometrically with body size in butterflies. Arthropod Structure & Development 38, 91100.CrossRefGoogle ScholarPubMed
Salt, G. (1937). The sense used by Trichogramma to distinguish between parasitized and unparasitized hosts. Proceedings of the Royal Society of London. Series B, Biological Sciences 122, 5775.Google Scholar
Schulze, H. (1926). Über die Fruchtbarkeit der Schlupfwespe Trichogramma evanescens Westwood. Zoomorphology 6, 553585.Google Scholar
Skrzipek, K.H. & Skrzipek, H. (1971). Die Morphologie der Bienenretina (Apis mellifica L.) in elektronenmikroskopischer und lichtmikroskopischer Sicht. Zeitschrift für Zellforschung 119, 552576.CrossRefGoogle Scholar
Skrzipek, K.H. & Skrzipek, H. (1974). The ninth retinula cell in the ommatidium of the worker honey bee (Apis mellifica L.). Zeitschrift für Zellforschung 147, 589593.CrossRefGoogle ScholarPubMed
Snyder, A.W. (1977). Acuity of compound eyes: Physical limitations and design. Journal of Comparative Physiology A, 116, 161182.CrossRefGoogle Scholar
Snyder, A.W. (1979). Physics of vision in compound eyes. In Handbook of Sensory Physiology, Vol. VII/6A, ed. Autrum, H., pp. 225313. Berlin, Germany: Springer.Google Scholar
Stavenga, D.G. (2003). Angular and spectral sensitivity of fly photoreceptors. II. Dependence on facet lens F-number and rhabdomere type in Drosophila. Journal of Comparative Physiology A 189, 189202.CrossRefGoogle ScholarPubMed
Stavenga, D.G., Kruizinga, R. & Leertouwer, H.L. (1990). Dioptrics of the facet lenses of male blowflies Calliphora and Chrysomyia. Journal of Comparative Physiology A 166, 365371.CrossRefGoogle ScholarPubMed
Varela, F.G. & Wiitanen, W. (1970). The optics of the compound eye of the honeybee (Apis mellifera). Journal of General Physiology 55, 336358.CrossRefGoogle ScholarPubMed
Wachmann, E., Richter, S. & Schricker, B. (1973). Feinstrukturen im Komplexauge der Blattschneiderbiene Megachile rotundata (F.) (Hymenoptera, Apidae). Zoomorphology 76, 109128.Google Scholar
Warrant, E.J. & McIntyre, P.D. (1993). Arthropod eye design and the physical limits to spatial resolving power. Progress in Neurobiology 40, 413461.CrossRefGoogle ScholarPubMed
Warrant, E.J. & Nilsson, D.E. (1998). Absorption of white light in photoreceptors. Vision Research 38, 195207.CrossRefGoogle ScholarPubMed
Wehner, R. (1989). The hymenopteran skylight compass: Matched filtering and parallel coding. The Journal of Experimental Biology 146, 6385.CrossRefGoogle Scholar