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Fine Structure of the Compound Eyes of Callitettix Versicolor (Insecta: Hemiptera)

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Fine Structure of the Compound Eyes of Callitettix Versicolor (Insecta: Hemiptera) MORPHOLOGY,HISTOLOGY, AND FINE STRUCTURE Fine Structure of the Compound Eyes of Callitettix versicolor (Insecta: Hemiptera) 1,2 1,3 LEI-PO JIA AND AI-PING LIANG Ann. Entomol. Soc. Am. 108(3): 316–324 (2015); DOI: 10.1093/aesa/sav007 ABSTRACT The external morphology and internal anatomy of the compound eyes of the adults of the rice spittlebug Callitettix versicolor (F., 1794) (Insecta: Hemiptera: Cercopidae) are described for the first time with light, scanning, and transmission electron microscopy observations. The eyes of C. versicolor are of the apposition type and each eye consists of 2,042 ommatidia. Each ommatidium is composed of a plano-convex corneal lens, a eucone-type crystalline cone, eight retinular cells, two pri- mary pigment cells, and an undetermined number of secondary pigment cells (probably six). The rhab- domeres of the eight retinular cells form a centrally fused rhabdom surrounded by palisades. The distal end of the rhabdom is funnel shaped around the proximal region of the crystalline cone. The microvilli of the rhabdom are arranged in orthogonal directions suggesting polarization sensitivity. With a small F-number of 1.48 and a large interommatidial angle Du of 7.7, the eye possesses high light sensitivity but low spatial resolution. With a large ommatidial acceptance angle Dq of 11.6, the eye can merely form a burred image of its surroundings, but the ratio Dq/Du of 1.5 indicates that the eye can provide a relatively good contrast. KEY WORDS Hemiptera, Callitettix versicolor, compound eye, rhabdom, microvilli Compound eyes play important roles in insect’s forag- largest xylemophagous group of insects with 1,500 ing, homing, prey detection, and other activities. The described species (Liang and Webb 2002). This group basic structural and functional units of the compound of insects is usually called spittlebugs because their lar- eyes are ommatidia. Each ommatidium generally con- vae live in the spit-like bubbles of foam they secrete, sists of a dioptric apparatus, a few primary and second- while their adults inhabit in a terrestrial setting. Pre- ary pigment cells, and retinular cells (Paulus 1979). vious work on the structure of the compound eyes of The morphological characteristics of a compound eye, the spittlebug species is limited to only one study of such as the organization of the retinular cells and the the meadow spittlebug Philaenus spumarius (L.) microvillus orientations, can provide valuable clues on (Keskinen and Meyer-Rochow 2004). the eye’s capability and limitation (Meyer-Rochow and Here, we are dealing with the compound eyes of an- Monalisa 2009). other spittlebug Callitettix versicolor (F., 1794) (Hemi- In Hemiptera, previous studies on the compound ptera: Cercopidae) which, compared with P. spumarius, eyes have focused mainly on the heteropteran species belongs to a different genus. Another difference be- (Schwind 1983, Settembrini 1984, Fischer et al. 2000, tween the two species is that P. spumarius has a world- Reisenman et al. 2002). However, the fine structure of wide distribution (Keskinen and Meyer-Rochow 2004), the eyes of the species in other hemipteran groups, i.e., but C. versicolor is only found in southern China, In- the Sternorrhyncha and the Auchenorrhyncha, is not dia, Myanmar, Thailand, Vietnam, and Malaysia (Met- well documented. To our knowledge, Drosicha steb- calf 1962). The adults of C. versicolor mainly feed on bingi (Sternorrhyncha: Coccoidea) and Philaenus spu- xylem fluid of rice and maize and are considered one marius (Auchenorrhyncha: Cercopoidea) are the only of the most notorious economic pests in these areas two species in these groups that have had their com- (Chen and Liang 2012). Field observations reveal that pound eyes studied (Ramachandran 1963, Keskinen the adults usually stay at the lower (abaxial) surfaces of and Meyer-Rochow 2004). leaves to avoid high-intensity sunlight for most of the The Cercopidae (Hemiptera: Auchenorrhyncha: Cer- day, and feed themselves at dawn (7 to 8 am) and dusk copoidea) is a superfamily of Auchenorrhyncha and the (5 to 7 pm; Lei et al. 1992). Mating activities occur around 5 pm (Lei et al. 1992) or between 4 and 6 pm (Cai and Xu 2001). 1 Key Laboratory of Zoological Systematics and Evolution, Institute Successful rearing of this insect species under labo- of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, ratory conditions (Chen and Liang 2012) makes it pos- Chaoyang District, Beijing 100101, P.R. China. sible for advanced behavioral and ecological 2 University of Chinese Academy of Sciences, Chinese Academy of Sciences, 19A Yuquanlu, Beijing 100049, P.R. China. researches. Given that visual capacity and limitation 3 Corresponding author, e-mail: [email protected]. have great influence on the insect’s mating and feeding VC The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: [email protected] May 2015 JIA AND LIANG:FINE STRUCTURE OF COMPOUND EYES OF C. versicolor 317 behavior, a thoroughly anatomical investigation on the observed with a regular optical objective (10Â, major visual organ, i.e., the compound eyes of the NA ¼ 0.3) and an oil immersion objective (100Â, adults of this species before any further studies seems NA ¼ 1.25) under a Nikon eclipse Ni-E muscope sys- necessary. tem (Nikon, Tokyo, Japan). The objectives of the present study are to provide a Statistics. All measurements were performed in detailed description of the external morphology and in- digital photographs and analyzed using the software ternal anatomy of the compound eyes in the adult of C. Image pro plus 6.0. SEM photographs were used to versicolor and give a brief discussion on the potential determine the dorso–ventral and anterior–posterior functions and limitations of the compound eyes of this lengths of the eye, total number of the ommatidia and pest species. the facet diameters. TEM photographs of cross-sec- tions of the eyes were used to determine the rhabdom diameters, the diameters of pigment granules of pri- Materials and Methods mary pigment cell and secondary pigment cell, as well as retinular cells. LM mugraphs of longitudinal sections Insect Specimens. The adult specimens of C. ver- of the ommatidia were used to determine the ommati- sicolor (10 mm in body length) used in this study dial lengths and the radii of the curvature of the facet. were the third or fourth generation of a laboratory col- The curvature radii of corneal facet lens, as show in ony. The adults of this spittlebug were reared on rice Fig. 3A, were calculated based on the coordinate data seedlings and maintained in the controlled laboratory of three homologous points on their surface (Tanaka condition at 27C, a photoperiod of 14:10 (L: D) h, and et al. 2009). 70% relative humidity (Chen and Liang 2012). Scanning Electron Microscopy (SEM). After decapitation, the heads of three adults were dehydrated Results in an alcohol series, critical point-dried with liquid car- bon dioxide (Leica EM CPD300, Leica Microsystems, External Morphological Features of the Wetzlar, Germany), and sputter-coated with gold at Eyes. The adult of C. versicolor possesses a pair of 40 mA current for 100 s (Leica EM SCD050, Leica brown hemispherical compound eyes on both sides of Microsystems, Wetzlar, Germany). The specimens were the head (Fig. 1A). Each eye measures finally observed under a FEI Quanta 450 scanning 927.3 6 75.5 mm in its dorso–ventral direction (eye electron muscope (FEI, Hillsboro, OR), operated at a height) and 746.7 6 16.5 mm in the anterior–posterior voltage of 30 kV. direction (eye width; Fig. 1A; Table 1). Each eye Transmission Electron Microscopy (TEM). The consists of 2,042 6 83 facets (Table 1). Most of the fac- specimens were decapitated and the heads were imme- ets are typical hexagonal in shape (Fig. 1C), but those diately fixed in 2.5% glutaraldehyde buffered in 0.1 M located close to the periphery region of the eye are cacodylate buffer (pH 7.4) during the day in the light- pentagonal (Fig. 1D). The center-to-center distances adapted state for at least 24 h. The specimens were between neighboring facets measure 18.7 6 3.3 mm postfixed in 1% OsO4, also buffered in 0.1 M cacody- (Table 1). Very sparse interfacetal hairs are present late buffer (pH 7.4) for 2 h at room temperature. The between facets and randomly distributed across the samples were then rinsed three times in the same buf- whole compound eye (Fig. 1B). The interfacetal hair fer and dehydrated in a graded series of ethanol. The is needle-shaped and situated between three neighbor- specimens were passed through different acetone/ ing facets (Fig. 1C). Each interfacetal hair measures Epon mixtures (3:1, 1:1, 1:3, pure Epon), embedded in 2.0–3.5 mm in length and 0.7–1.2 mm in diameter pure Epon (Serva, Heidelberg, Germany) and hard- at its base. The surface of the facets is covered with ened at a temperature of 60Cfor3d.Semithinsec- arrays of corneal nipples, which are randomly tions for light muscopy (LM; from cornea to basement arranged and no orderly nipple pattern is observed membrane) were cut on an ultramutome (Leica EM (Fig. 1C and D). UC6þFC6, Wetzlar, Germany) with a glass knife and Internal Anatomical Features of the stained with a 0.5% aqueous solution of toluidine blue. Eyes. General Organization. Each ommatidium is Ultrathin sections ( 65 nm) were cut on an ultramu- composed of two distinct structures: the dioptric appa- tome (Leica EM UC6þFC6, Wetzlar, Germany) with a ratus, consisting of corneal lens and crystalline cone, diamond knife (Diatome, Bienne, Switzerland) and and the photoreceptive layer, made up of retinular cells picked up on uncoated 200-mesh copper grids.
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