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Pedestal Hairs of the Ant Echinopla Melanarctos (Hymenoptera, Formicidae): Morphology and Functional Aspects

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Pedestal Hairs of the Ant Echinopla Melanarctos (Hymenoptera, Formicidae): Morphology and Functional Aspects Zoomorphology (2006) 125: 57–68 DOI 10.1007/s00435-005-0011-8 ORIGINAL ARTICLE Werner Gnatzy Æ Ulrich Maschwitz Pedestal hairs of the ant Echinopla melanarctos (Hymenoptera, Formicidae): morphology and functional aspects Received: 12 July 2005 / Accepted: 3 October 2005 / Published online: 23 February 2006 Ó Springer-Verlag 2006 Abstract The South East Asian arboreal Formicine Introduction Echinopla melanarctos, as well as some other members of this genus possess a cuticular structure unique in ants, In ants (Formicidae), presence of conspicuous covers of the pedestal hairs. In E. melanarctos, about 700 pedestal long and dense hairs, on the exoskeleton is rare hairs are situated on the dorsal and lateral surfaces of (Holldobler and Wilson 1990). However, workers of the head, the alitrunk, the petiole and the gaster. They ¨ species of the tropical ant tribes Basicerotini and Ste- are arranged in a polygon-like figuration. On the summit gomyrmecini possess two dominant forms of setae on of each of the up to 200-lm high pedestals, a single the dorsal surfaces of the body and outer surfaces of central hair inserts. This hair (up to 500-lm long) is legs: longer ‘brush’ hairs with splintered distal ends, and innervated by a single bipolar mechanosensitive sensory shorter ‘holding’ hairs that vary among species from cell. The lumen of each tube-like pedestal contains (1) plumose to blade-shaped or filiform. According to epithelial cells (2) the sensory cell and the auxiliary cells Holldobler and Wilson (1986), the two hair types usually of the central hair and (3) the long efferent ductules of ¨ but not invariably occur together to form a double layer. up to ten isolated bicellular glandular units. Each glan- The brush hairs evidently scrape or otherwise capture dular unit is composed of a secretory glandular cell and fine particles of soil. In this way, the camouflaged a duct cell, all of which are located at the base of a workers can hardly be distinguished from the soil. Other pedestal. The cytoplasm of a glandular cell contains a well-documented special cuticular hair structures are the well-developed end apparatus and is characterised by so-called ammochaetae, layers of long curved hairs sit- stacks of smooth and granular endoplasmic reticulum, uated on the lower surface of the head and on the numerous polyribosomes, a lot of mitochondria and mouthparts. They are found in various desert ants and some up to 5-lm large secretory vesicles. The secretion used for cleaning the body cuticle and also for transport of the gland cells is released on the apex of the pedestal and soil digging (Wheeler 1910; Maidl 1933). wall via small pores. Approximately 30 lm below their During ecological studies on the southeast-Asian summit, some pedestals possess additionally (up to six) arboreal formicine genus Echinopla (Maschwitz and mechanosensitive hairs that are arranged ray-like. We Reichard, personal communication), we came upon suppose that the pedestal hairs are important in nest- Echinopla melanarctos (Smith 1857), an ant species living space protection and find that only in ants with in small colonies in dead hollow branches lying on the high pedestals on the head (Echinopla melanarctos and ground or hanging in the vegetation. The habitus of this Echinopla pallipes), the compound eyes are stalked thus species is quite unique: head, alitrunk, petiole and gaster overtopping the pedestals. are dorsally fully covered with long black hairs, which are inserted in very obvious cuticular pedestals. These Keywords Pedestal hairs Æ Topography Æ structures also surround the compound eyes of the Fine structure Æ Mechanoreceptors Æ Gland cells species. As the eyes are sitting on stalks, they overtop the pedestal layer. Other species of Echinopla are also cov- ered with a dense hair layer, partly with or without W. Gnatzy (&) Æ U. Maschwitz pedestal structures (Smith 1857;Ho¨lldobler and Wilson Zoologisches Institut, J.W. Goethe-Universita¨t, 1990). Siesmayerstr. 70, 60323 Frankfurt, Germany E-mail: [email protected] Here, we give a detailed morphological and fine Tel.: +49-69-79824713 structural analysis of the pedestal hairs of E. melanarctos Fax: +49-69-79824820 that could contribute to future functional studies of 58 these unique structures. We used the techniques of light 1857, Echinopla striata Smith 1857; collection W.H.O. microscopy and scanning electron microscopy (SEM) to Dorow, Forschungsinstitut Senckenberg, Frankfurt) map the number, size and external structure of pedestal were mapped using a Wild M 5 microscope at a mag- hairs and the gland cell-complexes associated with each nification of 500·. of the pedestals. We found on head, alitrunk, petiole and gaster (1) cuticular pedestals with a long hair (= central hair) Ultrastructural studies inserting in the summit of each pedestal and (2) some pedestals which additionally posses shorter hairs Workers of E. melanarctos were anesthetised with car- (= secondary hairs) extending ray-like from the upper bon dioxide. Parts of the cuticle with pedestal hairs were third of the pedestal. Using transmission electron sectioned oblique in a drop of buffer with a razor blade. microscopy (TEM), we found out that (3) the central These fragments were prepared for the SEM or the and secondary hairs are cuticular mechanoreceptors of TEM. the ‘tactile hair’ type; i.e. each of these hairs is inner- vated by one bipolar sensory cell. Furthermore, (4) each tube-like pedestal contains in its lumen, the sensory cell and the auxiliary cells of the central hair and—if pres- Scanning electron microscopy ent—the sensory cells together with their auxiliary cells of the secondary hairs. Corresponding with the number For SEM, all preparations were prefixed for several of glandular units per pedestal, maximally ten efferent hours in 2% glutaraldehyde (in 80 mM sodium-caco- ducts pass through the pedestal lumen each of them dylate buffer and 3.9% sucrose, pH 7.25), postfixed for opening at the summit of the pedestal in a single small 2 h in 2% OsO4 solution in the same buffer, finally pore. Also, (5) below the base of each pedestal floating dehydrated in a graded ethanol series. After critical in the haemolymph space are located between two and point drying in a Polaron unit, using CO2 and amyl- up to ten bicellular glandular units, (type class III acetate (2·15 min), the samples were mounted vertically according to Noirot and Quennedey 1974, 1991) each on aluminium holders using double-sided conductive composed of a secretory cell and a duct cell. carbon tape in order to allow an investigation of the Materials and methods Animals In all the experiments, adult workers of E. melanarctos Smith 1857 were used. They were obtained from a col- ony, which contained about 50 workers and brood. The ants were collected in the Pasoh Forest Reserve, a pri- mary lowland dipterocarp forest in Negeri Sembilan in Peninsular Malaysia. The colony inhabited two hollow dead branches each about 20 mm in diameter. The branches lay 1.5 m apart from each other one on the ground and one hang loosely in the low vegetation. The colony was kept in a plastic container with a gypseous bottom layer where they lived within a bamboo culm 5– 10 mm in diameter. As food supply, honey/water (1:1) was offered. Fig. 1 Macro photo of a worker of Echinopla melanarctos, lateral view Image analysis and comparative morphology Table 1 Distribution of pedestal hairs of E. melanarctos-workers (n=3) The number and distribution of pedestal hairs on the exoskeleton of E. melanarctos (n=3) were counted using Location Number of hairs a Wild M 5 microscope at a magnification of 500·. The quantitative data were expressed as means. Head x ¼ 110 Alitrunk (mesonotum) x ¼ 245 Additionally, the distribution of various hair Petiole x ¼ 15 types and the shape of compound eyes in workers of Gaster x ¼ 353 E. melanarctos Echinopla and other three species R=723 (Echinopla lineata Mayr 1862, Echinopla pallipes Smith 59 Fig. 2 a–e Echinopla melanarctos. General morphology and hair c Tergite of first gastral segment, view from above. Note the types of a worker. SEM pictures. a Head, frontal view. White arrangement of the pedestal hairs. Buttress-like cuticular ridges of arrowheads mark pedestal hairs, arrow marks stalked eyes. b pedestal bases arrowheads. d Hairs on the petiole with short (black Gaster, dorsal view. White arrowheads mark pedestal hairs on the arrowheads) and long pedestals (white arrowheads). e Bristle hairs huge tergite of the large first gastral segment, black arrowheads on the leg of a worker ant without any pedestal (arrowhead). Mn mark hairs with short pedestal on the remaining gastral tergites Mandible, Sc base of scapus 60 inner and outer side of the specimens. Finally, the c specimens were gold coated in an Agar Sputter Coater, Fig. 3 a–e Echinopla melanarctos. Glandular units of pedestal hairs then investigated with a field-emission SEM equipment in a worker. a Semi-thin longitudinal-section through a pedestal on tergite of first gastral segment. The course of the ductules within (Hitachi S-4500) at an accelerating voltage of 1–5 kV. and out of the secretory gland cells (Glc) is indicated by white Some fragments were treated with hot 5% potassium arrowheads. b–e. Low power SEM pictures. b Partly cut-off hydroxide (KOH) for 10 min before SEM preparation. pedestal (Pe) with its gland cells (Glc). c Inner surface of a part Additionally, some specimens were freed from wax of the pronotum. Note the arrangement of the gland cells (Glc). Arrows mark bundles of muscle fibres. d Inner surface of a part of with chloroform–methyl alcohol (2:1) at 60°C before the pronotum after KOH-treatment. Note that the openings into SEM preparation (Bru¨ck and Stockem 1972).
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