A PREDATOR DEFENCE IN ONYCHIURUS ARMATUS (TULLB.) (COLLEMBOLA: ONYCHIURIDAE) R . A . BROWN
Collembola are small, often brightly coloured primitive insects known commonly as 'springtails' because of their habit of jumping away when disturbed by using a specialised springing organ or furca which arises from the fourth abdominal segment. These animals live at the soil surface, sometimes climbing plants, and are well known to most natural historians. However, several species lack pigment and live permanently under the soil surface. In these animals the furca is reduced or is vestigial and, because of their lifestyle, they are not well known. Onychiurus armatus (Tullb.) is of the latter type. It is 1-2 mm long, white, with no eyes and its furca is reduced to a cuticular Aap. Despite being relatively unknown, and having no recognised common name, O. armatus is one of the commonest and most widely distributed animals in the world. It has been recorded from every continent save Antarctica. In the British Isles it can be found in many different habitats, unlike the majority of collembola. I have found it in deciduous and mixed leaf litter, grassland, arable fields ranging from high chalk wolds to peat and silt fens, and in moorland. As most collembola, O. armatus feeds principally upon the decaying organic fraction of the soil, thus playing a part in the cycling of nutrients, albeit small in comparison to earthworms. O. armatus is, however, more catholic in its food choice than many collembola and has been observed feeding on freshly shed green leaves (Hutson, 1974), nematodes (Gilmore, 1979) and nematode cysts (Murphy and Doncaster, 1957). I have observed it eating green algae (Pleuroccocus spp.) and on astimatid mites (Tyrophagus spp.). O. armatus has also been named as a pest of bean seedlings (Edwards, 1971) 3 n d Â° f S U g a r " b e e t s e e d l i n 8 s ( B a k e r and Dunning, 1975; Heijbroek, Paragamasus lapponicus (Tragadh.) is an active and voracious predatory mesostigmatid mite living both on and below the soil surface. It is widely distributed in Europe and the British Isles. P. lapponicus feeds upon collembola, mites, and small larvae in the soil. It is 7 mm long and is reddish-brown in colour. Like O. armatus, P. lapponicus is unable to make its own burrows in the soil. Both animals live in voids, the cavities between soil aggregates, and these vary greatly in size. Generally O. armatus seek out the smallest possible voids, moving out of them as they grow, consequently the juveniles inhabit the smaller burrows. Because of its size, P. lapponicus is rarely able to penetrate the burrows of O. armatus juveniles, but shares the larger voids with the adults.
Trans. Suffolk Nat. Soc. 18 part 2.
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The interaction of adult O. armatus and P.
When P. lapponicus meets an adult O. armatus in a void there is little escape for the collembolan. The mite can easily outrun it, and O. armatus cannot spring away as it lacks an effective furca. To deal with this seemingly desperate Situation O. armatus has evolved a defence mechanism unique, to my knowledge, amongst collembola. It is best illustrated by reporting the events of such a meeting as observed under a microscope in the laboratory. The mite advances, constantly testing the substratum in front of it with its front legs. These lack claws and are modified. When it meets a collembolan (Fig. 1) it stops, and briefly touches it with its front legs for 4-5 seconds; this informs the mite that a prospective prey has been found. The mite then checks the prey's suitability by lightly holding it with its front legs and palpating the prey with its pedipalps for another 4 - 5 seconds or longer (Fig. 2). Ordinarily the mite would then grasp the prey firmly between the genu (a) and femur (b) and tear a hole in the body wall with its chelicirae ((c) shown extended in Fig. 1) and hold the collembolan close to its mouth, sucking out its body fluids and later discarding the body. P. lapponicus frequently lifts its prey from the substratum whilst feeding and continues to move forwards. However, when the mite starts to feel O. armatus with its front legs, the collembolan stands still and within 2 - 3 seconds a drop of milky liquid appears on abdominal segment five (e) in the vicinity of a collection of organs known as pseudocelli ( / ) . The collembolan then bends its abdomen forwards over its head and attempts to smear this liquid around the mouthparts of the attacking mite (as indicated in Fig. 3). If it succeeds, the mite quickly drops the collembolan and backs away, frantically rubbing its mouthparts with its front legs, and by the time it has apparently recovered, the collembolan has left. If P. lapponicus is kept solely with a number of (). armatus adults, it will eventually manage to eat some of them, but after it has been 'hit' with the milky liquid it avoids contact with the collembolan, giving up after it has made a preliminary feel with its front legs. O. armatus juveniles sometimes produce a clear liquid if attacked by P. lapponicus in the laboratory, but this does not seem to deter the mite. When given the choice of O. armatus adults or another common collembolan, Folsomia Candida (Willem), P. lapponicus wili avoid O. armatus altogether after a few abortive attacks (Sparkes pers. comm.). The milky fluid has been shown to be highly repulsive to other collembola (Usher and Balogun, 1967) and can be induced by attacking O. armatus with a fine brush, imitating a mite. The pseudocelli The milky fluid is released from pseudocelli on abdominal segment five (Huributt, 1965; Karg, 1961; Usher and Balogun, 1967). These organs were originally thought to be light sensitive and have been used extensively as taxonomic characters within the genus (e.g. Gisin, 1960). By sectioning and optical microscopy, Usher and Balogun suggested that they were spherical pits covered with a smooth continuation of the granular cuticle, underlaid by dark-staining cells. Scanning electron microscopy shows that they are shallow Trans. Suffolk Nat. Soc.
Figs 1, 2 and 3. The defence mechanism of Onychiurus armatus when attacked by Paragamasus lapponicus. (a) Genu of mite's leg, (b) Femur, (c) Chelicirae, (d) Pedipalp, (e) Drop of milky fluid, (f) Location of pseudocelli on abdominal segment five. Trans. Suffolk Nat. Soc.
A P R E D A T O R D E F E N C E IN O N Y C H I U R U S ARMATUS ( T U M . B . )
pits covered by a 'clam shell' like trap door (shown partly open in Fig. 4). The cuticle of O. armatus is scattered with these structures but it appears that only those on abdominal segment five (three on each side, closely spaced) are primarily used in defence. Acknowledgement I would like to thank the staff of the Electron Optic Unit, the University of Newcastle-upon-Tyne, for the electron micrograph. References Baker, A . N. and Dunning, R. A. (1975). Association of populations of Onychiurid collembola with damage to sugar beet seedlings. PI. Path. 24, 150. Edwards, C. A . (1962). Springtail damage tobean seedlings. PI. Path. 11,67. Gilmore, S. K. (1970). Collembola predation on nematodes. SEARCHAgriculture. (Cornell Univ., New York). 1, 1. Gisin, H . (1960). Collembolenfaunas Europas. Museum d'Historie Naturelle, Geneve. H e i j b r o e k , W. (1971). De mogelijkheden voor bestrijding van belangrijkste voorjaarsplagen. III De springstraart. (Onychiurus armatus Tullb.). Meded. Inst. Rat. Suikprod. 38,1.
Scanning electron micrograph of a pseudocellus, x 10,000. Trans. Suffolk Nat. Soc.
Suffolk Natural History, Vol. 18, Part 2
H u r i b u t t , H . W. (1965). Systematics and biology of the genus Veigaia (Acarina: Mesostigmata) from Maryland. Acaralogia. 7, 598. H u t s o n , B. R. (1974). The invertebrate fauna influencing soil development on industrial reclamation sites. Ph.D. Thesis, Univ. Newcastle-uponTyne. Karg, W . (1961). Ă–kologische untershungen von edaphischen gamasiden (Acarina, Parasitiformes). Pedobiologia. 1, 77. M u r p h y , P. W. and Doncaster, C. C. (1957). A culture method for soil meiofauna and its application to the study of nematode predators. Nematol. 2, 202. U s h e r , M. B. and Balogun, R. A. (1967). A defence mechanism in Onychiurus armatus (Collembola: Onychiuridae). Em. mon. Mag. 102, 237. R . A . Brown Half A c r e Cottage, Barrow, Bury St. E d m u n d s , Suffolk.
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