Fine structure of the gnathosoma of Archegozetes

JOURNAL OF MORPHOLOGY 272:1025–1079 (2011)

Fine Structure of the Gnathosoma of Archegozetes longisetus Aoki (Acari: Oribatida, Trhypochthoniidae) Gerd Alberti,1* Michael Heethoff,2 Roy A. Norton,3 Sebastian Schmelzle,2 Anna Seniczak,4 and Stanisl--aw Seniczak4 1

Zoological Institute and Museum, University of Greifswald, J.-S.-Bach-Str. 11/12, D-17487 Greifswald, Germany Institute for Evolution and Ecology, University of Tu¨bingen, Auf der Morgenstelle 28E, D-72076 Tu¨bingen 3 College of Environmental Science and Forestry, State University of New York, Syracuse, New York 13210 4 Department of Ecology, University of Technology and Life Sciences, ul. Kordeckiego 20, PL-85225 Bydgoszcz, Poland 2

ABSTRACT Oribatida are one of the main groups of Acari comprising mostly important decomposers in soils. Most species are particle feeders, an exceptional mode of nutrition in Arachnida. Hence, their feeding organs, the gnathosoma, are of special functional interest. We studied nearly all components using scanning and transmission electron microscopies as well as reconstructions based on synchrotron X-ray microtomography from the model oribatid Archegozetes longisetosus. Besides cuticular structures, we describe the full set of muscles and confirm the presence of a trochanter remnant at the base of the chelicera. Setae on the prodorsum and the anterior and posterior infracapitular setae are mechanoreceptors innervated by two dendrites ending with tubular bodies. Dendrites of adoral setae, anterior setae of the chelicerae, and the supracoxal setae show neither obvious tubular bodies nor wall or terminal pores. Thus their function remains obscure. For the first time, a muscular proprioreceptor has been found in Arachnida. It likely monitors the actions of muscles moving the movable digit of the chelicera. Glandular structures within and associated with the gnathosoma are described. Dermal glands represented by secretory porose areas are found within the infracapitulum. More complex associated glands comprise the podocephalic glands and the infracapitular glands, the ducts of which were traced completely for the first time. The components described are mostly fundamental for the gnathosoma of Actinotrichida (Acariformes), one of the two lineages of Acari, to which Oribatida belong. The gnathosoma is generally considered the most relevant putative synapomorphy of Acari. Since the monophyly of Acari has become more and more questionable during the last decades, a thorough reinvestigation of this body part is necessary for a comprehensive understanding of acarine and even arachnid phylogeny and evolution. This article provides a starting point of such a re-evaluation of the gnathosoma. J. Morphol. 272:1025–1079, 2011. Ó 2011 Wiley-Liss, Inc. KEY WORDS: Acari; functional morphology; gnathosoma; SR-lCT; muscles; sensory system

INTRODUCTION The Acari, comprising about 55,000 named species (Krantz and Walter, 2009), is the most speciesrich arachnid taxon, yet only two shared, derived features are prominent. One is the gnathosoma, a secondary body region associated with feeding, Ó 2011 WILEY-LISS, INC.

Note: species name, longisetosus, is misspelled in title

which includes the appendages and other elements of the cheliceral and pedipalpal segments. The other is the peculiar life cycle comprising five principal instars (stases): a hexapod larva and four subsequent octopod instars (protonymph, deutonymph, tritonymph, and adult). On the basis of these traits, Weygoldt and Paulus (1979a,b) concluded that Acari are monophyletic and represent the sister group of Ricinulei, which also have a hexapod larva. This view was tentatively supported in a careful, detailed study by Lindquist (1984), who recognized that feeding organs in Ricinulei form a kind of gnathosoma. Over the last two decades, the monophyly of Acari and its sistergroup relationship with Ricinulei have been accepted by most authors who dealt with systematics or phylogenetics of higher categories of Arachnida (e.g., Shultz, 1990, 2007; Wheeler and Hayashi, 1998; Dunlop, 2000; Paulus, 2004). This is despite the cautious nature of Lindquist’s (1984) conclusions and the convictions of other authors who interpreted the Acari as poly- (e.g., Vitzthum, 1940/43; Johnston, 1982) or diphyletic (e.g., Hammen, 1968a, 1972, 1989). Regardless of external relationships, the internal monophyly of the two major taxa of mites, Anactinotrichida (Parasitiformes s.lat) and Actinotrichida (Acariformes), is virtually certain. The only contentious issue has been whether the Opilioacarida Additional Supporting Information may be found in the online version of this article. Contract grant sponsors: Humboldt Foundation and the Polish Foundation for Science, German Academic Exchange Service (DAAD). *Correspondence to: G. Alberti, Zoological Institute and Museum, University of Greifswald, J.-S.-Bach-Str. 11/12, D-17487 Greifswald, Germany. E-mail: [email protected] Received 17 December 2010; Revised 20 March 2011; Accepted 24 March 2011 Published online 31 May 2011 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/jmor.10971

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are a subgroup of Anactinotrichida (Evans et al., 1961; Hammen, 1972, 1977) or a third major mite group (Walter and Proctor, 1999; Harvey, 2002; Coddington et al., 2004; Beccaloni, 2009). The former view seems best supported by including nontraditional characters such as sperm morphology (Alberti, 1980b,c, 1991, 2006; Lindquist, 1984; Bernini, 1986) and molecular characters (Giribet et al., 2002; Murrell et al., 2005; Klompen et al., 2006; Dabert et al., 2010; Pepato et al., 2010) and has been adopted for the new edition of the Manual of Acarology (Krantz and Walter, 2009; as in the previous edition). Because of profound differences between Actinotrichida and Anactinotrichida, Bernini (1986) was reluctant to accept mite monophyly, as was Alberti (2006), who pointed out a number of internal and ultrastructural characteristics that bring it into doubt. A similar position was recently taken by Dunlop and Alberti (2008) who reviewed and discussed the problem of acarine relationships within the Arachnida. The striking similarity in testis histology and sperm morphology of Actinotrichida and Solifugae, but not Anactinotrichida, and its likely relevance to systematics, has been known for decades (Alberti, 1980a–c, 2000, 2006; Alberti and Peretti, 2002; Klann et al., 2005, 2008). This same relationship has recently received molecular support (Dabert et al., 2010; Pepato et al., 2010), but the problem of acarine arachnid phylogeny is still far from being solved (Alberti, 2006; Dunlop and Alberti, 2008). Hence, the characters perceived to support mite monophyly need careful re-examination. One of these, a life cycle that includes a hexapod larva, maybe of limited value. Negative, regressive characters seem rather easily convergent, so the suppression of leg IV in the larva may have evolved in both (or three when considering also Ricinulei) taxa independently. Another similarity of the two groups of mites relates to life cycle: most Actinotrichida and the primitive anactinotrichid group Opilioacarida (but no others) have a sixth instar, the prelarva, which has not yet been discovered in Ricinulei. However, the prelarva of Opilioacarida differs profoundly from that of Actinotrichida (cf. Coineau, 1973; Hammen, 1989; Klompen, 2003; Alberti, 2006). The gnathosoma, the most important putative synapomorphy of Acari, has been the subject of doubt. Hammen (1970, 1972), after very detailed studies of representatives of all main taxa, was convinced that it is a convergent structure, having evolved independently in Anactinotrichida and Actinotrichida. Considering the vast diversity and well-documented evolutionary plasticity of arthropod mouthparts, the independent origin of the actinotrichid and anactinotrichid gnathosoma is not an outlandish idea. However, the cuticular traits that are typically studied with light microscopy seem insufficient Journal of Morphology

to confirm or reject their homology. An integration of cuticular data (including some newly examined traits) with ultrastructural and functional characters seems a necessary next step and is our overall goal. In this article, we start with a study of the gnathosoma of a member of the suborder Oribatida as a first representative of actinotrichid Acari. Most oribatid mites live in soil and most are particle feeders on plant remains or fungi, thus playing an important role as decomposers in terrestrial ecosystems (e.g., Schuster, 1956; Petersen and Luxton, 1982; Wilson, 1987; Norton, 1990; Alberti et al., 1996; Walter and Proctor, 1999; Weigmann, 2006; Norton and Behan-Pelletier, 2009). The capability of ingesting particulate food is rather exceptional within Arachnida and is only shared by some other Acari (Walter and Proctor, 1998, 1999) and Opiliones (Pinto-da-Rocha et al., 2007). Characters of the oribatid gnathosoma are frequently used in taxonomical studies, so the cuticular structures comprising its external morphology are well known (e.g. Willmann, 1931; Sellnick, 1960; Balogh and Mahunka, 1983; Norton, 1990; Woas, 2002; Weigmann, 2006; Norton and BehanPelletier, 2009) and are the subject of a complex terminology (Grandjean, 1957a; Knu¨lle, 1957; Hammen, 1968b, 1989). However, few authors have attempted to link external and internal gnathosomal morphologies in Oribatida, and these studies are almost completely based on light microscopy (see Evans, 1992; Moritz, 1993; Alberti and Coons, 1999; Norton and Behan-Pelletier, 2009). We chose to study the middle derivative oribatid mite Archegozetes longisetosus Aoki, 1965 (Trhypochthoniidae) because of its increasing importance as a ‘‘model’’ oribatid mite (see Thomas, 2002; Heethoff et al., 2007), the rather unspecialized nature of its gnathosoma, and the relative ease of culturing [In a previous article, A. longisetosus was addressed as an early derivative oribatid mite (Alberti et al. 2003), but middle derivative seems more appropriate (e.g., Norton and Behan-Pelletier, 2009)]. External details of the gnathosoma of trhypochthoniid mites have been described by Aoki (1965), Beck (1967), Sitnikova (1975), and Norton et al. (1996), with the latter including scanning micrographs. This study complements earlier extensive articles dealing with the digestive system and fat body of this mite (Alberti et al., 2003; Heethoff and Norton, 2009b) and a preliminary study on the gnathosoma (Alberti et al., 2004). Additional information on A. longisetosus was recently provided by a biomechanical study of the chelicerae by Heethoff and Norton (2009a). MATERIALS AND METHODS Specimens Archegozetes longisetosus mites were from the ran-lineage (Heethoff et al., 2007), which originated from a culture started

GNATHOSOMA OF Archegozetes (ORIBATIDA) by R. A. Norton in 1993 from eggs of one gravid female collected in Puerto Rico. Cultures were maintained in plastic containers with a moist bottom of plaster-of-Paris: charcoal mixture. Food provided was tree bark covered with green algae (mostly Protococcus sp.). As A. longisetosus is a parthenogenetic species, the investigated specimens consisted of females only. The study was mainly based on adults. So, if not otherwise indicated all figures refer to adults.

Electron Microscopy Adult mites were prepared for transmission electron microscopy (TEM) as follows. Living specimens were cut transversely into halves with a razor blade in ice-cold fixative (3.5% glutaraldehyde in phosphate buffer at pH 7.4; 0.1 mol L21). After 2 h in the cold fixative, specimens were rinsed in buffer solution for a further 2 h. Postfixation in 2% aqueous OsO4 solution for another 2 h was followed by rinsing in buffer solution for 10 min. The tissues were subsequently dehydrated using graded ethanols (60, 70, 90, 96, and 100%) and embedded in Araldite with propylenoxide as the intermedium. Polymerization occurred at 608C. Some specimens were also embedded in Spurr’s medium (Spurr, 1969) without the propylenoxide-intermedium step. These specimens were polymerized at 658C. Ultrathin sections (70 nm) were cut with a Leica Ultracut UCT and were double-stained with uranyl acetate and lead citrate (Reynolds, 1963). These sections were studied with a Zeiss EM 10A or a JEOL JEM-1011 TEM. Semithin sections stained according to Richardson et al. (1960) were used for general orientation. Light microscopy on these sections was performed using a compound microscope (Olympus BX60) and was recorded using a digital camera (DP 10). For scanning electron microscopy (SEM), mites were fixed in 70% ethanol. Some specimens were cut with a razor blade to make certain structures visible. Dehydration was with graded ethanols. After an intermediate step with amylacetate, specimens were critical point dried using liquid CO2 as the final medium. The specimens were placed on aluminum stubs with a double-stick carbon tape and coated with palladium-gold. The specimens were studied using LEO DSM 940A and Cambridge Stereoscan 250 Mk2 scanning electron microscopes.

Synchrotron X-Ray Microtomography Fresh specimens were cleaned with a fine brush and placed in a 6:3:1 mixture of 80% ethanol, 35% formaldehyde, and 100% acetic acid for 24 h. Specimens were then dehydrated in a graded ethanol series of 70, 75, 80, 85, 90, 95, and 100% with three changes at each concentration, and 10 min between steps. Finally, samples were placed in fresh 100% ethanol overnight, and then critically point dried in CO2 (CPD 020, Balzers). Tomography (holotomography) was performed at beamline ID19 (ESRF, Grenoble, France, experiment SC-2127) with an energy of 20.5 keV. The radiographs were recorded with a cooled CCD (ESRF FReLoN camera) with a 14-bit dynamic range, 2048 3 2048 pixels and an effective pixel size of 0.7 lm. One thousand five hundred projections were recorded over the 1808 sample rotation with an exposure time of 0.35 s for each projection. The detectorto-sample distances were 10 mm, 20 mm, and 45 mm for holotomography, the 20 mm scan was also used for a phase enhanced tomographic reconstruction. Resulting voxel data were analyzed in amiraTM (Mercury Computer Systems, Chelmsford, Massachusetts), VGStudio MAX (Volume Graphics, Heidelberg), and OsiriX (Rosset et al., 2004). A detailed description of this technique is given in Betz et al. (2007) and Heethoff and Cloetens (2008).

GENERAL REMARKS Without doubt, the most fundamental studies on the gnathosoma of oribatid mites are those of

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Grandjean (most importantly, 1957a, 1959) and the comprehensive work of Hammen (1968b, 1989). In the following, we will largely use the terminology and abbreviations introduced in the latter works (see also Hammen, 1980). Hammen (1980, 1989) considered the gnathosoma of Acari to be an anterior pseudotagma that is movable against the remainder of the body, that is, the idiosoma (Figs. 1, 2a, 3a, 14, and 15). These secondary body regions are distinct from the true chelicerate tagmata (prosoma and opisthosoma). The gnathosoma is not a ‘‘head’’ because it does not include the brain. The gnathosoma comprises two principal parts: the cheliceral frame, bearing the chelicerae (Ch), and the infracapitulum (also termed subcapitulum), bearing the pedipalps (Pdp; Figs. 1–4) [for a complete list of abbreviations see Supporting Information 1]. The cheliceral frame connects the chelicerae to the idiosoma and infracapitulum in a movable way, by means of flexible cuticle. Its dorsal part is the tegulum (TG). The cheliceral frame merges with a pair of flexible, invertible cheliceral sheaths (Cx; interpreted as coxal regions of the chelicerae by Hammen, 1968b, 1989) that allow independent motions of the two chelicerae: retraction (by means of extrinsic cheliceral retractor muscles) and protrusion (probably through hemolymph/hydrostatic pressure). Rather than attaching to the chelicera proximally, which is the plesiomorphic condition in Oribatida, in A. longisetosus the sheath attachment line (acx) encroaches distally, such that about onequarter of the cheliceral length is inside the body wall and functions as an apodemal extension (e.g., Norton, 1998). The chelae of the chelicerae are operated by intrinsic muscles that insert on the basal part of the movable digit (md; also called apotele); an upper (superior) tendon (ts) connects to the strong levator muscle and a lower (inferior) tendon (ti) connects to the smaller depressor muscle (Figs. 6, 7, 9–11, 12a, 13d, 14, and 15; Grandjean, 1947; Hammen, 1968b, 1989; Evans, 1992; Alberti and Coons, 1999; Heethoff and Norton, 2009a). The infracapitulum bears the pedipalps and includes the mouth (Mo; Figs. 9c, 14, 15, and 24e), which is surrounded by lips (Figs. 1, 3, and 4). In Actinotrichida, there are plesiomorphically four lips: an upper lip (labrum, LS), two lateral lips (LL), and a lower (also ventral or inferior) lip, the labium. The labium is present only in early derivative actinotrichid mites (‘‘Endeostigmata’’ and Palaeosomata) and thus is considered to be absent in A. longisetosus (but see below). The borders of the lips extend into the mouth (or even into the pharynx) as longitudinal furrows (so-called commissures). Plesiomorphically, in the presence of a labium, there are four commissures (two superior Js and Js0 and two inferior Ji and Ji0 ). However, most actinotrichid mites, lacking a labium, have only three (the two superior ones Js and Js0 and Journal of Morphology

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Fig. 1. Schematic drawings showing main structures of an oribatid gnathosoma (partly adapted from Hammen 1989 referring to Archegozetes magna). (a) Lateral view of body of the entire mite. Scale bar: 150 lm. (b) Lateral view of gnathosoma. Left side of rostral tectum, part of left prodorsum, left chelicerae, pedipalp and legs removed. Scale bar: 50 lm. af, manubrial fissure; a, anterior infracapitular seta; acx, line of attachment of cheliceral sheath to chelicera; AP, anal plate; bo, trichobothrium (bothridial seta); CX, cheliceral sheath; dj, dorsosejugal furrow; e, supracoxal seta; GP, genital plate; h, posterior infracapitular (mental) seta; in, interlamellar seta; LI, leg I; LIV, leg IV; le, lamellar seta; m, median infracapitular seta; MN, manubrium; Not, notogaster; or1or3, adoral setae 1–3; PD, prodorsum; Pdp, pedipalp; ro, rostral seta; rp, rostrophragma; Tg, Tra¨ga˚rdh’s organ.

one inferior Ji; Fig. 24e,f). The plesiomorphic actinotrichid mouth thus has a quadrangular cross section, while the more derivative cross section is triangular. As the ventral commissure is short (only separating the two LLs), the cross-sectional shape becomes a crescent in the fore gut (Figs. 6, 9, 10, and 24; Grandjean, 1957a; Alberti and Coons, 1999; Alberti et al., 2003, 2004). The LS is proximally attached to the cervix, that is, the dorsal unpaired part of the infracapitulum. Laterally, the infracapitulum is formed by large lateral ridges (LRs) including the bases of the pedipalps, which protrude anteriorly as a pair of malapophyses (MAs); the latter most likely represent endites of the palps (Figs.1b and 3g; Hammen 1980, 1989). The ventral part of each MA is called the gena (G; Fig. 3d,g). Anteriorly, the MA bears one of the paired LLs and, in some Endeostigmata and in all Oribatida, the rutellum (RU; Figs. 1, 2c,e, 3d–h, and 4b–d,f). The ventral unpaired part of the gnathosoma, that is, the part opposite the cervix, is termed mentum (M; Fig. 3g). Journal of Morphology

The gnathosoma of oribatid mites is movable against the idiosoma due to extrinsic muscles attaching to the capitular apodeme (ap.c; a proximal extension of the cervix cuticle; Figs. 6d–f, 12, 13, 14, 15, and 24), to its flexible proximal cuticle, and to a pair of lateral cuticular reinforcements (condyles k) positioned close to the base of legs I that establish an axis of rotation. The anterior lateral and dorsal borders of the idiosoma (prodorsum, PD) in Oribatida usually form an extensive, sclerotized roof-like protrusion, the rostral tectum (Figs. 1, 2, and 3a–e), which encloses a secondary cavity (secondary camerostome) in which the gnathosoma lies, protected dorsally and to some extent also laterally (Norton and Behan-Pelletier, 2009). The rostral tectum has a dorsal side, the rostrum (RO), and a ventral side called the rostrophragma (rp). The presence of a rostral tectum and secondary camerostome characterizes the derived condition called stegasimy. The plesiomorphic absence of these features is astegasimy (Grandjean, 1932, 1954a). A. longisetosus is stegasime. An analogous, but much smaller, sclerotized

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Fig. 2. Scanning electron micrographs of Archegozetes longisetosus. (a) Lateral view. Scale bar: 150 lm. (b) Frontal view. Scale bar: 150 lm. (c) Lateral view of tip of gnathosoma with rutellum and pedipalp. Scale bar: 10 lm. (d) Lateral view of gnathosoma protected under rostral tectum. Scale bar: 50 lm. (e) Dorsal view of gnathosoma. Note distinct border of rostrum, shape of chelicerae and tightly appressed rutella. Scale bar: 30 lm. a, anterior infracapitular seta; bo, trichobothrium (sensillus); Ch, chelicera; cha, posterior cheliceral seta; chb, anterior cheliceral seta; dj, dorsosejugal furrow (separating proterosoma from hysterososoma); e, supracoxal seta of pedipalp; h, posterior infracapitular (mental) seta; in, interlamellar seta; LI, leg I; LIV, leg IV; le, lamellar seta of rostrum; LS, labrum; m, median infracapitular seta; Not, notogaster (dorsum of hysterosoma); Pdp, pedipalp; RO, rostrum; ro, rostral seta; RU, rutellum.

Journal of Morphology

Fig. 3. Scanning electron micrographs of Archegozetes longisetosus (a–c tritonymph; d–i adult). (a) Laterofrontal view showing fully extended chelicerae. Note that cheliceral sheaths are completely unfolded. Scale bar: 40 lm. (b) Same specimen from dorsal view. Chelicerae are spread laterally so that the labrum and Tra¨ga˚rdh’s organs are visible. Part of the cheliceral frame (the TG) is also exposed. Scale bar: 50 lm. (c) Frontal view of same specimen. The proximal insertion of Tra¨ga˚rdh’s organs is visible (cf. Fig. 4g). Scale bar: 40 lm. (d) Ventrofrontal view with chelicerae in a more retracted position. Rostral tectum projects over the gnathosoma as a flat lamella. Note chela with toothed digits tightly paralleled by rutella. Lateral lips with adoral setae. Arrowhead points to flap covering the podocephalic canal (see inset). Scale bar: 30 lm. Inset: Detail of Figure 3d showing flap of podocephalic canal. Scale bar: 7.5 lm. (e) Similar view, but slightly turned to show proximal parts of chelicera. The cheliceral sheath is slightly exposed. Scale bar: 30 lm. (f) Anterior border of rutella with teeth and brush. Labrum visible, with small denticles. Scale bar: 10 lm. (g) Ventral view of gnathosoma showing infracapitulum with mentum and gena (ventral region of malapophyses) separated by faint labiogenal line (indicated by arrowheads). Note anterior parts of gena are separately protruding bearing the rutella and lateral lips. Scale bar: 50 lm. (h) Ventrofrontal view of portion of infracapitulum, showing rutella, and lateral lips with adoral setae. First adoral setae are spoon-like. Scale bar: 10 lm. (i) Ventral aspect of lateral lips with adoral setae. Note row of denticles on the paraxial side of rutella (indicated by arrow). Scale bar: 10 lm. a, anterior infracapitular seta; acx, line of attachment of cheliceral sheath to chelicera; bru, brush of rutellum; Ch, chelicera; cha, posterior cheliceral seta; chb, anterior cheliceral seta; CX, cheliceral sheath; e, supracoxal seta of pedipalp; fd, fixed digit of chelicera; G, gena; h, posterior infracapitular (mental) seta; LL, lateral lips; LR, large lateral ridge; LS, labrum; M, mentum; m, median infracapitular seta; md, movable digit (apotele) of chelicera; mnt, mentotectum; or1-or3, adoral setae 1–3; Pdp, pedipalp; RO, rostrum; ro, rostral seta; rp, rostrophragma; RU, rutellum; TG, tegulum; Tg, Tra¨ga˚rdh’s organ.

Fig. 4. Scanning electron micrographs of Archegozetes longisetosus (a–f adult; g–i tritonymph). (a) Dorsal aspect of gnathosoma. Note denticles on labrum and rutella. Scale bar: 5 lm. (b) Anterior tip of right chelicera. Note interdigitating teeth of fixed and movable digits, transversal rows of denticles on labrum. Scale bar: 10 lm. (c) Lateral view of labrum (arrow indicates lateral lamella), paraxial side of left chelicera (white arrowhead points to small tooth) and rutellum after removal of the right chelicera. The anterior part of Tra¨ga˚rdh’s organ is visible. Note adoral setae on lateral lips and small furrow (black arrowhead). Scale bar: 20 lm. (d) Anterior part of left rutellum with its denticles, lateral lips with adoral setae. Arrowheads indicate small furrow on lateral lip. Scale bar: 10 lm. (e) Aspect of mouth covered by the labrum (arrow points to lateral lamella) provided ventrally with rows of denticles. Tiny denticles on the wall of the mouth also visible. Scale bar: 10 lm. Inset: Denticles on wall of mouth in higher magnification. Scale bar: 1.5 lm. (f) Paraxial side of a partly broken rutellum showing denticles of the brush. Scale bar: 10 lm. (g) Dorsal aspect of one chelicera (principal segment) and Tra¨ga˚rdh’s organ. Scale bar: 20 lm. Inset: Detail of basal insertion of Tra¨ga˚rdh’s organ (cf. Fig. 3c). Note distinct ridge (arrow). Scale bar: 2.5 lm. (h) Ventrofrontal view of tip of labrum. Note rows of denticles. The denticles on the dorsal side point anteriorly, those on the ventral side posteriorly (towards the mouth). Arrows point to ventrally directed lamellae. Scale bar: 5 lm. (i) Dorsal aspect of anterior part of labrum. Note denticles forming the conspicuous corona (arrows) around the tip of the labrum. Scale bar: 5 lm. bru, brush on rutellum; Ch, chelicera; cha, posterior cheliceral seta; chb, anterior cheliceral seta; fd, fixed digit of chelicera; LI, leg I; LL, lateral lip; LS, labrum; md, movable digit of chelicera; or1, adoral seta 1; Pdp, pedipalp; RO, rostrum; ro, rostral seta; RU, rutellum; Tg, Tra¨ga˚rdh’s organ.

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fold projecting anteriorly from the coxisternum usually protects the idiosomal-infracapitular articulation ventrally; this is called the mental tectum (mnt; Fig. 3g; Hammen, 1968b, 1989).

A constitutive character of Actinotrichida is the presence of a paired podocephalic canal (cpc; Fig. 3d) that starts from an area dorsal or posteriodorsal to the leg I insertion and runs anteriorly, pass-

Figure 5.



ing above the proximal parts of the pedipalps and terminating dorsomedially at the base of the cervix under the chelicerae. Plesiomorphically, it collects the products of four glands, of which the three anterior ones are typical acinous glands (e.g., 1pGL; Fig. 15) and the posterior one is a, largely tubular, coxal gland (nephridium; 4pGL; Fig. 19a–c) Another pair, the infracapitular glands (iGLs), discharge their secretions independent of the podocephalic canal, through minute openings (ogi; Fig. 15) located close to the base of the LS. RESULTS The gnathosoma of A. longisetosus is directed toward the substrate, usually inclined against the body length axis by an angle of about 458 (Figs. 1, 2, 14, and 15). A series of cross sections (Figs. 5– 10) provides an overview of different parts of the gnathosoma; with chelicerae mostly retracted, the rutella (see below) are the most anterior parts. Integumental Characteristics The integument of the RO and gnathosoma has the normal general structure (Alberti et al., 1981; Alberti and Coons, 1999), composed of a cuticle and an underlying epidermis (Ep) that is usually a single flat epithelial layer underlain by a basal lamina. The cuticle of the body is only weakly sclerotized, giving the mite a ‘‘pale yellowish, sometimes light brown’’ color (For Archegozetes magna refer Hammen, 1989). The cuticle is much differentiated in various regions of the body according to functional needs. In general, it consists of the usual layers, that is, procuticle (prc) and epicuticle (ec). The procuticle of the more rigid structures (e.g., RO, chelicerae, genae, mentum) is rather thick, densely staining, and provided with pore canals (pc; Figs. 5e, 16b–e,h, 17, 18a–c,f, 19a, 20a, 21a, 22a–c, 23a,b, 26a,b,g, 27a–d, 29a–c, 30, and 31e,f). In other parts, it is densely staining and with pore canals but is rather thin and likely flexible (e.g., rostrophragma, cheliceral sheaths; Figs. 5c,e, 16a–d, 18a–c, 22a–c, and 23a,c). Internally projecting apodemes stain more or less densely and are likely stiff,

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but lack pore canals and, of course, an epicuticle (Figs. 18b,f,h, 19e, 22a,e, 24g,h, and 28b–e). Muscles attach either directly to these apodemes or to a tendon (t), a fibrous strand of modified and flexible cuticle that extends from the apodeme. In each case muscles are separated from the cuticle by a modified epithelial cell (also termed tendon cell, tc; Figs. 18b– f, 21b,c, 22, 23a,c, 24g,h, and 28a–e). In many regions, the procuticle forms distinct layers that probably have different mechanical properties. On the dorsal surface of the infracapitulum and LS, the inner layers stain densely and likely provide rigid skeletal support, whereas external layers are lucent and probably less hardened or even weak. These are covered by a very thin, densely staining exocuticle (and a very thin epicuticle, e.g., Fig. 24b,c,g). Pore canals are lacking or at least very minute (Figs. 21e,h–j, 24a–f, and 28b– d,f,g). On some flexible structures, such as oncophyses (op0 , opx) and Tra¨ga˚rdh’s organ (Tg), the cuticle almost completely comprises these thin layers (Figs. 21a,e,g, 23a,d, 24c–f, and 28e). In contrast, the rigid cheliceral digits and rutella are composed of three, almost unstructured procuticular layers without pore canals (Figs. 20d–l and 26a–c). In many oribatid mites, sclerotized cuticle may exhibit well-circumscribed areas having many, relatively wide pore canals, which are termed porose areas (po; areae porosae). Two different types of such areas have been distinguished: respiratory porose areas cover an unmodified thin epithelium, whereas secretory porose areas are underlain by thick cells, bearing many long microvilli that produce a lipid-containing secretion (Alberti and Norton, 1997). In A. longisetosus, the general body cuticle is highly porose, so no respiratory porose areas are clearly distinguishable. In the present study, secretory porose areas were found only on the infracapitulum of the gnathosoma (po.gen; Figs. 6c,d, 21e, 24d–g, 26a,g, and 29c).

Rostral Tectum The anterior dorsolateral border of the idiosoma in A. longisetosus projects as a simple duplication,

Fig. 5. Series of cross sections of Archegozetes longisetosus starting from anterior (TEM; compare Figs. 6 and 15) [‘‘cross’’ and ‘‘horizontal’’ in the heading of the figure legends refer to the specimen, not necessarily to the detail sectioned]. Scale bar in (a) refers to all figures: 10 lm. (a) Rutella with denticles (arrows). (b) Rutella (denticles indicated by arrows; one rutellum is broken), lateral lips, and rostral tectum (anteromost part consisting only of cuticle). Note flat part of spoon-like adoral setae or1. (c) Pedipalps, chelicerae (with teeth), and labrum are visible. Rostral tectum contains tissue, note difference in appearance and thickness of rostral/rostrophragmal cuticle. Note lateral lips with dorsal furrows and adoral setae. (d) Principal segment of chelicerae and movable digit. Note dorsal furrow in lateral lips (small arrows). Insertion of one of the adoral setae. (Rostral tectum not shown). (e) Rutella merged with malapophyses. Note oblique cuticular bars in malapophyses and small bars connected to bases of lateral lips (cf. Fig. 26a,b). The movable digits of the chelicerae deeply project into the principal segment. Labrum with lateral lamella (arrow). Preoral cavity completely surrounded by mouthparts and containing some food (arrowhead). a, anterior infracapitula seta; cha, posterior cheliceral seta; chb, anterior cheliceral seta; G, gena; Lb, cuticular bar associated with lateral lip; LL, lateral lips; lm, lamella on malapophysis; LS, labrum; MAL, malapophysis; Mb, cuticular bar in malapophysis; md, movable digit of chelicera; op0 , paraxial oncophysis of principal segment of chelicera; or1-or3, adoral setae 1–3; Pdp, pedipalp; pS, principal segment of chelicera; RO, rostrum; ro, rostral seta; rp, rostrophragma; RU, rutellum; t, teeth of cheliceral digits; Tg, Tra¨ga˚rdh’s organ; ti, inferior tendon of depressor muscle; ts, superior tendon of levator muscle.


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or fold of the sclerotized integument, forming the rostral tectum (Figs. 2, 3a–e, 4a, 5b–d, 6a,b, 8, 9a– c, 14, 15, and 16a–d). Unlike many oribatid mites, especially those with more heavily sclerotized cuticle, the tectum has no distinct solid, projecting

limb (cf. Hammen, 1968b) although the cuticle of the border is slightly thicker. Its dorsal wall (RO) is an extension of the PD (the dorsal anterior part of the idiosoma); its reflected ventral wall (rostrophragma, rp) reaches posteriorly to join the dorsal

Figure 6.



part (TG) of the cheliceral frame (Hammen 1968b, 1989). A precise delineation of the rostral tectum from more posterior cuticle is not possible, either dorsally or ventrally; therefore, we consider it to be imprecisely defined as the free cuticular flap that overhangs the gnathosoma. Anteriorly, the RO bears a pair of rostral setae (ro). The more posteriorly located prodorsal setae, the lamellar setae (le), the interlamellar setae (in), and the trichobothria (or sensilli, bothridial setae bo), insert posterior to the rostral tectum. All these setae have a solid cuticular shaft, that is, the trichogen cell has retracted leaving only a thin central strand of dense material (Figs. 16d–f and 17a,b). The simple setae ro, le, and in are barbed (Figs. 1, 2a,b,d,e, 4a, 14, and 17). They most likely represent simple mechanoreceptors inserted into a typical socket and connected to two dendrites, which terminate with tubular bodies (Tb; Figs. 16d,e and 17). The trichobothria are much more complex and resemble those of a distantly related oribatid mite, described by Alberti et al. (1994), but these are not considered further. The integument of the rostral tectum is not uniform (Figs. 5c,e, 6a,b, and 16c,d). The dorsal cuticle, the RO, is moderately sclerotized, anteriorly slightly folded (Figs. 2c–e and 16) and rather thick. Like the rest of the PD (Figs. 6c–f, 17, 18a– c,f, 22c,b, and 23), it is provided with numerous pore canals (pc; Fig. 16c–e,h). The ventral integument, that is, the rostrophragma (rp), bears only a very thin cuticle with indistinct pore canals. For both, the epidermis is thin (Fig. 16c,d). The space between the two (dorsal and ventral) integumental layers is occupied by hemolymph and includes also

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the nerves supplying the rostral setae. Anteriorly, the space between the two layers is divided medially by a very thin septum formed by extensions of the epidermal layers (Fig. 16c). In a restricted median region, probably in line with the septum, there is a peculiar rostral attachment site (ras) at which the two epidermal layers of RO and rostrophragma are connected (Figs. 15 and 16h). The cells of both layers resemble tendon cells at sites where muscles attach. They strongly interdigitate and are full of microtubules that stretch between the junctional complexes. However, muscles are not present in the rostral tectum (Figs. 5c,e, 6a–c, and 16c,d). Although there is no noticeable rostral limb (an exoskeleton plate consisting of cuticle only), the edge is reinforced by slightly reflecting dorsally to form a thicker, stronger cuticle (Figs. 2c–e, 5b,c, 8a–d, and 16a,b). Podocephalic Canal and Associated Glands The paired podocephalic canal system of A. longisetosus consists of the usual elements (see above). The canal itself (cpc) is a superficial, groove-like cuticular duct running more or less horizontally above the base of leg I (Figs. 3d, 6c–f, 9d, 10b,c, 18c,e, 19a,d, and 21a). It is overhung by a thin cuticular flap extending from its dorsal border. The duct extends from the first leg anteriorly toward the base of the infracapitulum. Here, the canal turns mediad and delivers the contents of the coxal glands (4pGL) and the three acinous glands (1-3pGL) onto the dorsal surface of the infracapitulum, that is, the cervix (or more precisely into the cheliceral grooves; see below; Fig. 3d). The coxal

Fig. 6. Continued series of cross sections of Archegozetes longisetosus from anterior to posterior (TEM; compare Figs. 7 and 15). Scale bar in (a) refers to all figures: 20 lm. (a) Malapophyses fused medially. Note rostral tectum extending lateroventrally. Movable digits ‘‘open’’ posterodorsally allowing tissues to enter. (b) Close to pedipalp articulation with the infracapitulum. Arrows indicate labiogenal line. Note small incision (inferior commissure) above the inferior comissural induration (compare Fig. 24j) and ventral folds of labrum (arrowheads; compare Figs. 21e, 24d,e, and 26a). (c) Shortly behind the mouth, the pharynx is formed showing the two superior commissures (Js, Js0 ). Note difference between dorsal and ventral pharyngeal cuticle. The ventral wall of the pharynx is fixed to the integument of the mentum. Rostral tectum has fused lateroventrally with the infracapitulum (see left side of figure). Note antiaxial infracapitular muscle, capitular saddle with strong cuticle separating cheliceral grooves, and vertical septum between chelicerae. The principal segment of the chelicerae is filled with intrinsic muscles comprising dorsal levator and ventral depressor muscles of the movable digit. Close to the bases of Tra¨ga˚rdh’s organs, the lamellated organs of the chelicerae are visible. Within rostral tectum first podocephalic gland appears. Note labral muscles. The strong cuticle of the cervix serves as origin site of the dorsal dilator muscles of the pharynx. The position of the base of supracoxal seta (e) is indicated (cf. Fig. 30f–h). (d) The vertical septum has ventrally reached the capitular saddle and thus the chelicerae are completely separated medially. The trochanter remnant of the chelicerae is sectioned. (e) Similar to d, but arrangement of pharynx dilator muscles more evident. Note infracapitular gland. (f) Within the trochanter remnants of the chelicerae intrinsic muscles are visible. The median retractors appear. The labral muscles attach posteriorly to the capitular apodeme which extends posteriorly into the body. The pharyngeal roof is lowered by transversal (depressor) muscles. Infracapitular gland (duct: dgi) is prominent. ant.m, antiaxial muscle of infracapitulum; acx, line of attachment of cheliceral sheath to chelicera (anterior border of apodemal part of cheliceral cuticle); ap.c, capitular apodeme; cha, posterior cheliceral seta (insertion); cpc, podocephalic canal; CX, cheliceral sheath; dep.m, depressor muscle of movable digit of chelicera; dg1, duct of first podocephalic gland; dgi, duct of infracapitular gland; dMu, dorsal dilator muscles of pharynx; e, supracoxal seta (insertion); G, gena; ici, inferior commissural induration; iGl, infracapitular gland; in.tr, intrinsic muscle of trochanter remnant of chelicera; Ji, inferior commissure of mouth; Js, Js0 , superior commissures of mouth and pharynx; k, condylar ridge (condyle) of infracapitulum; lam.m, muscle of lamellated organ; lam.org, lamellated organ of chelicera; le, lamellar seta; lev.m, levator muscles of movable digit of chelicera; Lm, labral muscle; lm, lamella on malapophysis; LS, labrum; MAL, malapophysis; md, movable digit of chelicera; mPdp, proximal muscles of pedipalp; opx, posterior oncophysis; PD, prodorsum; Pdp, pedipalp; 1pGL, first podocephalic gland; Ph, pharynx; po.gen, genal porose area; po.lc, laterocoxal porose area of infracapitulum; pS, principal segment of chelicera; RO, rostrum; rp, rostrophragma; se, capitular saddle; Tg, Tra¨ga˚rdh’s organ; ti, inferior tendon of depressor muscle; tMu, transversal depressor muscle of pharynx; Tr, trochanter remnant; ts, superior tendon of levator muscle; vS, vertical septum.


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gland consists of a proximal saccule, which continues into a (nephridial) tubule followed by a cuticlelined coxal gland duct, which opens into the podocephalic canal (Figs. 19a–c). The epithelium of the saccule consists of podocytes provided with numerous processes, pedicels, which are connected via slit membranes (Fig. 19a,c). The wall of the tubule is provided with cells showing structures typical of active transcellular transport, that is, mitochondria associated with infoldings of the basal plasmalemma thus forming a basal labyrinth. The epithelial cells (three in cross section) of the tubules are connected via peculiar junctional complexes, which are provided with thick electron-dense intracellular reinforcements (Fig. 19a,b). In addition to the products of the largely tubular coxal gland, each podocephalic canal also receives secretions from three acinous glands. These were studied here only to a limited extent. The anterior acinous gland is located under the anterior part of the PD extending even into the proximal parts of the rostral tectum (Figs. 6c–f, 9d, 10a–c, 11a,d, 15, 16e, 18f–h, and 19e–g). Its cytoplasm is dominated by rough endoplasmic reticulum. Small Golgi bodies are also present. The gland produces densely staining, likely protein-containing granules, which are extruded into a thin-walled duct provided with a proximal valve (Figs. 18f,g and 19e–g). Its duct (dg1) runs ventrad to join the podocephalic canal close to where it turns mediad (Figs. 10a, 11a,d, and 18d,e). The duct (dg2) of a second gland opens about halfway between the posterior end of the canal and the entrance of the first gland’s duct (Figs. 19d and 23a). The duct (dg3) of a third gland (Fig. 19a inset) opens close to the region where the coxal gland duct (dg4) meets the podocephalic canal. Ducts of all three acinous glands have a thin and slightly folded cuticular intima, showing a structure similar to a tracheal taenidium (Fig. 18f,g). In contrast, the cuticular terminal duct (dg4) of the coxal gland has a peculiar thick and largely electron-lucent cuticle (Fig. 19a,b). Fig. 7. Continued series of cross sections of Archegozetes longisetosus from anterior to posterior (TEM; compare Fig. 15). (a) Proximal region of mentum. Note retractor muscles of mentum inserting. Transition beween pharynx and esophagus. The synganglion appears. Note masses of muscles comprising dorsal and median retractors of chelicerae (retr.Ch). Part of the medial muscles attach to the prodorsum. Asterisk indicates modified cuticle in the pharynx floor. Scale bar: 20 lm. Inset: Insertion of mental retractor in higher magnification. Note modified cuticle (asterisk) of pharynx floor connected with cuticle of mentum via extensive junctional complexes (arrow) between epithelium of pharynx and that of mentum. Scale bar: 10 lm. (b) Slightly more posteriorly, the esophagus is located more dorsally and starts to pass through the synganglion. Scale bar: 20 lm. bo, trichobothrium (and its insertion); cpc, podocephalic canal; Es, esophagus; iGL, infracapitular gland; in, interlamellar seta in (insertion); LI, leg I; M, mentum; mnt, mentotectum; M.retr, retractor of mentum; PD, prodorsum; Ph, pharynx; retr. Ch, cheliceral retractors; SY, synganglion; tc, tendon cell.


Innervation of the Gnathosoma The gnathosoma is provided with a number of sensory elements, which include setal and nonsetal structures (see below). These and the various muscles are innervated by nerves arising from the synganglion. We were not able to trace these nerves completely. However, the following main nerves and nerve bundles could be distinguished, which branch into finer fibres anteriorly: A paired thick cheliceral nerve enters the principal segment and gives off branches to the lamellated organ and into the digits (Figs. 9d and 22b,d). An unpaired median nerve (min) runs into the infracapitulum underneath the cervix. It likely innervates the pharyngeal muscles (Figs. 9d, 11b–d, 15, 24h, and 25a). Two paired lateral nerve bundles run into


the LRs and MAs. One innervates the pedipalps, the other the sensory elements of the infracapitulum (Figs. 9d and 11c,d). Cheliceral Frame and Its Associated Structures The cheliceral frame of oribatid mites is the part of the body wall that flexibly connects the cheli-

Figure 8.

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cerae to the idiosoma (above) and infracapitulum (below). Hammen (1968b, 1989) named the largely dorsal the tegulum (TG), which anteriorly merges with the more rigid rostrophragma (rp; see above) and posteriorly joins the cheliceral sheaths (CX). As indicated above, we could not precisely determine the limits of these structures. The ventral (inner) wall of the rostral tectum, the rostrophragma, extends lateroventrally to reach the infracapitulum at about the region where the podocephalic canals (see above) turn mediad (Figs. 3d, 9d, and 10c). The TG forms a vertical septum (vS), which extends ventrally and connects with the capitular saddle (see below) separating the posterior parts of the chelicerae like a thin vertical plate (Figs. 6c,d, 9d, and 10a). A pair of small extrinsic muscles (m.retr) runs through this median fold (Figs. 6f, 7a,b, 10c, 13f,h, 14, 15, and 22b,c; Table 1) inserting likely at the anterior wall of the vertical septum. These muscles originate on the PD (Fig. 13f,h). In an anterior to posterior series of cross sections (Figs. 5–7 and 8–10), the posterior parts of the chelicerae become progressively more ensheathed and separated, starting with a ventral extension of the lateral parts of the tectum that finally meet and merge with the proximal infracapitulum (see Figs. 6c and 9d). From the TG (less likely the rostrophragma), a ventromedian ridge extends into a vertical septum (vS) that reaches between the main bodies of the chelicerae (Figs. 6c–d, 9d, and 10a). This septum finally merges with the capitular saddle (se) of the cervix, separating the chelicerae completely. The integuments of the chelicerae and the enclosing elements finally merge where the sheaths attach to the chelicerae (Figs. 6c,d, 18a–c, and 22a–c). The attachment line (acx) separates the external part of the cheliceral cuticle from the internal apodemal extension (ap; see below) (Figs. 6c–f, 9d, 10, 15, 18a–c,e,f, and 22b,c), and the border between these two regions

Fig. 8. Drawings depicting sequence of cross sections through gnathosoma of Archegozetes longisetosus from anterior to posterior (compare Figs. 9 and 15). Scale bar in a refers to all figures: 20 lm. (a) Anteromost part of rostral tectum, rutella and lateral lips. Note flattened distal parts of spoon-like first adoral setae or1. (b) Anterior part of rostrum, pedipalp of one side (only indicated), rutella and lateral lips. Note stalk part of spoon-like first adoral setae and furrow on lateral lips. (c) Chelicerae (fixed digits) begin in this section; note teeth of cheliceral digits. Adoral setae (or2 and or3) and anterior cheliceral setae (chb). (d) Note differences in cuticle of rostrum (dorsal part) and rostrophragma (ventral part) of rostral tectum. Chelicerae, shortly in front of articulation of movable digits, insertion of anterior cheliceral seta (chb). Note tooth on movable digit. Lateral lips with insertion of one of the adoral setae (or3). chb, anterior cheliceral seta; fd, fixed digit of chelicera; LL, lateral lips (with dorsal furrows); LS, labrum; or1-or3, adoral setae 1– 3; md, movable digit of chelicera; Pdp, pedipalp; pS, principal segment of chelicera; RO, rostrum; rp, rostrophragma; RU, rutellum.


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is distinct because of the abrupt disappearance of pore canals where the apodemal part begins. Cheliceral sheaths. Unless the chelicerae are not fully extended, these flexible, invertible sleeves are folded and seen as more or less ‘‘internally’’ directed duplications of the integument (see above for the continuation of the rostrophragma, etc.) that allow independent movement of the two chelicerae mainly in a longitudinal direction (i.e., protrusion

and retraction) and probably also to a lesser extent in a vertical or lateral plane. They are made of thin integument with indistinct pore canals (Figs. 3d, 18a–c, and 22a (inset),b,c). Although this is the generally described arrangement of cheliceral sheaths in Acari, in A. longisetosus it is hard to recognize, likely because of the development of the rostral tectum. In our preparations, we could clearly define the posterior border of a cheliceral sheath, that is, the

Figure 9.



line acx (see above), but we were not able to detect an anterior border, that is, the anterior edge of the inverted sleeve. It seems that the rostrophragma is continuous with the cheliceral sheath and may partly be able to fold (see Fig. 3a–c). The TG, located between the rostrophragma and the cheliceral sheath/cheliceral frame, similarly is not distinguishable in our materials. We hence have labeled those parts of the inverted (rostrophragma and its posterior continuation) cuticle as cheliceral sheath (CX) when it is close to the chelicerae (i.e., where the cuticles are parallel to each other and separated only by a narrow gap; Figs. 6c, 9d, and 10). Chelicerae. The paired chelicerae (Ch) have the chelate-dentate form found in the large majority of oribatid mites (Norton and Behan-Pelletier, 2009; Weigmann, 2010), that is, they are strong structures, which terminate distally with a large dorsal fixed digit (digitus fixus, fd) and a ventral movable digit (digitus mobilis or apotele, md), which together form a stout chela (Figs. 2b,e, 3a–e,h, 4c, and 15). The proximal part of the chelicera, on which the fixed digit is a distal extension, is termed here the principal segment (pS; also called basal segment or the ‘‘body’’ of the chelicera). It bears the usual two cheliceral setae, an anterior, short one (chb), positioned dorsally but slightly on the antiaxial side (Figs. 2e, 4b,c, 20a,b, and 23b) and a posterior long

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one (cha) placed paraxially (Figs. 2e, 3d, and 4c,g). Seta chb has an almost smooth surface, whereas cha is conspicuously barbed. They appear to be simple mechanoreceptors, being solid setae that are inserted in flexible sockets, and chb is innervated by two dendrites. However, the tubular bodies that indicate mechanosensitivity in arthropods were not found and must be very inconspicuous if present at all (Figs. 20a,b and 23b). Occasionally, a small cuticular tooth was seen on the paraxial side of the main body of the chelicera (Fig. 4c). The chelicerae do not possess slit sense organs (also called lyrifissures). The chelicerae are oriented in such a way that the digits move against each other in an almost vertical plane (Figs. 2b,e, 3a,c–e,h, 4b,c, 14, and 15). Each digit bears strong teeth that coapt with those on the opposite digit, ensuring a tight closure and firm grip (Fig. 4b). The cuticle of the digits is thick, heavily sclerotized and without pore canals (Fig. 20c–l). The procuticle of both digits is made of three layers, an outer dense layer (1), a median less dense layer (2), and an inner very dense layer (3). The latter maybe interrupted (Figs. 20c–l and 21a,f). In contrast, the remainder of the principal segment has a bilayered procuticle with numerous pore canals (Figs. 5e, 6a–d, 20a, 21a, 22a, and 23a,b). This porosity disappears posteriorly where the cheliceral sheath connects with

Fig. 9. Continued sequence of drawings depicting sequence of cross sections through gnathosoma of Archegozetes longisetosus from anterior to posterior (compare Figs. 10 and 15). In d, the main nerves of the gnathosoma are indicated. Scale bar in a refers to all figures: 20 lm. (a) Articulation of movable digits with principal segments of chelicerae. Note massive extension of movable digit into the principal segment. Note oncophysis (op0 ). Lamellae on malapophysis touch the movable digits ventrally. Posterior cheliceral setae (cha). Between labrum and chelicerae, Tra¨ga˚rdh’s organ is visible. Note that rutella are joined with their manubria to malapophyses. Malapophyses are separated medially, though lying close together. Arrow points to thin septum in rostral tectum. (b) Movable digits shortly in front of condyles (cf. Fig. 21). Note posterodorsal ‘‘opening’’ of movable digits allowing entrance of tissues. Each principal segment contains levator muscles attached to superior tendon. Note small bars in malapophyses and tissue belonging to secretory porose areae of genae. Arrow indicates thin septum in rostral tectum. (c) Inferior tendon of depressor muscle of movable digit is visible in one principal segment. Between infracapitulum and chelicerae, the posterior oncophysis (opx) is located. By joining the lateral borders of the labrum with the infracapitulum the mouth is formed. Note small ventral ridge (arrowhead) representing probably a remnant of a labium (cf. Fig. 24j). The infracapitulum is traversed by oblique cuticular bars of the malapophyses supporting the mouth region. They join with the tip of the mentum forming the inferior commissural induration (ici; compare Fig. 24j). Note thin ducts of infracapitular glands (dgi). At right, the duct is visible close to its opening antiaxially on the genal lamella. Palps join with the infracapitulum (left). Arrows indicate labiogenal line (articulation). (d) The lateral borders of the rostrum attach to the infracapitulum (left side). Here the podocphalic canal turns mediad. Note almost vertical muscles (antiaxial infracapitular muscles) connecting the rostrum/prodorsum with the condylar ridge (k) above podocephalic canal. Within the rostral tectum, cells of the anterior podocephalic glands (gland 1) are visible. The main gnathosomal nerves are indicated. Rostrophragma/cheliceral sheaths are partly joined (acx) to the wall of the principal segments of chelicerae. On the paraxial side of the principal segments, the peculiar lamellated organ is located close to the thick cheliceral nerve (compare Fig. 23a,d–f). Note beginning of infracapitular glands. The dorsal roof of the infracapitulum, the capitular saddle in particular, is strongly sclerotized (dark plates). Above the pharynx dilator muscles and one pair of strong labral muscles are visible. Roof and floor (asterisk) of pharynx have different cuticles. The two superior commissures of the mouth extending into the pharynx are evident. The ventral wall of the pharynx is fixed to the integument of the mentum. Arrows point to labiogenal line (no articulation is evident). acx, line of attachment of cheliceral sheath to chelicera (anterior border of apodemal part of cheliceral cuticle); ant.m, antiaxial muscles; ap, apodemal part of chelicerae; se, capitular saddle of cervix; cha, posterior cheliceral seta; Chn, cheliceral nerve; cpc, podocephalic canal; CX, cheliceral sheath; dep.m, depressor muscle of movable digit of chelicera; dg1, duct of first podocephalic gland; dgi, duct of infracapitular gland; dMu, dorsal (dilator) muscles of pharynx; e, supracoxal seta; G, gena (ventral cuticle of malapophysis); ici, tip of mentum (inferior commissural induration); iGL, infracapitular gland; Ji, inferior commissure; Js, Js0 , superior commissures of pharynx; k, condylar ridge; Lm, labral muscle; lm, lamellae on malapophysis; lam.m, muscle of lamellated organ; lam.org, lamellated organ of chelicera; Lb, cuticular bar associated with lateral lip; lev.m, levator muscle of movable digit of chelicera; lin, branches of lateral infracapitular nerve bundle; LS, labrum; MAL, malapophysis; Mb, cuticular bar in malapophysis; md, movable digit; min, median infracapitular nerve; Mo, mouth; op0 , paraxial oncophysis of principal segment of chelicera; opx, posterior oncophysis of chelicera; Pdp, pedipalp; 1pGL, first podocephalic gland; Ph, pharynx; ph.r, pharyngeal rod; Pn, pedipalpal nerve bundle; poc, preoral cavity; po.gen, porose area of gena; pS, principal segment of chelicera; RO, rostrum; ro, rostral seta ro (insertion); rp, rostrophragma; se, capitular saddle; Tg, Tra¨ga˚rdh’s organ; ti, inferior tendon of depressor muscle; ts, superior tendon of levator muscle; vS, vertical septum separating chelicerae medially.


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the chelicera (Figs. 6e,f, 9d, 10a–c, 18a–c, and 22a–b) and the apodemal part (ap) of the chelicera continues internally. From cross sections (Figs. 5c–

e, 8c,d, and 9a) and scanning electron micrographs (Figs. 2b,e, 3b,c, and 4b), it is evident that the anterior parts of the chelicerae are rather flat (later-

Figure 10.



ally compressed); only the posterior part of the principal segment has a more convex surface. The chelicerae are strongly innervated (Figs. 20, 21f,g, and 22b,d) by dendrites that extend into the digits. They enter the cuticle of the teeth and also the ventral cuticle of the movable digit where they terminate under tiny pores containing a dense material (Figs. 20d–j and 21f,g). The movable digit (md) extends into a ventral cavity of the principal segment (pS) with a dorsal arm of largely solid cuticle, on which the upper tendon inserts (Fig. 21a–c and 23b). Ventrally, the digit is ‘‘hollow,’’ containing the epidermal layer, nerves, and hemolymph, and it is this part of the digit that articulates with the principal segment (Figs. 21c–e and 24d). The condyles are regions of thick cuticle on both the movable digit and principal segment, connected by thin flexible cuticle (Figs. 11c and 21d,e). More precisely, each articulation is formed by two condyles provided by the principal segment, which fit into two sockets formed by the movable digit. The articulation is rather complex because of peculiar cuticular folds termed oncophyses (Figs. 5e, 6c,d, and 9a,c,d). These are extensions of different size and shape that externally cover the joint. In sections, it is evident that they are made of very flexible cuticle (very thin exocuticle and epicuticle). According to Hammen (1989), there are three oncophyses in another middle-derivative oribatid mite (Hermannia convexa): a ventral posterior one (opv), which we could not identify with certainty, a paraxial folded one (op0 ; Figs. 5e, 9a, 13e, 21a,c, and 28b) arising directly at the articulation (maybe this includes opv) and a further proximal and ventral (or coxal) oncophysis (opx; Figs. 6c,d, 9c,d, 21h, and 31e), which originates from the posterior border of the principal segment joining a peculiar short ‘‘trochanteral’’ region (see below), which connects to the cheliceral frame. The principal segment of each chelicera contains strong intrinsic muscle tissue (Table 1), which is of the cross-striated type, as are all muscles observed

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in the gnathosoma (and elsewhere in the mite). The muscles are differentiated into a small ventral depressor (dep.m) and a larger dorsal levator (lev.m; Figs. 6, 9b–d, 10a–c, 11d, 12a, 13d, 14, and 15) that insert on the movable digit via tendons [levator: superior tendon (ts): Figs. 6, 9, 10, 13d, and 21b,c; depressor: inferior tendon (ti): Figs. 9c and 31e]. For spatial orientation and functional morphology of the chelicera, see Heethoff and Norton (2009a). The levator muscle cells originate on the dorsoposterior walls of the principal segment (including the apodemal part, ap) to which they are connected by typical tendon cells. The depressor muscle cells originate on the ventrolateral walls of the apodemal part (Figs. 6, 9c,d, 10a–c, 12a, 13d, 18c,f, 22a–c, and 23a). The apodemal extension (ap) reaches rather deeply into the idiosoma starting from the line (acx) where the cheliceral sheath meets the principal segment (Figs. 9d, 10c, 18a–c, and 22a–c). The cuticle of this apodeme ‘‘opens’’ posteriorly allowing the entrance of hemolymph into the chelicera, as well as tissues such as the epithelial layers under the cuticle and the nerves that innervate the cheliceral digits, the cheliceral setae, and muscles (Figs. 6e,f, 10b,c, and 22). The trochanter remnant (Tr) is a small region of the chelicera, separated from the principal segment by cuticular indentations. This was interpreted as the trochanteral region by Hammen (1968b, 1989) and termed a trochanter remnant by Norton and Behan-Pelletier (2009); it is provided with nearly horizontally oriented intrinsic muscles (in.tr; Figs. 6f, 10c, 13e, and 23a,c; Table 1). Another muscle, connecting the trochanter remnant and the apodemal part, runs almost vertically (vmTr; Figs. 11b, 12a, 13e,f, 14, 15, and 25a; Table 1). The proximal oncophysis (opx; see above) starts from this region, as does Tra¨ga˚rdh’s organ (see below), both extending anteriorly (Figs. 5e, 6a–d, 9b–d, 10a, 15, 21a,e,h–j, 23a,b,d, 24c–f, 29c, and 31e). A small tooth (~) is present ventrally on the paraxial side of the principal segment, close to the base of Tra¨ga˚rdh’s organ (near a region of thin

Fig. 10. Continued sequence of drawings depicting sequence of cross sections through gnathosoma of Archegozetes longisetosus from anterior to posterior (compare Fig. 15). Scale bar in a refers to all figures: 20 lm. (a) The medial vertical septum of the rostrophragma/ tegulum has joined the capitular saddle. Ventrally in the chelicerae the trochanter remnants start. At left the posterior oncophysis (opx) fuses with that region. Note conspicuous lamellated organs. At left the duct of the first podocephalic gland is visible (dg1). Note sclerites in Tra¨ga˚rdh’s organs. Arrows indicate labiogenal line. (b) Close to podocephalic ducts (cpc) a small secretory laterocoxal porose area is located. The sclerite of the capitular saddle continues as the medial part of the capitular apodeme. The body of the infracapitular gland appears within the infracapitulum (left). (c) The apodemal parts of principal segments of chelicerae are evident. Note intrinsic muscles in trochanter remnants of chelicerae. The capitular apodeme serves as attachment site for the labral muscles. The infracapitular gland is conspicuous in the ventral part of the anterior idiosoma. At left the duct (dgi) of the infracapitular gland is starting, with a wide lumen (compare Fig. 31). Note dilator muscles of pharynx and muscles of the pedipalps. Dorsally, the posterior extensions of the anterior podocephalic glands are visible. ant.m, antiaxial muscles of infracapitulum; acx, line of attachment of cheliceral sheath to chelicera (anterior border of apodemal part of cheliceral cuticle); ap, apodemal part of cheliceral cuticle; ap.c, capitular apodeme; cpc, podocephalic canal; CX, cheliceral sheath; dep.m, depressor muscle of movable digit; dg1, duct of first podocephalic gland; dgi, duct of infracapitular gland; dMu, dorsal (dilator) muscles of pharynx; iGL, infracapitular gland; in.tr, intrinsic muscle of trochanter remnant of chelicera; k, condylar ridge; lam.m, muscle of lamellated organ; lam.org, lamellated organ of chelicera; le, lamellar seta; lev.m, levator muscle of movable digit; Lm, labral muscle; mPdp, proximal muscle of pedipalp; m.retr, median retractors inserting on anterior wall of vertical septum; opx, posterior oncophysis of chelicera; PD, prodorsum; 1pGL, first podocephalic gland; Ph, pharynx; ph.r, pharyngeal rods; po.gen, porose area of gena; po.lc, laterocoxal porose area of infracapitulum; Tg, Tra¨ga˚rdh’s organ; ti, inferior tendon of depressor muscle; tMu, transversal (depressor) muscle of pharynx; Tr, trochanter remnant; ts, superior tendon of levator muscle; vS, vertical septum.


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Fig. 11. Virtual sections through renditions of SR-lCT-data, as obtained in VGStudio Max 1.2, showing details of gnathosoma of Archegozetes longisetosus. (a) Lateral aspect (parasagittal section) with rostrum and prodorsum. Note cheliceral retractors (retr.Ch; for details see Fig. 13). Arrowheads indicate labiogenal line. (b) Sagittal section showing dilator muscles of the pharynx (dMu) and median infracapitular nerve (min). (c) Horizontal (frontal) section) with pedipalpal and lateral infracapitular nerve bundles. Arrowheads point to articulations of movable digits with principal segment of chelicerae. (d) Transversal section close to base of gnathosoma. a, anterior infracapitular seta; ant.m, antiaxial muscles; ap, apodemal part of chelicera; ap.c, capitular apodeme; bo, trichobothrium; Ch, chelicera; dep.m, depressor muscle of movable digit; dg1, duct of first (anterior) podocephalic gland; dMu, dorsal (dilator) muscles of pharynx; h, posterior infracapitular seta; ici, tip of mentum (inferior commissural induration); in, interlamellar seta in; in.tr, intrinsic muscles of trochanter remnant; k, condylar ridge; LI, leg I; le, lamellar seta; lin, lateral infracapitular nerve bundle; Lm, labral muscle; LR, large lateral ridge; M, mentum; md, movable digit; min, median infracapitular nerve; mnt, mentotectum; M.retr, retractor of mentum; m.retr, median retractors inserting on anterior wall of vertical septum; Mu, muscles in principal segment; 1pGL, first (anterior) podocephalic gland; Pdp, pedipalp; Ph, pharynx; ph.r, pharyngeal rods; Pn, pedipalpal nerve bundle; pS, principal segment of chelicera; retr.Ch, cheliceral retractors inserting on principal segment (for details see Figs. 12–15); rM, retractor muscle of infracapitulum inserting on capitular apodeme; RO, rostrum; ro, rostral seta; SY, synganglion; tM, transversal (depressor) muscles of pharynx; Tr, trochanter remnant; vmTr, vertical muscle in chelicerae.

cuticle; Fig. 28e). Slightly dorsal to this region the paraxial cuticle is thicker and sharply bent inward. In front of this area lies a peculiar lamelJournal of Morphology

lated structure, termed herein the lamellated organ (lam.org; Figs. 6c,d, 9d, 10a, and 23a,d–f). It is formed by a number of flat processes of neurons


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Fig. 12. SR-lCT data: virtual sections through the anterior body of Archegozetes longisetosus. (a) Parasagittal section through the gnathosoma showing some of the muscles. Note the retractor muscles of infracapitulum inserting on the capitular apodeme and of mentum originating on the endosternum. (b) Horizontal (frontal) section. Note retractor muscle of mentum and basal muscles of legs originating on the endosternum. (c) Cross section. Endosternum and muscles originating on it. ap, apodemal part of chelicera; ap.c, capitular apodeme; dep.m, depressor muscle of movable digit; d.retr.pS, dorsal retractor of chelicerae inserting on principal segment; dMu, dorsal (dilator) muscles of pharynx; EnS, endosternum; Es, esophagus; inf.retr.Ps, inferior retractor of chelicera inserting on principal segment; LI, base of leg I; lev.m, levator muscle of movable digit; M, mentum; Mb, cuticular bar in malapophysis; M.retr, retractor of mentum; PD, prodorsum; Pdp, pedipalp; 1pGl, first (anterior) podocephalic gland; Ph, pharynx; ph.r, pharyngeal rod; PrGL, preventricular gland (=granula rich diverticulum of the ventriculus); pS, principal segment of chelicera; rM, retractor of infracapitulum; retr. Tr, retractor of chelicera inserting on trochanter remnant; RO, rostrum; se, capitular saddle of cervix; vmTr, vertical muscle in chelicera.

separated by flat cells (i.e., modified epithelial cells or tendon cells) connected with the projections of a small muscle (lam.m). The muscle extends anteriorly and connects with the movable digit (likely via the superior tendon; Figs. 13e, 14, 15, and 23a,d). This cuticular area has a position close to that of the fenestrate area (fe1) in H. convexa, described by Hammen (1968b, 1989). Strong extrinsic muscles that move the whole chelicera (retraction and probably slight adjusting movements; see Hammen 1968b), here collectively called cheliceral retractors (retr.Ch), originate on the integument of the PD (Figs. 7, 11a, 12a, 13f,g, 14, 15, and 22a) and insert dorsally at the posteriolateral apodemal region (d.retr.pS; Figs. 13g, 14, 15, and 22a–c) or ventrally and medially on the apodemal region (inf.retr.pS; Fig. 13g, 14, and 15) or the trochanter remnant (retr.Tr; Figs. 12a and 13e,f). A further muscle (sup.retr.pS; Figs. 13g, 14, and 15) inserts dorsally and medially on the principal piece. The complete set of intrinsic and extrinsic muscles of the chelicerae is shown in Figure 13e–f (see also Table 1). Tra¨ga˚rdh’s organ. This is a thin, elongated, tapering, and distally acute extension (Tg) that lies closely parallel to the paraxial surface of each chelicera (Figs. 3b,c, 4c,g, 5e, 6a–d, 9b–d, 10a, 15,

21a,e,i,j, 23a,b,d, 24c–f, and 28e,f). It originates, like the more ventral proximal oncophysis (opx; see above), in the trochanteral region close to the modified cuticle connected to the lamellated organ. Over almost its entire length, it is a simple hollow tube of thin cuticle, much like that of the oncophyses. Only at its basal insertion some materials of cellular origin with lysosomal inclusions (retracted and degenerated epidermis?) maybe seen (Fig. 18a,d). Its paraxial wall is posteriorly provided with a thicker, likely sclerotized cuticle, which makes the structure slightly rigid and is responsible for the longitudinal ridge seen in SEM (Figs. 4g inset, 21e,i, and 24e). At its origin, the organ has some dense cuticular peculiarities that seem to strengthen the structure basally. Hammen (1968b, 1989) reported muscles attaching via tendons to thicker basal cuticle (sclerites) of Tra¨ga˚rdh’s organ in H. convexus, but we have seen no such insertions in that of A. longisetosus (Fig. 23a,d). Infracapitulum and Associated Structures The infracapitulum is a more or less coneshaped structure, which consists of the large LRs (Figs. 1b and 3g) representing the coxisternal regions of the pedipalps (Figs. 6c,d, 9d, 10a, 21e, Journal of Morphology

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G. ALBERTI ET AL.

Figure 13.



and 24d–i) where the trochanter of each pedipalp articulates (Figs. 2b–e, 3a,b,d,g, and 4c). The five free segments of the pedipalps are not considered further here. The large ridges border the medioventrally located mentum (M; Fig. 3g) and the mediodorsally located cervix (Figs. 14 and 15). The LRs extend (medially) beyond the pedipalpal trochanters by the MAs (likely endites of the pedipalps; Figs. 5e, 6a, and 9b). The ventrolateral surface of each MA, the gena (G), is thus also a paired structure (Figs. 3d,e,g and 25c). Anteriorly, both genae are separated medially. Each gena bears a RU considered to represent a hypertrophied seta (Figs. 1, 2c,e, 3a,d–h, and 4a–f). The small genal region on which the RU is situated is called the manubrium (MN; Figs. 1b and 24a,d). Each gena terminates anteriorly as a LL (Figs. 3d,e,g–i, and 4c,d), which border the preoral cavity (preoral groove, poc) ventrolaterally. The cavity is overhung dorsally by the LS (upper or superior lip), an unpaired structure, which is continuous posteriorly with the cervix (Figs. 3b,c, 4a–c,e,g–i, 14, and 15). The cervix thus is the short region from the base of the LS to the line of attachment of the cheliceral frame to the infracapitulum. Its surface is laterally continuous with the dorsal surfaces of the large ridges and MAs (e.g., Grandjean 1957a; Hammen 1980). Medially, the cervix forms an elevated ridge, the capitular saddle (se; Figs. 6c and 9d). The base of the LS demarcates the mouth (Mo; Figs. 9c and 15), which leads into the pharynx (Figs. 6, 9, 10, 14, and 15; e.g. Alberti et al., 2004). Between the cervical capitular saddle and the large ridge, there is a longitudinal depression on each side, the cheliceral groove, into which fit the ventral surface of the chelicerae (Figs. 6c and 7d). The cross-sectional shape of these structures continues onto the capitular apodeme (ap.c), posterior to the cheliceral frame (Figs. 6d–f and 7a,b; e.g., Grandjean, 1957a,b; Hammen, 1968b).

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Grandjean (1957a) developed a terminology describing different types of infracapitula of oribatid mites. An infracapitulum that has paired oblique ‘‘articulation lines’’ between mentum and genae (so-called labiogenal articulation) is of the stenarthric type. It has been suggested that the labiogenal articulation allows some movements of the RU during feeding (Evans 1992). Hammen (1989) considered the infracapitulum of A. magna to be stenarthric and A. longisetosus can be similarly classified, although the labiogenal articulations are indistinct (Fig. 3g), as described below. Labrum. The dorsal surface of the LS has several transverse rows of adjacent small denticles (Figs. 2c, 3b,c,f, 4a–c,g–i, 15, and 24a,b) that project anteriorly from small transverse, semicircular lamellae. At the tip of the LS, in a region sometimes termed the corona (Norton et al., 1996), the rows form a more intricate pattern (Fig. 4b,c,h,i). Ventrally, there are similar parallel transverse rows of denticles, but they are directed posteriorly (Figs. 4e,h, 24c, and 29c). All these denticles are solid protuberances of the cuticle (Figs. 24a,b and 28e). In cross sections, the LS shows an epidermal layer and a hemolymph space, but no nerves or muscles were seen. The cuticle is differentiated in a peculiar way, with apparently sclerotized areas and less sclerotized parts alternating, at least in the dorsal and lateral regions (Figs. 24b–d and 28c,e). The sclerotized structures of the labral cuticle probably represent the labral sclerite (sc.ls; e.g. Grandjean, 1958; Hammen, 1968b, 1989). A separate sclerite located deeper in the LS is not present. The LS continues proximally to meet and articulate with the cervix. The cervix overlaps the LS with a dorsal fold and a lateral fold, which fuse (Figs. 24e,f and 28a–c,f). At this basal region of the LS, two rather strong labral muscles (Lm) insert dorsally via tendon cells; these muscles originate on the proximal border of the capitular apo-

Fig. 13. Muscles of the gnathosoma of Archegozetes longisetosus renconstructed by amiraTM based on SR-lCT. For retractor muscles of mentum see Figures 11a, 12a,b, and 15. (a) Oblique posterior view into the gnathosoma and rostral tectum showing the antiaxial muscles inserting on a lateral condylar ridge (k) of the infracapitulum. Arrow indicates labiogenal line. (b) Sagittal section through part of the infracapitulum showing labrum, cervix, capitular apodeme and pharynx with associated muscles. (c) Ventral view of labrum, cervix and capitular apodeme and associated muscles. (d) Laterofrontal view of (transparent) chelicera showing intrinsic muscles of principal segment of chelicerae (except muscle of lamellated organ). (e) Lateral view of right chelicerae showing muscle of lamellated organ and muscles inserting on trochanter remnant. Principal segment rendered with transparency to observe lam.m. (f) Muscles associated with trochanter remnant (retr.Tr, vmTr) and median retractors (m.retr). (g) Cheliceral retractor muscles inserting on the principal segment of the chelicera. (h) The median retractors isolated inserting in a ventromedian region between the principal segments. ant.m, antiaxial muscles; ap.c, capitular apodeme; bo, bothridium of trichobothrium; dep.m, depressor muscle of movable digit; dj, dorsosejugal furrow; dMu, dorsal (dilator) muscles of pharynx; d.retr.pS, dorsal retractor muscles of chelicerae inserting on principal segment; ep, modified epithelia of floor of pharynx and mentum; Es, esophagus; fd, fixed digit of chelicerae; inf.retr.pS, inferior retractor muscle of chelicerae inserting on principal segment; in.tr, intrinsic muscle of trochanter remnant; k, condylar ridge; lam.m, muscle of lamellated organ; lev.m, levator muscle of movable digit; Lm, labral muscle; LR, large lateral ridge; LS, labrum; M, mentum; mCX, median parts of cheliceral sheath; md, movable digit; m.retr, median retractor muscles inserting on anterior wall of vertical septum; op0 , paraxial oncophysis of principal segment of chelicerae; PD, prodorsum; pS, principal segment of chelicera; retr.Tr, retractor muscle of chelicera inserting on trochanter remnant; rM, retractor muscle of infracapitulum inserting on capitular apodeme; RO, rostrum; se, capitular saddle of cervix; sup.retr.pS, superior retractor muscle of chelicera inserting on principal segment; ti, inferior tendon of depressor muscle; Tr, trochanter remnant; ts, superior tendon of levator muscle; vMu, ventral (dilator) muscles of pharynx; vmTr, vertical musle in chelicera inserting on trochanter remnant.


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Fig. 14. Virtual sagittal section of anterior part of the body of Archegozetes longisetosus, SR-lCT-data, as obtained in VGStudio Max 1.2 (cf. Figs. 1, 15). Scale bar: 50 lm. ap, apodemal part of cheliceral cuticle; ap.c, capitular apodeme; clI, claw of leg I; dj, dorsosejugal furrow; dep.m, depressor muscle of movable digit; dMu, dorsal (dilator) muscles of pharynx; d.retr.pS, dorsal retractor of chelicera inserting on principal segment; Es, esophagus; EnS, endosternite (with adjacent muscles); EV, esophageal valve; fd, fixed digit of chelicera; ici, tip of mentum (inferior commissural induration): inf.retr.pS; inferior retractor of chelicera inserting on principal segment; lam.m, muscle of lamellated organ; lev.m, levator muscle of movable digit; M, mentum; mnt, mentotectum; Mo, mouth; m.retr, median retractor muscles inserting on anterior wall of vertcal septum; PD, prodorsum; Ph, pharynx; PrGL, preventricular gland; retr.Tr, retractor of chelicera inserting on trochanter remnant; rp, rostrophragma; se, capitular saddle of cervix; sup.retr.pS; superior retractor of chelicera inserting on principal segement; SY, synganglion (partly shrunken); tMu, transversal (depressor) muscles of pharynx; Tr, trochanter remnant; ts, superior tendon of levator muscle; vmTr, vertical muscles in chelicera.

deme (ap.c; Figs. 11c,d, 13b,c, 15, and 28b–d; Table 1) and probably elevate and/or retract the LS (Figs. 15, 24g,h, and 28b–d,f). Alternating contraction of the labral muscles may also move the LS laterally. The sclerotized cuticle extends posteriorly in two lateral arms supporting the overlapping fold into which the LS is located proximally (Figs. 24f and 28b).Varying hemolymph/hydrostatic pressure may also assist in labral movements. Cervix and capitular apodeme. On the strong lateral cuticle of the cervix, and on its apodemal extension (ap.c; see below), originate 8–10 pairs of dorsal pharyngeal dilator muscles (dMu; Figs. 6c–f, 10, 11b,d, 12a, 13b, 14, 15, 24g,h, 25a, and 28a,b; Table 1). The more posterior muscles branch when extending toward the roof of the Journal of Morphology

pharynx. About 11 transversal depressor muscles (tMu) run horizontally across the roof of the pharynx alternating with the dilator muscles and their branches (Figs. 6f, 11b, 14, 15, and 24i; Table 1). In line with the transversal depressors, there are also ventral (dilator) muscles (vMu) that assist in moving the roof of the pharynx (Fig. 13b; Table 1; see also Alberti et al., 2003). In contrast with those of many other oribatid species (e.g. Grandjean 1957b; Norton et al., 1997), the cheliceral grooves are not provided with obvious porose areas. The capitular saddle (se) separating both grooves is the posterior continuation of the dorsal ridge of the LS and is reinforced by thick and rigid cuticle. The cuticle of the posterior border of the cervix extends into the anterior idiosoma and slightly branches into two lateral arm-like projections (Figs. 11b, 24g,h, and 28b–d), forming the capitular apodeme (ap.c; Grandjean 1957b; Hammen 1980, 1989). Retractor muscles (rM) insert on these arms via tendons (Figs. 11b, 12a, 13b,c, 15, and 28d) and may move the entire gnathosoma posteriorly likely in cooperation with the retractors inserting on the mentum (M.retr; see below); these muscles originate on the endosternum (Figs. 12a,b and 15; Table 1). The retractor muscles (rM) also may elevate the infracapitulum. At the posterior border of the cervix (the capitular epimeric furrow (Hammen, 1968b) or line of attachment of cheliceral frame to infracapitulum (Hammen, 1989)), the podocephalic canals (cpc) of both sides deliver their secretions into the cheliceral grooves (Figs. 6c and 9d; see above). Almost vertical antiaxial infracapitular muscles (ant.m, corresponding to ta of Hammen, 1989) run from the roof of the PD and attach to a small cuticular ridge close to the podocephalic canal (Figs. 6c,e,f, 10c, 11d, 13a, and 18e). The ridge probably represents the structure termed condyle k by Hammen (1968b, 1989). In A. longisetosus, it is not a distinct knob-like structure as it is in brachypyline oribatid mites. Hence, we use the term condylar ridge here. Ventrolateral of this ridge, the small, secretory laterocoxal porose area (po.lc), is located (Figs. 6e, 10b, and 18c,e). The capitular saddle increases in height posteriorly and finally merges with the medioventral septum (vS) of the cheliceral frame (see above). Lateral lips. These paired structures (LL) border the preoral cavity lateroventrally (Figs. 3d,e,g– i, 4c,d, 5b–d, 8a–d, 15, 26a, 29a, and 30). Apically each lip bears three adoral setae (or1, or2, and or3), which differ in shape (Figs. 3h,i and 4c,d). The most anteriorly positioned seta (or1) is spoonshaped and solid (Figs. 5b and 30e,f,h) and has an indistinct socket (Figs. 3h,i and 30f). The paired ‘‘spoons’’ are held horizontally and their distal expanded parts may overlap when the LLs are close together (Figs. 3h,i, 5b, 8a, and 30e). By contrast, the other adoral setae are normal, setiform, with more evident sockets (Figs. 3h,i and


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Fig. 15. Drawing depicting sagittal aspect of anterior part of body of Archegozetes longisetosus (based on SEM, SR-lCT, TEM; compare Figs. 14 and 5–10). Arrows with letters indicate position of cross sections shown in Figs. 8–10. Opening of infracapitular gland is visible when cuticle of lamella is considered transparent. Scale bar: 50 lm. acx, line of attachment of cheliceral sheath to chelicera (anterior border of apodemal part of cheliceral cuticle); ap, apodemal part of cheliceral cuticle; ap.c, capitular apodeme; chb, anterior cheliceral seta; bru, brush on rutellum; dj, dorsosejugal furrow; dMu, dorsal (dilator) muscles of pharynx; dep.m, depressor muscle of movable digit; d. retr.pS, dorsal retractor of chelicera inserting on principal segment; Es, esophagus; EnS, endosternite; EV, esophageal valve; fd, fixed digit of chelicera; ici, inferior commissural induration (tip of mentum); iGL, infracapitular gland; M, mentum; inferior retractor of chelicera inserting on principal segment; Mo, mouth; lev.m, levator muscle of movable digit; lam.m, muscle connnected to lamellated organ; lev.m, levator muscles of movable digit; LL, lateral lip; Lm, labral muscle; LS, labrum; md, movable digit of chelicera; min, median infracapitular nerve; m.retr., median retractor muscles inserting on anterior wall of vertical septum; ogi, orifice of infracapitular gland (lamella is considered transparent); or1-or3, adoral setae1–3; 1pGL, first podocephalic gland; Ph, pharynx; PrGL, preventricular gland; ras, rostral attachment site; retr.Tr, retractor of chelicera inserting on trochanter remnant; rM, retractor muscle of infracapitulum inserting on capitular apodeme; RO, rostrum; rp, rostrophragma; RU, rutellum; se, capitular saddle of cervix; sej, sejugal furrow; sup.retr.pS, superior retractor of chelicera inserting on principal segment; SY, synganglion; Tg, Tra¨ga˚rdh’s organ; tMu, transversal (depressor) muscles of pharynx; V, ventriculus (anterior part of midgut); vmTr: vertical muscle in chelicera.

30a,c,g,i,j), which are surrounded by peculiar dense cuticular material. All the adoral setae are innervated by two dendrites each (Fig. 30a,c,d,i,j), but tubular bodies were not seen. The dendrites of or2 and or3 enter into the hollow bases of the setae, but only for a short distance (Fig. 30g,i,j);

more distally the setae are solid (Fig. 30h). Each LL has a strong ventral cuticle that corresponds to the adoral sclerite (Hammen, 1989); the sclerite is provided with pore canals (Fig. 30f–i) and bears the adoral setae. Dorsally, the lip cuticle is thin and has a longitudinal furrow, which comes from Journal of Morphology

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Fig. 16. Rostral tectum with associated details of Archegozetes longisetosus (a–c, f–i: horizontal sections of specimen; d,e: cross sections). (a) Anterior detail showing rostral tectum and part of chelicerae, cross sections of posterior cheliceral setae (cha). Scale bar: 20 lm. (b) Detail showing anterior portion of rostral tectum consisting largely of rather thick cuticle. Scale bar: 2.5 lm. (c) Rostral tectum more posteriorly sectioned. Note dorsal thick cuticle of rostrum provided with many pore canals, ventral cuticle of rostrophragma being thin and pore canals not evident. An epidermal layer and a distinct hemolymph space, which is divided by a very fine vertical lamina (arrow), are present. Scale bar: 10 lm. (d) Base of rostral seta. The seta is massive and inserted into a socket allowing flexion due to suspension fibres. Scale bar: 10 lm. (e) Base of lamellar seta le inserted into a socket (like ro) on the prodorsum. The first podocephalic gland is present. Scale bar: 5 lm. (f) Detail from Figure 16c showing cross section of posterior cheliceral seta (cha) demonstrating its solid character. Scale bar: 2 lm. (g) Section of base of posterior seta (cha) showing its socket. Scale bar: 2.5 lm. (h) Rostral attachment site connecting the two epidermal layers of the rostral tectum (that of the dorsal rostrum and that of the ventral rostrophragma). Note numerous junctional complexes of interdigitating cells which contain numerous microtubules. Scale bar: 2.5 lm. cha, posterior cheliceral seta; Ep, epidermis; le, lamellar seta; N, nuclei; 1pGL, first podocephalic gland; pS, principal segment of chelicera; ras, rostral attachment site; RO, rostrum; ro, rostral seta; rp, rostrophragma; sf, suspension fibres; Tb, tubular body.

the denticle-rich mouth region (Figs. 4d,e, 26b, and 27a,d), runs anteriorly, and then turns around the apical border of the LL to its antiaxial side. The furrow is bordered by longitudinal rows of denticles. The inner (paraxial) row of denticles terminates slightly earlier than the outer (antiaxial) one (Figs. 4c,d, 15, 27a, 29a,b, and 30a,b,e–g). The furrow is paralleled laterally by a thin upright lamella (lm), which may touch the movable digit (md) of the chelicera (Figs. 5d,e, 6a,b, 8d, 9a–c, 15, 20j, 21a,e,f,g, 24d,e, 26b, 27a,d, 29a–c, and 30a,b,e–g). Large Lateral Ridges and Malapophyses. The supracoxal seta (e) inserts dorsolaterally on each LR, just behind the basal articulation of the pedipalp (Pdp). Each seta is innervated by a very small dendrite, which projects into a dense dendritic sheath. A tubular body was not observed (Figs. 1, 2e, 2a,b, and 31f–h). There are further cell processes containing microtubules. We could not determine whether these structures are also dendrites and/or extensions of glia or sheath cells. The LRs Journal of Morphology

contain the basal muscles of the pedipalps (Figs. 6c–f and 10). The palpal bases project anteriorly as the MAs (palpal endites), which terminate anterolaterally with free processes bearing the rutella (RU) and partly enclosing the medioventrally positioned LLs. The ventrolateral, sclerotized surfaces of the MAs (i.e., more specifically, the region posterior to the LLs and rutella) are termed genae (G; see above; Hammen, 1980; Fig. 3g). Rutella. The paired rutella (RU) are strong projections that parallel the much weaker and smaller LLs. At least the dorsal parts of the rutella may also partly coapt with the chelae of the chelicerae (Figs. 2c–e, 3a,d–h, 4a,b, 5a–d, 8, 14, and 15). According to the terminology developed by Grandjean (1957a), the RU of A. longisetosus is of the atelobasic type, in which the bases of the paired rutella are narrow and do not meet medially. Thus, the LLs are visible from the ventral side (Fig. 3d,e,g–i). The RU of A. longisetosus is strongly sclerotized and has several strong, sharp teeth anteriorly (Figs. 2c,e, 3d–h, and 4b–d). Proxi-


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Fig. 17. Lamellar seta le located on prodorsum (horizontal sections). (a) Longitudinal section of the barbed setal shaft and socket. Note that the shaft is solid. Scale bar: 5 lm. (b) Socket of seta. Note typical structures of a mechanosensillum: flexible socket and innervation by (in this case two) dendrites ending with tubular bodies. The cuticle is covered by a poorly developed cerotegument (secretion layer). Scale bar: 2 lm. Inset: One tubular body at higher magnification. The many microtubules (neurotubules) are evident. The tubular body is surrounded by a dense layer composed of semicircular structures produced from the sheath cells. Scale bar: 0.5 lm. Ce, cerotegument (secretion layer); ec, epicuticle; Ep, epidermis; le, lamellar seta; pc, pore canal; prc, procuticle; sf, suspension fibres; Shc, sheath cell; Tb, tubular body.

mally, it contains some cellular elements (Figs. 8, 5b–d, 26a,b, and 27a–c), but no sensory elements or nerves were detected. The procuticle of the RU lacks pore canals and mostly shows three layers (compare digits of chelicerae; Fig. 20d–i): a dense external layer (1), a thick median layer of low electron density (2), and a thin dense inner layer that can be interrupted (3). The teeth apparently are composed only from the external dense cuticle (Figs. 26a–c). On the inner (medial) side of the RU are two rows of small denticles, one dorsal and one ventral, that are mainly oriented longitudinally. Proximally, the rows are connected by an indistinct vertical row (Fig. 4f). The denticles can point in various directions, indicating that they are somewhat flexible (Figs. 2f, 4a–d,f, and 26b,c,d). The dorsal row is most conspicuous and has been termed the rutellar brush (bru; Hammen, 1968b). Its denticles are directed predominantly ventrally and the row runs a short distance around the anterior margin of the RU (Fig. 4c,d,f). Bacteria have been found at the base of the denticles (Fig. 26d). The base of the RU is called the collum (c; Grandjean, 1957a; Hammen, 1989). It is characterized by

the proximal end of the modified cuticle of the RU (mainly by the disappearance of layer 2). Malapophyses. Anteriorly, the MAs are more or less horizontally oriented. Here, they are paired structures, being completely separated until immediately in front of the mouth, where the medial borders of the genae meet the anterior tip of the mentum (Figs. 3d,e,g, 5e, and 9a,b). More posteriorly each MA starts to form a trough that may be bordered dorsally by the LS, when the latter is lowered (Figs. 5e, 6a,b, 9a,b, 21e, and 24d–f). The inner walls (directed toward the preoral cavity, poc) of the MAs are provided with numerous small denticles that project posteriorly (toward the mouth, Mo; Figs. 4e, 15, 26b, 27a,d, and 29c). From here on, the MAs are ventrally separated by the unpaired mentum (M). In oribatid mites with a stenarthric infracapitulum, the border between MAs and mentum is usually unsclerotized and represents the so-called labiogenal articulation. However, in A. longisetosus, this border is simply formed as a slight superficial ridge and shows no cuticular modifications that would indicate a functional articulation (Figs. 3g, 6b–d, 9c,d, 10a, and Journal of Morphology

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Fig. 18. Some details of prodorsum and proximal parts of gnathosoma reaching into the idiosoma (a,b,d,f–h: horizontal sections; c,e: cross sections). (a) Basal parts of chelicerae with end of cheliceral sheaths (acx). Proximally (internally) from here, the cheliceral cuticle (apodemal part) is without pore canals. Note median retractor muscles. Scale bar: 50 lm. (b) Detail showing end of cheliceral sheath (acx) and cross section through duct of first podocephalic gland. The antiaxial muscles attach to integument of prodorsum. Scale bar: 10 lm. (c) The antiaxial muscles connecting prodorsal integument and condylar ridge (k). Note cheliceral sheath and duct of anterior podocephalic gland. The podocephalic canal is an open furrow covered by a dorsal cuticular lid (see also Figs. 18e and 19d). Scale bar: 20lm. (d) Detail of Figure 18b showing muscle attachment site at prodorsum. Note numerous microtubules in epidermal cell modified as tendon cell. Scale bar: 0.1 lm. (e) Podocephalic canal close to the condylar ridge (k) where the vertical antiaxial infracapitular muscles insert (see Fig. 18c). The duct of first podocephalic gland is approaching the podocephalic canal into which it will open. Scale bar: 5 lm. (f) The first podocephalic gland containing dense secretory granules opens into its duct. Scale bar: 10 lm. (g) Detail of the duct showing its cuticular lining shaped as a taenidium like in tracheae. Scale bar: 0.5 lm. (h) Detail of the proximal beginning of the duct of the first podocephalic gland. Note valve-like structure (arrows) provided by cuticular projections. Apodemal part of cheliceral cuticle without pore canals. Scale bar: 1 lm. acx, posterior border of cheliceral sheath; ant.m, antiaxial muscle; ap, apodemal part of cheliceral cuticle; cpc, podocephalic canal; Cu, cuticle; CX, cheliceral sheath; dg1, duct of first podocephalic gland; ep, epithelium (partly retracted); ju, junctions between muscle cell and tendon cell; k, condylar ridge; m.retr, median retractor muscles inserting on anterior wall of vertical septum; Mt, microtubules; Mu, muscles; 1pGL, anterior podocephalic gland; PD, prodorsum; po.lc, laterocoxal porose area of infracapitulum.

24d–f). Hence, we prefer the term labiogenal line, with respect to this species. Following the structure from anterior to posterior, the bases of the rutella merge with the apical parts of the MAs (Figs. 5e, 9a,b, 26a,b, 27, and 29a,b). For some distance, only the cuticles merge, forming a distinct oblique plate. This plate (or MA Journal of Morphology

bar, Mb) becomes reduced from the ventral side (Figs. 5e, 6a, 9a,b, and 21e), thus providing an opening between the basal part of the MA and the RU through which epithelial tissue and hemolymph can enter the RU. A small nerve was seen lateral to the MA bar that probably is connected to the manubrial fissure af (Fig. 29c,d).


The sclerite of each LL continues posteriorly into a dorsal LL bar (Lb), which extends for a short distance posteriorly into the respective MA (Figs. 26b, 27a,d, and 29b). A thin lamella (lm) arises dorsally above the bar, which may touch the movable cheliceral digit (md) ventrally. At this area of contact, a dendrite was seen to penetrate the inner layers of the cuticle of the movable digit (see above and Fig. 21f,g). The lamella is the posterior continuation of the lamella seen on the corresponding LL (see above). It proximally runs more laterally with regard to the movable digit (Figs. 9a,b and 29c). Immediately in front of the mouth (Mo), the inner walls of the MAs are provided with small denticles directed toward the mouth (Figs. 4e, 26b, 27a,d, and 29c) and the lamellae increase in height. Each gena bears the anterior infracapitular seta a (genal seta) (Fig. 3d,e,g), which is positioned close behind the manubrium on the gena, and the minute median infracapitular seta (m). Both are probably simple mechanoreceptors. Figure 26a,e–g shows sections of seta a indicating its solid structure and the insertion in a typical socket with at least one prominent tubular body (the innervation of seta m has not yet been observed). The manubrium is bordered anteriorly by the collum (c; Figs. 26a,b and 27a,b,d). The posterior boundary is marked by a small manubrial fissure (af), which indents the cuticle from the interior (Fig. 26b and 27a). A small nervous element, likely a dendrite, enters this fissure. It likely comes from a small nerve found at the base of the manubrium (Fig. 27).The ventrolateral cuticle of each gena, including the manubrium, is provided with many pore canals (Figs. 21e, 24d–h, and 26a,g). Posterior to the manubrium, this is underlain by a conspicuous secretory epithelium provided with many long microvilli and producing numerous lipid droplets. We call this the genal porose area (po.gen), and this is the first report of it from oribatid mites (cf. Hammen, 1968b, 1989; Alberti and Norton, 1997; Norton et al., 1997). The pores of the manubrium are less conspicuous (only evident on the lateroventral side) and a secretory tissue was not obvious, although a small area with long microvilli was seen. Preoral cavity and mouth. Because of the reduction of the ventral lip, or labium (but see below), the preoral cavity (poc) theoretically has a triangular shape, but it is only vaguely evident in our sections. This is mainly the consequence of the ventral indendation of the LS (Figs. 5c–e, 6a,b, 9a–c, 21e, and 24a–e), which gives the cavity a more or less oval cross section. Furthermore, because the labium is lost (or at least much reduced; see below), the ventral floor of the cavity is formed by the LLs and the MAs, which are almost horizontally oriented. Anteriorly, the lateral borders of the preoral cavity are largely formed by

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the chelicerae (Ch) and rutella (RU). More posteriorly, close to the mouth, it is the inner surfaces of the MAs that contribute to the wall of the cavity. As described above, these various parts forming the cavity wall are provided with many small denticles directed posteriorly toward the mouth. The MAs remain separate structures almost back to the mouth (see above). Shortly in front of the mouth, the inner walls of the MAs and the anterior tip of the mentum (M) merge. In cross section, a small unpaired structure is visible filling the gap between the malapophyes, which is bordered by tiny longitudinal furrows (Fig. 24d–f,j). The cuticle of the mentum in this anterior region is tight and almost without pore canals (Fig. 24d–f), whereas that of the paired genae (G), lateral to the mentum, is strongly porose. Glandular tissue typical of secretory porose areas is located underneath this region (po.gen; see above). The mouth is dorsally formed by the fusion of the lamellae (lm) on the MAs with the distal folds of the cervix into which the LS is positioned (Fig. 24d–f). The ventral wall of the LS has a thicker cuticle in this region, which projects a little anteriorly and laterally (Figs. 6b, 9c, 21e, 24d,e, and 26a). This thick cuticle continues posteriorly as the dorsal wall of the pharynx (Figs. 24f). Anteriorly, the mouth has a peculiar shape in cross section, defined by its commissures (Fig. 24d–f). There are two conspicuous dorsal commissures (Js, Js0 ) as expected (see above). In addition, for a short distance, there are also two ventral commissures (Ji, Ji0 ; Figs. 9c, 21e, and 24d–f,j). However, moving posteriorly these ventral commissures quickly disappear, leaving the pharynx with the typical crescent shape (in the constricted state) known from most actinotrichid mites (Figs. 6c–f, 9c,d, 10, and 24g–i; Alberti and Coons, 1999; Alberti et al., 2003; Alberti, 2006). This region is reinforced by a strong cuticle (the MA bar, Mb) running obliquely on the oral side of each MA, from the cheliceral groove to the cuticle (Figs. 9c and 24e,f). The paired cuticular bars connect with the tip of the mentum (and/or the anterior cuticle of the labiogenal line) to form the ventromedially located inferior commissural induration (ici; Hammen, 1968b, 1989). This cuticular structure continues a short distance posteriorly, keeping the pharynx cuticle directly connected to the ventral cuticular wall of the infracapitulum (Figs. 9c, 10, and 24e–f). For further details of the pharynx, see Alberti et al. (2003). Mentum. The mentum (M) is the unpaired proximal and ventral region located between the large LRs (e.g., the articulation sites of the pedipalps), the MAs (with genae), and the articulation with the idiosoma (propodosoma). As defined by the labiogenal line, separating it from the LRs and MAs, the mentum has an almost triangular shape (Fig. 3g) with its tip pointing anteriorly (see above). Journal of Morphology

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Anteriorly, the cuticle of the mentum lacks pore canals (see above and Fig. 24d–f). It bears a pair of mental setae (h), which are provided with prom-

inent tubular bodies (Fig. 29e,g) and likely are simple mechanoreceptors. The ventral wall (floor) of the pharynx has a thick modified cuticle, which

Figure 19.



is quite electron-lucent (Fig. 6c–f, 9b, 10, and 24f– h). This lucent cuticle is paralleled by two distinct, electron-dense rods, termed here pharyngeal rods (ph.r; Fig. 25). These rods seem to start from the region of the inferior commissural induration (Fig. 24f) and in fact represent continuations of the MAs’ bars (Fig. 25a,c). They become thinner posteriorly and disappear close to the beginning of the esophagus (Fig. 25). For some distance, this peculiar cuticular pharyngeal floor is fixed to the median cuticle of the mentum, through modified epithelial cells (resembling tendon cells) provided by both layers (epithelium of pharynx and epithelium of mentum). More laterally the integument of the mentum serves as origin of the ventral muscles that probably are involved in dilating the pharynx (Fig. 13b; see also Alberti et al., 2003). This region of the infracapitulum further includes part of the paired iGL (iGL; see below). On the posteriolateral borders of the mentum, a pair of muscles (M.retr; Figs. 7, 11a,b, 12a,b, and 15) inserts, which may cooperate with the retractors (rM) inserting on the capitular apodeme to retract the infracapitulum, but they also may serve to lower the infracapitulum, as antagonists of the retractor muscles inserting on the infracapitular apodeme (Fig. 7). These retractors of the mentum (M.retr; Fig. 7) originate on the endosternum. Infracapitular gland. The paired iGLs, frequently called salivary glands, are located in the infracapitulum, where they parallel the pharynx (Figs. 6e,f, 10b,c, 15, 24h–i, and 26a). They are composed of a few large cells that extend posteriorly until they meet the synganglion (SY). Each cell contains many electron-lucent secretory granules that are formed from rough endoplasmic reticulum and small Golgi bodies. The nuclei are round and contain small patches of heterochromatin (Fig. 31a,b). Hence, these cells appear to be rather active. The granules are extruded in the merocrine way at an apical pole provided with few microvilli into a common space from which a cuticular duct starts (Fig. 31c). The duct of each gland soon becomes very thin and undulating, so that a single

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duct maybe cut several times in one section. The ducts open immediately in front of the mouth, lateral to the previously described lamellae (Figs. 21e, 24d–f, and 31e). DISCUSSION Our observations on the gnathosoma of A. longisetosus generally corroborate knowledge previously gained from light microscopic or limited scanning observations. Together with our previous articles on the digestive tract (Alberti et al., 2003; Heethoff et al., 2008; Heethoff and Norton 2009a,b), the nutritional system of this model oribatid mite is now rather fully described and analyzed, and this strong foundation should significantly aid more comprehensive functional and comparative studies. In the following, we discuss the main components under comparative and functional contexts. Cuticular Structures and Properties The integument and in particular the cuticle is much modified in the various parts of the gnathosoma and anterior body. Most conspicuous are the highly structured cuticles around the preoral cavity. The quite unusual sequence of layers (electron lucent and dense layers) likely give these areas (LLs, LS, oncophyses, Tra¨ga˚rdh’s organ) cushionlike properties, which might help to seal the region when sucking forces created by the pharyngeal pump need to be optimal for food intake (see also below). Another peculiar cuticle is found in the cheliceral digits and the rutella, where a middle layer (layer 2) is less electron-dense than the inner and outer layers. This layer likely is responsible for the birefringence of these structures. Birefringence of certain cuticular components is characteristic, and the source of the name, of actinotrichid mites (e.g., Grandjean, 1936, 1969; Zachvatkin, 1952; Evans et al., 1961). In Anactinotrichida birefringence is exceptional and only known in certain setae on the pretarsi of Opilioacarus (Grandjean 1936). In Oribatida, birefringence is found in all

Fig. 19. Sections of podocephalic system (a,e,g: cross sections; b–d,f: horizontal sections). (a) Podocephalic canal close to its posterior beginning with duct of fourth podocephalic gland (coxal gland 5 nephridium) close to its opening into the podocephalic canal. Note tubule of fourth podocephalic gland (coxal gland) and its sacculus. The sacculus cells (podocytes) contain large, dense inclusions. Scale bar: 10 lm. Inset: Proximal end of podocephalic canal with cuticular ducts of third and fourth podocephalic glands. Scale bar: 2 lm. (b) Tubule of coxal gland and nearby coxal gland duct. Note thick and mostly electron-lucent cuticle of the duct. The coxal gland tubule is composed of three cells in cross section which are connected by conspicuous junctional complexes (asterisks). Note numerous mitochondria between basal infoldings of plasmalemma (basal labyrinth). Scale bar: 5 lm. (c) Basal part of coxal gland tubule showing details of basal labyrinth and podocyte layer of sacculus comprising many pedicels (arrowheads) connected via slit membranes. Scale bar: 0.5 lm. (d) Podocephalic canal more distally with duct of second podocephalic gland approaching. Scale bar: 2 lm. (e) Anterior/first (acinous) podocephalic gland with its duct. The gland is characterized by many dense inclusions. Scale bar: 2 lm. (f) Extrusion pole of first podocephalic gland. Scale bar: 1 lm. (g) Detail of first podocephalic gland showing small Golgi body and rough endoplasmic reticulum and the dense secretion granules it produced. Scale bar: 1 lm. ap, apodemal part of cheliceral cuticle; BL, basal lamina (of tubule and sacculus epithelia); bL, basal labyrinth; cpc, podocephalic canal; dg1–dg4, ducts of podocephalic glands 1–4; Gb, Golgi body; Lu, lumen; Mi, mitochondrium; Mu, muscle; Mv, microvilli; N, nucleus; 1pGL, first podocephalic gland; 4pGL, fourth podocephalic gland (tubular part of coxal gland); rER, rough endoplasmic reticulum; S, sacculus of coxal gland; Se, secretion.


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Figure 20.



setiform organs except solenidia, and in the cheliceral digits and rutella. A structurally similar cuticular material was also seen in the setae in our sections but is absent from the cuticle of other regions. Hence we come to the same conclusion as Walzl (1987) with regard to layer 2 of the cheliceral digits and rutella as the birefringent layer. On the basis of the presence of birefringence, Grandjean (1947) concluded that the rutella of Oribatida are modified setae and that the cheliceral digits of Actinotrichida evolved from a complex of setae (Grandjean 1957a; see also Norton, 1998). Although the rutella indeed seem to be hypertrophied setae (they replace the ‘‘normal’’ setae of species lacking rutella), a similar origin for cheliceral digits is less convincing. Such chelae are a constitutive character of Chelicerata, and it seems unlikely that they should have evolved separately in Acari or Actinotrichida. Further cuticular properties are discussed below. Chelicerae, Cheliceral Frame In Actinotrichida, chelicerae are usually composed of two obvious parts, the principal segment projecting with the fixed digit and the movable digit or apotele (e.g., Vitzthum, 1940/43; Snodgrass, 1948; Hammen, 1989; Evans, 1992; Alberti and Coons, 1999; Krantz and Walter, 2009). Another more basal segment is prominent in Anactinotrichida, its presence in actinotrichid mites seems highly variable and is often unconfirmed. Among oribatid mites, one sees it as a distinct trochanter only in basal taxa, such as Palaeosomata (Grandjean, 1954b). In most oribatid species the basal segment has been considered to be represented by a ventral, reduced element, interpreted as a trochanteral region by Hammen (1989) and termed the trochanter remnant by Norton and Behan-Pelletier (2009). Still, light microscopy of the cuticle has been inconclusive about the segmental nature of this structure. Our study corroborates these earlier assumptions by finding that the basal segment is truly present and distinctly

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articulates with the principal segment, and that it contains intrinsic muscles, seen for the first time. Hence, the chelicera includes three segments (articles) in total with the most proximal (the trochanter remnant) being much reduced. Norton and Behan-Pelletier (2009; these authors did not count the apotele as a segment, thus reported two, not three segments in the chelicera) suggested that the reduction of the trochanter may correlate with a reorientation of the gnathosoma/chelicerae function from nearly vertical to nearly horizontal. Hammen (1968b, 1989) considered the flexible cheliceral sheaths to represent the coxal region of the chelicerae, which connects them to the cheliceral frame in such a way that the chelicerae can be protruded and retracted; this capability is certainly a derived condition. The fact that we could not discriminate distinct borders between cheliceral sheaths and cheliceral frame is likely a consequence of the presence of the rostral tectum, which has evidently incorporated the cheliceral frame. An indication of the latter maybe the presence of the vertical septum, which separates the two chelicerae proximally and maybe interpreted as the narrow sternal region of the cheliceral segment (Hammen, 1989). Consequently, the dorsal region of this septum indicates the area of the TG.

Sensory Elements This study is the first to examine nearly the full array of sensory structures on an oribatid mite gnathosoma (excluding those of the pedipalps and seta m) using electron microscopy. Remarkably, there seem to be no typical chemoreceptive setiform sensilla. Evidently, the task of preoral chemosensing of potential food is done mainly by special sensilla on the pedipalpal tarsus, which include solenidia (probably olfactory sensilla) and eupathidia (probably gustatory sensilla). Such sensilla have been found whenever this segment has been examined (e.g., Grandjean, 1935; Alberti and Coons, 1999).

Fig. 20. Details of chelicerae (a,b,j–l: cross sections; c–i: horizontal sections). (a) Principal segment of chelicera with socket of anterior cheliceral seta. Note ciliary segments of two dendrites (arrow) innervating the setal base. Scale bar: 2 lm. (b) The two receptor processes (ciliary segments) of seta chb in higher magnification. Scale bar: 0.5 lm. (c) Anterior part of chelicera. The section passes through fixed and movable digit. Note nervous structures in the fixed digit (arrow; compare Fig. 20f). Note oncophysis op0 made of cuticle only. Scale bar: 5 lm. (d) Movable digit of chelicera. Note cuticle comprised of three different layers (1–3; 1 includes epicuticle which is not discernable). Nervous tissue within the basal part of the digit. Dendrites penetrate into the cuticle of the teeth of the chela (arrows; compare Fig. 20e,g,h–j). Scale bar: 5 lm. (e) Dendritic processes (asterisk) within the electron-lucent cuticular layer (2) of the chela and dense material under a pore (arrowhead). Scale bar: 0.5 lm. (f) Detail of fixed digit showing nervous structures (arrows; compare Fig. 20c). Scale bar: 0.5 lm. (g) Cross section of a tooth showing the dendrite (asterisk) and dense material (arrowhead) in the peripheral dense layer (1). Scale bar: 1 lm. (h) Detail of Figure 20g (asterisk: dendrite; arrowhead: dense material). Scale bar: 0.25 lm. (i) Cheliceral digit showing three dendrites (arrows), one approaching the peripheral cuticular layer (arrow with asterisk). Scale bar: 0.5 lm. (j) Detail of movable digit with pore (arrow). Arrowhead indicates dense material, asterisk marks dendrites. Scale bar: 0.5 lm. (k) Detail of movable digit showing small nerve with three dendrites (asterisks) and microvilli from sheath cell (compare Fig. 20l). Scale bar: 0.5 lm. (l) Movable digit showing nervous elements (dendrites, sheath cells with microvilli). Arrow points to nervous element shown in higher magnification in Figure 20k. Scale bar: 2 lm. 1–3, layers 1–3 of cuticle (cf. Fig. 20d); fd, fixed digit of chelicera; lm, lamella on malapophysis; LS, labrum; md, movable digit; ne, nervous tissue; op0 , paraxial oncophysis of principal segment of chelicera; pc, pore canal; ps, principal segment of chelicera; sf, suspension fibres; Shc, sheath cell.


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Typical mechanoreceptive setae on the PD and gnathosoma were identified by their tubular bodies, which indicate this function in other arthropod sensilla (e.g., Altner, 1977; Thurm, 1984; Barth, 2002; Alberti and Coons, 1999; Coons and Alberti, 1999). These were detected in the prodorsal lamellar seta (le), the anterior infracapitular

seta (a), and the posterior infracapitular seta (h). It seems likely that the rostral seta (ro), interlamellar seta (in), and the middle infracapitular seta (m) are also mechanoreceptive sensilla because of their general similarity to setae le, a, and h. The paired adoral setae, however, are remarkably different, as none of the three appears to have tubu-

Figure 21.



lar bodies. This contrasts with the innervation of adoral setae of Tenuipalpidae (Prostigmata), which evidently show tubular bodies (Nuzzaci and de Lillo, 1989). The anterior seta (or1) of A. longisetosus differs strikingly from the other two with respect to its external shape (spoon-like) and lack of the distinct and peculiar socket found in or2 and or3. All three setae are provided with two dendrites, which evidently enter the ‘‘hollow’’ bases of the two posterior setae. The distal parts of all three setae are solid and do not contain sensory elements; hence, their function is unknown. The same is true of the supracoxal seta (e), which is innervated by at least one small dendrite, but again no tubular body was found. The nature of adjacent microtubules containing cell processes could not be clarified. These unusual setae might represent hygroreceptors, which in insects lack pores and include short dendritic processes. In insects such setae also maybe associated with a flattened dendrite, which is thought to represent a thermoreceptor (Steinbrecht, 1998), but such a dendrite was not seen in the mite setae. In any case, the function of the adoral setae and the supracoxal setae in A. longisetosus remains enigmatic. The setae located on the principal segment of the chelicerae also remain enigmatic to some degree. The posterior seta (cha) seems to be a simple mechanoreceptive sensillum, as maybe concluded from its similarity with other such setae, for example, on the PD. However, the anterior seta (chb) has a different external structure, and its basal innervation by two dendrites that evidently lack tubular bodies is peculiar. Sensory structures in the oribatid chelicera, other than the mentioned setae, had previously been detected in an oribatid mite by Walzl (1987), who also described pits on the teeth, which he considered to be located above the dendritic terminations. Thus, he suggested a gustatory function of these structures. Such dendritic processes running

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into the cheliceral digits and terminating under teeth or at the tip of stylets are also known from other actinotrichid as well as anactinotrichid mites (e.g., Andre´ and Remacle, 1984; Alberti and Coons, 1999; De Lillo et al., 2005). However, the cheliceral innervation in A. longisetosus is quite peculiar in that probably all the teeth are sensitive, being provided with dendritic processes that terminate under fine pores. These pores, here documented in an oribatid mite for the first time by TEM, strongly support the suggested chemosensitivity (Walzl, 1987; Alberti et al., 2004). However, some other parts also are innervated, for example, the ventral part of the movable digit opposite the thin lamellae of the LLs and MA. To our knowledge, a comparable innervation of chelicerae has been reported only from Ricinulei (Talarico et al., 2008). Information about this character from other arachnid taxa is lacking. The fine structure of the delicate lamellated organ found in the paraxial proximal region of the principal segment of each chelicera is also described herein for the first time. It corresponds with the paraxial fenestrate area (fe1) described by Hammen (1968b, 1989) from Hermannia convexa. Based on its peculiar morphology and association with a thin muscle, this structure likely represents a sensory organ that detects forces exerted on the chelae during feeding. Based only on cuticular studies with light microscopy, a structure of this general appearance is widespread in oribatid mites, perhaps even in all major groups other than Enarthronota, but often it is overlooked. There seems to be no evolutionary relationship with the nearby Tra¨ga˚rdh’s organ, because it is clearly present in taxa that lack the latter organ, such as Palaeosomata (Grandjean, 1954b) and Mixonomata (Grandjean, 1958). The lamellated organ also seems plesiomorphic in Astigmata, and Norton (1998) considered this structure (called therein the adaxial cheliceral fossa), a synapomorphy that

Fig. 21. Details of chelicerae, oncophyses and Tra¨ga˚rdh’s organ (cross sections). (a) Movable digit inserted into a ventral pouch of the principal segment of chelicera. Note the massive dorsal extension (arrow) to which the tendon of the levator muscles will attach, and oncophysis op0 . Scale bar: 10 lm. (b) Superior tendon of levator muscle inserting dorsally at the movable digit. Note very thin cuticle (arrows) forming the pouch of the principal segment into which the movable digit is inserted and which is continuous with the cuticle of the movable digit. Scale bar: 5 lm. (c) More posteriorly tissues are present within the movable digit. Scale bar: 10 lm. (d) The movable digit ‘‘opens’’ posteroventrally to allow entrance of tissues (arrow). Note formation of condyles between principal segment and movable digit (arrowheads). The cuticle is continuous but flexible in a small region (asterisks). Scale bar: 10 lm. (e) Cross section through preoral cavity just in front of the mouth showing the position of the articulation of the movable digits (arrowheads). Arrows indicate entrance of tissues into the movable digits (cf. Fig. 21d), labrum with its ventral fold (arrowhead), and lamellae on malapophysis extending between labrum and movable digits. Duct of infracapitular gland close to its termination (cf. Fig. 31e). The preoral cavity contains some food material. The malapophyses have fused medially. Scale bar: 20 lm. (f) The lamella touches the movable digit. Note receptor process (arrow) entering the cuticle of the movable digit. Scale bar: 0.5 lm. (g) Pore above receptor process opposite lamella. Scale bar: 0.25 lm. (h) Posterior of the articulation of the movable digit, the posterior oncophysis is sectioned filling the gap between chelicera and infracapitulum. Scale bar: 5 lm. (i) Cross section through Tra¨ga˚rdh’s organ showing its cuticular organization. Arrowhead indicates the ridge (compare Fig. 4g inset). Scale bar: 5 lm. (j) Tra¨ga˚rdh’s organ close to its base. Note internal cuticular structure (arrowhead). Scale bar: 5 lm. 1–3, layers 1–3 of cuticle; dgi, duct of infracapitular gland; Ji, inferior commissure; lam.org, lamellated organ of chelicera; lm, lamella on malapophysis; LS, labrum; md, movable digit; Mb, cuticular bar of malapophysis; md, movable digit; op0 , paraxial oncophysis of principal segment of chelicera; opx, posterior oncophysis; po.gen, porose area of gena; pS, principal segment of chelicera; Tg, Tra¨ga˚rdh’s organ; ti, inferior tendon of depressor muscle; ts, superior tendon of levator muscle; vS, vertical septum.


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Fig. 22. Details of chelicerae and associated structures (horizontal sections). (a) One chelicera with its intrinsic muscles (mostly of the levator muscles) inserting at the superior tendon and attaching at the apodemal part of the cheliceral cuticle. The extrinsic dorsal retractor muscle (d.retr.pS) is seen inserting at the apodemal part of the cheliceral cuticle (cf. Fig. 22b–e) and originating laterodorsally on the integument of the prodorsum. Scale bar: 20 lm. Inset: Cheliceral sheath and apodemal part of cuticle. Note conspicuous pore canals in the cheliceral cuticle distal of acx and abrupt lack of pore canals in the apodemal part, i.e., proximal of acx. Scale bar: 1 lm. (b) Slightly more dorsal than in Figure 22a, the median retractors are visible. Note conspicuous cheliceral nerves entering principal segment. Scale bar: 20 lm. (c) Even more dorsally sectioned, the median retractors are more evident. At the right chelicera, the insertion of the dorsal retractors is obvious (compare Fig. 22e). Scale bar: 20 lm. (d) Cheliceral nerve in higher magnification. Scale bar: 1 lm. (e) Detail showing attachment site in higher magnification. Scale bar: 5 lm. ap, apodemal part of cheliceral cuticle; acx, line of attachment of cheliceral sheath to chelicera; ant.m, antiaxial muscle; Chn, cheliceral nerve; Cx, cheliceral sheath; dg1, duct of first podocephalic gland; d.retr.pS, dorsal retractor muscles of chelicera; ep, epithelium (partly retracted); ju, junctions between muscle cells and tendon cells; Mi, mitochondria; m.retr, median retractors inserting on anterior wall of vertical septum; Mu, muscles; pc, pore canals; PD, prodorsum; pS, principal segment; 1pGL, first podocephalic gland; RO, rostrum; rp, rostrophragma; ts, superior tendon of levator muscle; vS, vertical septum.



supported his hypothesis that Astigmata originated within desmonomatan Oribatida. To our knowledge such a cheliceral lamellated organ is not yet known from in other groups of mites, or in any other order of Arachnida. On the contrary, several proprioreceptors associated with muscles or tendons have been described from various body regions in Xiphosura (e.g., Fahrenbach, 1999 with ref.). It resembles the muscle receptors described from other arthropods (e.g., Honomichl, 2008) and may functionally correspond to the muscle or tendon proprioreceptors found in vertebrates (Welsch, 2003; Storch and Welsch, 2005). The lamellated organs of A. longisetosus evidently differ from the proprioreceptors described from the leg joints of spiders, which are not connected with muscles (Foelix, 1992; Barth, 2002). Studies of this organ in other taxa are needed to reveal more comparative details. Thus, it seems evident that these seemingly ungainly chelicerae may play a significant sensory role. At the proximal border of the manubrium, all oribatid mites possess a lateral fissure (af). Earlyderivative sarcoptiform outgroups (endeostigmatic mites) seem to have a similar structure (e.g., Grandjean, 1939), which Grandjean (1957a) associated with a primitive manubrial articulation, but details are unknown. The articulation itself was presumably lost in most oribatid mites, and the remnant fissure has never been studied in detail. Interestingly, Grandjean (1957a) suggested that the sensory function of the modified seta (i.e., the RU) has been reduced in favor of a mechanical function (related to feeding; see below). We showed here that the slit in the procuticle contains a nervous element, likely a receptor process (dendrite). Hence, during the evolution of the RU, this fissure indeed might have retained some sensory function, responding to cuticular stress (pressure/tension) exerted on the RU in the manner of a slit sense organ (lyrifissure), but more details are needed to substantiate this very preliminary interpretation. Slit sense organs of Actinotrichida are uninvestigated, except by Alberti and Coons (1999), who found that a notogastral slit sense organ of the oribatid mite Scutovertex minutus was provided with rather inconspicuous tubular bodies; such bodies have not yet been seen in af of A. longisetosus. Tra¨ga˚rdh’s Organ and Oncophyses A rather unexpected result is that Tra¨ga˚rdh’s organ, characteristic of Nothrina, Brachypylina and some Mixonomata (Norton and Behan-Pelletier, 2009), has a rather simple fine structure. It does not appear to be a sensory structure as one might expect from its shape and as was suggested by Tra¨ga˚rdh (1910), who first described the structure. As a simple cuticular tube, it resembles the oncophyses seen on the chelicerae of all oribatid

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mites and to a lesser extent also those of other mites (Grandjean, 1959; Hammen, 1968b, 1989; see also below). We found no nervous structure connecting to Tra¨ga˚rdh’s organ nor did we detect tendons/muscles inserting at its base, as was depicted by Hammen (1968b, 1989). The functions of these peculiar structures are largely obscure (Hammen, 1980; Evans, 1992; Weigmann, 2006; cf. Alberti et al., 2004 and below). Baümler (1970) described how he could make the oncophyses and Tra¨ga˚rdh’s organ swell when slightly pressing the coverslide of his preparation. Labiogenal Articulation Archegozetes longisetosus superficially seems to have a typical stenarthric infracapitulum, which is how Hammen (1989) characterized that of the congeneric A. magnus. However, the paired labiogenal lines of A. longisetosus represent merely slightly elevated cuticular ridges, with cuticular properties similar to those of surrounding cuticle, and so it cannot function as a real articulation. Hence, in this species, the labiogenal line is probably not functionally related to the RU (e.g., providing mobility to the RU as suggested by Evans, 1992) and Beck (1967) was in a way correct in characterizing the infracapitulum as anarthric (without labiogenal articulation) because an articulation is not possible. Weigmann (1996, 2006) provided strong arguments that the stenarthric type of articulation is the plesiomorphic one, but it appears that anarthry has evolved multiple times by fusion of mentum and genae, sometimes with the labiogenal line indicated as a suture. Lips At first glance, A. longisetosus has a preoral cavity and mouth surrounded only by three lips, that is, the upper lip (LS) and two LLs, resulting in a triangular mouth in cross section bordered by three so-called commissures, two superior (Js, Js0 ) and one inferior (Ji). A ventral lip (labium) occurring in ‘‘Endeostigmata’’ and palaeosomatan oribatids is considered to be ancestral (e.g., Grandjean, 1957a; O’Connor, 1984; Norton 1998). In this plesiomorphic condition, there are also two inferior commissures (Ji, Ji0 ). Even if present, these inferior commissures are short and, unlike the superior commissures, do not extend into the pharynx. This results in a pharynx with a crescent-shaped cross section, which is a characteristic of Actinotrichida but not Anactinotrichida (e.g., Warren, 1947; Hammen, 1970; Evans, 1992; Norton, 1998; Alberti and Coons, 1999; Alberti, 2006). Remarkably, in A. longisetosus, we found two inferior commissures in a very restricted region, which seem to represent a vestige of the putative ancestral state in this middle-derivative oribatid mite. Journal of Morphology

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Figure 23.



Rutella The paired rutella are proximally ‘‘hollow’’ structures containing tissues of epithelial origin. No dendritic processes have been observed within the rutella of A. longisetosus and no distinct basal sockets were found. This is remarkable because the rutella have been interpreted as hypertrophied setae (Grandjean, 1957a), probably mechanoreceptive, which should have a basal flexibility and an innervation. Dendrites ending with tubular bodies could be expected. However, these were not yet detected. Only a small nervous element, probably a dendrite, was found in A. longisetosus entering the manubrial fissure af, which could be interpreted as a modification of a plesiomorphic condition. It may still retain some sensitive function comparable to a (simplified) slit sense organ (see above). In remarkable contrast to A. longisetosus, a nerve supply was found within the RU in the more primitive oribatid mite Hypochthonius rufulus by Alberti (2008). Furthermore, the corniculi of certain anactinotrichid mites, which have been considered to be rutellar homologs (Lindquist, 1984), contain dendritic elements (e.g., Nuzzaci et al., 1992; Di Palma et al., 2006; Alberti, 2008). As rutella and corniculi (if homology is accepted) are an important character in supporting the homology of the gnathosomata of Anactinotrichida and Actinotrichida, and thus the monophyly of Acari (Lindquist, 1984), further studies are needed to elucidate the mentioned differences (Alberti, 2006, 2008). In this respect the innervated fissure, af, close to the base of the manubrium in A. longisetosus might be relevant in clarifying the homology problem. Does such an innervation also occur in other oribatid (or actinedid mites)? To our knowledge, no such fissure adjacent to the corniculi has been reported from anactinotrichid mites. We found no evidence for mobility of the rutella in A. longisetosus. In contrast, each seems to be rather firmly connected to the respective MA, with

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their inner walls forming cuticular bars running into the MA and likely supporting the preoral cavity and mouth region. Denticles Many papers have indicated the presence of small denticles (sometimes termed cilia) on various mouthparts, including the LS, rutella, and chelicerae (e.g. Grandjean, 1957a,b, 1958; Beck, 1967; Hammen, 1968b; Norton et al., 1996; Alberti and Coons, 1999; Alberti et al., 2004). Rarely, they have been drawn on LLs (Norton et al., 1996) but have not been described in detail. As food particles and fluids are manipulated in the preoral cavity, the many small cuticular denticles seen on the LS, the rutella, the LLs, and the inner sides of the MAs may help direct them toward the mouth, where most of the denticles point. The denticles seen on the inner (paraxial) side of the rutella, particularly those of the dorsal row, commonly called the rutellar brush, may indeed clean the outer (antiaxial) parts of the chelicerae as the latter move past. They evidently can ‘‘capture’’ particles as small as bacteria. The inner (paraxial) sides of the chelicerae maybe kept clean by movements of the LS. Particles cleaned from chelicerae may thus be added to the food. By analogy, oribatid mites possess both a toothbrush (on the rutella and LS) and toothpaste (saliva). Porose Areas In A. longisetosus, the cuticle is strikingly porose over extensive areas of the body. As usual, these pores represent wide pore canals that never penetrate the cuticle completely, that is, the epicuticle always remains intact. These pores are found in varying densities, but only in cuticle of the body wall, that is, not in apodemal areas, which are internalized and unexposed to the external medium. Combined with their thin underlying epidermis,

Fig. 23. Details of chelicerae and associated structures (a–e: horizontal sections, f: cross section). (a) Section at level of trochanter remnant (in.tr indicates its intrinsic muscles). Note position of lamellated organ and its putative connection with the superior tendon through a small muscle. Basal insertion of Tra¨ga˚rdh’s organs. Several hemocytes (granulocytes) are visible. Scale bar: 10 lm. (b) Anterior part of principal segment of chelicera with insertion of anterior cheliceral seta (chb) and solid dorsal articulation process of movable digit. Arrows point to thin cuticle of pouch of principal segment (cf. Fig. 21a–e). Scale bar: 5 lm. (c) Ventroproximal part of chelicera, i.e. trochanter remnant. Note the distinct separation from the principal segment of the chelicera by cuticular inward projections of the latter (arrows). Intrinsic muscle of the region. Scale bar: 5 lm. (d) Base of Tra¨ga˚rdh’s organ in higher magnification (cf. Fig. 23a). Note that the organ is made of modified cuticle only. At its base cellular elements containing prominent lysosomes are visible. The lamellated organs with their thin muscle are visible. Scale bar: 2 lm. (e) Higher magnification of lamellated organ showing the flat processes of nerve fibres (electron-lucent, with many microtubules and some mitochondria) between the flat epidermal cells modified as tendon cells (electron-dense, note nucleus) which attach to the cuticle via short microvilli. At right, the junctional complexes of these cells with the muscle cell are visible. Scale bar: 0.5 lm. (f) One lamellated organ consisting of alternating flat (dense) epidermal cells, modified as tendon cells, and flat (light) processes of nerve cells.The cuticle is indented from the inner side. Note rather thick nerve close to lamellated organ. Scale bar: 2 lm. ant.m, antiaxial muscles; cha, posterior cheliceral seta; chb, anterior cheliceral seta; cpc, podocephalic canal; Cu, cuticle; CX, cheliceral sheath; dg1, duct of first podocephalic gland; dg2, duct of second podocephalic gland; ep, epithelium (partly retracted); Hc, hemocyte; ju, junctions between tendon cell and muscle cell; in.tr, intrinsic muscles of trochanter remnant; lam.m, muscle of lamellated organ of chelicera; lam.org, lamellated organ of chelicera; Ly, lysosomes; Mu, muscles; Mv, microvilli; N, nucleus; ne, nerve; pS, principal segment of chelicera; RO, rostrum; rp, rostrophragma; SY, synganglion; tc, tendon cell; Tg, Tra¨ga˚rdh’s organ; ts, superior tendon of levator; vS, vertical septum.


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this suggests that such pores are used for gas exchange. In many oribatid mites, such pores form well-circumscribed regions, the respiratory porose areas (Alberti and Norton, 1997), but in A. longisetosus such discrete areas could not be distinguished

in the cuticle of the infracapitulum or of any other part of the body. As A. longisetosus is rather active and has a relatively short life cycle for a member of Nothrina (Heethoff et al., 2007 and therein cited articles), the weak sclerotization and numerous

Figure 24.



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Fig. 25. Pharynx and pharyngeal rods (a–c: lCT; d: TEM; a, sagittal; c, horizontal (frontal), b and d cross sections). (a) The pharyngeal rods start from the ici/manubrial bar-region and run as peculiar cuticular fibers posteriorly paralleling the modified cuticle of the pharyngeal floor.The capitular apodeme covers the trochanter remnant (compare Fig. 25c). (b) The dorsal cuticular roof of the pharynx is in its resting position (compare Fig. 25d). Note condylar ridges (k) and labiogenal line (arrows). (c) The ventral part of the infracapitulum is shown as being cut open. The pharyngeal rods parallel the pharynx. (d) The pharynx is in its dilated state. Note distinctly different apearance (see also inset) of the pharyngeal rods compared to adjacent modified cuticle (asterisk) of pharyngeal floor which is connected to the mental integument via specialized cells (ep). (d) Scale bar: 10 lm. Inset: Scale bar: 2.5 lm. a, anterior infracapitular seta; ap.c, capitular apodeme; acx, line of attachment of cheliceral sheath to chelicera; chb, anterior cheliceral seta; CX, cheliceral sheath; dMu, dorsal (dilator) muscles; ep, epithelia; G, gena; ici, inferior commissural induration; k, condylar ridge; M, mentum; Mb, oblique cuticular bar in malapophysis; md, movable digit of chelicera; min, median infracapitular nerve; Pdp, pedipalp; Ph, pharynx; ph.r, pharyngeal rods; pS, principal segment of chelicera; RO, rostrum; RU, rutellum; tMu,transversal (depressor) muscles; Tr, trochanter remnant; vmTr, vertical muscle in chelicera.

Figure 24. Labrum, mouth and pharynx (cross sections). (a) Anteromost part of labrum. Note small denticles (arrowheads). Scale bar: 2 lm. (b) Slightly more posteriorly the labrum shows a dorsal elevated ridge and denticles on its dorsal surface (arrowheads). Arrow indicates lateral fold. Scale bar: 2 lm. (c) Labrum more posteriorly, note sclerotized cuticle (asterisks), lateral folds (arrows) and denticles (arrowheads). The distal ends of Tra¨ga˚rdh’s organs are visible. Scale bar: 2 lm. (d) Slightly in front of the mouth, the labrum shows a ventral fold (arrowheads) which will posteriorly continue as the dorsal roof of the pharynx. Note ventrally inferior commissure and ducts of the infracapitular gland (dgi). Preoral cavity with some food material. The infracapitulum forms dorsally two longitudinal cheliceral grooves into which the chelicerae are embedded with their ventral parts (see also Fig. 24d–f). Arrows indicate labiogenal line. Scale bar: 20 lm. (e) Mouth region. On the right side, labrum and lamella on malapophysis have fused already. Note oblique cuticular malapophysis bar separating the malapophysis paraxially from the mouth. Arrows indicate labiogenal line. Scale bar: 20 lm. (f) Slightly more posteriorly. Labrum completely fused with malapophyses, hence beginning of the pharynx. The cuticle of the base of the labrum is much differentiated including thick, sclerotized oblique bars (white arrowheads). Note superior commissures and inferior commmissure, which is in fact composed of two commissures (compare Fig. 24d–f,j). Dorsally at the capitular saddle a fold overlapping the base of the labrum is visible into which the labral sclerite extends (black arrowhead; cf. Fig. 28a–c). Arrows indicate labiogenal line. Scale bar: 20 lm. (g) More posteriorly, level with the trochanter remnant of the chelicerae, the capitular apodeme serves as origin for the dorsal (dilator) muscles of the pharynx. The two labral muscles are also seen. Note wide lumen of the pharynx and peculiar cuticle of its ventral floor (asterisk). Scale bar: 20 lm. (h) More posteriorly the dorsal roof of the pharynx is lowered. The infracapitular gland appears. Scale bar: 20 lm. (i) More posteriorly, the roof of the pharynx is elevated again. The infracapitular gland is prominent. Transverse (tMu) and dilating (dMu) muscles of the pharynx are evident. Scale bar: 20 lm. (j) Detail from Figure 24d showing anterior part of inferior commissure. It is evident, that the commissure in fact is formed by two small parallel commissures Ji and Ji0 (see also Figs. 21e and 24e,f). Scale bar: 2 lm. a.pc, capitular apodeme; Ch, chelicera; cha, posterior cheliceral seta; CX, cheliceral sheath; dgi, duct of infracapitular gland; dMu, dorsal (dilator) muscles; Hc, hemocytes; ici, inferior commissural induration; iGL, infracapitular gland; Ji, Ji0 , inferior commissures; Js, Js0 , superior commissures; Lm, labral muscles; lm, lamella on malapophysis; LS, labrum; Mb, oblique cuticular bar of malapophysis; min, median infracapitular nerve; Mo, mouth; opx, posterior oncophysis; Ph, pharynx; po.gen, porose area of gena; pS, principal segment of chelicera; se, capitular saddle; Tg, Tra¨ga˚rdh’s organ; tMu, transversal (depressor) muscle.


Journal of Morphology Stretch dorsally of pharynx roof between its lateral edges

tMu

Labral muscles

Lm

Dorsal base of labrum

Lateral roof of pharynx

dMu vMu

Dorsal (dilator) muscles of pharynx Ventral (dilator) muscles of pharynx Transversal (depressor/ constrictor) muscles

Apodemal parts of proximal segment of pedipalp Mediodorsal roof of pharynx

mPdp

Infracapitulum intrinsic Proximal muscles of pedipalps

Posterolateral on mentum Posterior border of capitular apodeme

M.retr rM

Condylar ridge of infracapitulum

Anterior wall of vertical septum

Medioventral on trochanter remnant

Stretches horizontally between walls of trochanter remnant

Dorsal on movable digit

Dorsal on movable digit

Ventral on movable digit

Dorsolateral on apodemal part of principal segment Ventromedial on apodemal part of principal segment Dorsomedial on apodemal part of principal segment Posterior part of trochanter remnant

Insertion

Retractor of mentum Retractor of capitular apodeme

ant.m

vmTr

Vertical muscle in chelicera

Infracapitulum extrinsic Antiaxial muscles

in.tr

Intrinsic muscle of trochanter remnant

m.retr

lam.m

Muscle of lamellated organ

Cheliceral frame Median retractor

lev.m

dep.m

retr.Tr

sup.retr.pS

inf.retr.pS

d.retr.pS

Abbreviation

Levator of movable digit

Chelicera extrinsic Dorsal retractor inserting on principal segment Inferior retractor inserting on principal segment Superior retractor inserting on principal segment Retractor of chelicera inserting on trochanter remnant Chelicera intrinsic Depressor of movable digit

Muscle

Stretch dorsally of pharynx roof between its lateral edges Posterior border of capitular apodeme

Lateral parts of cervix and capitular apodeme Lateral wall of mentum

Walls of large lateral ridge

Endosternum Endosternum

Anterolateral prodorsum

Posteromedial prodorsum

Inner, ventral and posterior wall of principal segment Inner dorsal and lateral wall of principal segment Inner, median wall of principal segment Stretches horizontally between walls of trochanter remnant Inner, dorsomedial wall of apodemal part of principal segment

Posterior prodorsum

Posterior prodorsum

Posterior prodorsum

Posterolateral prodorsum

Origin

TABLE 1. Muscles of the gnathosoma of Archegozetes longisetosus

Elevates roof of pharynx; widens pharynx lumen, creates sucking forces; moves food Elevates roof of pharynx; widens pharynx lumen, creates sucking forces; moves food Pull edges of pharynx mediad and thereby lowers/depresses the pharynx roof; constricts pharynx lumen; moves food Retracts and probably elevates labrum; alternating contractions may move labrum horizontally

Moves base of pedipalp

Uncertain; pulls prodorsum and infracapitulum together, elevates infracapitulum, moves hemolymph? Retracts and lowers infracapitulum Retracts and probably elevates infracapitulum

Uncertain; retraction of chelicerae, pulling chelicerae inward (mediad)?

Uncertain; regulating influx of hemolymph into chelicera?

Monitoring of forces of depressor and levator in cooperation with lamellated organ Uncertain; moving hemolymph into oncophyses and Tra¨garh’s organ?

Elevates movable digit; closes chela

Lowers movable digit; opens chela

Retraction of chelicera; pulls chelicera outward (laterad) and/or upward (dorsad) Retraction of chelicerae; pulls chelicera inward (mediad) and/or downward Retraction of chelicera; pulls chelicera inward (mediad) Retraction of chelicerae; pulls chelicera downward (ventrad)

Proposed function

1064 G. ALBERTI ET AL.


pores dispersed over most regions of the exposed body surface probably make up for the absence of tracheae or other internalized respiratory organs. The integument of oribatid mites also may be provided with numerous dermal glands, the cuticle of which looks much like that of respiratory porose areas in being provided with many and wide pore canals. However, these areas are underlain by a peculiar glandular tissue with cells having very long microvilli apically and containing mostly lipid inclusions (Alberti and Norton, 1997). Such secretory porose organs represent type I glands in the classification of Noirot and Quennedy (1974), that is, the gland cells are covered by a thin (epi)cuticle through which the secretion must pass. Possible functions of these secretory porose organs were discussed by Alberti and Norton (1997) and may differ according to species or body region. The secretions may provide a cleansing effect, have antimicrobial or hydrophobic properties, or provide secretions for intraspecific communication. In certain oribatid mites, the latter is suggested by striking sexual dimorphism in these organs (Behan-Pelletier and Eamer, 2010 and therein cited articles). Hammen (1968b) and Grandjean (1957b) observed three pairs of porose areas on the infracapitulum of Hermannia convexa and Xenillus clypeator, respectively, but because they studied only cuticular components, the true nature of those areas remained unknown to them. In these species, one of the areas is in the cheliceral groove, the second (manubrial porose area) occupies the dorsal region of the manubrium, and the third (laterocoxal or supracoxal) area lies between the supracoxal (postpalpal) seta and the anterior end of the podocephalic canal. In A. longisetosus, the laterocoxal porose area represents a secretory porose organ, the cheliceral groove area is not recognizable, and the manubrial area is only weakly developed. In contrast to the other two species, we found a secretory genal porose area that occupies a region more or less between the groove and manubrium. The microvilli of the underlying cells point to the porose cuticle of the genae, hence in the opposite direction of the groove. It could be that the manubrial porose area is merely an extension of the larger genal porose area in this species. Perhaps the three areas represent a secretory region that can vary in position and subdivision according to species, analogous to the humerosejugal series of secretory organs in poronotic Brachypylina (Alberti and Norton, 1997). On the RO of Hermannia convexa, Hammen (1968b, 1989) found a small cuticular region that he called the rostral porose area (A.r). We examined specimens of this species with light microscopy; the structure appears like a muscle sigillum, with well-circumscribed internal excavation and unusual cuticular structure, but no trace of poros-

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ity. In A. longisetosus, no such discrete area is visible but the peculiar rostral attachment site might correspond to the area in H. convexa. This attachment is remarkable, because the epidermal cells involved in connecting the two integumental layers are modified like tendon cells, yet no muscles are connected to this region. Thus, the structure resembles the peculiar tissue that connects the floor of the pharynx with the integument of the mentum (Alberti et al., 2003). These cells probably prevent separation of rostrum and rostrophragma when hydrostatic pressures within the idiosoma are increased, as when necessary to protrude the gnathosoma or chelicerae. Glands Associated with the Gnathosoma Some Actinotrichida have a rather complex set of gnathosoma-associated glands. For example, in many Prostigmata, there are unpaired or tracheal glands and paired podocephalic and iGLs (Alberti and Coons, 1999). An unpaired gland opening between the bases of the chelicerae and producing lipid secretions (e.g., Alberti and Storch, 1973; Alberti and Coons, 1999; Di Palma et al., 2009) is lacking in A. longisetosus. This seems to be generally the case in Oribatida (compare, e.g., Michael, 1884; Berlese, 1897; Warren, 1947; Woodring and Cook, 1962; Hoebel-Ma¨vers, 1967). Podocephalic glands and podocephalic canal. The paired podocephalic canal system is a constitutive feature of the order Actinotrichida (e.g., Grandjean 1938, Hammen 1989, Lindquist 1984, Bernini 1986, Alberti 1973, 2006) and is functionally related to the gnathosoma. The canal itself (cpc) is a superficial, groove-like cuticular duct, sometimes called a taenidium in the acarological literature (thus with a different meaning in the more general literature, in which the term refers to cuticular reinforcements stabilizing the tracheae). The name ‘‘podocephalic’’ derives from its location, which extends from the first leg (podos 5 foot) anteriorly toward the base of the ‘‘cephalon’’ (head), which in mites is a misleading synonym of gnathosoma. According to Woodring (1973), nonbrachypyline oribatid mites have the fundamental complement of podocephalic glands in actinotrichid mites. This includes a single largely tubular gland (coxal gland or nephridium) and three acinous glands (Grandjean, 1938; Alberti and Storch, 1973, 1977; Alberti et al., 1996; Alberti and Coons, 1999). The glands of A. longisetosus seem to fit this pattern; although we did not study all the prosomal glands in detail, we did find all the ducts. Hammen (1968b) concluded from macerated Hermannia convexa specimens that the tubular gland comprised two branches, but he later (1989) corrected this; one of the putative branches was the duct of the posterior (the third) acinous gland. Journal of Morphology

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The overall structure of the tubular gland was more or less histologically studied in oribatid mites by Michael (1884, referring to it as the supracoxal gland) and Warren (1947, calling it the oral gland).

They did structure, and Cook suggested

Figure 26.


not find the external opening of the but it was later detected by Woodring (1962). Remarkably, Michael (1884) had the gland was a nephridium, which was


not substantiated until Woodring (1973) observed the sacculus. Fine structural studies by Alberti and Storch (1973, 1977) and Alberti et al. (1996) further substantiated this interpretation that the gland is an excretory, or more strictly osmoregulatory, organ with the podocytes-lined sacculus functioning as an ultrafiltration site. The filtration barrier between hemolymph and sacculus lumen consists of the basal lamina and the slit membranes (see also Alberti and Coons 1999). The nephridial tubule modifies this ultrafiltrate. Most characteristic of oribatid nephridial tubules are peculiar junctional complexes between the cells, which are provided with thick electron-dense intracellular reinforcements thought by early authors to represent a cuticular skeleton. This interpretation should be discarded because the material is intracellular (Alberti and Storch 1977, Alberti et al. 1996, Alberti and Coons 1999). The podocephalic canal, which collects and delivers gland products onto the proximodorsal surface of the infracapitulum, is not a closed tube as in many actinedid mites (Alberti and Coons, 1999) but rather is an open furrow that is tightly covered by a cuticular lid. Such a furrow is the only form known from oribatid mites, but there are too few data to consider it a general feature of the group. The shape of the lid may vary among species (compare Alberti and Coons, 1999, Fig. 168C, Eupelops sp.). The gland products vary: those of the coxal glands (fourth podocephalic gland) are certainly related to water-/ion-/osmoregulation, while those of the acinous glands maybe related to other functions, for example, nutrition (saliva, flushing, and lubrication). Infracapitular glands. In addition to the podocephalic glands, there is a further pair of glands in the infracapitulum that extends backward into the anterior idiosoma. Previous histological studies of oribatid mites have shown ‘‘salivary glands’’ that assumed different positions and had various sizes, depending on species or author (e.g., Berlese, 1897; Woodring and Cook, 1962; Hoebel-Ma¨vers,

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1967). We have the impression that these glands and their openings were never depicted correctly, and from his cuticular studies, Hammen (1968b, 1989) could only speculate that the small, paired proximodorsal openings on the infracapitulum represented those of iGLs. So, the fact that we were able to trace the ducts of the glands to these openings in A. longisetosus proves for the first time that iGLs occur in Oribatida and supports the idea that iGLs are fundamental features of actinotrichid mites (Alberti, 1973; Alberti and Storch, 1973; Alberti and Coons, 1999; Alberti, 2006). It seems likely that production of saliva is really the role of these large glands. However, this fluid probably has little or no enzymatic activity, because food found in the ventriculus is rather intact (Alberti et al., 2003, 2004). Maybe the secretions facilitate the transport of food particles from the preoral cavity into the mouth and further on through the pharynx and esophagus, which is enabled by the sucking/pumping action of the pharynx. Saliva also may function as a cleansing fluid that flushes remnants of food material out of the preoral cavity; this maybe important to keep the sensory pores of the chelicerae functional (comparable to the glands associated with gustatory papillae on the tongue of mammals; e.g., Welsch, 2003). Remarkably, Hoebel-Ma¨vers (1967) observed flushes of a foamy secretion, presumably saliva, coming from the sides of the mouth in Euzetes globulus when transferring the oribatid mite into fixative. Muscles Hammen (1968b, 1989) examined gnathosomal muscles of Hermannia convexa in detail, but only through supposed tendons that resisted maceration in lactic acid (Table 1). Therefore, he could not distinguish between true tendons (cuticular strands surrounded by epithelial cells) and muscles, and most of his ‘‘tendons’’ certainly also included remnants of muscle cells. Gnathosomal

Fig. 26. Horizontal sections through infracapitulum. (a) Lateral lips, rutella and the pharynx are sectioned. Note distinct border (collum) between rutella and manubrium, the manubrial cuticle being provided in this rather ventral aspect with many pore canals composing the manubrial porose area. Bases of anterior infracapitular setae (a) are visible (cf. Fig. 26e–g). Arrowheads point to the ventral folds of the labrum which continue into the roof of the pharynx posteriorly (compare Fig. 24d,e). Asterisk indicates modified ventral cuticle of pharynx. Oblique cuticular bars in malapophyses (Mb, compare Fig. 24d–f). Scale bar: 25 lm. (b) Slightly more dorsally sectioned, the mouth is seen above the lateral lips. The dorsal lamellae on the lateral lips/malapophyses are visible (compare Fig. 24d,e). Denticles on the paraxial side of the rutella are indicated by arrows. Note tissue extending into the rutella. Arrowheads point to small denticles in the mouth area (compare Fig. 27a,d). Note position of antiaxial manubrial fissure af indicating posterior border of manubrium (compare Fig. 27). The small cuticular bar (Lb) connected to the base of the lateral lips is visible on the right. Scale bar: 25 lm. (c) Part of rutellum showing apical tooth consisting only of external dense cuticular layer. Note denticles. Scale bar: 5 lm. (d) Detail of rutellum showing denticle and bacterium (arrowhead). Scale bar: 2.5 lm. (e) Tubular body close to base of seta (a). Scale bar: 1 lm. (f) Base of infracapitular seta (a) set into a socket with connected tubular body. Scale bar: 2.5 lm. (g) Porose area of gena behind infracapitular seta (a). Note numerous long microvilli and lipid secretions (Se). Scale bar: 1 lm. 1–3, layers 1–3 of cuticle; a, base of anterior infracapitular seta; c, collum of rutellum; db, dense cuticular bar associated with base of lateral lips; dMu, dorsal dilator muscles of pharynx; ici, inferior commuı´ssural induration; iGL, infracapitular gland; Js, Js0 , superior commissures; Lb, cuticular bar associated with base of lateral lip; LL, lateral lips; Mb, cuticular bar in malapophysis; MA, malapophysis; MN, manubrium of rutellum; Mo, mouth; Mv, microvilli; Pdp, pedipalp; Ph, pharynx; po.gen, porose area of gena; po.mn, porose area of manubrium; RU, rutellum; Se, secretion; sf, suspension fibres; t, tooth of rutellum; Tb, tubular body.


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G. ALBERTI ET AL.

Fig. 27. Horizontal sections through base of rutellum and associated structures. (a) Slightly more dorsal than Figure 26a, the denticles of the mouth area and those paralleling the paraxial side of the small furrow in the dorsal side of the lateral lips/malapohyses are visible (white arrowheads; compare Figs. 26b and 4c,d). The denticles of a second more paraxial row are indicated by a black arrowhead, the denticles situated in the mouth area are marked by an arrow. Note distinct border (collum) between rutellum and manubrium due to abrupt modification of rutellar cuticle. The posterior border of the manubrium is indicated by the antiaxial manubrial fissure af. Scale bar: 5 lm. (b) Detail of manubrium showing nervous structure in manubrial fissure af. Note very thin epicuticle (compare Fig. 27a,c). Scale bar: 1 lm. (c) Detail of manubrial fissure af with small nervous structure structure (containing a mitochondrium). Note pore canals terminating under epicuticle. Scale bar: 0.5 lm. (d) Slightly more dorsal than Figure 27a. Note denticles in wall of mouth (arrowhead), duct of infracapitular gland and posterior border of manubrium with nerve beneath manubrial fissure af. Scale bar: 5 lm. (e) Detail of Figure 27d. Nerve associated with fissure af in higher magnification. Scale bar: 0.5 lm. af, manubrial fissure; c, collum of rutellum; Cu, cuticle; dgi, duct of infracapitular gland; ec, epicuticle; Lb, cuticular bar associated with base of lateral lip; lm, lamella on lateral lip/malapophysis; Mb, cuticular bar in malapophysis; Mi, mitochondrium; MN, manubrium of rutellum; ne, nerve; pc, pore canal; prc, procuticle; RU, rutellum.


Fig. 28. Horizontal sections through infracapitulum and chelicerae from ventral to dorsal (a–e: horizontal sections) and attachment sites of labral muscles (f,g: cross sections). (a) Dorsal (dilator) muscles of pharynx slighty below their insertion at cervix and capitular apodeme respectively. Note movable digits of chelicerae and their teeth. Arrow points to region where the labrum will arise. Scale bar: 25 lm. (b) Slightly more dorsally, the base of the labrum is visible. Note strong labral muscles and folds embracing the base of the labrum (white arrowheads), into which the labral sclerite continues (black arrowheads; compare Fig. 24f). The dorsal (dilator) muscles of the pharynx attach to capitular apodeme. Scale bar: 20 lm. (c) Even more dorsally, the labrum is sectioned in almost full length, labrum muscles posteriorly close to attachment site at capitular apodeme. Scale bar: 12.5 lm. (d) More dorsally, the attachments of labral muscles on the capitular apodeme are visible and also (on the right side) the attachment of the retractor muscles of the infracapitulum. D indicates articular tooth of trochanter remnant. Scale bar: 20 lm. (e) Detail from Figure 28c enlarged showing tip of labrum with rows of denticles (arrowheads). Note modified cuticle suggesting a sequence of sclerites (arrows) connected via flexible parts. Scale bar: 5 lm. (f) Base of labrum (cf. 24f) with labral muscles inserting (arrows). Scale bar: 20 lm. (g) Detail of attachment site (compare Fig. 28f right arrow) in higher magnification. Note modified epidermal cell containing numerous microtubules (tendon cell aspect) and junction with labral muscle cell. Both cells are strongly interdigitating. Scale bar: 1 lm. ap.c, capitular apodeme; Cu, cuticle; ep, epithelium (partly retracted); fd, fixed digit of chelicera; dMu, dorsal (dilator) muscles; FB, fat body; Hc, hemocyte (granulocyte); iGl, infracapitular gland; Lm, labral muscles; LS, labrum; md, movable digit; Mu, muscle; op0 , paraxial oncophysis of principal segement of chelicera; Pdp, pedipalp; Ph, pharynx; pS, principal segment of chelicera; rM, retractor muscle of infracapitulum (corresponding to Hammen’s tendons tp and tm1-3); sc.ls, labral sclerite; SY, synganglion; t, teeth of cheliceral digits; tc, tendon cell; Tg, Tra¨ga˚rdh’s organ; tr, trochanter remnant.

Fig. 29. Details of the infracapitulum (cross sections). (a) Base of rutellum close to its fusion with the basal part of the malapophysis (and the lateral lips). No nervous elements reach into the rutellum. Note lamella on lateral lip. The two rows of denticles are indicated by white and black arrowheads. Scale bar: 5 lm. (b) More posteriorly, the manubrium is fused to the basal part of the malapophysis but separated by a cuticular malapophysis bar (Mb). Paraxially a smaller bar is visible, which reaches backwards from the base of the lateral lip (Lb; compare Fig. 26a,b and also Fig. 24d–f). Denticles indicated by white and black arrowheads. Scale bar: 5 lm. (c) More posteriorly, in the mouth region, the malapophysis bar is already reduced ventrally. Note lamella on malapophysis and small denticles in the wall of the mouth and labrum (arrowheads). Arrow points to small nerve under malapophysis bar (see also Fig. 29d). Scale bar: 5 lm. (d) Nerve under malapophysis bar in higher magnification. Scale bar: 0.5 lm. (e) Insertion of posterior (mental) infracapitular seta (h) into a flexible socket. Note tubular body. Scale bar: 0.5 lm. (f) Tubular body of posterior infracapitular seta (h) in higher magnification. Scale bar: 0.25 lm. a, anterior infracapitular seta; Cu, cuticle; Ep, epidermis; h, posterior infracapitular seta; Lb, cuticular bar associated with base of lateral lip; LL, lateral lip; lm, lamella on gena/ malapophysis; Ls, labrum; md, movable digit; Mb, cuticular bar in malapophysis MN, manubrium; Mt, microtubules; ne, nerve; op0 , paraxial oncophysis of principal segment of chelicera; po.gen, porose area of gena; RU, rutellum; sf, suspension fibres; Tb, tubular body.


muscles of A. longisetosus all belong to the crossstriated type, as is usually the case in Euarthropoda. Tendons are extensions of the cuticular component of the integument accompanied by epithelial cells, which at attachment sites are modified as tendon cells, usually forming microtubule-associated junctional complexes with the muscle cells (for exceptions see Nuzzaci and Alberti, 1996, Alberti and Coons, 1999). Some muscles, for example, the dorsal extrinsic retractor muscles of the chelicerae, which originate dorsolaterally on the PD, insert directly on the apodemal part of each chelicera, that is, via tendon cells but without a tendon. By contrast, the intrinsic muscles of the principal cheliceral segment attach via tendons to the movable digit. As expected from studies of other mites (Evans 1992), the levator muscle is much stronger than the depressor and both are of the pinnate type, originating broadly on the cuticle of the inner sides of the chelicerae and tapering toward the tendons (Heethoff and Norton, 2009a). Other, extrinsic, muscles insert via tendon cells on the proximoventral structures of the chelicerae (trochanter remnant and/or principal segment). Some were seen by previous authors and termed cheliceral retractor muscles and cheliceral rotating muscles by Woodring and Cook (1962), cheliceral retractor muscles by Hoebel-Ma¨vers (1967) or cheliceral retractor-adductor muscles by Akimov and Yastrebtsov (1989). These authors depicted them as originating on the PD, which is confirmed by our study. The muscles are probably those represented by tendons tfi, tfs, ttr, tTi, and tTs in the drawings of Hammen (1968b, 1989). Through synchrotron X-ray microtomography (SR-lCT), it was possible to clarify the complexity of these extrinsic muscles in their natural three-dimenional orientation for the first time. Some probably adjust the movements of the chelicerae (Hammen 1968b) and Akimov and Yastrebtsov (1989) suggested that some may elevate (extend) the gnathosoma. The latter authors (and Sanders and Norton, 2004) also depicted muscles inserting on the base of the mentum, which are supposed to function antagonistically as gnathosoma flexors. These muscles were also found in A. longisetosus (retractor muscles of mentum, M.retr). For the first time, small intrinsic muscles were observed within the trochanter remnant of the chelicera, but their role, and the function of the remnant itself, remains to be discovered. Perhaps they indirectly move Tra¨ga˚rdh’s organ or modify the volume of the oncophyses by moving hemolymph (see above and Baümler, 1970). A further muscle not previously observed is the vertical muscle (vmTr), which may serve to adjust the relative position between the principal segment and the trochanter remnant, thereby controlling also partially the inner ‘‘opening’’ of the chelicera and the amount of hemolymph coming in.

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Pharyngeal muscles of A. longisetosus were previously described by Alberti et al. (2003). Labral and dorsal (dilator) muscles of the pharynx originate on the cervix and capitular apodeme. The ventral (dilator) muscles originate on the integument of the mentum and the transversal (depressor) muscles span between the lateral edges (continuations of Js, Js0 ) of the pharynx. It is evident from this arrangement that only the pharyngeal roof is moved, probably in a longitudinal wave (note different positions of the pharnygeal roof in Figs. 6 and 24). By contrast, the floor of the pharynx is fixed to the mental integument via specialized cells (see Alberti et al., 2003). A new finding is the presence of pharyngeal rods that parallel the pharynx; they are apparently sclerotized structures that differ distinctly from the adjacent electron-lucent cuticle of the pharyngeal floor. These rods are continuations of the oblique bars in the MAs, which originate on the inner base of the rutella. Hence, these oral and pharyngeal structures reveal a peculiar architecture, the functional significance is largely obscure but which may relate to the peculiar movements of the pharynx. In addition, there are muscles (rM; corresponding to tendons tp, tm1–3 of Hammen, 1968b, 1989) inserting on the capitular apodeme that may retract the infracapitulum or the entire gnathosoma. According to Sanders and Norton (2004), these muscles originate on the first apodeme (i.e., the most anterior apodeme of the coxisternum) in Euphthiracarus cooki. In A. longisetosus, SR-lCT shows these muscles to instead connect to the endosternum. Vertical antiaxial muscles (termed pedipalpal coxa-sternum retractor muscles by Woodring and Cook, 1962, lingula muscles by Hoebel-Ma¨vers, 1967, and subcapitular levators by Sanders and Norton, 2004) were found connecting the dorsolateral parts of the PD with a dorsolateral ridge, the condylar ridge (see above), of the infracapitulum. These muscles correspond probably to tendons ta (posterior antiaxial tendon of infracapitulum) of Hammen (1968b, 1989). We think that these muscles maybe serial homologs of the latero-dorsoventral muscles in the hysterosoma (which draw notogaster and ventral sclerites together) and, like them, are probably used to increase the hydrostatic pressure (see Sanders and Norton, 2004; Heethoff and Norton, 2009b) needed to protrude the gnathosoma or chelicerae by lowering the PD or elevating the infracapitulum, respectively. Another function maybe to resist hemolymph pressure that is created in the hysterosoma by the lateral dosoventral muscles. From the muscle arrangement and cuticular exoskeletal structures, it is evident that the chelicerae can be retracted (by all the retractors), probably spread (pulled apart by dorsal retractors) and adducted (pulled together by superior, inferior and median retractors). The movable digit can only be Journal of Morphology

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moved vertically, due to the dicondylic articulation of the movable digit with the principal segment; stimuli associated with this biting action are prob-

ably sensed by the peculiar cheliceral lamellated organ, described herein for the first time. Tra¨ga˚rdh’s organ is likely an elongated oncophysis that

Figure 30.



is moved only passively, as are other oncophyses and the LLs. The LS maybe retracted, elevated, and moved laterally. The rutella are anchored in the MAs, apparently in a rather rigid way, but maybe moved passively to a very limited degree. In particular, there is nothing resembling a flexible socket, as is typically found in mechanosensitive setae, from which the rutella are thought to have evolved. The forces acting on the rutella are likely perceived by the putative slit sense organ (manubrial fissure af). The infracapitulum (or gnathosoma) as a whole maybe slightly retracted by extrinsic muscles inserting on the capitular apodeme and originating on the endosternum and by retractors inserting on the proximal border of the mentum and originating also on the endosternum. Antagonistic forces that would protrude chelicerae, the LS, the infracapitulum, or the entire gnathosoma can only come from an increase of hydrostatic pressure created in the body of the mite; these likely are generated predominantly by the lateral dorsoventral muscles in the hysterosoma. Regarding the chelicerae, the vertical muscles (vmTr) may regulate the amount of hemolymph entering the chelicerae (see above). The antiaxial vertical infracapitular muscles maybe involved in these actions as indicated above. With respect to the infracapitulum or the entire gnathosoma, these movements can only be performed in a very restricted way, because the articulating cuticle along the ventral base of the gnathosoma is very narrow. The infracapitulum may also be slightly moved up and down by antagonistic activity of the muscles inserting on the capitular apodeme and the proximal mental border. This movement maybe possible due to a thin and probably flexible region of cuticle at the proximolateral base of the infracapitulum, just above the insertion of the antiaxial infracapitular muscle on the condylar ridge (k). Specific con-

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dyles (comparable to those of the movable digits of the chelicerae) were not seen on the base of the infracapitulum, though they exist in brachypyline oribatid mites (Grandjean, 1952). Hence, the entire gnathosoma likely can move up and down only to a limited degree in A. longisetosus. Nutritional Function of the Gnathosoma In Acari, the gnathosoma is the body region that is associated with the acquisition of food. In most oribatid mites, this food is particulate, in contrast to the fluid food of most other Acari and Arachnida (e.g., Heethoff and Norton, 2009b). As the food of A. longisetosus (both natural and in culture) ranges from decaying leaves to algae and/or fungi (Smrzˇ and Norton, 2004 and included references), according to the classifications of Schuster (1956) and Luxton (1972), it is a nonspecialist or panphytophagous species (see also Alberti et al., 2003 with further ref.). After testing food with the sensilla on the pedipalps, the mite starts to feed. Evidently, it uses the closely coapting cheliceral chela to take food particles from the substrate or from larger pieces of plants or fungi, applying the two chelicerae in alternation. The innervation of the teeth may relay some information about the quality of the food. By retracting it with the grasped piece of food, the chela will pass the toothed and rigid RU adjacent to its antiaxial side. In a scissoring action, the RU can trim off those parts of the food that extend sideward, as has been suggested by Grandjean (1957a), Dinsdale (1974) and Evans (1992). The resultant particle of food is presumably released by the chela and is small enough to fit in the preoral cavity. These actions may be monitored in two ways. On the infracapitulum, the manubrial fissure af (perhaps functioning like a simplified slit sense

Fig. 30. Details of lateral lips (a–d: horizontal sections; e–j: cross sections; compare Figs. 3h,i, 4c,d, 5, and 26a,b). (a) Tips of lateral lips and rutella (compare Fig. 26a). Rutella are made of strongly sclerotized cuticle. Note dense external layer. The lateral lips bear small denticles (arrows). Insertions of posterior adoral setae (or3). Note dense cuticular material in front of these setal bases (tangential sections through cuticular socket of adoral seta or2; compare Fig. 30g,i). Scale bar: 5 lm. (b) Slightly more dorsal section of anterior tips of lateral lips. Note lamellae on lateral lips paralleled paraxially by small denticles (arrowheads). Scale bar: 2 lm. (c) Setal region as in Figure 30a in higher magnification. Note that dendritic processes reach into the basal parts of the left adoral seta (or3). At right two ciliary segments (asterisk) of the receptor cells belonging to or2 are visible. Scale bar: 2 lm. (d) Ciliary segments (arrows) in higher magnification. Scale bar: 1 lm. (e) Anterior tip of lateral lips in cross section at the level where the small furrow turns antiaxially (compare Fig. 4c,d). Arrowhead indicates small denticles on lateral lips paralleling the lamella. In this region only cuticular structures are present (compare Fig. 30a,b). The flattened distal parts of the spoon-like first adoral setae or1 are sectioned and it is evident that they consist of cuticle only. Note that the flat parts overlap slightly. Scale bar: 2.5 lm. (f) Lateral lips slightly more posteriorly sectioned. Here the lips contain some tissue. A second row of denticles (black arrowheads) appears medially of the first (white arrowheads). Ventrolaterally the cuticle is thicker and more sclerotized. Note ventrally insertion of anterior adoral setae (or1; arrows). A flexible socket is not evident, no dense material around base. The setae are made of cuticle only. Scale bar: 2.5 lm. (g) Lateral lips slightly more posteriorly sectioned. The lamella and the two rows of denticles (white and black arrowheads) on each lip are evident. The bases of the posterior adoral setae (or3) are sectioned. Dense material around bases of setae. Scale bar: 2.5 lm. (h) Cross sections through all three adoral setae. Note that all setae are solid containing no dendrites. Only a fine dense core is present, which is artificially destroyed in the sectioned first adoral seta or1. Scale bar: 5 lm. (i) Detail of Figure 30g in higher magnification. Note that two dendrites enter the setal base of or3. The receptor processes of the more anterior adoral setae are located deeper in the lateral lip. Ciliary segments are sectioned of the receptor cells of or1. Scale bar: 1 lm. (j) Cross section through basal part of posterior adoral seta or3 containing two dendrites. Scale bar: 0.5 lm. LL, lateral lips; lm, lamella on lateral lip; or1-or3, adoral setae (and their innervation) 1–3; RU, rutellum.


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Fig. 31. Infracapitular gland and innervation of supracoxal seta e (a,b,d) horizontal, c,e–h: cross sections). (a) Nuclear region of infracapitular gland. The nucleus is scattered with heterochromatin and contains a large nucleolus. Scale bar: 2.5 lm. (b) Detail of infracapitular gland showing electron-lucent vesicles, rough endoplasmic reticulum and small Golgi body. Scale bar: 1 lm. (c) Extrusion pole of gland and beginning of cuticular duct, which is rather wide here. Scale bar: 2.5 lm. (d) Another aspect of infracapitular gland and its duct sectioned more distally. Scale bar: 5 lm. (e) The distally very thin cuticular duct of the infracapitular gland cut two times close to its opening in front of the mouth and antiaxially of the lamella on the malapophysis. The arrow indicates inferior tendon of depressor muscle close to its connection with the proximal cuticle of the movable digit (md). Scale bar: 10 lm. (f) Posterolateral edges of rostral tectum and infracapitulum. The position of receptor processes connected to the supracoxal seta e is indicated by an arrow (compare Figs. 2e, 3a,d, and 6c). Scale bar: 5 lm. (g) Detail indicated in Figure 31f in higher magnification. A very small dendrite is recognizable (arrow). Scale bar: 0.5 lm. (h) Same region more anteriorly sectioned shows one receptor process (white arrow) close to the base of the seta (indicated by the presence of suspension fibres) reaching into a dense sheath. The black arrow indicates another cell process of unknown nature (another dendrite or sheath/glia cell process?). Scale bar: 0.5 lm. dgi, duct of infracapitular gland; Gb, Golgi body; lm, lamella on malapophysis; LS, labrum; md, movable digit; Mv, microvilli; N, nucleus; nu, nucleolus; opx, posterior oncophysis; Pdp, pedipalp; po.gen, porose area of gena; pS, principal segment of chelicera; rER, rough endoplasmic reticulum; RO, rostrum; rp, rostrophragma; Se, secretion; sf, suspension fibres.

organ), probably measures cuticular stress in the RU. Hence, the mite could avoid breaking the RU if, the material to be cut is too strong. On the cheJournal of Morphology

licera, the lamellated organ probably monitors the activity of the strong levator muscles and the stress impinging on the cuticular elements. This


could prevent damage to these essential elements, because the relative bite forces in A. longisetosus are quite high, well above those known for vertebrate jaws, and close to those generated by decapod chelae (Heethoff and Norton, 2009a). The manubrial fissure af and lamellated organ appear to be the only two sensory structures capable of monitoring stress in feeding actions. Other slit sense organs, such as those ancestrally present on the chelicerae of some other actinotrichid mites, appear to have been lost in oribatid mites. The particulate material in the preoral cavity is probably mixed with fluids coming from the podocephalic glands and/or iGLs, and this suspension must reach the mouth to enter the digestive tract. This can only be achieved by sucking forces provided by the pharynx and its strongly developed musculature (Alberti et al., 2003). To make this force effective, it seems necessary to seal the preoral cavity as completely as possible, but the three-dimensional complexity of the cavity makes this a morphological challenge (cf. Fig. 5e). The chelicerae provide the dorsolateral seal. The LS is positioned in such a way that it probably seals the space between the chelicerae; to make this most effective, it has thin longitudinal lamellae directed lateroventrally, which could touch the paraxial walls of the chelicerae. The LLs and MAs form the ventral seal; they have similar lamellae on their dorsolateral surface, and these probably can touch the ventral surface of the chelicerae. This contact maybe perceivable by the sensory structures in the movable digits of the chelae; alternatively and probably more likely, these structures perceive passing fluids. The members of the paired MAs and LLs closely approach each other medially, so that the preoral cavity is sealed here too. This region may also act in an opposite way, allowing the passage of unwanted material from the preoral cavity by widening the space between the members. It is evident from their cuticular peculiarites that the LLs are slightly flexible at the base. This flexibility may allow the mite to lower or raise the lips, thus bringing the spoon-like (or1) setae into a position that helps to keep food particles in the preoral cavity. If the lips are movable, the forces must come from varying hydrostatic pressures and may depend on cuticular elasticity, because we found no muscles attaching to the lips. Information gained from the sensory properties of the adoral setae might aid this process, but the role of these setae is still obscure, neither indications of mechanoreceptivity (tubular bodies) nor chemoreceptivity (e.g., pores in the setae) were seen. The shape, structure, and position of the enigmatic Tra¨ga˚rdh’s organ suggest a role in this context. As it is evidently not sensory, but probably is indirectly movable and perhaps inflatable by hemolymphic pressure, they could be used to help seal the space between LS and chelicerae (Alberti et al.,

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2004). Such a function was suggested previously by Grandjean (1959). Sealing may also be needed before pharyngeal suction to retain saliva in the preoral cavity. The course of secretions from the acinous podocephalic glands is across the surface of the cervix and anteriorly along the dorsum of the LS; to reach the material in the preoral cavity, it has to pass down the sides of the LS. The salivary secretions of the iGL apparently follow a more precise course guided by the small lamellae on the MAs and LLs. Tra¨ga˚rdh’s organ may thus seal the longitudinal cleft between chelicerae and LS dorsal of the path of these secretions. We do not think that Tra¨gardh’s organs can function like ‘‘tooth-picks’’ as is sometimes suggested (e.g., Walzl, 1987), because distally they appear to be rather weak. A similar role in sealing of the preoral cavity can be suggested for the oncophyses of the chelicerae. Like Tra¨ga˚rdh’s organ, these seem to be modulated by varying hemolymphic pressures (see observations by Baümler 1970). The anterior oncophyses (op’ and, if present, opv) are arranged as modifications of the arthrodial membranes close to the articulation of the movable digits with the principal segments of the chelicerae. These articulations would not work properly if they are blocked by particulate material. Because most oribatid mites are particle feeders, this maybe a serious problem and may explain the pronounced presence of oncophyses in this group of mites. The posterior oncophysis (opx; coming from the trochanteral region) seals the space between the ventral border of the chelicera and the cuticle of the cheliceral groove, thus keeping the space between the chelicerae and the dorsal infracapitulum tight. This might prevent loss of secretions of either the iGLs or the podocephalic system. All these sealing functions likely are effective due to the apparently weak or soft properties of parts of the cuticular structures surrounding the preoral cavity. CONCLUSION AND PERSPECTIVE Following the work of Alberti et al. (2003, 2004), Smrzˇ and Norton (2004) and Heethoff and Norton (2009a,b), our study completes to some extent a structural investigation of the nutritional apparatus of A. longisetosus, which is now the bestknown oribatid mite in this regard. Although detecting a number of new features, including the important discovery of a probable proprioreceptor, the lamellated organ, in the chelicerae, we largely confirmed the fundamental organization of the gnathosoma as described by Grandjean (1957a) and Hammen (1968b, 1989). Frequently, the mouthparts of oribatid mites are regarded as being rather uniform, but in fact they vary greatly in form and probably in function. Families such as Phenopelopidae, Suctobelbidae, and Gustaviidae are just a few examples of groups Journal of Morphology

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with strikingly unusual chelicerae and rutella deviating much from the more frequent chelate dentate type described in this article (e.g. Grandjean, 1957a,b; Alberti and Coons 1999; Norton and Behan-Pelletier, 2009). However, if intricate features such as denticles are taken into account the functional distinctness of this latter type maybe even more evident and may appear less uniform. From the comparative aspect, the presence of the protective rostral tectum (stegasime gnathosoma) in most Oribatida, including A. longisetosus, makes the interpretation of parts of the cheliceral frame difficult. In fact, these parts are largely obscured in this species and to understand the fundamental nature of the cheliceral frame one should study an early derivative (astegasime) oribatid mite, or even species in more distantly related taxa, such as Endeostigmata or certain Prostigmata. Also, an oribatid mite showing a well-developed labiogenal articulation should be investigated to better understand the composition of the infracapitulum. Such an improved understanding would certainly facilitate comparisons with the mouthparts of anactinotrichid mites and other arachnids.

ACKNOWLEDGMENTS The authors appreciate the technical assistance of H. Fischer, E. Lipke, A. Meuche, P. Michalik, and R. Thurmann (University of Greifswald). They thank P. Cloetens and L. Helfen (ESRF) and Paavo Bergmann and Michael Laumann (University of Tu¨bingen) for great support while obtaining the tomographic data on beamline ID19, based on the ESRF project SC2127.

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