An Atlas of Book Lung Fine Structure in the Order Scorpiones (Arachnida)

CARSTEN KAMENZ; LORENZO PRENDINI

doi:10.1206/316.1

How to translate text using browser tools

24 December 2008 An Atlas of Book Lung Fine Structure in the Order Scorpiones (Arachnida)

CARSTEN KAMENZ, LORENZO PRENDINI

Author Affiliations +

Bulletin of the American Museum of Natural History, 2008(316):1-359 (2008). https://doi.org/10.1206/316.1

Abstract

The fine structure of the book lungs of scorpions is diverse and phylogenetically informative, but has not been comprehensively investigated across the major lineages of the order. In this contribution, we present a fully illustrated atlas of the variation in book lung fine structure among 200 exemplars from 100 genera and 18 families of extant scorpions. We document variation in the surface sculpturing of the respiratory lamellae, the edges of the lamellae in the atrial chamber, and the posterior valvelike edges of the spiracles. These data provide insights into the phylogenetic relationships among Recent scorpions at several branches of the tree.

Introduction

According to Weygoldt and Paulus (1979b), Arachnida Lamarck, 1801, represent the monophyletic terrestrial lineage of Metastomata 43 Weygoldt and Paulus, 1979, which includes the extinct aquatic Eurypterida Burmeister, 1894. With few exceptions (e.g., some Acari Sundevall, 1833 and Araneae Clerck, 1757), all arachnid species occupy terrestrial habitats today. There are several challenges associated with a terrestrial lifestyle, arguably the most severe being the evaporative water loss that results from breathing air. Different solutions for breathing air, in the form of internalized respiratory organs, have evolved among different terrestrial animals. Examples include the lungs of vertebrates, the tracheae of insects, and the gills, modified for air breathing, of terrestrial crustaceans.

The respiratory organs of scorpions, Scorpiones C.L. Koch, 1837, and tetrapulmonate arachnids, Megoperculata Börner, 1902, are called book lungs due to the booklike appearance of the layered, sheetlike lamellae (fig. 1). Book lungs are the primary organs for respiration in arachnids, presumed to have evolved as a consequence of terrestrialization in the stem group of Arachnida (Scholtz and Kamenz, 2006). Book lungs are homologous with, and/or functionally substituted by tracheae in entelegyne spiders and apulmonate arachnids, Apulmonata Firstman, 1973 (Hilken, 1998; Weygoldt and Paulus, 1979a).

Fig. 1

Euscorpius carpathicus candota Birula, 10-3: 1 ♀ (HUB): diagrammatic representation of longitudinal histological section through book lung (foreground), showing cuticular structures in three dimensions.

The book lungs of Recent scorpions are homologous (Scholtz and Kamenz, 2006). Their similar structural complexity and identical positions within the fourth to seventh opisthosomal segments (fig. 2) are indicative of common ancestry. Several substructures, present in all scorpions examined thus far, are hypothesized to have been present in the common ancestor of arachnids (Scholtz and Kamenz, 2006). For example, bridging trabeculae (cuticular rods) connecting the proximal surfaces of adjacent lamellae and cellular pillars inside the lamellae (fig. 13) occur in all scorpions that have been studied, and also in tetrapulmonates (Scholtz and Kamenz, 2006). Other characters, e.g., spinelike processes on the lamellar edges, are widespread among scorpions and tetrapulmonates. These characters are synapomorphic for Arachnida, but have undergone secondary modifications in Scorpiones and all remaining terrestrial arachnids, called Lipoctena Pocock, 1893 (Scholtz and Kamenz, 2006).

Fig. 2

Broteochactas delicatus (Karsch, 1879), 1 juv. ♂ (AMNH), KOH-macerated cuticle: dorsal view of internal aspect of ventral mesosoma, showing location of book lungs.

The most obvious feature of the book lungs—their lamellate design (fig. 1)—recalls the book gills of aquatic ancestors. Gills are probably synapomorphic for Euchelicerata 43 Weygoldt and Paulus, 1979. Similar structures are retained in the four species of extant horseshoe crabs, Xiphosura Latreille, 1802. Book lungs are therefore hypothesized to be homologous to the book gills of xiphosurans (Lankester, 1881a, 1881b; Kingsley, 1885) and probably became internalized during the terrestrialization of Arachnida (Weygoldt and Paulus, 1979a).

The importance of book lung morphology for the phylogeny and classification of scorpions was first recognized by Laurie (1896) and Pavlovsky (1926). Pavlovsky (1926) presented a survey of book lung morphology in 35 species from 31 genera and 11 families of scorpions (table 1), based on light microscopy. Except for mention of the shape of the spiracles in various taxonomic and phylogenetic works, no comparative studies of book lung morphology were subsequently conducted until Kamenz et al. (2005). Using scanning electron microscopy (SEM), Kamenz et al. (2005) confirmed Pavlovsky's (1926) discoveries in an examination of the fine structure of book lungs in 29 species from 28 genera and 10 families of scorpions. Due to limitations on the availability of material and constraints on the number of illustrations that could be published, the study by Kamenz et al. (2005) provided only an overview of variation in the book lung fine structure of scorpions; major lineages were not documented, restricting the utility of the data presented for phylogenetic interpretation. The aim of the study presented here is to expand the work of Kamenz et al. (2005) by providing a more comprehensive, fully illustrated survey of book lung fine structure across all the major lineages of scorpions. Exemplar species representing all scorpion families and as many genera as possible were studied and illustrated in the course of this study, providing a standardized framework that can be used to describe and define characters for phylogenetic analyses at multiple branches of the scorpion tree.

Table 1

States of the book lung characters recorded by Pavlovsky (1926) Numbers refer to states defined by Pavlovsky (1926). “Fig.” denotes state indicated only in figures

We present one interpretation of the variation observed by describing three characters, defined by Kamenz et al. (2005), which appear to be phylogenetically informative among the taxa studied (table 2): the surface sculpturing of the respiratory lamellae, the edges of the lamellae in the atrial chamber, and processes on the posterior valvelike edge of the spiracles. We chose these three characters because they are readily apparent with the SEM, and appear to be consistent within species as determined by the examination of multiple specimens. Further genetic, cellular, developmental and ultrastructural studies of the book lungs remain to be undertaken. The standardized illustrations provided in this atlas are intended to serve as a reference for further interpretation and provide a foundation upon which future studies of the book lungs of scorpions, and other arachnids, can be built.

Table 2

States of the book lung characters observed in exemplar species of Scorpiones Lamellar surface (Lam. surf.): simple trabeculae (1); branched trabeculae (2); slender venation (3); ribbed venation (4). Lamellar edge (Lam. edge): bristles (1); spines (2); thorns (3); smooth/wrinkled (4); meandering (5); arcuate bows (6); padded (7). Posterior spiracle edge (Spir. edge): hillocks (1); subconical (2); hairlike (3); flattened (4); scaly (5); chisel-like (6); hexagonal tiles (7); treelike (8); subtree-like (9); polygonal columns (10); clublike (11); spiked macelike (12)

Materials and Methods

Taxon Sampling

The study presented here applies the “exemplar approach” (Yeates, 1995; Prendini, 2001), according to which an exemplar species represents a supraspecific taxon (usually, but not exclusively, in the context of a phylogenetic analysis). The advantages of this method are obvious: (1) it is impossible to gather data from all species, but the use of exemplars enables the variation to be systematically surveyed in a subsample; (2) exemplar species make no assumptions about the monophyly of the supraspecific taxa they represent, allowing monophyly to be rigorously tested during a phylogenetic analysis; (3) multiple sources of data (anatomy, morphology, behavior, DNA, etc.) are readily combined if gathered from the same exemplar species; (4) the use of exemplars restricts data matrices to manageable sizes for computational purposes.

The exemplar approach is more powerful (i.e., it provides a more rigorous test of the hypothesis of monophyly) when more exemplar species are studied per higher taxon, and when these species are selected to represent the maximum morphological diversity within each higher taxon (Prendini, 2001). In the present study, 200 exemplars in 100 genera were selected to represent all 18 scorpion families (table 2; appendix 1) listed in the status quo classification scheme presented by Prendini and Wheeler (2005). Type species of genera were selected preferentially, when available. Multiple species were sampled from diverse and speciose genera, e.g., Tityus C. L. Koch, 1836, to assess the extent of variation among congeners. Contingent on the availability of suitable material, congeneric exemplars were selected to maximize morphological diversity (Prendini, 2001). In this atlas of book lung fine structure, data gathered from the exemplar species selected are presented and discussed by family for operational purposes, with putative phylogenetically related families (e.g., buthoids, chactoids, and scorpionoids) discussed in sequence, rather than in alphabetical order. Within each family, the figures for the species are presented in alphabetical order by genus. This study makes no assumptions about the monophyly or content of these families, however. It serves primarily to document the variation in book lung fine structure and stimulate further investigation into the subject.

Material, Preparation, and Terminology

Material examined was borrowed from or studied in situ at the following collections: American Museum of Natural History, New York (AMNH); Museum National d'Histoire Naturelle, Paris (MNHN); Museum für Naturkunde, Berlin (MfN), bearing ZMB accession numbers. Available collection data for voucher specimens studied are provided in appendix 1. Mounted SEM stubs are also deposited in these collections.

Standard SEM techniques were used for the preparation and investigation of book lungs. Book lungs were dissected from scorpions preserved in 70–100% ethanol. Several specimens were fixed in Bouin's fluid (15 ml saturated picric acid, 5 ml 35% formaldehyde, and 1 ml acetic acid) or using a method adapted by Karnovsky (1965), in a solution of 0.1 M phosphate-buffered saline (PBS: 10.9 g Na₂HPO₄ [anhydrous], 3.2 g NaH₂HPO₄ [anhydrous], and 90 g NaCl in 1000 ml distilled water, pH 7.2), 3.7% formaldehyde, and 2.5% glutaraldehyde plus postfixation in 2% osmiumtetroxide. Bouin's fluid was washed out with 70% ethanol and Karnovsky's fixatives using PBS first and 40% ethanol in subsequent steps. The ethanol concentration was sequentially increased to 100% for dehydrating the tissues. The ethanol was then removed in critical point dryers, BAL-TEC CPD 030 at the Humboldt-Universität, Berlin (HUB), Emitech K850 (MNHN), or in an oven (AMNH) at 60°C.

After dehydration and prior to examination with the SEM, the lungs were dissected to expose the interior structures before mounting on common stubs. The prepared lungs were then sputter-coated with gold template in a BAL-TEC SCD 005 (HUB), or with gold-paladium in a Polaron SC 7640 (MfN), Joel JFC-1200 Fine Coater (MNHN), or DENTON Desk II (AMNH). The following SEMs were used in the course of the study: a Leo 1540 VP (MfN), a Joel JSM-840 A (MNHN), and a Hitachi S 4700 (AMNH). Images of the book lungs prepared for each species studied were assembled into plates using Adobe Photoshop and Illustrator. Terminology for book lung structures follows Kamenz et al. (2005), a detailed explanation of which follows in the section on Fine Structure of Scorpion Book Lungs.

Results

Gross Morphology and Function of Scorpion Book Lungs

Position of book lungs

The respiratory organs of scorpions occur on the inner surface of the ventral exoskeleton in the mesosoma (fig. 2). A pair of book lungs is situated laterally on the sternites of the third to sixth visible opisthosomal segments (identical to the fourth to seventh embryological opisthosomal segments; Brauer, 1895; Simonnet et al., 2006), following the pectinal segment. A mostly slitlike, in some cases oval or almost circular spiracle (fig. 3) demarcates the posteromedial margin of the book lung. The spiracle is the respiratory opening leading into the atrium of the book lung. The distance from the spiracle to the anterior margin of the sternite is approximately equal to three times the distance between the posterior margin and the spiracle. The longitudinal axis of the spiracle is inclined toward the transverse axis with the medial end lying anteriad.

Fig. 3

Brotheas granulatus Simon, 1877, 1 ♂ (MNHN RS 8508): ventral view of dextral surface of sternite, showing position of spiracle, slanted with anterior margin (top) toward the midline (left).

Lung morphology

Each book lung consists of a stack of leaflike lamellae situated above the ventral sternite (Treviranus, 1812; figs. 1, 4). We define the lamellae as a double layer of cuticle that is flooded by hemolymph and surrounded by air. The adjacent layers of cuticle surrounding the air between the lamellae are saclike in all terrestrial arachnids and are therefore called air sacs (fig. 5). The air sacs are held in place by bandlike ligaments (fig. 6) from an overlying layer of connective tissue in the hemolymph space, called the fenestrated membrane (Farley, 1990; fig. 7). The fenestrated membrane covers the lung from above and is held to the pericard of the heart by the hypocardial ligament (figs. 7, 8).

Fig. 4

Hottentotta jayakari (Pocock, 1895), 1 subad. ♀ (HUB): lateral view of longitudinal section through book lung, showing position of book lung morphology characters discussed in the atlas (arrowheads): lamellar surface (1); distal lamellar edge (2); posterior spiracle edge (3); (A–C) arrangement of characters in the plates, (A) lamellar surface, (B) distal lamellar edge, (C) posterior spiracle edge; arrowheads and arrows indicate characters and states.

Fig. 5

Cercophonius sulcatus Kraepelin, 1908, 1 ♂ (AMNH [LP 1618]): dorsal view of lateral part of sternite, illustrating shape of seven median air sacs of book lung.

Fig. 6

Hadogenes sp., 1 ♂ (HUB): ventral view of book lung, with fenestrated membrane removed, showing ligaments holding air sacs.

Fig. 7

Hadogenes sp., 1 ♂ (HUB): dorsolateral view of fenestrated membrane, covering sternite and book lung.

Fig. 8

Hadogenes sp., 1 ♂ (HUB): median lateral view of body cavity, with midgut removed.

The lamellae are not in direct contact with the inner cuticular surface of the sternites, but are separated from it by a flat layer of the epidermis and a narrow hemolymph space (fig. 1). The stack of lamellae is slanted dorsoventrally with the medial side of the book lung situated closest to the inner surface of the sternite and the uppermost lamella situated on the lateral margin of the sternite (fig. 9). The proximal surfaces of the parallel lamellae are shallowly inclined, each lamella sloping slightly from dorsomedial to ventrolateral, to almost horizontal. The distal edges of the lamellae are more steeply inclined in the same direction. There are fewer lamellae, aligned almost horizontally, in smaller species. The lamellae are more numerous and inclined, to almost vertically aligned, in larger species.

Fig. 9

Broteochactas delicatus (Karsch, 1879), 1 ♂ (AMNH), KOH-macerated cuticle: dorsal view of lateral part of sternite, showing cuticular parts of book lung.

Each air sac (fig. 5) has the shape of an almost straight or bent oval that is distally truncated. The straight distal edge of one lamella merges with the distal edge of the adjacent lamella to form the entrance of an air sac (fig. 1). All the distal lamellar edges together form a grill, merging continuously into the wall of the atrium. The atrial chamber (figs. 1, 4) is lined by cuticle, which is strongly folded and covered with small wartlike cuticular processes (fig. 10). An area of almost unfolded and smooth, wart-free cuticle occurs laterally at the regions of transition (with respect to the axis of the spiracle) where the atrium joins the posterior edge of the spiracle (figs. 1, 11). Cuticular processes, shaped like shallow bars or flat lobes (fig. 11), occur on the central region of transition from the atrial wall to the posterior spiracle edge. The shape of these processes changes closer to the posterior spiracle edge, where they transform into the taxon-specific structures described in more detail below.

Fig. 10

Didymocentrus lesueurii (Gervais, 1844), 1 ex. (MNHN): view from lamellae toward atrial wall, showing transition to posterior spiracle edge.

Fig. 11

Vaejovis spinigerus (Wood, 1863), 1 ♂ (AMNH [LP 1811]): anterior view of posterior spiracle edge with transition to sternite and wall of atrium, anterior parts of sternite removed. Note change in shape of cuticular processes from flat-oval (box) to subconical structures on spiracle edge (character 3, denoted with arrowhead); a movable flap normally closes the spiracle unless pulled open by contraction of the poststigmaticus muscle. Inset: Urophonius iheringii Pocock, 1893, 1 ♀ (AMNH [LP 3457]): magnified posterior view of flat-oval processes on transition from spiracle edge to atrial wall.

Lamellae

Each lamella comprises two very thin, parallel layers of epidermal cells on both outer surfaces (Scholtz and Kamenz, 2006). Each layer of epidermal cells is supported by a thin layer of cuticle that separates the inner hemolymph space of the lamellae from the outer air space (figs. 1, 12). The hemolymph space, inside the lamella, is maintained at a uniform width by cellular pillars (figs. 1, 13). These cellular pillars are situated at regular intervals across the inner surfaces of the lamellae, providing a constant space for hemolymph between the inner surfaces of the two adjacent cuticle layers within each lamella. Each pillar comprises two or more cells, which originate on adjacent surfaces and meet each other in the middle, and is filled almost entirely by the nuclei of the pillar cells (Scholtz and Kamenz, 2006).

Fig. 12

Euscorpius carpathicus candiota Birula, 1903, 1 ♀ (HUB): lateral view of proximal parts of book lung (longitudinal section) showing lamellae and blind ends of air sacs.

Fig. 13

Euscorpius flavicaudis (DeGeer, 1778), 1 ex. (MNHN): internal view into lamella showing cellular pillar in hemolymph space.

The cuticular surface of the lamellae is covered with cuticular structures that prevent the air space from collapsing. The proximal one-third to one-fifth of the lamellar surface is covered, in all scorpions, with bridging trabeculae (described further below). The distal two-thirds to four-fifths of the lamellar surface are covered with one of two kinds of cuticular structures that are not connected to the adjacent lamellae (Laurie, 1896): reticulate venation or papillate trabeculae. Venation, observed in buthoid scorpions, covers both sides of the lamellae (fig. 15C, D). Papillate trabeculae (fig. 15A, B), observed in nonbuthid scorpions, occur only on the ventral surfaces of the lamellae; their free ends are directed toward the adjacent lamellar surfaces.

Bridging trabeculae

Trabeculae are cuticular processes (figs. 12, 15) that separate adjacent lamellae from one another and prevent collapse of the air space with consequent reduction in the respiratory surface. Bridging trabeculae (fig. 12) are unique in forming continuous columns between adjacent lamellae. Due to their equal size and perpendicular arrangement at regular intervals, bridging trabeculae hold the lamellae at a very constant distance apart, resulting in the parallel appearance of the proximal surfaces of the lamellae.

Bridging trabeculae are present in the book lungs of all arachnids (Scholtz and Kamenz, 2006) and occur on the proximal surfaces of the book lung lamellae of all scorpions (figs. 1, 12), regardless of the presence of venation or trabeculae on the distal surfaces of the lamellae. Bridging trabeculae are situated in a bandlike zone along the anterior to medial margin of each lamella (fig. 5).

Gas exchange

Air flows through the spiracle into the atrium (figs. 1, 4) of the book lung and from there into the air sacs between the lamellae, where it is separated from the hemolymph only by a single layer of epidermis and cuticle. Gas exchange, by diffusion to and from the hemolymph inside the lamellae, occurs across this extremely thin lamellar surface. Hemolymph flows through the lamellae from the ventral hemolymph sinus to the lateral pneumocardial sinus (fig. 8) receiving oxygen and releasing carbon dioxide along the way. The oxygenated hemolymph is transported dorsally to the heart and then distributed throughout the body.

Spiracles and ventilation

Each spiracle (fig. 3) is a small circular, oval or slitlike opening to the book lung in the sternite. The spiracle regulates the influx of gases and can be closed to prevent loss or penetration of gases, liquids, and solid particles. Cuticular processes on the spiracle and the distal edges of the lamellae probably reduce the penetration of dust particles.

Opening of the spiracle is regulated by sensory cells detecting the concentration of carbon dioxide and the pH of the hemolymph (Farley, 1990). The poststigmaticus muscle (fig. 1), attached to the posterior edge of the spiracle (Fraenkel, 1930; Pavlovsky, 1926; Du Buisson, 1925; Vyas and Laliwala, 1972, 1976; Farley, 1990), connects to the posterior part of the sternite or the posterior intersegmental membrane (fig. 14). The spiracle is opened on contraction of this muscle, which causes the posterior edge to roll or flap back, away from the anterior edge. This mechanism serves to regulate the partial pressure of oxygen and carbon dioxide (Fincke and Paul, 1989). Closure of the spiracle is a passive process. The posterior edge of the spiracle is flexible and closes the spiracle on relaxation.

Fig. 14

Broteochactas delicatus (Karsch, 1879), 1 ♂ (AMNH), KOH-macerated cuticle: dorsal view of attachment site of poststigmaticus muscle on posterior edge of book lung spiracle. Posterior edge normally closes spiracle unless pulled open by contraction of poststigmaticus muscle.

Whether gas exchange in scorpions occurs by diffusion or active ventilation has not been conclusively demonstrated. Fraenkel (1930) described pumping movements of the book lung due to pulsation of the heart, transmitted via pneumocardial bands, the hypocardial ligaments described by Farley (1990), and ventilation by muscles attached to the posterior spiracle edge and the atrium. However, Fincke and Paul (1989) contradicted the suggestion of effective ventilation. Their physiological investigations on the mygalomorph spider, Eurypelma californicum Ausserer, 1871, the entelegyne spider, Cupiennius salei (Keyserling, 1877), and the scorpion, Pandinus imperator (C.L. Koch, 1841) did not reveal any rapid, rhythmic movements of the spiracle in dormancy or during phases of high activity as occur, for example, in vertebrates. Rhythmic stirring of the hemolymph stream through the book lung, generated by pulsation of the heart, might support gas exchange (Farley, 1990), but this remains to be demonstrated.

Fine Structure of Scorpion Book Lungs

Lamellar surfaces

The distal lamellar surfaces of scorpions may be covered with two distinct kinds of structures (character 1; fig. 15): reticulate venation or cylindrical, rodlike (papillate) trabeculae. Distal, in the sense used here, refers to the main part of the lamellar surface, distinguishing it from the surfaces along the proximal edges of the air sacs (fig. 5), where adjacent lamellae are connected by bridging trabeculae. There are two distinct states for both structures (reticulate venation and papillate trabeculae), resulting in four states for the character: simple trabeculae (state 1); branched trabeculae (state 2); slender venation (state 3); ribbed venation (state 4).

Fig. 15

Book lung, lamellar surface (character 1): A. Paruroctonus becki (Gertsch and Allred, 1965), 1 juv. ♀ (AMNH [LP 4991]), state 1: simple trabeculae (arrow); B. Pandinus cavimanus (Pocock, 1888), 1 ♀ (AMNH [LP 3259]), state 2: branching trabeculae (arrow), branch (arrowhead); C. Parabuthus leiosoma (Ehrenberg, 1828), 1 ♀ (AMNH [LP 1845]), state 3: slender venation (arrow), perpendicular ridge (arrowhead); D. Zabius fuscus (Thorell, 1876), 1 juv. ♀ (AMNH [LP 1759]), state 4: ribbed venation, polygonal surface (arrow), parallel ribs (arrowhead); numbers in arrows refer to character states.

The two types of papillate trabeculae were previously described by Kamenz et al. (2005). Simple trabeculae (state 1) are observed in most nonbuthid scorpions. These trabeculae are blunt or knoblike apically. Branched trabeculae (state 2) are slender columns with as many as five narrower branches apically.

Slender venation (state 3), first described by Kamenz et al. (2005), consists of branching, reticulate veins that enclose slender areas directed toward the lamellar edges. Ribbed venation (state 4), identified here for the first time, is characterized by veins surrounding polygonal surfaces, which are broader than the surfaces characteristic of state 3 but become consistently more slender near the distal lamellar edges. Each polygonal surface contains up to five parallel ribs, directed toward the distal lamellar edge. Ribbed venation is a new state, not previously mentioned by Kamenz et al. (2005).

Distal edges of lamellae

Structures on the lamellar edges (character 2) differ significantly from those on the lamellar surfaces and are restricted to the immediate edge of the lamella (fig. 16). Although a gradation is sometimes observed from structures on the lamellar surfaces to those on the lamellar edges, the change is usually rather abrupt. Seven different states of structures on the lamellar edge can be distinguished, six of which have already been described by Kamenz et al. (2005): bristles (state 1); spines (state 2); thorns (state 3); smooth/wrinkled (state 4); meandering (state 5); arcuate bows (state 6); padded (state 7). Padded structures are described here for the first time.

Fig. 16

Book lung, distal lamellar edge (character 2): A. Pandinus cavimanus (Pocock, 1888), 1 ♀ (AMNH [LP 3259]), state 1: bristles on lamellar edge (arrow); B. Timogenes mapuche Maury, 1975, 1 ♂ (AMNH [LP 4312]), state 2: spines on lamellar edge (arrow), narrow base of spine (arrowhead); C. Orthochirus innesi Simon, 1910, 1 ♀ (MNHN RS 5440), state 3: thorns on lamellar edge (arrow), broad base of thorn (arrowhead); D. Rhopalurus princeps (Karsch, 1879), 1 ♂ (AMNH [LP 1566]), state 4: smooth (arrow) to wrinkled (arrowhead) lamellar edge; E. Iurus dufoureius asiaticus Birula, 1903, 1 juv. (HUB), state 5: meandering, winding bulges (arrowhead) surrounding winding surfaces (arrow); F. Liocheles waigiensis (Gervais, 1843), 1 ♀ (AMNH [LP 1502]), state 6: arcuate bows (arrow); G. Chaerilus sp., 1 ♀ (MNHN RS 0607), state 7: pillowlike pad (arrow), perforated network (arrowhead); numbers in arrows refer to character states.

The first three states of lamellar edge structures are similar. Bristlelike (state 1) and spinelike (state 2) structures have narrow bases, are rather thin, and taper slightly at the ends. Both structures occur on lamellae covered with trabeculae, but are readily distinguished from the latter, which are shorter and more cylindrical in shape. Whereas bristles are soft and flexible, spines are rigid and straight. Bristles point in all directions and often occur side by side around the semicircular (cross section) lamellar edge. Spines are usually arranged almost parallel to one another, projecting away in the same plane as the lamella. The third state of similar structures, thorns (state 3), are rather short and usually exhibit a broad base. Thorns usually arise from wrinkled venation and occur more sporadically along the lamellar edges than spines.

Venation often merges with a smooth or sometimes wrinkled (state 4) lamellar edge. Wrinkles may be very deep but are clearly distinct from meandering structures (state 5), which occur together with trabeculae on the lamellar surfaces. Meandering structures consist of more or less slender areas winding along the lamellar edges, surrounded by winding, raised bulges, sometimes enclosing groups of small spines.

The remaining states of lamellar edges are quite different from one other and from all others. Arcuate bows (state 6), the ends of which merge with the lamellar edge to create a complex, irregular reticulate vault, are always observed together with trabeculae on the lamellar surfaces. Flat or pillowlike pads (state 7), observed only in Chaerilus Simon, 1877, cover the lamellar edges with a deeply perforated network.

Posterior edge of spiracle

The posterior spiracle edge (character 3) exhibits the greatest diversity of structures (fig. 17). Twelve character states, five of which (states 8–12) are described here for the first time, can be clearly defined: hillocks (state 1); subconical (state 2); hairlike (state 3); flattened (state 4); scaly (state 5); chisel-like (state 6); hexagonal tiles (state 7); treelike (state 8); subtree-like (state 9); polygonal columns (state 10); clublike (state 11); spiked macelike (state 12). The first three character states are simple processes, the others more complex structures containing distinct substructures.

Fig. 17

Book lung, posterior spiracle edge (character 3): A. Karasbergia methueni Hewitt, 1913, 1 ♂ (AMNH [LP 1724]), state 1: hillocks (arrow); B. Orthochirus innesi Simon, 1910, 1 ♀ (MNHN RS 5440), state 2: subconical processes (arrow); C. Centromachetes pocockii (Kraepelin, 1894), 1 ♀ (ZMB 35145), state 3: hairlike processes (arrow); D. Urodacus yaschenkoi (Birula, 1903), 1 ♂ (AMNH [LP 1659]), state 4: flattened processes (arrow), pointed tips (arrowhead); E. Bothriurus coriaceus Pocock, 1893, 1 ♂ (ZMB 8322), state 5: scaly processes (arrow); F. Liocheles waigiensis (Gervais, 1843), 1 ♀ (MNHN RS 8350), state 6: chisel-like processes (arrow), distinct teeth (arrowhead); G. Scorpio maurus subsp., 1 ♀ (MNHN), state 7: hexagonal tiles (arrow), columellar shaft (arrowhead); H. Urophonius iheringii Pocock, 1893, 1 ♀ (AMNH [LP 3457]), state 8: treelike processes (arrow), branches (arrowhead); I. Centromachetes obscurus Mello-Leitão, 1932, 1 ♂ (AMNH [LP 2436]), state 9: subtree-like processes (arrow), short branches (arrowhead); J. Paruroctonus stahnkei (Gertsch and Soleglad, 1966), 1 ♂ (AMNH [LP 3566]), state 10: polygonal columns (arrow); K. Teuthraustes atramentarius Simon, 1878, 1 ♀ (MNHN RS 0784), state 11: clublike processes (arrow), slender shaft (arrowhead); L. Uroctonites huachuca (Gertsch and Soleglad, 1972), 1 ♀ (AMNH), state 12: spiked macelike processes (arrow), spikes (arrowheads); numbers in arrows refer to character states.

Kamenz et al. (2005) described simple cuticular processes on the posterior edge of the spiracle, ranging from small, shallow hillocks (state 1), through subconical processes that are higher than wide (state 2), to very long, hairlike processes (state 3). Kamenz et al. (2005) described lobelike, flattened processes, the tips of which vary from a single blunt end to several pointed tips, as state 4. The flattened structures described by Kamenz et al. (2005) are sometimes broadened, and overlap one another to a lesser extent than scales (state 5). Chisel-like structures (state 6) are characterised by a nearly cylindrical shaft with a flattened tip, bearing a few distinct teeth. The flattened, scaly and distinct chisel-like structures appear to be points on a continuum of variation.

The hexagonal pillars (state 7), described by Kamenz et al. (2005), are here renamed hexagonal tiles to avoid confusion with the pillar cells inside the lamellae (Scholtz and Kamenz, 2006). This amended term refers to the regular arrangement of each hexagonal plate in a particular surface, and the very regular, jointlike gaps between them. The height of these structures varies from almost zero, when only the hexagonal plates are visible, to about five times the diameter of the plate. The more slender shaft is usually cylindrical to hexagonal.

Treelike structures (state 8), i.e., spinelike to hairlike cuticular processes with several branches, are observed on the posterior spiracle edge of the bothriurid scorpion, Urophonius iheringii. Structures on the posterior spiracle edge of the bothriurids, Centromachetes obscurus and Timogenes mapuche, exhibit similar outgrowths, but the branches on these structures are short and thornlike. These subtree-like structures (state 9) may be an intermediate step in the transformation between subconical and treelike structures.

The structures on the posterior spiracle edge of Paruroctonus Werner, 1934 are superficially similar to hexagonal tiles (state 7). However, the apical plates of these structures are smaller, almost as wide as the shaft, irregular in shape, and do not all lie in the same plane. The gaps between the plates are much larger and less regular than in state 7. These structures, not considered to be homologous with the hexagonal tiles, are termed polygonal columns (state 10).

A unique, distally expanded clublike structure (state 11) is observed on the posterior spiracle edge of Teuthraustes Simon, 1878. Another unique structure, a spiked mace, shaped somewhat like a flattened hillock, densely covered with subconical thorns (state 12), is observed on the posterior spiracle edge of Uroctonites huachuca.