Description of the first species of Glomeridesmida from Thailand (Diplopoda, Glomeridesmida, Glomeridesmidae)

Abstract With three genera and 35 previously known species from India, SE Asia, Central and South America, Glomeridesmida are one of the least diverse Diplopoda groups. Here we describe Glomeridesmus siamensissp. nov., the first species of the order Glomeridesmida from Thailand. The geographically nearest confamiliar species have been described from southern India, Sumatra and Java. The species is described combining photographs, light- and scanning electron microscopy of mature and younger males, females and juveniles. Several characters are illustrated for the first time for an Asian representative of the family Glomeridesmidae. In addition to the type locality of G. siamensissp. nov. from Krabi province, locality data of unidentified Glomeridesmus from Thailand are also given. These data are providing further evidence that the Glomeridesmida are not uncommon, but overlooked as they are small and difficult to collect. The unusual telopods and other morphological characters of G. siamensissp. nov. differ considerably from the few Glomeridesmus males described from Central and South America as well as from India, but the unclear status of two generic names available for species from Indonesia prevents us from adding another generic name to this small and understudied order.


Introduction
The third smallest millipede order (Diplopoda) in terms of diversity is the Glomeridesmida with 35 described species in three genera (Jeekel 2003;Iniesta et al. 2012;Enghoff et al. 2015;Mauriès 2020). The Glomeridesmida are currently classified as the basalmost order within the Pentazonia (Blanke and Wesener 2014), which also includes the volvatory (rolling-up) millipede orders Glomerida and Sphaerotheriida, but might actually be the sister-group to the Holarctic pill millipedes, the Glomerida (Oeyen and Wesener 2018). The Glomeridesmida is divided into two families (Enghoff et al. 2015), the obligate termitophilous Termitodesmidae (5 species) and the Glomeridesmidae (30 species). While the Termitodesmidae are restricted to India and continental Southeast Asia (Malaysia and Vietnam), the Glomeridesmidae show a much wider and disjunct distribution with representatives in the Caribbean, Central America and the northern half of South America, India, Southeast Asia (Shelley and Golovatch 2011) and Oceania (Shelley 2011). No described Glomeridesmus species is known from the Southeast Asian states of Thailand (Enghoff 2005), Laos (Likhitrakarn et al. 2014), Cambodia (Likhitrakarn et al. 2015) or Myanmar (Likhitrakarn et al. 2017). As recently shown, Glomeridesmidae are not rare in Javan rainforests (Hilgert et al. 2019).
The unusual appearance of the Glomeridesmida might partly resemble the groundplan of chilognathan Diplopoda (Enghoff 1990). While the first species of a glomeridesmid was described in 1844 (Gervais), the first male specimens were not encountered until almost 100 years later (Loomis 1936) and still needed another five years to be recognized as such (Carl 1941). Until then, the exceptionally large and conspicuous female ovipositors were interpreted as male 'penes'. However, either live observations, or even male specimens of Glomeridesmida are still unknown for nearly all species or very rare (Mauriès 1980(Mauriès , 2020Iniesta et al. 2012). The male telopods (terminal legs modified for mating) provide the most important taxonomic characters in pentazonian millipedes at the generic level (Mauriès 2005;Wesener and VandenSpiegel 2009;Oeyen and Wesener 2018). However, telopod characters are still only known from nine of the 35 glomeridesmid species (Jeekel 2003). Only five species have been extensively described, based on numerous specimens, and thus allowing for detailed comparisons to be made: a single species each from India (Carl 1942), Central America (Mauriès 1980) and a cave in Brazil (Iniesta et al. 2012), and two species recently described from French Guiana (Mauriès 2020). However, males are still undescribed for SE Asian glomeridesmids. Reliable taxonomic characters of the Glomeridesmidae on the species-or generic-level, aside from habitus, body size and colour pattern, have not been established yet. Therefore, we document as many potential taxonomic characters as possible to allow future comparisons with other Glomeridesmida species. The first representative of the group from Thailand is described here based on male and female specimens: somatic as well as sexual characters are described in detail.

Preparation, illustrations and terminology
Specimens were preserved in 95% ethanol and are stored in the collections of the ZC-SWU and ZFMK. Dissections and examinations were done using an Olympus SZX12 stereo-microscope. For scanning electron microscopy, the samples were dehydrated via an ethanol series, mounted with conductive tape on a stub and dried overnight. The stub was sputter-coated with gold with a Cressington 108 auto sputter coater. Images were obtained using a Zeiss Sigma 300 VP SEM. Multi-layer photographs were taken with a Leica Z6 Imaging-System based at the ZFMK. Stacked images were put together using the Zerene Stacker version 1.04. All images were later modified using Gimp 2.10 and assembled into plates using Inkscape 1.0.1.
Terminology of morphological characters follows Iniesta et al. (2012), for other morphological characters the terminology of Sphaerotheriida (Wesener 2016) and Glomerida (Oeyen and Wesener 2018) was utilized. Usually in pentazonians (e.g. Wesener 2016), specimens with an incomplete number of segments and/or leg pairs are defined as juveniles, while specimens with the full number of segments and legs, but immature secondary sexual characters, are named immatures. This distinction into juveniles and immatures is difficult in Glomeridesmida whose development is only rudimentarily known (Enghoff et al. 1993;Mauriès 2020). Here, we call specimens without the full complement of leg pairs or segments, but with visible ovipositors or telopods immatures and smaller specimens without visible secondary sexual characters juveniles. Additional specimens of undescribed species are housed in the collection of the NHMD. Remarks. The family Glomeridesmidae was partly re-characterized recently (Iniesta et al. 2012;Enghoff et al. 2015).
Distribution. Central America and northern half of South America and the Caribbean (26); India (1); Indonesia (2); Thailand (1 described below). Unidentified specimens from various localities in SE Asia and Oceania (Shelley 2011).
Comment. The position of the new species in the genus Glomeridesmus is tentative at best. As two genus names (Zephroniodesmus, Javadesmus) synonymized with Glomeridesmus (Loomis 1936, Carl 1942 are available for SE Asian Glomeridesmidae and were based on female specimens, both require redescriptions based on topotypic male material. Therefore, we hesitate to introduce a third genus name, which might later turn out to be synonymous. The species from Thailand described here differs significantly from the known Indian and American species at least in the telopod morphology, and potentially in other previously undocumented morphological characters. Suea), overgrown rocks next to rubber plantation, 08°07'23.8"N, 098°55'18.9"E. leg. 27.VII.2017, Wesener, Wongthamwanich, Nawanetiwong, Moritz.
Head: General shape typical for the family (Figs 1D, E, 2C). Epicranium glabrous; frons, clypeus and labrum with several isolated setae (Fig. 2C). Antennae widely separated by a distance slightly longer than twice width of first antennomere (Fig. 1A, E). Antennae and organ of Tömösváry both surrounded by individual cuticular rims, both on an elevated plateau (Fig. 2D). Genae (area below the antennae) almost non-existent, with incisura lateralis. Undivided basal joint of mandible large and visible in dorsal view.
Tömösváry organs as large as antennal base, of well-rounded oval shape, interior covered by a sclerotized plate; surrounded by cuticular rim and several very short setae (Fig. 2C, D).
Mandible: Basal joint massive, undivided (Figs 1D, E, 2C). Apical joint (mandibular gnathal lobe) damaged during preparation, but with long slender external tooth and a long condylus. Inner tooth 4-combed. Seven rows of pectinate lamellae, large intermediate area covered by scale-like spines. Additional intermediate area located at a lower level next to molar plate with more elongated spine-plates. Molar plate plane, without indentations or grooves, margins entirely surrounded by thick membranous fringes (Fig. 6D).
Tergites 2-19 (20) very thin, difficult to distinguish from one another. Width from tergite 1 to 8 gradually increasing, then decreasing to last tergite (Figs 1A, B, 7A). Each tergite bearing 6-8 longitudinal striae. Distances between striae increasing towards posterior margin. Surface of tergites with sparse isolated setae (Fig. 7A, B). Tergite 11 onwards posterior-lateral edge pronounced into a sharp-edged tip, becoming a longer and spine-like process at tergite 17. Limbus (posterior margin of tergite) smooth, without any structures. Endotergum (underside of posterior margin of tergite) smooth area without any specific structures (Fig. 7C). Posterior margin of tergite 19 and 20 with several short teeth (Fig. 7D) Pleurites of rectangular shape, posterior margin overlapping first third of subsequent pleurite (Fig. 7B), wider than long. Pleurites similar to one another, but last pleurite on posterior margin with a well-rounded central indentation, providing space for the movements of the last leg.
Penultimate leg with coxosternite narrow, with stigma opening and sternal part located below (instead of lateral to) of coxal part. Femur slightly longer than prefemur, 1.3 × longer than wide, tarsus shorter, >7 × longer than wide, apically with claw, apical spine and paronychium (Fig. 3E, F).
Anal shield: glabrous, with a well-rounded edge. Subanal plate located behind last pair of legs, large and hyaline.
Sexual characters: Female: second coxae on posterior side with prominent ovipositors protruding back to leg pair 5. Coxa protruding mesally as a short lobe. Ovipositors basally supported by an undivided plate (sternite?) (Fig. 4C). Ovipositor with a basal part consisting of 21 or 22 segments of (eversible?) half-rings, each carrying isolated setae in a regular distance to each other. Half rings anteriorly and posteriorly interrupted by two different, much slender tubes, also consisting of half-rings, running along the whole length of the ovipositor. Apical part of ovipositor with opening surrounded by four larger plates, each arising out of a tube of rings. All four plates covered by longer setae (Fig. 4D). Male: second coxa with gonopore located mesally (Fig 3C). Gonopore flanked by two sclerotized, plates resembling an open bivalve shell. Apical part of both plates with 2 or 3 longer setae (Fig. 5C).
Male telopod consisting of syncoxite with inner horns and 4 podomeres (Figs 1C, 5A, D). Syncoxite covering basal podomeres laterally and in anterior view, medially rising into a smooth glabrous process. Process apically with two long inner horns; horns basally fused, completely separating more apically, diverging and running parallel to one another. Each horn apically slightly widening and spoon-shaped. Whole surface of horns sparsely covered by isolated, minute setae (Fig. 5D).
Podomere 2 wide, rectangular, apically with a large membranous area and mesally with a long and slender process. Membranous area well rounded, consisting of several inverse membranous folds. Slender process strongly elongated, as long as podomere 2, protruding between movable and immovable finger, inner surface excavated (Fig. 5A, B).
Podomere 3 long and slender, only 1/3 of width of podomere 2, inserting laterally on podomere 2. Posterior-lateral aspect of podomere 3 in apical part with slender, finger-shaped and well-rounded process called immobile finger, which makes up ca. half the length of podomere 3, inner surface of immobile finger excavated. Length of podomere 3, without immobile finger, 2 times longer than wide, with few isolated setae at margins in apical half (Fig. 5A, B). Immobile finger protruding up to 3/4 of length of podomere 4, called mobile finger (Fig. 5A, B).
Mobile finger (podomere 4), articulated to podomere 3 at base of immovable finger (Fig. 5A, B), slender and glabrous, 5 × longer than wide, posteriorly with an excavated area; at apex with a single long spine reaching 2/3 of length of immobile finger Immature male. The immature male has the same number of tergites, but one walking leg pair less than the mature male. The immature male is almost 1/3 shorter than the mature male. Coxal pouches starting at leg pair 9 as in mature male. Last pleurite with small well-rounded indentation at posterior margin. Telopod only slightly different from mature male: process of podomere 2 shorter, podomere 3 and 4 slenderer, immobile finger almost protruding up to apical end of movable finger.
Ecology. All specimens were collected by hand in the morning during rainy season in Krabi province, the second reported area for Glomeridesmida in Thailand (the first in Shelley 2011). They were found in a karst landscape covered with evergreen forest (Fig. 8A, B) in soils at a depth of 10-20 mm near horizontal roots on a partially overgrown rock. Despite numerous attempts, no Glomeridesmus was discovered outside the less than 30×30 centimeter of habitat, showing that their distribution might be dependent on some unknown microhabitat requirements. The habitat was a flat area on a western aspect (Fig. 8C). Average air temperature and relative humidity during observation was approximately 29 °C and 85%, respectively. The specimens were fast moving (at least as fast as Chordeumatida), capable of bending their flexible body 180° Figure 5. Glomeridesmus siamensis sp. nov., male holotype (ZCSWU Myr D000011), male sexual characters A telopod, anterior view B telopod, posterior view C gonopore on leg 2, posterior view D inner horns, anterior view. Abbreviations: I -IV = telopoditomeres, ff = immobile finger, gp = gonopore, ih = inner horns, ma = membranous area, pr = projection. Scale bars: 50 µm (A, B, D), 20 µm (C).  to quickly change directions. Furthermore, the male holotype carried an 'amphoromorph' fungus on one of its legs (Fig. 3B).
Additional locality data of unidentified Glomeridesmus from Thailand.

Taxonomic characters in the Glomeridesmida
Descriptions of Glomeridesmus species were previously based on dubious somatic characters, i.e. species were most often separated by head morphology, body size, coloration and geography alone (e.g. Loomis 1964). The apparent paucity of males in Glomeridesmus populations makes precise taxonomic descriptions and comparisons across taxa challenging. Aside from one study of G. marmoreus Pocock, 1894 from Guadeloupe (Mauriès 1980), the intraspecific variation of taxonomic characters has not been evaluated due to the lack of material. Males were not known before 1936 (Loomis) and not thoroughly described until later (Carl 1941). Our sample also includes only a single mature male and a single immature male. Numerous Glomeridesmus species were described from female material only. Only nine of the 30 described species include a description of the telopods, which provides genus-and often species-specific characters in the closely related orders Glomerida and Sphaerotheriida. A comparison of the telopods of the nine known species with those of G. siamensis sp. nov., described here, highlights the usefulness of telopods as taxonomic characters. No future Glomeridesmus species should be described without male specimens and a telopod illustration. In doing so, researchers should be aware that the telopods of smaller males are difficult to distinguish from those of larger males. Unlike in the Glomerida and Sphaerotheriida, the telopods seem to lack characters identifying them as belonging to immature males. Considering G. siamensis sp. nov. the telopod of the smaller male has a relatively shorter projection on podomere 2, the unique character of G. siamensis. It is therefore currently entirely possible to accidentally describe the telopods of a smaller, potentially immature, male of a Glomeridesmus as those of a different species.
Contrary to the male sexual characters, the female ovipositors, while prominent, do not seem to carry much valuable information. The ovipositors of the Brazilian G. spelaeus Iniesta & Wesener, 2012 and of the Indian G. indus Carl, 1942 differ only slightly in the number of segments from G. siamensis sp. nov., for which the intraspecific variability is unknown, and which are difficult to count as basal parts are hidden.
Besides sexual characters, somatic characters also need to be assessed for their taxonomic importance. For example, it has been shown for the Glomerida and Sphaerotheriida that the endotergum, the legs and the antennae can carry relevant characters (Wesener 2016;Oeyen and Wesener 2018).
For the Glomeridesmida, the presence or absence of coxal pouches (Fig. 4B), as well as on which leg pair they start, seem to be important characters. Specimens must be well preserved to make this determination.
The modified ultimate leg-pair, the sensory legs, seem to contain few taxonomically important characters, but more comparisons between different species are necessary to evaluate this character. At least G. siamensis sp. nov. differs significantly in the shape of the sensory leg from other species of the genus, especially by the unusual shape of podomere 1 (Fig. 3G, H).
Surprisingly, the lamellae linguales of the gnathochilarium seem to carry taxonomically important characters in the Glomeridesmidae, as was discovered recently by Mauriès (2020). The lamellae linguales can be completely fused, both with one another and with the mentum (as in G. spelaeus from Brazil), divided from one another as well as from the mentum by sutures (as in Glomeridesmoides Mauriès, 2019) or fused with one another but separated from the mentum by a suture as in G. siamensis sp. nov. (Fig. 6A).

Glomeridesmida diversity in Southeast Asia
Based on our findings and the insights from a Myriapoda inventory of a rainforest in Java (Hilgert et al. 2019), we suggest that the Glomeridesmida are far more diverse in Southeast Asia than previously known and are often overlooked when collecting by hand. This under sampling might result from their ability to move quickly to evade collection or their small size and inconspicuous appearance, especially compared to their larger relatives, the conspicuous pill millipedes (Glomerida) and giant pill-millipedes (Sphaerotheriida). Another possibility is that they are confined to micro-habitats. We found Glomeridesmus siamensis sp. nov. only on a single ca. 30×30 cm spot in a karst environment, which is known to provide micro-habitats and to show a great degree of endemism (Clements et al. 2006). The description of specimens faces two further challenges: the lack of mature male individuals, including among existing collections, and the low number of taxonomic experts for the group.
Only two species of Glomeridesmidae from Southeast Asia were described previously, G. sumatranus Pocock, 1894 from Sumatra and G. javanicus Attems, 1907 from Java; both are only known from female specimens. G. sumatranus was assigned to the genus Zephroniodesmus Pocock, 1894, which was later synonymized with Glomeridesmus by Loomis (1936) and Carl (1942). For G. javanicus, Verhoeff (1929) erected the genus Javadesmus Verhoeff, 1929, which was subsequently synonymized with Glomeridesmus by Carl (1942). Therefore, Javadesmus and Zephroniodesmus are available names that could be assigned to the Southeast Asian Glomeridesmidae. As the type species of both Javadesmus and Zephroniodesmus are only known from insufficiently described female specimens, we refrain from assigning G. siamensis sp. nov. to one of these genera. A study of male topotypic material is needed to clarify the affinities of the Southeast Asian Glomeridesmus species. The male sexual characters of G. siamensis sp. nov. are strikingly different from those of the South American and Indian species. Several representatives of Glomeridesmida from throughout Southeast Asia, including Sumatra, are currently under study.