Research Article |
Corresponding author: Leif Moritz ( moritz.leif@gmail.com ) Academic editor: Andy Sombke
© 2021 Leif Moritz, Thomas Wesener.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Moritz L, Wesener T (2021) A tarsal spinning organ in glomeridesmid millipedes (Diplopoda: Pentazonia: Glomeridesmida). Arthropod Systematics & Phylogeny 79: 555-567. https://doi.org/10.3897/asp.79.e70002
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Abstract
The production of sticky threads from spinnerets is known from various myriapod groups including some representatives of the millipedes (Diplopoda). In Diplopoda the thread-producing glands are mostly seta-like and positioned terminally on the telson, and the secretion product is typically used to build molting chambers or egg sacs. So far, no such secretions or organs have been documented for the subgroup Pentazonia. Here we describe thread-producing glands from the species-poor Glomeridesmida. These putative spinning organs are single circular fields of small pores (spinning fields) positioned on the outer side of the tarsi of all walking legs of mature and juvenile individuals of both sexes. These pores are the openings of cuticular tubuli (conducting canals), which extend from the tarsus to an aggregation of cells, a putative gland, within the femur. In several specimens thin threads were observed to be extruded from the pores. The tarsal spinning fields are present in all 21 investigated Glomeridesmida morphospecies, including Termitodesmidae and Glomeridesmidae from South East Asia, the Indian subcontinent, Oceania, and South and Central America. These organs might constitute an apomorphic character of the Glomeridesmida, as similar organs are absent in other Myriapoda. The function of the extruded threads in Glomeridesmida remains speculative, because observations of living specimens of the group are almost non-existing. We suggest that the secretion might be used for defense, to build molting chambers or to secure tunnels burrowed in the substrate.
exocrine gland, Glomeridesmus, leg, Limacomorpha, scanning electron microscopy, silk, spinnerets, Termitodesmus
Exocrine glands, which produce superficially silk-like threads and are often referred to as spinning organs or spinnerets, can be found in several Myriapoda taxa, including millipedes (Diplopoda), and differ in their structure and position on the body. Spinning glands are not known for Pauropoda but are present in Symphyla, where they open on appendages of the preanal segment (spinnerets) (
For the Pentazonia, which include large and conspicuous animals like the Holarctic pill millipedes (Glomerida) and the giant pill-millipedes (Sphaerotheriida), as well as the small and poorly known glomeridesmid millipedes (Glomeridesmida) (
Here we present first evidence for the presence of tarsal thread-producing organs (putative spinning organs) in the Glomeridesmida combining scanning electron microscopy, histology, and light microscopy.
Glomeridesmida and the distribution of the tarsal spinning organ. A: Glomeridesmidae (Glomeridesmus cf. javanicus), photograph of living specimen in Indonesia by Jan-Philip Oeyen. B: Termitodesmidae (Termitodesmus sp.) in a termite nest in Malaysia, photograph of living specimen by Munetoshi Maruyama and Taisuke Kanao. C: Habitus of adult female with 35+1 legs, schematic drawing, each walking leg is equipped with a spinning organ. D: Schematic representation of the spinning organ in a walking leg. Abbreviations: as = anal shield, co = collum, cx = coxa, fe = femur, gl = glandular cells, L1 = walking leg 1, L35 = walking leg 35, pof = postfemur, prf = prefemur, sf = spinning field, sL = sensory leg, ta = tarsus, ti = tibia, tu = tubuli, v = stigmatic plate.
19 morphospecies of the family Glomeridesmidae from South East Asia, the Indian subcontinent, Oceania, and South and Central America, spanning the known geographical distribution of the family, and two morphospecies of the family Termitodesmidae from Vietnam and Malaysia were studied. Investigated specimens included mature females (20 tergites (T) + anal shield (AS)) and males (19 tergites + anal shield) and immatures/juveniles (9–19 tergites + anal shield) (tergite number including collum). All material, including mostly undescribed species, is deposited in the collections of different museums (Table
Material examined. Abbreviations: H = histology, LM = light microscopy without Toluidine, LMT = light microscopy with Toluidine, SEM = scanning electron microscopy, TW = SEM images obtained previously by TW, WS = SEM images obtained previously by William A. Shear.
Species | Locality | Method |
Glomeridesmus siamensis Wesener, Wongthamwanich & Moritz, 2021 | THAILAND • 1 ♂, 1 ♀, 2 juv (19T+AS); Krabi Province, N. of Krabi Town, western aspect of Tiger Cave temple (Wat Tham Suea); 08°07′23.8″N, 098°55′18.9″E; 27.VII.2018; Wesener, Wongthamwanich, Nawanetiwong, Moritz leg.; overgrown rocks next to rubber plantation; ZCSWU-MyrD000011, |
SEM + LM |
Glomeridesmus spelaeus Iniesta & Wesener, 2012 | BRAZIL • 1 ♀; Pará, Curionópolis, iron cave SL 31; E 0650189m, N 9339714m; R.A. Zampaulo, leg.; in bat guana pile far from entrance; ISLA MII GEM 176150 | LMT |
Glomeridesmus cf. sumatranus Pocock, 1894 | INDONESIA • 1 ♂, 1 ♀, 2 juv (19+AS; 15+AS); Sumatra, West Sumatra Province, Mt. Merapi, ca. 15 km SE of Bukittinggi; 0°23′32′′S, 100°26′54′′E; 1650–1700 m a.s.l.; 4.VI.2006; A. Schulz leg.; hill forest; |
SEM + LMT + H |
Glomeridesmus sp. | INDONESIA • 1 ♂, 1 ♀, 1 juv (19T+AS); Sumatra, West Sumatra Province, Mt. Merapi, ca. 15 km SE of Bukittinggi; 0°23′32″S, 100°26′54″E; 1650–1700 m a.s.l.; 4.VI.2006; A. Schulz leg.; hill forest; |
SEM + LMT |
Glomeridesmus cf. javanicus Attems, 1907 | INDONESIA • 1 ♀; Java, Jawa Barat, Cikaniki Research Station, Erstes Bachtal von der Station aus (HAL92); 6°44′54″S, 106°32′21″E; 1082 m a.s.l.; 19.IV.2016; Myriapoda Team leg.; Winklerextraktion; |
LMT |
Glomeridesmus sp. | MALAYSIA • 1 juv (19T+AS); Pahang, Cameron Higlands, “Orang Asli vill.“ env. Gunung Perdah [Mt.]; 4°29.2N, 101°22.1E; 1575 m a.s.l.; 2–14.V.2009; Petr Baňař leg.; Sifting leaf litter in shallow ravine; |
LMT |
Glomeridesmus sp. | THAILAND • 1 juv (9T+AS, 8 leg-pairs); Doi Sutep; 1150 m a.s.l.; 29.IX.1958; B. Degerbøl leg.; Lok 3a; Zool. Mus. Kbh. 1/7 59; |
LM |
Glomeridesmus sp. | PAPUA NEW GUINEA • 1 ♀; New Britain, Valoka; 12.V.1962; Noona Dan Exp. 61–62 leg.; |
LM |
Glomeridesmus sp. | FIJI • 1 juv (19T+AS); Colo-i-Surva Forest Park; 29.III.–6.IV.199?; van Harten A. leg.; |
LM |
Glomeridesmus sp. | FIJI • 1 juv (15T+AS); Colo-i-Surva Forest Park;9.II.1997; van Harten A. leg.; |
LM |
Glomeridesmus sp | PHILLIPINES • 1 ♀; Panay, Sibaliw; 11°49′37″N, 121°56′21″E; 220 m a. s. l.; 2007; leg. Prof. Curio leg.; |
SEM TW |
Glomeridesmus sp. | INDIA • 1 ♀, 1 juv (10T+AS, 13 leg-pairs); Chennai (Madras), Anamalai Hills, au-dessud d’Aliyar Dam; 1150 m a.s.l.; 18.XI.1972; C. Besuchet & I. Löbl leg.; tamisages en foret, au pied d′un groupe d′arbras envahis par les lianes; |
LMT |
Glomeridesmus sp. | INDIA • 1 ♀; Meghalaya, Khasi Hills: en-dessous de Cherapunjee;1200 m a.s.l.; 26.X.1978; C. Besuchet & I. Löbl leg.; |
LMT |
Glomeridesmus sp. | SRI LANKA • 1 ♂; Sinharaja; 400 m a.s.l.; 2.XII.1979; V. Mahler leg.; |
LM |
Glomeridesmus sp. | PANAMA • 1 juv (19T+AS); Gamboa; 01.XI.1983; W. Netwig leg.; |
|
Glomeridesmus sp. | ECUADOR • |
SEM WS |
Glomeridesmus sp. | ECUADOR • 1 ♀; Pichincha, Río Palenque Station, 47 km S Santo Domingo; 700 ft; 18.V.1975; S. B. Peck & J. Kukalova-Peck leg.; |
SEM TW |
Glomeridesmus sp. | COLOMBIA • 1 ♂; Nevada del Ruiz; 3700–3800 m a.s.l; 10.X.1978; H. Sturm leg. (78/94); under Calamagrostis; |
LM |
Glomeridesmus sp. | BRAZIL • 1 juv (18T+AS); Taperinka, Santarém; 3./11.70, Pr. 9–10 Myriapoda, S.I. Tuxen & O. Densen; |
LM |
Termitodesmus calvus Attems, 1938 | VIETNAM • 1 ♀; Cat Tien; 16.I.2012; Semenyuk leg.; termite nest; |
SEM + LM |
Termitodesmus sp. | MALAYSIA • 1 ♀; 06.VI.2012; M. Maruyama leg.; Odontotermes termite nest; |
SEM TW |
To study the external morphology and structure of the putative spinning organs SEM was used. SEM data was obtained for three Glomeridesmus and one Termitodesmus morphospecies (Table
The legs were examined microscopically with transmitted light to check for the presence of the putative spinning organs and to investigate their internal morphology. Legs, unstained or stained (Table
Histological sections were obtained for mid-body legs of a female Glomeridesmus cf. sumatranus Pocock, 1894 (SUM06/08 01). Legs were embedded in epoxy resin (Araldite CY212, Agar Scientific Ltd (Stansted, UK), R1030) and semi-thin sections with a thickness of 0.5 µm were obtained with a Leica HistoCore NANOCUT R microtome (Leica Biosystems, Wetzlar, Germany) with a DiATOME histo Jumbo diamond blade (Diatome Ltd, Nidau, Switzerland). Semi-thin sections were stained with 1% Toluidine blue for 2 minutes. The mounted legs and histological sections were photographed with a Zeiss AxioCam HRc camera mounted to a Zeiss Imager.Z2m light microscope (Carl Zeiss AG, Oberkochen, Germany). The histological sections are deposited at the
The terminology for the podomeres of the walking legs follows
The investigated mature males, mature females, and juveniles of the 19 Glomeridesmidae morphospecies and two Termitodesmidae morphospecies (Table
The putative spinning organ in the Glomeridesmidae, external morphology, SEM. A–C: Glomeridesmus sp. (SUM06/08 02), female, mid-body leg. A: Overview of leg. B: Detail of tarsus. C: Detail of spinning field. D, E: Glomeridesmus cf. sumatranus (SUM06/08 01), female, spinning fields on tarsi of leg pair 2 with extruded threads/secretion. Abbreviations: cx = coxa, fe = femur, pof = postfemur, prf = prefemur, se = secretion, sf = spinning field, st = stigmata, su = suture, ta = tarsus, ti = tibia, v = stigmatic plate.
The tarsal spinning fields were 3–5 µm in diameter, slightly recessed into the tarsal cuticle, and comprised of 20–30 pores, which faced distally. Each pore had a diameter of ca 0.35 µm in the studied specimens (Figs
The putative spinning organ in the Termitodesmidae, mid-body leg of Termitodesmus calvus Attems, 1938, female. A–C: External morphology, SEM. A: Overview of leg. B: Detail of tarsus. C: Detail of spinning field. D: Detail of the spinning field with the underlying tubuli, mid-body leg stained with Toluidine blue, light microscopy. Abbreviations: fe = femur, pof = postfemur, prf = prefemur, sf = spinning field, ta = tarsus, ti = tibia, tu = tubuli.
In the 16 Glomeridesmidae and the single Termitodesmidae species studied with light microscopy (Table
The putative spinning organ of the Glomeridesmidae, internal morphology of a mid-body leg of Glomeridesmus cf. sumatranus (SUM06/08 01), female, light microscopy. A, B: Mid-body leg stained with Toluidine blue. A: Overview, terminology for the musculature follows
We suggest that Glomeridesmida possess tarsal spinning organs in the form of exocrine glands, which release threads through a field of pores on their walking legs’ tarsi. Such threads are thin filaments of unknown composition and were observed to be extruded from the pores on some legs (Fig.
The spinning organ of the Glomeridesmida is an aggregated gland with several secretory units; cells are clustered within the femur, but open via separate tubuli (conducting canals), which run through the podomeres to the tarsus (Figs
Exocrine glands positioned on the legs are known from several millipede taxa but are typically restricted to males and differ in their position (i.e. on which legs and/or podomeres) from those in Glomeridesmida, in which pores are present in both sexes and in juveniles on the tarsi of all walking legs (Fig.
Although spinning organs are reported from various millipede (Diplopoda) taxa, these differ largely in their location and structure from the putative spinning organs found in Glomeridesmida. In Glomeridesmida these are porous fields on the tarsi (Fig.
In addition to the structure of the putative spinning organ, the structure of the threads observed in Glomeridesmida differs from that found in other millipede taxa with spinning abilities. Thus, the threads released from telsonian spinnerets are rather flattened in Chordeumatida (
From the other pentazonian taxa Glomerida and Sphaerotheriida, which are comparatively well-studied, including SEM images of the legs (e.g.
The actual function of the extruded threads in the Glomeridesmida remains speculative because the biochemical composition of the threads (as for most millipedes) is unknown, and no spinning activity or spinning product has been observed so far in living specimens. For Polydesmida, it has been shown by staining experiments that the threads are not true silk (i.e. made of fibrous protein) but consist of mucopolysaccharides (
In insects thread-producing or spinning organs can be found on the apical podomeres of several taxa, like webspinners (Embioptera), dance flies (Diptera: Empididae), and some ants (Hymenoptera: Formicidae). In these insects the secretions serve to build tunnels as in Embioptera (
To clarify the function of the spinning product in Glomeridesmida, behavioral observations of living specimens are needed. Until now such observations of living specimens are rare and mostly anecdotal (
For Glomeridesmida
For this study we only had access to material from museum collections, which has been initially fixed and subsequently stored over a long period in ethanol (70% or 96% EtOH), resulting in the suboptimal preservation of soft tissue and in artefacts, as visible in the histological sections (Fig.
Glomeridesmida possess exocrine glands in their walking legs, which open through a field of pores (spinning field) on their tarsi and extrude threads. These putative spinning glands, are present in both major groups of the Glomeridesmida, the Glomeridesmidae and Termitodesmidae, and are probably an apomorphic character of the group. The function of these threads remains speculative, but we suggest that the threads serve for a defensive function against predation and during molting, or that they are involved in tunneling. To clarify the structure and function of the glands and their excretion ultrastructural examination and behavioral observations of living specimens are needed.
We greatly thank Juliane Vehof (
Figures S1–S5
Data type: .pdf
Explanation note: Figures S1–S5 including legends.