- Last updated on 2021.11.16 by Frans Janssens
Checklist of the Collembola: Internal Anatomy

Frans Janssens, Department of Biology, University of Antwerp, Antwerp, B-2020, Belgium

Integumentary system. The integument represents the largest organ in the collembolan body, and it is reponsible for the success of Collembola in the terrestrial environment. As in all Arthropoda, the integument is a tissue that covers the body and all ectodermal invaginations that arise from it, such as the buccal cavity, the fore-gut and hind-gut. The integument consists of an inner epidermis (sometimes called hypodermis), a single layer of epidermal cells, and an outer cuticula, an extra-cellular more or less inert membrane (Wigglesworth, 1965:25). The multilayered cuticle consists of an outer epicuticula and an inner procuticula. The procuticula itself is composed of an outer exocuticula and inner endocuticula. The ultrastructure of the epicuticle is one of the most striking features of the cuticle (Hopkin, 1997:51). This unique epicuticular ultrastructure is a collembolan autapomorphy. The epidermal cells can differentiate into trichogen cells that form setae and/or scales, tormogen cells that form setal sockets, nerve cells that support setal sensory subsystems, glial cells that envelope nerve cells, glandular cells that produce cuticular secretions, such as pheromones and wax. Pigmentation of the intugement is dependant on the light circumstances; in light conditions, the pigmentation is more intens; in obscurity, the pigmentation is more pale (Thibaud, 1970:183).

Fig.2b. Nervous system
Smynthurus signatus
(= Allacma fusca)
After Nicolet H., 1842 Pl.4 fig.1
Fig.2c. Nervous system
Mesaphorura sylvatica
After Panina, I.V. & al., 2019 Fig.4CD

Nervous system. The nervous system (fig. 2b) comprises a cephalic complex of a superoesophageal ganglion (b) combined with the optic lobes and a suboesophageal ganglion (c), forming the brain, and several ventral ganglia, of which three thoracic ganglia; in Symphypleona the prothoracic and mesothoracic ganglia are fused (d) (Nicolet, 1842:45). The abdominal ganglia are fused to the metathoracic ganglion (e) (Cassagnau & Juberthie in Vandel, 1970:3268) (Panina & al., 2019:10) which usually extends into the first abdominal segment (Brauner 1981 cited from Hopkin 1997:64). Unlike those of larger species of Collembola (Lubbock, 1873), the brain and suboesophageal ganglion of Mesaphorura sylvatica extend into the prothorax. This causes the three thoracic ganglia to shift their position posteriad by one segment (fig. 2c). In larger Collembola species, an extension of the metathoracic ganglion to the first abdominal segment was reported (Lubbock, 1873; Hopkin, 1997). (Panina & al., 2019:18). The ganglia are longitudinally interconnected by a pair of lateral connectives; the unpair, median nerve of Leydig runs from one ventral ganglion to the other inbetween the lateral connectives (Cassagnau & Juberthie in Vandel, 1970:3268).
Intercalary nerve; nerve of Hoffmann. To be completed.
Sensory organs: antennal sensory structures, postantennal organ, eyes, setiform organs, oval organs, proprioceptors. To be completed.

Circulatory system. Circulation in the body cavity of the blood which bathes the organs is maintained by the pulsating (60 to 160 pulsations per minute) dorsal blood vessel or 'heart' (Nicolet, 1842:48-49). Unlike most insects, Collembola appear to lack specialised circulatory organs for pumping blood into the antennae (Pass 1991 cited from Hopkin 1997:59).

Muscular system. Each thoracic and abdominal segment comprises a pair of dorsal and ventral longitudinal muscles (Palissa, 2000:26). The mesothoracic, metathoracic and abdominal segments, in addition, bear a basic configuration of segmental, intersegmental and lateral dorsoventral muscles (Palissa, 2000:26). When the furca is present, the fourth abdominal segment bears additional muscles to operate the furca (Palissa, 2000:26). To be completed.

Endocrine system. The neurosecretory system, that stores and releases the neurosecretion substance, is of the most primitive type, as in Annelida; it corresponds to two cephalic suboesophageal neurohaemal organs, without proper secretory cells (Juberthie & Cassagnau, 1971:77). In Neanura, Tomocerus, Orchesella and Bourletiella, the neuroglandular cells, that produce the neurohormone, are situated in the latero-dorsal part of the protocerebron and in the pars intercerebralis, both of the superoesophageal ganglion complex. The group of axons of the latero-dorsal protocerebral neuroglandular cells form a nerve called the nervus corporis cardiacus 1. The nervi corporis cardiaci 1 form a chiasma: the left neuroglandular cells are connected to the right neurohaemal organ and vice versa. The group of axons of the intercerebral neuroglandular cells form a nerve called the nervus corporis cardiacus 2.
Note: the names of both nerves are in analogy with nerves found in Insecta, but are misleading in Collembola, since Collembola lack corpora cardiaca.
The dilated apical part of the axons of the nervi corporis cardiaci connect to the outer wall of the aorta (that forms a sleeve around the oesophagus) in Neanura and Tomocerus, and to a blood sinus in Orchesella and Bourletiella, in which the neurohormone is released (Juberthie & Cassagnau, 1971:61-63,69,70,75).
The ventral ganglia host four types of neuroglandular cells; the metathoracic-abdominal ganglia complex contains most neuroglandular cells (Cassagnau & Juberthie in Vandel, 1970:3268).
The corpus allatum, a retrocerebral endocrine gland of ectodermal origin, secretes the juvenile hormone, which mainly regulates the pre-adult characters, and induces the type of behaviour appropriate to the type of growth or reproductive activity that is to follow (Wigglesworth, 1965:178). In the Poduromorpha, the corpora allata are in para-oesophageal and peri-aortic position and in direct contact with the cerebral neurohaemal organs (Juberthie & Cassagnau, 1971:74). In Tomocerus, Orchesella, and Bourletiella, the corpora allata are innervated by a suboesophageal nerve, the nerve of Hoffmann, establishing the relation with the cerebral neurohaemal organs (Juberthie & Cassagnau, 1971:73,74). In Sphyrotheca multifasciata, the innervation of the corpora allata is exclusively suboesophageal, without any connection to the neurohaemal organs or the supra-oesophageal ganglion complex (Prabhoo & Seshian, 1967 cited from Juberthie & Cassagnau, 1971:71-72).
To be completed.

Excretory system. The abscence of Malpighian tubules in Collembola suggests that mineral deposition in the midgut epithelium serves an excretory function; excretion is achieved by the renewal of the entire intestinal epithelium, which occurs at each moulting (Humbert, 1979:43,53). Integumental wax glands occur in Neelidae, Dicyrtomidae and Sminthuridae (Palissa, 2000:9). In Onychiuridae and Tullbergiidae, so-called pseudocelli may secrete a drop of a repelling fluid as defensive mechanism (Pallisa, 2000:9). The salivary glands rise immediately behind the mouth, passing posteriad along the oesophagus, to which they are firmly attached (Von Olfers cited from Lubbock, 1873:74). Three to four pair of salivary glands secrete enzymes onto the food in the buccal cavity (Hopkin, 1997:59). Some neanurids have very large salivary glands which extend posteriorly into the prothorax (Lee 1980 cited from Hopkin, 1997:59).
Labial nephridia. To be completed.

Fig.Ds. Digestive system
Mesaphorura sylvatica
After Panina, I.V. & al., 2019 Fig.4AB
Fig.Ds2. Midgut pushes ingested food further
Entomobrya sp. juvenile
2021.11.13%© Cheng, H.-J.

Digestive system. The begin of the digestive tract opens in the buccal cavity of the head capsule (Nicolet, 1842:46). The tubular intestinal canal passes straight through the body without any circumvolutions from anterior to posterior end (Nicolet, 1842:46). While Nicolet (1842:46) identifies five intestinal regions, they fall in three main divisions (Von Olfers cited from Lubbock, 1873:74). The alimentary canal consists of a rather long and narrow foregut or stomodeum, a capacious sac-like midgut (stomach, ventriculus, intestine) or mesenteron, and a narrow hindgut (caecum, rectum) or proctodeum (after Nicolet, 1842:46-47; Lubbock, 1873:74; Thibaud, 1970:151; Adams & Salmon, 1972:279). The foregut comprises at least the pharynx and oesophagus (Thibaud, 1970:151). A temporary local dilatation of the oesophagus may be present as result of the feeding process (Nicolet, 1842:46). Adams & Salmon (1972:279) distinguish in the fore gut: pharynx, oesophagus, crop and gizzard. The foregut and hindgut are lined with cuticle which is shed at every moult (Thibaud, 1970:152). The midgut is lined with epithelial microvilli in direct contact with a peritrophic membrane that is secreted by a ring of cells posterior to the junction between the foregut and midgut (Hopkin, 1997:60). At the junction between midgut and hindgut, a muscular sphincter, known as the pyloric region (Nicolet's 'intestin grêle') (Nicolet, 1842:46-47; Dallai 1980 cited from Hopkin 1997:62) or rectal valve (Adams & Salmon, 1972:281), is situated. Tiny 'malpighian papillae' are present at the anterior end of the hindgut (Dallai, 1980 cited from Hopkin, 1997:60). Note that the observation of malpighian vessels by Nicolet (1842:47) and Von Olfers (cited from Lubbock, 1873:75) is neither confirmed by Laboulbéne (1864 cited from Lubbock, 1873:75) nor Lubbock (1873:74,75) and definitly refuted by Dallai (1980 cited from Hopkin, 1997:60). The midgut is surrounded by a network of circular and longitudinal muscles (Nicolet, 1842:47; Lubbock, 1873:75) which mix food in the lumen and force residues of digestion into the hindgut by peristaltic movement (Nicolet, 1842:47; Dallai et al. 1989 cited from Hopkin 1997:60). The strongly muscular rectum, being provided throughout its whole length with transverse muscles (Lubbock, 1873:76) forms the faecal pellets (Hopkin 1997:63). The end of the digestive tract opens via the anus on the sixth abdominal segment (Nicolet, 1842:38,47) which bears three eversible anal sacs of unknown function (Leinaas 1988 cited from Hopkin 1997:50); anal sacs in retracted condition (Janssens, F. © 1999), anal sacs in eversed condition (Reed, D. © 2007.03.10).

Respiratory system.
Fig.3. Cephalic branching trachaea
Deuterosminthurus delatorrei
2016.06.09 © Palacios-Vargas, J.G.
Fig.3a. Branching trachaeal system
Allacma fusca 2nd instar
After Betsch & Vannier 1977 in Betsch 1980:Fig.7F
Most Collembola respirate through a mechanism of epidermal gass diffusion, in which the eversible vesicles of the collophore play an important role (Ruppel, 1953 cited from Palissa, 2000:31). Only Actaletoidea and some Symphypleona have trachaeae, that may form a cephalic and thoracic/abdominal branching system of tubes (Betsch, 1980:22; Hopkin, 1997:59) (fig.3, 3a).
Fig.3b. Spiracle without occlusion mechanism
Allacma fusca 1st instar
After Betsch & Vannier 1977 in Betsch 1980:Fig.7A
Fig.3c. Cephalic trachaea unbranched
Papirinus ankaratrensis
After Betch 1980:Fig.5
In contrast to Insecta, that have spiracles (or stigmata) in each trunk segment, Collembola have only two spiracles that are situated posteriorly in the head (fig.3a), at the place where the head is attached to the trunk, between head and prothorax (Lubbock, 1873:90-91). The stigmata do not have an occlusion mechanism (Betsch,1980:22) (fig.3b).
Fig.3d. Cephalic trachaea tree-branched
Sphyrotheca madagascariensis
After Betch 1980:Fig.5
Fig.3e. Cephalic trachaea tree-branched with secondary branched tree in thorax and abdomen
Bourletiella sp.
After Betch 1980:Fig.5
The cephalic trachaeae are formed by unbranched epidermal invaginations, such as in Papirinus (fig.3c), Dicyrtoma and Temeritas, while in Pararrhopalites, the cephalic trachaeae are branched in a Y-shape, in Sphyrotheca, in a tree-shape (fig.3d), and in Sminthurus, Allacma, Bourletiella and Vatomadiella, the trachaeal tree has 2 main branches, one forming the primary cephalic tree of tubes, and one forming a secondary trachaeal tree into the thorax and abdomen (Betsch,1980:22-23) (fig.3e).
Nicolet (1842:38,47-48) described in error a trachaeal system, based on metamere pneumatic sacs, that open with a total of eight stigmata pairwise on the first four abdominal segments. This was disputed by Lubbock (1873:77-81), who found trachaeae in Smynthurus(sic) only, that open in just two large spiracles. It was also disputed by Willem (1900:21): "je pense que Nicolet a pris pour des organes de cette nature des bandes de tissu adipeux." Given that Nicolet (1842:42-43) failed to find any reproduction organs, we presume that he misinterpreted the long tubular and segmented testes and/or ovaries, such as those found in Podura aquatica, as pneumatic sacs.
The Spinothecidae possess a pair of unusual tubular organs encircling the neck from a ventral insertion, the foramen magnum (Greenslade, 1982:81). These peculiar 'neck organs' could have an accessory respiratory and/or homeostatic function since they are internally without structure and appear to be filled with haemolymph in life (Greenslade, 1982:94). The structure of the cuticle on the neck organs is very similar to that of some plastron-bearing spiracular gills described by Hinton (1968) for immature stages of Diptera (Greenslade, 1982:94).

Fig.Rs. Reproductive system
Mesaphorura sylvatica ♀
After Panina, I.V. & al., 2019 Fig.4EF

Reproductive system. The generative organs are similar in the two sexes (Lubbock, 1873:81). In males, the sperm are produced from the paired tubular testes, one lying on each side of the abdomen, that are posteriorly united to form a vas deferens, that opens ventrally immediately between the anus and the base of the furca (Lubbock, 1873:81). In females, the eggs are produced from the paired broad tubular ovaries, one lying on each side of the abdomen, that are posteriorly united to form a vagina, that opens ventrally immediately between the anus and the base of the furca (Lubbock, 1873:81). The ovaries are not composed of discrete ovarioles (Bilinski 1976; Krzysztofowicz 1971, 1977; Matsuzaki 1973; Palévody 1976 cited from Hopkin 1997:134). Each ovary is divided into two main regions, the germanarium which contains chain-like clusters of germ cells, and the vitellarium where the central cell of each chain differentiates into an oocyte and is nourished by nurse cells on either side (Jablonska et al. 1993 cited from Hopkin 1997:134-135).