http://www.collembola.org/publicat/egg.htm - Last updated on 2016.07.29 by Frans Janssens
Checklist of the Collembola: Model of the Formation of the polar Caps of the Egg

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

Model of the formation of the polar caps of the egg of Collembola

Fig.0. Egg cluster of Proisotoma minuta.
Hatching juvenile at arrow.
Janssens, F. © 2007.12.10
Fig.00. Egg batch of Isotomurus cf. maculatus.
Zungri, D. © 2008.05.09
In general, eggs are produced every other moulting period (Joosse & Veltkamp, 1970). Egg production shows a clear relationship with moulting. Since the moulting process is temperature dependent it thus can be expected that egg laying will be more frequent at higher temperatures, due to the increased moulting rate (Joosse & Veltkamp, 1970). In Isotoma viridis, the number of egg laying periods being reported as 3 by Hale (1965), and a maximum of 8 by Joosse & Veltkamp (1970). In Isotoma viridis, a mature female lays one batch of 27-54 eggs (after Milne, 1960).
Fig.000. Sminthurus sp. depositing eggs.
Sikes, D. © 2012.08.10
Fig.001. Sminthurides aquaticus depositing egg.
Huskens, M.L. © 2016.07.28
The eggs of Ceratophysella armata are laid in small clumps in damp situations under surface of loose stones, wood, or leaves (Tiegs, 1942:154).
Sminthurus viridis attains sexual maturity during the sixth instar when oviposition may already take place. On very wet soil the eggs are laid on elevations and surface litter. On dry soil the eggs are deposited in more moist cracks. The female eats soil that is being excreted as a sticky mixture which is used to cover the eggs. The eggs are laid in batches. The female stands with widespread legs and elevated abdomen (fig. 000). A drop of soil excreta is slowly forced out of the anus, followed by the extrusion from the gonopore of the shapeless egg which quickly assumes a spherical form. The abdomen is then depressed and the egg is firmly pressed against the soil by means of a cicular movement of the abdomen, the excreta serving to anchor the egg. A further drop of soil excreta is then spread over the egg. Uncovered eggs may be eaten by the female or other springtails. Oviposition may take several minutes for each egg. 12 hours may be spent on laying a single egg batch. Oviposition may commence during the sixth instar and continue up to the tenth instar. A female lays about 15 to 87 eggs during her lifetime. Egg batches of several different females may be clustered (up to 700 eggs in laboratory conditions). (After Walters, 1967:23-24).
In Sminthurides aquaticus eggs are deposited in cuplike depressions of the epidermis of Lemna minor (Fig.001). The cups have been chewn out by the female. After deposition, the egg is covered by a faecal pellet.

Fig.1. Eggs at oviposition.
Lynch, T. © 2001
Fig.1a. Sminthurinus atrapallidus
Egg cluster at oviposition
Zungri, D. © 2012.04.09
"La forme de l'oeuf, sa couleur et le tissu de l'enveloppe varient non seulement d'un genre à l'autre, mais encore d'espèce à espèce; les oeufs à enveloppe solide sont en général très peu transparents, lisses, d'une couleur brune plus ou moins foncée et plus souvent oblongs que sphériques: ils appartiennent surtout au genre Podure.
Ceux à enveloppe molle offrent plus de variété dans la forme et la texture de la membrane extérieure; ils sont tantôt oblongs ou ovoïdes, tantôt sphériques ou en sphéroïde aplati de deux côtés; leur couleur est généralement pâle, ou plutôt blanche, mais légèrement lavée de blue, de jaune, de rose ou de violet, selon les espèces. Leur transparence permet de suivre jusqu'à un certain point le développement de l'embryon. La membrane extérieure est lisse dans la plupart des espèces, pointillée ou réticulée dans quelques unes; dans ce dernier cas, les oeufs sont parfois velus; garnis de poils longs et serrés; d'autres sont plutôt épineux que velus; les épines longues, flexibles et un peu frisées comme de la laine, affectant toutes les formes et toutes les directions, sont larges à leur base et aiguës à leur extrémité; elles naissent chacune d'une espèce de bulbe formé de deux renflements placés l'un au dessus de l'autre, dont le premier ou l'inférieur est hémisphérique, et le second ou le supérieur, en disque arrondi; c'est au centre de ce dernier qu'est attachée l'épine.
Dans les oeufs réticulés et velus, c'est du point de jonction des lignes qui forment les mailles du réseau, que sortent les poils; ils sont droits ou perpendiculaires au centre de l'oeuf et n'ont jamais de bulbe pour base." (Nicolet, 1842:16-17).

Fig.1b. Eggs of Pseudosinella rolfsi
Bernard, E.C. © 2006
The eggs of Ceratophysella armata are spherical measuring not more than 0.12 mm in diameter (Tiegs, 1942:154). The eggs of Isotoma viridis are smooth surfaced and globular and measure 0.21 mm in diameter before development (Milne, 1960). Oviposition always occurs on the surface and on laying the eggs have an orange-red pigmentation (Milne, 1960). The eggs of Sminthurus viridis are spherical and measure about 0.27 mm in diameter (Tiegs, 1942:162).
At oviposition (fig.1, 1b), many eggs of Collembola are spherical and smooth (Lubbock, 1873:82). The eggs have a smooth external shell (Kühnelt, 1961:162), called the 'chorion' (Wigglesworth, 1965:1). E.g., the eggs of Isotoma Walkerii(sic) (now Desoria albella) are spherical, glistening white, with the chorion very transparent. (Packard, 1871? cited from Lubbock 1873:84). In Hypogastruridae, the eggs are spherical, whitish, opaque and shiny; the chorion is smooth, in general; the egg is moist and sticky (Thibaud, 1970:127). In Folsomia candida, the fresh egg is milky white and has a diameter of 0.110-0.126 mm; the surface of the egg shell is finely granulated (Gao, Bu, Luan & Yin, 2006:519). In Hypogastruridae, at oviposition, the egg diameter is about 140-260 micron (Thibaud, 1970:128). In subterraneous species, the number of eggs per batch decreases, while the size of the eggs increases (Thibaud, 1970:130).
In Hypogastruridae, the incubation period (time between oviposition and eclosion) is about 24-45 days at 9-12°C (Thibaud, 1970:130). In Folsomia candida, the incubation period is about 7 to 10 days (Gao, Bu, Luan & Yin, 2006:519). In Megalothorax, the incubation period is about 16 days at 20°C (Blancquaert & Mertens, 1979:126). In Hypogastruridae, the eggs can develop and hatch under water (Thibaud, 1970:181).

Fig.1cc. Egg cluster of Lepidocyrtus sp.
Brito, N.P. © 2014
Fig.1c. Egg of Pseudosinella alba
After Tiegs, 1942:161 Text-Fig.3
The chorion of the egg in Lepidocyrtus (Fig.1cc) and in Pseudosinella alba is furnished with long delicate spines in the early stage of ventral flexure of the embryo when the chorion is not yet ruptured (Fig.1c) (Tiegs, 1942:160-161).
Due to the formation of a dorsal organ, the form of the egg changes by the rising of the dorsum of the growing embryo (Schaller, 1970:51). The dorsal organ consists of filamentous processes arising from a pit in the anterior dorsal region that are grown on to the lower pole of the egg (Tiegs, 1942:161) (Wigglesworth, 1965:5). It is suggested that these filaments may be concerned in the absorption of water (Tiegs, 1942:165-166) (Wigglesworth, 1965:5).
The egg swells soon after deposition (Davidson, 1932:867; Schaller, 1970:51; Thibaud, 1970:130-132), due to absorption of water (Thibaud, 1970:130). The eggs do not remain spherical at all; they increase in size rapidly after oviposition, to remain stable halfway the incubation period (Thibaud, 1970:130-131). As a result, usually on the second to fourth day of embryonic development, the chorion bursts (Schaller, 1970:51). And the blastodermic cuticle takes it place as the protecting sheath for the embryo (Tiegs, 1942:156). The egg of Ceratophysella armata, now enlarged, measures 0.17 mm in diameter (Tiegs, 1942:156). The rupture of the chorion in Sminthurus viridis takes place later than in Ceratophysella (Tiegs, 1942:162). In many species, the chorion does not split randomly, but symmetrically at the equator of the egg (Davidson, 1932:867; Schaller, 1970:51; Thibaud, 1970:132). The ruptured chorion adheres in two pieces to the blastodermic cuticle (Tiegs, 1942:156). The two chorion caps thus formed, due to the swelling of the egg, gradually separate to form two symmetric caps at the poles of the egg, the 'polar caps' (fig.2) (Nicolet, 1842:19; Davidson, 1932:867; Schaller, 1970:51).

Fig.2. Polar caps in eggs of Collembola:
Protaphorura armata (left)
Deuteraphorura inermis (middle)
Orchesella cincta (right)
After Handschin in Kühnelt, 1961:162
Nicolet, 1842:19 is the first to describe the forming of polar caps (fig.6): "Dès que les yeux commençent à paraître, l'oeuf se comprime de manière à prendre la forme d'un sphéroïde aplati; l'enveloppe extérieure se fend dans son plus grand diamètre et forme deux hémisphères qui s'éloignent insensiblement l'un de l'autre; leur sommet s'affaisse, et leur donne bientôt l'apparence de bonnets grecs, appliqués de chaque côté de la nouvelle membrane, qui devient alors, jusqu'à l'éclosion, membrane extérieure de l'oeuf."
Fig.3a. Transparent eggs showing ocular patches
Chamberlain, P.M. © 2002
Fig.3aa. Willowsia buski from the USA
Egg of 0.3 mm showing ocular patches
Zungri, D. © 2009.04.25
Fig.3ab. Eggs of Lepidocyrtus sp. showing ocular patches
Brito, N.P. © 2014.11.08
Directly as the eggs of Isotoma viridis are laid they begin to enlarge due to uptake of water from the atmosphere. In an atmosphere of 100% relative humidity eggs reach maximum size in a few hours. Further enlargement does not take place until the growth of the embryo begins after about 20% of the developmental period (Hale, 1965c). The eggs become coloured due to the formation of pigment in the body of the embryo, however eye spots appear before the body colouration. Development can be characterized as epimetabolic (Weber, 1968), which means a gradual differentiation occurs during development.

The separating chorion caps reveal the embryo surrounded by a transparant membraneous inner shell (called the 'vitelline membrane' (Wigglesworth, 1965:1)) (Davidson, 1932:867; Thibaud, 1970:132). In Hypogastruridae, between the 12th to 15th day, the limbs can be recognised through the transparant vitelline membrane; around the 16th day, in pigmented species, the two ocular patches can be seen (Thibaud, 1970:132) (fig.3a, 3aa and 3ab).
Fig.4. Egg of Orchesella cincta
After Bretfeld in Schaller, 1970:51
In some cases, the eggs which are at first apparently smooth, after a few days will be found to be covered with long hairs (Lubbock, 1873:83). The after the chorion split freed vitelline membrane surface carries in many species (such as in Orchesellinae and Tomoceridae) numerous processes, (fig.2 right, fig.4) in other species (such as in Onychiuridae) flattened nipples (fig.2 middle) (Kühnelt, 1961:162; Schaller, 1970:51). These structures enable the egg to adhere firmly to the substrate on which it has been deposited (Kühnelt, 1961:162) (protection against flotation due to in the soil penetrating rain water) (Schaller, 1970:51).

Fig.4a. Folsomia candida
Egg in anaphase
Chorion is split in two polar caps
After Gao et al. 2006 Fig.3.5
A schematic animation of the formation of the polar caps of the egg of Folsomia candida WILLEM, 1902 based on observations of a specimen culture kept from 1994 to 1996 (Janssens, 1994:6-10; Janssens, 1996:120-125): fig.5 shows three orthogonal views at the same time: upper left: frontal view, upper right: lateral view, and lower left: dorsal view. Due to the swelling of the egg, the chorion bursts at the equator of the egg. The two halves of the chorion are pushed towards the poles of the egg, while the originally spherical egg evolves into a laterally flattened ellipsoid shape. The chorion halves fold in the shape of a craterlike depression at the poles, forming in such a way two polar caps. The polar caps are eventually 'ejected' from the egg surface (not shown).

Fig.5. Polar caps formation
on the egg of
Folsomia candida WILLEM, 1902

Animation by Janssens, F. © 1999
Fig.6. "Rupture de l'enveloppe externe
de l'oef."
Desoria cinerea = Vertagopus cinereus
After Nicolet, H. 1842 Pl.1 fig.8,9

Fig.3b. Embryo of Sminthurides aquaticus in transparant egg ready to hatch.
Robertson, A. © 2009.05.17
Fig.3bb. Embryo's of Sminthurides aquaticus.
Huskens, M.L. © 2016.07.27
In Sminthurides aquaticus, at the end of the embryonic development, the eggshell is completely transparant revealing the fullgrown embryo ready to hatch. (Fig.3b,3bb)

Fig.3c. Newly hatched Folsomia candida.
After Tully, T. 2008 ©
In Folsomia candida, at the end of the embryonic development, the diameter of the egg reaches 0.180-0.185 mm. (Gao, Bu, Luan & Yin, 2006:519). Freshly deposited eggs are orange-brown. The egg swells during embryonic development, the chorion bursts and forms two polar caps. The newly hatched instar is about 0.35 mm in length.

Fig.3d. Newly hatched Isotomurus cf. palustris.
Janion, C. © 2007
Newly hatched young of Isotoma viridis measure 0.57-0.63 mm in length and 0.15 mm in head width. A red pigment, possibly carotenoid is present in the body fluid of this species, giving the young a pale red colouration (Milne, 1960). The surface pigmentation only becoming apparent after the first ecdysis (Milne 1960).

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