http://www.collembola.org/publicat/spermato.htm - Last updated on 2017.06.27 by Frans Janssens
Checklist of the Collembola: Note on the Spermatophores of Collembola

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

Fig.S. Spermatophore of Orchesellinae from France, Francheville.
2007.10.16 © Lebeaux, P.

Spermatophore. Etymology:
from 'sperma' (Greek) = that what is sown, i.e. seed; from 'speirein' (Greek) = to sow
from 'spermatos' (Greek) = genitive form of 'sperma' = of seed
from 'phoros' (Greek) = bearer; from 'pherein' = to bear
'spermatophore' = bearer of seed.

A spermatophore is a 'packet' of spermatozoa produced by the male (modified after Hopkin 1997:136), and functioning in the insemination of the female. Males of Orchesella cincta produce a mean of five spermatophores per day at 20°C but do this only for about half the intermoult period; spermatophores are deposited only in alternate instars (Hopkin 1997:136).

Fig.Gf. Tetrodontophora bielanensis
from Czechia
Female genital orifice
2008.08.17 © Deml, M.
Fig.Gm. Tetrodontophora bielanensis
from Czechia
Male genital orifice
2008.08.17 © Deml, M.
Genital opening. The genital opening is located ventrally on the 5th abdominal segment. Collembola have separate sexes (see fig.Gf and Gm) and reproduce by means of indirect sperm transfer (modified from Hopkin 1997:134). Spermatophores are deposited by the males on the substrate (Christiansen in Dindal, 1990:968), and subsequently picked up by the female, or placed directly on the female genital opening (Hopkin 1997:134).

In general, spermatophores are produced every other inter-moulting period (Joosse & Veltkamp, 1970). Males may produce up to 200 spermatophores during such a reproductive instar phase.
Spermatophore structure

Fig.x. Spermatophore structural parts
2009.12.03 © Valentine, B.
Fig.Orchvsd. Orchesella villosa from Italy
Spermdrop with peripheral coat
After Dallai, R. et al., 2009 Fig.1C
Fig.Ent. Entomobryidae from Holland
Stalk penetrates spermdrop
2015.11.06 © Wieringa, P.

Several species fertilise the females by direct transfer of sperm to the female genital aperture and have no need for an elaborate spermatophore (Hopkin 1997:136). In some Collembola, the spermdrop is surrounded by a resitant coat which protects against dessication (Schaller 1970:43; Hopkin 1997:136) (Fig.Orchvsd). The surrounding coat may be very thin or even absent in Collembola in which the spermatophore is produced shortly before acceptance by the female (Hopkin 1997:136). The coat contains glycogen, tyrosin (scleroprotein) and chitin (Schaller 1970:43).
Fig.Orchvs. Orchesella villosa from Italy. Cross-section of stalk of spermatophore.
After Fanciulli P.P. et al., 2012 Fig.13C
Fig.Orchvsmgo. Orchesella villosa from Italy. Male genital opening.
After Fanciulli P.P. et al., 2012 Fig.12B

The spermatozoa are stored in the spermdrop with curled-up tail and are inactive; they become active when the peripheral coat is bursted (Schaller 1970:43). The sperm in the spermdrop of spermatophores may survive 2 days. The original glass transparent spermdrop then becomes opale translucent.

The spermdrop is often held above the substrate on a thin stalk which may extend into the sperm droplet or be expanded into a small ledge to provide support (Hopkin 1997:136).

In Sminthurus viridis, the stalk is produced by secretion of the stalk material from the male genital opening, then by pressing the secreted drop against the substrate, and finally by raising the abdomen to extrude the stalk (modified after Hopkin 1997:136,137).

A cross section through the basal most part of the spermatophore stalk shows 3 + 3 secretory filaments (Fig.Orchvs(*)). The filaments are produced by the male genital opening (fig. Orchvsmgo) by squeezing out a secretion through 3 + 3 cuticular slits. The secretion hardens quickly and the filaments get twisted and glued together to form a rigid stalk. (After Fianciulli et al., 2012).

Spermatophore shape

Fig.1x. Variation in sizes of spermatophores
l. Allacma fusca (Sminthuridae)
m. Orchesella cincta (Entomobryidae)
r. Podura aquatica (Poduridae)
After Schliwa, W. 1965 Abb.56
Fig.1b. Variation in shapes of spermatophores
a. Podura aquatica (Poduridae)
b. Monobella grassei (Neanuridae)
c. Deutonura monticola (Neanuridae)
d. Isotoma viridis (Isotomidae)
e. Dicyrtomina minuta (Dicyrtomidae)
After Cassagnau, P. 1971 Fig.1,2
In some species, several spermatophores may be produced at once and are attached to the tips of a branching structure (Hopkin 1997:136) (Fig.1b.c).
Fig.Pas. Podura aquatica from Germany
Spermatophore dimensions
After Schliwa, W. 1965 Abb.56 rechts
Fig.1a. Spermatophore
Podura aquatica
After Schaller 2001.
Fig.Poda. Podura aquatica from France
Spermatophore
2009.09.dd © Lebeaux, P.

Poduridae. In Podura aquatica, the spermatophore is fixed at the substrate through a base from which a stalk rises of about 60 µm long.
(after Cassagnau 1971:609).
Fig.Bg. Bilobella grassei from France
Spermatophore anterior aspect
After Cassagnau, P. 1971 Fig.1D

Neanuridae. In Bilobella grassei the spermatophore is fixed at the substrate through a base from which a short stalk rises (15-25 µm long and 5-10 µm in diameter). Stalks up to 70 µm are found occasionally. The subspheric spermdrop is about 30-35 µm in diameter.
Composite spermatophores of 2 to 3 have been found.
(after Cassagnau 1971:610-612).
Fig.Bg. Bilobella aurantiaca from France
Spermatophore anterior aspect
C. composite spermatophore
D. detail apical button dorsal aspect
E. detail apical button lateral aspect
After Cassagnau, P. 1971 Fig.1E,2C,D,E

Neanuridae. In Bilobella aurantiaca, the spermatophore is fixed at the substrate through a rhizoid base from which a stalk rises (40 µm long and 3-5 µm in diameter). The ovoid spermdrop is about 20 µm wide and 30 µm high. The spermdrop lacks any superficiel nerves.
Composite spermatophores of 3 to 6 have been observed.
(after Cassagnau 1971:612-614).
Fig.Bm. Bilobella matsakisi from France
F. Spermatophore anterior aspect
A. Spermdrop in profile aspect after release of sperm
B. Spermdrop in apical pole aspect after release of sperm
After Cassagnau, P. 1971 Fig.1F,2A,B

Neanuridae. In Bilobella matsakisi, the spermatophore is fixed at the substrate through a rhizoid base from which a stalk rises of variable length. Medium length is 70-80 µm, but extremes of 50 µm and 150 µm have been observed. The diameter of the stalk ranges from 8 to 12 µm. The ovoid spermdrop is about 30 µm wide and 40-45 µm high. The spermdrop has nerves that form two windows from which the sperm is released (fig BmB).
Composite spermatophores of 3 to 7 have been observed.
(after Cassagnau 1971:614).
Fig.Lm. Lathriopyga monticola from France:
A. spermatophore anterior aspect
B. spermatophore head posterior aspect
C. spermatophore head lateral aspect
F. composite spermatophore
After Cassagnau, P. 1971 Fig.1A,B,C,2F

Neanuridae. In Deutonura monticola previously designated Lathriopyga monticola, the spermatophore comprises a stalk of about 100 µm high, 7 to 10 µm in diameter, and a spherical spermdrop of 40 to 45 µm diameter. The spermdrop is encapsulated in a membrane hold in shape by 2 nerves, doubled at their base, and united at the opposite distal pole into a button in the shape of a spiral (fig.LmA,B,C). The spermdrop opens by the rupture of the membrane between the fork of nerves (see arrows in fig.LmA,C).
Spermatophores are occasionally deposited on eachother forming a composite spermatophore (fig.Lm2F).
This composite spermatophore is one of the most evolved spermatophores among the Poduromorpha.
(after Cassagnau 1971:614).

Isotomidae. The stalk of the spermatophore penetrates the sperm drop at the basis and creates at the top of the drop a local nipple-like projection of the drop surface (fig.1d, fig.Kb, fig.Iso2).
Fig.Kb. Kalaphorura burmeisteri,
mirrored in spermatophore of Isotominae.
Specimen from the UK, Worthing.
2006.12.24 © Valentine, B.
Fig.Iso2. Spermatophore of Isotomidae.
Specimen from the UK, England, Nottingham.
2012.03.01 © Nurcombe, E.
Fig.Iso. Spermatophore of Isotominae.
Specimen from Holland, Schoonloo.
2012.12.19 © van Duinen, J.

Fig.IsoBV. Spermatophore of Isotominae from the UK, England, West Worthing.
Compare size with ♂ Dicyrtomina saundersi
2013.01.05 © Valentine, B.
Fig.Isov. Spermatophore of Isotominae
Specimen from the UK, West Worthing.
2013.12.15 © Valentine, B.
Fig.Isouk. Spermatophore of Isotominae.
Specimen from the UK, Moreton Morrell.
2013.12.17 © Phillips, E.

Fig.Isouk2. Spermatophore of Isotominae.
Specimen from the UK, Moreton Morrell.
2014.01.22 © Phillips, E.
Fig.Isouk3. Spermatophore of Isotominae.
Specimen from the UK.
2014.12.14 © Cunningham, T.
Fig.Isov2. Spermatophore of Isotominae
Specimen from the UK, West Worthing.
2017.01.09 © Valentine, B.

Spermatophores of Isotoma viridis consist of a stalk which is 235 µm long, which is attached to the substrate by a large basal plate. The tip of the stalk ends in a fine hook, from which the sperm drop of 100 µm diameter hangs. The terminal hook is located in an apical protuberance of the sperm drop (Poinsot-Balaguer, 1970; Betsch-Pinot, 1974) (fig.Iso, Isouk, Isouk2).

Entomobryidae.
Fig.Orchc. Orchesella cincta
Spermatophore shape
After Schliwa, W. 1965 Abb.56 Mitte
Fig.Orchv. Orchesella villosa from Italy. Spermatophore (sd=spermdrop; s=stalk).
After Fanciulli P.P. et al., 2012 Fig.13A

In Orchesella, where the males guard their freshly deposited spermatophores, the spermathophores are inspected regularly and aged spermatophores are eaten and replaced by new ones.
Fig.Orch. Aged spermatophore of Orchesella sp.
Specimen from Belgium, Profondeville.
2008.04.17 © San Martin, G.
Fig.Orch2. Spermatophore of Orchesella sp. Height 0.25mm
Specimen from Belgium, Limburg, Opitter.
2016.12.05 © Huskens, M.L.

Fig.Lep. Lepidocyrtus sp.
Spermatophore shape
2014.11.08 © Brito, N.P.
Brazil, Paraiba, Joao Pessao, in culture.
Fig.Lep. Lepidocyrtus sp.
"Field" of spermatophores
2014.11.08 © Brito, N.P.
Brazil, Paraiba, Joao Pessao, in culture.

Spermatophores are deposited in groups ("fields") and are guarded by the males.

Deuterosminthurus bicinctus
Sperm deposition and pick-up
2005 © Kozlowski MW & Aoxiang S.

Bourletiellidae. In Deuterosminthurus bicinctus the male deposits a spermdrop in front of the female. The female then immediately picks up the spermatophore. Male and female continue then in a kind of 'post-mating' ritual.

In Deuterosminthurus pallipes f. repandus the spermatophore has a very short stalk. It is deposited by the male in front of the female. As part of the courtship ritual the female partly eats the spermdrop. The male guides the female to the spermatophore by a thread that he produced by dipping his antenna in the freshly deposited capsule of the spermdrop.
Fig.Dpr. Deuterosminthurus pallipes f. repandus from Belgium, Limburg, Opitter
Spermatophore partly eaten by female during coutship ritual
2017.06.20 © Huskens, M.L.

Katiannidae.
Fig.Katsp. Katiannidae Genus nov. sp. nov. from the UK, England, Surrey
Spermatophore
2009.12.12 © Barton, T.
Fig.Kat. Katiannidae Genus nov. sp. nov. from the UK, England, Surrey
♀? with consumed spermatophore
2009.12.12 © Barton, T.
Fig.Kat2. Katiannidae from France. Spermatophores.
2012.08.21 © Lebeaux, P.

 
Fig.Kat3. Katiannidae Genus nov. sp. nov. from the UK, England, Staffordshire
♂ depositing spermatophore
2017.02.07 © Phillips, E.


Dicyrtomidae. In Dicyrtomina ornata, the spermatophore is 45 µm in diameter and contains about 600 spermatozoa (Hopkin 1997:136). In Dicyrtomina, the stalk of the spermatophore penetrates the sperm drop at the basis and continues out of the drop at the top (fig.1e, fig.Ds, Sminth, Sminthc, Sminthb). When the sperm drop has been picked-up by the female, the stalk remains empty (fig.Do, Dos).

Fig.Ds. Dicyrtomina saundersi: head close-up,
with spermatophore in front.
Specimen from the UK, England, Worthing.
2006 © Valentine, B.
Fig.Do. Dicyrtomina ornata
with empty stalk and spermatophore.
Specimen from the UK, England, Worthing.
2007.12.09 © Valentine, B.
Fig.Dos. Dicyrtomina ornata
with empty stalk, the remains of a just consumed spermatophore.
Specimen from the UK, England, Worthing.
2009.12.10 © Valentine, B.
Fig.DosF. Dicyrtomina ornata
Spermatophore.
Specimen from France, Cévennes.
2012.10.28 © Lebeaux, P.
Fig.Sminth. Sminthurus multipunctatus from France, Cévennes, inspecting freshness of spermatophore of ???.
2012.10.28 © Lebeaux, P.
Fig.Sminthc. From France, Cévennes. Spermatophore: close-up of spermdrop.
2012.10.28 © Lebeaux, P.

 
Fig.Ds. Dicyrtomina saundersi
Spermatophore with reduced spermdrop.
Specimen from the UK, Moreton Morrell.
2012.11.20 © Phillips, E.
Fig.Ds2. Dicyrtomina saundersi
Spermatophore inspected by ♂.
Specimen from the UK.
2015.12.14 © Phillips, E.
Fig.Ds3. Dicyrtomina saundersi
Spermatophore inspected by ♂.
Specimen from the UK.
2016.10.31 © Phillips, E.
Fig.Df. Dicyrtoma fusca
Specimen from Belgium.
2016.12.11 © Huskens, M.L.
Fig.D. Dicyrtomina sp.
Specimen from the UK.
2017.01.24 © Horton, M.

Sminthuridae.
Fig.Alfu. Allacma fusca as Sminthurus fuscus
Spermatophore shape
After Schliwa, W. 1965 Abb.56 links
Fig.Al.fu. Allacma fusca
Spermatophore stalk 614 µm
After Schaller, F. in Beier, M. 1970 Fig.70

In Allacma fusca, the stalk of the spermatophore ends in a fine, long, pointed filament, that is apically slightly curved, and that is penetrating deeply in the spermdrop. The curvature of the filament is evidently caused by the mass of the spermdrop. (After Schliwa, 1965:485).

Some examples of sizes of spermatophores

TaxonHeight of stalk (µm)Diameter of stalk (µm) base(top)Diameter of
spermdrop (µm)
Volume of
spermdrop (µm3)
Ratio stalkheight/spermdropRatio spermdrop/stalkdiameterReference
Stenaphorura quadrispina0-31-3915599-310590-Schaller (1970:43)
Protaphorura armata0-72-83195432-2993870-Schaller (1970:43)
Podura aquatica63846509651.405.8Schliwa (1965:489)
Pogonognathellus longicornis408-898?82-136288696-13170904.89-6.60?Schaller (1970:43)
Isotoma viridis235?1005235992.35?Poinsot-Balaguer (1970)
Betsch-Pinot (1974)
Orchesella cincta2405(1,4)40335106.008(28.6)Schliwa (1965:489)
Orchesella villosa264-409?49-7261601-1954325.39-5.68?Schaller (1970:43)
Entomobrya muscorum140-195?40-5333510-779523.50-3.68?Schaller (1970:43)
Sminthurides aquaticus0-43-5141630-694560-Schaller (1970:43)
Allacma fusca580-61411,2(4,2)1106969105.27-5.589.8(26.2)Schliwa (1965:489)
Schaller (1970:43)
Sminthurus viridis620-662?49-7261601-19543212.65-9.19?Schaller (1970:43)
Dicyrtomina minuta550-787?65-143143793-15311118.46-5.50?Schaller (1970:43)
Tab.I. Size of spermatophore.

Acknowlegdements

We would like to thank, in alphabetical order, Toby Barton, Nathan Paiva Brito, Thomas Cunningham, Miroslav Deml, Mark Horton, Marie Louise Huskens, Philippe Lebeaux, Eddie Nurcombe, Ed Phillips, Gilles San Martin, Brian Valentine, Jan van Duinen, and Peter Wieringa for granting us permission to use their images as illustrations.

Bibliography