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).
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
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.
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).
According to Cassagnau (1971:614), composite spermatophores are of the
most evolved spermatophores among the Poduromorpha,
but in culture, spermatophores are occasionally deposited on eachother
forming as such a composite spermatophore (fig.Lm.F).
(after Cassagnau 1971:614).
Isotomidae.
Anurophorinae.
In Cryptopygus antarcticus the spermatophore is between 0.18-0.2 mm high
and has a distinct basal plate of 0.05 mm diameter.
The stalk tapers apically.
The diameter of the spermdrop is 0.05 mm.
(Schaller & Kopeszki 1991:221).
Fig.Ca. Cryptopygus antacticus,
Specimen from Antarctica.
After Schaller, F. & Kopeszki, H. 1991 Abb.3
Isotominae.
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).
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).
The ratio spermdrop diameter / stalk height D/H in Isotomidae
is about 2.4 to 3 (fig.IsoTB).
Orchesellidae.
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.
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.
In Fasciosminthurus quinquefasciatus the male deposits a spermatophore
by pressing it genital opining against the substrate. Then it raises its
abdomen slowly while the stalk of the spermatophore is formed. Eventually
a spermdrop is placed on top of the stalk.
Sminthurididae.
In Stenacidia violacea, the male, clasped to the antennae of the female,
deposits a spermatophore in front of the female (Fig.Sv).
The spermatophore is quite big, relatively speaking.
According to Bretfeld (1999:61), the mating behaviour is unknown.
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, DoFB, DoMLH1, DoMLH2).
When the sperm drop has been picked-up by the female, the
stalk remains empty (fig.Do, Dos).
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
Taxon
Height of stalk (µm)
Diameter of stalk (µm) base(top)
Diameter of spermdrop (µm)
Volume of spermdrop (µm3)
Ratio stalkheight/spermdrop
Ratio spermdrop/stalkdiameter
Reference
Stenaphorura quadrispina
0
-
31-39
15599-31059
0
-
Schaller (1970:43)
Protaphorura armata
0
-
72-83
195432-299387
0
-
Schaller (1970:43)
Podura aquatica
63
8
46
50965
1.40
5.8
Schliwa (1965:489)
Pogonognathellus longicornis
408-898
?
82-136
288696-1317090
4.89-6.60
?
Schaller (1970:43)
Cryptopygus antarctica
130-150
?
50
65450
2.6-3.0
?
Schaller & Kopeszki (1991:222)
Isotoma viridis
235
?
100
523599
2.35
?
Poinsot-Balaguer (1970) Betsch-Pinot (1974)
Orchesella cincta
240
5(1,4)
40
33510
6.00
8(28.6)
Schliwa (1965:489)
Orchesella villosa
264-409
?
49-72
61601-195432
5.39-5.68
?
Schaller (1970:43)
Entomobrya muscorum
140-195
?
40-53
33510-77952
3.50-3.68
?
Schaller (1970:43)
Homidia taibaiensis
170
?
34
20569
5.0
?
Cheng (2022:pers.com.)
Sminthurides aquaticus
0
-
43-51
41630-69456
0
-
Schaller (1970:43)
Allacma fusca
580-614
11,2(4,2)
110
696910
5.27-5.58
9.8(26.2)
Schliwa (1965:489) Schaller (1970:43)
Sminthurus viridis
620-662
?
49-72
61601-195432
12.65-9.19
?
Schaller (1970:43)
Dicyrtomina minuta
550-787
?
65-143
143793-1531111
8.46-5.50
?
Schaller (1970:43)
Tab.I. Size of spermatophore.
Acknowlegdements
We would like to thank, in alphabetical order,
S. Aoxiang,
Toby Barton,
Nathan Paiva Brito,
Turner Brockman,
Hsin-Ju Cheng,
Thomas Cunningham,
Miroslav Deml,
Benjamin Fabian,
Mark Horton,
Marie Louise Huskens,
M.W. Kozlowski,
Philippe Lebeaux,
Eddie Nurcombe,
Ed Phillips,
Jérôme Picard,
Brigitte Reinach,
Gilles San Martin,
Fred's Uncle,
Brian Valentine,
Jan van Duinen,
David W,
Peter Wieringa,
Mirella Zeeders
for granting us permission to use their images as illustrations.
