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Acta Zoologica (Stockholm) 82: 331– 349 (October 2001)
Functional morphology of the male genitalia and copulation
in lower Hymenoptera, with special emphasis on the
Tenthredinoidea s. str. (Insecta, Hymenoptera, ‘Symphyta’)
Blackwell Science Ltd
Susanne Schulmeister
Institut für Zoologie und Anthropologie,
Abteilung Systematik, Morphologie und
Evolutionsbiologie, Berliner Str. 28,
D–37073 Göttingen, Germany
Keywords:
Hymenoptera, Tenthredinoidea,
morphology, male genitalia, copulation
Accepted for publication:
5 April 2001
Abstract
Schulmeister, S. 2001. Functional morphology of the male genitalia and
copulation in lower Hymenoptera, with special emphasis on the Tenthredinoidea
s. str. (Insecta, Hymenoptera, ‘Symphyta’). — Acta Zoologica (Stockholm) 82:
331–349
A general description of the male reproductive organs of lower Hymenoptera
is given. The terminology of the male genitalia is revised. The male external
genitalia of Tenthredo campestris are treated in detail as a specific example of
the morphology. The interaction of the male and female parts during copulation is described for Aglaostigma lichtwardti. The possible function of sclerites
and muscles of the male copulatory organ of Tenthredinoidea s. str. is discussed. Additional observations on morphology and function made in nontenthredinoid lower Hymenoptera are included. The assumption that the
gonomaculae act as suction cups is confirmed for the first time. The evolution
of obligate and facultative strophandry is discussed. The stem species of all
Hymenoptera was probably orthandrous and facultatively strophandrous.
Susanne Schulmeister. Institute of Zoology, Berliner Str. 28, D – 37073 Göttingen,
Germany. E-mail: sschulm@gwdg.de
Introduction
The lower Hymenoptera known as ‘Symphyta’ or sawflies
are a paraphyletic grouping lacking the wasp-waist of the
Apocrita. Among them, the Tenthredinoidea s. str. [Argidae,
Cimbicidae, Diprionidae, Pergidae (= Pterygophoridae) and
Tenthredinidae] are probably monophyletic ( Vilhelmsen
1997, 2001). With about 7400 described species, the
Tenthredinoidea s. str. comprise the majority of the approximately 8000 described sawfly species (Goulet and Huber
1993).
Since the ‘Symphyta’ are the basal groups of Hymenoptera, they play an important role in the elucidation of the
relationships between holometabolous insect groups. Many
morphological features of lower Hymenoptera have already
been studied intensively and used for phylogenetic analysis
(Königsmann 1976, 1977; Vilhelmsen 1997, 2000; references therein), but very few characters of the male external
genitalia were employed in these studies. Of the five male
genital characters included in Vilhelmsen (2001), two were
coded as invariant in the Hymenoptera, and therefore only
three were potentially informative for the phylogenetic rela-
© 2001 The Royal Swedish Academy of Sciences
tionships among Hymenoptera. This scarcity of male genital
characters is due to the fact that a comparative analysis in a
phylogenetic context does not exist. The detailed investigation of the morphology and function of the male copulatory
organ of the Tenthredinoidea s. str. presented here was
undertaken to serve as the basis for such an analysis.
To date, the most extensive publication on the male external genitalia of ‘Symphyta’, especially their musculature, is
that of Boulangé (1924). Other noteworthy papers on this
topic are those of Birket-Smith (1981), Crampton (1919),
Peck (1937), Ross (1945), Michener (1956), E. L. Smith
(1969, 1970a, 1970b, 1972), and Snodgrass (1941). The
copulation of sawflies is discussed in Boulangé (1924),
Rohwer (1915), d’Rozario (1940), and E. L. Smith (1970a).
The function of the genital muscles of a male braconid
(Apocrita) was studied by Alam (1952). However, the present
paper treats the morphology and especially the function in
much more detail.
There has been a lot of confusion about the terminology
of the parts of the male genital organ in Hymenoptera. A
main source for this confusion is the fact that early authors
studied mainly Apoidea, in which the male copulatory organ
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Male genitalia and copulation in Hymenoptera • Schulmeister
is highly derived, and later on their terms were often applied
to non-homologous parts in other Hymenoptera. A treatment
of all terms that have been applied to the male external genitalia of Hymenoptera is beyond the scope of this paper, but
is in preparation. However, the usage of the most important
of the many existing terms is discussed in the present paper.
An interesting feature of the male genital organ of Xyelinae
and Tenthredinoidea s. str. is that it is revolved as a whole by
180° on its median axis (Crampton 1919). The normal condition is called orthandrous (orthandrious), the rotated condition strophandr(i)ous (Crampton 1919). In strophandrous
sawflies, the true ventral side becomes the apparent dorsal
side of the genital organ, which Boulangé (1924) termed exventral. In this paper, the terms ventral and dorsal always
refer to the original (i.e. orthandrous) condition, i.e. ‘ventral’
always means ‘anatomically ventral’. Strophandry probably
evolved independently in Xyelinae and Tenthredinoidea
s. str. ( Vilhelmsen 1997, 2001). According to Rasnitsyn (1969;
in Ronquist et al. 1999), the torsion is already present in the
pupa in Tenthredinoidea s. str., while in Xyelinae it appears
during eclosion. No anatomical differences in the torsion of
the male genitalia could be observed in these two taxa.
However, in the copulation of orthandrous as well as
strophandrous Hymenoptera the ventral side of the male
genitalia is always facing up, whereas the dorsal side is always
facing down, towards the substrate. In orthandrous species
this is achieved, for example, by curving the abdomen so that
the tip of the abdomen comes to lie upside down. In
strophandrous species such a measure is unnecessary
because the male genitalia already are upside down.
Material and Methods
The species studied are shown in Table 1.
All specimens were fixed in Bouin’s fluid and kept in
ethanol (70%) until the preparation. If possible, two or more
Acta Zoologica (Stockholm) 82: 331– 349 (October 2001)
exemplars from each species were examined. The male
genitalia were dissected under a Zeiss stereomicroscope
Stemi SV 6 (maximum magnification 50). Viewing the
objects under light coming from the side (obtained by pointing the tip of a goose-necked lamp at the side of the preparation dish) proved sufficient for a discrimination of the parts,
so that staining was not necessary. Drawings were made with
the aid of a camera lucida.
Sclerites and membranes of the male genitalia can be hard
to distinguish at the beginning. It proved useful to dry a genital organ in a critical point dryer, apply a gold-coating (as for
electron microscopy), and examine it under a stereomicroscope. Sclerites treated in this manner appear smooth and
shining, whereas membranes appear rough and dull.
Copulations were either observed (rather coincidentally)
in the field (in C. pygmeus, E. koehleri and T. temula) or initiated by putting a female and a male together in a vial (in
C. pygmeus, A. lichtwardti and M. ferruginea). Pairs fixed in
copula were obtained by drowning them in alcohol (70 – 95%)
during copulation. The pairs stayed coupled in about 30 –
50% of the attempts. Four pairs in copula of A. lichtwardti
were dissected.
Aglaostigma lichtwardti was chosen for a detailed study of
copulation because it was the only tenthredinoid species of
which several pairs in copula could be obtained. However,
the drawings in the morphological part of this paper show
mainly Tenthredo campestris, because its male copulatory
organ is less derived than that of Aglaostigma and therefore
facilitates comparison with other species. However, the differences are not substantial, so that the general conclusions drawn about the functional morphology in the present
paper should apply to both these species and most other
Tenthredinoidea s. str. as well. (The differences between
these two species can be deduced to some extent from
Fig. 2A,B vs. 4B,C; Fig. 8A vs. 8D; Fig. 7F vs. 9 A, and from
Fig. 6)
Table 1 Species studied in this paper
Xyeloidea:
Xyelidae:
Macroxyela ferruginea (Say, 1824)
Tenthredinoidea:
Blasticotomidae
Tenthredinidae:
Runaria reducta (Malaise, 1931)
Nematus abbotii (Kirby, 1882)
Tenthredo campestris (Linnaeus, 1758)
Tenthredo temula (Scopoli, 1763)
Macrophya annulata (Geoffroy, 1785)
Aglaostigma lichtwardti (Konow, 1892)
Elinora koehleri (Klug, 1817)
Arge rosae (Linnaeus, 1758)
Arge rustica (Linnaeus, 1758)
Lophyrotoma analis (Costa, 1864)
Macrodiprion nemoralis (Enslin, 1917)
Argidae:
Pergidae:
Diprionidae:
Pamphiliidae:
Megalodontes cephalotes (Fabricius, 1781)
= klugi (Leach, 1817) = spissicornis (Klug, 1824)
Cephalcia sp.
Cephoidea:
Cephidae:
Cephus pygmeus (Linnaeus, 1767)
Siricoidea:
Siricidae:
Anaxyelidae:
Xeris spectrum (Linnaeus, 1758)
Syntexis libocedrii Rohwer, 1915
Pamphilioidea:

Megalodontesidae:
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Schulmeister • Male genitalia and copulation in Hymenoptera
Fig. 1—Male reproductive organs.
—A. Schematic drawing to show the
relations of the membranous parts of the
integument, the sclerites and the inner
reproductive organs. —B. One half of the
male genitalia of Tenthredo campestris, looking
onto the medio-sagittal plane (cf. Fig 7E,F).
Scale in all figures: 1 mm.
Results
The male reproductive organs consist of inner and outer
parts. The latter have been called genitalia, external genitalia,
genital appendages, genital armature, armatura genitalis,
genital capsule, phallus, genital or copulatory organ, genital
or copulatory or phallic apparatus. The genital capsule is
situated between the ninth and tenth sternum, but due to displacement it does not lie ventrally but rather at the tip of the
abdomen concealed in the genital chamber, that is above the
hypopygidium (ninth sternum) and below the proctiger (anal
papilla). The ninth sternum often has an apophysis, called
the spiculum, at its anterior tip.
In Hymenoptera, the male copulatory organ is connected
to the rest of the abdomen only via a thin membrane, the
ducti ejaculatorii, muscles, tracheae and nerves; it can easily
be pulled out and removed. It can also be easily turned
around. In strophandrous sawflies, Xyelinae and Tenthredinoidea s. str., the rotated condition of the male genitalia is
permanent. In the past, there has been some confusion as to
the condition in the Blasticotomidae, but work by Togashi
(1970) and Vilhelmsen (1997) and my own observation (in
Runaria reducta Malaise) show that at least Blasticotoma
filiceti Klug and Runaria reducta are orthandrous.
Inner reproductive organs
The inner reproductive organs consist of the testes, vasa
deferentia, vesiculae seminales, glandulae mucosae (accessory
glands) and ducti ejaculatorii (Fig. 1A). The vasa deferentia
lead from the testes to the glandulae mucosae. The vesicula
seminalis is basically the enlarged proximal part of the vas
© 2001 The Royal Swedish Academy of Sciences
deferens and is coiled into a spiral or lump before fusing with
the side of the glandula mucosa. The latter can be described
as a blind sac which can assume different shapes. An extreme
example is a striking apomorphy observed in Megalodontes
cephalotes which has not been described until now. In this
species, the glandula mucosa has three blind ends instead of
one, and the vesicula seminalis is ‘nestling’ among these
three ends. It would be interesting to examine other species
of the Megalodontesidae in order to find out whether it is an
autapomorphy of the whole group. The caudal ends of the
glandulae mucosae continue into the ducti ejaculatorii,
which fuse to become the unpaired ductus ejaculatorius
before entering the external genitalia.
Membranous parts of the external male genitalia
Figure 1A shows the relationships between the sclerotized
and the membranous parts of the integument of the external
male genitalia, which is continuous with the internal ducts.
The ductus ejaculatorius passes between the two penisvalvae
(Fig. 1B cf. Fig. 4B,D) before being enlarged to constitute
the endophallus, which is a more or less sac-like structure in
the centre of the genital organ (Fig. 1A,B). The transition
from the ductus ejaculatorius to the endophallus can be
formed in a way that produces the incorrect impression that
they were separate structures and that the ductus penetrated
the wall of the endophallus. This transition is called the original or primary gonopore. However, the ductus ejaculatorius
is in no way separated from the endophallous, just as the
endophallic membrane is continuous with the ectophallic
membrane which constitutes the surface of the copulatory
organ. The opening of the endophallus to the outside is called
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Male genitalia and copulation in Hymenoptera • Schulmeister
Fig. 2—Male external genitalia of Tenthredo campestris.
—A. (Morphologically) dorsal side (which is actually ventral, due to
the strophandry). —B. Ventral side. —C. Cupula, seen from inside.
—D. Gonostipites and one harpe, dorsal view. —E. Same, from
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ventral. —F. Penisvalva. —G. Volsella, outer face. —H. Volsella,
inner face. —I. Parossiculus, distivolsella dotted. —J. Parossiculus,
distivolsellar apodema dotted.
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the phallotrema, secondary gonopore, or gonotrema. The
phallotrema is on the ventral side of the genital apparatus and
closed to a slit (Fig. 2B). Snodgrass (1941) wrote that the
endophallus ‘Probably ( ... ) is always eversible’, but I could
only observe this in Cephidae.
The term penis has probably been applied to nonhomologous structures in the different insect orders. In
Hymenoptera, the membrane situated between the distal
heads of the penisvalvae, i.e. the valvicepes, was sometimes
termed penis (e.g. Michener 1956). Some authors (e.g.
Snodgrass 1941) call this distal portion of the endophallic
membrane a penis only if it forms a structure separate from
the penisvalvae, as is the case in Apoidea. In ‘Symphyta’ there
is no structure to which this second definition would apply.
The word aedoeagus is usually understood as meaning the
intermittent part of the genitalia, which in Hymenoptera
are the valvicepes and the membrane between them. For
the definition of phallus see Snodgrass (1941; p. 3). In the
Hymenoptera, the phallus is the entire male genital capsule.
Sclerites of the male genitalia
In Hymenoptera, the male copulatory organ consists of four
main sclerites which are connected only through membrane
and muscles (unless secondarily fused): an unpaired basal
ring, two pairs of clasping organs serving to grip the female
during copulation, and a pair of median skeletal supports for
the intromittant organ. These main sclerites are described in
detail below.
An overview of the most important terms for sclerites of
the male genitalia and their different usages is given in Fig. 3.
Tables like this and lists of synonyms are numerous in the
literature (e.g. Boulangé 1924; Beck 1933; Snodgrass 1941;
Michener 1956; E. L. Smith 1970a,b; Birket-Smith 1981;
Kopelke 1982), but none of them is entirely correct.
Cupula. The proximal basis of the genital organ is surrounded
by the unpaired cupula [coined by Birket-Smith (1981) after
cupule (Audouin 1821); = basal ring (Crampton 1919) ]
(Fig. 2A– C).
Michener (1944a,b, 1956) called the cupula gonobase,
but ‘gonobasis’ is also being used for non-homologous parts
in basal insects (e.g. Willmann 1998).
In the primitive condition, the cupula is a closed ring
which is broad dorsally, but narrow on the ventral side, where
it is medially protruded into an apophysis, the gonocondyle
(Crampton 1919). The ventral side of the cupula can be
strengthened by an internal ridge (Fig. 2C) or thickening.
The cupula surrounds the basal opening termed foramen
genitale (Snodgrass 1941). It can be fused in part with the
gonostipites, e.g. in Arge. The dorsal portion can be reduced
to a narrow string as in Aglaostigma lichtwardti (Fig. 4B) or
completely reduced as in Arge (Fig. 4A) and Megalodontes
cephalotes. The cupula can also be missing completely as in
Lophyrotoma analis.
© 2001 The Royal Swedish Academy of Sciences
Schulmeister • Male genitalia and copulation in Hymenoptera
Latimere. The latimere (new term) consists of the gonostipes
(see discussion below) and the harpe (Crampton 1919)
(Fig. 2D,E). In Cephidae, Orussidae and many Apocrita, the
‘outer clasper’ of the male external genitalia is represented
only by a single piece. For this piece Peck (1937) proposed
to employ a term of its own – for which he chose gonoforceps
– because we cannot tell for certain whether this single piece
evolved through a fusion of gonostipes and harpe and is,
hence, homologous to the latimere or through a total reduction of the harpe, thus being homologous to the gonostipes
alone. Some authors claimed that there was a line on the
gonoforceps in certain species which is taken as evidence of
a fusion, but even if there were such a line it could still have
originated secondarily.
Until now, the word harpes has not only been used for the
plural, but erroneously for the singular as well (e.g. by Ross
1945; Wong 1963; Königsmann 1976).
The term stipes was applied to a part of the male external
genitalia of Hymenoptera for the first time by Thomson
(1871/72). He used it for Bombus in which the harpe is
reduced and the volsella merely a small scale on the medial
face of the gonostipes (according to Snodgrass 1941), which
is not depicted in Thomson’s figure. Therefore it is impossible to say which parts Thomson understood as stipes.
Crampton (1919) changed Thomson’s term to ‘gonostipes’
and applied it to what is today called gonostipes and volsella.
Later on, Crampton’s term ‘gonostipes’ has been mistakenly
used to stand for the gonostipes alone, without the volsella
(e.g. Peck 1937; Ross 1945; Königsmann 1976). But since
gonostipes is a well-known term and as today’s meaning has
consistently been applied, I do not want to change this and
use it in its modern sense, i.e. excluding volsella. I want to
point out that the term should not imply any homology to
any parts of mouthparts or legs.
Birket-Smith (1981) suggested the use of stipes instead
of gonostipes (according to the rule of priority), but used the
term stipes for gonoforceps/latimere, i.e. differently from
either the original or the modern sense of gonostipes. Since
this would only add confusion and because the term stipes
already exists for a mouthpart (which is why Crampton
replaced it with gonostipes), I reject the use of the word
stipes. I also do not follow Birket-Smith’s (1981) suggestion
to use the term harpide (Audouin 1821) instead of harpe
because Audouin coined the term harpide for a genital
part of the bumblebees, which do not have a harpe.
Therefore the harpide cannot be homologous to the part
called harpe.
Gonostipes and harpe have also been called gonocoxite
and gonostylus (Michener 1944a, 1944b, 1956). The terms
imply a homology with coxa and stylus, and I prefer to
employ neutral terms for the time being. Furthermore, if
parts of the hymenopterous male genitalia are homologous to
the gonocoxa, this would probably be the cupula, gonostipes
and volsella together and not just the gonostipes. Regarding
the stylus, there was disagreement whether this would be the
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Acta Zoologica (Stockholm) 82: 331– 349 (October 2001)
Fig. 3—Some terms of the male genitalia of Hymenoptera as used – but not necessarily coined – by some authors. Apostrophes indicate
different uses of the same term.
harpe (e.g. E. L. Smith 1969, 1970a,b) or the digitus
(Birket-Smith 1981).
The popular term paramere is highly ambiguous, even if
only its application to the hymenopterous genitalia is considered: in Fig. 3 there are just two of many different usages.
Verhoeff (1893) applied the term paramere to gonostipes,
harpes and volsella. Beck (1933) and Peck (1937) employed
it for the penisvalva. Snodgrass used it first for the harpe only
(Snodgrass 1941) and later on for gonostipes and harpe
together (Snodgrass 1957), arguing that both are derivatives

of the lateral larval phallomeres (= ‘parameres’). Moreover,
if the cupula is a derivative of the gonostipites – and not a
newly formed sclerotization of the basal ectophallic membrane, as Snodgrass assumed – the term paramere would also
have to comprise one half of the cupula. (The same problem
is inherent to the term ‘basimere’.) Most contemporary
hymenopterists (except for Königsmann 1976) still use the
word paramere in the sense of Snodgrass (1941), obviously
not realizing that Snodgrass (1957) himself objected to this
with good reason. Because the term paramere is highly
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Schulmeister • Male genitalia and copulation in Hymenoptera
Fig. 4 —Male external genitalia of —A. Arge rustica (morphologically) dorsal side —B. Aglaostigma lichtwardti, dorsal —C. same, ventral,
and —D. Macrodiprion nemoralis, dorsal.
ambiguous and used incorrectly in adult Hymenoptera, I
prefer not to use it at all.
The discussion about the terms paramere sensu Snodgrass
(1941) (= harpe) gets even more complicated when considering the Apocrita. The stem species of the Apocrita probably
had a gonoforceps, i.e. no or no separate harpe. In some
Apocrita, however, the gonoforceps is secondarily divided
into two parts (Snodgrass 1941; Königsmann 1976). If we
assume that the gonoforceps developed through fusion of
gonostipes and harpe, so that the distal portion of the gonoforceps corresponded to the harpe, one could assume – as
Snodgrass (1941) did – that the secondary appendix in some
© 2001 The Royal Swedish Academy of Sciences
Apocritans corresponds to the original harpe and can therefore be designated with the same name. But the secondary
division itself is not identical to the primary division.
Moreover, secondary divisions probably evolved several
times independently in the Apocrita. To make clear that the
appendices of some Apocrita are not directly derived from
the primary appendices (= harpes) of some lower Hymenoptera, one should consider naming each independently
derived secondary appendix differently. For this reason,
Birket-Smith (1981) proposed the term kleisiades for the
secondary appendix in Lapidus and Dorylus (Dorylidae,
Formicoidea).
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The gonostipites are the central and largest sclerites of
the genital organ and constitute its main framework. The two
gonostipites abut dorsally as well as ventrally so that they
surround the genital apparatus (Fig. 2D,E). The medial area
of the dorsal side of the gonostipes is called the parapenis
(Crampton 1919). In some Tenthredinoidea, the parapenis is
set off against the rest of the gonostipes (Fig. 4B), sometimes
only connected to it by a narrow bridge (Figs 2D, 4D).
Boulangé (1924) mentioned it as ‘le pont reliant le parapenis au flanc ...’ The connection between the parapenis
and the rest of the gonostipes, be it a narrow bridge or a
rather abstract cranial-caudal line (as in Fig. 4B), has been
termed the parapenisjugum in the present study.
In the primitive condition, the parapenes touch each
other, but are not fused (Figs 2D, 4B). In some species, however, a proximal fusion occurs secondarily (Fig. 4A,D).
Crampton (1919) only employed the term parapenis when
this structure was clearly set off. Boulangé (1924; p. 59)
argued that the insertion site of muscle j should be called
parapenis, even if not set off against the rest of the gonostipes. But since the insertion site of a muscle can wander to
a different place during the course of evolution (see below),
it cannot be decisive for naming a sclerite. Therefore, the
parapenis is here defined as the baso-medial part of the dorsal
gonostipes. In all but one of the species I examined, this area
is the insertion site of muscle j; only in Megalodontes cephalotes, did muscle j insert on an inflection of the medial edge
of the dorsal gonostipes; in this case it is uncertain which part
is homologous to the parapenis.
The basal edge of the gonostipes (including the parapenis)
is reinforced by an inflection (Fig. 2D). Where the parapenis
is set off against the rest of the gonostipes, its lateral edge is
reinforced by a thickening (Fig. 2E). On the ventral side, the
median edge of the gonostipes does not always form a distinct line, but may instead turn gradually into membrane.
Basally, the gonostipes is elongated into a brace-like structure, the gonostipital arm (Crampton 1919) (Fig. 2D,E).
However, it is not possible to draw a clear line between the
gonostipal arm and the rest of the gonostipes (except maybe
in extreme cases as in the Pamphilioidea and Xiphydriidae).
The tip of the gonostipital arm is an insertion site for muscles
h and i and is here termed the apex gonostipitis (new term)
(Fig. 2E).
Boulangé (1924) called it apophyse principal (which has
been mistaken as being synonymous with the gonostipal
arm), but it is not an apophysis sensu Snodgrass (1935).
Each harpe is formed like a hollow dish and situated at
the disto-lateral edge of a gonostipes. The harpes are covered
with many bristles (which are not depicted in the drawings
presented in this paper). There is a membranous area called
the gonomacula (Crampton 1919) = ventouse (french for
sucker; Dufour 1854) = cupping disk (Snodgrass 1941) on
the distal tip of the harpe (Fig. 7C) in Xyelidae, Pamphiliidae, Megalodontesidae, Siricidae and Xiphydriidae. The
gonomaculae are absent in Tenthredinoidea s. str., Cephidae,
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Anaxyelidae, Orussidae and Apocrita. The absence of
gonomaculae in the only extant anaxyelid Syntexis libocedrii
(Middlekauff 1964) was confirmed in the present study.
Although the gonomacula is coded as absent in the Blasticotomidae Runaria reducta, Paremphytus flavipes (Takeuchi) and
Blasticotoma filiceti in Vilhelmsen (in press), I found a tiny
rest of a gonomacula in the blasticotomid Runaria reducta,
but was not able to study any other species of that family.
Since a muscle inserts on the gonomacula, several authors
assumed that it probably functions like a suction cup. So far,
this theory had not been confirmed.
Volsella. On the ventral side of the male external genitalia,
between the gonostipes and the penisvalva, lies the volsella
(sensu Snodgrass) (Fig. 2G–J ). It is a pincer-like structure
and consists of two separate sclerites, the lateral parossiculus
and the smaller gonossiculus (both Crampton 1919) =
digitus (volsellaris) (Snodgrass 1941). Both sclerites are
attached to each other along their middle parts by a narrow
unpigmented, but sclerotized line. In some Hymenoptera
(e.g. Cephalcia sp., Cephus pygmeus and Xeris spectrum), the
volsella is fused secondarily with the gonostipes.
Dufour (1841) coined the term volselle after the Latin
word volsella and marked it in his drawings of the male
genitalia of some Apocrita. His definition and figures are
quite vague, but it seems that he applied ‘volselle’ to different structures, namely the penisvalva, the volsella sensu
Snodgrass, and the ventral lamella of the gonoforceps. Peck
(1937), Snodgrass (1941), Ross (1945), Alam (1952),
Michener (1944a,b, 1956), Königsmann (1976), Gauld and
Bolton (1988), Schedl (1991), and Ohl (1996) – among
others – called the gonossiculus and parossiculus together
the volsella. Although Birket-Smith (1981) wanted ‘to use
only terms that never have been used for more than one
structure in the Hymenoptera’, he employed the word
volsella in the sense of Crampton (1919), i.e. for the parossiculus only, obviously not realizing that contemporary
authors were using it differently and that the term had not been
coined by Crampton himself. Crampton (1919), Boulangé
(1924), and Birket-Smith (1981) did not have a specific term
to summarize gon- and parossiculus. E. L. Smith (1969,
1970a, 1970b, 1972) employed the expression ‘Section 3 of
gonocoxite lX’. Since there exists no good alternative and
since nearly all authors used and still use the term volsella in
the sense of Snodgrass (1941), I do not want to replace this
popular term in spite of its ambiguity. Contrary to the case
of the word paramere, there is no morphologically correct or
wrong meaning for volsella.
The parossiculus consists of a basal ‘handle’, termed the
basivolsella, and a distal ‘hook’, the distivolsella (Fig. 2I),
part of which is a basally directed muscle insertion site called
distivolsellar apodeme (Fig. 2J ) (all three terms by Peck
1937). The distivolsella (including the apodeme) was termed
cuspis (volsellaris) by Snodgrass (1941). It must be emphasized that the basivolsella and distivolsella (cuspis) are not
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separate in any way, they make up one contiguous sclerite.
Cuspis and digitus are usually opposable and are used as a
clasper. In summary, the volsella can be distinguished either
in parossiculus and gonossiculus or in basivolsella, cuspis
(distivolsella) and digitus (gonossiculus).
When used together, the terms basivolsella and distivolsella have the disadvantage that this combination seems
to imply that together they form the entire volsella, which can
lead to two misinterpretations: Either, that the volsella was
identical with the parossiculus, without the gonossiculus =
digitus [which might have led Birket-Smith (1981) to use
volsella in this way, contrary to all contemporary authors], or
to the misinterpretation that the distivolsella comprises not
only the cuspis but also the digitus (e.g. in Schedl 1991).
Similarly, the fact that the terms cuspis and digitus are usually used together as a pair has similarly led people to believe
that they together make up the whole volsella, i.e. that the
cuspis would be the entire parossiculus (e.g. in Kimsey and
Bohart 1990; Kopelke 1982).
The basivolsella runs parallel to the median edge of the
gonostipes and although parts of it can be hidden behind the
gonostipes and membrane (Figs 2B, 4C), it is an external
structure. The carina volsellaris = volsellar ridge (both terms
Snodgrass 1941) = volsellar strut (Peck 1937) is an apodeme
running across the length of the basivolsella, forming a ridge
internally and a sulcus externally (Fig. 2G,H). The distivolsella bears bristles (not depicted).
According to the definitions of structural terms given
by Ronquist and Nordlander (1989), the carina volsellaris
is a ridge and not a carina, since they define carina as an
‘external, simple ridge’. Others, however, seem to regard a
carina also as an internal ridge (e.g. Gibson 1985).
Ross (1945) wrote about the gonossiculus: ‘The gonolacinia has an apical portion or apiceps (ap) and a basal prolongation or basiura (ba).’ Unfortunately, it does not become
clear from his text or figures where he drew the line to these
parts. Therefore, I replace his terms with digiceps and
digiura and define the digiura as the free proximal handle of
the gonossiculus, and the digiceps as the rest, which is connected to the parossiculus (Fig. 2G).
Penisvalva. In the middle of the external genitalia, parallel to
the medio-sagittal plane, lie the two penisvalvae (Crampton
1919), each of which has approximately the shape of a spoon
(Fig. 2F). The apical ‘disc’ is called valviceps, the long
‘handle’ valvura (both terms by Ross 1945). Along its rim
(dorsally, apically and ventrally), the valviceps is continuous
with ectophallic membrane, by which it is connected to the
other valviceps (Fig. 1A,B). The ventral membrane stretches
dorsally to form a trough, the endophallus. In some ‘Symphyta’
(e.g. Cephus pygmeus and Xeris spectrum) and in many Apocrita, the valvicepes are not separate dorsally. The valvura is
not connected to any membrane, because it is an internal
apodeme of the valviceps extending into the lumen of the
genital organ. In many species, e.g. Tenthredo campestris, the
© 2001 The Royal Swedish Academy of Sciences
Schulmeister • Male genitalia and copulation in Hymenoptera
valvurae are long enough to pass through the foramen
genitale. Where the valviceps connects to the valvura, there
is a small side branch, the ergot (french for spur; Boulangé
1924), which serves as an insertion site for several muscles.
The ergot can be reduced, e.g. Tenthredo campestris; in this
case the muscles simply insert on the valvura at the position
where the ergot would have sat.
In the Nematinae (Tenthredinidae), the penisvalvae show
a derived, complicated structure, described by Ross (1945)
and Wong (1963). The fine structure and evolution of the
penisvalvae were treated extensively by E. L. Smith (1969,
1970a, 1972).
Other sclerites of the aedoeagus. The median sclerotized style
(Ross 1937) = detached rhachies (E. L. Smith 1969, 1970a,b)
= ventral rod of aedoeagus (Snodgrass 1941) is present in
the Cephidae and Siricidae and, according to Smith (1970a),
has arisen through splitting from the penisvalvae. It is a long,
thin sclerite and lies on the median axis of the ventral side of
the external genitalia, between the two penisvalvae. The
median rod is situated in the place where in other groups
would be the phallotrema. In Cephidae, its basal end is fused
with the gonostipes, but in Siricidae it is not.
In Apoidea there are different sclerotizations of the dorsal
penis membrane, e.g. median rod, spatha (see Snodgrass
1941).
Fibula ducti. There is a very small sclerite situated on the
ducti ejaculatorii where they unite to form an unpaired ductus (Fig. 4A). In Arge rosae, for example, it is represented by
two small sclerotic plates situated ventrally and dorsally of
the ductus ejaculatorius, and dissection shows that there is a
minute sclerotized bridge connecting the dorsal and ventral
parts in the median plane. The one depicted in Fig. 4A is
unusually large; normally this sclerite is much smaller, often
transparent and inside the ductus, so that it is difficult to see.
To my knowledge, this sclerite has been depicted in a sawfly
only by D. R. Smith (1990; p. 46), in Perreyiella, a pergid, but
not named, and I term it fibula ducti.
In Lophyrotoma analis, the fibula ducti is unusually large.
In Arge rosae, it is large as well, but transparent, while in
numerous other tenthredinoid and non-tenthredinoid
‘Symphyta’ there is often only a trace of the fibula ducti. In
other species, e.g. Tenthredo campestris, it is absent.
Clausen (1938: 247 f.) described a similar sclerite situated
inside the unpaired ductus ejaculatorius of Formica rufa,
which he termed Sperrkeil. Further research has to be done
to determine whether the fibula ducti and the Sperrkeil are
homologous. The fibula ducti might even have a homologue
in Mecoptera, the Ostialsklerit ( Willmann 1981, 1989). The
Ostialsklerit is also situated at the end of the ductus ejaculatorius, but – contrary to the fibula ducti and the Sperrkeil –
is furnished with a pair of muscles. All these sclerites seem
to support the assumption that the ductus ejaculatorius is of
ectodermous origin (Snodgrass 1941: 41957 : 2).
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Fig. 5—Male and female Aglaostigma
lichtwardti in copula. Male parts are dotted.
Of the female, only the end of the abdomen is
shown. Of the male, the end of the abdomen
is shown in A. In B –D the male abdomen was
removed so that only the genitalia are
shown. —A. Lateral view. —B. Same,
left half of female removed except for the
seventh sternum. —C. Ventro-lateral view.
—D. Ventral view.
Copulation
Observations in live Tenthredinidae show that during copulation male and female of these strophandrous species are
both standing on the substrate facing opposite directions.
The male slips the tip of his abdomen under that of the
female and presses his harpes onto the sides of her seventh
sternum. In Elinora koehleri and Tenthredo temula, I observed
that the male often has one or both of his hind legs on the
female’s wings during copulation. The females sometimes
move during copulation, dragging the male behind.
Pairs of the orthandrous species Cephus pygmeus were
observed to copulate with the male on the female’s back.
Some females kept feeding on pollen and after a while moved
their saws against the male genitalia, seemingly trying to
remove them.

Although the males of Macroxyela are orthandrous, I
observed that pairs of Macroxyela always copulated in the
manner of strophandrous sawflies, i.e. end-to-end with both
sexes standing on the substrate.
Preparations of pairs of Aglaostigma lichtwardti killed during copulation are pictured in Fig. 5. The harpes are pressed
against the lateral sides of the seventh sternum of the female
(Fig. 5A). The exerted pressure can be strong enough to dent
the female’s sternum. The volsellae hold the seventh sternum
of the female between cuspis and digitus (Fig. 5B). The
penisvalvae are inserted into the female genital opening
(Fig. 5B,C).The parapenes lie dorsally of the female’s
seventh sternum, i.e. the sternum is ‘squeezed’ between the
parapenes and the rest of the gonostipes (Fig. 5C,D).
The assumption that the gonomaculae (which are not
present in Tenthredinoidea s. l., Cephidae, Orussidae and
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Apocrita) can act as suction cups could be shown to be
correct in the present study. When a male and a female of
Macroxyela ferruginea were put together in a vial, the male
usually stretched his copulatory apparatus out of the genital
chamber. During this stage, the gonomaculae of several males
became attached to the glass of the vial through adhesion.
The males were then unable to pull away although they
braced themselves against the glass, exerting all possible
force. This could last for 1 or 2 minutes, during which a
pulsating action of the gonomaculae was observed through
the glass of the vial under the stereomicroscope. In some
cases, the male could be freed only by pulling it with a pair
of tweezers from the vial.
Morphology and function of the muscles of the external
male genitalia
Boulangé (1924) studied 46 species of ‘Symphyta’ and found
25 pairs of muscles, which he named with lower case letters
from a to v, plus x, z and si. When Snodgrass (1941) cited
Boulangé’s work, he changed the letters to numbers. Figure 6
compares the two nomenclatures and gives the insertion sites
of all muscles presently known in lower Hymenoptera. Not
all muscles are present in every species; Tenthredo campestris,
for example, has 18, Macroxyela ferruginea 21.
The genital organ is connected to the hypopygidium
(ninth sternum) by three pairs of muscles (Fig. 7A). Muscle
a runs from the spiculum to the gonocondyle. Muscle b
begins at the spiculum and ends at the ventral side of the cupula. Muscle c inserts on the gonocondyle and laterally on the
ninth sternum. These three muscles work to move the genital
capsule as a whole: muscle c pulls it distally, a and b act
antagonistically. The action of muscle c can probably be
enhanced through the application of haemolymphic pressure
at the end of the abdomen (Kluge 1895; p. 189). The muscles
b and c are presumably able to turn the genital capsule sideways as well. In strophandrous species, these three muscles
are twisted and crossed due to the inversion of the copulatory
organ (Fig. 7A); the muscles b both pass the gonocondyle on
the same side (cf. E. L. Smith 1972).
Cupula and gonostipes are connected through up to four
pairs of muscles. In the presumed plesiomorphic condition
(e.g. in Macroxyela ferruginea, Fig. 7C,D), all four pairs are
present: d and e on the ventral side, f and g on the dorsal side.
Muscles d and f begin medially at the cupula and end laterally at the gonostipites. Both pairs of muscles pull the gonostipites laterally, away from each other, so that they open up
to be able to fit around the abdomen of the female. Muscles
e and g insert laterally on the cupula and medially on the gonostipites. They act in antagonism to muscles d and f to pull
the gonostipites towards each other, especially to grasp the
female during copulation. In all examined Tenthredinoidea
s. str. except for Nematus abbotii, only two pairs of muscles
are present (Fig. 7B), and in species with a partly or totally
reduced cupula there might be just one or none at all. In Ten-
© 2001 The Royal Swedish Academy of Sciences
Schulmeister • Male genitalia and copulation in Hymenoptera
thredo campestris, muscle f is derived in that it inserts laterally
on the cupula.
Each penisvalva is moved (mainly) by five pairs of muscles
which run to the gonostipes, four of which move the penisvalva in the medio-sagittal plane (Fig. 7F). Muscles h and i
connect the penisvalva to the ventral apex gonostipitis,
whereas muscles j and k insert on the dorsal parapenis; j on
the main part of the inner face of the parapenis, k on its
median edge. At the penisvalva, muscles h and j insert on the
apex of the valvura and i on the ergot (or the equivalent
place). k is a more or less fan-shaped muscle which extends
from the parapenis to the median side of the penisvalva
(Figs 7F, 9A). The contraction of any one of these four
muscles can have different consequences, depending on the
state or action of the others. Of course, another important
factor for the movements of the penisvalvae are the spatial
relations of the insertion sites, which can differ considerably
between taxa. Figure 9 shows the male external genitalia of
Aglaostigma lichtwardti in the normal position (Fig. 9A)
and in copula with revolved penisvalva (Fig. 9B).
Muscle l (Fig. 7G) begins at the ergot (or the equivalent
point on the penisvalva) and ends (dorso)laterally at the gonostipes. In species with a demarcated parapenis, the insertion
site lies laterally of the parapenisjugum. The muscles l thus
pull the penisvalvae laterally, i.e. away from each other, probably after insertion of the penisvalvae into the genital opening
of the female. Since the lateral movement of the penisvalvae
is apparently more restricted proximally than distally, the
contraction of the muscles l probably spreads them apart distally. This action presumably opens the phallotrema to make
way for the sperm and anchors the male copulatory apparatus in the female.
Muscle m – not found in Tenthredinoidea s. str. – extends
from the apex of the valvura to the digiceps. Muscle n runs
from the apex of the valvura to the digiura (Fig. 7E). The
insertion sites of the muscles m and n are thus very close to
each other. However, m and n differ by the course they take
from one insertion site to the other: m lies laterally of the
penisvalva and of muscle i (and s, if present), whereas n runs
medially of the penisvalva over most of its length, before
crossing the penisvalva to reach the digiura. In its middle,
muscle n is often attached to the endophallic membrane,
close to the primary gonopore and can then appear bipartite.
Due to this connection muscle n possibly serves to open or
close the primary gonopore. Apart from this, the function of
muscles m and n is difficult to deduce since both of their
ends insert on movable elements.
Two muscles connect the volsella, or rather the parossiculus, to the gonostipes: o and p (Figs 8A–D, 9C). Muscle o
inserts on the lateral basal portion of the basivolsella and distally on the gonostipes (near the harpe). Muscle p runs from
the distivolsella to the basal section of the gonostipes. I found
that three muscles instead of two connect parossiculus and
gonostipes in the species Aglaostigma lichtwardti, Nematus
abbotii and Runaria reducta. Two of these three muscles seem
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Male genitalia and copulation in Hymenoptera • Schulmeister
Fig. 6 — Genital musculature of male lower Hymenoptera with
special reference to Tenthredo campestris (T. c.) and Aglaostigma
lichtwardti (A. l.). The first and second columns list the names of the
muscles introduced by Boulangé (1924) and Snodgrass (1941). The
third column shows the changes made in the present paper; if the cell

Acta Zoologica (Stockholm) 82: 331– 349 (October 2001)
in the third column is left empty, the names of Boulangé have been
used. The insertion sites given for muscles d–g correspond to the
plesiomorphic condition. In the sixth and seventh column is
indicated which muscles are present (+) or lacking (–) in the species
mentioned above.
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Fig. 7—Muscles of the male external genitalia of lower Hymenoptera
(part 1), shown for Tenthredo campestris and Macroxyela ferruginea.
(C, D) —A. Dorsal side of ninth sternum, ventral side of external
genitalia, and muscles a, b and c. —B. Inner face of cupula with
muscles e and f. —C. Ventral side of external genitalia with muscles
© 2001 The Royal Swedish Academy of Sciences
Schulmeister • Male genitalia and copulation in Hymenoptera
d and e. —D. Dorsal side of external genitalia with muscles f and g.
—E. One half of external reproductive organs, showing muscle n in
the medio-sagittal plane. —F. Same, with muscle n removed,
showing muscles h, i, j, k and si. —G. Gonostipes (without
parapenis), harpe, and penisvalva with muscles l and i.
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Acta Zoologica (Stockholm) 82: 331– 349 (October 2001)
Fig. 8—Muscles of the external male genitalia of lower Hymenoptera
(part 2), shown for Tenthredo campestris and Aglaostigma lichtwardti
(D). A–D show the volsella with muscles o, p and qr: — A, D, seen
from the outside of the genitalia, —B, C. viewed from the inside.
—E. Dissected male genitalia (ventral view) showing muscles i, n
and si. Some parts have been removed, including the distal part of
n on the left part of the figure. —F. Harpe and distal part of
gonostipes with muscles t′, t′′ and u.
to have evolved through splitting of o; therefore I termed
them o′′ and o′′′. Muscle o′′ lies in the same position as o,
whereas o′′′ inserts more distally on the basivolsella.
However, at present I cannot say with absolute certainty
that o′′ and o′′′ have evolved through the splitting of o. Moreover, even if this was the case, it is possible that some species
which have only one muscle connecting basivolsella and gonostipes (e.g. Tenthredo campestris), evolved from an ancestor
having both o′′ and o′′′, so that this single muscle would
correspond to muscle o′′ and not o. Many more species
would have to be studied in order to elucidate the evolution
of the muscles of the ‘o-complex.’
The muscle o′′′ has not been described in ‘Symphyta’ until now,
but Snodgrass (1941) described a muscle (termed 20), which,
according to his description, seems to have the same insertion sites as muscle o′′′. Snodgrass (1941) found this muscle
only in Vespoidea. At present, it is not possible to make a
statement as to whether muscle 20 is homologous to muscle o′′′.

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Fig. 9 —External male genitalia of Aglaostigma lichtwardti in normal
position (A) and from a specimen killed during copulation
(B, C). See text for explanation. —A, B. one half of genitalia,
looking onto the medio-sagittal plane. —C. Ventral view.
In species in which the parossiculus is fused with the
gonostipes (e.g. Cephalcia sp., Cephus pygmeus and Xeris
spectrum), none of the o muscles is present.
Muscles o, o′′, o′′′ and p move the volsella as a whole. Muscle
p can also aid muscle qr to bend the distivolsella (see below),
provided that the parossiculus is secured in its position –
either by contraction of muscle o/o′′ or by being immovably
fused with the gonostipes. That muscle p should have this
second purpose is suggested by the fact that p – in contrast
to o – is still present in Cephalcia (Pamphiliidae), in which the
volsella is secondarily immovably fused with the gonostipes.
Muscles q and r both begin at the distivolsellar apodeme
and end at the basal section of the basivolsella: q laterally, r
medially of the carina volsellaris (Fig. 8A,C,D). Muscles
© 2001 The Royal Swedish Academy of Sciences
Schulmeister • Male genitalia and copulation in Hymenoptera
q and r lie side by side and mostly appear as one muscle, so
I cannot say that they should be considered as two muscles,
just because the insertion site happens to be on both sides of
the carina volsellaris in certain species. Snodgrass (1941)
regarded q and r as one muscle, which he termed 18. I follow
him in that I treat q and r as one muscle, qr. Muscle qr pulls
the distivolsellar apodeme towards the basivolsella.
Muscle s extends from the medial basal part of the
basivolsella to the digiura. Its function is probably to pull the
digiura basad to open the volsella. Muscle si starts next to s
at the basivolsella and ends at the ergot or the equivalent spot
of the penisvalva (Fig. 8E). The muscle si got its name
because Boulangé (1924) found that its position is intermediate between the muscles s and i. Both s and si are present
in Cephalcia sp. In Macroxyela ferruginea and Xeris spectrum,
I found only muscle si. Boulangé (1924) claimed that both
muscles are present in the Tenthredininae, but the Tenthredininae examined in this study had only one muscle. Macrophya annulata and Aglaostigma lichtwardti lack muscle s, and
in Tenthredo campestris there is one muscle which runs from
the basivolsella to a membrane between the digiura and the
penisvalva (Fig. 8E) and is therefore intermediate between s
and si. At present, I cannot say whether this muscle is homologous to both s and si or only to one of these.
In those ‘Symphyta’ in which a harpe is present, Boulangé
(1924) found two muscles which connect the harpe to the
gonostipes: t and u (Fig. 8F). My own studies show that t has
the tendency to separate into two parts, t′′ and t′′′; but there
seems to be some variation in the degree of separation of these
parts even within one species. Muscle t′′′ inserts laterally on
the gonostipes and on the edge of the medial face of the harpe.
Muscle t′′ runs parallel to t′′′, a bit more distally. Both muscles
probably bend the harpe inwards. The fan-shaped muscle u
begins at the distal edge of the gonostipes and ends with its
fanned side in the harpe – sometimes on its medial face, sometimes on the lateral. Muscle u probably works as an antagonist
to t′′ and t′′′. The present study showed that in some nontenthredinoid species (e.g. Macroxyela ferruginea, Megalodontes
cephalotes and Cephalcia sp.) u is divided into two separate,
fan-shaped muscles running parallel to each other.
A gonomacula, if present, is worked by muscle vs. When
the gonomacula is pressed against a surface and muscle v contracts at the same time, the gonomacula acts as a suction cup.
According to Boulangé (1924), there is an exceptional
muscle in Abia lonicerae L., named x, which connects the two
valvurae near their apices.
In Cephus pygmeus, muscles z extend between the unpaired
median rod and the two valvurae.
Discussion
Copulatory behaviour
Enslin (1912) and Boulangé (1924) noted that the tenthredinoid male walks backwards towards the rear end of the
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Male genitalia and copulation in Hymenoptera • Schulmeister
female, slips the tip of his abdomen under hers and places his
harpes on the sides of her seventh sternum. Gordh (1975)
observed several copulations from laboratory-reared virgin
specimens of Hemitaxonus dubitatus (Norton). He describes
that in this species, the male first climbs on the female,
vibrates his wings for a few seconds and then moves off the
female, his body now at a right angle relative to that of the
female and his hind legs on her thorax. He probes the mesosternum with his genitalia and moves towards the end of her
abdomen, his hindlegs remaining on top of the female. He
then positions himself so that their heads face in opposite
directions. While inserting his aedoeagus, his hindlegs are on
her abdomen and wings. Gordh notes that the coitus lasted
70 s on average. After about 30 s of copulation, during which
the pairs remained motionless, several females started to
move, dragging the males backwards. Some females tried to
dislodge the males by pressing their hindlegs against the male
genitalia.
Function of the male genitalia
Enslin (1912) and Boulangé (1924) assumed that the
aedoeagus is introduced into the female genital opening at
the base of the saw. This and the assumption that the volsellae
grasp the edge of the female sternum (Boulangé 1924) is
shown to be correct in the present study. The observed deformation of the female sternum shows that the harpes, too,
serve a grasping function, contrary to the belief of Boulangé
(1924; p. 100), who thought they would only be used to feel
for and maybe excite the female.
Boulangé (1924) assumed that the gonomacula can act as
a suction cup, but was unable to prove this. He rejected
Crampton’s (1919) theory that the gonomacula was a ‘sensory area’, because he found that the nerve leading into the
harpe does not reach the gonomacula. Here it is demonstrated (in Macroxyela) that the gonomacula can indeed be
used as a suction cup. The fact that a pulsating action of the
gonomaculae was observed is an indication that the attachment is indeed achieved through suction and not through
a sticky substance secreted by glands. Boulangé (1924)
depicted thin sections of the gonomacula of Sirex juvencus
(Linnaeus 1758) which do not show any glands.
D’Rozario (1940) observed in several pairs of Nematus
ribesii (Scopoli 1763) fixed in copula that ‘the penis’ (meaning aedoeagus) ‘is inserted deep into the vagina and its valves
open wide apart while its tip lies well under the spermathecal
opening into the vagina.… The sperm (s) are ejaculated in a
mass into the vagina (v) along with the secretion (agf ) from
the male accessory gland (…)’.
E. L. Smith (1970a) wrote: ‘The male grasps the female
from above or behind, depending on whether the genital capsule is rotated. The female genital orifice between the gonapophyses is exposed either voluntarily or through pressure by
the male on her gonocoxites, and the volsellae appear to
clutch or hook the labia. The gonapophyses (and penis, if
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Acta Zoologica (Stockholm) 82: 331– 349 (October 2001)
present) are then thrust into the vagina. Sperm is injected
probably both by peristalic motion in the gonapophyses (the
pectines and setae would sweep the material distally) and
pressure from the fluid of the accessory glands. The gonapophyses of Tenthredinoidea thrust alternately, and sperm
must be transferred mostly by this motion since phallic structures are absent.’ But since he neither gives an account of
how he derived at this description nor cites any evidence,
it seems that parts of it are assumptions drawn from the
morphology.
Possible movements of the volsella
Muscle qr pulls the distivolsella towards the basivolsella. If
the basivolsella were a simple sclerotic plate, the parossiculus
would assume the shape of a semi-circle (in lateral view). But
because it is strengthened through the carina volsellaris, the
basivolsella retains its shape, and the distivolsella is bent
against the basivolsella, forming an angle of approximately
70° between them (Fig. 9C). The gonossiculus follows this
movement, since it is immovably fused along its middle part
with the distivolsella. Figure 9C shows the copulatory
apparatus of a male of A. lichtwardti taken in copula. The
volsella on the right side of the drawing is in the relaxed
position, in which the volsella is slightly open, whereas the
volsella on the left shows the closed condition in which the
distivolsella is pulled towards the basivolsella. (Note that it
can only be seen from a different angle whether the volsellae
are open or closed.) When the right, relaxed distivolsella or
muscle p (of the distivolsella) was pulled basally with a pincer, the digiceps moved towards the distivolsella so that the
volsella closed, even though the digitus had not been moved
directly. I do not yet understand the mechanism by which
this movement is achieved.
When the digiura of the relaxed volsella was pulled basally
– simulating the action of muscles s and si – the digiceps
moved further away from the distivolsella, so that the volsella
opened more than in the relaxed position.
Description of presumed muscular actions during the copulation in
strophandrous Tenthredinidae
When the male walks backwards towards the female, he
pushes his copulatory organ out of the genital chamber probably by haemolymphic pressure and the help of muscles c.
He opens the latimeres by contracting muscles d and f,
reaches around the ventral side of the female abdomen, and
– after finding her genital opening – contracts e and g to pull
the latimeres together and t′′ and t′′′ to bend the harpes. At the
same time or shortly after, the male moves the penisvalvae by
muscles h, i, j and k into the female genital orifice. He opens
the volsellae by contraction of s, possibly moves them around
using o and p, and – upon sensing (presumably with the
parossicular bristles) that he found the right place – closes
them around the seventh sternum by contracting muscles
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Acta Zoologica (Stockholm) 82: 331– 349 (October 2001)
p and qr. He might then contract muscles n to open the
primary gonopore and pull apart the penisvalvae in the female
by contracting the muscles l. These actions could serve to
open the secondary gonopore (phallotrema) and to make
way for the sperm. The male might push the sperm out by
alternately moving the penisvalvae by muscles h, i, j and k.
At the end of the copulation, the gonostipites and harpes
are opened through relaxing the muscles t′′, t′′′, e and g, and
contraction of muscles u, d and f. The volsellae are opened
to release the female seventh sternum by relaxing o, p and qr
and contraction of s. The copulatory organ is pulled back
into the genital chamber by relaxation of c and the haemolymphic pressure and contraction of muscles a and b.
Ways of holding the female in a strophandrous species
During copulation of strophandrous as well as orthandrous
species, the female often moves around (own observations in
T. temula, E. koehleri and C. pygmeus). In a species in which
the male is on top of the female during copulation this is not
much of a problem, contrary to strophandrous or facultatively strophandrous species, in which the moving female
drags the male behind her. In these species, a strong attachment of the male to the female is therefore often essential for
copulatory success.
In Aglaostigma lichtwardti, a number of different measures
ensure this attachment no matter in which direction the
female moves. (1) Pressing the harpes against the sides of the
female abdomen provides hold if the female moves sideways. (2) Grasping the edge of the seventh sternum with the
volsellae ensures attachment during forward movement of
the female. (3) insertion of the parapenes above the seventh
sternum prevents the female from pulling her abdomen
upwards. (4) placing his hindlegs on her wings prevents her
from pulling her abdomen upwards and from opening her
wings to fly away (which is probably supported through the
plantulae of the hind tarsi). (5) The male’s position behind
and under the female prevents backwards and downwards
movement. All in all, the male’s attachment is ensured
against movements in any possible direction.
Possible evolutionary advantage of strophandry
In species copulating end-to-end, the holding of the female
has to be accomplished through additional measures. This
leads us to question what the evolutionary advantage of
this copulation posture could be. In orthandrous and
strophandrous copulation, the orientation of the male
genitalia in relation to the female genitalia is the same; the
anatomically ventral side (which carries the volsellae) always
faces upside during copulation. The orientation of the genitalia can therefore not have played a role in the evolution of
strophandry; the advantage must lie in the position of the
male. My own observations of the orthandrous species
Cephus pygmeus showed that the male has to twist his abdo-
© 2001 The Royal Swedish Academy of Sciences
Schulmeister • Male genitalia and copulation in Hymenoptera
men and genitalia in a complicated manner to reach the
female genital opening. Drawings, photographs and descriptions of the copulation in three species of Xiphydria show that
the male clings to the very tip of the female abdomen, with
his abdomen upside down under hers, not giving the impression of a secure hold on the female (Rohwer 1915; Chrystal
and Skinner 1932; Jänicke 1981). It can be assumed that the
finding of the female genital opening could be rather difficult
when the male has to grope around with a twisted abdomen,
which could mean losing energy and time, the latter enhancing the probability of becoming a victim of predators during
the copulation. E. L. Smith (1970b) mentions that some
Tenthredinoidea are carnivorous and indicates that strophandry would prevent the male from being attacked by the
female, but since the ancestral species which evolved
strophandry was probably not carnivorous, this cannot have
played a role in the evolution of strophandry.
Orthandry, strophandry and facultative strophandry
As mentioned above, the Xyelinae and Tenthredinoidea s. str.
are strophandrous, all other Hymenopterans orthandrous.
In the present study, it was found that the orthandrous
species Macroxyela ferruginea copulates in the manner of
strophandrous sawflies, i.e. end-to-end. I will call this
facultative strophandry. Similar observations had already
been made by Eidt (1965) in the orthandrous Cephalcia
fascipennis (Cresson) (Pamphiliidae): ‘Without courtship, he
mounts, then turns, all very quickly, so that the pair in copula
face in opposite directions in the manner of the strophandrious sawflies. This explains the specimen of A[cantholyda]
burkei with the genitalia rotated 180° found by Middlekauff
(1958) who adds that it was taken in copula. However,
mated males of C. fascipennis and other species, when mating
terminated naturally, had their genitalia returned to the
upright position of orthandrious sawflies.’ and by Borden et al.
(1978) in Cephalcia lariciphila ( Wachtl 1898) or C. alpina
(Klug 1808): ‘... the female turned head-to-head with the
male, then both turned or moved past each other and
coupled tail-to-tail.’
This means that at least one macroxyelid and three
pamphiliid species exhibit facultative strophandry, whereas
members of the orthandrous groups Cephidae (own observation in Cephus pygmeus), Xiphydriidae (Rohwer 1915;
Jänicke 1981), and Siricidae ( Jänicke 1978) were observed
copulating with the male clinging to the abdomen of the
female. For the other orthandrous groups, namely the
Blasticotomidae, Megalodontesidae, Anaxyelidae, and
Orussidae, the copulation posture is not known.
The fact that the male of C. fascipennis first mounts the
female and then turns around is an indication that the male
might not be able to revolve his genitalia by himself. He probably attaches his genitalia firmly to the female (by using the
gonomaculae) so that they become rotated automatically
while he turns around. Unfortunately, I cannot remember
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Male genitalia and copulation in Hymenoptera • Schulmeister
whether the males of Macroxyela mounted the female first
before assuming the end-to-end posture, but I doubt that this
was the case. The observation of Borden et al. (1978) indicate that in some species the males might be able to actively
turn their genitalia around.
Even though Siricidae are orthandrous and Sirex juvencus
(Linnaeus 1758) has been observed to copulate in the corresponding manner (Jänicke 1978), Rasnitsyn (1969) notes
that a live Xeris spectrum male was capable of actively turning
its genitalia 180° and back.
We could now ask the question of how strophandry and
facultative strophandry evolved. Unfortunately, if we code
three different character states (O, FS, and OS), code the
orthandrous taxa of which the copulation posture is
unknown as ‘O or FS’, and optimize this character on the
cladogram of lower Hymenoptera in Vilhelmsen (2001),
this does not result in a single most-parsimonious scheme. If
the Blasticotomidae were truely orthandrous, it would be
more parsimonious to assume orthandry at the base of the
hymenopteran tree; if they were facultatively strophandrous,
we would have to assume this state in the groundplan of the
Hymenoptera (both under the assumption that the outgroups are orthandrous). To determine whether the ancestor
of the Hymenoptera was orthandrous or facultatively
strophandrous, it would also be important to know what
copulation posture must be assumed at the base of the
Mecopterida and the Coleoptera + Neuropterida.
Acknowledgements
I want to thank Rainer Willmann for suggesting the topic
and supporting my work. I thank Malte Jänicke, Stefan
Schmidt, David R. Smith and Lars Vilhelmsen for providing
me with valuable specimens. David R. Smith kindly helped to
find and catch Macroxyela ferruginea. I am indebted to Lars
Vilhelmsen, Volker Mauss, Rainer Willmann, Jim Carpenter,
and Ward Wheeler for reviewing the manuscript and making
helpful suggestions. I especially thank Oliver Niehuis for his
indispensable help and support.
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