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Annales de la Société entomologique de France (N.S.)
International Journal of Entomology
ISSN: 0037-9271 (Print) 2168-6351 (Online) Journal homepage: http://www.tandfonline.com/loi/tase20
An investigation of the roof of the genital chamber
in female plant-bugs with special emphasis on the
“dorsal sac” (Hemiptera: Heteroptera: Miridae)
Dominique Pluot-Sigwalt & Armand Matocq
To cite this article: Dominique Pluot-Sigwalt & Armand Matocq (2017): An investigation of the roof
of the genital chamber in female plant-bugs with special emphasis on the “dorsal sac” (Hemiptera:
Heteroptera: Miridae), Annales de la Société entomologique de France (N.S.)
To link to this article: http://dx.doi.org/10.1080/00379271.2017.1285723
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An investigation of the roof of the genital chamber in female plant-bugs with special emphasis on
the “dorsal sac”(Hemiptera: Heteroptera: Miridae)
Dominique Pluot-Sigwalt*& Armand Matocq
Institut de Systématique, Évolution, Biodiversité (ISyEB), Muséum national d’Histoire naturelle, UMR 7205 CNRS MNHN UPMC
EPHE, C. P. 50, 57 rue Cuvier, Paris cedex 05 F –75231, France
(Accepté le 19 Janvier 2017)
Summary. In Miridae, the roof (dorsal wall) of the female genital chamber (bursa copulatrix) is often neglected in
taxonomic studies, rarely represented in its entirety and its importance is usually underestimated. It contains several organs
that are relevant for taxonomy and phylogeny, namely the ringed glands (parieto-vaginal glands) encircled by the widely
used sclerotized rings, the spermathecal gland (vermiform gland), and the lateral oviducts; it may also display various
“dorsal sacs”or pouches and other poorly known structures. The comparison of 24 species belonging to seven mirid
subfamilies, and various additional literature data, suggest that the general architecture of the roof and the topographic
relations of its different organs may be used to ascertain relationships of higher taxa. Information is mainly provided on the
“dorsal sac”, i.e. a very variable pouch-like structure usually medially located in the vicinity of the lateral oviducts and the
spermathecal gland. The dorsal sac is derived from the roof of the genital chamber, i.e. is a differentiation of the vaginal
wall, and cannot be derived from the common oviduct as claimed by several authors. Apparently, the common oviduct does
not exist in Miridae. A dorsal sac, variously shaped, occurs within most subfamilies examined (Cylapinae, Orthotylinae,
Phylinae, Bryocorinae, Deraeocorinae, Mirinae). Some representatives of the tribe Mirini and Stenodemini (Mirinae) exhibit
two types of dorsal sac. The subfamily Isometopinae as well as some species in each of the other subfamilies examined
seem to be devoid of dorsal sac. Apparently, dorsal sacs are adaptive pouches which receive and lodge some parts of the
phallus during copulation. At species level, the dorsal sac is informative in providing diagnostic characters. At supraspecific
levels (genus, tribe, subfamily) the dorsal sac must be examined jointly with other equally informative structures of the roof:
architecture of the sclerotized rings; location of the spermathecal gland; location, length and aspect of the lateral oviducts;
aspect and size of the infoldings of the lateral margins of the genital chamber (mainly in Phylinae and Orthotylinae); shape
of the genital chamber in dorsal view; and the presence, aspect and size of the paired lateral apodemes of the genital
chamber.
Résumé. Investigations sur le plafond de la chambre génitale femelle des Miridae, avec une attention particulière
pour le « sac dorsal » (Hemiptera : Heteroptera). Chez les Miridae, le plafond (paroi dorsale) de la chambre génitale
(bourse copulatrice) de la femelle est encore peu souvent examiné en taxonomie, rarement représenté dans son ensemble, et
son importance est généralement sous-estimée. Il reçoit pourtant plusieurs organes utiles en taxonomie et phylogénie, à
savoir : les « ringed glands » (glandes pariéto-vaginales) entourées par un anneau sclérifié, la glande spermathécale (glande
vermiforme), les oviductes latéraux ; il peut aussi former une poche dite « sac dorsal » et d’autres structures peu connues.
La comparaison de 24 espèces représentant sept sous-familles de Miridae, ainsi que diverses données de la littérature
suggèrent que l’architecture générale du plafond et les relation topographiques des différents organes peuvent être utilisées
pour établir des relations de parenté entre taxons au rang de sous-famille ou de tribu. Des informations sont données sur le
« sac dorsal », poche membraneuse très variable souvent située à proximité des oviductes latéraux et de la glande
spermathécale. Le sac dorsal qui est une différenciation de la paroi du plafond est d’origine vaginale et ne peut être
formé par l’oviducte commun ainsi que le prétendent plusieurs auteurs. Apparemment, l’oviducte commun n’existe pas
chez les Miridae. Un sac dorsal de formes très diverses existe dans la plupart des sous-familles examinées (Cylapinae,
Orthotylinae, Phylinae, Bryocorinae, Deraeocorinae, Mirinae). Quelques représentants des tribus Mirini et Stenodemini
(Mirinae) possèdent deux types de sac dorsal. Les Isometopinae, ainsi que diverses espèces dans chaque sous-famille
examinée, sont dépourvus de sac dorsal. Selon toute apparence, le sac dorsal est une structure adaptative recevant tout ou
partie du phallus pendant l’accouplement. Au niveau espèce, le sac dorsal fournit des caractères diagnostiques. Au niveau
supra-spécifique (genre, tribu, sous-famille) le sac dorsal doit être examiné avec les autres structures du plafond tout aussi
informatives : architecture des anneaux sclérifiés, emplacement de la glande spermathécale, longueur et aspect des oviductes
latéraux, aspect et dimensions du repli des marges latérales de la chambre génitale (chez les Phylinae et Orthotylinae),
forme de la chambre génitale en vue dorsale, présence, aspect et dimensions des apodèmes musculaires latéraux de la
chambre génitale.
Keywords: Miridae; female genitalia; genital chamber; dorsal sac; diagnostic characters; compared anatomy
*Corresponding author. Email: dps@mnhn.fr
Annales de la Société entomologique de France (N.S.), 2017
http://dx.doi.org/10.1080/00379271.2017.1285723
© 2017 Société entomologique de France
Three major authors, Kullenberg (1947), Slater (1950)and
Davis (1955), have thoroughly described the female geni-
tal tract in Miridae; morphology, anatomy, histological
structure and functional aspects of the genital system
have thus been documented in numerous species.
Although more frequently examined and used for
mirid taxonomic studies for several decades, the internal
female genitalia remain much less studied than the male
genitalia. They provide valuable characters first demon-
strated by Slater (1950). Since this pioneer work –a
widely comparative study on the mirid female genitalia –
attention has mainly focused on several sclerotizations
which are observed on the cuticular intima of the genital
chamber (bursa copulatrix, gynatrium): i.e. the sclerotized
rings and associated structures and the posterior wall with
inter-ramal sclerites and lobes. Various sclerotized struc-
tures associated with the vulvar area and the vestibulum
were also more recently considered in Phylinae and
Orthotylinae (see references until 2005 in Pluot-Sigwalt
& Matocq 2006; Schuh 2006; Forero 2008,2009;
Schwartz 2011; Menard & Schuh 2011; among others).
The roof, or dorsal wall, of the mirid genital chamber,
has remained less well documented (except for the asso-
ciated sclerotized rings), very rarely illustrated in its
entirety and often underestimated, in spite of many notable
exceptions (see among others: Schmitz 1968; Ehanno
1990a,1990b,1990c,1991,1993, Stonedahl 1991;
Matocq 1993,1996,2004; Rosenzweig 1997; Ehanno &
Ribes 1994; Chérot 2002; Carpintero & Chérot 2002;
Malipatil & Chérot 2002; Chérot & Malipatil 2003;
Wyniger 2004,2006,2010,2011; Sadowska-Woda et al.
2006; Matocq & Pluot-Sigwalt 2001,2005,2006a,2006b,
2012,2014; Yasunaga & Schwartz 2007; Pagola-Carte &
Ribes 2007;Cassis & Wall 2010; Cassis et al. 2012; Pluot-
Sigwalt & Chérot 2013; Gapon 2014). Recently, it has
been extensively studied within the Bryocorinae by
Namyatova & Cassis (2012,2013,2015,2016) and sev-
eral characters supplied by the roof were used in phylo-
genetic analysis.
The roof of the female genital chamber is a function-
ally important area containing the ringed gland (a gland-
ular epithelium encircled by sclerotized rings), the
spermathecal gland (vermiform gland), the lateral ovi-
ducts, and a structure called the “dorsal sack”(sensu
Kullenberg 1947). The dorsal sac is centrally located on
the roof, usually in the vicinity of the spermathecal gland
and the paired oviducts, these structures being part of the
membranous area adjacent and posterior to the dorsal
labiate plate (sensu Davis, i.e. a partially sclerotized
plate-like region of a dorsal wall bearing the sclerotized
rings).
We have had the opportunity to dissect many species
and carefully examine the dorsal wall of the female genital
chamber. In this paper we focus attention on the dorsal
wall region and particularly on the still poorly known
“dorsal sac”. First, we will show that the dorsal sac cannot
be all or part of the common oviduct as claimed by several
authors, but is a membranous differentiated part of the
vagina. Second, we will examine the possible functions
of the dorsal sac. Third, we will give a survey of the
different types of roof and dorsal sac (or dorsal pouch)
on the basis of our own observations in seven mirid
subfamilies and also from literature. Finally, we will try
to clarify the main features of the roof that are potentially
relevant in taxonomy and phylogeny.
Material and methods
Species examined
Female were examined or re-examined in 24 plant bug species,
mostly Palearctic, belonging to seven subfamilies. We follow the
suprageneric classification of Cassis and Schuh (2012) except for
the subfamily Bryocorinae recently revised and analyzed by
Namyatova and Cassis (2016) and Namyatova et al. (2016)
who gave a new tribal-group classification of the subfamily.
ISOMETOPINAE: Isometopus intrusus (Herrich-Schaeffer,
1835) (France). CYLAPINAE Fulviini: Fulvius oxycarenoides
(Reuter, 1878) (France); Fulvius carayoni (Pluot-Sigwalt &
Chérot, 2013) (Cameroon); Vanniini: Afrovannius sp. (Reunion
Island). ORTHOTYLINAE Orthotylini: Cyllecoris ernsti Matocq
& Pluot-Sigwalt, 2006) (Crete Island); Heterotoma planicornis
(Pallas, 1772) (France); Orthotylus neoriegeri (Matocq & Pluot-
Sigwalt, 2014) (Morocco); Halticini: Euryopiocoris nitidus
(Meyer-Dür, 1843) (France). PHYLINAE Phylini: Amblytylus
albidus (Hahn, 1834) (France); Plagiognathus arbustorum
(Fabricius, 1794) (France); Psallus flavellus Stichel, 1933
(France); Hallodapini: Cremnocephalus alpestris Wagner, 1941
(France). BRYOCORINAE Bryocorini: Bryocoris pteridis
(Fallen, 1807) (France); Monaloniini: Afropeltis bergrothi
(Reuter, 1892) (Guinea). DERAEOCORINAE Deraeocorini:
Alloeotomus pericarti (Matocq, 1998) (Crete); Deraeocoris rub-
ber (Linnaeus, 1758) (France). MIRINAE Mirini: Aphanosoma
italicum A. Costa, 1842 (Greece); Brachycoleus decolor Reuter,
1887 (Greece); Closterotomus izyai Matocq & Pluot-Sigwalt,
2006 (Crete); Hadrodemus m-flavum (Goeze, 1778) (France);
Lygus pratensis (Linnaeus, 1758) (France); Orthops palus
(Taylor, 1947) (Reunion Island); Stenodemini: Notostira sp.
(Bulgaria); Stenodema holsata (Fabricius, 1787) (France).
Methods
Female abdomen was cleared in cold 10% KOH solution for one
day, then rinsed in water, placed in glycerol and dissected. The
genital tract was then stained with chlorazol black, placed in a
depression slide containing glycerol and examined and drawn
using a microscope with camera lucida. For a full view of the
roof of the genital chamber and associated structures, it is neces-
sary to dissociate and remove the gonapophyses 9 (valvulae 2).
In some cases, it is also necessary to remove the strongly pig-
mented posterior wall. Genitalic preparations were stored in
glycerol in a microvial fixed to the pinned specimens.
Illustrations: Only the roof of the genital chamber and its
associated structures are illustrated; fields covered with spinules
or microtrichia are not represented on the drawings, as well as
possible underlying dark structures visible by transparency.
Terminology: We follow Davis (1955); however, instead of
the term “sack”we prefer to use “sac”(from the Latin “saccus”),
2D. Pluot-Sigwalt & A. Matocq
more appropriate in anatomical study. The frequently used term
“dorsal sac”refers apparently to various non-homologous pouch-
like structures. Herein we maintain this probably inappropriate
but convenient designation until more detailed comparative data
are available about these structures.
The “dorsal sac”: a membranous differentiation of the
vaginal wall
First described under this name by Kullenberg (1947:
dorsal sack) then by Davis (1955) in several species of
Miridae, the dorsal sac is usually a centrally located
pouch-like differentiation of the dorsal wall of the female
genital chamber; it is more or less prominent, expansive,
symmetrical or asymmetrical. Kullenberg (1947)
described it also as expandable. In many species, particu-
larly in Mirinae, the spermathecal gland opens into the
dorsal sac (see in particular: Kullenberg 1947; Davis
1955; and hereafter).
Davis (1955) following Kullenberg (1947) interpreted
the dorsal sac as being all or part of the common oviduct
which would be modified in Miridae, not tube-like as in
other heteropteran families and many insects. Several
authors retained this interpretation (Youdeowei 1972;
Stonedahl 1991; Wyniger 2004; Yasunaga & Schwartz
2007) but did not precisely show the common oviduct
on their drawings; following Davis (1955), several authors
used the ambiguous formulation “the combined structure
of common oviduct and roof of genital chamber”.
The present work leads us to interpret the dorsal sac as
a differentiated part of the vagina, and not of the common
oviduct, which Schmitz (1968) and Carayon (1977) made
implicitly in their studies on Bryocorinae, and other
authors as well in other mirid subfamilies (Pendergrast
1957; Rosenzweig 1997; Chérot et al. 2000). Admittedly,
only a study of the morphogenesis of the ectodermal
genital tract would settle the question. However, several
facts strongly support this hypothesis.
In Miridae, the paired lateral oviducts are well indivi-
dualized and distinct on the roof of the genital chamber in
which they open separately or contiguously. The sper-
mathecal gland is always inserted medially (except in
some Bryocorinae: see below).
If the spermathecal gland (in Miridae as in other
cimicomorphan families) is really homologous with the
true functional spermatheca present in other groups –as
claimed by several authors (Kullenberg 1947; Carayon
1954,1961; Davis 1955; Dupuis 1955,1963,1970;
Scudder 1959; Schmitz 1968)–then it should open into
the vagina, not into the common oviduct. In all
Heteroptera where it exists, the true spermatheca arises
from the vagina as it is the rule in other insect orders,
never from the common oviduct (Snodgrass 1933,1935;
Matsuda 1976). The genital chamber in Miridae is, strictly
speaking, the copulatory cavity, and is the part of the
vagina which can be named bursa copulatrix, or gynatrium
sensu Štys (1962).
The usually thick cuticular intima of the dorsal sac is
mainly formed by endocuticule; see the drawings made from
histological sections at this level by Kullenberg (1947)and
Carayon (1984) in several species. This intima presents the
characteristic features of the vaginal intima observed in
many Heteroptera and other insects, not at all those of the
common oviduct, which is consistently ultra-thin, soft and
transparent with internal spicules (pers. obs. in Heteroptera
and Coleoptera). We do not see any sign of its presence in
Miridae. In all probability the common oviduct does not exist
in Miridae, as for instance in Ephemeroptera (Matsuda 1976)
or in some Trichoptera (Hünefeld 2009).
Functional aspects of the mirid dorsal sac
We do not know precisely the function of the mirid dorsal
sac. According to Davis (1955) and Youdeowei (1972),
the epithelium of the dorsal sac is well developed and may
be glandular, but we do not know the nature of the secre-
tion if any. On the other hand, Kullenberg (1947) and
Carayon (1984) did not describe the glandular epithelium
at the level of the dorsal sac. However, around the point of
entry of the lateral oviducts into the roof of the genital
chamber, we have observed, in many species, minute short
ductules inserted in the cuticular intima that could be
efferent ductules of secretory cells (Figures 7,10,22).
In the current state of the limited knowledge, the only
function which can be hypothesized is a role during copu-
lation. During mating, some parts of the phallus and para-
meres penetrate into the genital chamber, and are likely to
lodge and anchor into the cavity of the dorsal sac
(Kullenberg 1947; Kerzhner & Konstantinov 1999;
Konstantinov 2003). In Bryocorinae, the phallic hooks or
spicules of the male even enter inside the lateral oviducts
(Schmitz 1968; Carayon 1977). In various mirid species,
Carayon (1984) described scars and wounds within the
thick vaginal cuticle intima of the dorsal sac, caused by
some sharp part of male genitalia. Moreover, the “vaginal
pouch”anteriorly located in Closterotomus spp. (Mirinae)
and in some allied species of the Calocoris complex
studied by Rosenzweig (1997) obviously houses the apical
part of the phallic spiculum during mating, and functions
to anchor it in place (see Figure 20,Brachycoleus). In the
genus Closterotomus Fieber, only the species having a
phallic spiculum in the male possess a dorsal sac in the
female; the species devoid of phallic spiculum are also
devoid of a dorsal sac (Matocq & Pluot-Sigwalt 2006b).
Comparison of the roof of the genital chamber in seven
mirid subfamilies and various aspects of the dorsal sac
The results obtained in the few mirid representatives
examined are presented below. At the same time, in
Annales de la Société entomologique de France (N.S.) 3
order to strengthen and extend our finding, we have ana-
lyzed and summarized the information found in the litera-
ture. In the literature, the dorsal sac is variously mentioned
(pouch, vaginal pouch, common oviduct, combined struc-
ture of common oviduct and roof of the genital chamber,
dorsal sac, membranous projection of vagina); frequently
it is not mentioned and only illustrated. Only clear
descriptions of the roof of the genital chamber and unam-
biguous illustrations have been retained. Many illustra-
tions difficult to interpret or not complete were not
retained.
ISOMETOPINAE (Figure 1). The roof of the genital cham-
ber has been illustrated in about 10 species and five genera by
Akingbohungbe (1996). From these illustrations and the
examination of Isometopus intrusus (Figure 1), it appears
that the roof is not particularly complex in this subfamily,
except laterally for two conspicuous sclerotized rings remark-
ably thick and elongated. There is no dorsal sac or pouch. The
well-developed lateral oviducts open posteriorly close
together into the genital chamber. The spermathecal gland is
centrally located and enters directly into the chamber.
Note that, when studying Lindbergiola aureopilosa
Carvalho, Scudder (1959) considered that the genital cham-
ber was not as complicated in this species as in other mirids.
He also did not find the spermathecal gland but it is present
as shown by Akingbohungbe (1996)andFigure 1.
CYLAPINAE (Figures 2–4). A conspicuous, well-
defined, and differently shaped dorsal sac was found in
two species of Fulvius (Pluot-Sigwalt & Chérot 2013; this
paper) (Figures 3,4) as well as in other representatives of
the genus (Sadowska-Woda et al. 2006; Chérot et al.
2007). In another Fulviini, Mimofulvius Schmitz, no dorsal
sac was described or illustrated by Schmitz ( 1978), as in
Afrovannius sp., a vanniine species examined here
(Figure 2). The condition of the sclerotized rings varies
within the subfamily. In many species and genera, they are
paired (Gorczyca & Chérot 1998,2002; Chérot &
Gorczyca 1999; Gorczyca 2000; Yasunaga 2000; Cassis
et al. 2003; Cassis & Montheith 2006), whereas in other
they are not paired, crescent-like and anteriorly located
(Yasunaga 2000), or they may be absent (Schmitz 1970;
Sadowska-Woda et al. 2006). The peculiar genus
Palaucoris, recently tentatively placed within the
Cylapinae by Konstantinov (2012) also lacks sclerotized
rings according to this author. The trend towards the loss
of sclerotized rings is mainly observed within the Fulviini
in which several species possess unsclerotized and unpig-
mented almost indistinct small rings. In all cylapines
examined until now, the lateral oviducts are long, often
pleated and twisted and widely separated. The spermathe-
cal gland opens directly into the genital chamber, poster-
iorly (Fulviini) or centrally (Vanniini), between the lateral
oviducts.
ORTHOTYLINAE (Figures 5–8). The roof of the genital
chamber appears quite different in Orthotylini and
Halticini.
Orthotylini (Figures 5–7). The most constant feature
observed on the roof is a discreet medio-longitudinal V-
or U-shaped structure, membranous and usually finely
pleated; the two narrow branches close together poster-
iorly. The lateral oviducts open in the middle of each
branch and are thus widely separated. The spermathecal
gland, centrally located, enters directly into the genital
chamber between the branches of the V-shaped structure,
in a medio-longitudinal groove clearly distinct in many
species (Figures 5,6).
It is not clear to us whether the V-shaped structure is a
pouch-like differentiation of the wall of the genital cham-
ber, or if it is formed by the enlarged base of the lateral
oviducts. In any case, this striking feature is observed and
illustrated by many authors in orthotyline species. See in
particular Kullenberg (1947:Cyllecoris, Dryophilocoris
(as Cyllecoris), Orthotylus, Heterotoma), Davis (1955:
Lopidea), Matocq & Pluot-Sigwalt (2006a:Cyllecoris),
Pagola-Carte & Ribes (2007,2008:Orthotylus), Forero
(2009:Chileria), Pagola-Carte (2010:Brachynotocoris),
Knyshov & Konstantinov (2013a:Platycranus;2013b:
Hyoidea), Matocq & Pluot-Sigwalt (2014:Orthotylus),
Pagola-Carte (2015:Orthotylus).
According to the species examined, the V-shaped
structure (or pouch) may be present either alone
(Figure 5:Cyllecoris) (Matocq & Pluot-Sigwalt 2006a,
2014), or anteriorly associated with a conspicuous dorsal
sac: as a paired subtriangular pouch (Figure 6:Orthotylus)
(Matocq & Pluot-Sigwalt 2014)or a large roundish med-
ian pouch (Figure 7:Heterotoma) (Kullenberg 1947),
Cassis & Wall (2010:Myrmecoroides).
Halticini. There is no median V-shaped structure as in
Orthotylini and no median longitudinal groove. From the
examination of Euryopiocoris nitidus (Figure 8) and the
illustrations given by Schuh & Lattin (1980:
Myrmecophyes), Ehanno (1991,1993:Dimorphocoris)
and Ehanno & Ribes (1994:Dimorphocoris) a median
rounded dorsal sac is present. It receives dorsally the sper-
mathecal gland. The lateral oviducts, short and wide, open
apparently against the posterior part of the dorsal sac.
PHYLINAE (Figures 9–12). Within the subfamily (here
restricted to the tribes Phylini and Hallodapini), the pre-
sence of a dorsal sac is less obvious than in most other
subfamilies.
Phylini. At least two types of membranous differentiation
of the dorsal wall can be observed in the median area of
the genital chamber.
Type 1 (Figures 10, 11). A dorsal sac is present as a trans-
verse membranous pouch, apparently relatively flat, usually
4D. Pluot-Sigwalt & A. Matocq
located posterior to the lateral oviduct, between the sclero-
tized rings and consistently fastened to the internal line of the
rings. It is variously expanded according to the genera exam-
ined, and more or less widely associated with the rings. The
lateral oviducts are short and contiguous; it is not clear
whether they open into the adjoining posterior sac or not.
The spermathecal gland, opens just at the junction of the
lateral oviducts against their anterior margin. Similar features
previously have been illustrated: see Kullenberg (1947:
Psallus, Plagiognathus); Matocq (1989:Psallus; 1991:
Figures 1–4. Female genital chamber in Miridae Isometopinae and Cylapinae, dorsal view. 1,Isometopus intrusus (see also
Akingbohungbe 1996); 2,Afrovannius sp.; 3,Fulvius carayoni (adapted from Pluot-Sigwalt & Chérot 2013); 4,Fulvius oxycarenoides
(see also Sadowska-Woda et al. 2006). Abbreviations: ap = apodeme; ds = dorsal sac; dlp = dorsal labiate plate; f 8 = fibula 8 (ramus 8);
lo = lateral oviduct; sgl = spermathecal gland; sc = internal sclerite at base of the lateral oviduct; sr = sclerotized ring; sd = seminal
depository. Scale bars: 0.2 mm.
Annales de la Société entomologique de France (N.S.) 5
Conostethus;1997and2013:Psallus); Wyniger (2004:
Psallus;2011:Coquillettia, Leutiola); Pagola Carte &
Zabalegui (2007:Psallus); Matocq & Magnien (2008:
Adelphophylus); Duwal et al. (2010:Plagiognathus;2012:
Psallus); Matocq & Pluot-Sigwalt (2011:Psallus);
Vinokurov&Luo(2012:Psallus).
Type 2 (Figure 9). In other several phyline genera, there is
no clear evidence for a pouch. One can distinguish only a
V-shaped membranous fold, just anterior to the adjacent
spermathecal gland and lateral oviducts. This fold is more
or less marked according the species examined. See also
Kullenberg (1947:Harpocera, Chlamydatus); Ribes &
Figures 5–8. Female genital chamber in Miridae Orthotylinae Orthotylini and Halticini, dorsal view; 5,Cyllecoris ernsti (adapted from
Matocq & Pluot-Sigwalt 2006a); 6,Orthotylus neoriegeri (adapted from Matocq & Pluot-Sigwalt 2014); 7,Heterotoma planicornis; the
sclerotized rings hidden under the lateral folds are not distinct; 8,Euryopiocoris nitidus. Abbreviations: ap = apodeme; ds = dorsal sac;
du = ductule; mlg = median longitudinal groove; sd = seminal depository; V-sp = V-shaped pouch. Scale bars: 0.2 mm.
6D. Pluot-Sigwalt & A. Matocq
Ribes (2000:Pachyxyphus); Matocq (1994:Dasycapsus;
2001:Chrysochnoodes;2003:Dasycapsus;2008:
Megalocoleus); Matocq & Pluot-Sigwalt (2001:
Orthonotus; 2005: Lopus; 2012: Amblytylus,
Megalocoleus). As in the type 1, lateral oviducts are
short and contiguous but seem to open directly into the
genital chamber; the spermathecal gland opens between
the lateral oviducts.
Hallodapini (Figure 12). From the examination of
Cremnocephalus alpestris (Figure 12) and the illustrations
given by Wyniger (2006:Hallodapus, Systellonotus,
Omphalonotus, Cremnocephalus, Mimocoris) and Ribes
et al. (2008:Systellonotus), the dorsal sac in Hallodapini
is mainly a transverse semi-circular membranous pouch
between the sclerotized rings and fastened to them as in
Plagiognathus (Figure 10) and other Phylini. Likewise, as
Figures 9–12. Female genital chamber in Miridae Phylinae Phylini and Hallodapini, dorsal view. 9,Amblytylus albidus (adapted from
Matocq & Pluot-Sigwalt 2012); 10,Plagiognathus arbustorum (see also Kullenberg 1947; Duwal et al. 2010); 11,Psallus flavellus
(adapted from Wyniger 2006; Matocq & Pluot-Sigwalt 2011; 12,Cremnocephalus alpestris (see also Wyniger 2006). Abbreviation:
ds = dorsal sac; sd = seminal depository. Scale bars: 0.2 mm.
Annales de la Société entomologique de France (N.S.) 7
in the above phyline type 1, the short and contiguous
lateral oviducts open into the dorsal sac. The spermathecal
gland opens between the lateral oviducts, against their
anterior margin.
BRYOCORINAE (Figures 13, 14). The roof of the geni-
tal chamber appears radically different in Bryocorini and
Monaloniini. However, both tribes exhibit very peculiar
and variable sclerotized rings.
Bryocorini (Figure 13). The roof of the genital chamber
has been described and illustrated by Kullenberg (1947)in
Bryocoris and Monalocoris. Both species examined by
him, one of them B. pteridis (Figure 13) examined here,
show similar features. A dorsal sac (pediculate in the case
of Monalocoris) is posteriorly located; it receives short
and contiguous lateral oviducts and, just posterior to them,
the spermathecal gland. A single, large unsclerotized ring,
more or less trapezoidal, unpigmented and hardly distinct,
is centrally located. Because this single ring is almost
indistinct, several authors considered that sclerotized
rings were probably absent in Bryocorini (Slater 1950;
Carayon 1977).
According to Kullenberg (1947) a large seminal
depository is present, but we did not observe it during
dissection.
Monaloniini (Figure 14). In this tribe (sensu Namyatova
et al. 2016), the roof of the genital chamber has been
thoroughly documented in many representatives (Schmitz
1968:Afropeltis (as Helopeltis); 1987: Sahlbergella;
Carayon 1977:Sahlbergella, Distantiella, Afropeltis (as
Helopeltis); Stonedahl 1991:Helopeltis; Namyatova &
Cassis 2012:Schuhirandella; 2013: Rayeria; 2015:
Volkelius; 2016: Monaloniini). A dorsal sac is usually
well developed, greatly folded and variable. It may be
symmetric or asymmetric, not paired or paired, and more
or less swollen. In the paired dorsal sac condition, each
oviduct enters into one sac (Schmitz 1987; Namyatova &
Cassis 2015). The sclerotized rings are variable and often
exhibit peculiar features and a curious location on the
roof. According to the genera or the species examined,
they may be: paired and well-separated; posteriorly or
anteriorly fused; sometime not paired and encircling the
genital chamber (Schmitz 1968; Carayon 1977; Stonedahl
1991). In their comprehensive studies, Namyatova and
Cassis (2012,2013,2015,2016) distinguished two types
of sclerotization within the tribe: the usual sclerotized
rings (paired or not paired) and “sclerotized bands some-
times with fine striations”(encircling the roof). We suspect
that the “sclerotized bands”could be in fact modified
sclerotized rings but this remains to be demonstrated.
These authors also indicated that several genera are devoid
of sclerotized rings and bands. Within the Monaloniini,
the lateral oviducts are consistently long and pleated; they
exhibit quite clearly the modified apical segment
(Figure 14) described by Carayon (1977) under the name
“infundibulum”, a complex structure having a function
during the migration of the spermatozoa towards the
Figures 13, 14. Female genital chamber in Miridae Bryocorinae Bryocorini and Monaloniini, dorsal view. 13,Bryocoris pteridis (see
also Kullenberg 1947); the seminal depository, not distinct, was not drawn; 14,Afropeltis bergrothi (see also Carayon 1977).
Abbreviations: ds = dorsal sac; inf = infundibulum; sd = seminal depository; sr = sclerotized ring. Scale bars: 0.2 mm.
8D. Pluot-Sigwalt & A. Matocq
ovary. The spermathecal gland is usually inserted medially
in the vicinity of the lateral oviducts, either between them,
or just anteriorly or posteriorly. Only Schmitz (1987:in
Sahlbergella) and Namyatova & Cassis (2015,2016:in
several genera) described the case of a spermathecal gland
shifted to the right or left side.
For the tribes Dicyphini, Eccritotarsini Felisacini,
not examined in this paper, we can only report literature
data. For the Dicyphini, Heiss & Ribes (1998:
Macrolophus) did not indicate the presence of a dorsal
sac, but illustrate long lateral oviducts and paired lateral
sclerotized rings. The figure given by Matocq & Ribes
(2004:Dicyphus) shows roughly similar structures and
illustrates a very large bilobed dorsal sac, each lateral
oviduct entering in the middle of each lobe. For the
Eccritotarsini, Schmitz (1970:Rhodocoris) did not men-
tion a dorsal sac, only paired sclerotized rings; long lateral
oviducts posteriorly located and almost contiguous; the
spermathecal gland opens between them. For the
Felisacini, we have the illustration given by Namyatova
et al. (2016:Felisacus); it seems that a roundish poster-
iorly located dorsal sac is present and receives the sper-
mathecal gland and the lateral oviducts.
DERAEOCORINAE (Figures 15, 16). The genital cham-
ber has been illustrated in three tribes of the subfamily
(Clivinemini, Hyaliodini, Deraeocorini): see Kullenberg
(1947:Bothynotus), Carayon (1960:Stethoconus),
Ehanno (1989:Deraeocoris), Chérot (1998:
Deraeocoris), and Matocq (1998:Alloeotomus). From
these illustrations, the roof seems devoid of sac-like struc-
ture. However, after examination of two species (in
Deraeocoris Kirschbaum and Alloeotomus Fieber), we
regard the membranous median area greatly expanded in
both species as a poorly differentiated and badly delimited
pouch; Chérot (1998) illustrated a similar widely
expanded pouch-like structure in another species of
Deraeocoris. This pouch may be asymmetrical as in
Alloeotomus (Figure 16) in which it is more developed
on the right side (see also Matocq 1998). The long or
short, pleated lateral oviducts are consistently widely sepa-
rated and open laterally into the pouch. The centrally
located spermathecal gland also opens into the pouch.
MIRINAE (Figures 17–22). A well-differentiated and
variable dorsal sac has been illustrated or described in
many Mirini and Stenodemini. In Mirini, see Kullenberg
(1947:Calocoris, Lygocoris (as Plesiocoris), Lygus);
Davis (1955:Taylorilygus (as Lygus)); Schmitz (1976:
Taylorilygus (as Lygus)); Ribes & Ribes (1999:
Phytocoris); Chérot & Pauwels (2000:Peltidopeplus);
Ribes & Heiss (2001:Phytocoris); Malipatil & Chérot
(2002:Adelphocorisella); Carpintero & Chérot (2002:
Volumnus); Chérot et al. (2007:Calocorisca);
Namyatova et al. (2013:Stenotus); and Gapon (2014:
Charagochilus, Dichelocentrum, Polymerus). In
Stenodemini, see Kullenberg (1947:Leptopterna (as
Miris), Myrmecoris, Notostira, Pithanus, Stenodema,
Figures 15, 16. Female genital chamber in Miridae Deraeocorinae Deraeocorini, dorsal view. 15,Deraeocoris rubber;16,Alloeotomus
pericarti (see also Matocq 1998). Abbreviations: ap = apodeme; ds = dorsal sac; sd = seminal depository. Scale bars: 0.2 mm.
Annales de la Société entomologique de France (N.S.) 9
Teratocoris, Trigonotylus), Davis (1955:Leptopterna (as
Miris)), and Schmitz (1976:Trigonotylus). In both tribes,
the dorsal sac is usually a median pouch more or less
expanded, symmetrical or asymmetrical.
The Mirini exhibits large dorsal sacs (Figures 17, 18)and
also the most greatly expanded, convoluted and complex
dorsal sacs within Miridae, as for example those described
by Yasunaga & Schwartz (2007:Philostephanus, Liocapsus,
Orientocapsus). Within these three genera, the dorsal sac may
be thickened by inner sclerotizations (Yasunaga & Schwartz
2007). A well-developed dorsal sac apparently is widespread
within the subfamily and also may be absent in some species
such as Hadrodemus m-flavum, not illustrated here, in which
the roof is flat. According to Gapon (2014), Charagochilus
representatives do not possess a dorsal sac except for C.
consanguineus. In some cases, we suspect also that what
appears at first sight as a pouch-like structure could be in
fact not a true dorsal sac; for instance, the posterior triangular
area illustrated in Orthops palus (Figure 19)seemstooflat and
not truly soft and membranous to be interpreted as a pouch.
Within the mirine Brachycoleus (Figure 20), and the
stenodemine Trigonotylus, a second small, fine and
smooth dorsal sac may be present, anteriorly to the first
one which receives the lateral oviducts (Kullenberg
1947;Schmitz1976). This second sac is located at the
junction dorsal labiate plate/seminal depository; it may
be present alone or not in other mirine species
(Rosenzweig 1997,2001:Closterotomus, Reuterista,
Brachycoleus; Ribes & Ribes 2003:Closterotomus;
Matocq & Pluot-Sigwalt 2006b:Closterotomus).
However, within these genera, several species lack this
particular second dorsal sac.
In both tribes, the lateral oviducts are widely sepa-
rated; they open either into the dorsal sac (Figures 17, 20)
Figures 17–20. Female genital chamber in Mirinae Mirini, dorsal view. 17,Aphanosoma italicum;18,Lygus pratensis (see also
Kullenberg 1947); 19,Orthops palus;20,Brachycoleus bicolor. Abbreviations: ap = apodeme; lo = lateral oviduct; ds = dorsal sac;
sd = seminal depository. Scale bars: 0.2 mm.
10 D. Pluot-Sigwalt & A. Matocq
or directly into the genital chamber (Figure 18); the sper-
mathecal gland consistently opens medially into the sac.
Concluding comments
The present comparative study must be regarded as a pre-
liminary investigation of the different structures located on
the roof of the female genital chamber within Miridae. It is
based on a few representatives of seven mirid subfamilies
and also on data from the literature, some of which were
difficult to interpret. Obviously, the very small number of
species studied only allows general conclusions. This study
was planned to investigate the dorsal sac of the genital
chamber. As work progressed, we also decided to show
that the entire dorsal wall of the genital chamber and its
topography may provide many characters, in addition to
those usually used such as the general shape of the genital
chamber and the shape and location of the sclerotized rings.
It is indeed interesting to consider and to compare the topo-
graphic relations between the main elements of the roof of
the genital chamber: chiefly sclerotized rings, dorsal sac,
openings of the spermathecal duct and of the lateral oviducts.
Here, we focus attention only to several features that are
potentially relevant for species discrimination and for the
phylogenetic reconstruction of higher-level relationships.
Form and topography of the roof
The overall shape of the roof and the arrangement of its
different elements do not change in related species and
might be useful in suprageneric taxa. In the literature,
many authors trace the outline of the roof of the genital
chamber; however, too frequently the roof is incompletely
illustrated, lateral oviducts and spermathecal gland being
often missing on the drawings, as well as other structures
such as membranous pouch or sac. Yet, we think that the
respective relations of the different organs which open into
the genital chamber are important to specify and may
reveal specific characters and distinctive trends at subfam-
ily or tribal level. In this respect, tribe Monaloniini of the
subfamily Bryocorinae has been thoroughly investigated
(Schmitz 1968; Carayon 1977; Stonedahl 1991;
Namyatova & Cassis 2012,2013,2015,2016). Carayon
(1977) considered that the female genital tract (and asso-
ciated structures) presented greater utility for higher-level
relationships than the male genitalia and a more reliable
basis for bryocorine taxonomy and classification.
Sclerotized rings
The sclerotized rings are well known and routinely exam-
ined and used in taxonomic studies since the work of
Slater (1950). However, according to Chérot (pers.
comm.), several structures are still misunderstood or
badly known and remain to be clarified. Here, we will
add only the following remark. As said above about two
subfamilies, a similar trend towards regression and loss of
the rings exists in Cylapinae and Bryocorinae. Within both
subfamilies the sclerotized rings are, in addition, variable
and often strangely modified (not paired or paired,
Figures 21, 22. Female genital chamber in Mirinae Stenodemini, dorsal view. 21,Stenodema holsata;22,Notostira sp. Abbreviations:
ds = dorsal sac; du = ductule; sd = seminal depository. Scale bars: 0.2 mm.
Annales de la Société entomologique de France (N.S.) 11
location, aspect: see above). In this regard, the literature
appears sometimes imprecise and too vague, or even con-
tradictory. These aspects of the sclerotized rings should be
re-examined and clarified.
Dorsal sac
There are at least two main types of dorsal sacs. The
most widespread and centrally located within Miridae, is
frequently, but not constantly, associated with the sper-
mathecal gland and the lateral oviducts. It is observed in
all subfamilies herein examined, except the
Isometopinae. It displays a considerable diversity (size,
shape, aspect, location), may be paired or not paired,
small or conspicuous, pleated or wrinkled, sometimes
poorly differentiated or even absent. A second type of
dorsal sac quite distinct and certainly not homologous
with the principal one is present at the junction of dorsal
labiate plate and seminal depository; to date it is only
observed within Mirini and Stenodemini (see Mirinae
above). Both types of dorsal sacs can be considered as
vaginal pouches functionally correlated with some part of
the phallus during copulation.
We have confidence that the dorsal sac may be highly
informative if it is jointly examined with other structures
of the roof of the genital chamber. In this way, we think
that it may bring phylogenetic information, and ascertain
phylogenetic relationships at suprageneric level (subtribe,
tribe, and subfamily). But above all, the dorsal sac may be
of great value in species recognition and to distinguish
allied congeners. This has been demonstrated for instance
in the cylapine Fulvius (Sadowska-Woda et al. 2006;
Chérot et al. 2007; this paper), in several monaloniine
genera (Schmitz 1968; Carayon 1977; Stonedahl 1991;
Namyatova & Cassis 2012,2013,2015), in several mirine
genera (Yasunaga & Schwartz 2007; Gapon 2014), and we
will demonstrate this in a forthcoming paper about the
phyline genus Psallus (Pluot-Sigwalt & Matocq, in
preparation).
The spermathecal gland
The structure of the spermathecal gland is constant
throughout the Miridae and its general shape shows a
great uniformity. However, the aperture of the sper-
mathecal gland may vary and it is important to docu-
ment whether it goes through a dorsal sac (some
Mirinae), directly into the genital chamber
(Isometopinae, Cylapinae, some Orthotylinae), or adja-
cent to the contiguous lateral oviducts (Phylinae).
Usually it opens medially (Kullenberg 1947;Davis
1955; this paper), except, as observed above, in some
Bryocorinae Monaloniini in which the spermathecal
gland is shifted to the right or left side (Schmitz 1987;
Namyatova & Cassis 2015,2016).
The lateral oviducts
The lateral oviducts are variable in shape, length, orienta-
tion and location but retain constant features within a
group of related species, subtribe, tribe or subfamily. For
instance, they are particularly long, wide and pleated in
Cylapinae and bryocorine Monaloniini, short and widely
separated in Orthotylinae, short and contiguous in
Phylinae, or often widely separated in Mirinae.
The aperture of the seminal depository (seminal sac) into
the genital chamber
The ultra-thin membranous seminal depository opens into
the genital chamber through a slit-like orifice between the
dorsal and ventral labiate plates (Davis 1955). In many
subfamilies (Deraeocorinae, Mirinae, Orthotylinae,
Phylinae), this aperture is wide, as wide as the genital
chamber. In contrast, it is narrow in several Cylapinae
(Figures 3,4) (see also Sadowska-Woda et al. 2006), in
Bryocorinae Monaloniini (Figure 14) (see also Schmitz
1970,1987; Carayon 1977), and in Bryocorinae
Dicyphini (see Matocq & Ribes 2004). According to
Chérot (pers. comm.) and our own observations, the semi-
nal depository exhibits other potentially diagnostic char-
acters. Its size and general shape are variable as well as
various aspects of the paired or not paired glandular area
(s) delimited by a fine cuticular line more or less serrated.
The lateral folds of the genital chamber in Othotylinae
and Phylinae
In both subfamilies, a portion of the lateral margins of the
labiate plates is usually upturned upon the sclerotized
rings (Slater 1950; Schuh 1974). Many times, we have
seen evidence that the shape, length and magnitude of
these subtriangular folds thus formed are informative at
the genus level in Orthotylinae (Figures 5–8) and also in
Phylinae in which the lateral foldings may exist (compare
Figures 10 and 11) or may be missing (Figure 9).
According to Chérot (pers. comm.), lateral infoldings
may also exist within the subfamily Deraeocorinae.
The lateral cuticular apodemes
Paired lateral apodemes (= tendons of Davis 1955), which
provide a cuticular attachment for muscles, can be
observed in dorsal view on each side of the dorsal labiate
plate; two pairs according to Davis in Leptopterna (as
Miris), Taylorilygus (as Lygus) and Plagiognathus.
Meticulous authors (see among others Kullenberg 1947;
Schmitz 1968; Ehanno & Ribes 1994; Chérot 2002;
Pagola-Carte 2010; Gapon 2014) have drawn these apo-
demes in their illustrations. At the beginning of our inves-
tigation we were not aware of their possible importance;
12 D. Pluot-Sigwalt & A. Matocq
as a consequence, these apodemes may have been
neglected on occasion and may be missing in some of
our drawings. Now, we believe that they may be informa-
tive and should be compared in each subfamily and tribes.
Their variation in number, length, arrangement and loca-
tion could be significant. They are absent or indistinct in
several species (in Isometopinae, Cylapinae Fulviini,
Bryocorinae) (Figures 1,3,4,13, 14), some Mirini dis-
tinctly exhibit two pairs (Figures 17, 18, 20), or only one
(Figure 19); the halticine Euryopiocoris large and long
particular apodemes (Figure 8); in Deraeocoris there are
three pairs of apodemes, two pairs being associated to the
posterior margin of the sclerotized rings (Figure 15). In
Phylinae, the apodemes seem consistently short and thin
(Figures 9–12).
Conclusion
In conclusion we stress that it is extremely important
to examine and to illustrate the entire surface of the
roof of the genital chamber. We also emphasize that it
is important to pay attention to the topographic rela-
tions of the different elements of the roof. Based on
our preliminary survey, there is clear evidence that the
dorsal sac has, in several mirid subfamilies, great value
in species recognition and may distinguish, jointly with
the other elements of the roof, allied congeners. We are
also confident that further studies on the roof of the
genital chamber may allow ascertain phylogenetic rela-
tionship of higher level taxa.
Acknowledgments
We are very grateful to Michael D. Schwartz and Thomas Henry
who kindly corrected the English language, to Frédéric Chérot
and Pavel Štys who made useful comments on a first draft of the
manuscript and to an anonymous reviewer.
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