CHARACTERS OF THE EXTERNAL FEMALE GENITALIA WHICH CAN … · Elena Mădălina Morariu are for...

Analele Științifice ale Universității „Alexandru Ioan Cuza” din Iași, s. Biologie animală, Tom LVIII, 2012

CHARACTERS OF THE EXTERNAL FEMALE GENITALIA

WHICH CAN BE USED IN THE SYSTEMATICS OF

PENTATOMINAE (HETEROPTERA: PENTATOMIDAE)

Elena Mădălina MORARIU

Faculty of Biology, Alexandru Ioan Cuza University of Iași, B-dul Carol I, no. 20A, 700505 Iași, Romania;

[email protected]

Abstract. In this paper we analyse the external female genitalia of 10 species (Aelia acuminata (Linné, 1758);

Eysarcoris aeneus (Scopoli, 1763); Stagonomus amoenus (Brullé, 1832); Rubiconia intermedia (Wolff, 1811);

Holcosthetus vernalis (Wolff, 1804); Carpocoris purpureipennis (De Geer, 1773); Dolycoris baccarum (Linné,

1758); Piezodorus lituratus (Fabricius, 1794); Pentatoma rufipes (Linné, 1758); Eurydema ornata (Linné, 1758))

belonging to genera of the subfamily Pentatominae. The external female genitalia of Stagonomus amoenus are

considerably distinctive from the other female genitalia of the subfamily Pentatominae.

Keywords: external female genitalia, laterotergites, gonocoxites, spermatheca, Pentatomidae.

Rezumat. Caractere ale genitaliei externe la femelă, utile în sistematica subfamiliei Pentatominae

(Heteroptera: Pentatomidae). În această lucrare analizăm genitalia externă la femele aparținând la 10 specii din

(Aelia acuminata (Linné, 1758); Eysarcoris aeneus (Scopoli, 1763); Stagonomus amoenus (Brullé, 1832);

Rubiconia intermedia (Wolff, 1811); Holcosthetus vernalis (Wolff, 1804); Carpocoris purpureipennis (De Geer,

1773); Dolycoris baccarum (Linné, 1758); Piezodorus lituratus (Fabricius, 1794); Pentatoma rufipes (Linné,

1758); Eurydema ornata (Linné, 1758)) genuri ale subfamiliei Pentatominae. Genitalia femelă, în cazul speciei

Stagonomus amoenus este evident diferită de ale altor specii ale aceleași subfamilii.

Cuvinte cheie: gentalia externă la femelă, laterotergite, gonocoxite, spermateca, Pentatomidae.

Introduction Pentatomidae is a family of bugs with the body covered in a strong cuticula (Kis,

1984; Schuh & Slater, 1995). The antennae are made up of five joints. They present 2 ocelli

(Kis, 1984; Derjanschi & Péricart, 2005; Rider, 2006). Many of the species feed on plants,

some of them damaging the croplands (Panizzi et al., 2000; Mihalache et al., 1969; Kis,

1984; Schuh & Slater, 1995). As a particular feature of the subfamily Pentatominae,

scutellum is triangular, shorter than the abdomen and it does not cover the hemielytra (Kis,

1984; Derjanschi & Péricart, 2005).

Some of the first authors who started analysing external genitalia on Pentaomoidea

were Crampton (1920, 1922) and Dupuis (1951, 1952, 1953, 1970). They described both

male and female genitalia. External male genitalia are easier to be analysed since

noninvasive methods of research can be used (Dupuis, 1951, 1953; Štys, 1961; Tay, 1969;

Schaefer, 1968; Gapon, 2001). Dupuis described the external female genitalia, particularly at species belonging to genus Eurydema (Dupuis, 1951, 1953, 1970). He analysed the

structures resulted from modifications of the segments eight and nine. McDonald (1966)

started to study the external genitalia of the North American genera of Pentatomoidea in

order to clarify the relationships between them. He made a key using only features of the

external male genitalia. The external female genitalia are used for describe difficult genera

- 31 -

Elena Mădălina Morariu

are for reviews. Derjanschi and Péricart in „Faune de France” use female genitalia only for

difficult genera (Aelia, Sciocoris) (Derzhansky & Péricart, 2005).

The objective of this paper is to examine the female genitalia of Pentatominae and

to establish the characteristics useful for systematics.

Material and Methods

The external female genitalia of 10 species in 10 genera were studied (Tabel 1).

Almost all the species were collected with the entomological net from two Romanian (RO)

counties: Iasi (IS) (Botanical Garden, Ciric area, Bârnova forest) and Vrancea (VN)

(Paltin). They were kept in alcohol 70% until they were mounted on cards. The mounting

was made in such a manner that the taxonomical features were easy to notice. This way, the bugs are better preserved (Millar et al., 2000).

When studying the external female genitalia, we first detached the last segments of

the abdomen (sixth-tenth segments) and then boiled them in NaOH 10% for about 15-20

minutes. Afterwards, we washed them with alcohol, and easily detached the external female

genitalia. We embedded them in Faure solution and drew them with a Reichart drawing

tube.

Morphological terms used in text. The female genitalia of Pentatomidae are the

plate-shaped type, situated on abdominal segments eight and nine. The tenth and eleventh

segments represent the anal segments (Dupuis, 1951, 1955, 1970; Štys, 1961; McDonald,

1966; Schaefer, 1968, 1998; Kis, 1984; Derjanschi & Péricart, 2005). There are two

categories of components of the external genitalia which can be used in taxonomy: the structures resulted from modification of the eighth and ninth segments and receptaculum

seminis (spermatheca) (Dupuis, 1970).

The last visible tergite is the eighth one. It is folded ventrally on each side and

forms the laterotergites. Each laterotergite bears an articulated gonocoxite (Dupuis, 1970;

Derjanschi and Péricart, 2005), also called valvifer (Snodgrass, 1935; Schaefer, 1968).

Gonocoxites carry the gonapophyses (Dupuis, 1970; Derjanschi and Péricart, 2005), also

called valvulae (Snodgrass, 1935; Schaefer, 1968). As compared to some other groups of

bugs, gonapophyses are strongly reduced, determining the gonocoxites and laterotergites to

become the most important parts of the ovipositor. Their main role is to protect the genital

aperture (Dupuis, 1951, 1970).

The parts of the first pair of valvifers are generally separated from each other. The

second pair of valvifers is fused on the median line. The first pair of valvulae is fused in one piece, triangulum, and the second pair of valvulae is fused in one piece, arcus (Dupuis,

1970; Schaefer, 1968).

Receptaculum seminis (spermatheca) presents the following parts: an orificium

receptaculi, ductus receptaculi (spermathecal duct), a pars intermedialis (spermathecal

pump) and capsula seminalis (Snodgrass, 1935; Dupuis, 1970; Derjanschi & Péricart,

2005).

Results

Aelia acuminata (Linné, 1758) (Plate 5, Fig. 2)

The first pair of valvifers, laterotergites 8, the second pair of valvifers and

laterotergites 9 are covered up with long setae, symmetrically distributed. Capsula seminalis is globose, with two lateral long expansions which surpass the anterior annular

- 32 -


creste. The posterior annular creste is well developed as the anterior annular creste. The

latter is narrow.

Table 1. List of specimens examined.

Species Number of specimens

Data labels

Aelia acuminata 3 Ciric area (IS; RO), 28.06.2007 3 Botanical Garden (IS; RO), 9.07.2007 5 Bârnova (IS; RO), 18.07.2007 2 Bârnova (IS; RO),18.08.2007 2 Botanical Garden (IS; RO), 28.09.2007 3 Botanical Garden (IS; RO), 7.05.2008 2 Ciric area (IS; RO), 10.05.2008 1 Botanical Garden (IS; RO), 30.06.2008 6 Botanical Garden (IS; RO), 29.07.2008

Eysarcoris aeneus 1 Botanical Garden (IS; RO), 9.07.2007 1 Bârnova (IS; RO), 18.07.2007 1 Paltin (VN; RO), 8.07.2009

Stagonomus amoenus 1 Botanical Garden (IS; RO), 9.07.2008

Rubiconia intermedia 1 Botanical Garden (IS; RO), 9.07.2007 5 Bârnova (IS; RO), 18.07.2007 1 Botanical Garden (IS; RO), 28.09.2007

Holcosthetus vernalis 1 Bârnova (IS; RO), 18.07.2007 ♀, 2 Paltin (VN; RO) (leg. Chiriac N.), 8.07.2009 2 Paltin (VN; RO), 10.07.2009

Carpocoris purpureipennis 1 Ciric (IS; RO), 28.06.2007 6 Bârnova (IS; RO), 18.07.2007 1 Botanical Garden (IS; RO), 28.09.2007 1 Botanical Garden (IS; RO), 9.07.2008 2 Botanical Garden (IS; RO), 29.07.2008 1 Botanical Garden (IS; RO), 12.08.2008

Dolycoris baccarum 1 Ciric (IS; RO), 28.06.2007 1 Botanical Garden (IS; RO), 9.07.2007 2 Bârnova (IS; RO), 18.07.2007 1 Bârnova (IS; RO), 18.08.2007 1 Botanical Garden (IS; RO), 28.09.2007 1 Ciric (IS; RO), 10.05.2008 1 Bârnova (IS; RO), 27.06.2009 1 Bârnova (IS; RO), 5.07.2009 3 Paltin (VN; RO), 8.07.2009

Pentatoma rufipes 10 Bârnova (IS; RO), 18.07.2007 2 Bârnova (IS;RO), 18.08.2008 1 Bârnova (IS; RO), 22.08.2009

Piezodorus lituratus 1 Botanical Garden (IS; RO), 29.07.2008 1 Paltin (VN; RO), 8.07.2009

Eurydema ornata 2 Bârnova (IS; RO), 18.07.2007

Eysarcoris aeneus (Scopoli, 1763) (Plate 3, Fig. 1)

The first pair of valvifers, laterotergites 8 and the second pair of valvifers,

laterotergites 9 and the tenth segment of the abdomen are covered with both long and short

setae. They are symmetrically distributed. Capsula seminalis is globose, without

expansions. The posterior annular creste well developed. The anterior annular creste is narrow.

Stagonomus amoenus (Brullé, 1832) (Plate 3, Fig. 2)

The first pair of valvifers, valvulae and laterotergites 8 are merged. The tenth

segment of the abdomen and the laterogites 9 are sharp at the posterior border. The anterior

- 33 -


border of the tenth segment of the abdomen is concave. Capsula seminalis is ovoid. The

proportion between length and width of capsula seminalis is 1.6. The anterior annular creste

is narrow. The posterior annular creste is difficult to notice.

Rubiconia intermedia (Wolff, 1811) (Plate 4, Fig. 1)

The first pair of valvifers, laterotergites 8, the second pair of valvifers,

laterotergites 9 and the tenth segment of the abdomen are covered with long setae. Capsula

seminalis is globose, with three spur like expansions. The anterior annular creste is narrow.

The posterior annular creste is difficult to notice.

Holcosthetus vernalis (Wolff, 1804) (Plate 4, Fig. 2)

The first pair of gonocoxites, laterotergites and the second pair of laterotergites

and gonocoxites are covered up and the tenth segment of the abdomen are covered with setae. The anterior border of the gonocoxite 9 is concave. Capsula seminalis is ovoid; the

proportion between length and width of capsula seminalis is 1.8. Capsula seminalis has one

sleazy expansion.

Carpocoris purpureipennis (De Geer, 1773) (Plate 3, Fig. 3)

The first pair of gonocoxites is covered with setae only on the posterior and

internal borders. Gonocoxites 9, laterotergites 8 and 9 and the tenth segment of the

abdomen are covered with setae regularly distributed. Capsula seminalis is globose without

any expansions. The posterior annular creste is well developed. The anterior annular creste

is very well developed.

Dolycoris baccarum (Linné, 1758) (Plate 4, Fig. 3)

Gonocoxites 8, laterotergites 8 and 9 and the tenth segment of the abdomen are covered with setae. The anterior annular creste is broad. The posterior annular creste is well

developed. Capsula seminalis is globose without any expansions.

Pentatoma rufipes (Linné, 1758) (Plate 5, Fig. 1)

Gonocoxites 8 are covered with numerous long setae. Gonocoxites 9, laterotergites

8 and 9 and the tenth segment of the abdomen is covered with long setae. The

gonapophyses 9 is strongly concave. Capsula seminalis is globose with two long

expansions which surpass the anterior annular creste. The posterior annular creste is

conspicous.

Piezodorus lituratus (Fabricius 1794) (Plate 5, Fig. 3)

Gonocoxites 8 are covered with setae only on the posterior and internal borders.

Gonocoxites 8, laterotergites 8 and 9 and the tenth segment of the abdomen are covered up

with few setae. The anterior border of the gonapophyses 9 is somehow convex. The diameter of the anterior annular creste is smaller than the diameter of capsula seminalis.

Capsula seminalis has a particular form (Plate 5, Fig. 4).

Eurydema ornata (Linné, 1758) (Plates 1, 2)

Gonocoxites 8, laterotergites 8 and 9 and the tenth segment of the abdomen are

covered up with setae. The setae of gonocoxites 8 are denser on the posterior and internal

borders. The tenth segment of the abdomen is easily concave. The anterior and posterior

annular creste are well developed. The proportion between the length and the maximum

width of the capsula seminalis is 1.6. The apical half of capsula seminalis is distended.

Discussion and Conclusions

The female genitalia of Stagonomus amoenus is considerably distinctive from the other female genitalia of the subfamily Pentatominae. The tenth segment of the abdomen

- 34 -


and the laterogites 9 are sharpened on the posterior border and, therefore, the apex of the

abdomen is sharp too. Another distinctive feature is the mergence of the laterotergites, the

gonocoxites and gonapophyses 8.

The distribution of the setae on the gonocoxites and the laterotergites is an

important criterion. For example, the gonocoxites 8 of Carpocoris purpureipennis and

Piezodorus lituratus are covered up with setae only on the internal and posterior sides.

The shape of the anterior edge of the tenth segment is another feature useful for

systematics. The anterior edge can be concave (Pentatoma rufipes, Holcostethus vernalis,

Stagonomus amoenus), convex (Piezodorus lituratus, Eysarcoris aeneus) or almost straight.

Two other important criteria are the form of capsula seminalis and the presence or

absence of expansions at this level. At the species Aelia acuminata, Eysarcoris aeneus, Carpocoris purpureipennis, Dolycoris baccarum, Pentatoma rufipes and Rubiconia

intermedia, capsula seminalis is globose.

A particular form of capsula seminalis is encountered at Piezodorus lituratus.

Capsula seminalis is ovoid at the species Stagonomus amoenus, Holcostethus vernalis and

Eurydema ornata.

The expansions of capsula seminalis are absent at the species Stagonomus

amoenus, Piezodorus lituratus, Eysarcoris aeneus, Carpocoris purpureipennis, Dolycoris

baccarum and Eurydema ornata. Rubiconia intermedia has three spur like expansions.

Aelia acuminata and Pentatoma rufipes have two long expansions. Holcostethus vernalis

has just one expansion of capsula seminalis.

The anterior annular creste can be narrow as in most of the species or broad as in Carpocoris purpureipennis and Dolycoris baccarum.

McDonald (1966) described spermatheca of the species Eysarcoris aeneus as

follows: “Spermathecal dilation constricted proximally forming a large distal chamber and

a smaller more elongate proximal chamber, spermatheca otherwise normal” (Plate 6). In

our research McDonald's findings are confirmed as it can be seen from the drawings (Plate

3, Fig. 1; Plate 6): there is a constriction in spermathecal dilation and capsula seminalis

lacks expansions.

Candan et al. (2010) described the morphology of Dolycoris baccarum’s

spermatheca, using electronic microscopy. In our research we used optical microscopy and

the findings were similar to those presented by Candan et al. (2010).

The main similarities and differences found by us between female external

genitalia are summarized in the following key: 1 Gonocoxites and laterotergites 8 merged; posterior edge of tenth segment and

laterotergites 9 sharp (Plate 3, Fig. 2) Stagonomus amoenus

- Gonocoxites and laterotergites 8 not merged; posterior border of tenth segment and

laterotergites 9 unsharpened 2

2 Capsula seminalis globose 3

- Capsula seminalis of different form 8 3 Capsula seminalis with three spur-like expansions (Plate 4, Fig. 1)

Rubiconia intermedia

- Capsula seminalis with two long expansions or without 4

4 Capsula seminalis without expansions 5

- Capsula seminalis with two expansions 7

- 35 -


5 Gonocoxites 8 covered with setae only on posterior and internal edges (Plate 3, Fig. 3)

Carpocoris purpureipennis

- Gonocoxites 8 covered with setae on the whole surface 6

6 Anterior annular crest broad (Plate 4, Fig. 3) Dolycoris baccarum

- Anterior annular crest narrow (Plate 3, Fig. 1) Eysarcoris aeneus

7 Gonocoxites 9 strongly concave (Plate 5, Fig. 1) Pentatoma rufipes

- Gonocoxites 9 almost straight (Plate 5, Fig. 2) Aelia acuminata

8 Capsula seminalis of particular form; proportion between length and smallest width 3.2-

3.4 (Plate 5, Figs. 3, 4) Piezodorus lituratus

- Capsula seminalis ovoid; proportion between length and smallest width 1.6-1.8 9

9 Capsula seminalis with long expansion (Plate 4, Fig. 2) Holcostethus vernalis - Capsula seminalis without expansions (Plates 1, 2) Eurydema ornata

Plate 1. Generalized female genitalia in pentatomides – Eurydema ornata (Linné, 1758).

median dilation

capsula seminalis (spermathecal bulb)

pars intermedialis (spermathecal pomp)

posterior annular crest (distal flanges)

ductus receptaculis (distal spermathecal duct)

anterior annular crest (proximal flanges)

sclerotized median dilation

thickening of vaginal intima

proximal spermathecal duct

gonapophysis 8 (valva I, triangulin)

orificium receptaculi

gonocoxite 8 (valvifer I)

gonapophysis 9 (valva II, arcus)

gonocoxite 9 (valvifer II)

paratergite (laterosternite) 9

paratergite (laterosternite) 8

tenth segment

- 36 -


Plate 2 (Figs. 1-2). Female genitalia of Eurydema ornata (Linné, 1758) 1. Segment 8; 2. Segments 9

and 10.

- 37 -


Plate 3 (Figs. 1-3). Female genitalia: 1. Eysarcoris aeneus (Scopoli, 1763); 2. Stagonomus amoenus (Brullé, 1832); 3. Carpocoris purpureipennis (De Geer, 1773).

1 2

3

- 38 -


Plate 4 (Figs. 1-3). Female genitalia: 1. Rubiconia intermedia (Wolff, 1811); 2. Holcostethus vernalis (Wolff, 1804); 3. Dolycoris baccarum (Linné, 1758).

- 39 -


Plate 5 (Figs. 1-4). Female genitalia: 1. Pentatoma rufipes (Linné, 1758); 2. Aelia acuminata (Linné,

1758); 3. Piezodorus lituratus (Fabricius, 1794); 4. P. lituratus, detail of capsula seminalis.

1

2

3 4

- 40 -


Plate 6. Spermatheca of Eysarcoris aeneus (after McDonald, 1966).

The analysis of the female genitalia of pentomines shows the existence of

distinctive characters, at least between genera. The most important characteristics that may be used in systematics are: the chaetotaxy, the shape of the ninth gonocoxite’s anterior

edge, the shape of capsula seminalis and the number of its expansions.

Aknowledgements

I would like to thank Dr. Petr Kment for providing references, Dr. Ovidiu Popovici

for assisstance and guidance in my research and Dorina Pascu for her kindness in helping

me translates the paper.

References

Candan, S., Erbey, M., Sümeyye Yilmaz, F., 2010. Surface Morphology of the Spermatheca of Dolycoris

baccarum (Linnaeus, 1758) (Heteroptera: Pentatomidae). Entomological News, 121(4): 334-341.

Crampton, G.C., 1920. Remarks on the basic plan of the terminal abdominal structures of the males of winged

insects. The Canadian EntomologistI, 52(8): 178-183.

Crampton, G.C., 1922. The genitalia of the males of certain hemiptera (Heteroptera) and homoptera. Bulletin of

Brooklyn Entomological Society, XVII: 46-57.

Derjanschi, V., Péricart, J., 2005. Hémiptères Pentatomoidea Euro-méditerrnéens vol. I Généralités Systématique:

Première Partie, Faune de France (France et régions limitrophes). Fédération des Sociétés des

Sciences Naturelles, 494 pp.

Dupuis, C., 1951. Les espèces françaises du genre Eurydema Laporte (Hemiptera, Pentatomoidea, subfam.

Pentatominae). Révision systematique avec une introduction à l’étude morphologique des organes

génitaux externes des Pentatomoidea. Annales de la Société Éntomologique de France, 118: 1-29.

Dupuis, C., 1952. Donné sur la morphogenese des genitalia males des insectes. Leur importance pour une

nomenclature rationelle de ces structures. Transsactions of the Ninth International Congress of

Entomology, 1: 151-154.

- 41 -


Dupuis, C., 1953. Les génitalia mâles des hémiptères hétéroptères leur utilisation en systématique. Transsactions

of the Ninth International Congress of Entomology, 2: 7-10.

Dupuis, C., 1955. Les genitalia des hemipteres Heteropteres (Genitalia externes des deux sexes; Voies

ectodermiques femalles). Revue de la morphologie. Lexique de la nomenclature. Index bibliographique

analytique. Memoires du Museum d'Histoire Naturelle, 6: 183-278.

Dupuis, C., 1970. Heteroptera, pp. 190-208. In : S.L. Tuxen (Editor). Taxonomist´s glossary of insects.

Copenhagen, Munksgaard, Denmark 359 pp.

Gapon, D., 2001. Inflation of heteropteran aedeagi using microcapillaries (Heteroptera: Pentatomidae).

Zoosystematica Rossica, 9(1): 157-160.

Kis, B., 1984. Heteroptera – partea generală și suprafamilia Pentatomoidea, Fauna Republicii Socialiste

România, vol. VIII, fasc. 8. Editura Academiei Republicii Socialiste România, București, 216 pp.

McDonald, F.J.D., 1966. The genitalia of North American Pentatomoidea (Hemiptera: Heteroptera). Quaestiones

Entomologicae 2: 7-150.

Mihalache, C., Săvescu, A., Buguleanu, Gh., Paulian, Fl., Balaj, D., Pașol, P.,1969. Entomologie agricolă. Editura

Agrosilvică, București, 564 pp.

Millar, I.M., Uys, V.M., Urban, V.P. (eds.), 2000. Collecting and preserving insects and arachnids. R. P., Plant

Protection Research Institute, Pretoria, South Africa.

Panizzi, A.R., McPherson, J. E., James, D.G., Javahery, M., McPherson, R.M., 2000. Stink Bugs (Pentatomidae).

In Schaefer, C.W., Panizzi A.R. (eds.) Heteroptera of economic importance. CRC Press LLC: 421-474.

Rider, D.A., 2006. Family Pentatomidae Leach, 1815. In Aukema, B., Rieger, Ch. (eds) Catalogue of the

Heteroptera of the Palaearctic Region. Volume 5. Pentatomomorpha II. The Netherlands

Entomological Society, Amsterdam: 233-402.

Schaefer, C.W., 1968. The Homologies of the Female Genitalia in the Pentatomoidea (Hemiptera-Heteroptera).

New York Entomol. Society, 76: 87-91.

Schaefer, C.W., 1998. Phylogeny, Systematics, and Practical Entomology: The Heteroptera (Hemiptera). Anais da

Sociedad Entomológica do Brasil, 27(4): 499-511.

Schuh, R.T., Slater, J.A., 1995. True bugs of the world (Hemiptere: Heteroptera). Cornell University Press, 337

pp.

Snodgrass, R.E., 1935. Principles of insect morphology. McGraw-Hill Book Co., Inc., New York & London, 667

pp.

Štys, P., 1961. Morphology of the abdomen and female ectodermal genitalia of the trichophorus Heteroptera and

bearing on their classification. 11th International Congress of Entomomolgy, Wien, 17-25.VIII.1960.

Verhandl., Bd. I, sect. I-IV: 37-43.

Tay, E.B., 1969. Morphology of the external genitalia of some pentatominae (Heteroptera). Papers of Department

of Entomology of University of Queensland, 2: 75-84.

- 42 -

CHARACTERS OF THE EXTERNAL FEMALE GENITALIA WHICH CAN … · Elena Mădălina Morariu are for...

Documents

Transcript of CHARACTERS OF THE EXTERNAL FEMALE GENITALIA WHICH CAN … · Elena Mădălina Morariu are for...