The Biological Context and Evolution of Pendergrast's Organs Of

The biological context and evolution of Pendergrast’s organs of Acanthosomatidae (Heteroptera, Pentatomoidea)1

C. FISCHER

Abstract: The Pendergrast’s organs of Acanthosomatidae have been the subjects of many investigations. The present study summarizes and reviews previous data and hypotheses. In addition a survey on the presence of Pendergrast’s organs of more than 100 acanthosomatid species is presented for the first time. Transformations of the Pendergrast’s organs within the Acanthosomatidae are discussed. The reproduc- tive behaviour of Cyphostethus tristriatus is described for the first time. It reveals that the Pendergrast’s organs are involved in the biological context of oviposition. Female acanthosomatids rub their hind tarsi over the setose area of the Pendergrast’s organs, spin the eggs, then place and attach them with their hind tarsi to the oviposition site. The smearing behaviour of Acanthosomatidae performed during oviposition is homologised with the grooming behaviour of Heteroptera. A scenario on the evolution of Pendergrast’s organs and the involved oviposition behaviour is presented.

Key words: Acanthosomatidae, behaviour, grooming, Heteroptera, Lestoniidae, oviposition, Pender- grast’s organs.

Introduction Pendergrast’s organs are grooves on each side of the sternum and can be present on Many authors have contributed to the female abdominal segments V, VI and VII. study of Pendergrast’s organs (PENDERGRAST The majority of acanthosomatid species 1953; CARAYON 1981; STADDON 1990; have Pendergrast’s organs on the abdominal FISCHER 1994a, 1994b, 2000) and proposed segments VI and VII (Tab. 1). The grooves several – sometimes quite conflicting – hy- bear numerous bristles and have a more or potheses on the biological role of these or- less oval shape with the greater diameter gans. BREDDIN (1903) was the first to recog- usually orientated in the dorsoventral axis. nise the setose areas on the female abdomen In Elasmostethus spp. the dorsoventral diam- of Acanthosomatidae and used the term eter measures about 0.5 mm (FISCHER „Copulationsgruben“ (copulation grooves), 1994b). Size and number of bristles differ which suggests that the Pendergrast’s organs between the grooves of the abdominal seg- are involved in mating behaviour. Other au- ments VI and VII. In most species of the thors favoured a hypothesis that Pender- Acanthosomatidae the grooves of the ab- grast’s organs are involved in oviposition. In dominal segment VII are bigger and bear order to be able to verify each of the hy- more bristles than those of segment VI. The potheses, the mating and oviposition behav- length of the bristles varies from 0.4 mm up iour of Cyphostethus tristriatus (FABRICIUS to 0.6 mm. From SEM-photographs, duc- 1787) was studied. Both nymphs and adults tules opening into pores with a diameter of of Cyphostethus tristriatus feed on the fruits of 10 µm can be detected between the bristles Juniperus communis, a shrub. Juniperus com- (Fig. 11). The epidermis underlying the se- munis is also used as the mating and oviposi- tose areas is much thicker than the sur- tion site of Cyphostethus tristriatus. rounding epidermal tissue (Fig. 12). TEM- Denisia 19, zugleich Kataloge 1I dedicate this paper to Ernst Heiss, who always has been interested in the research of beginners in Heteropterology der OÖ. Landesmuseen and encourages them to go on. I was one of them. Neue Serie 50 (2006), 1041–1054

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Figs 1-6: Oviposition of Cyphostethus sections clearly display that the cells con- the stem-species pattern of Acanthosomati- tristriatus (Acanthosomatidae) (1) egg just tain numerous vacuoles. The contents of dae (FISCHER 1993, 1994a). This character deposited (2) after egg is deposited the female rubs her hindtarsi across the these cells are still unknown. Nevertheless, was thought to be an apomorphy of the Pendergrast’s organs (po) (3) secretion is a secretory function of the Pendergrast’s or- Acanthosomatidae until the „disc-like or- applied by rotating the egg with both gans is most likely. Cross-sections display gans“ of Lestoniidae (Pentatomoidea) were hindtarsi before glue hardens (4-6) a studied using lightmicroscopical and SEM- microsymbiont sac (symb) is applied onto ductules, which open into pores between the egg surface. Microsymbionts, which are the bristles. SEM-photographs of the inner techniques (FISCHER 2000). It became evi- transferred onto the egg, originate from a side of the cuticle exhibit typical gland cells dent that the disc-like organs present only unique cuticular pouch of the female in female Lestoniidae are homologous to the genitalia in Acanthosomatidae. (FISCHER 1994b, 2000). Pendergrast’s organs of female Acanthoso- Phylogenetic analysis of Acanthoso- matidae (FISCHER 2000). The disc-like or- matidae has demonstrated that paired Pen- gans of Lestoniidae are present only on the dergrast’s organs on the female abdominal abdominal segment VII. Being homologous sternum of segment VI and VII belong to as paired abdominal sternal glands in fe-

1042 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at males, Pendergrast’s organs of Acanthoso- matidae and disc-like organs of Lestoniidae are hypothesized as a synapomorphy sup- porting a sistergroup relationship of these two taxa (FISCHER 2000). Additionally, several other morphological characters (FISCHER 2000) and combined analyses of morphological and molecular data (GRAZIA et al., in press) support a sistergroup relationship of Acanthosomatidae and Lestoniidae. For the stem-species of Acanthosomatidae, paired Pendergrast’s organs on the female abdominal segment VII are a plesiomorphy and paired Pendergrast’s organs on the abdominal segment VI are an apomorphy.

The self-stimulation hypothesis As mentioned above, several conflicting hypotheses on the function and biological role of Pendergrast’s organs were proposed during the last 100 years. PENDERGRAST (1953) investigated the morphology of the female setose areas in detail with light-mi- croscopical techniques. Although he was The egg-clutch Figs 7-8: Pyrrhocoris apterus grooming not very confident in his interpretation of abdomen (7) Note the position of the the „cell-like bodies“ as being nerve cells, he protection hypothesis hindtarsi while taking up dirt and particles, proposed a stimulating function for the se- which is similar to the position of the PENDERGRAST (1953) also considered a hindtarsi of Cyphostethus tristriatus while tose areas. He proposed that rubbing the possible secretory function for this organ. In taking up secretion from the Pendergrast’s hindtarsi across the setose areas should self his view the secretion should be transferred organs (see Fig. 2) (8) brushing off uptaken stimulate the female to oviposit her eggs. It onto the eggs by the hind tarsi. Because of dirt by rubbing both hindtarsi against each other (compare with Fig. 3) (drawings by should be clearly stated that Pendergrast the lack of evidence of secretion, Pender- courtesy of Antje Fischer). himself was not very convinced by this hy- grast discarded this hypothesis. The hypoth- pothesis. Indeed, self-stimulation by the fe- esis of a secretion transfer onto the eggs male does not make much sense. Several ar- gained new evidence from a phylogenetic guments can be put forward against this hy- analysis of Acanthosomatidae (FISCHER 1993, pothesis. First, why should a female stimu- 1994a). Indeed, the egg-smearing behaviour late herself to oviposit her eggs? There are can be observed, as it is described for countless other insects that deposit their Cyphostethus tristriatus in this study. eggs without any evidence of mechanical self-stimulation. Second, transformations The secretion of the Pendergrast’s or- within the Acanthosomatidae, e.g. neither gans most likely functions as a repellent the enlarged Pendergrast’s organs areas over against predators and parasitoids. An indi- three abdominal segments of Sniploa obsole- rect indication comes from Elasmucha tus nor the complete loss of Pendergrast’s or- species. It has been known for a long time gans in Elasmucha-species can be explained that females of Elasmucha-species perform by this self-stimulation-hypothesis. Third, if maternal care. Elasmucha-species do not there really is a self-stimulation, a rather have Pendergrast´s organs (Tab. 1). As complex system must be present. A signal paired Pendergrast’s organs on the female must be sent to the hindtarsi rubbing across abdominal segments VI and VII belong to the setose. These setose areas must be sensi- the stem-species pattern of Acanthosomati- tive and send signals to stimulate the ovipo- dae, the absence of Pendergrast’s organs in sition behaviour. This is neither very likely Elasmucha species has to be considered as a nor parsimonious. secondary loss in the stem-species pattern of

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Tab. 1: Presence of Pendergrast’s organs on the pregenitalia segments of Elasmucha (FISCHER 1993, 1994a). Females Acanthosomatidae-species. that protect eggs and nymphs against preda- V VI VII Reference tors and parasitoids should have a higher fit- Abulites fuscosparsus (STÅL 1854) - - + KUMAR 1974 ness. Indeed, the maternal care of the Elas- Abulites sparsus GERMAR 1837 - - + CF mucha females is very effective (FROST & Acanthosoma axillaris JAKOWLEFF 1889 - + + CF HABER 1944; STRAWINSKI 1951; JORDAN Acanthosoma dentata DE GEER 1773 - + + CF 1958; MELBER et al. 1980; MELBER & Acanthosoma forciparum REUTER 1881 - + + CF SCHMIDT 1984; HONBO & NAKAMURA 1985; Acanthosoma haemorrhoidale (LINNAEUS 1758) - + + PENDERGRAST 1953, CF KUDO et al. 1989; MAPPES & KAITALA 1994) Acrophyma frigidula BERGROTH 1916 - + + KUMAR 1974 with nearly 100 % of the deposited eggs sur- Aesepus signoretii STÅL 1876 - - + KUMAR 1974 viving. If maternal care is an effective way Agamedes pilicornis STÅL 1876 - - - KUMAR 1974 Amphaces elongata DISTANT 1910 - + - CF of protecting eggs and nymphs against pred- Amphaces ferruginea DALLAS 1851 - + - CF ators and parasitoids, and if the secretion of Amphaces proxima DALLAS 1851 - + - CF Pendergrast’s organs has a protective func- Amphaces subrufescens (VAN DUZEE 1905) - + - CF tion, Pendergrast’s organs became absent, Andriscus amartus (DALLAS 1851) - + + CF but not before maternal care evolved in the Andriscus recurvus WALKER 1867 - + + KUMAR 1974 stem-lineage of Elasmucha. Andriscus telifer (WALKER 1867) - + + CF Anischys luteovarius (WESTWOOD 1837) - + + KUMAR 1974 Bebaeus punctipes DALLAS 1851 - - - KUMAR 1974, CF Why do phytophagous insects Blaudus ruficornis STÅL 1872 - + + KUMAR 1974 have to protect their eggs? Catadipson aper BREDDIN 1903 - - - KUMAR 1974, CF Additional support for the function of Catadipson imernensis (CACHAN 1952) - - - KMENT 2005 Catadipson sus BREDDIN 1906 - - - CF Pendergrast’s organs can be gained from a Cylindrocnemia plana MAYR 1864 - + + KUMAR 1974, CF comparison to the biology of other phyto- Cyphostethus tristriatus (FABRICIUS 1787) - + + CF phagous insects. With the exception of Elasmostethus elasmosthethoides (BREDDIN 1903) - + + BREDDIN 1903, CF Asopinae, all Pentatomoidea are phyto- Elasmostethus tenuispinum (BREDDIN 1903) - + + BREDDIN 1903 phagous (SCHAEFER & AHMAD 1987). Phy- Elasmostethus sastragaloides (BREDDIN 1903) - + + BREDDIN 1903, CF tophagous insects face several problems and Ditomotarsus punctiventris SPINOLA 1852 - + + KUMAR 1974, CF require evolving solutions to these problems. Duadicus pallidus DALLAS 1851 - + + KUMAR 1974, CF MITTER et al. (1988) gave a general outlook Ea australis DISTANT 1911 - + + KUMAR 1974, CF on the evolutionary steps that insects have Elasmostethus atricornis (VAN DUZEE 1904) - + + THOMAS 1991, CARTER & HOEBEKE 2003 to confront when crossing the barrier be- Elasmostethus cruciatus (SAY 1831) - + + THOMAS 1991 tween zoophagy and phytophagy. Phy- Elasmostethus interstinctus (LINNAEUS 1758) - + + PENDERGRAST 1953, tophagy not only means exploiting the nu- THOMAS 1991, CF trient resources of plants, but also involves Elasmostethus minor HORVÁTH 1899 CF ethological and morphological characters Elasmucha amurensis KERZHNER 1972 - - - CF that can be attributed to phytophagy. Fe- Elasmucha aspersa (WALKER 1867) - - - KUMAR 1974 males of a phytophagous species often lay Elasmucha cordillera THOMAS 1991 - - - THOMAS 1991 their eggs on the host-plants, which the Elasmucha dorsalis (JAKOVLEV 1876) - - - CF Elasmucha ferrugata (FABRICIUS 1787) - - - KUMAR 1974, CF nymphs can use as a food resource. After Elasmucha fieberi (JAKOVLEV 1865) - - - CF hatching, the nymphs are already on the Elasmucha flammatum (DISTANT 1974) - - - THOMAS 1991 host-plant. Choosing the food plant as an Elasmucha grisea (LINNAEUS 1758) - - - PENDERGRAST 1953, oviposition site is certainly an advantage for KUMAR 1974, CF the offspring, but causes some disadvantages, Elasmucha lateralis (SAY 1831) - - - THOMAS 1991, CF too. Eggs that are deposited on plants are ex- Elasmucha nipponica (ESAKI & ISHIHARA 1950) - - - CF posed and therefore easily visible and acces- Elasmucha punctata (DALLAS 1851) - - - KUMAR 1974 sible for predators and parasites. To minimise Elasmucha putoni SCOTT 1874 - - - KUMAR 1974, CF the loss of eggs, females insert eggs into the Elasmucha salebrosa (BREDDIN 1903) - - - BREDDIN 1903, CF Elasmucha signoreti SCOTT 1874 - - - KUMAR 1974, CF plant tissues or protect them by chemical or Elasmucha truncatula (WALKER 1867) - - - KUMAR 1974 behavioural strategies (HILKER 1994). Esbenia major JENSEN-HAARUP 1931 - + + KUMAR 1974 Esbenia minor JENSEN-HAARUP 1931 - + + CF Eupolemus picturatus DISTANT 1910 ? ? ? KUMAR 1974 Galgacus labidus (ERICHSON 1842) - - + KUMAR 1974, CF

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Materials and Methods V VI VII Reference Hellica nitida HAGLUND 1868 - - + CF Specimens of 60 species of Acanthoso- Hiarchas crassicornis (WALKER 1867) ? ? ? KUMAR 1974 matidae and Lestoniidae were studied by the Hyperbius geniculatus (SIGNORET 1863) - + + KUMAR 1974, CF author; bring the total number of species ob- Ibocoris ficivora ROCHE 1947 - - - KUMAR 1974, served to more than 100 (Tab. 1). Specimens KMENT 2005, CF in the collection of the following museums Laccophorella bornemiszae HORVÁTH 1904 - + + KUMAR 1974, CF were studied: British Museum of Natural Lanopis rugosus SIGNORET 1863 - + + KUMAR 1974 History London, American Museum of Nat- Lindbergicoris armifer (LINDBERG 1934) - + + ZHENG & WANG 1995 Lindbergicoris difficilis (LIU 1988) - + + ZHENG & WANG 1995 ural History New York, Museum für Lindbergicoris distinctus (LIU 1988) - + + ZHENG & WANG 1995 Naturkunde der Humboldt-Universität Lindbergicoris elegans ZHENG & WANG 1995 - - + ZHENG & WANG 1995 Berlin, Naturhistorisches Museum Vienna, Lindbergicoris elegantulus ZHENG & WANG 1995 - - + ZHENG & WANG 1995 National Museum of Natural History Wash- Lindbergicoris forfex (DALLAS 1851) - + + ZHENG & WANG 1995 ington, Zoological Collection of the Zoolog- Lindbergicoris hochii (YANG 1933) - + + ZHENG & WANG 1995 ical Institute of Freie Universität Berlin, Lindbergicoris pulchellus ZHENG & WANG 1995 - - + ZHENG & WANG 1995 Staatliches Museum für Naturkunde Karl- Mahea andriai (CACHAN 1952) - - - KMENT 2005 sruhe, Zoological Museum of St. Petersburg, Mahea distanti KMENT 2005 - - - KMENT 2005 Zoological Museum University of Copen- Mahea durrelli KMENT 2005 - - - KMENT 2005 hagen. Mahea parvula KMENT 2005 - - - KMENT 2005 Mahea sexualis DISTANT 1909 - - - KMENT 2005 The mating and oviposition behaviour Mazanoma variada ROLSTON & KUMAR 1974 - + + ROLSTON & KUMAR 1974 of Cyphostethus tristriatus was observed in Microdeuterus aequalis WALKER 1867 - - + CF the field (Eschwege, Germany). Four males Microdeuterus megacephalus and three females of Cyphostethus tristriatus (HERRICH-SCHAEFFER 1845) - - + KUMAR 1974, CF Mochus fortis DISTANT 1910 ? ? ? KUMAR 1974, were collected in the field and kept in insect CF no females boxes (20 cm x 20 cm x 10 cm) in the labo- Monteithiessa distincta KUMAR 1974 - + - KUMAR 1974 ratory. Branches of Juniperus communis were Nopalis sulcatus SIGNORET 1863 - - + KUMAR 1974, CF placed in the boxes to provide resources as Noualhierida rufa CACHAN 1952 ? ? ? KMENT 2005 food and oviposition sites for Cyphostethus Noualhieridia marginata CACHAN 1952 ? ? ? KMENT 2005 tristriatus. Noualhieridia ornatula BREDDIN 1898 - + + KUMAR 1974, KMENT 2005 Macrophotographs were used to prepare Oncacontias brunneipennis BREDDIN 1903 - + + BREDDIN 1903 ink drawings of the oviposition behaviour. Oncacontias vittatus (FABRICIUS 1787) - + + PENDERGRAST 1953, KUMAR 1974, CF The biological role Panaetius lobulatus STÅL 1866 - + + KUMAR 1974, CF of Pendergrast’s organs Phorbanta variabilis (SIGNORET 1863) - - - CF Planois bimaculatus (SPINOLA 1852) - + + KUMAR 1974, CF Different functions of the Pendergrast’s Praesus incarnatus STÅL 1872 - - 2 KUMAR 1974 organs in several biological contexts had Proctophantasta colax BREDDIN 1903 - - - KUMAR 1974, CF been assumed previously 1) mating and 2) Proctophantasta diabolus BREDDIN 1903 - - - CF egg laying self-stimulation and/or egg smear- Proctophantasta pseustes BREDDIN 1903 - - - CF ing (see introduction). Rhopalimorpha alpina (WOODWARD 1953) - + + KUMAR 1974 Rhopalimorpha lineolaris PENDERGRAST 1950 - + + PENDERGRAST 1953, Mating behaviour KUMAR 1974, CF of Cyphostethus tristriatus Rhopalimorpha obscura DALLAS 1842 - + + PENDERGRAST 1953, KUMAR 1974 Males approach the female from behind. Sangarius paradoxus STÅL 1866 - - + KUMAR 1974 With his antennae the male drums the fe- Sastragala guttasanguiis BREDDIN 1903 - - - CF male’s abdomen at first, then the thorax and Sastragala scutellata (SCOTT 1874) ---CF the head. While the male mounts on the Sinopla perpunctatus SIGNORET 1863 - + + KUMAR 1974, CF (some YY without, some with dorsum, he continues drumming with his p.o. on VII or VI+VII) antennae. Finally, the male exposes his gen- Sniploa obsoletus SIGNORET 1863 + + + KUMAR 1974, CF ital capsule and makes contact with the fe- Stauralia chlorocantha DALLAS 1851 - - + CF male’s genital segments. Still maintaining Stauralia compuncta BERGROTH 1895 - - + CF the contact with the female genitalia, the Tolono decoratus ROLSTON & KUMAR 1974 - - + ROLSTON & KUMAR 1974 male turns to the right side and dismounts Uhlunga typica DISTANT 1892 - - - KUMAR 1974, CF from the female dorsum. This procedure re- Xosa lugubris (THUNBERG 1822) - + + KUMAR 1974, CF

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Oviposition in Cyphostethus tristriatus and the involvement of the Pendergrast’s organs Immediately after copulation, which can last a couple of days, the females can be observed searching for an oviposition site. Oviposition starts with heavy contrac- tions of the genital segments of the female. The egg’s movement can be observed through the slightly opened genitalia plates. The egg is then rotated within the vagina for several seconds before it eventually leaves the vagina, passing the now fully opened genitalia plates. The glue for attach- ing the egg to the plant surface is clearly visible on the pole of the egg as it emerges. The egg is attached to the plant surface in an up- right orientation. However, the glue does not harden until the female puts the secre- tions of the Pendergrast’s organs onto the egg. Repeatedly the female touches the setose areas of the Pendergrast’s organs with the distal part of the hindtibia and hindtarsi about five times. The secretion is transferred onto the surface of the egg while the female spins the egg around 360°. During this treatment, the egg remains glued to the plant surface. The egg is moved around by the hindleg, which has been touching the Pendergrast’s organs, while the other hindleg gives support to the distal end of the egg, where it is glued to the plant surface. A typical egg-clutch of Cyphostethus tris- sults in a rotation of the male genitalia seg- triatus comprises 14 eggs, which are arranged Fig. 9: Diagram showing the ments of 180°. While the tail-to-tail copula- in two parallel rows on a needle of Juniperus homologization of grooming behaviour tion position is kept for several hours, the communis (see Tab. 2). The number of eggs with egg-smearing behaviour in per clutch corresponds well with the num- Acanthosomatidae (Pentatomoidea) and couple is able to walk around. Typically, the Apiomeris flaviventris (Reduviidae). As the female goes in front with the male walking ber of ovarioles. Each of the two ovaries of egg-smearing behaviour in both taxa are backwards. When not walking around, the Cyphostethus tristriatus is composed of seven derived from the grooming behaviour, but telotrophic ovarioles, each producing at the smearing behaviour itself is not male and female hold their abdomens in an least four eggs. At a given time, fourteen homologous, this case qualifies as an elevated position, forming an angle of about example of homoiology (refer to text for 30°. During these periods, the couple per- eggs are within a corresponding develop- further information and discussion). forms jerky vertical and faint lateral body mental stage. movements. Finally, the female drums the However, there are deviations from the male pregenital abdominal segments with number of fourteen eggs within the egg- her hindtarsi. During 16 hours of observa- clutch and from the arrangement of the tion on four mating pairs, neither the male clutch. Two egg-clutches were laid onto the nor the female was ever observed touching plain surface of the insect boxes. These two the Pendergrast’s organs. Pendergrast’s or- clutches lacked the typical arrangement of gans were not involved in mating behaviour the eggs in two rows. This may indicate that or copulation. the needle of Juniperus is essential to provide

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some structural guidance for female thosomatidae bear unique symbiont transfer Figs 10-12: Morphology of Pendergrast’s organs of female Elasmostethus Cyphostethus tristriatus to produce a two-row organs (ROSENKRANZ 1939; FISCHER 1993). interstinctus (Acanthosomatidae) egg-clutch. In those cases where the female A fold of the second valviferes enveloped by (10) SEM-photograph of pregenitalia laid fewer than 14 eggs she might have been the first valviferes forms this paired struc- segments VI and VII. There are less bristles disturbed and was consequently not able to ture. on the abdominal segment VI than on the lay a 14 egg clutch. abdominal segment VII (11) The ductules of the subepidermal gland cells open into Presence of Pendergrast’s organs in pores (glop) between the bristles. Placement of symbiont droplet Acanthosomatidae-species (12) semi-thin-section of Pendergrast’s The placement of the symbiont droplet The presence of Pendergrast’s organs in organs. Epidermis underlaying the setose area of the Pendergrast’s organs is much has never been taken into consideration to Acanthosomatidae has been recorded and thicker (arrows) (modified from FISCHER be involved with the Pendergrast’s organs. studied by numerous authors (BREDDIN 1993). Glop = pore opening of gland cells, As the present study aimed to describe the 1903; PENDERGRAST 1953; KUMAR 1974; Po = Pendergrast’s organs, S = stigma, Trb = trichobothria. whole process of oviposition of Cyphostethus ROLSTON & KUMAR 1974; THOMAS 1991; tristriatus, the placement of the symbiont FISCHER 1993,1994a, 1994b, 2000; ZHENG & droplet was carefully observed. There is no WANG 1995; CARTER & HOEBEKE 2003). evidence of any involvement of the Pender- Since then, several new Acanthosomatidae grast’s organs in the symbiont droplet trans- species have been described. fer. For the first time, a list of acanthoso- Shortly after the egg is deposited, a matid species is presented referring to the brown secretion sac becomes visible, which presence of Pendergrast’s organs. So far, this issues from the female genital opening. The is the most comprehensive data available of brown sac is moved under the egg using the Pendergrast’s organs in Acanthosomatidae. hindlegs. The brown sac contains mi- Table 1 includes data from literature as well crosymbionts, which are essential for the as results of my own studies. The data of hatched nymph (MÜLLER 1956). Immedi- species, which had been studied by others, ately after hatching, the nymphs suck on were checked as far as specimens were avail- the contents of the brown sac. Before the able. Tab. 1 also includes acanthosomatid next egg is issued, the female moves fore- species, where data with respect to the Pen- Tab. 2: Egg-clutch size of Cyphostethus and backward repeatedly touching the just dergrast’s organs is not available. In most of tristriatus. deposited egg with the bristles of the geni- Egg-clutch no. Number of eggs Shape of clutch Egg-clutch attached to talia plates. 1 14 two parallel rows needle of J. communis The placement of the microsymbionti- 2 14 two parallel rows needle of J. communis cal sac in Acanthosomatidae differs from 3 12 two parallel rows needle of J. communis that of Pentatomidae. In Pentatomidae the 4 9 two parallel rows needle of J. communis microsymbiontical droplet is placed in the 5 14 two parallel rows needle of J. communis gap between the eggs. In contrast to other 6 3 not arranged insect box pentatomoid Heteroptera, females of Acan- 7 16 + 4 not arranged insect box

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ever, there are several deviations from this stem-species pattern. In all these species, ex- cept two, we find a reduced number of Pen- dergrast´s organs. Pendergrast’s organs are present only on the abdominal segment VI in four Amphaces-species (Figs 13-15). How- ever, KUMAR (1974) noted Elasmostethus nebulosum and Monteithiessa distincta also possess this condition, but I have been un- able to verify these data. In all of the investigated species of Abu- lites, Aesepus, Duadicus, Microdeuterus (Fig. 19), Nopalis, Sangarius, Stauralia and Tolono, Pendergrast’s organs are present only on the abdominal segment VII. While most of the species of the genus Lindbergicoris resemble the stem-species pattern of Acanthosomati- dae with respect to the Pendergrast’s organs, L. pulchellus, L. elegantulus and L. elegans have Pendergrast’s organs only on abdominal segment VII. In contradiction to KUMAR (1974), Pendergrast’s organs in Galgacus labidus are only present on abdominal segment VII based on my own observations. In species of the genera Agamedes, Bebaeus, Catadipson, Mahea, Phorbanta, Elasmucha, Ibocoris, Proctophantasta (Figs 20-21), and Uhlunga, Pendergrast’s organs are totally absent. Sniploa obsoletus and Praesus incarnatus are unique with regard to the number and shape of setose areas. In Sniploa obsoletus the setose area of the Pendergrast’s organs not only covers the abdominal segments V, VI and VII, but also forms a uniform, single area (Fig. 22). Praesus incarnatus differs from all other Acanthosomatidae in having two setose patches on each side of abdominal Figs 13-18: Pendergrast’s organs on female these cases, females were not present in the segment VII, but lacks setose areas on any pregenitalia segments of studied collections or specimens were of Acanthosomatidae (13) ventral view of other abdominal segments. I have not been questionable condition. abdomen of Amphaces ferruginea able to check any specimens of Praesus in- (14) Pendergrast´s organs of Amphaces The results of this study corroborate carnatus and the description of KUMAR ferruginea on abdominal segment VI with raised cuticular ring (15) ventral view of most of the data of previous investigations, (1974) does not reveal any further details. abdomen of Amphaces elongata but reveal some conflicts and contradic- Therefore, it is pure speculation whether (16-18) lateral view of abdomen tions. In Acanthosomatidae, Pendergrast’s the pair of setose areas develops from a sin- (16) Ea australis (17) Xosa lugubris organs can be present on the female abdom- gle patch, which became divided during on- (18) Esbenia minor. inal sterna of segment V, VI and VII. Near- togenesis or is the result of duplication. ly half of the investigated Acanthosomati- dae-species have Pendergrast’s organs on ab- Setose areas on the abdominal dominal segments VI and VII. This charac- segments of male Acanthosomatidae ter state represents the stem-species pattern While this study deals with the setose of Acanthosomatidae based on cladistic areas of Pendergrast’s organs of female analyses (FISCHER 1993, 1994, 2000). How- Acanthosomatidae, it is noteworthy to

1048 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at mention some unique features of the male abdomen found in two acanthosomatid species. In Panaetius lobulatus both sexes possess setose areas on the posterior pregen- italian segments. While Pendergrast’s organs are present on the female abdominal segments VI and VII (Figs 23, 24), setose areas are also present on the male abdominal segments V, VI and VII (Figs 25, 26). The setose areas of the male Panaetius lobulatus specimens resemble the morphology of the female Pendergrast’s organs. The male setose areas are shallow grooves with numerous bristles and pores. These similarities with the Pendergrast’s organs of the female might allow us to assume that the male setose areas have a glandular character. In contrast to the female setose areas, the males have an additional paired setose area on abdominal segment V. There are no de- tailed morphological, chemical, or behavioural studies. STADDON (1990) described male sternal pheromone glands in Acantho- of Mochus fortis and there is no data avail- Figs 19-22: Transformations of somatidae from Great Britain. However, able on the presence of Pendergrast’s organs Pendergrast’s organs within the these glands are typically present on the pre- Acanthosomatidae (19) ventral view of the in female Mochus fortis (see Tab. 1). abdomen of Microdeuterus megacephalus. genital segments V and VI. In male Acan- Although I discuss a similar function of Only a small, paired setose area is present thosoma haemorrhoidale and Elasmucha grisea on the abdominal segment VII gland areas are present on the sterna of the the male setose areas to the female Pender- (20) lateral view of the abdomen of abdominal segments III, IV, V, and VI. In grast’s organs at least for Panaetius lobulatus, Proctophantasta pahangiensis. another likely hypothesis may be that these Pendergrast’s organs are absent. Procto- contrast to the setose areas of male Panaetius phansta is closely related to Elasmucha, lobulatus, the sternal gland areas of male areas produce pheromones, which may play which perfom maternal care (21) lateral Acanthosoma haemorrhoidale, Cyphostethus an important role during the mating behav- view of abdomen of Proctophantasta colax tristriatus, Elasmostethus interstinctus, and iour. Sternal abdominal gland areas are de- (22) lateral view of the abdomen of scribed as occurring in both sexes of diverse Sniploa obsoletus. Note the extended Elasmucha grisea bear neither bristles nor setose area, which covers the abdominal shallow grooves. Pentatomoidea (CARAYON 1981; STADDON segment V, VI and VII. This is an unique 1990). It will be a subject for future investi- feature within the Acanthosomatidae. As nothing is known about the biology gations to address these interesting ques- Panaetius lobulatus of , an ad hoc hypothesis tions. that the male setose areas do have a similar function as proposed for the females is no more than speculation, but can provide Discussion some interesting predictions on the male be- It is evident from this study on the mat- haviour. The males of Panaetius lobulatus ing and oviposition behaviour of Cypho- should perform paternal investment by stethus tristriatus that Pendergrast’s organs transferring their own secretion to the fe- function only within the context of oviposi- male or directly onto the eggs. tion. The same behaviour is known from Another unique feature of the male ab- two other European and one North Ameri- domen is found in Mochus fortis. A long, in- can acanthosomatid species: Acanthosoma clined groove is present on the abdominal haemorrhoidale (FISCHER 1993), Elasmo- segment V (Fig. 27). The groove starts with stethus interstinctus (Fischer unpubl.), and a slight impression until it reaches its deep- Elasmostethus atricornis (CARTER & HOEBEKE est point in the segment midline. The shape 2003). Although some questions on the bio- and proportions resemble those of the hind- logical role of the Pendergrast’s organs still tarsus. Nothing is known about the biology remain unanswered, two major aspects of

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Some characters can have a main function and one or more additional functions. In evolutionary terms, we assume that both functions were present in the past, with the main function preceding the additional function. In some cases the main function can be reduced or totally lost and it is only the additional function that persists. The concept of homology and evolutionary transformation can be applied to all properties of organisms. As behavioural characters are properties of an organism, we can make hypotheses on the homology of behavioural characters. The oviposition of Acanthosomatidae is composed of several behavioural aspects and morphological structures. Females touch the setose areas of their Pendergrast’s organs, rubbing the tarsi onto the eggs, spinning the egg and finally placing the symbiont sac under the egg. This reveals that the hind legs are used in a rather elaborate way. On the morphological side, we have to note the evolution of sternal abdominal glands and the setose areas to hold and store the secretion. How did this complex of behaviour and structure evolve? To take this question a step further: What was first: behaviour or structure? An answer to this question can be given easily as it is true for nearly all organisms. Most evolutionary changes start with a change of behaviour. But what did each component of this behavioural-morphologi- Figs 23-27: Setose areas of female and the Pendergrast’s organs are clear: the bio- cal complex of oviposition of Acanthoso- male Acanthosomatidae (23) ventral view logical context and morphological-behav- matidae derive from? In order to address this of the female abdomen of Panaetius question, the oviposition complex has to be lobulatus (24) lateral view of the female ioural function. These two results provide a taken in pieces (Fig. 9). abdomen of Panaetius lobulatus sound basis for addressing one of the always- (25) ventral view of the male abdomen of new „old“ questions of evolutionary biolo- Panaetius lobulatus (26) lateral view of the Homology of behavioural elements in male abdomen of Panaetius lobulatus gists: How did this complex of structures oviposition (27) lateral view of the male abdomen of and behaviour evolve? Mochus fortis. Abdominal segment V has Oviposition of acanthosomatid species is composed of several behavioural ele- an inclining groove. Evolution of smearing behaviour is ments. In fact, there are two main sub-com- derived from grooming plexes: deposition of the egg and applying Every morphological structure and be- the secretion of the Pendergrast’s organs on- havioural character is used in a specific bio- to the eggs. In evolutionary terms, the logical context. Behavioural characters are placement of an egg within the clutch is properties of an organism just like morpho- achieved by the position of the genitalia logical characters are properties of an organ- opening and the hindlegs to arrange the ism. Both are subject to natural selection. form of the clutch is a common shared char-

1050 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at acter of pentatomoidean taxa. Females pro- As the Pendergrast’s organs on the abdomi- duce an egg clutch in which the eggs are nal segment VII are an apomorphy of the carefully arranged in parallel rows. The stem-species of Acanthosomatidae + Le- hindlegs are used to place an egg next to the stoniidae the behavioural elements in trans- previously deposited egg. Sensilla on the ferring the secretion have to be considered genital plates seem to play an important role as an apomorphy of the stem-species of in achieving the complex egg clutch Acanthosomatidae + Lestoniidae too. Rub- arrangement. As soon as the egg is placed in bing the hindlegs across the abdomen has to the right position the female touches the be homologised with grooming (main func- egg clutch with her genital plates while tion) and the transfer of Pendergrast’s or- moving her body for- and backwards and gans secretion is an additional function swinging from left to right. Eventually the which evolved in the common ancestral lin- female moves her body slightly forwards and eage of Acanthosomatidae + Lestoniidae. either to the left or to the right, depending where the next egg is going to be placed Evolution of Pendergrast’s organs within the clutch. As described in detail in the morpholo- The second sub-complex of oviposition gy section, Pendergrast’s organs are a com- in Acanthosomatidae refers to the applica- plex of abdominal epidermal glands with tion of the secretion of the Pendergrast’s or- pores opening into abdominal grooves. Nu- gans onto the eggs. In this section, I will merous bristles hold the secretion, which is particularly focus on the behavioural ele- taken up by the hindtarsi. Epidermal glands ments. After the egg is deposited on the leaf, are present in all insects. Many pentatomoid the female rubs the Pendergrast’s organs on Heteroptera have sternal gland complexes her abdomen with her hind legs. With the on the abdominal segments (CARAYON hindtarsi she takes up and transfers the se- 1981; STADDON 1990). Sternal abdominal cretion onto the eggs. This behaviour re- glands may be already present in the stem- sembles the grooming behaviour of other species of Acanthosomatidae + Lestoniidae. Heteroptera (FISCHER & ZAKRZEWSKI 2005). Using the hindtarsi for grooming and ovipo- Bugs are grooming their abdomen with their sition it may have occurred that particles hindlegs (Figs 7, 8). The hindlegs start rub- from the abdomen have been transferred to bing across the abdomen. Numerous bristles eggs, but also secretion from the sternal ab- on the hindtarsi function as a brush to wipe dominal glands. In the beginning, the secre- off dirt and other particles from the abdom- tion of these glands should have small effect inal sternites and pleurites. The hindlegs on the eggs. However, they should not de- even reach the abdominal tergites and crease the viability of eggs. Within the pop- wings. Dirt accumulated in bristles of the ulation, a variability of the secretion com- hindtarsi is brushed off by rubbing both ponents has to be assumed. Females that hindtarsi against each other. While the bugs produce secretion with protective chemical keep attached to the substrate with the fore components should have an increased fit- and middle legs, the hindlegs are totally ness. Over time, there should be an increase stretched posteriorly (Fig. 8). Both structure of females within the population producing and process of grooming behaviour and ap- protective secretion. plying the Pendergrast’s organs secretion on- Why are Pendergrast’s organs present to the eggs are very similar. Based on these solely on the posterior pregenitalic seg- similarities I conclude that the grooming be- ments? The midline of the abdominal seg- haviour and the transfer behaviour of Pen- ments VI and VII are within an area that dergrast´s organs secretion is homologous. can be reached most easily by the hindtarsi The homology of grooming behaviour during the grooming behaviour. In fact, se- and the transfer of Pendergrast’s organs setose areas of the Pendergrast’s organs cretion provokes the question which is ple- evolved first on the abdominal segment VII. siomorphic and which apomorphic. Groom- This viewpoint is supported by the recon- ing the abdomen with the hindlegs belongs structed stem-species pattern of Acanthoso- to the stem-species pattern of Heteroptera. matidae + Lestoniidae. The anterior abdom-

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inal segments are much more difficult to these African and Oriental species. reach. In fact, no Pendergrast’s organs are present on the abdominal segments II, III, Egg-clutch protection in Apiomeris IV or V. There are more species that lack flaviventris: A case of homoiology Pendergrast’s organs on the abdominal seg- Most interestingly, females of the redu- ment VI than species that lack Pender- viid Apiomeris flaviventris have similar struc- grast´s organs on the abdominal segment tures, and perform a behaviour, which shows VII. some remarkable similarities to the oviposition behaviour of Acanthosomatidae- In a next hypothetical step, grooves and species that possess Pendergrast’s organs. bristles evolved. Grooves and bristles are Apiomeris flaviventris bears setose areas on its able to hold back the secretion. Additional- abdominal segments and uses camphor, ly, a bigger amount of secretion can be easi- which it takes from plants not only to hunt ly stored and picked up for use in a single prey but also to protect its eggs against pred- transfer. While the majority of acanthoso- ators and parasites (EISNER 1988). Camphor matid species have shallow grooves, some is known to be a very effective insecticide. species evolved deeper grooves. Another In contrast to the Acanthosomatidae, Api- evolutionary solution to achieve a bigger omeris flaviventris does not produce a repel- storage evolved in Sniploa obsoletus, where lent by itself, but rather is able to use a plant females possess a unique large area of Pen- repellent, which evolved to protect the dergrast’s organs (Fig. 22). The Pendergrast’s plant against insects. organs on the abdominal segments V, VI and VII is enlarged and fused to form a uni- The analogous behaviour and structures form Pendergrast’s organs. A different way of Apiomeris flaviventris and Acanthosomati- of increasing the volume of setose areas can dae can be used to support the egg-protec- be found in the genus Amphaces. The cuticle tion hypothesis proposed for Acanthoso- grooves are deeper than in other species and matidae. Moreover, the above-discussed hy- are surrounded by an additional cuticular pothesis on the evolution of egg-smearing ring (Fig. 13). Amphaces-species have Pen- behaviour in Acanthosomatidae gains fur- dergrast’s organs only on the abdominal seg- ther support. It clearly shows that compara- ment VI, while Pendergrast’s organs are ab- ble evolutionary pressure leads to similar so- sent on the abdominal segment VII. The lutions under the given constraints and pos- presence of a double pair of setose areas on sibilities of the same body plan. the abdominal segment VII in Praesus incar- Females of A. flaviventris take up cam- natus is unique in Acanthosomatidae (KU- phor fluids from plants with their tarsi and MAR 1974). However, Praesus incarnatus store them in unique setose patches on the lacks Pendergrast’s organs on abdominal seg- venter of the abdominal segments. This re- ment VI. duviid species catches prey by using its Pendergrast’s organs are totally absent in forelegs. The stored camphor fluids are ap- species of the genera Agamedes, Bebaeus, plied onto the foretibia, which exhibits an Catadipson, Elasmucha, Ibocoris, Mahea, enormous area of bristles (fossula spon- Phorbanta, Proctophantasta, and Uhlunga. giosa). Females also transfer camphor fluids The absence of Pendergrast’s organs in Elas- to their egg-clutches. The fluids are taken mucha-species correlates with the presence up by the hindtarsi rubbing across the setose of maternal care, which the females of these areas on the abdomen. species perform (FROST & HABER 1944; The egg-smearing behaviour of A. fla- STRAWINSKI 1951; JORDAN 1958b; MELBER viventris shows remarkable similarities with et al. 1980; MELBER & SCHMIDT 1984; HON- both the grooming behaviour and the smear- BO & NAKAMURA 1985; KUDO et al. 1989). ing behaviour described for Acanthosomati- The females guard their eggs and nymphs. dae. The similarities of the egg-smearing be- Catadipson, Ibocoris, Proctophantasta, and haviour of A. flaviventris with the grooming Uhlunga are closely related to Elasmucha behaviour can be easily interpreted as homol- (FISCHER 1993). Corresponding studies to ogous (Fig. 9). Arguments that are used to these of Elasmucha-species are welcome for homologize the smearing behaviour of Acan-

1052 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at thosomatidae with the grooming behaviour somatidae werden dargestellt und diskutiert. can be applied in the same manner. Howev- Das Fortpflanzungs- und Eiablageverhalten er, the egg smearing of Acanthosomatidae von Cyphostethus tristriatus wird erstmals be- and A. flaviventris is not homologous. There schrieben. Dabei zeigt sich, dass die Pender- is no support for a close relationship, i.e. sis- grast’schen Organe eine wichtige Rolle bei tergroup relationship, of A. flaviventris and der Eiablage spielen. Weibchen reiben mit Acanthosomatidae. Apiomeris flaviventris be- ihren Hintertarsen über das Borstenfeld der longs to the Reduviidae which are a subordi- Pendergrast’schen Organe, drehen das Ei nated taxon of the Cimicomorpha. Acantho- mehrmals und platzieren es mit ihren somatidae are a subordinated taxon of Pen- Hintertarsen auf der Pflanze. Das Beschmie- tatomoidea, which belong to the Pentatomo- ren der Eier mit den Sekreten der Pender- morpha, the sistergroup of the Cimicomor- grast’schen Organe bei den Acanthosomati- pha. As no further cases of such an egg- dae wird als Verhalten mit dem Putzverhal- smearing behaviour in other cimicomorphan ten der Heteropteren homologisiert. Die and pentatomomorphan species have been Evolution der Pendergrast’schen Organe described, it is most parsimonious to assume a und des damit verbundenen Verhaltens wird convergent evolution of egg-smearing in A. Schritt für Schritt erklärt. flaviventris and the Acanthosomatidae. If the hypothesis of homology of egg smearing of References these both taxa would be proposed one would be forced to assume that their last common BREDDIN G. (1903): Missdeutete und neue Hemipteren-Arten der indo-australischen stem-species would have that property, whilst Fauna. — Sitzber. Ges. naturf. Freunde Berlin it got lost in all other taxa. This is not very 5: 195-221. parsimonious. CARAYON J. (1981): Dimorphisme sexuel des glan- des tégumentaires et production de In summary the egg smearing in A. fla- phéromones chez les Hémiptères Pentato- viventris and Acanthosomatidae evolved in- moidea. — C. r. hébd. Séanc. Acad. Sci. 229 dependently, but derived from the homolo- (Série III): 867-870. gous grooming behaviour. This type of con- CARTER M.E. & E.R. HOEBEKE (2003): Biology and sea- sonal history of Elasmostethus atricornis (VAN vergent evolution based on a homologous DUZEE) (Hemiptera: Acanthosomatidae), with pattern is named homoiology. descriptions of the immature stages and notes on Pendergrast organs. — Proc. Ento- mol. Soc. Wash. 105 (3): 525-534.

Acknowledgements EISNER T. (1988): Insekten als fürsorgliche Eltern. — Verh. Dtsch. Zool. Ges. 81: 9-17. I am very grateful to Albrecht Manegold (Forschungsinstitut und Naturmuseum FISCHER C. (1993): Phylogenetisch-systematische Analyse der Acanthosomatidae (Heteroptera, Senckenberg, Frankfurt) and Antje Fischer Pentatomoidea). — Diploma thesis, Freie Uni- (Humboldt-Universität Berlin) for many versität Berlin: 1-190. stimulating discussions and comments on FISCHER C. (1994a): Phylogenetisch-systematische earlier drafts of this paper. I thank Randall Analyse der Acanthosomatidae (Heteroptera, T. Schuh (American Museum of Natural Pentatomoidea). — Verh. Dtsch. Zool. Ges. 87: 220. History, New York) and Pavel Stys (Charles FISCHER C. (1994b): Das Pendergrast Organ der University, Prague) for valuable comments. Acanthosomatidae (Heteroptera, Pentato- moidea): Schutz des Eigeleges vor Räubern und Parasiten? — Sitzber. Ges. naturf. Fre- Zusammenfassung unde Berlin 33: 129-142. Die vorliegende Studie fasst alle bisheri- FISCHER C. (2000): The disc-like organ of the Le- stoniidae (Heteroptera: Pentatomoidea), gen morphologischen Untersuchungen und with remarks on lestoniid relationships. — In- Hypothesen zur Funktion der Pendergrast’- sect Syst. Evol. 31: 201-208. schen Organe der Acanthosomatidae zu- FISCHER A. & A. ZAKRZEWSKI (2006): Das Putzverhal- sammen. Zum ersten Mal wird das Vorhan- ten der Insekten unter phylogenetischen und densein von Pendergrast’schen Organen bei evolutionsbiologischen Gesichtspunkten. — Sitzber. Ges. naturf. Freunde Berlin 44: 51-70. über 100 Acanthosomatidae-Arten aufgelis- FROST S.W. & V.R. HABER (1944): A case of parental tet. Evolutive Transformationen der Pender- care in the Heteroptera. — Ann. Ent. Soc. Am. grast’schen Organe innerhalb der Acantho- 37: 161-166.

GRAZIA J., SCHUH R.T. & W.C. WHEELER: Phylogenetic to the genera of the Western Hemisphere. — relationships of family groups in Pentato- J. N. Y. Entomol. Soc. 82 (4): 271-278. moidea based on morphology and DNA se- ROSENKRANZ W. (1939): Die Symbiose der Pentato- quences (Insecta: Heteroptera). — Cladistics, miden (Hemiptera, Heteroptera). — Z. in press. Morph. Ökol. Tiere 36: 279-309. HILKER M. (1994): Egg deposition and protection of SCHAEFER C.W. & I. AHMAD (1987): The food plants eggs in Chrysomelidae. — In: JOLIVET P.H., COX of four pentatomoid families (Hemiptera: M.L. & E. PETITPIERRE (Eds), Novel aspects of the Acanthosomatidae, Tessaratomidae, Urostyli- biology of Chrysomelidae, Kluwer Acad. Publ., Dordrecht: 263-276. dae, and Dinidoridae). — Phytophaga 1: 21- 34. HONBO Y. & K. NAKAMURA (1985): Effectiveness of parental care in the bug Elasmucha putoni STADDON B.W. (1990): Male sternal pheromone SCOTT (Hemiptera: Acanthosomatidae). — Jpn. glands in acanthosomatid shield bugs from J. Appl. Ent. Zool. 29: 223-229. Britain. — J. Chem. Ecol. 16 (7): 2195-2201.

JORDAN K.H.C. (1958): Die Biologie von Elasmucha STRAWINSIKI K. (1951): Biology of Elasmucha ferru- grisea L. (Heteroptera: Acanthosomatidae). gata. — Ann. Un. M. Curie-Sklod. 6: 149-164. — Beitr. Ent. 8: 385-397. THOMAS D.B. (1991): The Acanthosomatidae (Het- KMENT P. (2005): Revision of Mahea DISTANT, 1909, eroptera) of North America. — Pan-Pacif. En- with a review of the Acanthosomatidae (In- tomol. 67: 159-170. secta: Heteroptera) of Madagascar and Sey- ZHENG L. & H. WANG (1995): Contribution to the chelles. — Acta Entomol. Mus. Nat. Pragae taxonomy of Lindbergicoris LESTON (Hemi- 45: 21-50. ptera: Acanthosomatidae). — Ent. Scand. 26: KUDO S., SATO M. & M. OHARA (1989): Prolonged 17-26. maternal care in Elasmucha dorsalis (Het- eroptera: Acanthosomatidae). — J. Ethol. 7: 75-81.

KUMAR R. (1974): A revision of world Acanthoso- matidae (Heteroptera: Pentatomidae): Keys to and descriptions of subfamilies, tribes and genera, with designations of types. — Austr. J. Zool. (Suppl. Series) 34: 1-60.

MAPPES J. & A. KAITALA (1994): Experiments with Elasmucha grisea L. (Heteroptera: Acanthoso- matidae). Does a female parent bug lay as many eggs as she can defend? — Behav. Ecol. 5: 314-317.

MELBER A. & G. SCHMIDT (1975): Sozialverhalten zweier Elasmucha-Arten (Heteroptera: Insec- ta). — Z. Tierpsychol. 39: 403-414.

MELBER A., HÖLSCH L. & G. SCHMIDT (1980): Further studies on the social behaviour and its eco- logical significance in Elasmucha grisea L. (Hem.-Het.: Acanthosomatidae). — Zool. Anz. 205: 27-38.

MELBER A. & G. SCHMIDT (1984): Das Sozialleben der Wanzen. — Spektrum der Wissenschaft, Feb- ruar: 110-121.

MITTER C., FARRELL B. & B. WIEGMANN (1988): The phylogenetic study of adaptive zones: has phytophagy promoted insect diversifications? — Am. Nat. 132: 107-128.

MÜLLER H.J. (1956): Experimentelle Studien an der Symbiose von Coptosoma scutellatum GEOFFR. Address of the Author: (Hem. Heteropt.). — Z. Morph. Ökol. Tiere 44: 459-482. Dr. Christian FISCHER

PENDERGRAST J.G. (1953): Setose areas on the ab- Freie Universität Berlin domen in female of some Acanthosominae Institut für Biologie / Zoologie (Heteroptera, Pentatomidae). — The Ento- Evolutionsbiologie mologist 86: 135-138. Königin-Luise-Str. 1-3 ROLSTON L.H. & R. KUMAR (1974): Two new genera and two new species of Acanthosomatidae 14195 Berlin, Germany (Hemiptera) from South America, with a key E-Mail: [email protected]

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