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Turkish Journal of Zoology Turk J Zool (2014) 38: 491-499 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1312-30

New teratological cases in and ()

1 1, 2 Ovidiu Alin POPOVICI , Mircea-Dan MITROIU *, David G NOTTON 1 Faculty of Biology, Alexandru Ioan Cuza University of Iaşi, Iaşi, Romania 2 Department of Life Sciences, Terrestrial Invertebrates Division, Darwin Centre, The Natural History Museum, London, UK

Received: 16.12.2013 Accepted: 27.02.2014 Published Online: 20.05.2014 Printed: 19.06.2014

Abstract: Very few cases of teratological specimens, i.e. specimens displaying morphological abnormalities, have been cited among Platygastridae and Pteromalidae. From the Platygastridae we present 5 cases of symphysocery [A8–A9 in Metaclisis sp.; A3–A5 and A7–A9 in Sceliomorpha sp.; A5–A6 in Scelio sp. 1; A9–A10 in Idris sp., and a completely modified antenna in Gryon monspeliense (Picard 1924)]; a helicomery in Opisthacantha sp.; a hypertrophied interantennal prominence and central keel in Triteleia peyerimhoffi (Kieffer 1906); a schistocery concerning A5 in Apegus sp.; and a gynandromorph specimen of Scelio sp. 2. In the Pteromalidae we found 2 cases of symphysocery in Systasis parvula (Thomson 1876) (A4–A5 and A5–A9) and 1 inPteromalus sp. (A8–A10); 1 case of hypertrophy concerning the antennomeres in S. parvula (A5) and 1 in Norbanus africanus Subba Rao 1973 (A6–A8); 1 case of cyclopy and head asymmetry in N. africanus; and 1 petiole asymmetry in Sphegigaster sp.

Key words: Parasitoid, Platygastridae, Pteromalidae, morphological abnormality, asymmetry, cyclopy, schistocery, symphysocery, helicomery, hypertrophy

1. Introduction was not neglected in the Parasitica, e.g., The families Platygastridae and Pteromalidae consist of (Pisică, 1966; Bordera and Tormos, 1986; Penteado-Dias small to very small that live as parasitoids of the et al., 2005), and was even studied in microhymenoptera, immature stages of and arachnids. Because of their e.g., (Ceballos, 1921; Ogloblin, 1936; biology, some members of these families are important Szabó, 1959; Bin, 1972, 1976; Sveum, 1980; Hilpert, agents in the biological control of pests (Orr, 1988; Bouček 1985; Rajmohana and Narendran, 1999), Chalcidoidea and Rasplus, 1991). (Caltagirone, 1970; Beserra et al., 2003; Pereira et al., 2003; Teratology is the study of malformations (Asiain and Zhang and Zhu, 2007), and (Fergusson, Márquez, 2009). The problem of teratology in insects 1978; Dessart, 1993). was largely debated by Balazuc (1948, 1958, 1969), Until now, very few teratological specimens of who provided a classification of and terminology for Platygastridae have been published: Fabritius (1968) different morphological abnormalities found in this described a male Trimorus algicola (Kieffer, 1911) from group of . Balazuc (1948, 1958) considered Romania that had a monocyclic helicomery of the second these abnormalities “monstruosités”. Perhaps the best- metasomal tergite; Safavi (1968) noted some antennal known and most well-studied type of teratology is gynandromorphy, which has been found in almost all malformations in Trissolcus grandis (Thomson, 1860); major groups of insects. Huggert (1977) found 3 gynandromorphic specimens of Teratology in Hymenoptera was discussed extensively Idris piceiventris (Kieffer, 1908), and Popovici et al. (2011) by Balazuc (1958). This phenomenon has been studied found a female Triteleia peyerimhoffi (Kieffer, 1906) with more thoroughly in larger Hymenoptera, e.g., the interantennal prominence hypertrophied. Among (Laidlaw, 1932; Leclercq, 1953; Fyg, 1964; Akre, 1982; the Pteromalidae, the published cases of teratological Nilsson, 1987; Celary and Wisniowski, 2001; Engel, 2007; specimens are even scarcer. From the thousands of Lucia et al., 2009; Michez et al., 2009) and specimens examined, Graham (1969) mentioned only 1 (Berndt and Kremer, 1983; Acosta and Martinez, 1984; example of a teratological specimen, a male of Miscogaster Berndt and Wisniewski, 1984; Borsato, 1995; Eck, 1998), but elegans Walker, 1833. * Correspondence: [email protected] 491 POPOVICI et al. / Turk J Zool

The aim of this paper is to give a brief overview of the For Idris, Gryon, Scelio, Metaclisis, Systasis, and presence of teratological specimens among Hymenoptera Pteromalus, both antennae were removed and mounted in and to present new cases of such specimens from the Canada balsam. For Gryon and Scelio the aedeagus and the families Platygastridae and Pteromalidae, about which ovipositor and ovary, respectively, were also mounted on very few examples have been published so far. microscope slides. After removal of the antennae, the body of each specimen was mounted on triangular or rectangular 2. Materials and methods cards. Card-mounted specimens and appendages on slides The terminology of abnormalities follows Balazuc (1958) were photographed using a Leica DFC500 digital camera on and Michez et al. (2009), except for the term “schistocery”, a Leica 205A stereomicroscope. The acquired images were proposed by us as an opposite of “symphysocery” in then processed with Zerene or Helicon Focus software and order to illustrate the division of an antennomere in 2 or their clarity was further enhanced using Adobe Photoshop more new antennomeres. Morphological terms used in CS3. The antennomeres are abbreviated A1–A13 starting this paper were matched to the Hymenoptera Anatomy from the scape and the gastral tergites T1–T7. Ontology Portal (HAO; Yoder et al., 2010; Seltmann et al., 2012). Identifiers (URIs) represent anatomical concepts in 3. Results the HAO (Table 1). The teratologies observed in 8 genera of Platygastridae and The specimens used in this study (Table 2) are kept in 4 genera of Pteromalidae are summarized in Table 2 and the personal collections of O Popovici (OPPC) and MD detailed below. Mitroiu (MICO), except for the specimen of Triteleia Platygastridae (Figures 1–21) peyerimhoffi, which is in the Canadian National Collection Apegus sp. of Insects, Arachnids and Nematodes, Ottawa, Canada In 1 male, the A5 (“sex-segment”) is divided into (CNC), and the 2 specimens of Norbanus africanus, which 2 segments (schistocery) (Figures 19 and 20), so both are in the collection of the Natural History Museum, antennae are 13-segmented; in normal specimens the London, UK (BMNH). number of antennomeres is 12. The division of A5 can

Table 1. Morphological terms used in the paper and their corresponding identifiers in the HAO.

Term URI aedeagus http://purl.obolibrary.org/obo/HAO_0000091 anellus http://purl.obolibrary.org/obo/HAO_0000287 antenna http://purl.obolibrary.org/obo/HAO_0000101 antennomere http://purl.obolibrary.org/obo/HAO_0000107 basiconic capitate peg sensilla http://purl.obolibrary.org/obo/HAO_0000172 eye http://purl.obolibrary.org/obo/HAO_0000217 frons http://purl.obolibrary.org/obo/HAO_0001523 gaster http://purl.obolibrary.org/obo/HAO_0000369 head http://purl.obolibrary.org/obo/HAO_0000397 laterotergite http://purl.obolibrary.org/obo/HAO_0001861 ovipositor http://purl.obolibrary.org/obo/HAO_0000679 pedicel http://purl.obolibrary.org/obo/HAO_0000706 petiole http://purl.obolibrary.org/obo/HAO_0000020 scape http://purl.obolibrary.org/obo/HAO_0000908 sternite http://purl.obolibrary.org/obo/HAO_0000955 tergite http://purl.obolibrary.org/obo/HAO_0001005 tyloid http://purl.obolibrary.org/obo/HAO_0001199

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Table 2. Specimens examined.

Species Type of anomaly Collection data Platygastridae Apegus sp. ♂ Schistocery ESTONIA: Sõõru, 13–27.viii.2011, leg. V. Soon (OPPC-PAp01) ROMANIA: Tulcea, Macin Mountains, 23.vii.2004, sweep net, leg. M.-D. Gryon monspeliensis ♂ Symphysocery Mitroiu (OPPC-PGr01) ROMANIA: Iasi, Botanical Garden, 2.viii.2004, sweep net, leg. O. Idris sp. ♂ Symphysocery Popovici (OPPC-PId01) ROMANIA: Iasi, Botanical Garden, 28.iv.2005, sweep net, leg. O. Metaclisis sp. ♂ Symphysocery Popovici (OPPC-PMe01) JAPAN: Hokkaido, Soranuma-dake, Sapporo-shi, 27.vii.–21.viii.2007, Opisthacantha sp. ♂ Helicomery Malaise trap, leg. A. Ueda (OPPC-POp01) ROMANIA: Constanta, Vadu, 27.viii.2004, sweep net, leg. O. Popovici Scelio sp. 1 ♂ Symphysocery (OPPC-PSc01) UGANDA: Kibale N.P. Kanyawara Biol. Station, 22–29.viii.2010, Scelio sp. 2 Transversal gynandromorphy Malaise trap, leg. Katusabe & Co. (OPPC-PSc02) FRENCH GUIANA: Kaw Mountains, 17.ix.–2.x.2006, Malaise trap, leg. Sceliomorpha sp. ♂ Symphysocery K. Sarv (OPPC-PScl01) Triteleia peyerimhoffi♀ Hypertrophy HUNGARY: Veröce, 2–18.ix.2005, Malaise trap, leg. Z. Nyiro (CNC) Pteromalidae KENYA: Machakos dis., Kiboko, 1000 m ex larva Chilo sp. in maize Norbanus africanus ♀ Cyclopy; asymmetry stem, coll. 26.ix.1990, M.J.W. Cock (BMNH) KENYA: Machakos dis., Kiboko, 1000 m ex larva Chilo sp. in maize Norbanus africanus ♀ Hypertrophy stem, coll. 26.ix.1990, M.J.W. Cock (BMNH) ROMANIA: Iasi, Ciric izvor, meadow, 30.vii.2007, leg. O. Popovici Pteromalus sp. ♀ Symphysocery (MICO-310)

Sphegigaster sp. ♀ Asymmetry ROMANIA: Vaslui, Poienesti, clearing near forest, 15.07.94 (MICO-S31)

ROMANIA: Botosani, Vorona, alfalafa flowers, 31.viii.2006, leg. C. Systasis parvula ♀ Symphysocery; hypertrophy Lisenchi (MICO-309) ROMANIA: Neamt, Varatec, veg. nr. stream, 18.07.1999, leg. M.-D. Systasis parvula ♂ Hypertrophy Mitroiu (MICO-47) be seen only on the ventral side, the dorsal side being constituent antennomeres. The fused antennomeres are undivided. A9–A10 are also fused in both antennae wider than the normal ones from the male antenna, so in (Figures 19 and 21). the malformed antenna, the fused antennomeres look like Gryon monspeliense (Picard 1924) the clava of a female antenna. Other than the left antenna, One male has the left antenna modified (Figure 7), the specimen looks perfectly normal. whereas the right antenna is normal (Figure 12). In this Idris sp. case the left antenna is 1.2 times shorter than the right One male has a symphysocery affecting A9–A10 of the antenna. Additionally, for the left antenna, only the scape left antenna (Figure 13). In this case, A9–A10 are fused, (A1) and the pedicel (A2) are separate, and all the other but a trace of the division between them can be observed antennomeres are fused: A3 is fused with A4 without a (Figure 20). Except for the fusion of these antennomeres, clear division between them and A5–A12 also are fused in there are no other differences between the teratological a mass in which it is almost impossible to distinguish the antenna and normal one (Figure 8).

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Figures 1–13. Teratological Platygastridae. 1, 2, Metaclisis sp., male: 1. teratological antenna, 2. normal antenna; 3, 4, 9, Sceliomorpha sp., male: 3. teratological antenna, 4. normal antenna, 9. habitus in lateral view, with teratological antenna; 5, 6, Scelio sp. 1, male: 5. teratological antenna; 6. normal antenna; 7, 12, Gryon monspeliense, male: 7. teratological antenna; 12. normal antenna; 8, 13, Idris sp., male: 8. normal antenna, 13. teratological antenna; 10, 11, Triteleia peyerimhoffi, female: 10. head detail of normal specimen, 11. head detail of teratological specimen.

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Figures 14–21. Teratological Platygastridae. 14, 15, Opisthacantha sp., male: 14. habitus of teratological male in dorsal view, 15. detail with helicomery of metasoma; 16–18, Scelio sp. 2, gynandromorph specimen: 16. habitus in lateral view, 17. left antenna, 18. right antenna; 19–21, Apegus sp., male: 19. teratological antenna, 20. detail of A5, 21. detail of A9–A10.

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Metaclisis sp. A8, A10, and A11 are noticeably shorter, while A2–A6 and One male has a symphysocery affecting A8–A9 of the A8 are wider than the corresponding antennomeres of the left antenna. The fusion between these antennomeres is left antenna. Thus, for Sceliomorpha, in the teratological complete, with no traces of articulation, except for a small antenna, the affected antennomeres are shorter and wider depression in the middle of the newly formed segment. than the normal antennomeres, and the tyloids from A4 The length of the teratological antenna is slightly shorter and A5 seem to be modified, being morphologically closer than the length of the normal one; this is largely due to the to the basiconic capitate peg sensilla that are present on the length of the fused antennomeres (A8–A9) being shorter female antenna. than the length of A8 and A9 taken together in the normal Triteleia peyerimhoffi (Kieffer, 1906) antenna. A4 of the normal antenna has a more expanded One female has a hypertrophied interantennal outer apical corner than in the teratological antenna prominence and central keel on the frons (Popovici et al., (Figure 1). In the teratological antenna, the width of A4 2011). In the affected female, the distance between toruli is and A5 is a little smaller than the width of A4–A5 in the almost twice that in the normal specimens. Except for this normal antenna, and, by contrast, the width of A6–A10 is malformation, the rest of the specimen is perfectly normal a little bit greater than the width of the same antennomeres (Figures 10 and 11). in the normal antenna (Figure 2). Pteromalidae (Figures 22–30) Opisthacantha sp. Norbanus africanus Subba Rao 1973 One male with a helicomery affecting the second and Cyclopy and head asymmetry can be observed in one third gastral tergites (T2–T3) was observed, the limit female that has only the right compound eye present, the between these tergites being almost impossible to establish left being completely absent (Figure 23). The area where (Figures 14 and 15). The rest of the gaster is unaffected. The the eye should have been displays normal sculpture, except sternites are not affected, but the second right laterotergite for a tiny oval structure, and has the same coloration as the has a well-developed overlap over a very small area of the rest of the head capsule; however, this side of the head is second sternite. evidently smaller (less high) than the right side. Another Scelio sp. 1 female from the same sample displays a hypertrophy of One male has the A5–A6 of the right antenna connected A6–A8 of the left antenna, each of these antennomeres by a weak sclerotized membrane (Figure 5). While the being distinctly swollen and darker compared to the antennomeres can still be distinguished, they appear to corresponding antennomeres of the right antenna (Figure be rigidly joined, so there is no functional articulation. In 22). this case, the teratological antenna is not so different in Pteromalus sp. size from the normal one, with only negligible differences One female is characterized by a symphysocery between the length of the 2 antennae and between the length and width of the corresponding antennomeres affecting A8–A10 of the right antenna (Figure 25), the left (Figure 6). one being normal (Figure 26). The 3 antennomeres are Scelio sp. 2 fused only on the ventral side; on the opposite side their One gynandromorph specimen (Figure 16) was limits are clearly visible (Figure 25). identified (transversal gynandromorphy). It looks like Sphegigaster sp. a female, but both antennae are 10-segmented (Figures One female has the gastral petiole clearly asymmetric 17 and 18). In Scelio, the number of antennomeres is and wider than normal. The asymmetry is especially visible dimorphic (10 in males and 12 in females). The ovipositor at the level of the 2 lateral projections of the petiole and at and ovaries were found by dissecting the specimen. The its connection with the gaster (Figure 24). right antenna does not differ from a male antenna (Figure Systasis parvula (Thomson, 1876) 18), but the left one is slightly wider (Figure 17), being One female has both antennae affected by intermediate in shape between a male and female antenna. malformations. The right antenna (Figure 28) has a Sceliomorpha sp. symphysocery affecting all funicular segments (A5–A9), One male shows a double symphysocery of the right while the left antenna has a symphysocery affecting A4– antenna (Figures 3 and 9). This malformation affects A3– A5 and a hypertrophy of A5, which appears as if another A5 and A7–A9 (Figure 3). The malformed right antenna is antennomere is fused laterally with it (Figure 27). One shorter (2.2 mm without scape) than the normal antenna male has a hypertrophy of A5 at the level of the left antenna (2.6 mm without scape). A3–A5 are completely fused (Figure 29). However, the 2 anelli cannot be observed, on the dorsal side, but on the ventral side a trace of the which may also indicate a symphysocery affecting A3–A5. articulations between them can be seen. A7–A9 are not as Additionally, the pedicel (A2) looks displaced (Figure 29). modified as A3–A5. In the teratological antenna A2, A4– The right antenna is normal (Figure 30).

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Figures 22–30. Teratological Pteromalidae. 22, 23, Norbanus africanus, females: 22. teratological (left) and normal (right) antennae, 23. cyclopy; 24, Sphegigaster sp., petiole asymmetry; 25, 26, Pteromalus sp., female: 25. teratological antenna, 26. normal antenna; 27, 28, Systasis parvula, female, teratological antennae; 29, 30, S. parvula, male: 29. teratological antenna, 30. normal antenna.

4. Discussion (1984), who proposed low humidity as a cause of these Teratologies among platygastrids and pteromalids have malformations, because of the reduction of fluid available not been frequently cited. This subject was no doubt to extend these appendages. Safavi (1968) found 3 causes neglected because of the small size of these wasps, but, for the appearance of malformed antenna: host eggs that even so, from our experience, teratologies appear to be were fresh but dehydrated, old host eggs, and a compression rare within these groups. Malformed specimens may also of antennae during the pupal stage. Safavi also noted that be hard to discover due to poor preparation (e.g., wings the presence of these antennal malformations strongly obscuring the metasoma or with antennae in glue or affected mating behavior: the affected wasps did not under the specimens). The causes of these malformations mate successfully, and so any hereditary component or are not clear, but are considered to be either genetic predisposition underlying these malformations could not or environmental. The presence of antenna and leg be tested. In Safavi’s experiments, only males of Trissolcus deformities was described by Berndt and Wisniewski grandis showed malformed antennae. This is similar to the

497 POPOVICI et al. / Turk J Zool examples presented above, where we found only males of the metasoma have also been a source of taxonomic with teratological antennae. errors, for example in Pteromalidae: Miscogaster elegans According to Balazuc (1948), symphysocery affecting Walker, 1833 was described by the same author under the antennomeres A6–A11 was common, A4–A5 less name Lamprotatus helenor Walker, 1846 on the basis of a common, and A3–A4 rare. In the first category we found 4 teratological specimen with the gastral petiole abnormally examples (Metaclisis, A8–A9; Sceliomorpha, A7–A9; Idris, short (Graham, 1969). A9–A10; and Pteromalus, A8–A10), in the second category In the specimens described above, the various 1 example (Systasis, A4–A5), and in the last category malformations affecting the antennae were by far the most 1 example (Gryon, A3–A4), as well as an intermediate common. Among these, symphysocery (the fusion of 2 or case (Sceliomorpha, A3–A5). Balazuc (1958) proposed as more antennomeres) seems to be the most frequent. causes of helicomery affecting metasomal terga heredity, It is difficult to assess the frequency of such exposure to ultraviolet radiation, mechanical shock, malformations in the studied groups. In a single sample abnormally high heat, and parasitoids such as Strepsiptera. from Kenya we found 2 malformed specimens, while in In the case of the Opisthacantha specimen presented hundreds of other samples no such specimens could be above, we can exclude parasitism by Strepsiptera since identified. there is no physical evidence for it and the host range of strepsipterans does not include Platygastridae. Acknowledgments Teratological antennae can be a source of taxonomic The senior author thanks his friend Takuma Yoshida mistakes, e.g., Erdős and Novicky (1955) described the (Japan), who provided the specimen from Japan; Dr new genus Birous (Hymenoptera: ) based on Villu Soon (Estonia) for the gift of specimens from the number of antennomeres. Bouček and Graham (1978), Estonia and French Guiana; and Dr Lubomir Masner however, found that the type specimen of this genus is a (CNC) for his unconditional support. The second author teratological female belonging to Microterys. In the case thanks Dr Andy Polaszek (BMNH) for providing the 2 of the monotypic genus Prosinostemma Kieffer 1914, specimens of Norbanus. This study was funded by a grant Masner and Huggert (1989) stated that the genus was from the Romanian National Authority for Scientific probably established on a teratological specimen with a Research, CNCS-UEFISCDI, Project Number PN-II-RU- symphysocery affecting 2 antennomeres. Malformations TE-2012-0057.

References

Acosta FJ, Martinez MD (1984). Algunas anomalias en Leptothorax Beserra EB, Querino RB, Parra JRP (2003). Occurrence of rabaudi Bond., 1818 (Hym., Formicidae). B Asoc Espan Ent 8: gynandromorphism in Trichogramma pretiosum Riley 41–45 (in Spanish). (Hymenoptera: ). Neotrop Entomol 32: Akre RD, Catts EP, Zack RS, Klostermeyer XC (1982). 507–509. Gynandromorphs of rotundata (Fab) (Hymenoptera: Bin F (1972). Un nuovo caso di ginandromorfismo in Ashmeadopria Megachilidae). Ent News 93: 85–94. Kieffer (Hymenoptera, Proctotrupoidea, ). Entomol Asiain J, Márquez J (2009). New teratological examples in Neotropical Bari 8: 55–59 (in Italian). Staphylinidae (Insecta: Coleoptera), with a compilation of Bin F (1976). Record of a teratological Trichopria Ashm. previous teratological records. Rev Mex Biodivers 80: 129–139. (Hymenoptera. Diapriidae). Entomol Bari 12: 67–70 (in Italian Balazuc J (1948). La tératology des coléoptères et experiences de with an abstract in English). transplantation sur Tenebrio molitor L. Memoir Mus Natl Hist Bordera S, Tormos J (1986). Un braconido y tres ichneumonidos 25: 1–293 (in French). teratologicos (Hym., Ichneumonoidea). B Asoc Espan Ent 10: Balazuc J (1958). La tératologie des Hymenoptéroïdes. Ann Soc 335–338 (in Spanish). Entomol Fr 127: 167–203 (in French). Borsato W (1995). Segnalazione di una teratologia su Sulcopolistes Balazuc J (1969). Supplément à la tératologie des coléoptères. Redia sulcifer Zimmermann (Hymenoptera, Vespidae). Boll Mus Civ 51: 39–111 (in French). Stor Nat Verona 19: 453–455 (in Italian). Berndt KP, Kremer G (1983). New categories in the Bouček Z, Graham MWR de V (1978). Chalcidoidea. In: Fitton gynandromorphism of . Insectes Soc 30: 461–465. MG, Graham MWR de V, Boucek ZRJ, Fergusson NDM, Berndt KP, Wisniewski J (1984). Zur Teratologie der Korperanhange Huddleston T, Quinlan J, Richards OW, editors. A Check List bei der Pharaoameise Monomorium pharaonis (L.) of British Insects. 2nd ed. Handbooks for the Identification (Hymenoptera, Formicidae). Zool Anz 213: 313–321 (in of British Insects, Vol. XI. London, UK: Royal Entomological German). Society, pp 67–110.

498 POPOVICI et al. / Turk J Zool

Bouček Z, Rasplus JY (1991). Illustrated Key to West-Palaearctic Masner L, Huggert L (1989). World review and keys to genera of Genera of Pteromalidae (Hymenoptera: Chalcidoidea). Paris, the subfamily Inostemmatinae with reassignment of the taxa France: INRA. to the and Sceliotrachelinae (Hymenoptera: Caltagirone LE (1970). Gynandromorphism in the polyembryonic Platygastridae). Mem Entomol Soc Can 147: 1–214. encyrtid Pentalitomastix plethoricus Cali. (Hymenoptera, Michez D, Rasmont P, Terzo M, Vereecken NJ (2009). A synthesis of Encyrtidae.). Boll Lab Entomol Agrar Filippo Silvestri 28: gynandromorphy among wild (Hymenoptera: Apoidea), 98–112. with an annotated description of several new cases. Ann Soc Ceballos G (1921). Nota sobre un himenóptero ginandromorfo. Entomol Fr 45: 365–375. Mem Real Soc Esp Hist Nat 50: 79–81 (in Spanish). Nilsson GE (1987). A gynandromorphic specimen of Evylaeus Celary W, Wisniowski B (2001). An interesting case of albipes (Fabricius) (Hymenoptera, Halictidae) and a discussion gynandromorphism in Andrena helvola (L., 1758) of possible causes of gynandromorphism in haplo-diploid (Hymenoptera: Apoidea: Andrenidae). Folia Biol 49: 291–293. insects. Not Entomol 67: 157–162. Dessart P (1993). Un Conostigmus et un Ceraphron a antennes Ogloblin AA (1936). Un ginandromorfo de Acanthopria (Diapriidae, teratologiques (Hymenoptera: Ceraphronoidea). Bull Inst R Hym.). Rev Arg Ent 1: 33–36 (in Spanish). Sci Nat Belg Ent 63: 51–58 (in French). Orr DB (1988). Scelionid wasps as biological control agents: a review. Eck R (1998). A teratological report on a Polistes specimen (Insecta: Fla Entomol 71: 506–528. Hymenoptera: Vespoidea: Polistinae). Entomol Abh 58: 141– Penteado Dias AM, Fiorelini Nunes J, Mitio Shimbori E (2005). 142. Observations on some teratological Braconidae (Hymenoptera, Engel MS (2007). A lateral gynandromorph in the genus Thyreus Ichneumonoidea) from Brazil. Entomotropica 20: 113–114. and the sting mechanism in the Melectini (Hymenoptera: ). Am Mus Novit 3553: 1–11. Pereira RAS, Prado AP, Kjellberg F (2003). Gynandromorphism in pollinating fig wasps (Hymenoptera: Agaonidae). Entomol Erdős J, Novicky S (1955). Genera Encyrtidarum regionis News 114: 152–155. palaearcticae. Beitr Entomol 5: 165–200 (in Latin). Pisică C (1966). Morphologische Anomalien bei einigen Fabritius K (1968). Eine Anomalie des Abdomnens bei der Gattung Lissonotinae–und Ephialtinae–Arten aus Rumanien Trimorus (Hym., Scelionidae). An St Univ Al I Cuza Iasi 14: (Hymenoptera: Ichneumonidae). Beitr Entomol 16: 607–614 1–2 (in German). (in German). Fergusson NDM (1978). A teratological specimen of Dendrocerus Popovici OA, Bin F, Masner L, Popovici M, Notton DG (2011). carpenteri (Curtis 1829) (Hymenoptera: Ceraphronoidea). Triteleia peyerimhoffi comb. n., a remarkably variable circum- Entomol Bari 14: 25–30. Mediterranean scelionid (Hymenoptera, ). Fyg W (1964). Anomalies and diseases of the queen . Annu ZooKeys 140: 71–99. Rev Ent 9: 207–224. Rajmohana K, Narendran TC (1999). An interesting teratological Graham MWR de V (1969). The Pteromalidae of north-western Trichopria Ashmead (Diapriidae; Proctotrupoidea) from Europe (Hymenoptera: Chalcidoidea). Bull Brit Mus Nat Hist India. Zoos Print J 14: 94–96. (Ent) Supplement 16: 1–908. Safavi M (1968). Etude biologique et étologique des Hyménoptères Hilpert H (1985). Ein Fall von Gynandromorphismus bei der Wespe parasites des oeufs des punaises des céréales. Entomophaga 13: Belyta quadridens Kieff. (Hymenoptera, Diapriidae). Mitt Bad 381–495 (in French). Landesver Naturk u Naturschutz Freiburg i Br 13: 425–428 (in German). Seltmann KC, Yoder MJ, Mikó I, Forshage M, Bertone MA, Agosti D, Austin AD, Balhoff JP, Borowiec ML, Brady SG et al. (2012) A Huggert L (1977). Three gynandromorphic specimens of Idris hymenopterists’ guide to the Hymenoptera Anatomy Ontology: piceiventris (Kieffer) (Hymenoptera, Proctotrupoidea, utility, clarification, and future directions. J Hymenopt Res 27: Scelionidae). Entomol Scand 8: 158–160. 67-88. Laidlaw WBR (1932). A gynandromorphic form of Bombus, with other notes on bees and wasps in Scotland. Scott Nat 193: Sveum P (1980). A record of gynandromorphism in Basalys 25–27. Westwood (Hymenoptera, Diapriidae) from Norway. Fauna Nor B 27: 77. Leclercq J (1953). Un cas extraordinaire de gynandromorphisme chez Halictus sexcinctus (Hym. Apidae). Bull Inst R Sci Nat Szabo JB (1959). Notes on a gynandromorph Diapriid from Belg Ent 29: 1–4 (in French). Hungary (Hym. Proct. Diapr.). Folia Entomol Hung 12: 495– 496. Lucia M, Abrahamovich AH, Alvarez LJ (2009). A gynandromorph of Xylocopa nigrocincta Smith (Hymenoptera: Apidae). Neotrop Yoder MJ, Mikó I, Seltmann KC, Bertone MA, Deans AR (2010). A Entomol 38: 155–157. gross anatomy ontology for Hymenoptera. PLoS ONE 5: 1–8. Masner L (1993) Superfamily Platygastroidea. In: Goulet H, Huber Zhang YZ, Zhu CD (2007). A gynandromorph of Microterys ishiii JT, editors. Hymenoptera of the World: An Identification Guide Tachikawa (Hymenoptera: Chalcidoidea: Encyrtidae). Acta to Families. Ottawa, Canada: Agriculture Canada, pp. 558–565. Entomol Sin 50: 868–870.

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