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Turkish Journal of Zoology Turk J Zool(2014) 38: 491-499© TÜBİTAKdoi:10.3906/zoo-1312-30

New teratological cases in Platygastridae and Pteromalidae (Hymenoptera)

Ovidiu Alin POPOVICI1, Mircea-Dan MITROIU1,*, David G NOTTON2

1Faculty of Biology, Alexandru Ioan Cuza University of Iaşi, Iaşi, Romania2Department of Life Sciences, Terrestrial Invertebrates Division, Darwin Centre, The Natural History Museum, London, UK

* Correspondence: mircea.mitroiu@uaic.ro

1. IntroductionThe families Platygastridae and Pteromalidae consist of small to very small wasps that live as parasitoids of the immature stages of insects and arachnids. Because of their biology, some members of these families are important agents in the biological control of pests (Orr, 1988; Bouček and Rasplus, 1991).

Teratology is the study of malformations (Asiain and Márquez, 2009). The problem of teratology in insects was largely debated by Balazuc (1948, 1958, 1969), who provided a classification of and terminology for different morphological abnormalities found in this group of arthropods. Balazuc (1948, 1958) considered these abnormalities “monstruosités”. Perhaps the best-known and most well-studied type of teratology is gynandromorphy, which has been found in almost all major groups of insects.

Teratology in Hymenoptera was discussed extensively by Balazuc (1958). This phenomenon has been studied more thoroughly in larger Hymenoptera, e.g., Apoidea (Laidlaw, 1932; Leclercq, 1953; Fyg, 1964; Akre, 1982; Nilsson, 1987; Celary and Wisniowski, 2001; Engel, 2007; Lucia et al., 2009; Michez et al., 2009) and Vespoidea (Berndt and Kremer, 1983; Acosta and Martinez, 1984; Berndt and Wisniewski, 1984; Borsato, 1995; Eck, 1998), but

was not neglected in the Parasitica, e.g., Ichneumonoidea (Pisică, 1966; Bordera and Tormos, 1986; Penteado-Dias et al., 2005), and was even studied in microhymenoptera, e.g., Proctotrupoidea (Ceballos, 1921; Ogloblin, 1936; Szabó, 1959; Bin, 1972, 1976; Sveum, 1980; Hilpert, 1985; Rajmohana and Narendran, 1999), Chalcidoidea (Caltagirone, 1970; Beserra et al., 2003; Pereira et al., 2003; Zhang and Zhu, 2007), and Ceraphronoidea (Fergusson, 1978; Dessart, 1993).

Until now, very few teratological specimens of Platygastridae have been published: Fabritius (1968) described a male Trimorus algicola (Kieffer, 1911) from Romania that had a monocyclic helicomery of the second metasomal tergite; Safavi (1968) noted some antennal malformations in Trissolcus grandis (Thomson, 1860); Huggert (1977) found 3 gynandromorphic specimens of Idris piceiventris (Kieffer, 1908), and Popovici et al. (2011) found a female Triteleia peyerimhoffi (Kieffer, 1906) with the interantennal prominence hypertrophied. Among the Pteromalidae, the published cases of teratological specimens are even scarcer. From the thousands of specimens examined, Graham (1969) mentioned only 1 example of a teratological specimen, a male of Miscogaster elegans Walker, 1833.

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 in Pteromalus 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

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

Research Article

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The aim of this paper is to give a brief overview of the presence of teratological specimens among Hymenoptera and to present new cases of such specimens from the families Platygastridae and Pteromalidae, about which very few examples have been published so far.

2. Materials and methodsThe terminology of abnormalities follows Balazuc (1958) and Michez et al. (2009), except for the term “schistocery”, proposed by us as an opposite of “symphysocery” in order to illustrate the division of an antennomere in 2 or more new antennomeres. Morphological terms used in this paper were matched to the Hymenoptera Anatomy Ontology Portal (HAO; Yoder et al., 2010; Seltmann et al., 2012). Identifiers (URIs) represent anatomical concepts in the HAO (Table 1).

The specimens used in this study (Table 2) are kept in the personal collections of O Popovici (OPPC) and MD Mitroiu (MICO), except for the specimen of Triteleia peyerimhoffi, which is in the Canadian National Collection of Insects, Arachnids and Nematodes, Ottawa, Canada (CNC), and the 2 specimens of Norbanus africanus, which are in the collection of the Natural History Museum, London, UK (BMNH).

For Idris, Gryon, Scelio, Metaclisis, Systasis, and Pteromalus, both antennae were removed and mounted in Canada balsam. For Gryon and Scelio the aedeagus and the ovipositor and ovary, respectively, were also mounted on microscope slides. After removal of the antennae, the body of each specimen was mounted on triangular or rectangular cards. Card-mounted specimens and appendages on slides were photographed using a Leica DFC500 digital camera on a Leica 205A stereomicroscope. The acquired images were then processed with Zerene or Helicon Focus software and their clarity was further enhanced using Adobe Photoshop CS3. The antennomeres are abbreviated A1–A13 starting from the scape and the gastral tergites T1–T7.

3. ResultsThe teratologies observed in 8 genera of Platygastridae and 4 genera of Pteromalidae are summarized in Table 2 and detailed below.

Platygastridae (Figures 1–21)Apegus sp.In 1 male, the A5 (“sex-segment”) is divided into

2 segments (schistocery) (Figures 19 and 20), so both antennae are 13-segmented; in normal specimens the 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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be seen only on the ventral side, the dorsal side being undivided. A9–A10 are also fused in both antennae (Figures 19 and 21).

Gryon monspeliense (Picard 1924)One male has the left antenna modified (Figure 7),

whereas the right antenna is normal (Figure 12). In this case the left antenna is 1.2 times shorter than the right antenna. Additionally, for the left antenna, only the scape (A1) and the pedicel (A2) are separate, and all the other antennomeres are fused: A3 is fused with A4 without a clear division between them and A5–A12 also are fused in a mass in which it is almost impossible to distinguish the

constituent antennomeres. The fused antennomeres are wider than the normal ones from the male antenna, so in the malformed antenna, the fused antennomeres look like the clava of a female antenna. Other than the left antenna, the specimen looks perfectly normal.

Idris sp. One male has a symphysocery affecting A9–A10 of the

left antenna (Figure 13). In this case, A9–A10 are fused, but a trace of the division between them can be observed (Figure 20). Except for the fusion of these antennomeres, there are no other differences between the teratological antenna and normal one (Figure 8).

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)

Gryon monspeliensis ♂ Symphysocery ROMANIA: Tulcea, Macin Mountains, 23.vii.2004, sweep net, leg. M.-D. Mitroiu (OPPC-PGr01)

Idris sp. ♂ Symphysocery ROMANIA: Iasi, Botanical Garden, 2.viii.2004, sweep net, leg. O. Popovici (OPPC-PId01)

Metaclisis sp. ♂ Symphysocery ROMANIA: Iasi, Botanical Garden, 28.iv.2005, sweep net, leg. O. Popovici (OPPC-PMe01)

Opisthacantha sp. ♂ Helicomery JAPAN: Hokkaido, Soranuma-dake, Sapporo-shi, 27.vii.–21.viii.2007, Malaise trap, leg. A. Ueda (OPPC-POp01)

Scelio sp. 1 ♂ Symphysocery ROMANIA: Constanta, Vadu, 27.viii.2004, sweep net, leg. O. Popovici (OPPC-PSc01)

Scelio sp. 2 Transversal gynandromorphy UGANDA: Kibale N.P. Kanyawara Biol. Station, 22–29.viii.2010, Malaise trap, leg. Katusabe & Co. (OPPC-PSc02)

Sceliomorpha sp. ♂ Symphysocery FRENCH GUIANA: Kaw Mountains, 17.ix.–2.x.2006, Malaise trap, leg. K. Sarv (OPPC-PScl01)

Triteleia peyerimhoffi ♀ Hypertrophy HUNGARY: Veröce, 2–18.ix.2005, Malaise trap, leg. Z. Nyiro (CNC)

Pteromalidae

Norbanus africanus ♀ Cyclopy; asymmetry KENYA: Machakos dis., Kiboko, 1000 m ex larva Chilo sp. in maize stem, coll. 26.ix.1990, M.J.W. Cock (BMNH)

Norbanus africanus ♀ Hypertrophy KENYA: Machakos dis., Kiboko, 1000 m ex larva Chilo sp. in maize stem, coll. 26.ix.1990, M.J.W. Cock (BMNH)

Pteromalus sp. ♀ Symphysocery ROMANIA: Iasi, Ciric izvor, meadow, 30.vii.2007, leg. O. Popovici (MICO-310)

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

Systasis parvula ♀ Symphysocery; hypertrophy ROMANIA: Botosani, Vorona, alfalafa flowers, 31.viii.2006, leg. C. Lisenchi (MICO-309)

Systasis parvula ♂ Hypertrophy ROMANIA: Neamt, Varatec, veg. nr. stream, 18.07.1999, leg. M.-D. Mitroiu (MICO-47)

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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.One male has a symphysocery affecting A8–A9 of the

left antenna. The fusion between these antennomeres is complete, with no traces of articulation, except for a small depression in the middle of the newly formed segment. The length of the teratological antenna is slightly shorter than the length of the normal one; this is largely due to the length of the fused antennomeres (A8–A9) being shorter than the length of A8 and A9 taken together in the normal antenna. A4 of the normal antenna has a more expanded outer apical corner than in the teratological antenna (Figure 1). In the teratological antenna, the width of A4 and A5 is a little smaller than the width of A4–A5 in the normal antenna, and, by contrast, the width of A6–A10 is a little bit greater than the width of the same antennomeres in the normal antenna (Figure 2).

Opisthacantha sp.One male with a helicomery affecting the second and

third gastral tergites (T2–T3) was observed, the limit between these tergites being almost impossible to establish (Figures 14 and 15). The rest of the gaster is unaffected. The sternites are not affected, but the second right laterotergite has a well-developed overlap over a very small area of the second sternite.

Scelio sp. 1One male has the A5–A6 of the right antenna connected

by a weak sclerotized membrane (Figure 5). While the antennomeres can still be distinguished, they appear to be rigidly joined, so there is no functional articulation. In this case, the teratological antenna is not so different in size from the normal one, with only negligible differences between the length of the 2 antennae and between the length and width of the corresponding antennomeres (Figure 6).

Scelio sp. 2One gynandromorph specimen (Figure 16) was

identified (transversal gynandromorphy). It looks like a female, but both antennae are 10-segmented (Figures 17 and 18). In Scelio, the number of antennomeres is dimorphic (10 in males and 12 in females). The ovipositor and ovaries were found by dissecting the specimen. The right antenna does not differ from a male antenna (Figure 18), but the left one is slightly wider (Figure 17), being intermediate in shape between a male and female antenna.

Sceliomorpha sp. One male shows a double symphysocery of the right

antenna (Figures 3 and 9). This malformation affects A3–A5 and A7–A9 (Figure 3). The malformed right antenna is shorter (2.2 mm without scape) than the normal antenna (2.6 mm without scape). A3–A5 are completely fused on the dorsal side, but on the ventral side a trace of the articulations between them can be seen. A7–A9 are not as modified as A3–A5. In the teratological antenna A2, A4–

A8, A10, and A11 are noticeably shorter, while A2–A6 and A8 are wider than the corresponding antennomeres of the left antenna. Thus, for Sceliomorpha, in the teratological antenna, the affected antennomeres are shorter and wider than the normal antennomeres, and the tyloids from A4 and A5 seem to be modified, being morphologically closer to the basiconic capitate peg sensilla that are present on the female antenna.

Triteleia peyerimhoffi (Kieffer, 1906)One female has a hypertrophied interantennal

prominence and central keel on the frons (Popovici et al., 2011). In the affected female, the distance between toruli is almost twice that in the normal specimens. Except for this malformation, the rest of the specimen is perfectly normal (Figures 10 and 11).

Pteromalidae (Figures 22–30)Norbanus africanus Subba Rao 1973Cyclopy and head asymmetry can be observed in one

female that has only the right compound eye present, the left being completely absent (Figure 23). The area where the eye should have been displays normal sculpture, except for a tiny oval structure, and has the same coloration as the rest of the head capsule; however, this side of the head is evidently smaller (less high) than the right side. Another female from the same sample displays a hypertrophy of A6–A8 of the left antenna, each of these antennomeres being distinctly swollen and darker compared to the corresponding antennomeres of the right antenna (Figure 22).

Pteromalus sp.One female is characterized by a symphysocery

affecting A8–A10 of the right antenna (Figure 25), the left one being normal (Figure 26). The 3 antennomeres are fused only on the ventral side; on the opposite side their limits are clearly visible (Figure 25).

Sphegigaster sp.One female has the gastral petiole clearly asymmetric

and wider than normal. The asymmetry is especially visible at the level of the 2 lateral projections of the petiole and at its connection with the gaster (Figure 24).

Systasis parvula (Thomson, 1876)One female has both antennae affected by

malformations. The right antenna (Figure 28) has a symphysocery affecting all funicular segments (A5–A9), while the left antenna has a symphysocery affecting A4–A5 and a hypertrophy of A5, which appears as if another antennomere is fused laterally with it (Figure 27). One male has a hypertrophy of A5 at the level of the left antenna (Figure 29). However, the 2 anelli cannot be observed, which may also indicate a symphysocery affecting A3–A5. Additionally, the pedicel (A2) looks displaced (Figure 29). The right antenna is normal (Figure 30).

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4. DiscussionTeratologies among platygastrids and pteromalids have not been frequently cited. This subject was no doubt neglected because of the small size of these wasps, but, even so, from our experience, teratologies appear to be rare within these groups. Malformed specimens may also be hard to discover due to poor preparation (e.g., wings obscuring the metasoma or with antennae in glue or under the specimens). The causes of these malformations are not clear, but are considered to be either genetic or environmental. The presence of antenna and leg deformities was described by Berndt and Wisniewski

(1984), who proposed low humidity as a cause of these malformations, because of the reduction of fluid available to extend these appendages. Safavi (1968) found 3 causes for the appearance of malformed antenna: host eggs that were fresh but dehydrated, old host eggs, and a compression of antennae during the pupal stage. Safavi also noted that the presence of these antennal malformations strongly affected mating behavior: the affected wasps did not mate successfully, and so any hereditary component or predisposition underlying these malformations could not be tested. In Safavi’s experiments, only males of Trissolcus grandis showed malformed antennae. This is similar to the

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.

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examples presented above, where we found only males with teratological antennae.

According to Balazuc (1948), symphysocery affecting antennomeres A6–A11 was common, A4–A5 less common, and A3–A4 rare. In the first category we found 4 examples (Metaclisis, A8–A9; Sceliomorpha, A7–A9; Idris, A9–A10; and Pteromalus, A8–A10), in the second category 1 example (Systasis, A4–A5), and in the last category 1 example (Gryon, A3–A4), as well as an intermediate case (Sceliomorpha, A3–A5). Balazuc (1958) proposed as causes of helicomery affecting metasomal terga heredity, exposure to ultraviolet radiation, mechanical shock, abnormally high heat, and parasitoids such as Strepsiptera. In the case of the Opisthacantha specimen presented above, we can exclude parasitism by Strepsiptera since there is no physical evidence for it and the host range of strepsipterans does not include Platygastridae.

Teratological antennae can be a source of taxonomic mistakes, e.g., Erdős and Novicky (1955) described the new genus Birous (Hymenoptera: Encyrtidae) based on the number of antennomeres. Bouček and Graham (1978), however, found that the type specimen of this genus is a teratological female belonging to Microterys. In the case of the monotypic genus Prosinostemma Kieffer 1914, Masner and Huggert (1989) stated that the genus was probably established on a teratological specimen with a symphysocery affecting 2 antennomeres. Malformations

of the metasoma have also been a source of taxonomic errors, for example in Pteromalidae: Miscogaster elegans Walker, 1833 was described by the same author under the name Lamprotatus helenor Walker, 1846 on the basis of a teratological specimen with the gastral petiole abnormally short (Graham, 1969).

In the specimens described above, the various malformations affecting the antennae were by far the most common. Among these, symphysocery (the fusion of 2 or more antennomeres) seems to be the most frequent.

It is difficult to assess the frequency of such malformations in the studied groups. In a single sample from Kenya we found 2 malformed specimens, while in hundreds of other samples no such specimens could be identified.

AcknowledgmentsThe senior author thanks his friend Takuma Yoshida (Japan), who provided the specimen from Japan; Dr Villu Soon (Estonia) for the gift of specimens from Estonia and French Guiana; and Dr Lubomir Masner (CNC) for his unconditional support. The second author thanks Dr Andy Polaszek (BMNH) for providing the 2 specimens of Norbanus. This study was funded by a grant from the Romanian National Authority for Scientific Research, CNCS-UEFISCDI, Project Number PN-II-RU-TE-2012-0057.

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