INSTRUMENTA BIODIVERSITATIS VII: 1-9; juin 2006

MALICA CARAGANAE RICHTER (DIPTERA, TEPHRITIDAE, TRYPETINAE): REMARKS ON ITS BIOLOGY AND A DESCRIPTION OF THE 3RD INSTAR LARVA Severin V. KORNEYEV1 & Valery A. KORNEYEV2 1the

Ukrainian Entomological Society, c/o I. I. Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, Bohdan Chmielnicky str. 15, UA-01601, Kiev-30, MSP, Ukraine. E-mail: [email protected] 2the I. I. Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, Bohdan Chmielnicky str. 15, UA-01601, Kiev-30, MSP, Ukraine. E-mail: [email protected] Malica caraganae Richter (Diptera, Tephritidae, Trypetinae): remarks on its biology and a description of the 3rd instar larva. - The Caragana bean fly, Malica caraganae Richter, was rediscovered in several localities in Kyrghyzia 20 years after its original description. Notes on its biology are given. The third instar larva is described and the adult is redescribed. Possible phylogenetic relationships inferred from larval morphology are discussed. M. caraganae is distantly related to the species of the predominantly African genus Notomma Bezzi, showing African relationships, which are not common for the fauna of Middle Asia. Keywords: Tephritidae - Malica caraganae - larva - Caragana - Middle Asia. INTRODUCTION Malica caraganae Richter is one of the most enigmatic species of Palaearctic Tephritidae. The species with very uncommon appearance and trophic connections was described only in 1974, and afterwards, not rediscovered for 20 years. It was reared from beans of Caragana turkestanica Kom. in Sary-Chelek Natural Reserve, Kyrghyzstan (Richter, 1974). No other Palaearctic fruit fly is known to be associated with fabaceous plants (except for Notomma mutilum (Bezzi) in Israel and Egygpt), and relationships of this monotypic genus remained vague even after terminalia of both sexes were described (Korneyev, 1996). It is known to occur so far only in Kyrghyzstan, and the only genus, which is believed to be related, is Notomma Bezzi from Africa. In the latter genus, larvae induce galls on twigs of Acacia (Munro, 1952). The subtribe Notommatina was established to include both Malica and Notomma and was assigned to Carpomyini (Korneyev, 1996), because of its similarity of male epandrium and surstyli with some Notomma and Rhagoletis Loew, but relationships remained obscure. In 1994 and1995, further specimens were found among the material collected by L. V. Peck and P. Duelli in additional localities in Kyrghyzstan, and in June 1996 E. P. Kameneva and the second author (VAK) observed and collected numerous adult flies

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in Caragana stands in Boom [= Boam] Ravin near the western end of Lake Yssyk-Kul and later, in August 1998, they collected beans of Caragana infested by larvae of M. caraganae. These observations and descriptions of larvae are the subject of the current paper. The investigative responsibilities were distributed between the authors in the following way: SVK dissected larvae and prepared figures with the use of a compound microscope equipped with a camera lucida, prepared final computer graphics, provided description of larvae and compared larval characters with known descriptions of other tephritid larvae. VAK wrote the introduction, redescription of adult flies and added some taxonomic conclusions based upon studies of larvae and adults. MATERIAL AND METHODS This study is based on specimens which are deposited in the following institutions: MHNG SIZK USNM ZISP

Muséum d'histoire naturelle, Genève, Switzerland. Schmalhausen Institute of Zoology, Kiev, Ukraine. National Museum of Natural History, Smithsonian Institution, Washington DC., USA. Zoological Museum of Russian Academy of Science, St. Petersburg, Russia.

Morphological terminology used here generally follows White et al. (1999) with several terms used by Kandybina (1977) for larva. RESULTS AND DISCUSSSION Malica caraganae Richter, 1974 Malica caraganae Richter, 1974: 134; Foote, 1984: 97; Korneyev, 1987: 42; Korneyev, 1996: 34; Korneyev & Peck, 1996: 296; Norrbom et al., 1999: 165. MATERIAL. Holotype / and paratypes 15?, 11/: Kyrghyzstan: Sary-Chelek Natural Reserve, ex Caragana turkestanica Kom. fruits, exit 15.05–4.06.1968 (Makhnovskiy) (ZISP). Non-type material: Kyrghyzstan: labels as in holotype, ?, / not included in type series (headless; dissected). Suusamyr Valley, 19.06.1963, 1/ (Toktouchikova) (ZISP); Suusamyr Valley, Western Karakol River, 2,500 m, 8.07.1978, sex? (abdomen lost) (Peck); Orto-Tokoy, 1,800 m, 20.06.1970, 1/ (Peck) (SIZK); [road between] Issik-Kul–Karakul [lakes], 2050 m, 18.06.1995, 1? (Duelli) (MHNG); Boom Valley, 1,900 m, on Caragana kirghizorum Pojark., 22.06, 12?, 9/, 24.06, 1?, 25.06.1996, 7?,1/ (Kameneva); S Yssyk-Köl, Kadji-Sai, ex beans of Caragana sp.17.07.1998 — exit 05.1999, 2?, 2/ (V. Korneyev); idem, 25 3rd instar larvae, in alcohol (SIZK). Alcohol samples (adult, larvae) have been proceeded to Michigan University. Series of specimens from Boom Valley are deposited also in MHNG, USNM and several other collections.

THIRD INSTAR LARVA Figs 1-9 DIAGNOSIS. Creamy white, superficially smooth, elongate, cylindrical, tapered and bluntly rounded anteriorly, and gradually increasing in width to its obliquely truncate posterior end. DESCRIPTION. Cephalic segment or gnathocephalon (Figs 1–2). Short, with sensory lobes separated by shallow medial depression, smooth, without scale-like or tooth-like cuticular structures. Antenna 2-segmented, with basal segment as long as apical segment; apical segment almost spherical. Maxillary sense organ (= palpus) with 3 sensillae visible in main part and additional sensilla slightly anterolaterally to it.

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FIGS 1–9 Malica caraganae Richter, third instar larva. 1, total, lateral view; 2, facial mask, antero-ventral view; 3, cephalopharyngeal skeleton. lateral view; 4, subhypostomal sclerite, ventral view; 5, anterior spiracle; 6, creeping welt, ventral view; 7, spinules of creeping welt, enlarged; 8, caudal segment, posterodorsal view; 9, posterior spiracle.

Preoral (stomal sensory) organ without teeth; number of peg-like sensillae unknown or sensillae indistinguishable. Mouth opening surrounded with 15–18 oral ridges with smooth edges. Accessory plates lateral to oral ridges and anterior to mouth opening poorly expressed. Median oral lobe (= labial lobe sensu Belcari, 1989) between mouth hooks not developed. Mouthhook (mandibular sclerite) (Fig. 3). Large, with long and wide, slightly curved apical hook and without additional preapical tooth. Hypopharyngeal (hypostomal) sclerite 1.5 times as long as mandibular sclerite, heavily sclerotised and fused

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to pharyngeal sclerite. Parastomal sclerite in lateral view appearing at medial part of hypostomal sclerite. Dental sclerite indistinguishable. Labial (subhypostomal) sclerite (Fig. 4) with elongate lateral arms. Thoracic and abdominal segments. Smooth, without dorsal and lateral spinules, but with ventral spinules (Fig. 7) restricted to creeping welts (Fig. 6). Anterior spiracle mostly subsurface, with 6, rarely 5 or 7 tubules (Fig. 5). Caudal segment (Fig. 8). With spiracular area oblique in profile, limited by poorly expressed ridges dorsally and ventrally, with transverse oval area slightly elevated anterodorsally of spiracles. Posterior spiracle with 3 lateroventrally directed short oval spiracular openings, 2 times as long as wide (Fig. 9). Spiracular hairs indistinguishable or absent. Anal lobes moderately large. Length. 8.1–10.8 mm long, 1.6–2.5 mm wide (N=15) (Fig. 1). ADULT

Figs 10-23 DIAGNOSIS. Yellow-brown flies (both alive and dead) with spotted head, characteristical wing pattern of fused yellow-brown crossbands and abdomen orange-brown to black (in female) or brownish-yellow (in male, Figs 22-23). REDESCRIPTION. Head (Fig. 10). Subspherical; height : length :width ratio 1:1:1.2. Frons as long as wide, 2.1 times as wide as eye; gena 0.8–0.9 times as high as eye; eye 0.9–1.1 times as high as long; 1st flagellomere twice times as long as wide. Frons reddish yellow with more or less regular pattern of 8–10 pairs of round, large and small black and brown spots; ocellar triangle shiny black, very small, vertical plate shiny yellow, 0.25 times as long as frons; frontal plate sparsely yellow microtrichose; frontal vitta matt. When alive compound eye reddish-green, with 2 brown longitudinal stripes. Lunula shiny yellow, protuberant, with pair of round black spots. Face matt yellow, slightly receding, with deep antennal grooves, sharply separated by flat, ventrally bifurcated carina, with 3 round, matt black spots: one between antennae and pair at ventral margin (sometimes below it, on clypeo-facial membrane). Facial ridge yellow, with 0–3 small black spots; parafacial as wide as 1st flagellomere, long, matt, with 5–8 black spots; gena matt yellow, with 6–10 black spots. Occiput uniformly yellow, except spots at border with gena and vertex, swollen, with shallow but conspicuous vertical and oblique wrinkles and furrow posterior to orbit, at dorsal 2/3 of eye. Ocellar, postocellar and postvertical setae very minute or absent; 2 approximated, reclinate orbital setae; 2, rarely 3 or 4 moderately short frontal setae in anterior 1/3 of frontal plate; genal seta poorly differentiated; frons setulose; facial ridge with short and fine setulae; medial and lateral vertical seta black, moderately short and fine; occipital setulae moderately short and numerous; 6-7 fine, poorly differentiated postocular setulae; all setae and setulae dark brown to black. Antenna yellow, scape and pedicel black setulose; pedicellar notch deep; one row of sparse and fine setulae at margin; 1st flagellomere bluntly pointed apically; arista short, 2-segmented, with 2nd segment incrassate basally. Palpus yellow, 0.8 times as long as 1st flagellomere and 2.5 times as long as wide, with rather short, but dense setulae in apicoventral 1/3. Proboscis fleshy, densely brown setulose, as long as 1st flagellomere, with small yellow prementum. Thorax. Light brown to dark yellow, with yellow postpronotum, notopleuron and scutellum. Mesonotum 1.5 times as long as wide at level of presutural supra-alar

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FIGS 10–21 Malica caraganae Richter, adult. 10, head, lateral view; 11, wing; 12, claw; 13, epandrium, lateral view; 14, phallapodeme, ventral view; 15, phallus glans, right lateral view; 16, oviscape, dorsal view; 17, eversible membrane, ventral view; 18, same, dorsal view; 19, aculeus, ventral view; 20, same, lateral view; 21, spermathecae (13–14, from Korneyev, 1987; 16–21, from Korneyev, 1996, with permission).

setae, brownish with 4 light yellow to brownish red, white microtrichose vittae forming lyrate pattern; setulae black, evenly distributed, one row of dorsocentral setulae differentiated. Scutellum moderately swollen, matt, evenly sparsely setulose over posterodorsal portion. Prosternum yellow, broad trapezoidal, with blackish setulae on margins. Postpronotum and proepisternum black setulose. Anepisternum shiny brown, dorsal and ventral margins yellow; katepisternum, anepimeron and entire posterior part of pleuron brown, black setulose. Anatergite and katatergite bare, mediotergite shining

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yellow. Setae black and moderately short, 0–1 scapular, 1 postpronotal, 1 presutural and 1 postsutural supra-alar, 1 dorsocentral aligned with postalar setae, 1 acrostichal, 1 intra-alar and 1 postalar setae; 2 pairs of scutellar setae; 2 subequal notopleural setae; 1 anepisternal, 1 katepisternal and 1 anepimeral seta. Wing. As on Fig. 11, narrow, 2.9–3.0 times as long as wide, with yellow, brownish margined and spotted pattern. Costal cell 1.2–1.3 times as long as pterostigma in both sexes. Vein R1 completely setulose on dorsal surface, without gap at level of apex of subcostal vein. Vein R4+5 dorsally sparsely setulose to level of R-M and bare ventrally. Crossvein R–M distally of R1 apex; section of vein M between BMCu and R-M 2.0–3.0 times as long as section between R-M and DM-Cu. Medio-basal portion of cell br with hyaline spot devoid of microtrichia. Cell bcu closed by receding crossvein, with almost indistinguishable posteroapical lobe. Calypters narrow, stripelike; upper calypter yellow with brownish fringe, lower calypter pale yellow, short whitish microtrichose at margin. Halter creamy white. Legs. Yellow, with black setae and setulae; apical halves of tarsomeres usually brownish. Ventral row of setae on fore femur with 2–4 thickened, but not spur-like setae. Mid femur with semi-erect, moderately long setulae on anterior surface. Mid tibia with 1 strong ventro-apical seta. Hind femur with 2 semi-erected preapical dorsal setae. Claws double (Fig. 12). Abdomen. With tergites yellowish brown, black setulose and sparsely microtrichose in male, reddish brown to dark brown, non-microtrichose, slightly shagreened in female. Tergite 6 of female half as long as tergite 5. Male terminalia. Epandrium (Fig. 13) yellow, with short, slightly posteriorly curved lateral surstylus lacking additional lobes, medial surstylus with 2 oval prensisetae and 10–12 setulae dorsal to them. Hypandrium rather symmetrical. Phallapodeme as in Fig. 14, with widely separated vanes. Phallus narrow and rather short, with glans (Fig. 15) very large, almost half as long as, and twice as wide as stipe; left lateral lobe very large, flapped onto right side of glans corpus, forming very large sinus with inner surface sculptured with sparse transverse oval granulose structures; topologically, this surface loosely corresponds median sclerite (sensu Han, 1999); acrophallus, dorsal sclerite (sensu Han, 1999) and apico-dorsal lobe not differentiated; dorso-apical membranous lobe without longitudinal sclerotised portion. Female terminalia. Oviscape (Fig. 16) strongly swollen, reddish, shiny, with short black setulae, pair of lateral apodemes and longitudinal ridge dorsally. Eversible membrane (Figs 17–18) with very short taeniae, ventrally and laterally almost evenly covered with moderately sharp, short monodentate scales, and dorso-medially with fine and acute spinulae. Aculeus (Figs 19–20) apically acute and slightly compressed laterally. Two peer-like, papillose spermathecae (Fig. 21). Figs 24-25 BIOLOGY. Adults occur from the end of May and are abundant on Caragana shrubs at the end of blossom and beginning of fructification period (June, mainly 2nd and 3rd decades). Adults walk on branches inside the spiny bush (that explains their rarity in collections). Wing hamation and synchronous supination were observed. During copulation (Figs 24–25), the male holds the female abdomen at 3rd segment.

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FIGS 22–25 Malica caraganae Richter. 22–23, male; 24–25, male and female, in copula.

Females oviposit into young beans, usually in the middle, holding it with mid and hind legs and inserting the aculeus at a right angle. In August, each bean contains one, rarely 2 or 3 third instar larvae, which eating out the entire contents. As the bean breaks, the maggots drop and pupate in the soil. However, many larvae pupated also in dry beans. The species hibernates as pupae and is univoltine. After hibernation, adults emerge in May or, in the laboratory, in April–June in the following year. PHYLOGENETIC RELATIONSHIPS. Based upon studies of adult morphology, Malica is believed to be related to the African genus Notomma Bezzi. Members of both genera have similar wing pattern, laterally compressed aculeus and are associated with fabaceous (in the broad sense) plants. The subtribe Notommatina established for them by Korneyev (1996) and, with some reservations, was assigned to Carpomyini (Trypetinae), but this relationship should be further investigated. Further data, inferred from the study of larval morphology, are as follows. Malica certainly belongs in the subfamily Trypetinae, and is not associated with Dacini. Its elongate subhypostomal sclerite is similar to that in Adramini, Trypetini and some primitive Carpomyini (for instance, Rhagoletis alternata Fallén) (see Kandybina, 1977: Fig. 12), and can be considered a synapomorphy of these taxa. The presence of numerous oral ridges and single tooth of mandibular sclerite, as well as the stomal sense organ without teeth are plesiomorphies, which can be found in similar condition in the Rhagoletis alternata group (Carpomyina) or in some Adramini (Euphranta

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(Rhacochlaena) ortalidina Portschinsky, E. (R.) oshimensis Shiraki). Certain features (parastomal sclerite fused to hypostomal sclerite, visible in profile only at the middle of the latter; strongly sclerotised, elongate hypostomal sclerite) might be synapomorphies with Trypetini and Adramini, but they can also be treated as homoplasies of adaptive origin, for feeding in tissues harder than fleshy fruits. On the other hand, Malica does not share some characters of Trypetini (accessory plates lateral to facial ridges, etc.), which are believed to be synapomorphies of this tribe and therefore does not belong there. As a conclusion, larval characters confirm that Malica may belong in the lineage including Trypetini, Carpomyini and Adramini. Further molecular and biological studies are needed to clarify its position. ACKNOWLEDGEMENTS Adult specimens were borrowed or examined through the courtesy of Dr Bernhard Merz (MHNG), Dr Vera A. Richter (ZISP) and the late Dr Ludmila V. Peck (Institute of Biology, Bishkek). We thank Dr Elena P. Kameneva, who first observed and collected most adult flies in the field. Photographs of adult flies that emerged in the laboratory were taken by M. Vladimir Rayevski in the winter 1999; we greatly appreciate his assistance. The trip of VAK to Kyrghyzstan in 1998 was funded by a grant to Prof. Guy L. Bush, University of Michigan, East Lansing. We dedicate this paper to the memory of Dr Maria Nikolaevna Kandybina (1926–2004), whose excellent figures and descriptions prepared with the use of a very simple microscope, remain so far the best standard of such a work. REFERENCES BELCARI, A. 1989. Contributi alla conoscenza dei ditteri tefritidi. IV. Descrizione della larva di terza età di Acanthiophilus helianthi (Rossi), Dacus oleae (Gmel.), Ceratitis capitata (Wied.), Acidia cognata Wied. e considerazioni preliminari sulle differenziazioni morfologiche legate al diverso trofismo. Frustula Entomologica (n.s.) 10 (1987): 83-125. FOOTE, R. H. 1984. Family Tephritidae (Trypetidae) (pp. 66–149). In: SOOS, Á. & PAPP, L. (eds). Catalogue of Palaearctic Diptera, Volume 9, Micropezidae–Agromyzidae. Akadémiai Kiadó, Budapest and Elsevier, Amsterdam, 460 pp. HAN, H.-Y. 1999. Phylogeny and behavior of flies in the tribe Trypetini (Trypetinae) (pp. 253–297). In: ALUJA, M. & NORRBOM, A. L. (eds). Fruit flies (Tephritidae): Phylogeny and evolution of behavior. CRC Press, Boca Raton, XVI + 944 pp. KANDYBINA, M. N. 1977. Lichinki plodovykh mukh-pestrokrylok (Diptera, Tephritidae). [Larvae of fruit-infesting fruit flies (Diptera, Tephritidae)]. Opredeliteli po faune SSSR, izdavaemye Zoologicheskim Institutom Akademii nauk SSSR. Nauka, Leningrad 114: 1-210. (In Russian) KORNEYEV, V. A. 1987. The asparagus fly and its position in the system of the family Tephritidae (Diptera). Vestnik Zoologii 1987(1): 39–44. (In Russian) KORNEYEV, V. A. 1996. Reclassification of Palaearctic Tephritidae (Diptera). Communication 3. Vestnik Zoologii 1995(5–6): 25–48. (In Russian) KORNEYEV, V. A. & PECK, L. V. 1996. Sem. Tephritidae (Trypetidae) –mukhi-pestrokrylki [Fam. Tephritidae (Trypetidae) – fruit flies]. – Kadastr genofonda Kyrghyzstana. Tom III. Nadklass Hexapoda (Entognatha i Insecta) [Genetical Fund Cadastre of Kyrghyzstan. Volume III. Superclassis Hexapoda (Entognatha and Insecta)]. Aleine, the Ecological Movement of Kyrghyzstan & Institute for Biology and Pedology, Kyrghizian Aca-

demy of Sciences, Bishkek: 296–299. (In Russian)

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MUNRO, H. K. 1952. A remarkable new gall-forming trypetid (Diptera) from southern Africa, and its allies. Entomology Memoirs. Republic of South Africa. Department of Agriculture 2: 329-341. NORRBOM, A. L., CARROLL, L. E., THOMPSON, F. C., WHITE, I. M. & FREIDBERG, A. 1999. Systematic database of names (pp. 65-251). In: THOMPSON, F. C. (ed.). Fruit Fly Expert Identification System and Systematic Information Database. Myia 9 (1998): VII + 524 pp. & Diptera Data Dissemination Disk (CD-ROM) (1998) 1. RICHTER, V. A. 1974. A new genus of Tephritidae (Diptera) from Middle Asia. Zoologicheskiy Zhurnal 53(1): 133–135. (In Russian) WHITE I. M., HEADRICK D. H., NORRBOM A. L. & CARROLL L. E. 1999. Glossary (pp. 881–924). In: ALUJA, M. & NORRBOM, A. L. (eds). Fruit flies (Tephritidae): Phylogeny and evolution of behavior. CRC Press, Boca Raton, XVI + 944 pp.