Review of the genus Stenodera with a description of the first instar larva of S . puncticollis ( Coleóptera : Meloidae )

The first instar larva, or triungulin, of Stenodera puncticoHis (Chevrolat, 1829) is described. Its characters indicate that Stenodera is the most primitive member of the subfamily Nemognathinae and support the recognition of the monotypic tribe Stenoderini, as previously proposed on the basis of adult morphology. The bionomic information on this genus is summarized, and an annotated catalogue and key to the species based on adults are presented.


INTRODUCTION
The genus Stenodera was described by Eschscholtz (1818) for Mylabris sexmaculata Fabricius, 1794, ajunior synonym of Meloe caucasica Pallas, 1781.Later it was confused by some authors with the Central Asian genus Megatrachelus sensu Abeille de Perrin, 1880(not Motschulsky, 1845).Beauregard (1889), Escherich (1891aEscherich ( , 1891bEscherich ( , 1897a) ) and Pic (1912a) designated Stenodera as a distinct genus.Maran (1942) revised this genus, described new species and divided it into two subgenera, the nominate, and Stenoderina Aksentjev, 1988. Finally, Aksentjev (1978) described a new species from Eastern Siberia, and Bologna (1991) presented a partial review of the taxonomy and bionomics of the genus.This relatively small genus, with eight species, is distributed from the Balkans and Near East through Central Asia to China.
Although the systematic position of Stenodera was variously considered in the literature, all specialists treat it as a primitive member of the Nemognathinae.Selander (1964Selander ( , 1966) ) proposed a monotypic tribe Stenoderini, based on the plesiotypic state of certain adult characters, which he discussed in great detail in his 1991 paper, and formally described the tribe.Kaszab (1969) and Bologna (1991) preferred to consider Stenodera as the most primi tive genus of the tribe Nemognathini, and did not divide the subfamily as proposed by Selander (1964).
Recently we obtained the triungulin of S. puncticollis (Chevrolat, 1829) from southern Anatolia.The first instar larva of this species is very distinct from those of other Nemognathinae, showing several primitive features in common with the subfamily Meloinae.This larva was utilised in a recent phylogenetic analysis of the family (Bologna & Pinto, 2001), which corroborated the basal position of Stenodera in the Nemognathinae.Although few characters support a tribal status, Bologna and Pinto followed Selander (1991)in recognizing the Stenoderini.
The main purposes of this paper are to describe the first instar larva of Stenodera, provide a key and synopsis of the genus, and to compare its adult and larval characters with those of other Nemognathinae.The opportunity to examine specimens of S.foveicollis (Fairmaire, 1897) and S. djakonovi Aksentjev, 1978, two species for which only the original descriptions exist, also permitted us to better define the limits of this genus, and to present an annotated catalogue.
Morphological analyses and illustrations were produced using an Olympus SZX12 stereomicroscope for living and alcohol preserved material, and a Leitz Laborlux S light microscope for material mounted on slides in Canada balsam; both microscopes were equipped with a drawing tube.A Philips XL30 scanning electron microscope for the high magnification study of material mounted on stubs after critical point dehydration and gold sput tering.Measurements reported in the descriptions are based mainly on cleared, slide-mounted larvae.The terminology of larval structures follows Lawrence (1991), MacSwain (1956) and Bologna & Pinto (2001).For the description of larval chaetotaxy we adopted some of the notational conventions suggested by Selander (1990) (see Bologna & Di Giulio, 2002).

Description of the triungulin of S.puncticollis
Egg. Pale yellow, stout, ovoid, round at both ends, dis tinctly wider at one apex; chorion of mature eggs smooth, light brown.Length 0.5 mm, width 0.2 mm.
Head.Strongly transverse (width/length = 1.4) and subglobose (Figs 2a-2d), widest just behind antennal fos sae, partially invaginated into prothorax; sides of epicra nial halves evenly convergent from antennae to base; basal elevation absent; anterior margin of head (fronto clypeal margin) rounded.Epicranial suture Y shaped (Fig. 2a); frontal sutures oblique, only slightly sinuate distally, complete to antennal fossae.Stemmata unique (Figs 2a,2b,3a), appearing comma-shaped under light microscopy, dorsolaterally positioned; each stemma consisting of a smooth, swollen dorsal area (the normal discoid stemma), with a narrow, anteriorly curved, slightly reticulate (probably because of the light sclerotization of the cuticle), and irregularly swollen ventral section (Fig. 3a,arrow).Frontoclypeal region with a total of 16-18 setae (Fig. 2a); frontoclypeal row (FCR) of 3 pairs of setae, setae FCR1 FCR2 and FCR3, sensory pit present between FCR2 and FCR3; 5-6 pairs of setae posterior to FCR arranged in 3 irregular rows.Dorsum of each epicranial half with a basal group of 4 very small setae and 1 pit; 2 medial setae with an intermediate pit along the frontal arms of epicranial suture; 6 setae around the stemma arranged as in Figs 2a-2b; ocular seta subequal in length to adjacent setae, positioned anterior to the stemma and slightly anteriorly displaced to the ocular sensory pit; 4 additional setae and 2 pits positioned lateroventrally.Antennae (Fig. 3b) short, anterolaterally directed; seg ment I and II very short, ring-like, I with 2 sensory pits dorsally, II slightly longer than I, dorsally with 3 setae, 2 long and 1 short, and 1 intermediate pit; sensory appendix on segment II, ventrolaterally positioned, conical, acute at apex, broader and slightly longer than segment III; seg ment III slender, slightly wider at apex, as long as seg ments I and II combined, with an apical seta more than twice length of antenna; III with 3 subapical setae, similar in size and position to those of segment II, and 1 addi- tional medial elongate seta and 1 opposed short, truncate sensorial appendix (Fig. 3b,arrow).Gulamentum (Fig. 2c) weakly sclerotised with 2 small setae anteriorly.Labrum (Fig. 2d) directed ventrally, transverse, laterally rounded, dorsally with 8 setae of different length, the most lateral one on each side about 4 times as long as the others, with 2 medial pits.Epipharynx coarsely granulate.2d) without mola, broad at base, dis tinctly narrowed and falcate in apical half, the two areas separated by 1 dorsal and 2 ventral transverse grooves, ental surface of apical half grooved, smooth; outer margin with 2 setae; 2 large dorsal sensory pits just behind mesal transverse groove.Maxillae (Fig. 2c) with broad stipes, membranous dorsally, with 5 setae, one row of 3 setae, the lateral two much longer than the middle one, and an apical row of two elongate setae; mala simple, lobiform, slightly protruding, with 6-8 thick setae; maxillary palpi with segments I and II subequal, broad and short, ring like; segment I with 2 sensory pits; segment II with 2 setae; segment III cylindrical, about 3 times as long as II, slightly swollen apically, with 1 small dorsolateral seta, 1 apical long socketed stick-like sensory appendix, and 10 shorter setae-like papillae; outer surface of segment III with 1 slender digitiform sensillum; cardo not sclerotised, with 1 very small seta.Mentum (Fig. 2c) with 1 or 2 pairs of short setae and 1 pair of sensory pits basally; prementum with 1 pair of medial setae and 1 pair of basal sensory pits, 2 small ligular setae dorsally; labial palpi with segment I short; segment II cylindrical, about 3 times as long as I, with 1 stout, cylindrical, socketed apical sensory appendix, obliquely truncate at apex, nearly as long as segment II and with a crown of 8 shorter setae-like papillae.

Mandibles (Figs 2b-
Thorax.Segments (Fig. 1a) transverse, subrectangular, wider than head, decreasing in length from pro-to meta thorax; prothorax with anterior and posterior margins convex, lateral margins straight; meso-and metanotum slightly rounded laterally.Ecdysial line well marked and complete only on pro-and mesonotum.Pronotum about twice as wide as long, with about 25 small setae plus pits on each side of ecdysial line, arranged symmetrically, most placed on anterior (AR) and posterior rows (PR); prosternum (Fig. 1c) with 3 pairs of setae medially.Meso-and metanotum approximately 2/3 as long as pro notum with about 17 small setae plus pits on each side of ecdysial line, arranged in 3 transverse subparallel rows; meso-and metasternum with 2 medial pairs of setae.
Abdomen.Slightly fusiform (Fig. 1a), well sclerotised, with transverse, narrow, rectangular tergites; maximum width at segment III; ecdysial line absent; spiracle bearing laterotergites (Fig. 1b) well sclerotised, pleurites poorly sclerotised; sternites I-VII poorly sclerotised, more or less divided into plates, sclerotisation increasing from segment I to VII, sternites VIII and IX undivided and well sclerotised.Tergite I (Fig. 1a) with approximately 3 rows of small setae: AR with 3-4 pairs of setae and 1 pair of medial pits; MR with 3 regularly spaced setae; PR with 7 setae and 1 medial pit; tergites II-VIII with the same pattern of setae and pits except for the reduction in size (or loss) of 1 lateral and 1 medial seta on AR and the presence of 1 additional lateral seta on PR; tergite IX with similar setation but 1 pair of setae on PR (caudal setae) elongate, slightly longer than segment IX. Pleurites (Fig. lb) fused with sternum only on segment IX; epipleurites with 2 setae, the posterior longer; hypopleurites with 1 seta.Sternites (Fig. 1c) with 1 pair of short medial setae on AR, 1 pair of short medial setae on MR and 3 pairs of setae of different lengths on PR.Pygopod (Fig. 3c) mod erately produced, membranous, transversely divided into 2 parts: the dorsal one semicircular with 6 small setae, transversally lined, and the ventral one longitudinally divided into 2lobes.
Larval features and relationships.The first instar larva of Stenodera can be distinguished from that of other Meloidae by its unique C-or comma-shaped stemmata (Fig. 3a), the truncate seta-like appendix on antennal seg ment III (Fig. 3b), the transverse division of the mandi bles (Fig. 2d), and the obsolete spiracles on abdominal segments II-VIII.Stenodera is also distinguished from all members of its subfamily, the Nemognathinae, by fea tures correlated with non-phoretic behaviour (Bologna & Pinto, 2001).
Major characters distinguishing it from other nemognathines include the following: the labrum (Fig. 2d) is free and visible from above rather than fused to the head capsule and turned under the ventral surface.The stem mata (Fig. 2a) are positioned on the dorsal surface of the head capsule, not laterally.The mandibles (Figs 2b, 2d) are directed forward and move in a plane parallel rather than perpendicular to the frontal plane of the head capsule.The ental surface of the mandibles is smooth, lacking prominent toothlike transverse ridges.The antenna (Figs 2d,3b) has a distinctly conical sensory appendix and the apical seta of antennal segment III is very long (Figs 2a,2b).The gula of the head capsule (Fig. 2c) is short and poorly sclerotized.The femora are shorter than the tibiae (Fig. 1b), not subequal, and the tibiae taper noticeably to the apex.Also, the abdominal sterna (Fig. lc) are poorly rather than well sclerotized, and the gen eral body shape (Figs 1a-1c) is short and robust, not fusi form as in other members of the subfamily.Abdominal spiracles (Fig. 3f) positioned on laterotergites, spiracle VIII unmodified as in the tribe Horiini.A comparison of Stenodera puncticollis with other genera of Meloidae based on 101 larval characters is given by Bologna & Pinto (2001).
In agreement with Selander (1991), a recent phyloge netic analysis of Meloidae placed Stenodera in its own tribe and the genus at the base of the subfamily Nemog nathinae (Bologna & Pinto, 2001).The latter study con sidered the Nemognathinae as the sister group of the Tetraonycinae, and both as sister taxa of the Meloinae.Because Stenodera is almost certainly non-phoretic, this hypothesis assumes the independent evolution of phoresy in the Tetraonycinae and Nemognathinae.
The taxonomic position of Stenodera depends on cer tain derived features suggesting nemognathine affinity, coupled with the generally primitive, non-nemognathine form of the larva as well as the primitive condition of critical adult features.A summary of these characters fol lows: derived adult traits of Stenodera linking it to nemognathines include the serrate ventral margin of the claws, the unarmed aedeagus (Figs 5a-5g) and the reduced styli on the female gonocoxites (Gupta, 1971;Selander, 1991).The relatively slender filiform antennae, the shape of abdominal sternum IX in males (see review in Gupta, 1971), and general body shape also suggest nemognathine affinity.Larval features characteristic of the Nemognathinae are few (Bologna & Pinto 2001) but include reduced labial palpi and the position of the ocular seta relative to the ocular sensory pit.Adult male features generally considered primitive, and which within the Nemognathinae are unique to Stenodera, are the incom pletely fused gonostyli (Figs 5a-5g), the undivided sternum VIII, and the partially sclerotized tergum IX.All three features also characterize male Meloinae and Tetra onycinae (see Gupta, 1971).
Tribal status for Stenodera, although first proposed by Selander (1964Selander ( , 1991)), is not strongly supported by adult characters, and for this reason was not adopted by Bologna (1991).In fact, with the possible exception of one trait (separation of maxillary palpifer from stipes by a well-marked suture), the features used to justify the Stenoderini by Selander (1991), either also characterize the Meloinae (male gonostyli partially fused, sclerotized male tergum IX) or are present in other Nemognathinae (non lamellate male sternum IX, single row of teeth on claw).It is the first instar larva of Stenodera, which suggests tribal status.First of all, as the only known non-phoretic larva of Nemognathinae, it is phenetically distant and immediately separable from all other members of the sub family (Bologna & Pinto, 2001).Although these features alone, probably primitive for the family, do not argue for tribal status, they are coupled with several unique traits, which if synapomorphic for the genus do present a case for significant hierarchical ranking.Unique larval features of S. puncticollis include the occluded and presumably non-functional abdominal spiracles II-VIII (Fig. 3f), the unique shape of the stemma (Fig. 3a), the transverse divi sion of the mandibles (Fig. 2d), and the truncate appendix at the base of antennal segment III (Fig. 3b).
The unique comma-shaped stemma of Stenodera larvae is interesting in relation to other meloids and deserves comment.In all first instar larvae of Meloinae, there is only a single stemma on each side of the head and it is circular in shape.In most Nemognathinae there are two stemmata on each side and they also are circular.Ste nodera and, presumably, Horia are the only nemog nathines with a single stemma, but only in Stenodera is this structure so uniquely shaped.The condition in Ste nodera possibly represents an intermediate state between one stemma, the universal condition in Meloinae, and two which characterizes virtually all Nemognathinae.
Geographical and ecological distribution.Stenodera has a fragmented distribution both in the Palaearctic and in the Transitional Chinese regions (see Palestrini et al., 1987) (see Figs 6-9).It is primarily a Central Asiatic-Mediterranean element (see Vigna Taglianti et al., 1999), with two subranges in isolated areas of East Asia.The genus is longitudinally distributed from the W Balkans (Dalmatia: about 15°W) to the Primor'e Territory (about 147°E); and latitudinally from Moldava and Podolia (about 48°N) to Fukien (about 25°S).The nominate sub genus includes four species: S. caucasica, widely distrib uted from the Balkans to Central Asia (Turkmenistan), S. oculifera endemic to the Palestinian area, S. djakonovi restricted to the Primor'e Territory (Far East Siberia), and S. foveicollis endemic to the Eastern Chiang-hsi and Fukien (South East China).The subgenus Stenoderina, with four species (S. anatolica, S. coeruleiceps, S. palaestina, S.puncticollis), is restricted to the Middle East.
This disjunct distribution is very uncommon in the Palaearctic fauna and it is more or less paralleled by some late Tertiary relict elements such as the Euchiridae scarab beetles of the genus Propomacrus Newman, 1837, or the discoglossid toads of the genus Bombina Oken, 1816.
From an ecological point of view, Stenodera is a genus primarily associated with steppe (S. anatolica, S. cauca sica, S. coeruleiceps) or xeric Mediterranean (S. oculifera, S. palaestina, S. punticollis) habitats, or both (e.g. S. coeruleiceps and S. oculifera), at least the Balkan and western Asiatic species.No specific information is available on the eastern Asian species.The Primor'e Ter ritory is characterised by a mixture of temperate deciduous forest and grassland, while the Kiang hsi and Fukien regions, are characterised by wet evergreen forests andgrassland (Tomaselli, 1981).
Records of altitudinal distribution are very scarce.Some data, based on personal collections or museum material, are available for the following species: (a) S. caucasica occurs primarily from 100 to 1400 m a.s.l. in western and central Turkey, with records to 2000 m in the Eastern Provinces.Although detailed elevation data are not available from other areas, records from the Caucasus and Kopet dagh (Iran) indicate an occurrence in montane habitats.(b) S. puncticollis is distributed from sea level to 700 m a.s.l. in southern Turkey, and to 2000 m a.s.l. in Lebanon.(c) S. coeruleiceps an eurizonal species, com monly occurring in the highlands of central Turkey from 1000 to 1400 m a.s.l., with isolated records to 2000 m in the Eastern Provinces, as well as at sea level in southern Turkey.No detailed records are available for other spe cies, but according to the localities of collections, S. ana tolica is distributed in the high plateau of Anatolia, whereas S. oculifera and S.palaestina seem to occur from sea level to middle elevations (ca.1000 m a.s.l.).
Adult activity and plant preferences.Adults are diur nal, thermophilic and primarily active in spring and early summer.Based on examined material and literature records, adults are active in the following months: for species of the nominate subgenus -S.caucásica: May to June in all areas, with single records in March and April (Israel, Lebanon and southern Turkey) and in July (Turkestan, Turkey); S. djakonovi: June; S. foveicollis: March; S. oculifera: March and April.For species of the subgenus Stenoderina -S.anatolica: April to May; S. coeruleiceps: May and June; S. palaestina: February and April; S.punticollis April and May.
Behaviour.Sexual behaviour is important in the higher classificationof the Meloidae (Selander 1964).Characters of the subfamily Nemognathinae include a very short courtship, which lacks significant display (as well as sexually dimorphic morphological features correlated with such display), and a dorsally mounted copulatory position.By contrast in the Meloinae courtship generally is prolonged and characterized by overt tactual display.This behaviour is commonly correlated with various structural modifications of the male (see Bologna & Pinto, 2001 for a review).Males of four species of Stenodera, representing both subgenera, have modifications that suggest a somewhat complex courtship.In S. djak onovi and S. foveicollis the first segment of the fore tarsi is ventrally enlarged, rounded and laterally compressed depressed.S. anatolica and S. coeruleiceps have the same tarsus modified, but it is less enlarged and not com pressed, and the first segment of metatarsi is also enlarged.Courtship has never been observed in these spe cies.Brief field observations (MAB) on two Stenodera species with unmodified tarsi (S. caucasica and S.puncticollis) suggest that male courtship is restricted to brief sequences of dorsal courtship as is typical for most Nemognathinae.Copula was not observed, but the pres ence of an unarmed aedeagus suggest only a dorsal copu lation as in other Nemognathinae.The only known cases of male dimorphism in Nemognathinae, other than Ste nodera, is in primitive genera of the tribe Horiini (Cissites Latreille, 1804, Synhoria Kolbe, 1897, Horia Fabricius, 1787) and in Australian taxa (Palaestra Laporte de Castelnau, 1840, Palaestrida White, 1846, one unde scribed genus).
Antennal cleaning was observed in S. puncticollis: the fore legs are used simultaneously to stroke each antenna.
As concerns larval behaviour, data on development are noted in the paragraph "Material and methods".The triungulins, observed in the rearing box, use both legs and pygopod to climb on the box wall and to walk on the ground.Although this behaviour is typical of phoretic lar vae, it is known in certain meloine taxa lacking phoresy (Bologna & Pinto, 2001).

S. foveicollis).
Similarities include the presence of white setation on the inferior part of body, and the anteriorly narrowed pronotum.It differs primarily by the unmodi fied foretarsi.Elytral colouration is highly variable in this species.It typically is orange brown with 3 black spots (2 anterior and 1 posterior) but these spots can be variously reduced in number and size.Abeille de Perrin (1880), Escherich (1897a), Maran (1942) and Bologna (1991) described and figured several variations.

Stenodera djakonovi
Type material.The male Holotype, not examined, is in the Academy of Sciences of Sanct Petersburg.
Remarks.Bologna (1991), following Kaszab (in verbis, 1980), considered this species as a possible synonym of S. caucasica.The examination of two speci mens (1 male, 1 female, the only material known other than the type) in the NHB collections, supports the dis tinction of S. djakonovi and its inclusion into the nomi nate subgenus of Stenodera.
This species is extremely close to S. foveicollis from southeastern China.It is treated as distinct but the small number of specimens examined (2 S. djakonovi, 12 S. foveicollis), from a single population, do not permit an adequate evaluation of variability.Some characters listed in the key (e.g.shape of head, shape of pronotal foveae, pronotum dimensions) are tentatively used to distinguish these species.
The main differences of S. djakonovi vs. S. foveicollis can be summarised as follows: (a) head in lateral view shorter (ratio mouthparts/head capsule = 0.60 vs. 0.95); (b) shiny frontal area less extensive, head punctures larger, interpunctal surfaces more opaque; (c) antennae shorter -in female not attaining the first black spot of ely tra, and, in male, barely attaining posterior border of black spot (vs.clearly attaining the basal black spot in both sexes); (d) pronotum wider in the middle (ratio width/length = 0.88 vs. 0.78); (e) punctures of pronotum denser with interpunctal surface more opaque due to pres ence of more numerous micropunctures (vs.punctures sparse and surface shiny); (f) pronotal foveae positioned in a surrounding wide depression (vs.foveae well delim ited, not positioned in a wider depression).
Remarks.Fairmaire (1897) compared S. foveicollis to S. caucasica.Maran (1942) transferred this species from Megatrachelus Motschulsky, 1845 to Stenodera without examining the type.Bologna (1991) discussed this assignment and proposed its possible inclusion in the genus Zonitoschema Peringuey, 1909.The generic and subgeneric assignment proposed by Maran (1942) is con firmed after examining the Fukien specimens, the only material known other than the type.These additional specimens were collected in a region close to the type locality, and are in complete agreement with the Fairmaire's description.Assignment to Stenodera, is sup ported primarily by the structure of male genitalia (Fig. 5c), last abdominal sternite and maxillary palpi.
As shown by Maran (1942), this species is distinctly isolated from the primary geographic range of the genus.The recent description of a second eastern and similarly isolated species (S. djakonovi, from Primor'e Territory), close to S. foveicollis, supports the hypothesis of a rela tively recent fragmentation in the range of the genus.The extreme similarity of these two nominal species and their possible conspecificity were previously discussed.Escherich, 1891a: 54;Escherich, 1897a: 102;Maran, 1942: 19, 23 (not Motschulsky, 1872: 53).Stenodera oculifer: Escherich, 1897a: 102.Stenodera (Stenodera) oculifera : Bologna, 1991: 448.Type locality."Nazareth, Jaffa, Beyrouth" (Near East).Type material.Types of this species are preserved in the Abeille de Perrin collection (MP) and were examined.Two pos sible types of S. bipunctata Chevrolat from "Syrie" were exam ined in the MP collections.
Remarks.This species is phenetically isolated within its subgenus from both S. caucasica and the Eastern Asian complex as indicated by the rounded shape of its pronotum, colour of its elytra, and the unmodified tarsi.
The complex synonymy of this species was discussed by Bologna (1988Bologna ( , 1991)), who clarified that S. impressicollis Motschulsky is a junior synonym of Zonitis flava Fabricius, 1775.
Male genitalia are represented in Fig. 5d.

Fig. 3 .
Fig. 3. Stenodera puncticollis, SEM photographs of first instar larva, a -lateral view of left stemma (the arrow indicates the ven tral section of the stemma); b -dorsal view of left antenna (the arrow indicating the truncate sensory appendix); c -right lateral view of pygopod; d -posterior view of tarsungulus of left mesothoracic leg; e -left mesothoracic spiracle; f -left abdominal spira cles I-II (the arrow indicates the spiracle II closed) (scale bar =10 pm).