Nomioides patruelis, Cockerell, 1919

Rozen, Jerome G., 2008, Biology and Immature Stages of the Bee Nomioides patruelis (Halictidae: Halictinae: Nomioidini) and of Its Cleptoparasite, Chiasmognathus pashupati (Apidae: Nomadinae: Ammobatini), with a Preliminary Phylogeny of the Halictidae Based on, American Museum Novitates 3604 (1), pp. 1-24 : 13-21

PUPA OF NOMIOIDES PATRUELIS

Figures 17, 18 , 21–26

DIAGNOSIS: The reader is referred Rozen and Özbek (2008), where the pupa of this species was compared in some detail with other known halictid pupae. Although pupae of all Halictinae possess a conspicuous tubercle partway down on the outer surface of the forewing pad, this tubercle in Nomioides patruelis is much closer to the wing base than in other known pupae and thus is not certainly homologous with the others.

The pupa of Nomioides patruelis can easily be distinguished from that of its cleptoparasite, Chiasmognathus pashupati , because the host has limited integumental spiculation and lacks a pair of long, erect, spiculate, hornlike tubercles arising from the vertex. In addition, there are obvious differences in the dorsal mesosomal tubercles between host and cleptoparasite.

HEAD: Integument without setae, spiculate as described below. Outer surface of scape bearing several low indistinct swellings but no distinct tubercles; inner surface (next to compound eye) of scape of female (but not male) with tubercle with indistinct apical tubercle; outer surface of pedicle of female (but not male) with tubercle; inner surface of pedicle of female (but not male) with tubercle; first flagellomere of male (but not female) with pronounced tubercle on outer surface; flagellum of male about 1.5 times longer than that of female (as in adults); flagellomeres of male tending to have more pronounced tuberclelike swellings on outer surface than those of female. Vertex spiculate near midline, with moderately large rounded tubercle immediately mesad of each adult lateral ocellus; each adult ocellus covered with small, low, rounded convexity; two more smaller rounded tubercles immediately laterad of lateral adult ocellus; upper frons with large (largest on head) lateral tubercles on each side, with less pronounced tubercle-like swelling immediately mesad of each; genal tubercle below eye apparently absent; clypeus without tubercles; labrum of male unmodified, of female with rounded, median apical tubercle; galea spiculate, with apical tubercle (presumably accommodating developing adult setae); maxillary palpi spiculate.

MESOSOMA: Integument without setae, spiculate as described below. Posterior margin of pronotum and lateral lobe swollen; mesoscutum (figs. 17, 18, 23) with pair of small, rounded paramedian tubercles medially and another, even lower pair of paramedian tubercles close to posterior margin; axilla produced as small erect tubercle (figs. 17, 24); mesoscutellum (figs. 17, 18, 24) with pair of large, strongly produced, erect, apically tapering, acutely rounded, spiculate tubercles; metanotum with similar, slightly smaller, spiculate paired tubercles (figs. 17, 18, 24); propodeum with median section spiculate. Tegula (figs. 17, 18, 25) with strongly projecting, large, nonspiculate tubercle, longer than basal diameter; forewing with outer surface irregular and with tubercle (fig. 26) less than one-quarter distance to wing apex. Male forecoxa without tubercles; 4 foretrochanter with large apical tubercle; forefemur somewhat produced at base, nontuberculate; mid- and hind coxae and midtrochanter, each with moderately small, pointed, apical tubercle; hind trochanter with somewhat larger, pointed apical tubercle; hind tibia with large, projecting, spiculate tubercle on outer surface near base (fig. 27); other leg segments without unusual tubercles. Female leg tubercles about as described for male except hind trochanter with larger apical tubercle.

METASOMA: Integument without setae, spiculate in some dorsal areas and sterna more distinctly spiculate; T2–6 (male) or T2–5 (female) with posterior transverse row of moderately large, erect, mostly sharply pointed tubercles on each side; tubercles closest to midline tending to be largest; apex of metasoma with rounded median apical tubercle. Male S1– 4 each with median rounded apical tubercle; male S5 with small apical projection medially

4 Because of the small body size and the transparency of the pupal exoskeleton, the descriptions of the basal leg tubercles need to be verified with more recently preserved material.

but not rounded; shape of female S1 unknown; female S2–4 each with median projection.

MATERIAL STUDIED: Two male and two female pupae: Pakistan: Sind Province: Gharo , 38 mi E of Karachi, May 8, 1984 (J.G. Rozen, S. Lodhi, I. Stupakoff) .

POSTDEFECATING LARVA OF CHIASMOGNATHUS PASHUPATI

Figures 12–16

For comparative purposes, this description follows the format of a recently described larva of another nomadine bee ( Rozen et al., 1997).

DIAGNOSIS: The one feature whereby the mature larva of Chiasmognathus pashupati can be distinguished from those of all other known Nomadinae is the faint extension of the epistomal ridge mesad of each of the anterior tentorial pits on the cleared specimen, although the two sections of the ridge fade completely before meeting at the midline. At best, this ridge is difficult to see on such a small specimen. In all other respects the larva has all of the features of other Nomadinae, the monophyly of which is strongly supported by numerous other larval characters as given by Rozen (1996: 10–11). The larva closely resembles those of other known Ammobatini ( Rozen and McGinley, 1974), but differs in that it possesses low but distinct paired tubercles on most body segments (fig. 12). Of all others it seems most similar to that of Ammobates carinatus Morawitz (ibid.: figs. 10–17), in that they share the following: greatly recessed labiomaxillary area, with the hypopharynx strongly projecting and its leading edge sharply projecting in lateral view (fig. 15); maxillary palpus very large, though not long (fig. 15); labroclypeal area large, strongly projecting in lateral view, extending well beyond other mouthparts (fig. 15); and mandible swollen at base so that base almost globose. (Contrary to the description in Rozen and McGinley, 1974, a reexamination of the mandible of A. carinatus revealed that it has very fine serrations on the dorsolateral and ventral apical edges, similar to but much finer than those of C. pashupati .) The similar appearing vertices as seen in lateral views (fig. 15; cf. Rozen and McGinley, 1974: fig. 17) may or may not be homologous; in C. pashupati the swelling extends across both parietals, whereas in A. carinatus it is restrict- ed to the median and does not extend laterally.

DESCRIPTION: Length approximately 3.5 mm. Head (figs. 14, 15): Unpigmented except for internal ridges, which are weakly pigment- ed; sensilla non-setiform; spiculation, including that of hypopharynx, absent.

Head size small compared with body; head capsule wider than long in frontal view; as seen in lateral view (fig. 12), parietals at top of head projecting forward on each side almost on level with vertex, well above antenna (see ‘‘Remarks’’ for discussion). Tentorium absent except at pits, presumably because specimen was about to molt (but presumably very thin as judged by remains of weak arms); anterior tentorial pit very small, apparently slightly closer to anterior mandibular articulation than to lower edge of antennal disc (but position of anterior mandibular articulation difficult to identify); posterior tentorial pit small, in front of cervical fold and posterior to curve of hypostomal ridge as ridge bends upward toward presumed junction with postoccipital ridge; postoccipital ridge not evident so that hypostomal ridge fading completely as its posterior end bends upward as if to meet postoccipital ridge; posterior margin of head capsule a faint line extending dorsolaterally to cervical fold (hence, same as second line as defined in Rozen et al., 1997; for further analysis of this feature in the Nomadinae, see Rozen, 1996: 6–7); integument in front of posterior margin sclerotized, nonspiculate, integument behind margin becoming conspicuously spiculate. Median longitudinal thickening of head capsule absent; hypostomal ridge moderately broad but weak; pleurostomal ridge weak, not clearly defined though moderately broad; epistomal ridge mesad of anterior tentorial pit broad but weak, extending diagonally upward immediately mesad of antennal disc before fading completely. Parietal band scarcely evident. Antennal prominence low, small; antenna positioned very low on face in frontal and lateral views (figs. 14, 15), perhaps in part because of exaggerated parietal above it; antennal disc and papilla not clearly differentiated; papilla bearing two sensilla. Labroclypeal region strongly projecting beyond frontal area with labrum large, without sclerite, with two sharply defined, apically acute, small tubercles; epipharynx a simple curved surface.

Mandible (fig. 16) (too small to be dissected from head but interpreted through cleared head capsule) short, robust (almost globular) at base, apically strongly curved toward mouth, and sharply pointed; cusp and apical concavity not differentiated, without denticles, outer surface with approximately five (possibly sensilla-bearing) scattered denticles; dorsal and ventral apical edges with conspicuous, sharply pointed, apically directed teeth. Maxilla strongly fused to labial region, its apex (except for palpus) small, surpassed by hypopharynx; galea and maxillary sclerites absent; palpus large at base, tapering rapidly to pointed apex, so that palpal length clearly shorter than basal diameter. Labium not divided into pre- and postmentum; premental sclerite absent; labial palpus presumably represented only by a sensillum somewhat posterior to salivary opening. Salivary opening simple, circular, without lips. Hypopharynx projecting compared with labium and maxilla, but much less so than labroclypeal area in lateral view (fig. 15); hypopharyngeal groove presumed to be faint line close to salivary opening in frontal view (fig. 14).

Body (figs. 12, 13): Without setae but with large spicules on prothorax and on venters of other thoracic segments; spicules becoming successively smaller on venters of following abdominal segments and absent on abdominal segment 8–10; integument without spines or sclerotized tubercles. Body form slender, elongate; intersegmental lines weakly incised between most body segments but becoming more deeply incised after abdominal segment 6; dorsolateral intrasegmental lines not evident; thoracic and abdominal segments 1–7 with paired dorsolateral tubercles, those of segment 8 much less obvious and those of segments 7; paired tubercles absent on segments 9, 10; all dorsolateral tubercles moderately low, conical (i.e., not transverse); venter of abdominal segment 9 not produced; segment 10 not bulging ventrally, attached centrally to 9; anus a transverse slit, apical on 10; perianal area with dorsolateral and ventral lips (fig. 13). Spiracles subequal and moderate in size, except those of abdominal segment 8 with width of atrium about one-half of that of other spiracles; spiracles projecting beyond body wall, apparently without rims; peritreme present, moderately wide; atrium globular; atrial wall without denticles or rings; primary spiracular open with collar; subatrium moderately short, with about 10 chambers. Sex characters unknown.

MATERIAL STUDIED: One postdefecating larva, Pakistan: Sind Province: Gharo , 38 mi E of Karachi, May 8, 1984 (J.G. Rozen, S. Lodhi, I. Stupakoff) from Nomioides nest #2 .

REMARKS: The forward-projecting parietals of Chiasmognathus pashupati are probably not homologous with the paired swellings on the vertices of most larval Brachynomadini because the swelling of the latter are more localized and are faintly wrinkled. The swellings of the parietals of C. pashupati are not discrete, but rather the top of each parietal is forward projecting, and its surface is not wrinkled.

PUPA OF CHIASMOGNATHUS PASHUPATI

Figures 19, 20 , 28–31

DIAGNOSIS: Because of the pair of long, ‘‘furry’’ tubercles rising from the top of the head (figs. 19–22), the pupa of this bee can immediately be distinguished from those of other Nomadinae (including other Ammobatini) currently known (see references in McGinley, 1989; Rozen, 1989, 1992, 1994, 1997a, 1997b, and 2000). The absence of sharply pointed, apically pigmented tubercles on the vertex and/or mesoscutum is also unusual compared with pupae of other Nomadinae, except for those of the Brachynomadini (see Rozen, 1994, 1997a). The densely spiculate pupal integument has not been noted in other Nomadinae, but this is the first SEM study of a pupa of any cleptoparasitic bee, no matter the family.

Among the Ammobatini, the pupae of only the Old World Ammobates carinatus and new world Oreopasites vanduzeei Cockerell and O. favreauae Rozen have been described before ( Rozen and McGinley, 1974; Rozen, 1992). In addition to the characters discussed above, the pupa of Chiasmognathus pashupati can be distinguished by its smaller size, geographic distribution, and host preference. Chiasmognathus is strictly Old World, known only to attack nests of Nomioides ( Engel, 2007) , the only other known cleptoparasite of which is Sphecodes nomioidis Pesenko ( Radchenko, 1980; Pesenko, 1979). The pupa of C. pashupati will not run successfully in the preliminary key to cleptoparasitic bee pupae ( Rozen, 2000).

DESCRIPTION: Length 3.5 mm. Head: Integument without setae, but many areas pale, velvety (a feature unknown for other bee pupae); when viewed with SEM, velvety appearance due to densely set spicules (fig. 29). Vertex without rounded mounds or tubercles except each side with erect, elongate, hornlike tubercle (figs. 19, 20, 28, 29), beset with microscopic spicules somewhat more elongate than spicules elsewhere on head; these tubercles arising about midway between lateral ocelli and upper orbits; elsewhere head lacking tubercles; apex of clypeus with rounded, downward-projecting swelling on each side of labrum (these swellings referred to as tubercles by Rozen and McGinley, 1974, who recognized them as allowing for the development of the specialized hair tufts of adult males); pupal ocelli weakly defined. Labrum swollen medially, projecting in lateral view; as in adults with mouthparts folded, mandibles directed posteromedially, resting alongside labrum, not crossing labrum; mandibles vaguely swollen subapically, both adorally and medially.

Mesosoma: Integument covered in most areas with pale, dense, velvety, microscopic spiculation; setae absent. Posterior lobes of pronotum normal, not produced. Mesepisternum without tubercles; mesoscutum without rounded or sharp tubercles or even verrucae; axillae unmodified, not elevated; mesoscutellum with pair of paramedian, apically rounded, low but distinct tubercles (best seen in lateral profile); metanotum not pronounced. Tegula not produced, without tubercle(s); wings without tubercles but with a few irregular swellings. All coxae, trochanters, femora, tibiae, and tarsi without tubercles.

Metasoma: Integument covered in most areas with pale, velvety spiculation; setae absent. T1 with one or two small dorsolateral tubercles near posterior margin on each side; T2–T6 with submarginal row of three to four dorsolateral tubercles on each side; larger tubercles sharply pointed though apparently unpigmented; T7 without tubercle. Sterna without tubercles. Apex of metasoma produced as parallel-sided (when seen from above), apically rounded, nonspiculate terminal spine (fig. 31). Spiracles and anus unpigmented at time of preservation.

MATERIAL STUDIED: One male pupa, Pakistan: Sind Province: Gharo , 38 mi E of Karachi, May 8, 1984 (J.G. Rozen) from nest of Nomioides patruelis . The specimen had obviously been preserved soon after it eclosed; there was no hint of pigmentation .

REMARKS: This pupa seems very unlike the known pupae [ Oreopasites and Pasites (5 Morgania )] of other Ammobatini ( Rozen and McGinley, 1974) because it lacks sharppointed vertical and mesoscutal tubercles. However, it agrees with these because of the presence of paired, downward-projecting swellings at the lower end of the clypeus next to the labrum (ibid.: fig. 29). The pale, velvety, dense spiculation covering most of the pupal integument of Chiasmognathus pashupati has not been noticed among other pupal Nomadinae (although future studies of these pupae should include SEM examination). Its function is uncertain as is the function of the paired, hornlike, vertical tubercles.

Figures

Figs. 17–20. 17, 18. Diagrams of pupa of Nomioides patruelis, lateral view, entire pupa (with tergal tubercle enlargement), and front end of pupa, dorsal view, respectively. 19, 20. Diagrams of front end of pupa of Chiasmognathus pashupati, dorsal view, and of entire pupa, lateral view, respectively. Scale (5 1.0 mm) refers to all figures.

Figs. 21–25. SEM micrographs of pupa of Nomioides patruelis, approximate anterolateral view. 21. Anterior part of pupa with numbers referring to close-ups in figs. 22–25. 22. Close-up of frons and vertex. 23. Close-up of anterior mesoscutal tubercles. 24. Close-up of mesocutellar, axillary, and metanotal tubercles. 25. Close-up of tegular tubercle.

Figs 26–27. SEM micrographs of pupa of Nomioides patruelis, approximate anterolateral view. 26. Close-up of wing tubercle. 27. Close-up of hind-tibial tubercle.

Figs. 12–16. Postdefecating larva Chiasmognathus pashupati. 12. Entire larva, lateral view. 13. Apex of abdomen, lateral view 14, 15. Head, frontal and lateral views, respectively. 16. Right mandible outer, surface.

Figs 28–31. SEM micrographs of pupa of Chiasmognathus pashupati, approximate lateral views. 28. Entire pupa, showing broad distribution of dense spicules. 29. Close-up of left vertical tubercle; note left lateral, nonspiculate ocellus behind tubercle. 30. T3, T4 showing dense spiculation and row of sharply pointed tubercles at posterior margin of each. 31. Apex of metasoma showing widespread spiculation and nonspiculate terminal spine.