Diptera: Syrphidae

2 downloads 0 Views 1MB Size Report
Shannon, 1925; and one species of Sphiximorpha Rondani, 1850. We describe and ... States was loaned to us by the United States National. Museum (USNM) ...
MORPHOLOGY, HISTOLOGY AND FINE STRUCTURE

The Early Stages and Breeding Sites of 10 Cerioidini Flies (Diptera: Syrphidae) A. RICARTE,1 M. A. MARCOS-GARCI´A,1,2 G. E. ROTHERAY,3

AND

E. G. HANCOCK4

Ann. Entomol. Soc. Am. 100(6): 914Ð924 (2007)

ABSTRACT Approximately 197 species comprise the widespread syrphid tribe, the Cerioidini (Diptera: Syrphidae), but rearing data are known for ⬍5% of species. We obtained puparia of 10 species from Þeldwork in Costa Rica, Cuba, and Me´xico and from material loaned to us from Australia, Brazil, Costa Rica, and the United States. These species are included in four of the Þve genera recognized in the tribe: two species of Ceriana RaÞnesque, 1815; three species of Monoceromyia Shannon, 1925; four of Polybiomyia Shannon, 1925; and one species of Sphiximorpha Rondani, 1850. We describe and compare these puparia. They all possessed the diagnostic characters for the tribe. However, no early stage characters were correlated, hence early stages did not form groups based on shared characters. Some structures were relatively constant in form such as head skeletons and locomotory organs, but characters that showed plasticity included integumental vestiture and respiratory organs. A few features such as the unusually broader than long posterior respiratory process of Ceriana ornata Saunders, 1845, the spicules on the dorsum of the prothorax of Sphiximorpha barbipes (Loew, 1853), and the mesothoracic hooks of Monoceromyia tricolor (Loew, 1861) were unique to these species. Most cerioidine larvae were reared from tree sap but others came from tree holes, the liquid center of a cut agave (Agavaceae) and bee nests (Hymenoptera, Apidae). Field observations of larvae and their breeding site suggested functional explanations for some morphological features. KEY WORDS immature stages, Cerioidini, sap run, tree hole, bee nest

Cerioidine adults (Diptera: Syrphidae) include some of the most perfect mimics of noxious Hymenoptera known (Waldbauer 1970, Waldbauer and Sheldon 1971, Waldbauer et al. 1977). The afÞnities of the tribe are not resolved, but early stage characters suggest a relationship with the Xylotini (Rotheray and Gilbert 1999). In the adult stage, the tribe is distinguished by the combination of bare eyes, tuberculate face, antenna with a terminal style, anterior cross-vein beyond the middle of the discal cell, and petiolate abdomen (Thompson 1972). In the larval stage, the tribe is distinguished by mandibles and mandibular lobes invaginated into the mouth, aggregated groups of spicules on the prothoracic anterior fold, and absence of pupal spiracles (Rotheray and Gilbert 1999). Five genera comprise the Cerioidini, although their validity is not entirely settled: Ceriana RaÞnesque, 1815; Monoceromyia Shannon, 1925; Polybiomyia Shannon, 1925; Sphiximorpha Rondani, 1850; and Primocerioides Shannon, 1927. Unusually for syrphid tribes, cerioidines are fairly evenly distributed across biogeographical regions with 34 species in the Afrotropical region (Whit1 Instituto de Biodiversidad CIBIO, Universidad de Alicante, P.O. Box 99, E-03080 Alicante, Spain. 2 Corresponding author, e-mail: [email protected]. 3 National Museums of Scotland, Chambers Street, Edinburgh EH1 1JF, United Kingdom. 4 Zoology Museum, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, United Kingdom.

tington 2003), 31 in the Australasian region (Evenhuis et al. 2007), 23 in the Nearctic (Vockeroth and Thompson 1987), 47 in the Neotropics (Thompson 1999), 35 in the Oriental region (Evenhuis et al. 2007), and 27 in the Palaearctic (Thompson and Rotheray 1998). Of these 197 species, the biology and early stages of just nine (4.5%) are apparently known (Lundbeck 1916, Bhatia 1931, Heiss 1938, Lane and Carrera 1943, Maier 1982, Maier 1987, Rotheray et al. 1998, Sivova et al. 1999, Krivosheina 2001 and Rotheray et al. 2006). Since 1996, we have carried out Þeldwork in the Neotropics and Europe for syrphid early stages, including cerioidines and collaborators in various countries have supplied us with reared material. In this article, the breeding sites and puparia of 10 species are described and compared: Ceriana ornata (Saunders, 1845); Ceriana tridens (Loew, 1872); Monoceromyia rubrobrunnea (Hull 1944); Monoceromyia superba (Williston, 1887); Monoceromyia tricolor (Loew, 1861); Polybiomyia bergrothi (Williston, 1892); Polybiomyia macquarti Shannon, 1925; Polybiomyia pedicellata (Williston, 1887); Polybiomyia signifera (Loew, 1853); and Sphiximorpha barbipes (Loew, 1853). Materials and Methods Early stages were obtained during Þeldwork in Costa Rica, Cuba, and Me´ xico. Additional reared material from Australia, Brazil, Costa Rica, and the United

0013-8746/07/0914Ð0924$04.00/0 䉷 2007 Entomological Society of America

November 2007

RICARTE ET AL.: EARLY STAGES OF CERIOIDINE SYRPHIDS

States was loaned to us by the United States National Museum (USNM), Washington, DC, and the Instituto Nacional de Biodiversidad (INBio), Costa Rica. Other sources of material are acknowledged under each species. Due to lack of taxonomic data, larvae collected in the Þeld could not be identiÞed to species, and they were reared in the laboratory to obtain the adult stage for identiÞcation. Rearing usually took place in a controlled chamber at 20⬚C, 65Ð 85% humidity, and in the dark. Larvae were reared in plastic boxes containing material from the breeding site in which they were found. For respiration a hole was cut in the lid and covered with netting. Boxes were checked daily to ensure they were sufÞciently moist and to remove puparia. Puparia were reared individually on damp tissue in 55-mm-diameter petri dishes and checked daily until adults emerged. Adults were identiÞed using Thompson (1999); “A conspectus on Australian ßower ßies,” “Mesoamerican ßower ßies with particular references to Costa Rica,” and “Primer Taller de IdentiÞcacio´ n: Syrphidae del Nestro´ pico, February 2006, Cali, Colombia” (F. C. Thompson, unpublished data) and by comparison with named specimens in the collections of INBio in Costa Rica and the USNM. Descriptions of early stages are based on the puparial stage that retains all the features of the thirdstage larva (Rotheray 1993). Head skeletons were examined by softening puparia in a cold solution of KOH for ⬇30 min and removing them from the anteroventral margin of the puparium by using pins. Illustrations were made using a binocular microscope Þtted a drawing tube. Photomicrographs were obtained using a Hitachi S3000N scanning electron microscope (SEM) operated at 20 kV. Measurements were made using an eyepiece micrometer Þxed to a binocular microscope. Puparium length was measured on the ventral surface from the anterior margin that is part of the prothorax to the apex of the anal segment. Width was the maximum of structures measured. The length of the posterior respiratory process (prp) is a useful diagnostic character, but it is not measurable along its entire length because in most specimens the base is hidden within the folds of the anal segment. To overcome this difÞculty, comparisons between species were made by measuring the length of the prp above the transverse band to the apex, with the result expressed as a proportion of the width of the prp at the transverse band. The transverse band encircles the prp below the apex. It is a characteristic feature of the prp in Eristalinae (Syrphidae) and has various states from a raised ridge, a narrow band of striations or other distinctive surface sculpture to an indented groove (Rotheray and Gilbert 1999). To compare head skeletons the length of the ventral cornu was measured and in addition, an indentation index calculated for each species (Ferrar 1987). The indentation index is a measure of the extent the dorsal cornu is available as a surface for muscle attachment that may be correlated to the liquidity of the food. The longer the dorsal cornu, the greater the index and the

915

area for muscle attachment and the more powerful is the cibarial pump. In species with larvae developing in water-Þlled tree holes a low index and a less powerful cibarial pump could be expected compared with species developing in viscous tree sap. The index is calculated by expressing the length of the dorsal cornu as a proportion of the degree it is indented posteroapically at the junction with the rest of the basal (⫽pharyngeal) sclerite (Ferrar 1987). Terminology follows Hartley (1961) and Rotheray (1993) for gross morphology and Hartley (1963), Roberts (1970), and Rotheray and Gilbert (1999) for head skeleton structure. For the early stages of each species rather than provide full, individual descriptions that would necessarily involve much repetition, we give Þrst a list of shared, external characters from across the body and also from the head skeleton. These are characters that provide an account of the morphology of the species studied that should enable future comparisons. Characters unique to the sample in relation to outgroup taxa such as Xylotini and those variable in states and are hence potentially useful as diagnostic characters for individual or groups of species are also listed. For measured characters, ranges are given over the entire sample of included taxa. Under the descriptions of each species individual values for measured characters are given and also unique and diagnostic characters and states relative to the species considered here. After each description a separate taxonomic section follows in which species sharing suites of characters are discussed and characters that enable species to be recognized and distinguished are noted. Additional details of material examined, provenance and breeding sites are also given. The following initials indicate the institutions where material is deposited: CIBIO, Centro Iberamericano de la Biodiversidad, University of Alicante (Alicante, Spain); INBio, Instituto Nacional de Biodiversidad (Santo Domingo de Heredia, Costa Rica); NMS, National Museums of Scotland (Edinburgh, Scotland); USNM, United States National Museum (Washington, DC); and SI, Smithsonian Institution (Washington, DC). Initially, label SI was used, but now USNM is used. Results Early Stage Characters Shared by the Cerioidine Described Species Larva with saprophagous mouthparts, i.e., mandible and mandibular lobes invaginated into the mouth and functioning as a Þlter for separating suspended food (Roberts 1970, Rotheray and Gilbert 1999) and “shorttailed,” i.e., length of anal segment between 0.25 and 1.0⫻ body length; truncate anteriorly, tapered posteriorly, subcyclindrical to slightly dorso-ventrally ßattened in cross-section; length 9Ð13 mm, width 3.7Ð5.3 mm; head skeleton between 1.1 and 2.2 mm long with indentation index varying from 13 to 28%; dorsal cornu much shorter than ventral cornu, between 15 and 37% of its length; dorsal bridge, dorsal and ventral bridge and cibarial

916

ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA

ridges present; basal (⫽pharyngeal) sclerite varying in degree of sclerotization; prothorax broad apically with Þve aggregated groups of dark brown-to-black spicules on the anterior fold (curved down apex of the prothorax above the antennae and below the longitudinal grooves on the dorsum of the prothorax); below the mid-dorsal groups of spicules setae coating the base of the anterior fold; anterior spiracles with 4Ð12 spiracular openings on an inclined, outwardly facing, apical spiracular plate and length of the process between 1 and 2⫻ basal width; mesothoracic prolegs present with crochets in three rows, number of primary crochets varying from 6 to 16; parallel longitudinal folds on the lateral margins of the mesothorax beyond sensilla 4 and 5 with aggregations of spicules or hooks (C. tridens); abdomen with sensilla 7 and 8 on segments 1Ð7 approximated on a basal ßeshy papilla; integument of body usually pale but ground color often obscured by adhering material from the breeding site; vestiture (integumental setae) varying in length from 0.02 to 0.2 mm and in color from translucent to black; vestiture arranged in various ways and densities on the dorsum and lateral margins of the body, from transverse to inclined bars and clumps of various sizes and arrangements; anal segment with three pairs of approximately equidistant lappets, third posterior pair longer than the Þrst two pairs; prolegs present on the Þrst six abdominal segments, bearing crochets in three rows, 7Ð17 primary crochets on abdominal segment one, 5Ð11 primary crochets on segment 6; crochets red-brown to black; posterior respiratory process (prp): pale to darkbrown; tapering at apex; transverse band varying from an indented groove to a clear or indistinct line bordering changes in surface sculpture; surface sculpture ranging from striations to pits and punctures and from shiny to matt; variable in length from 0.4 to 2.3 mm; spiracular plate with three pairs of spiracular openings, dorsal and ventral openings usually tilde-shaped (⬇), middle pair either tilde-shaped or recurved (convoluted in C. ornata); interspiracular setae usually multibranched and conspicuous; pupal spiracles absent. Taxonomic Notes Cerioidine early stages (larva and puparium) are most similar to those of Xylotini and Tropidia Meigen, 1822 in being short-tailed with equidistant lappets, mandibles and mandibular lobes invaginated into the mouth, a broad and truncate prothorax with a well developed anterior fold and prolegs with crochets. Cerioidini are readily distinguished from other shorttailed larvae by grouped spicules on the anterior fold and absence of pupal spiracles. In basal Eristalinae, the mandibular lobes are ßeshy, coated in food-gathering cirri, and partially external being continuous with the pseudocephalon (ßeshy head) on their outside margins and attached to the mandibles on their inside margins. In derived Eristalinae such as Cerioidini, they are internal and function as Þlters anterior to the mouth. Externally, their food-gathering function is replaced by the lateral lobes that lie either side of the mouth and that are coated in broad setae basally and Þne setae apically. However, lateral lobes are protho-

Vol. 100, no. 6

Figs. 1–2. Whole puparia of two cerioidine species in lateral view, with head to the right (scale line ⫽ 4 mm). 1: Ceriana ornata; 2: Polybiomyia bergrothi. as, anterior spiracle; p, proleg; c, crochets.

racic in origin as revealed by the position of landmark sensilla (Rotheray and Gilbert 1999). Within segments, a complex pattern of sensilla, impressed lines, and folds in addition to segmental boundary lines is present. However, these sensilla, lines and folds are relatively constant within Syrphidae, including Cerioidini, but they are useful markers for particular segmental positions. Similarly constant are the prolegs that in higher Eristalinae, including Cerioidini become smaller from the Þrst to the sixth abdominal segment and in the orientation of crochets from being on the anterior margin on segment 1 to the lateral margin on segment 6. Species Descriptions Ceriana ornata (Saunders) (Figs. 1 and 3, 7, 16) Larva (puparium represented in Fig. 1). Length: 10.83Ð11.17 mm; width 5.25Ð5.5 mm (n ⫽ 3); head skeleton (Fig. 3): length of ventral cornu 1.34 mm; indentation index 15%; pharyngeal sclerite with heavily sclerotized dorsal cornu, which is upright, not curved; sclerotization extending linearly along the medial part of the ventral cornu; anterior spiracles: length 0.19 Ð 0.22 mm, basal width 0.2Ð 0.21;12 spiracular openings (n ⫽ 3); mesothoraic prolegs with 7Ð10 crochets in the primary row; abdomen: vestiture of Þne, 0.04 mm long, translucent setae arranged in rows across the secondary folds of each segment; vestiture shorter on the ventral surface; integumental markings absent; prolegs with seven to nine crochets in the primary row of segment 1, and eight in the primary row of segment 6; prp (Figs. 7 and 16): width at transverse band 0.86 Ð1.06 mm; width at apex 0.62Ð 0.64 mm; length between transverse band and apex 0.2Ð 0.28 mm (n ⫽ 3); dark brown with the transverse band taking the form of a deep groove; faint striations below

November 2007

RICARTE ET AL.: EARLY STAGES OF CERIOIDINE SYRPHIDS

917

Ceriana tridens (Loew) (Figs. 8 and 17)

Figs. 3–5. Type head skeletons (scale line ⫽ 1 mm). 3: Ceriana ornata; 4: Monoceromyia superba; 5: Polybiomyia macquarti. dc, dorsal cornu; ps, pharyngeal sclerite; vc, ventral cornu.

the band and above, coriaceous with conspicuous domed surface, shiny and with a deep longitudinal, mid-dorsal impression from apex to transverse band on both dorsal and ventral margins; spiracular plate with a raised border bearing highly convoluted spiracular openings. Taxonomic Notes. Readily distinguished from all other species considered here by the respiratory organs. The anterior spiracles have 12 openings, other species have six or four. The prp is wider than long with a grooved transverse band and the spiracular openings are convoluted, not simple curves. No other species has these characters. However, in having abdominal vestiture of Þne setae arranged in rows across the secondary folds within segments C. ornata is similar to M. superba, M. tricolor, P. pedicellate, and P. signifera. Material Examined. AUSTRALIA: Brisbane: one puparium (labeled together with an adult), Trigona parasite, January 1888, H. Hoskings (SI); 30 larvae and three puparia, ex hive of Trigona carbonaria Smith, 1854 bees (Hymenoptera, Apidae), February 2002, T. A. Heard (NMS).

Puparium. Length 10.67 mm; width 4.17 mm (n ⫽ 1); head skeleton: length of the ventral cornu 1.56 mm; indentation index 15.2%; pharyngeal sclerite at junction of dorsal and ventral cornea with area of black sclerotization small, like M. superba (Fig. 4); anterior spiracles: missing from specimen; mesothoracic prolegs: with six to seven crochets in the primary row; abdomen: vestiture of 0.04 Ð 0.12 mm long setae; middorsal line of the puparium almost bare, pale; upper lateral margin of each abdominal segment with an inclined band of black setae; lower lateral margin with U-shaped bands of setae forming an almost continuous line; between these bands sensilla surrounded by groups of black setae; prolegs with dark-brown crochets; seven to eight crochets in the primary row of segment one and six in the primary row of segment 6; prp (Figs. 8 and 17): width at transverse band 0.48 mm; width at apex 0.32 mm; length between transverse band and apex 0.84 mm; light-brown, with a distinct transverse band; light and conspicuous striations below the band and above, shiny and with coarse punctures gradually smaller toward the apex; dorsal and ventral spiracular openings almost straight, middle openings recurved. Taxonomic Notes. The following characters distinguishes the early stages of this species: length of prp above transverse band ⬍2⫻ width at transverse band; vestiture absent on mid-dorsum of abdominal segments 1Ð7; middle pair of spiracular openings on prp recurved. Most similar to M. tricolor and P. macquarti in having a short prp but the recurved middle spiracular openings and absence of mid-dorsal, abdominal vestiture separates C. tridens. Material Examined. USA: California: one puparium (labeled with its adult): Contra Costa Co., 14-IV-12, pres. by J. G. Grundel, identiÞed by F. C. Thompson, 76 (SI). Monoceromyia rubrobrunnea (Hull) (Figs. 9 and 18) Puparium. Length 11.67 mm; width 4.17 mm (n ⫽ 1); head skeleton: length of the ventral cornu 2.2 mm; indentation index 18.5%; pharyngeal sclerite at junction of dorsal and ventral cornea black and sclerotized, sclerotization extending linearly along the upper margin of the ventral cornu; anterior spiracles: missing from specimen; mesothoracic prolegs: with 13Ð16 crochets in the primary row; abdomen: vestiture varied in size and color from 0.02 to 0.16 mm long setae; vestiture forming a complex pattern of long black setae and short pale setae; mid-dorsally and on each abdominal segment is a H-shaped arrangement of black setae forming a broad interrupted band of dark setal patches; upper lateral margin of each abdominal segment with an inclined band of black setae; lower lateral margin with U-shaped bands of setae forming an almost continuous line; between these bands sensilla surrounded by groups of black setae; ventral surface

918

ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA

mostly bare without vestiture; prolegs with 12Ð14 black crochets in the primary row of segment 1 and 5 on segment 6; prp (Figs. 9 and 18): width at transverse band 0.62 mm; width at apex 0.44 mm; length between transverse band and apex 1.6 mm; transverse band indistinct; light striations below the band and shiny and Þnely punctured above; spiracular openings slightly curved. Taxonomic Notes. The early stages of this species can be distinguished by the following characters: length of prp above transverse band between 2 and 2.5⫻ width at transverse band; mid-dorsal vestiture on abdominal segments 1Ð7 forming H-shapes; spicules absent on dorsum of prothorax; middle spiracular openings slightly curved, not recurved. The early stages of this species are most similar to P. bergrothi and S. barbipes in having a mid-dorsal, H-shaped arrangement of vestiture on abdominal segments 1Ð7. However, in M. rubrobrunnea the length of prp above the transverse band is 2.5⫻ the width at transverse band that separates it from P. bergrothi, which is 3⫻ as long in relation to width and S. barbipes, which is 2.5⫻ as long. Material Examined. COSTA RICA: Guanacaste: one puparium (labeled with its adult), Santa Rosa, ex sap exudations on Guanacaste trees, 26-VI-2000, E. G. Hancock and G. E. Rotheray. Monoceromyia superba (Williston) (Figs. 4 and 10, 19) Puparium. Length10 Ð12.17 mm; width 3.8 Ð 4.67 (n ⫽ 4); head skeleton (Fig. 4): length of the ventral cornu 1.72 mm; indentation index 16.7%; pharyngeal sclerite only black and heavily sclerotized at the base of dorsal cornu; dorsal cornu recurved; anterior spiracles: length 0.13Ð 0.14 mm; width 0.13Ð 0.17; four spiracular openings (n ⫽ 3); mesothoracic prolegs: prolegs with Þve or six crochets in the primary row; abdomen: vestiture translucent and inconspicuous, 0.03 mm long and arranged in rows across the secondary folds of each segment; prolegs with 11Ð15 crochets in the primary row of segment 1, and Þve or six in the primary row of segment 6; prp (Figs. 10 and 19): width at transverse band 0.64 Ð 0.76 mm; width at apex 0.4 Ð 0.46 mm; length between transverse band and apex 1.2Ð1.52 mm; transverse band indistinct; light striations below the band and shiny and inconspicuously punctured above; spiracular opening slightly curved. Taxonomic Notes. The early stages of M. superba are most similar to P. pedicellata and P. signifera in having the length of the prp ⬎2⫻ the width at the transverse band and having rows of vestiture on the abdomen. The following characters separate the early stages of M. superba: length of prp above transverse band ⬎2⫻ the width at transverse band; dorsum of abdomen with vestiture arranged in rows on secondary folds; middle spiracular openings of the prp slightly curved. Material Examined. COSTA RICA: one puparium (labeled with its adult) collected as larva, San Jose´ , Mora, Z.P. El Rodeo, camino a rõ´o Jaris, 800m, LN-

Vol. 100, no. 6

Fig. 6. Monoceromyia tricolor pro- and mesothorax in ventral view (scale line ⫽ 1 mm). af, anterior fold; as, anterior spiracle; c, crochets; h, hooks; p, proleg; s, spicules.

210450N, 504400E, from unknown substrate, 15-V-97, M. Zumbado; one puparium (labeled with its adult) collected as larva, Guanacaste, A´ rea de Conservacio´ n Guanacaste, Estacio´ n Santa Rosa, 300 m, LN-313000, 359800E, ex hole in Spondias mombin L. (Anacardiaceae), 26-VI-2000, E. G. Hancock and G. E. Rotheray; two puparia (labeled with their adults), Guanacaste, Santa Rosa, ex sap exudations on Guanacaste trees, 26-VI-2000, E. G. Hancock and G. E. Rotheray. Monoceromyia tricolor (Loew) (Figs. 6 and 11, 20) Puparium. Length 10 Ð10.83 mm; width 3.67Ð 4.17 mm (n ⫽ 2); head skeleton: length of the ventral cornu 1.6 mm; indentation index 13%; pharyngeal sclerite black and heavily sclerotized at the junction of dorsal and ventral cornea and extending into the dorsal cornu; anterior spiracles: length 0.12; basal width 0.1 mm; with four spiracular openings; mesothoracic prolegs: with nine crochets in the primary row; mesothorax with apices of the pair of parallel longitudinal folds on the lateral margins beyond sensilla four and Þve with three or four hooks on lower fold with four to six larger hooks on the upper fold (Fig. 6); abdomen: vestiture translucent, 0.05 mm long in rows on secondary folds of the abdominal segments; prolegs with nine crochets in the primary row of segment 1, and six in the primary row of segment 6; prp (Figs. 11 and 20): width at transverse band 0.48 Ð 0.6 mm; width at apex 0.38 Ð 0.56 mm; length between transverse band and apex 0.9 Ð 0.98 mm; transverse band distinct; light striations below the band and deeply punctured above; dorsal and ventral spiracular openings almost straight, middle openings recurved. Taxonomic Notes. Easily distinguished from all other species considered here by the hooks on the mesothorax (Fig. 6). However, in having abdominal vestiture of Þne setae arranged in rows across the secondary folds within segments M. tricolor is similar to C. ornata, M. superba, P. pedicellate, and P. signifera. It shares a recurved middle pair of spiracular openings on the prp with P. pedicellata. P. signifera and shares

November 2007

RICARTE ET AL.: EARLY STAGES OF CERIOIDINE SYRPHIDS

919

Figs. 7–15. Posterior respiratory processes (prp) of cerioidine species showing the tube sculpture in dorsal view (scale line ⫽ 1 mm). 7: Ceriana ornata; 8: Ceriana tridens; 9: Monoceromyia rubrobrunnea; 10: Monoceromyia superba; 11: Monoceromyia tricolor; 12: Polybiomyia bergrothi; 13: Polybiomyia macquarti 14: Polybiomyia pedicellata; 15: Sphiximorpha barbipes. Drawing notes: transverse band marked by an arrow; realistic color shades are not represented to show clearly the diagnostic characters; P. bergrothi, P. pedicellate, and S. barbipes prp drawn reticules are not so conspicuous in the real specimens.

with C. ornata a short prp, ⬍2⫻ as long as the width of the transverse band. Material Examined. CUBA: La Habana, Jardõ´n Bota´nico: two puparia labeled and one adult collected as larvae, ex exudation of sap from tree of an unidentiÞed Clusia L. (Clusiaceae), 10-II-2001, M. A. Marcos-Garcõ´a (CIBIO). Polybiomyia bergrothi (Williston) (Figs. 2 and 12, 21) Puparium (Fig. 2). Length 9.2Ð9.92 mm; width 4 Ð 4.33 mm (n ⫽ 4); head skeleton: as in P. macquarti (Fig. 5), except length of the ventral cornu 1.58 mm; indentation index 24.1%; pharyngeal sclerite black and heavily sclerotized at the junction of dorsal and ventral cornea and extending anteriorly along the base of dorsal cornu; anterior spiracles: length 0.19 Ð 0.2 mm; width 0.16 Ð 0.17 mm; six spiracular openings (n ⫽ 4); mesothoracic prolegs: with 8 Ð10 crochets in the primary row; abdomen: vestiture varied in size from 0.14 to 0.18 mm long; forming a complex pattern of long

brown and short setae; mid-dorsally and on each abdominal segment is a H-shaped arrangement of brown setae forming a broad interrupted band of brown setal patches; upper lateral margin of each abdominal segment with an inclined band of brown setae; lower lateral margin with U-shaped bands of setae forming an almost continuous line; between these bands sensilla surrounded by groups of brown setae; ventral surface with transverse rows of setae between the prolegs; prolegs with 7Ð11 primary crochets on segment 1 and 2 to four primary crochets on segment 6; prp (Figs. 12 and 21): width at transverse band 0.5Ð 0.72 mm; width at apex 0.28 Ð 0.4 mm; length between transverse band and apex 1.68 Ð2.6 mm (n ⫽ 4); distinctly tapered toward the apex, with an indistinct transverse band; faint striations below the band; mostly shiny above with very Þne punctures aggregated about the medial region and less so toward the apex. Taxonomic Notes. The early stages of P. bergrothi are most similar to M. rubrobrunnea and S. barbipes in having a mid-dorsal, H-shaped arrangement of vesti-

920

ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA

Vol. 100, no. 6

beled with their adults) collected as larvae, 26-II-99, D. Bricen˜ o, E.G. Hancock and G. E. Rotheray. Polybiomyia macquarti Shannon (Figs. 5 and 13, 22)

Figs. 16–24. Posterior respiratory processes (prp) of cerioidine species showing the spiracular plate in polar view (scale line ⫽ 1 mm). 16: Ceriana ornata; 17: Ceriana tridens; 18: Monoceromyia rubrobrunnea; 19: Monoceromyia superba; 20: Monoceromyia tricolor; 21: Polybiomyia bergrothi; 22: Polybiomyia macquarti; 23: Polybiomyia pedicellata; 24: Sphiximorpha barbipes. so, spiracular openings. Drawing notes: up is dorsal and down is ventral; realistic color shades are not represented to show clearly the diagnostic characters.

ture on abdominal segments 1Ð7. P. bergrothi may be distinguished from these species by the very long prp, which is 3⫻ longer above the transverse band than the band is wide. The prp is shorter in both other species. Also by the anterior spiracles, which have six spiracular openings, four in the other species. Material Examined. COSTA RICA: Limo´ n, Talamanca, Sixaola, San Miguel, Sendero El Cerrillo, 10 Ð 65 m, LS-39100N, 612000E, ex sap exudation on Carapa guianensis Aubl. (Meliaceae): four puparia (la-

Puparium. Length 8.58 Ð9.33 mm; with 3.33Ð 4.08 mm (n ⫽ 4); head skeleton (Fig. 5): length of the ventral cornu 1.18 mm; indentation index 14.3%; pharyngeal sclerite black and heavily sclerotized at the junction with the dorsal cornu, which is recurved; area of sclerotisation extending linearly along the upper margin of the ventral cornu; anterior spiracles: length 0.14 Ð 0.16 mm; width 0.1Ð 0.12 mm; (n ⫽ 4); four spiracular openings; mesothoracic prolegs: with 7Ð10 crochets in the primary row; abdomen: vestiture varied in size and color, from 0.04 to 0.1 mm long, forming a complex pattern with long blackish-brown setae and short paler setae and dark, mid-dorsal integumental markings on abdominal segments 1Ð7; upper lateral margin of each abdominal segment with an inclined band of setae; lower lateral margin with U-shaped bands of setae forming an almost continuous line; between these bands sensilla on a black ßeshy papillae; ventral surface mostly bare; prolegs with 8 Ð10 crochets in the primary row of segment 1 and 5Ð10 in the primary row of segment 6; prp (Figs. 13 and 22): width at transverse band 0.4 Ð 0.5 mm; width at apex 0.28 Ð 0.38 mm; length between transverse band and apex 0.64 Ð 0.72 mm (n ⫽ 4); with a distinct, transverse band; light but clear striations below the band and shiny and moderately-coarse punctured above; spiracular openings slightly curved. Taxonomic Notes. The early stages of this species are similar to those of others such as M. rubrobrunnea, P. bergrothi, P. signifera, and S. barbipes that have a complex pattern of vestiture on the abdomen. However, P. macquarti is easily separated from these species by the dark, blotch-like markings on the middorsal line of the abdomen, a character shared only with P. signifera and from that species by the short prp which is 1.5⫻ as long above the transverse band as it is wide at the band. Material Examined. COSTA RICA: Guanacaste: three puparia (labeled with their adults) collected as larvae, Can˜ as, Palmira, 200 Ð250 m, LN-280500N, 418650E, ex exuding sap on Spondias purpurea L. (Anacardiaceae), 13-VI-99, J. D. Gutie´ rrez (INBio); one puparium (labeled with its adult) collected as larva, 7-VI-2000. Polybiomyia pedicellata (Williston) (Figs. 14 and 23) Puparium. Length 8.58 Ð11.33 mm; width 3.33Ð 4.17 mm (n ⫽ 4); head skeleton length of the ventral cornu 1.88 mm; indentation index 14.3%; pharyngeal sclerite pale, and slightly sclerotized at the junction of dorsal and ventral cornea, with this sclerotisation extending linearly along the upper margin of the ventral cornu; anterior spiracles: length 0.15Ð 0.18 mm; width 0.12 mm; four spiracular openings (n ⫽ 4); mesothoraic

November 2007

RICARTE ET AL.: EARLY STAGES OF CERIOIDINE SYRPHIDS

921

Figs. 25–27. Polybiomyia signifera SEMs showing general morphology of cerioidine thoracic plate, prp and sipracular plate (scale in each picture). 25 (scale ⫽ 1 mm): pupal plate bearing anterior spiracles in dorsal view; 26 (scale ⫽ 1 mm): prp in ventro-lateral view; 27 (scale ⫽ 200 ␮m): prp showing the spiracular plate and setae in polar view (up is dorsal and down is ventral). af, anterior fold; as, anterior spiracle; so, spiracular openings; tb, transverse band.

prolegs: with 9 Ð13 crochets in the primary row; abdomen: vestiture of Þne, 0.14 mm long, translucent setae arranged in rows across the secondary folds of each segment; vestiture shorter on the ventral surface; integumental markings absent; prolegs with 11Ð17 crochets in the primary row of segment 1 and four to six in the primary row of segment 6; prp (Figs. 14 and 23): width at transverse band 0.48 Ð 0.56 mm; width at apex 0.3Ð 0.4 mm; length between transverse band and apex 1.36 Ð1.72 (n ⫽ 3); yellowish-brown, with an indistinct, transverse band; conspicuous striations and matt surface below the band; aggregated punctures above the band; middle spiracular openings recurved, dorsal and ventral openings slightly curved. Taxonomic Notes. The early stages of P. pedicellata are most similar to those of M. superba and P. signifera in having transverse rows of abdominal vestiture and a prp with length above the transverse band of 2⫻ the width at the band. They can be distinguished from those of P. signifera by the uniform length of the abdominal vestiture and from those of M. superba by the recurved middle pair of spiracular openings on the prp. Material Examined. COSTA RICA: Guanacaste: four puparia (labeled with their adults) collected as larvae, A´ rea de Conservacio´ n Guanacaste, Estacio´ n Santa Rosa, Bosque Hu´ medo, 300 m, LN-313000, 359800E, ex hole with leaves and decaying organic material in tree of Hymenaea courbaril L. (Fabaceae), 25-I-2001, D. Bricen˜ o. Polybiomyia signifera (Loew) (Figs. 25 and 26, 27) Puparium. Length 12.67Ð13.83 mm; width 4.08 Ð 4.75 mm (n ⫽ 4); head skeleton: length of the ventral cornu 1.86 mm; indentation index 28%; pharyngeal sclerite at junction of dorsal and ventral cornea black and sclerotized and sclerotization extending linearly along the upper margin of the ventral cornu; anterior spiracles (plate bearing them, in Fig. 25): length 0.12Ð 0.14 mm; width 0.08 Ð 0.1 mm; four spiracular openings (n ⫽ 4); mesothoracic prolegs: with 10 Ð12 crochets in the primary row; abdomen: vestiture varied in size and color, from 0.04 to 0.2 mm long, forming a complex pattern with long blackish brown setae and short paler setae

and dark, mid-dorsal integumental markings on abdominal segments 1Ð7; upper lateral margin of each abdominal segment with an inclined band of setae; lower lateral margin with U-shaped bands of setae forming an almost continuous line; between these bands sensilla on a black ßeshy papillae; ventral surface mostly bare; prolegs with seven to nine crochets in the primary row of segment 1, and four or Þve in the primary row of segment 6; prp (Figs. 26 and 27): width at transverse band 0.54 Ð 0.68 mm; width at apex 0.38 Ð 0.48 mm; length between transverse band and apex 1.44 Ð1.8 mm (n ⫽ 4); transverse band indistinct, below without obvious striations and above moderately coarse punctured; spiracular openings slightly curved. Taxonomic Notes. The early stages of P. signifera are similar to those of others such as M. rubrobrunnea, P. bergrothi, P. macquarti, and S. barbipes that have a complex pattern of vestiture on the abdomen. However P. signifera is easily separated from these species by the dark, blotch-like markings on the mid-dorsal line of the abdomen, a character shared only with P. macquarti and from that species by the long prp, which is ⬎2⫻ as long above the transverse band as it is wide at the band. Material Examined. ME´ XICO: Hidalgo: eight puparia collected as larvae, Santo Domingo, the wet central part of a cut “Maguey” (Agave L., Agavaceae), 15-VI-2006, M. A. Marcos-Garcõ´a, CIBIO. Pupation (P) and adult (A) emergence dates: 1 male and 1 female, P/14-VII-2006, A/26-VII-2006; 1 male, P/2VIII-2006, A/12-VIII-2006; 1 female, P/18-VIII-2006, A/4-IX-2006; 1 female, P/29-VIII-2006, A/15-IX-2006; 1 female, P/10-X-2006, A/22-X-2006. Sphiximorpha barbipes (Loew) (Figs. 15 and 24) Puparium. Length 10.33Ð11.33 mm; width 3.5Ð 4.33 mm (n ⫽ 3); head skeleton: length of the ventral cornu 1.96 mm; indentation index 16%; pharyngeal sclerite at junction of dorsal and ventral cornea black and sclerotized, sclerotization extending linearly along the upper margin of the ventral cornu; prothorax: anterior margin of the dorsum with 7Ð 8 spicules; anterior spiracles: length 0.18 Ð 0.2, basal width 0.1Ð 0.11 mm; four spiracular openings (n ⫽ 2); mesothoracic prolegs

922

ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA

with 12Ð14 crochets in the primary row; abdomen: vestiture varied in size and color from 0.02 to 0.12 mm long, forming a complex pattern of long blackish setae and short paler setae; mid-dorsally and on each abdominal segment is a H-shaped arrangement of setae forming a broad interrupted band of dark setal patches; upper lateral margin of each abdominal segment with an inclined band of setae; lower lateral margin with U-shaped bands of setae forming an almost continuous line; between these bands sensilla surrounded by groups of black setae; ventral surface bare; prolegs with 11Ð15 brown crochets in the primary row of segment one and 10 Ð11 in the primary row of segment 6; prp (Figs. 15 and 24): width at transverse band 0.66 Ð 0.72 mm; width at apex 0.4 Ð 0.42 mm; length between transverse band and apex 1.4 Ð1.46 mm (n ⫽ 3); dark brown, transverse band distinct; below the band coriaceous and smooth and above shiny, with very Þne punctures aggregated about the medial region and less so toward the apex; dorsal and ventral spiracular openings almost straight, middle openings recurved. Taxonomic Notes. The early stages of S. barbipes are identiÞable from the unique character of spicules on the dorsum of the prothorax. Apart from this, the following combination of characters separates the early stages of S. barbipes from other species studied here: length of prp above transverse band ⬎2⫻ width at transverse band; mid-dorsal vestiture on abdominal segments 1Ð7 forming H-shapes; spicules on dorsum of prothorax; 10 Ð11 crochets on prolegs of abdominal segment 6. The early stages of this species are most similar to M. rubrobrunnea and P. bergrothi in having a mid-dorsal, H-shaped arrangement of vestiture on abdominal segments 1Ð7 and either side of which are clumps of setae and inclined bars. From a distance, the puparia of these species look mottled due to this pattern. A similar mottled appearance is present in the puparia of C. tridens and P. macquarti but mid-dorsally vestiture is absent in the former species and black integumental markings not setae are present in the latter species. Material Examined. BRAZIL: Bahia: one puparium (labeled with its adult), ex tree hole, March 1929, Rockefeller Foundation., Lab. Shannon; two puparia (labeled with their adults), same data but collected in Piraje from bamboo, April 1929 (SI). Discussion The absence of pupal spiracles, invaginated mandibles and mandibular lobes and grouped spicules on the prothoracic anterior fold are diagnostic early stage characters for the Cerioidini (Rotheray and Gilbert 1999). The puparia of the 10 species described here also possess these characters and this adds support to their diagnostic value. Other early stage characters shared by the species studied here and those described previously where these characters are either Þgured or described, are a tapered apex to the prp and developed mesothoracic and abdominal prolegs with three rows of relatively large crochets per proleg.

Vol. 100, no. 6

Within the Cerioidini, the validity of genera, their limits and included species are not settled (Shannon 1927, Riek 1954, Vockeroth 1971, Whittington 2003). We studied the early stages of two species of Ceriana, three of Monoceromyia, four of Polybiomyia and one Sphixomorpha but did not Þnd any characters that either uniquely or in combination, support these genera. Nor did we Þnd groupings of species based on shared characters irrespective of these genera. For example the 10 species can be divided into two equal groups based on those that have complex patterns of vestiture (M. rubobrunnea, P. bergrothi, P. macquarti, P. signifera and S. barbipes) and those that have uniform rows of vestiture (C. ornata, C. tridens, M. superba, M. tricolor, and P. signifera). However, no other characters correlate to these groups, either in the locomotory or respiratory organs and no correlations were found between the various states of these latter characters and particular taxa or breeding site. Furthermore, we found no correlations between the indentation index and the length of the ventral cornu in the head skeleton and variation in these features did not correlate with genera or liquidity of breeding site. This could mean that early stages are not informative for supraspeciÞc relationships within Cerioidini. But, this would be unusual because in other Syrphidae early stages are a valuable source of phylogenetic information (Rotheray and Gilbert 1999, Ståhls et al. 2003). Alternatively, lack of support from early stages could mean that currently recognized genera do not represent monophyletic groups. It also could indicate that supraspeciÞc groups do not exist within the Cerioidini but with a lineage of 197 species, this seems unlikely. The problem is probably inadequate sampling. When a greater proportion of early stages are studied, characters will probably be found that better evaluate proposed genera and their limits. Published descriptions of cerioidine early stages involve only nine species (Lundbeck 1916, Bhatia 1931, Heiss 1938, Lane and Carrera 1943, Rotheray et al. 1998, Sivova 1999, Krivosheina 2001, Rotheray et al. 2006). Unfortunately, many of these lack the detail required for evaluating the validity of cerioidine genera. Nonetheless, from these studies and the descriptions presented here certain characters are clearly more plastic than others. For example, integumental vestiture is varied in size, shape, color, and density. In the simplest state vestiture is translucent and uniform in size and density as in C. ornata, M. superba, and P. pedicellata. In other species it forms patterns involving bars and clumped setae of varying size, density, and color like in M. rubrobrunnea and S. barbipes. Such patterning may be enhanced by pale or dark markings within the integument as in C. tridens, P. macquarti, and P. signifera. However, these markings are conÞned to the puparium. The posterior respiratory process (prp) is also very variable not only in length but also in surface sculpturing and shape of the spiracular openings (Figs. 7Ð24, 26, and 27). Such variability contrasts with structures like the head skeleton that varies little in size or

November 2007

RICARTE ET AL.: EARLY STAGES OF CERIOIDINE SYRPHIDS

shape and the locomotory organs that tend to be uniform varying only in the color and occasionally the number of crochets. For example, M. superba and C. tridens stand out in having mesothoracic prolegs with a mean of six primary crochets in contrast to the remaining species that have a mean of nine. There are also unique characters such as the very convoluted spiracular openings and broader than long prp of C. ornata and the mesothoracic hooks of M. tricolor. Most cerioidine rearing records come from exuded tree sap (Lundbeck 1916, Bhatia 1931, Heiss 1938, Maier 1982, Maier 1987, Rotheray et al. 1998, Sivova 1999, Krivosheina 2001). However, exceptions exist. For example, Lane and Carrera (1943) reared Ceriana odontomera (Curran 1941) from cut bamboo. But, Rotheray et al. (1998) reared this species from tree sap. Rotheray et al. (2006) reared Ceriana vespiformis (Latreille, 1809) from wet, decaying, Fraxinus L. tree roots. Sivova (1999)) reared Ceriana nigerrima Violovitsh, 1974 from holes in Ulmus L. trees, and Krivosheina (2001) reared Ceriana naja Violovitsh, 1974 from holes in Populus L. trees. But, both species also were reared from tree sap. Further exceptions to tree sap are recorded in our study. In Australia, C. ornata was reared from the nests of Trigona bees, but Cockerell (personal communication in Rayment 1932) says “they are not really parasites.” Then, larvae are probably saprophagous feeding on debris of the bee colony. In Me´ xico, P. signifera was reared from the liquid center of a cut Agave. In Brazil, S. barbipes was reared from tree holes and bamboo. Finally, in Costa Rica, M. superba and P. pedicellata were reared from tree holes. The nature of the various breeding sites may explain some of the morphological features of cerioidine early stages. The spicules of the anterior fold are large and well developed in relation to other eristaline syrphid larvae. In sticky, viscous media such as tree sap, the spicules probably protect the front of the larva during feeding and forward locomotion which involves the thorax being expanded forward and retracted repeatedly. Facilitating expansion and contraction, the thorax collapses along characteristic impressed lines that cover the thorax (Rotheray and Gilbert 1999). However at the front of the thorax, large spicules may interfere with contraction. To overcome this restriction, spicules are absent along the impressed lines of the anterior fold. This results in the diagnostic cerioidine feature of Þve spicule groups (Fig. 6). In other eristaline larvae that have spicules on the anterior fold, those next to impressed lines may be reduced in size or density but none examined to date, have grouped spicules. In the larva of S. barbipes the dorsum of the prothorax has several large spicules and in the larva of M. tricolor, hooks are present on the antero-lateral margins of the mesothorax (Fig. 6). As in many xylotines, armature like this protects the integument from wear and tear during movement (Rotheray and Gilbert 1999). Presumably, these hooks and spicules facilitate access or movement through the material of the breeding site in some specialized way in relation to congenerics, but this has yet to be demonstrated.

923

Pupation sites of ceriodine larvae are frequently exposed, within or close to the breeding site such as on bark in species breeding in tree holes and exudations of tree sap. Under these circumstances, they are probably exposed to predation. Complex patterns of vestiture, which in species such as C. tridens and P. macquarti also include integumental markings, may be disruptive in function and part of crypsis. They break up the outline of the puparium from visually hunting insectivores such as birds. Furthermore, as suggested by Bhatia (1931), absence of pupal spiracles, one of the diagnostic features of cerioidine early stages, may be explained by their habit of pupariation in exposed places in comparison with many eristalines, which characteristically pupate in partially or wholly submerged conditions. Pupal spiracles which protrude from the front of the puparium enable respiration in such conditions. Among other syrphids, loss of pupal spiracles is only a feature of higher Syrphinae which similarly pupariate in exposed places, in this case on plant substrates (Rotheray and Gilbert 1989). By lifting up the anal segment, the elongate and tapered prp can be exposed to the air for respiration. When this happens, the spiracular plates bearing the respiratory openings are “anchored” at the surface of the breeding medium by the water repellent, hinged, interspiracular setae which splay out and surround the apex of the prp. Presumably helped by surface tension, they prevent the openings from being blocked or ßooded. Hence, the larva can respire yet move and feed at the same time. The wide variation observed in the length of the prp may correlate to characteristic depths at which larvae feed and respire. However, such correlations have yet to be demonstrated. All tree hole species in our sample had relatively long prps, and depths are probably greater in holes than in exudations of tree sap. However, two species with long prps were reared from only exuding sap, M. rubrobrunnea (Figs. 9) and P. bergrothi (Figs. 2 and 12). The prp of C. ornata is exceptionally short being broader than long (Figs. 7 and 16). The larva of this species develops in bee nests where a short prp may be protective in that it cannot be grabbed by worker bees, or it may simply reßect a way of life where it is rarely submerged. Acknowledgments We thank Chris Thompson for help, encouragement, and access to manuscript keys and for arranging loans of material from the United States National Museum. We thank Manuel Zumbado for help during Þeldwork in Costa Rica and for arranging a loan of material from INBio. We also thank the Diptera parataxonomists who helped Þnd, collect, and rear cerioidines, particularly Manuel Solis, Duvalier Bricen˜ o, and Daniel Gutie´ rrez. Thanks to Tim Heard for larvae of C. ornata from Australia and to Francis Gilbert who helped arrange for us to see this material. We are particularly grateful to the Leverhulme Trust in the United Kingdom for a research fellowship to G.E.R. Financial support was provided by “Agencia Espan˜ ola de Cooperacio´ n Internacional” A/4426/ 05, the Spanish “Ministerio de Educacio´ n y Ciencia” project CGL2005-07213/BOS, and grant AP 2003-4001.

924

ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA References Cited

Bhatia, M. L. 1931. Life histories of Indian Syrphidae. Indian J. Agric. Sci. 1: 503. Evenhuis, N. L., T. Pape, A. C. Pont, and F. C. Thompson. 2007. Biosystematic Database of World Diptera. (http:// www.sel.barc.usda.gov/Diptera/biosys.htm). Ferrar, P. 1987. A guide to the breeding habits and immature stages of Diptera Cyclorrhapha, Entomograph vol. 8. Lubrecht & Cramer Ltd, Leiden, The Netherlands. Hartley, J. C. 1961. A taxonomic account of the larvae of some British Syrphidae. Proc. Zool. Soc. Lond. 136: 505Ð 573. Hartley, J. C. 1963. The head apparatus of syrphid larvae and its relationship to other Diptera. Proc. Zool. Soc. Lond. 141: 261Ð280. Heiss, E. M. 1938. A classiÞcation of the larvae and puparia of the Syrphidae of Illinois exclusive of aquatic forms. Univ. Ill. Bull. 36: 1Ð142. Hull, F. M. 1944. Studies of ßower ßies (Syrphidae) in the Vienna Museum (Natural History). J. Wash. Acad. Sci. 34: 398Ð404. Krivosheina, M. G. 2001. To the biology of the xylophilous ßies of the genus Ceriana RaÞnesque, 1815 (Diptera: Syrphidae) with the descriptions of the larvae and puparia of C. caesarea Stackelberg and C. naja Violovitsh. Int. J. Dipterol. 12: 57Ð64. Lane, J., and M. Carrera. 1943. Soˆ bre o geˆ nero Cerioides (Diptera, Syrphidae, Cerioidini). Rev. Entomol. Rio de Janeiro 14: 167Ð173. Loew, H. 1853. Neue Beitrage zur Kenntniss der Dipteren. Erster Beitrag. Progr. K. Realschule Meseritz 1853: 1Ð38. Loew, H. 1861. Diptera aliquot in insula Cuba collecta. Wien. Entomol. Monatschr. 5: 33Ð 43. Loew, H. 1872. Diptera Americae septentrionalis indigena. Centuria decima. Berl. Entomol. Z. 16: 49 Ð124. Lundbeck, W. 1916. Diptera Danica, 5 (Lonchopteridae, Syrphidae). Copenhagen, Denmark. Maier, C. T. 1982. Larval habitats and mate seeking sites of ßowerßies (Diptera, Syrphidae, Eristalinae). Proc. Entomol. Soc. Wash. 84: 603Ð 609. Maier, C. T. 1987. New distributional and rearing records for the Neotropical ßower ßies (Diptera, Syrphidae). Proc. Entomol. Soc. Wash. 89: 369. Rayment, T. 1932. The stingless bees of AustraliaÐ5. Is there a symbiotic association? Vict. Nat. 49: 39 Ð 43. Riek, E. F. 1954. The Australian syrphid ßies of the subfamily Cerioidinae (Diptera: Syrphidae): systematics and wing folding. Austr. J. Zool. 2: 100 Ð130. Roberts, M. J. 1970. The structures of the mouthparts of syrphid larvae (Diptera) in relation to feeding habits. Acta Zool. Stockh. 51: 43Ð 65. Rotheray, G. E. 1993. Colour guide to hoverßy larvae (Diptera: Syrphidae). Dipterist Digest No. 9. Derek Whitely, ShefÞeld, United Kingdom. Rotheray, G. E., and F. Gilbert. 1989. The phylogeny and systematics of European predacious Syrphidae (Diptera) based on larval and puparial stages. Zool. J. Linn. Soc. 95: 29 Ð70.

Vol. 100, no. 6

Rotheray, G. E., and F. Gilbert. 1999. Phylogeny of Palaeartic Syrphidae (Diptera): evidence from larval stages. Zool. J. Linn. Soc. 127: 1Ð112. Rotheray, G. E., E. G. Hancock, and C. T. Maier. 1998. The larvae of two Ceriana species (Diptera: Syrphidae) breeding in exuded tree sap. Entomol. Mon. Mag. 134: 223Ð228. Rotheray, G. E., C. Dussaix, M. A. Marcos-Garcı´a, and C. Pe´rez-Ban˜ o´ n. 2006. The early stages of three Paleartic species of saproxylic hoverßies (Syrphidae, Diptera). Micron 37: 73Ð 80. Saunders, W. W. 1845. On the species of the genus Ceria Fab. Trans. Entomol. Soc. Lon. 4: 63Ð 66. Shannon, R. C. 1925. The syrphid-ßies of the subfamily Ceriodinae in the U.S. National Museum Collection. Insecutor Inscit. Menstr. 13: 48 Ð52, 53Ð 65. Shannon, R. C. 1927. Notes on and descriptions of syrphid ßies of the subfamily Cerioidinae. J. Washington Acad. Sci. 17: 38 Ð53. Sivova, A. V., V. A. Mutin, and D. I. Gritskevich. 1999. Syrphid larvae (Diptera: Syrphidae) living in Ulmus pumila L. in Komsomolsk-on-Amur. Far East. Entomol 71: 1Ð 8. Ståhls, G., H. Heikki, G. E. Rotheray, J. Muona, and F. Gilbert. 2003. Phylogeny of Syrphidae (Diptera) inferred from combined analysis of molecular and morphological characters. Syst. Entomol. 28: 433Ð 450. Thompson, F. C. 1972. A contribution to a generic revision of the Neotropical Milesiinae (Diptera, Syrphidae). Arq. Zool. (Sao Paulo) 23: 73Ð215. Thompson, F. C. 1999. A key to the genera of the ßower ßies (Diptera: Syrphidae) of the Neotropical Region including descriptions of new genera and species and a glossary of taxonomic terms. Contrib. Entomol. Int. 3: 322Ð378. Thompson, F. C., and G. E. Rotheray. 1998. Family Syrphidae, pp. 81Ð139. In L. Papp and B. Darvas [eds.], Contributions to a manual of Palaearctic Diptera, vol. 3. Science Herald, Budapest, Hungary. Vockeroth, J. R. 1971. Some changes in the use of the generic names in the tribe Cerioidini (Diptera: Syrphidae). Can. Entomol. 103: 282Ð283. Vockeroth, J. R., and F. C. Thompson. 1987. Syrphidae, pp. 713Ð743. In J. F. McApline [ed.], Manual of Neartic Diptera, vol. 2. Agriculture Canada, Ottawa, ON, Canada. Waldbauer, G. P. 1970. Mimicry of hymenopteran antennae by Syrphidae. Psyche 77: 45Ð 49. Waldbauer, G. P., and J. K. Sheldon. 1971. Phenological relationships of some aculeate Hymenoptera, their dipteran mimics and insectivorous birds. Evolution 25: 371Ð382. Waldbauer, G. P., J. G. Sternberg, and C. T. Maier. 1977. Phenological relationships of wasps, bumblebees, their mimics and insectivorous birds in an Illinois sand area. Ecology 58: 583Ð591. Whittington, A. E. 2003. The Afrotropical Syrphidae fauna: an assessment. Studia Dipterologica 10: 579 Ð 607. Williston, S. W. 1887. Synopsis of the North American Syrphidae. Bull. U.S. Natl. Mus. (1886) 31, xxx ⫹ 335 pp. Williston, S. W. 1892. Fam. Syrphidae. Biol-Centr.-Am. Ins: Dipt. 3: 1Ð56; 57Ð72; 73Ð78. Received 3 April 2007; accepted 28 June 2007.