Research Article |
Corresponding author: Michael S. Engel ( msengel@ku.edu ) Academic editor: Michael Ohl
© 2015 Jakub Straka, Abdulaziz S. Alqarni, Katerina Jůzová, Mohammed A. Hannan, Ismael A. Hinojosa-Díaz, Michael S. Engel.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Straka J, Alqarni AS, Juzova K, Hannan MA, Hinojosa-Díaz IA, Engel MS (2015) Rediscovered parasitism of Andrena savignyi Spinola (Hymenoptera, Andrenidae) by Stylops (Strepsiptera, Stylopidae) and revised taxonomic status of the parasite. ZooKeys 519: 117-139. https://doi.org/10.3897/zookeys.519.6035
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Parasitism of Andrena (Suandrena) savignyi Spinola (Hymenoptera: Andrenidae) by Stylops Kirby (Strepsiptera: Stylopidae) has been recorded only once, and from an individual collected in Egypt almost a century ago, with the parasite described as Stylops savignyi Hofeneder. The recent rediscovery of this Stylops from an individual of A. savignyi permits a reinterpretation of the species and its affinities among other Stylops. The bee was collected at flowers of Zilla spinosa (Turra) Prantl. (Brassicaceae) in Amariah, Riyadh, Kingdom of Saudi Arabia. Based on DNA barcode sequences from material sampled across Africa, Asia, and Europe, it is apparent that S. savignyi is conspecific with S. nassonowi Pierce, and we accordingly synonymize this name (syn. n.), with the latter representing the senior and valid name for the species. A differential diagnosis is provided for S. nassonowi and the morphology of the female is described, as well as the first instars.
Stylopidae , Apoidea , Anthophila , Andrenidae , parasitoid, taxonomy, morphology
Strepsiptera (twisted-wing parasites) are an order of minute entomophagous insects that are found throughout the world. Despite the fact that Strepsiptera comprise relatively few species for a lineage of Holometabola (ca. 600 species), the breadth of hosts is considerable and includes at least seven insect orders (Zygentoma, Blattaria, Mantodea, Orthoptera, Hemiptera, Hymenoptera, and Diptera) (
Contributing to the ‘mystery’ of the order is their complex parasitoid life cycle and conspicuous sexual dimorphism, with pronouncedly neotenic females. The male has an ephemeral, free-living adulthood, whereas adult females are obligatory endoparasites, with the sole exception of the basal family Mengenillidae, and are concomitantly tied to their host throughout their maturity (
The genus Stylops is the most diversified lineage of the family Stylopidae. Species are obligate parasites of solitary bees of the genus Andrena Fabricius (
One such taxonomic mystery that has persisted for nearly a century centers on the proper identity of Stylops savignyi
Individuals of A. savignyi were collected mostly from flowers of Zilla spinosa (Turra) Prantl. (Brassicaceae) at five localities around Amariah, Riyadh, Saudi Arabia (Al Oyanah, Al Kharj, Rouma, Derab, and Al Amariah, the last of which was where most material was sampled), although the species has also been encountered at various localities throughout Saudi Arabia and the Arabian peninsula (e.g., Dathe 2009; Engel pers. obs.). Details of the collection site are available in Alqarni et al. (2012,
Female of Andrena (Suandrena) savignyi Spinola from Riyadh, Saudi Arabia parasitized by Stylops nassonowi Pierce 1 Dorsal habitus of bee 2 Lateral habitus of bee (image inverted); one female of parasite observable at apex of tergum IV 3 Detail of setae at bee’s metasomal apex showing numerous first instars of the parasite.
Basic measurements of cephalothoraxes of Stylops aterrimus Newport and S. nassonowi Pierce (W = width at spiracles; L = length). All measurements in millimeters.
Species | Voucher | W | L | W of head | L of head | Intermandibular diameter |
---|---|---|---|---|---|---|
S. aterrimus | SAg1 | 1.35 | 1.29 | 0.77 | 0.34 | 0.14 |
SBm1a | 1.29 | 1.26 | 0.67 | 0.31 | 0.19 | |
SBm1b | 1.34 | 1.24 | 0.69 | 0.29 | 0.21 | |
STig2 | 1.07 | 1.10 | 0.64 | 0.37 | 0.19 | |
Ssp1 | 1.27 | 1.20 | 0.67 | 0.33 | 0.21 | |
SCa7 | 1.31 | 1.17 | 0.70 | 0.31 | 0.21 | |
SCa8 | 1.20 | 1.17 | 0.64 | 0.31 | 0.19 | |
S. nassonowi | SCa1 | 1.41 | 1.19 | 0.76 | 0.3 | 0.19 |
SCa4 | 1.41 | 1.27 | 0.74 | 0.32 | 0.19 | |
SCa5 | 1.21 | 1.19 | 0.70 | 0.35 | 0.19 | |
SCa6 | 1.09 | 1.10 | 0.61 | 0.31 | 0.18 | |
SCa9a | 1.19 | 1.17 | 0.70 | 0.32 | 0.20 | |
SCa9b | 1.33 | 1.18 | 0.70 | 0.30 | 0.20 | |
SCa10 | 1.10 | 1.11 | 0.61 | 0.30 | 0.18 | |
SSg1 | 1.05 | 1.24 | 0.60 | 0.30 | 0.19 | |
SHo1 | 1.36 | 1.27 | 0.67 | 0.34 | 0.19 | |
STi2 | 1.16 | 1.04 | 0.70 | 0.30 | 0.17 | |
STi4 | 1.27 | 1.19 | 0.69 | 0.34 | 0.19 | |
STi6 | 1.26 | 1.19 | 0.69 | 0.31 | 0.19 | |
STi5 | 1.26 | 1.21 | 0.73 | 0.36 | 0.19 |
The specimens of Stylops examined for the present study (
Morphological terminology of first-instar larvae follows that of
For DNA analysis, the entire body of a female strepsipteran was lysed by Proteinase K (Qiagen). Afterwards, DNA was isolated with a DNA Isolation Kit (Qiagen). Partial DNA sequences were amplified using the primers for Cytochrome oxidase subunit I (COI) (Jůzová et al. in press), and using an annealing temperature of 50 °C. Chromatograms were edited with the program Chromas Lite 2.01 (Technelysium Pty Ltd.) and aligned in BioEdit 7.0.9 (
Distances in DNA base composition were compared pairwise (Table
DNA distance matrix among samples of Stylops nassonowi Pierce, S. aterrimus Newport, and other representative species. Distances below 2% are highlighted yellow, showing closely related individuals; Stylops Kirby from Andrena (Suandrena) savignyi Spinola in Saudi Arabia indicated in red.
Stylops | S. m. | S. nev. | S. spreta | S. m. | S. ater | S. a. | S. a. | S. a. | S. a. | S. a. | S. a. | S. a. | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
voucher | SFl1 | SFu1 | SMi1 | SNi1 | SVa2 | SAg1 | SBm1 | STig1 | STig2 | Ssp1 | SCa7 | SCa8 | |
S. nevinsoni | SFu1 | 0.1075 | - | - | - | - | - | - | - | - | - | - | - |
S. spreta | SMi1 | 0.1243 | 0.1456 | - | - | - | - | - | - | - | - | - | - |
S. melittae | SNi1 | 0.0035 | 0.1081 | 0.1243 | - | - | - | - | - | - | - | - | - |
S. ater | SVa2 | 0.1440 | 0.1451 | 0.1746 | 0.1453 | - | - | - | - | - | - | - | - |
S. aterrimus | SAg1 | 0.1300 | 0.1355 | 0.1511 | 0.1276 | 0.1437 | - | - | - | - | - | - | - |
S. aterrimus | SBm1 | 0.1176 | 0.1353 | 0.1448 | 0.1157 | 0.1337 | 0.0151 | - | - | - | - | - | - |
S. aterrimus | STig1 | 0.1300 | 0.1355 | 0.1511 | 0.1276 | 0.1437 | 0.0000 | 0.0151 | - | - | - | - | - |
S. aterrimus | STig2 | 0.1410 | 0.1465 | 0.1632 | 0.1383 | 0.1533 | 0.0017 | 0.0178 | 0.0017 | - | - | - | - |
S. aterrimus | Ssp1 | 0.1300 | 0.1374 | 0.1489 | 0.1276 | 0.1415 | 0.0017 | 0.0134 | 0.0017 | 0.0035 | - | - | - |
S. aterrimus | SCa7 | 0.1155 | 0.1331 | 0.1426 | 0.1136 | 0.1315 | 0.0168 | 0.0017 | 0.0168 | 0.0196 | 0.0151 | - | - |
S. aterrimus | SCa8 | 0.1176 | 0.1353 | 0.1448 | 0.1157 | 0.1337 | 0.0151 | 0.0000 | 0.0151 | 0.0178 | 0.0134 | 0.0017 | - |
S. nassonowi | SCa1 | 0.1286 | 0.1387 | 0.1385 | 0.1245 | 0.1484 | 0.0431 | 0.0414 | 0.0431 | 0.0438 | 0.0412 | 0.0433 | 0.0414 |
S. nassonowi | SCa2 | 0.1265 | 0.1337 | 0.1375 | 0.1242 | 0.1406 | 0.0410 | 0.0394 | 0.0410 | 0.0416 | 0.0393 | 0.0412 | 0.0394 |
S. nassonowi | SCa4 | 0.1285 | 0.1357 | 0.1394 | 0.1262 | 0.1426 | 0.0428 | 0.0411 | 0.0428 | 0.0434 | 0.0410 | 0.0429 | 0.0411 |
S. nassonowi | SCa5 | 0.1345 | 0.1418 | 0.1457 | 0.1321 | 0.1492 | 0.0446 | 0.0429 | 0.0446 | 0.0435 | 0.0427 | 0.0448 | 0.0429 |
S. nassonowi | SCa6 | 0.1265 | 0.1337 | 0.1375 | 0.1242 | 0.1406 | 0.0410 | 0.0394 | 0.0410 | 0.0416 | 0.0393 | 0.0412 | 0.0394 |
S. nassonowi | SCa9 | 0.1285 | 0.1357 | 0.1394 | 0.1262 | 0.1426 | 0.0428 | 0.0411 | 0.0428 | 0.0434 | 0.0410 | 0.0429 | 0.0411 |
S. nassonowi | SCa10 | 0.1330 | 0.1401 | 0.1439 | 0.1305 | 0.1428 | 0.0464 | 0.0447 | 0.0464 | 0.0472 | 0.0446 | 0.0466 | 0.0447 |
S. nassonowi | SHo1 | 0.1262 | 0.1335 | 0.1392 | 0.1240 | 0.1404 | 0.0375 | 0.0358 | 0.0375 | 0.0378 | 0.0357 | 0.0376 | 0.0358 |
S. nassonowi | SSa1 | 0.1290 | 0.1340 | 0.1397 | 0.1267 | 0.1410 | 0.0411 | 0.0395 | 0.0411 | 0.0417 | 0.0393 | 0.0413 | 0.0395 |
S. nassonowi | SSg1 | 0.1285 | 0.1357 | 0.1394 | 0.1262 | 0.1426 | 0.0428 | 0.0411 | 0.0428 | 0.0434 | 0.0410 | 0.0429 | 0.0411 |
S. nassonowi | STi1 | 0.1285 | 0.1357 | 0.1394 | 0.1262 | 0.1426 | 0.0428 | 0.0411 | 0.0428 | 0.0434 | 0.0410 | 0.0429 | 0.0411 |
S. nassonowi | STi2 | 0.1285 | 0.1357 | 0.1394 | 0.1262 | 0.1426 | 0.0428 | 0.0411 | 0.0428 | 0.0434 | 0.0410 | 0.0429 | 0.0411 |
S. nassonowi | STi4 | 0.1285 | 0.1357 | 0.1394 | 0.1262 | 0.1426 | 0.0428 | 0.0411 | 0.0428 | 0.0434 | 0.0410 | 0.0429 | 0.0411 |
S. nassonowi | STi6 | 0.1265 | 0.1337 | 0.1375 | 0.1242 | 0.1406 | 0.0410 | 0.0394 | 0.0410 | 0.0416 | 0.0393 | 0.0412 | 0.0394 |
Stylops | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | S. nass. | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
voucher | SCa1 | SCa2 | SCa4 | SCa5 | SCa6 | SCa9 | SCa10 | SHo1 | SSa1 | SSg1 | STi1 | STi2 | STi4 | |
S. nevinsoni | SFu1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. spreta | SMi1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. melittae | SNi1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. ater | SVa2 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. aterrimus | SAg1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. aterrimus | SBm1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. aterrimus | STig1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. aterrimus | STig2 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. aterrimus | Ssp1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. aterrimus | SCa7 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. aterrimus | SCa8 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. nassonowi | SCa1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
S. nassonowi | SCa2 | 0.0035 | - | - | - | - | - | - | - | - | - | - | - | - |
S. nassonowi | SCa4 | 0.0017 | 0.0017 | - | - | - | - | - | - | - | - | - | - | - |
S. nassonowi | SCa5 | 0.0018 | 0.0052 | 0.0035 | - | - | - | - | - | - | - | - | - | - |
S. nassonowi | SCa6 | 0.0000 | 0.0033 | 0.0017 | 0.0017 | - | - | - | - | - | - | - | - | - |
S. nassonowi | SCa9 | 0.0017 | 0.0017 | 0.0000 | 0.0035 | 0.0017 | - | - | - | - | - | - | - | - |
S. nassonowi | SCa10 | 0.0053 | 0.0050 | 0.0033 | 0.0070 | 0.0050 | 0.0033 | - | - | - | - | - | - | - |
S. nassonowi | SHo1 | 0.0141 | 0.0134 | 0.0151 | 0.0157 | 0.0134 | 0.0151 | 0.0185 | - | - | - | - | - | - |
S. nassonowi | SSa1 | 0.0106 | 0.0101 | 0.0118 | 0.0123 | 0.0101 | 0.0118 | 0.0152 | 0.0135 | - | - | - | - | - |
S. nassonowi | SSg1 | 0.0017 | 0.0017 | 0.0000 | 0.0035 | 0.0017 | 0.0000 | 0.0033 | 0.0151 | 0.0118 | - | - | - | - |
S. nassonowi | STi1 | 0.0017 | 0.0017 | 0.0000 | 0.0035 | 0.0017 | 0.0000 | 0.0033 | 0.0151 | 0.0118 | 0.0000 | - | - | - |
S. nassonowi | STi2 | 0.0017 | 0.0017 | 0.0000 | 0.0035 | 0.0017 | 0.0000 | 0.0033 | 0.0151 | 0.0118 | 0.0000 | 0.0000 | - | - |
S. nassonowi | STi4 | 0.0017 | 0.0017 | 0.0000 | 0.0035 | 0.0017 | 0.0000 | 0.0033 | 0.0151 | 0.0118 | 0.0000 | 0.0000 | 0.0000 | - |
S. nassonowi | STi6 | 0.0000 | 0.0033 | 0.0017 | 0.0017 | 0.0000 | 0.0017 | 0.0050 | 0.0134 | 0.0101 | 0.0017 | 0.0017 | 0.0017 | 0.0017 |
Stylops nassonowi
Stylops savignyi Hofender 1924: 254 [F]. New synonyms.
Female puparium. The female puparium of S. nassonowi is almost indistinguishable from its sibling species, S. aterrimus Newport (compare Figures
First instar. Body elongate as in other species of Stylops except for S. melittae, which has wider abdomen. Head dorsally with two olfactory foveae and four pairs of setae in contrast to S. melittae, which has seven pairs of setae and no foveae. The frontal margin of the maxillae is not sagging in S. aterrimus and S. melittae, in contrast to that of S. nassonowi. The cervix is indistinct in S. nassonowi rather than more defined in S. melittae, the latter possessing a narrower head ventrally. The caudal margins of the dorsal segments have spinullae, except for the pro- and mesothoracic segments, which are covered basally (bases are covered by the tergal margin and therefore not visible rather than fully exposed), while in S. melittae some spinullae are covered and there is a gap in the center of dorsum where no spinullae are present. The sternal plates are broader than in S. melittae.
Ventral (6–19) and dorsal views (20, 21) of cephalothoraxes of female puparia from Stylops nassonowi Pierce (6–13, 20, 21) and S. aterrimus Newport (14–19) 6 Voucher SCa5 (Czech Republic) 7 Voucher SCa6 (Czech Republic) 8 Voucher SHo1 (Turkey) 9 Voucher SSa1 (Saudi Arabia) 10 Voucher SSg1 (Czech Republic) 11 Voucher STi2 (Hungary) 12 Voucher STi4 (Czech Republic) 13 Voucher STi6 (Czech Republic) 14 Voucher SAg1 (Tunisia) 15 Voucher SBm1a (Czech Republic) 16 Voucher SBm1b (Czech Republic) 17 Voucher STig2 (Tunisia) 18 Voucher SCa7 (Switzerland) 19 Voucher Ssp1 (Tunisia) 20 Voucher SCa10 (Czech Republic) 21 Voucher STi6 (Czech Republic).
Female and female puparium. Head two times wider than long, width to length 1.97–2.53 (n = 13, x = 2.15 mm), width 0.60–0.76 mm (x = 0.68 mm), length 0.30–0.36 mm (x = 0.32 mm); head posteriorly defined by single incomplete or ill-defined cephalic ridge on dorsal surface, paired cephalic ridge on ventral surface and posterior head thickening (lower margin of brood opening). Head corners short and narrow on ventral surface, slightly diverging posteriorly, head corners shorter than head on dorsal surface laterally, but inner posterior extension of ventral cephalic ridge (joint of ventral cephalic ridge and posterior head thickening) extends as far as head posterior margin on dorsal surface; ventral cephalic ridge posteromedially oriented; head corners not produced laterally beyond prothorax, head narrower than prothorax and thus cephalothorax continuously diverging posteriorly. Mandibles large, not extending from head contour in ventral view; inner apical tooth well-developed; apex ventrally with 5–8 sensilla, intermandibular distance 0.17–0.20 mm (x = 0.19 mm). Labiomaxillary area about 2–2.5× longer than wide; maxillary area distinctly prominent, overlapping mandible at about one third of its width, maxilla with 7–16 sensilla laterally; labial area without sensilla, more or less prominent and faintly divided into two parts medially (probably postmentum and prementum). Oral ridge (hypopharynx) well developed, rectangular, apically straight, occupying about half of intermandibular area; epipharynx slightly produced, pale, about as long as oral ridge. Hypostomal ridge (from outer margin of mandible to cephalic ridge and separating maxillary area from head corner) slightly sinuous, about as long as intermandibular distance or slightly longer. Labral area well developed, large, arcuate apically, slightly darker than clypeus in most specimens. Clypeus transverse, exceeding mandibles laterally and apically, apex straight or slightly concave, lateral corners prominent, with about 10–30 short sensilla laterally. Brood opening wide, distinctly wider than distance between mandibles; prothoracic flange (dorsal cover of brood opening) sclerotized, arcuate, laterally curved more than medially, apical margin almost straight, in some specimens more produced forward than in others; posterior head thickening (lower margin of brood opening) more uniformly arcuate than flange; overlap of prothoracic flange and posterior head thickening relatively short, about as long as cephalic ridge thick; joint of posterior head thickening and ventral cephalic ridge small, often serrate, slightly lighter than cephalic ridge. Cephalothorax usually slightly wider than long, but longer than wide in some specimens, width to length 0.85–1.18 (x = 1.05), width 1.05–1.41 mm (x = 1.24 mm), length 1.04–1.27 mm (x = 1.18 mm); cephalothorax compact, all segments fused, pigmentation denser laterally than medially. Pro- and mesothoracic intersegmental ridges distinct medially on ventral surface; paired pro- and mesothoracic ridges variable in size, usually distinct on dorsal surface. Pro- and mesothorax uniformly light yellowish-brown except pale prothoracic ridge and slightly darker surrounding integument, posterior part of mesothorax with pair of dark brown spots variable in size (absent in some specimens), distinct lighter area in center of mesothoracic ridge; metathorax uniformly pigmented with paired posterolateral dark brown spots (absent in some specimens); abdominal part of cephalothorax dichromatic, apical part lightest of cephalothorax, nearly transparent, and basal band dark brown, basal band short, not extending toward spiracles, division between basal band and remainder of cephalothorax nearly straight in all parts. Spiracles not prominent, positioned at widest part of posterior part of cephalothorax. Canalis prolifer on abdominal segments I–VII; single median tuba prolifera positioned on posterior third of segments II–VI.
First instar. Body length 135–192 μm (without caudal setae); caudal setae approximately one half body length; with minute terminal leaf-like structure (“Haftlappen”: vide
Posterior margin of dorsal tergites with spinullae, all spinullae covered basally by tergal margin except for pro- and mesothoracic segments. Each thoracic tergite with two submedian and lateral rows of setae. Coxae broad; each coxa bearing one coxal bristle and 6–7 cuticular outgrowths distributed among three coxal teeth at anterior part of coxa; coxal bristle on pro- and mesothorax at least two times as long as coxal teeth. Trochanterofemur always with femoral spur and bristle almost as long as coxal bristle, and one cuticular outgrowth. Pro- and mesotarsi elongate and slightly enlarged, metatarsi rod-like. Sternal plates broad, with one pair of setae on each plate, with a few outgrowths (about 6) on their posterior margins. Precoxal pleural membrane with small number of microtrichia (about 3) on prothorax, and with transverse row of microtrichia on meso- and metathorax. Short row of cuticular outgrowths (“Spinulaeplatte” sensu
Stylops nassonowi differs significantly in DNA barcode sequence distance, which is consistently about 4% or more from other species, including S. aterrimus. At the same time, the distances within the species are about 1.5% in distance or even less (Table
Phylogenetic analysis of species of Stylops sampled from a diversity of hosts (
Stylops aterrimus and S. nassonowi are close sibling species and are almost indistinguishable morphologically. The two lineages exhibit sequence distances of about 4%, which is quite distinct when compared to many other species. Although we readily admit that there is no definable metric value of percent sequence difference for conferring specific status, 4% is greater than many other closely related species that are easily diagnosed on the basis of additional characters outside of the sequences themselves. Intraspecific variance in the DNA distances of each species is well below 2% and the variability is not overlapping (Table
The present study demonstrates how a seemingly happenstance and serendipitous encounter with a stylopized female of A. savignyi permitted a significant shift in a long-standing taxonomic obstacle. Clarification of the identity of S. savignyi provides one further step toward a revised classification of Stylops supported by both morphological and molecular data. Given the increased awareness of native pollinators (many of which are wild bees) and their importance for ecosystem health, numerous initiatives are underway to study such species. These endeavors are making available new samples from previously under-collected regions and with this increased effort the probability of acquiring fresh material of their parasites, some unseen for decades. Melittologists and pollination biologists should develop an awareness and maintain alertness for stylopized females, and where possible obtain data on their impact on the host’s behavior and development as it not only makes less known the Strepsiptera but simultaneously enhances our knowledge of the hosts.
This work was supported by the Visiting Professor Program at King Saud University, Deanship of Scientific Research. We are further grateful to Dr. Fahad J. Alatawi for his assistance in preparing scanning electron micrographs and other images of the parasites, to Mrs. Kellie K. Magill Engel for her support and patience during the composition of the manuscript, and to two anonymous reviewers for their helpful input. J.S. and K.J. are grateful for support for the SVV project (Integrative Animal Biology) No. SVV 260 208/2015.
Material of species of Stylops used for taxonomic comparison
Here we provide specimen and collective event details for the various specimens of species of Stylops used in our comparative studies, along with the hosts from which they were sampled. In addition, specimens tied to specific sequences deposited in GenBank are identified and their numbers provided.
Stylops ater
Material examined. Czech Republic: Bohemia: Prokopské údolí, Praha-Jinonice, 1F, host: A. (Melandrena) vaga Panzer, 1♂, 13.iii.2007, J. Straka lgt., voucher SVa2, DNA barcode, GenBank: KF803529.
Figs
Stylops spencii auctorum (nec
Stylops aterrimus
Material examined. Czech Republic: Bohemia, Velký Luh, sandpit, 2FF+1EMP, host: A. (Plastandrena) bimaculata (Kirby), 1♀, 20.iv.2010, J. Straka lgt., voucher SBm1, DNA barcode, GenBank: KP213298. Switzerland: Zürich env., 1F, host: A. (Hoplandrena) carantonica Pérez, 1F, 25.v.2010, collector unknown, voucher SCa7, DNA barcode, GenBank: KP213300; ditto, 1F+1EMP, voucher SCa8, DNA barcode, GenBank: KP213299. Tunisia: Gafsa env., 1F, host: A. (P.) bimaculata, 1F, 1.iv.2006, J. Batelka et J. Straka lgt., voucher STig2, DNA barcode, GenBank: KF803522; Tamerza env., 1F, host: A. (Agandrena) agilissima (Scopoli), 1F, 31.iii.2006, J. Batelka et J. Straka lgt., voucher SAg1, DNA barcode, GenBank: KF803428; ditto, 1F, host: A. (P.) bimaculata, 1F, voucher STig1, DNA barcode, GenBank: KF803521; Wadi Raml, 4.5 km E Douz, 1F, host: A. (H.) sp., 1F, 4.iv.2006, J. Batelka et J. Straka lgt., voucher Ssp1, DNA barcode, GenBank: KF803504.
Stylops melittae
Material examined. Czech Republic: Bohemia, Čelákovice env., 1F, host: A. (Zonandrena) flavipes Panzer, 1♂, 1.v.2006, J. Batelka lgt., voucher SFl1, DNA barcode, GenBank: KF803453; Bohemia, Prokopské údolí, Praha-Jinonice, 1F, host: A. (Melandrena) nigroaenea (Kirby), 1♀, 6.iv.2009, J. Straka lgt., voucher SNi16, DNA barcode, GenBank: KF803488.
Figs
Stylops nassonowi
Stylops savignyi Hofender 1924: 254 [F]. Type locality: Egypt.
Material examined. Czech Republic: Bohemia, Divoká Šárka, Praha-Liboc, 1F, host: Andrena (Hoplandrena) carantonica Pérez, 1♂, 15.iv.2006, J. Straka lgt., voucher SCa2, DNA barcode, GenBank: KF803434; Bohemia, Chvalské skály, Praha-Horní Počernice, 2FF, host: A. (H.) carantonica, 1♀, 3.vi.2005, J. Straka lgt., voucher SCa9, DNA barcode, GenBank: KF803436; Bohemia, Sušice env., 1F, host: A. (Plastandrena) tibialis (Kirby), 1♀, 9.iv.2007, L. Dvořák lgt., voucher STi1, DNA barcode, GenBank: KF803518; ditto, 2FF, voucher STi6, DNA barcode, GenBank: KP213303; Bohemia, Závišín, Blatná env., 1F, host: A. (P.) tibialis, 1♂, 4.iv.2009, P. Bogusch lgt., voucher STi4, DNA barcode, GenBank: KP213302; Moravia, Dolní Dunajovice env., 1F+1EMP, 16.iv.2007, P. Bogusch lgt., voucher SCa10, DNA barcode, GenBank: KP213304; Moravia, Dolní Věstonice env., 1F, host: A. (H.) carantonica, 1♂, 5.iv.2008, J. Batelka et J. Straka lgt., voucher SCa5, DNA barcode, GenBank: KP213305; Moravia, Dolní Věstonice env., 1F+1EMP, host: A. (H.) carantonica, 1♂, 6.iv.2009, P. Bogusch lgt., voucher SCa6, DNA barcode, GenBank: KF803435; ditto, 3FF, host: A. (H.) spinigera (Kirby), 1♂, voucher SSg1, DNA barcode, GenBank: KF803503; Moravia, Lednice env., 1F, host: A. (H.) carantonica, 1♀, 13.vi.2006, J. Straka lgt., voucher SCa1, DNA barcode, GenBank: KF803433; Hungary: Budaörs, Budapest env., 1F, host: A. (H.) carantonica, 1♀, 25.iv.2009, J. Straka et P. Bogusch lgt., voucher SCa4, DNA barcode, GenBank: KP213301; Örkeny (puszta), 1F, host: A. (P.) tibialis, 1♂, 24.iv.2009, J. Straka et P. Bogusch lgt., voucher STi2, DNA barcode, GenBank: KF803519; Saudi Arabia: Riyadh, Al Amariah, Majra Al-gasim, 2FF, host: A. (Suandrena) savignyi Spinola, 1♀, 5.iii.2011, M.A. Hannan lgt., voucher SSa1, DNA barcode, GenBank: KP213306; Turkey: Hakkari prov., Gözeldere 25 km E, 1F, host: A. (P.) sp., 1♀, 22.vi.2010, Mi. Halada lgt., voucher SHo1, DNA barcode, GenBank: KF803463.
Stylops nevinsoni
Material examined. Czech Republic: Bohemia, Chýnice, 1F, host: A. (A.) fulva (Müller), 1♀, 22.iv.2006, J. Batelka et J. Straka lgt., voucher SFu1, DNA barcode, GenBank: KF803457.
Stylops spencei
Material examined. Czech Republic: Bohemia, Chýnice, 1F, host: A. (Micrandrena) minutula (Kirby), 1♀, 22.iv.2006, J. Batelka et J. Straka lgt., voucher SMi1, DNA barcode, GenBank: KF803477.
Stylops thwaitesi
Material examined. Spain: Maranchón 3km NW, Castilla-La Mancha prov., 1F, host: A. (Taeniandrena) albofasciata Thomson, 1♀, 10.iv.2012, K. Černá, K. Jůzová et J. Straka lgt., voucher SOv3, DNA barcode, GenBank: KF803494.