Research Article |
Corresponding author: Serguei V. Triapitsyn ( serguei.triapitsyn@ucr.edu ) Academic editor: Michael S. Engel
© 2015 Serguei V. Triapitsyn, Toby R. Petrice, Michael W. Gates, Leah S. Bauer.
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:
Triapitsyn SV, Petrice TR, Gates MW, Bauer LS (2015) Two new species of Oobius Trjapitzin (Hymenoptera, Encyrtidae) egg parasitoids of Agrilus spp. (Coleoptera, Buprestidae) from the USA, including a key and taxonomic notes on other congeneric Nearctic taxa. ZooKeys 498: 29-50. https://doi.org/10.3897/zookeys.498.9357
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Oobius Trjapitzin (Hymenoptera, Encyrtidae) species are egg parasitoids that are important for the biological control of some Buprestidae and Cerambycidae (Coleoptera). Two species, O. agrili Zhang & Huang and O. longoi (Siscaro), were introduced into North America for classical biocontrol and have successfully established. Two new native North American species that parasitize eggs of Agrilus spp. (Buprestidae) are described and illustrated from the USA: O. minusculus Triapitsyn & Petrice, sp. n. (Michigan), an egg parasitoid of both A. subcinctus Gory on ash (Fraxinus spp.) and A. egenus Gory on black locust (Robinia pseudoacacia L.) trees, and O. whiteorum Triapitsyn, sp. n. (Pennsylvania), an egg parasitoid of A. anxius Gory on European white birch (Betula pendula Roth). A taxonomic key and notes on the Nearctic native and introduced Oobius species are also included.
Emerald ash borer, new species, congener identification key, Oobius agrili, Nearctic, egg parasitoid, biological control
The rather poorly known encyrtid genus Oobius Trjapitzin (Hymenoptera: Encyrtidae) currently includes 41 species worldwide, and seven are known from North America (
As egg parasitoids of Buprestidae, Cerambycidae (Coleoptera;
Here two new species of Oobius are reported and a taxonomic key to the known native and introduced species of Oobius in North America is provided. One of the newly described species was reared initially from eggs of the native buprestid Agrilus subcinctus Gory in Michigan, whose larvae feed on the dead twigs of ash trees. This parasitoid was previously reported by
Collecting and rearing new species of Oobius. Ash tree twigs with A. subcinctus eggs and black locust twigs with A. egenus eggs were collected in the field in Ingham and Clinton counties, Michigan in 2013 and 2014. Eggs were monitored in the laboratory for parasitoid emergence. Voucher specimens of the parasitoids were preserved in 95% ethanol and sent to the senior author for identification. See
Taxonomic studies. Parasitoid specimens used in the taxonomic studies were critical point dried from ethanol and point-mounted. Selected specimens were then dissected and slide-mounted in Canada balsam, examined under a Zeiss®™ Axioskop 2 plus compound microscope using Nomarski differential interference contrast optics. Stereomicroscopic images were compiled with Auto-Montage 4.02 (Synchroscopy®™) to illustrate select specimens. Images of specimens were produced by scanning electron microscopy (SEM) and an EntoVision Imaging Suite. A Nikon®™ SMZ1500 and Leica®™ MZ 9.5 stereomicroscope with 10X oculars (Nikon C-W10X/22) and Chiu Technical Corp.®™ Lumina 1 FO-150 and fiber optic light source was used for pinned specimen observation. Mylar film was placed over the ends of the light source to reduce glare. Scanning electron microscope (SEM) images were taken with a Hitachi®™ TM3000 desktop unit (Tungsten source). Some specimens were manually cleaned of external debris with forceps or brushes and affixed to 12.7X 3.2 mm Leica/Cambridge aluminum SEM stubs with carbon adhesive tabs (Electron Microscopy Sciences, #77825-12). Stub-mounted specimens were imaged uncoated or sputter coated using a Cressington Scientific 108 Auto with a gold-palladium mixture from at least three different angles to ensure complete coverage (~20–30nm coating). Color images were obtained using an EntoVision Imaging Suite, which includes a firewire JVC KY-75 3CCD digital camera mounted to a Leica M16 zoom lens via a Leica z-step microscope stand. Slides of O. buprestidis and O. dahlsteni were imaged with a Leica DMRB compound microscope fitted with Leica HCX PL “Fluotar” 5× and 10× metallurgical grade lenses. Both systems fed image data to a desktop computer where Cartograph 5.6.0 (Microvision Instruments®™, France) was used to capture a fixed number of focal planes (based on magnification); the resulting focal planes (manually captured via Archimed 5.5.0 on the DMRB) were merged into a single, in-focus composite image. Uniform lighting was achieved using a LED illumination dome with all four quadrants set to 99.6% intensity. The images were then retouched where necessary using Adobe Photoshop®™ CS4/CS6 with plates assembled using InDesign CS4/CS6.
Terms used for morphological features are those of
Acronyms for depositories of specimens are as follows: BMNH, The Natural History Museum, London, England, UK; EMEC, Essig Museum of Entomology, University of California, Berkeley, California, USA; IZCAS, Institute of Zoology, Chinese Academy of Sciences, Beijing, China; MSUC, Albert J. Cook Arthropod Research Collection, Department of Entomology, Michigan State University, East Lansing, Michigan, USA; PSUC, Frost Entomological Museum, Pennsylvania State University, University Park, State College, Pennsylvania, USA; UANL, Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Monterrey, Mexico; UCRC, Entomology Research Museum, University of California, Riverside, California, USA; UNCA, Institute of Agricultural Entomology, University of Catania, Catania, Sicily, Italy; USNM, National Museum of Natural History, Washington, District of Columbia, USA.
Oobius
Avetianella
Szelenyiola
Oobius:
Avetianella:
Oophagus Liao in
Szelepyiola:
Oobius is a cosmopolitan genus as defined by
(Oobius depressus (Girault) not included)
1 | Tarsi 4-segmented (Fig. |
O. agrili Zhang & Huang |
– | Tarsi 5-segmented (Figs |
2 |
2(1) | Clava entire (Figs |
O. nearcticus (Trjapitzin) |
– | Clava 3-segmented (Figs |
3 |
3(2) | Body length (dry-mounted specimens) at most 0.53 mm; mps only on F6 (Fig. |
O. minusculus sp. n. |
– | Body length (dry-mounted specimens) at least 0.66 mm; mps on F6 and other funicle segments (Figs |
4 |
4(3) | Mps on F5 and F6 (Fig. |
O. buprestidis (Gordh & Trjapitzin) |
– | Mps on F4–F6 (Figs |
5 |
5(4) | Linea calva “open” posteriorly (Fig. |
O. longoi (Siscaro) |
– | Linea calva interrupted posteriorly by a line (or lines) of setae (Figs |
6 |
6(5) | F5 and F6 each notably longer than F4 (Fig. |
O. whiteorum sp. n. |
– | F5 and F6 each subequal in length to F4 (Fig. |
O. dahlsteni (Trjapitzin) |
1–4 Oobius agrili female (from USDA Forest Service laboratory colony, East Lansing, Michigan, USA; of China origin), 1 hind leg 2 antenna 3 lateral habitus 4 forewing base 5–6 Oobius buprestidis female (holotype), 5 lateral habitus 6 antenna 7–8 Oobius dahlsteni female (holotype) 7 dorsal habitus 8 antenna.
9–10 Oobius nearcticus female (holotype), 9 antenna 10 clava 11a–11b: 11a holotype slide of O. minusculus 11b holotype slide of O. whiteorum 12–16 Oobius minusculus 12 antenna (holotype female) 13 mesosoma and metasoma (holotype female) 14 metasoma (paratype male) 15 head (paratype female) 16 pedicel and flagellum (paratype male).
17–18 Oobius depressus female 17 dorsal scutellum (lectotype) 18 dorsal habitus (paralectotype) 19 Oobius zahaikevitshi female (environs of Volgograd, Krasnoarmeyskiy District, Volgograd Province, Russia), forewing 20–21 Oobius hasmik female (paratype) 20 antenna 21 forewing 22–23 Oobius longoi female (from University of California laboratory colony, Riverside, California, USA; of Australia origin), 22 antenna 23 forewing 24 Oobius nearcticus female (holotype), lateral habitus.
25 Oobius minusculus male (paratype), mesosoma 26–29 Oobius whiteorum 26 antenna (holotype female) 27 a pair of wings (holotype female) 28 dorsal habitus (holotype female) 29 genitalia (paratype male) 30 Oobius zahaikevitshi female (environs of Volgograd, Krasnoarmeyskiy District, Volgograd Province, Russia), antenna 31 Oobius minusculus female (holotype), a pair of wings 32 Oobius whiteorum (paratype male), antenna.
Oobius agrili Zhang & Huang in
Oobius agrili Zhang & Huang:
USA, Michigan, Ingham Co., East Lansing, United States Department of Agriculture (USDA) Forest Service Northern Research Station, laboratory culture of O. agrili reared in Agrilus planipennis eggs: 37th-generation progeny, emerged 10.viii.2014, D.L. Miller, originally from CHINA, Jilin (Jingyuetan Forest Park, Changchun), 2006, T. Zhao (Zhao Tonghai), from eggs of A. planipennis [10 ♀, UCRC]; 6–7th-generation progeny, emerged 31.vii.2014, D.L. Miller, originally from CHINA, Jilin (Jingyuetan Forest Park, Changchun), 2008, T. Zhao, from eggs of A. planipennis [11 ♀, UCRC]; 4–8th-generation progeny, emerged 10.viii.2014, D.L. Miller, originally from CHINA, Jilin (Jingyuetan Forest Park, Changchun), 2009, T. Zhao, from eggs of A. planipennis [16 ♀, UCRC]; 9th-generation progeny, emerged 18.vii.2014, D.L. Miller, originally from CHINA, Jilin (Jingyuetan Forest Park, Changchun), 2008, T. Zhao, from eggs of A. planipennis [11 ♀, UCRC].
China (
Agrilus planipennis Fairmaire.
Oobius agrili is a solitary thelytokous egg parasitoid of A. planipennis, discovered in 2004 during foreign exploration for natural enemies in northeast China (
Avetianella buprestidis
Avetianella buprestidis:
Oobius buprestidis (Gordh & Trjapitzin):
Holotype female [USNM] on point mount labeled with following seven labels: “Ex egg of Bupretus [sic] aurulentus”, “Portland, Ore., F.D. Keen Colr.”, “Hopk. US No. 33150-D”, “Lot No. 41-14524”, “Habrolepoidea n. sp. det. Gahan”, “Avetianella sp.n. Det Trjapitzin et Gordh”, [red] “Holotypus Avetianella buprestidis G. & T.”. The head and antenna are slide mounted separately: [left label] “♀ Holotype, Head & antenna, Avetianella buprestidis Gordh & Trjapitzin”, [right label] “Portland, Oregon, Hopkins #33150-D, Lot #41-14524, Ex eggs Buprestus aurulentus”. The forewing is mounted on an additional slide with the forewing of a male paratype: [left label] “♂ Forewing, top, Avetianella buprestidis G.&T., Portland, Ore., Lot # 41-14524, Hopkins # 33150-D, ♂ paratype”, [right label] “♀ Forewing, bottom, (Holotype) Ex. eggs Buprestus aurulentus, F.P. Keen, col. Head & antenna, Avetianella buprestidis Gordh & Trjapitzin, [right label] “Portland, Oregon, Hopkins #33150-D, Lot #41-14524, Ex eggs Buprestus aurulentus”.
USA (Oregon) (
Buprestis aurulenta L. (
The point-mounted portion of the type (Fig.
Avetianella dahlsteni
Avetianella dahlsteni:
Oobius dahlsteni (Trjapitzin):
Holotype female [EMEC] on slide labeled: [left label] “Avetianella dahlsteni Trjapitzin ♀, Trjapitzin 1970, CFL III-69, Ch. phenol gum damar, Div. Biol. Conn. Univ. Calif [“holotype” handwritten at top, middle, and bottom of label in red ink]”, [right label] “McCloud Flat, Siskiyou Co. Calif., July, 1968, D. brevicornis rearing carton, A900, MF2-5 SR., D. L. Dahlsten”.
USA (California) (
Unknown.
The holotype (Fig.
Habrolepoidea depressa
Avetianella depressa (Girault):
Lectotype female [USNM], designated by Trjapitzin & Gordh (1984), on point with following six labels: “Morristown XII-8-14 Ill”, “ExEggs Cylene robinae”, “JRMalloch Coll.”, [red] “Paratype No. 20328 U. S. N. M.”, “Avetianella Det. Trjapitzin et Gordh”, [red] “Lectotypus ♀ Habrolepoidea depressa Grlt Des. Trjapitzin et Gordh”. Paralectotypes, 2 males, 2 females: 1 female [USNM] on point with following six labels: “Morristown XII-8-14 Ill”, “ExEggs Cylene robinae”, “JRMalloch Coll.”, [red] “Paratype No. 20328 U. S. N. M.”, [red] “Paralectotypus ♀ Habrolepoidea depressa Grlt Des. Trjapitzin et Gordh”, “Avetianella depressa (Girault) ♀ Det. V. Trjapitzin May 1997”; 1 female [USNM] on point with following six labels: “Morristown XII-8-14 Ill”, “ExEggs Cylene robinae”, “JRMalloch Coll.”, [red] “Paratype No. 20328 U. S. N. M.”, 5. “Habrolepoidea depressa Gir Type”, “LECTOTYPE Habrolepoidea depressa Girault By B.D. Burks”; 2 males [USNM] on points, each with following four labels: “Morristown XII-8-14 Ill”, “ExEggs Cylene robinae”, “JRMalloch Coll.”, [red] “Paratype No. 20328 U. S. N. M.”. All specimens of the type series lack the heads and antennae (
USA (Illinois) (
Megacyllene robiniae (Forster) (Cerambycidae) (
The identity of this species remains unclear because the original description is poor and without any illustrations; unfortunately, the slide with a head and a forewing of each sex (
Avetianella longoi
Avetianella longoi:
Oobius longoi (Siscaro):
Australia, New South Wales, Corowa, 22.i.2006, Q. Wang, from eggs of Phoracantha recurva [1 ♀, 1 ♂, UCRC]. Portugal: Lisboa, Montijo, Pegões, viii.1992, P. Albino, M. R. Paiva, from eggs of Phoracantha semipunctata [9 ♀, 11 ♂, UCRC]. Viseu, Villa Cova à Coelheira, viii.1992, P. Albino, M. R. Paiva, from eggs of P. semipunctata [11 ♀, UCRC]. USA, California, Riverside Co., Riverside, University of California campus, Department of Entomology Insectary, laboratory culture on eggs of P. semipunctata on Eucalyptus sp.: 29.ix.1994, L. Hanks (originally from Australia) [4 ♀, UCRC]; 1998, S. McElfresh, J. Gould (originally from: Australia, Victoria, Melbourne, Bundoora, La Trobe Wildlife Sanctuary, i.1992, Q. Wang, from eggs of P. semipunctata on fallen Eucalyptus sp.) [25 ♀, 22 ♂, UCRC].
Australia (indigenous); introduced (in some cases possibly unintentionally) into Hungary, Italy, Portugal, South Africa, Spain, USA (California), and Zambia (
Phoracantha recurva Newman and P. semipunctata (Fabricius) (Cerambycidae) in California, USA (Wang et al. 2008); its other longhorned beetle hosts in Australia are listed by
Oobius longoi is well known as an effective biological control agent and a successfully established parasitoid of P. recurva and P. semipunctata in California and elsewhere in the world (
Avetianella sp.:
Holotype female [UCRC] on slide (Fig.
Paratypes: USA, Michigan: Clinton Co. (same data as the holotype), 2 ♀ on points [MSUC, UCRC] and 1 ♀, 1 ♂ on slides [UCRC]. Ingham Co., Michigan State University Tree Research Center, 42°40'12"N, 84°28'12"W, 267 m, 14.viii.2014, T. R. Petrice, emerged in laboratory (East Lansing) from parasitized Agrilus egenus Gory eggs on black locust, Robinia pseudoacacia, twigs: emerged 22.viii.2014 [3 ♀ on points, MSUC, UCRC, USNM]; emerged 29.viii.2014 [3 ♀ on points, MSUC, UCRC, USNM, and 1 ♂ on slide, UCRC]; emerged 6.ix.2014 [1 ♀ on point, UCRC]; emerged 17.ix.2014 [1 ♂ on slide, UCRC].
FEMALE (holotype). Body dark brown to black except scutellum and propodeum brown; scape and pedicel brown, flagellum light brown; legs whitish or pale yellowish with wide brown bands on coxae, femora, and tibiae.
Frontovertex and mesonotum with faint mesh-like or lineolate sculpture [very difficult to see in dry-mounted specimens, best observed in slide-mounted ones (as in Fig.
Head (as in Fig.
Antenna (Fig.
Mesosoma a little shorter than gaster (Fig.
Wings (Fig.
Mesotibial spur a little longer than mesobasitarsus.
Ovipositor occupying a little more than 0.5× length of gaster, exserted markedly beyond gastral apex (by 0.2× own length) (Fig.
Measurements of the holotype (mm, as length or length:width). Body (of the dry-mounted specimen prior to slide-mounting): 0.462; mesosoma: 0.233; gaster: 0.245; ovipositor: 0.173. Antenna: radicle: 0.03; rest of scape: 0.103; pedicel: 0.045; F1: 0.012; F2: 0.012; F3: 0.011 (0.012); F4: 0.012; F5: 0.015; F6: 0.03; clava: 0.103. Forewing: 0.495:0.234; longest marginal seta: 0.021; hindwing: 0.357:0.085; longest marginal seta: 0.025.
Variation (paratypes). Body length 0.43–0.46 mm (dry-mounted specimens from A. subcinctus, Fig.
MALE (paratype from A. subcinctus). Head dark brown, mesosoma and gaster dark brown to black except mesoscutum with a brownish tinge, base of gaster whitish; antenna with scape and pedicel brown to dark brown, flagellum light brown. Antenna (Fig.
Variation (paratypes from A. egenus). Body length 0.4–0.5 mm (critical-point dried specimens).
This species is similar to the European O. zahaikevitshi Trjapitzin (Figs
Oobius minusculus differs from O. zahaikevitshi in having the palpal formula 4–1, a relatively smaller F5 of the female antenna and also by F6 being longer than wide and almost concolorous or often concolorous with other flagellomeres (Fig.
Oobius minusculus is the only described native Nearctic species of Oobius s. str., as characterised by
The name of this new taxon is an adjective referring to its small size.
Agrilus subcinctus on ash (Fraxinus spp.) and A. egenus on black locust (Robinia pseudoacacia).
Originally reported by
The following specimens of O. zahaikevitshi were examined: Bulgaria, Plovdiv Prov., Klisura, 27.vi–8.vii.1975, A. Atanasov, from eggs of Agrilus cuprescens (Ménétriés) on Rosa sp. [1 ♂, BMNH] (det. V. A.
Szelenyiola nearctica
Oobius nearcticus (Trjapitzin):
Holotype female [EMEC] on point mount with following four labels: “UC Blodgett Forest 8 mi E. Georgetown, El Dorado Co., California Coll. F. M. Stephen 1970”, “Traps A-1094”, [red] “Holotypus Szelenyiola nearctica Trjapitzin”, “U.C. Berkeley EMEC 82,322”. Paratype female [EMEC] on point with following five labels: “UC Blodgett Forest 8 mi E. Georgetown, El Dorado Co., California Coll. F. M. Stephen 1970 A-1094 Traps”, “Head with appendages on slide No. 1955”, “Also forewing”, “Paratypus”, [red] “Szelenyiola nearctica Trjapitzin ♀”.
USA (California) (
Unknown.
The holotype (Fig.
Avetianella sp.:
Holotype female [UCRC] on slide (Fig.
Paratypes: same data as the holotype, 4 ♀ on points and 1 ♂ on slide [UCRC].
FEMALE (holotype). Body somewhat flattened, dark brown to black; appendages brown except tarsi light brown; scape and pedicel a little darker than flagellum, and F6 just slightly lighter than other flagellar segments but still brown.
Frontovertex and mesonotum with faint mesh-like sculpture [very difficult to see in dry-mounted specimens]. Pronotum, mesoscutum, axillae, and scutellum with short, dusky setae; scutellum also with a pair of long, fine setae near posterior margin.
Head (Fig.
Antenna (Fig.
Mesosoma (Fig.
Wings (Fig.
Mesotibial spur as long as mesobasitarsus.
Ovipositor occupying about 0.5× length of gaster, exserted markedly beyond gastral apex (by 0.36× total ovipositor length); ovipositor length:metatibia length ratio 1.3:1. Outer plate of ovipositor with 1 subapical seta.
Measurements of the holotype (mm, as length or length:width). Body (of the dry-mounted specimen prior to slide-mounting): 0.66; head: 0.19; mesosoma: 0.313; gaster: 0.35; ovipositor: 0.283. Antenna: radicle: 0.039; rest of scape: 0.151; pedicel: 0.06; F1: 0.021; F2: 0.021; F3: 0.021; F4: 0.028; F5: 0.035; F6: 0.044; clava: 0.155. Forewing: 0.677:0.314; longest marginal seta: 0.021; hindwing: 0.5:0.133; longest marginal seta: 0.024.
Variation (paratypes). Body (Fig.
MALE (paratype). Body length (of the dry-mounted specimen prior to slide-mounting) 0.66 mm. Head and mesosoma dark brown, gaster brown; scape and pedicel brown, flagellum light brown; legs light brown to brown. Antenna (Fig.
Among the Nearctic species of Oobius, O. whiteorum is most similar to O. dahlsteni, from which it differs by the proportions of the funicle segments of the female antenna, as indicated in the key. In
Agrilus anxius Gory on European white birch (Betula pendula).
This species is named in honor of Lisa and Michael White of Chicago, Illinois, USA, good friends of the author’s family.
According to
The following paratypes [UCRC] of O. hasmik were examined, all collected at Las Barracas (~30 km E of Santiago, 23°28'02"N, 109°27'01"W, 50 m), Baja California Sur, Mexico: 1 ♀ on point with following five labels: “Mex. Baja Cal. Sur Las Barracas 17 - V - 1985”, “Coll. P. DeBach Pan trap”, “Avetianella ♀ Det. V. Trjapitzin May 1997”, [red] “Paratypus ♀ Avetianella hasmik Trjapitzin”, “Praep. micr. 22M” (an antenna, head, and a forewing were detached from this specimen; they are mounted on a slide with following two labels: “Avetianella hasmik ♀ Trjapitzin México: Baja California Sur, Las Barracas. Pan trap 17.V.1985 (Coll. P. DeBach) 22M Antena, cabeza, ala anterior”, [red] “Paratypus Avetianella ♀ hasmik Trjapitzin”); also 16 ♀, 1 ♂ on points, all collected by P. DeBach during 1985 and 1986, as indicated by
Oobius sp. n.:
Oobius sp. n. aff. rudnevi (S. Nowicki, 1928):
One female [UANL] of this undescribed species from Mexico, which has no host information, was mentioned by
We thank Natalie Dale-Skey Papillod (BMNH) and Robert L. Zuparko (EMEC) for the loans of specimens, Vladimir V. Berezovskiy (UCRC) for making excellent point- and slide-mounts, and Deborah L. Miller (USDA Forest Service, NRS, Lansing, Michigan, USA) for providing laboratory-reared specimens of O. agrili. Thanks to Taina Litwak (USDA-SEL) for adjusting the slide images and Dylan Johnston-Jordan for imaging O. agrili. Valuable comments by Robert Haack, Therese Poland, and two anonymous reviewers have contributed to the improvement of the manuscript. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.