Research Article |
Corresponding author: Serguei V. Triapitsyn ( serguei.triapitsyn@ucr.edu ) Academic editor: Petr Janšta
© 2020 Serguei V. Triapitsyn, Sharon A. Andreason, Nancy Power, Fatemeh Ganjisaffar, Lucian Fusu, Chrysalyn Dominguez, Thomas M. Perring.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Triapitsyn SV, Andreason SA, Power N, Ganjisaffar F, Fusu L, Dominguez C, Perring TM (2020) Two new species of Ooencyrtus (Hymenoptera, Encyrtidae), egg parasitoids of the bagrada bug Bagrada hilaris (Hemiptera, Pentatomidae), with taxonomic notes on Ooencyrtus telenomicida. Journal of Hymenoptera Research 76: 57-98. https://doi.org/10.3897/jhr.76.48004
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In support of a biological control program in California, USA, against the bagrada bug, Bagrada hilaris (Burmeister) (Hemiptera, Pentatomidae), an invasive pest of Asian origin, colonies of two species of Ooencyrtus Ashmead (Hymenoptera, Encyrtidae) are maintained using B. hilaris eggs as host. One of them, Ooencyrtus mirus Triapitsyn & Power, sp. nov., is of Pakistani origin. It displays natural preference for bagrada bug eggs and is being evaluated in quarantine as a candidate for classical biological control. The other, Ooencyrtus lucidus Triapitsyn & Ganjisaffar, sp. nov., appears to be native to California, and we believe it switched to B. hilaris from native pentatomid hosts. Both new species are described and illustrated, as is the Old World species Ooencyrtus telenomicida (Vassiliev), for which a neotype is designated. The presented morphometric evidence as well as mitochondrial and nuclear ribosomal DNA sequence data separate Ooencyrtus mirus from O. telenomicida. A lectotype is designated for Ooencyrtus californicus Girault from California, which is morphologically similar to O. lucidus.
Chalcidoidea, natural enemy, invasive pest, California, Pakistan, biological control, genetic analysis, taxonomy
The painted bug, also known as bagrada bug, Bagrada hilaris (Burmeister) (Hemiptera, Pentatomidae) (Fig.
In addition to the classical biological control efforts with the exotic Ooencyrtus sp., surveys for resident egg parasitoids of B. hilaris have been conducted throughout California since 2017 using sentinel egg cards. In this project, we collected a variety of parasitoid species from the B. hilaris eggs. A species of Ooencyrtus Ashmead was recovered from sentinel cards in Riverside, California. Because the taxonomy of the Nearctic species of Ooencyrtus is in flux and there are no keys to the 11 described species, the first author physically compared specimens collected in our study to the types and specimens of all described species from North America. In addition, he tried to identify our specimens with keys from other regions (i.e. Neotropical, Oriental, and Palearctic). These efforts were unsuccessful, suggesting that our insect was an undescribed native species. Therefore, we also describe this parasitoid as a new taxon.
During our investigations, we attempted to compare our insects to Ooencyrtus telenomicida (Vassiliev) and to other egg parasitoids in the O. telenomicida species complex. However, we were unable to locate the type series of Encyrtus telenomicida Vassiliev (now Ooencyrtus telenomicida). Therefore, we collected Ooencyrtus sp. from eggs of Eurygaster Laporte, the host genus of Encyrtus telenomicida, in the same general habitat as indicated in the original description and matched the morphology of the new collections both with that description and with non-type specimens reared before 1950 from the original host in both Russia and Ukraine, not too far from its type locality. Based on the morphological congruence, we designated a neotype for Encyrtus telenomicida and supplement this designation with DNA sequence data necessary for the differentiation of Ooencyrtus telenomicida from morphologically similar species in the complex. Throughout the paper we are using the term ‘O. telenomicida species complex’ for those species that are genetically and morphologically close to O. telenomicida. The group was defined morphologically by
Ooencyrtus species of Pakistan origin
Compared to other pentatomids, B. hilaris has an unusual ovipositional behavior of laying eggs singly or in small clusters on live plant material, in detritus and in soil (
Ooencyrtus species native to California
Sampling surveys for B. hilaris parasitoids were initiated in October 2017 and are still in progress. For the present study, B. hilaris adults were collected from a greenhouse colony where they were raised on seedlings of broccoli (Brassica oleracea var. italica), canola (Brassica napus L.), mustard greens (Brassica juncea L.), and sweet alyssum (Lobularia maritima (L.) Desvaux). Thirty adult mating pairs were placed in round plastic containers (15 cm diameter × 6 cm depth) (Durphy Packaging Co., Warminster, Pennsylvania, USA) with 2 screen openings on opposite sides for air circulation (Fig.
Ooencyrtus telenomicida (Vassiliev) from Europe
Specimens of O. telenomicida, reared in Russia and Ukraine from eggs of Eurygaster integriceps Puton (Hemiptera, Scutelleridae) in 1948 and 1950, were borrowed from the Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia. Unfortunately, PCRs failed on all the specimens that were extracted. Therefore, new specimens of O. telenomicida were reared in Ipatele, Iaşi County, Romania, from eggs of Eurygaster sp. found on wheat. We were able to extract DNA from these specimens, and the primary molecular vouchers were individually slide-mounted in Canada balsam or chemically dried and point mounted.
For the taxonomic descriptions of the new species, the morphological terms of
Specimens for morphometric studies were dried from ethanol using a critical point drier, then point-mounted and labeled. Selected specimens then were dissected and slide-mounted in Canada balsam. Slide mounts were examined under a Zeiss Axioskop 2 plus compound microscope (Carl Zeiss Microscopy, LLC, Thornwood, New York, USA) and photographed using the Auto-Montage system (Syncroscopy, Princeton, New Jersey, USA). Photographs were retouched where necessary using Adobe Photoshop (Adobe Systems, Inc., San Jose, California, USA). In addition, the body length of 24 male and 24 female O. mirus wasps were measured from the anterior end of the head to the posterior end of the gaster, not including the ovipositor or aedeagus, with a Leica Wild M10 stereoscope using a Bausch & Lomb 0.1 mm and 0.01 mm micrometer.
For the morphometric analysis, we measured characters in adult females and males to determine the following ratios: 1) ovipositor length to mesotibia length; 2) fore wing length to maximum width; 3) scape length to width (excluding the radicle); 4) clava length to width; 5) F1 length to pedicel length; and 6) F2 length to F1 length. For all parameters, the ranges, means, and standard deviations were determined.
For O. mirus and O. telenomicida we also used multivariate ratio analysis (MRA) (
Specimens examined are deposited in the collections with the following acronyms:
AICF Alexandru Ioan Cuza University, Iaşi, Romania (Lucian Fusu collection);
Paratype specimens of O. lucidus and O. mirus were selected for genetic analysis. Genomic DNA from three females (
Paired with morphological descriptions, confirmation of novel species was based on analysis of a fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene and the nuclear internal transcribed spacer 2 (ITS2) region. PCRs were performed using the reagents at concentrations described in
For O. telenomicida sequencing of the ITS2 with the primers in
Interspecific variation among O. lucidus, O. mirus, O. telenomicida, and other populations and species of Ooencyrtus was estimated by calculating uncorrected pairwise distances (p-distances) of the COI fragment and ITS2 region and by phylogenetic analysis. MEGA X (
Ooencyrtus californicus
Girault:
Holotype
female, deposited in
Paratypes. USA, California, Riverside County, Riverside, University of California at Riverside (UCR): Agricultural Operations, 33.966002N, 117.343198W, 304 m, cards with fresh sentinel eggs of Bagrada hilaris placed in squash field 26–29.x.2018, parasitoids emerged 13–15.xi.2018, F. Ganjisaffar [4 females on points, 4 females on slides (including 3 molecular vouchers of S. A. Andreason,
USA: California, Merced County, Merced, 24.viii.1938, R. Rose, “Ex eggs of Acrosternum hilaris” [1 female, 1 male,
There are no comprehensive keys for Ooencyrtus in North America and only 3 described species have been identified from California (
In
Morphometric ratios and measurements (µm) of Ooencyrtus lucidus female morphological characters. All measurements are from slide-mounted specimens.
Length ovipositor: length mesotibia | Length: width fore wing | Length: width hind wing | Length: width scape | Length: width clava | Length F1: length pedicel | Length F2: length F1 | |
---|---|---|---|---|---|---|---|
Range | 1.0–1.2 | 2.2–2.5 | 4.7–5.3 | 5.7–7.5 | 2.9–3.6 | 0.45–0.55 | 0.9–1.1 |
Mean | 1.1 | 2.4 | 4.9 | 6.6 | 3.2 | 0.5 | 1.0 |
n | 10 | 9 | 8 | 10 | 10 | 10 | 10 |
Length F1 | Length F2 | Length F3 | Length F4 | Length F5 | Length F6 | ||
Range | 29–35 | 27–38 | 24–36 | 34.85–39.39 | 41–45 | 38–42 | |
Mean | 33 | 33 | 32 | 37 | 43 | 41 | |
n | 10 | 10 | 10 | 10 | 10 | 10 |
Female (holotype and paratypes). Body length of dry-mounted, critical point-dried paratypes 825–1025 µm, and of slide-mounted paratypes 1045–1125 µm.
Color. Body (Fig.
Sculpture. Head with faint, inconspicuous sculpturing; mesoscutum reticulate, with sculpture cells mostly wider than long; axilla and anterior 1/3 or so of scutellum with a rather weak cell-like sculpture, remainder of body smooth.
Pubescence. Frontovertex, pronotum, mesoscutum, axilla, and scutellum with short, dark setae except scutellum with a few pairs of long, dark setae in posterior half.
Head
(Fig.
Antenna
(Fig.
Mesosoma
(Fig.
Wings
(Fig.
Legs. Mesotibial spur about as long as mesobasitarsus.
Gaster
(Fig.
Measurements (µm) of the holotype. Mesosoma 394; gaster 480; ovipositor 379; mesotibia 358. Antenna: radicle 48; rest of scape 179; pedicel 70; F1 35; F2 38; F3 30; F4 38; F5 45; F6 42; clava 129. Fore wing 852:369; longest marginal seta 33. Hind wing 603:123; longest marginal seta 48.
Male (paratypes). Body length of dry-mounted, critical point-dried paratypes 595–795 µm, and of slide-mounted paratype 940 µm. Head and mesosoma shining black with metallic reflections (Fig.
Bagrada hilaris populations have declined in California. We believe that parasitoids like O. lucidus are responsible for this decline. “Lucidus” is an adjective derived from Latin, meaning “lucid, clear.” It is chosen for this species name referring to the elucidation of why populations of B. hilaris have declined in California.
Nearctic region: USA (California and Texas).
Pentatomidae: Bagrada hilaris (Burmeister), Chinavia hilaris (Say), and Chlorochroa sayi Stål. In California, O. lucidus apparently switched from its native host(s), such as the green stink bug Chinavia hilaris, to parasitize eggs of the invasive bagrada bug.
The following specimens of O. californicus have been examined. Lectotype female [
Also present in
Holotype
female, deposited in
Paratypes. USA: California, Riverside Co., Riverside, UCR Quarantine laboratory, N. Power, from colony on Bagrada hilaris of Pakistan origin (via USDA ARS laboratory, Stoneville, Mississippi, USA), received 3.xii.2015, S&R # N-15–30: 3.ii.2017 [6 females on points and 2 females on slides,
This new species is close to a small group of species of Ooencyrtus which are similar to O. telenomicida (Vassiliev), as defined by
Morphometric ratios and measurements (µm) of Ooencyrtus mirus female morphological characters. All measurements are from slide-mounted specimens.
Length ovipositor: length mesotibia | Length: width fore wing | Length: width hind wing | Length: width scape | Length: width clava | Length F1: length pedicel | Length F2: length F1 | |
---|---|---|---|---|---|---|---|
Range | 0.92–1.02 | 2.28–2.48 | 4.52–4.97 | 5.64–6.89 | 3.00–3.71 | 0.48–0.60 | 0.91–1.08 |
Mean | 0.95 | 2.36 | 4.75 | 6.33 | 3.30 | 0.54 | 1.00 |
n | 10 | 10 | 10 | 10 | 10 | 10 | 10 |
Length F1 | Length F2 | Length F3 | Length F4 | Length F5 | Length F6 | ||
Range | 28–40 | 28–40 | 34–46 | 39–51 | 40–49 | 40–50 | |
Mean | 35 | 35 | 41 | 45 | 45 | 45 | |
n | 10 | 10 | 10 | 10 | 10 | 10 |
The LDA ratio extractor, which is a tool for identifying the best ratios for separating two groups, found that the best ratio to separate the two species is scape width / F5 length, the ratios being almost non-overlapping (Table
Because the commonly used morphometric parameters and ratios of O. telenomicida and O. mirus are so similar, the importance of their clear separation based on the presented genetic data can not be overestimated.
In
Female (holotype and paratypes). Body length of dry-mounted, critical point-dried paratypes 595–1025 µm.
Color. Head and mesosoma (Fig.
Sculpture. Head with faint cell-like sculpture; mesoscutum reticulate, more so anteriorly; axilla reticulate; scutellum more strongly reticulate than mesoscutum or axilla (except sometimes almost smooth at apex), remainder of body more or less smooth.
Pubescence. Frontovertex, pronotum, mesoscutum, axilla, and scutellum with short, inconspicuous, not very dark setae except scutellum with a few pairs of long, dark setae.
Head
(Fig.
Antenna
(Fig.
Mesosoma
(Fig.
Wings
(Fig.
Legs. Mesotibial spur about as long as mesobasitarsus.
Gaster
(Fig.
Measurements (µm) of the holotype. Mesosoma 400; gaster 431; ovipositor 321; mesotibia 351. Antenna: radicle 43; rest of scape 194; pedicel 68; F1 37; F2 40; F3 46; F4 49; F5 48; F6 46; clava 135. Fore wing 839:369; longest marginal seta 36. Hind wing 601:129; longest marginal seta 51.
Male (paratypes). Body length of dry-mounted, critical point-dried paratypes 660–890 µm, and of slide-mounted paratypes 950–960 µm. Head and mesosoma black with metallic reflections (Fig.
Morphometric ratios and measurements (µm) of Ooencyrtus mirus male morphological characters. All measurements are from slide-mounted specimens.
Length body | Length genitalia | Length: width fore wing | Length: width scape | |
---|---|---|---|---|
Range | 947–959 | 172–191 | 2.2–2.4 | 3.4–3.8 |
Mean | 953 | 181 | 2.3 | 3.6 |
n | 2 | 4 | 4 | 3 |
Variation (female and male body length, non-type specimens from the colony in UCR quarantine laboratory). The female body lengths, male body lengths, and paired differences, analyzed by the Shapiro-Wilks normality test in R (
The name is an adjective meaning “remarkable” or “amazing.” The name is given to this species because the authors find its biology to be quite remarkable.
Oriental region: Pakistan. The population in the quarantine laboratory in UC Riverside that served for the description of this species originated from the Toba Tek Singh District, Punjab, Pakistan.
Pentatomidae: Bagrada hilaris (Burmeister). We conducted host studies on O. mirus and found it to reproduce on the eggs of eight other species in Pentatomidae, one species in Rhopalidae, and one species in Coreidae (Hemiptera), as well as on one species in Noctuidae (Lepidoptera). Of all the potential host species we evaluated, only one, in Pyralidae (Lepidoptera), was not utilized as a host, likely because its eggs were too small. These findings show O. mirus to be a generalist parasitoid, although it prefers and reproduces more successfully on B. hilaris than on the other hosts evaluated.
Ooencyrtus mirus, a uniparental species, typically produces about 99% females. However, the percentage of males can be increased by providing new eggs to the same female wasps daily for more than two weeks. This depletes the supply of Wolbachia bacteria in the ovaries (
This species was initially identified from digital images of both dry- and slide-mounted specimens as Ooencyrtus telenomicida sensu lato (J. S. Noyes and E. Guerrieri, personal communications). This determination was ambiguous, however, since O. telenomicida was not clearly defined prior to this communication, despite the availability of its numerous diagnoses and redescriptions (e.g.,
Encyrtus telenomicida Vassiliev, 1904: 117–108. Original type locality: Kupiansk, Kharkov oblast’, Ukraine (as “Kupjansk”, “Gouvern. Charkov” [then Kharkov Governorate of the Russian Empire]). Unspecified number of syntype females and males [type depository not indicated in the original description], lost (not examined).
Schedius flavofasciatus
García Mercet, 1921: 315–318. Type locality (of the lectotype designated by
Ooencyrtus telenomicida
(Vassiliev):
Neotype female [
Romania, Iaşi County, Ipatele, 46.918781N, 27.442949E, 317 m, 10.vi.2017, L. Fusu, O. A. Popovici, V. Chinan (from eggs of Eurygaster sp. on wheat) [3 females, two from egg mass # 22, one from # 32,
Color. Body (Fig.
Sculpture. Head with stronger sculpture on frontovertex; mesoscutum and axilla reticulate; scutellum (Fig.
Pubescence. Frontovertex, pronotum, mesoscutum, axilla, and scutellum with short, inconspicuous, fine, light setae except scutellum with a pair of longer, dark setae.
Head
(Fig.
Antenna
(Fig.
Mesosoma
(Fig.
Wings
not abbreviated, fore wing extending well beyond apex of gaster. Fore wing (Fig.
Legs. Mesotibial spur almost as long as mesobasitarsus (Fig.
Gaster
(Fig.
Measurements (µm) of the neotype. Mesosoma 418; gaster 400; ovipositor 370; mesotibia 375. Antenna: radicle 45; rest of scape 200; pedicel 70; F1 40; F2 40; F3 50; F4 50; F5 60; F6 50; clava 140. Fore wing 900:370; longest marginal seta 33. Hind wing 725:135; longest marginal seta 48.
Female. Variation (non-type specimens from Romania, Russia, and Ukraine). Body length of dry-mounted, air-dried specimens 860–925 µm. Body (Figs
Male (non-type specimens from Russia). Body length of dry-mounted, air-dried specimens 600–900 µm. Body (Fig.
Morphometric ratios and measurements (µm) of morphological characters of female Ooencyrtus telenomicida from Russia and the Ukraine. All measurements are from slide-mounted specimens.
Length ovipositor: length mesotibia | Length: width fore wing | Length: width hind wing | Length: width scape | Length: width clava | Length F1: length pedicel | Length F2: Length F1 | |
---|---|---|---|---|---|---|---|
Range | 0.89–1.02 | 2.22–2.71 | 4.13–5.20 | 6.19–8.75 | 2.56–4.09 | 0.47–0.65 | 1.00–1.17 |
Mean | 0.94 | 2.43 | 4.6 | 7.2 | 3.4 | 0.55 | 1.09 |
n | 12 | 9 | 10 | 10 | 10 | 10 | 10 |
Length F1 | Length F2 | Length F3 | Length F4 | Length F5 | Length F6 | ||
Range | 34–49 | 37–51 | 40–55 | 43–58 | 49–65 | 46–62 | |
Mean | 39 | 43 | 50 | 52 | 55 | 52 | |
n | 10 | 10 | 10 | 10 | 10 | 10 |
Morphometric ratios and measurements (µm) of morphological characters of male Ooencyrtus telenomicida from Russia. All measurements are from slide-mounted specimens.
Length body | Length genitalia | Length: width scape | ||||
---|---|---|---|---|---|---|
Range/Value | 836 | 175 | 2.9–6.3 | |||
Mean | – | – | 4.6 | |||
n | 1 | 1 | 2 | |||
Length F1 | Length F2 | Length F3 | Length F4 | Length F5 | Length F6 | |
Range/Value | 74 | 74–80 | 74 | 74 | 74–77 | 65 |
Mean | 1 | 77 | 74 | 74 | 75 | 1 |
n | – | 2 | 2 | 2 | 2 | – |
Morphometric ratios and measurements of morphological characters of two female Ooencyrtus telenomicida, including the neotype, from Romania. All measurements are from slide-mounted specimens.
Body length | Length ovipositor: length mesotibia | Length: width fore wing | Length: width scape | Length: width clava | Length F1: length pedicel | Length F2: length F1 | |
Range | 978 | 0.92–0.96 | 2.45–2.49 | 6.0–8.0 | 3.0–3.4 | 0.60–0.64 | 1.0 |
Mean | – | 0.94 | 2.47 | 7.0 | 3.2 | 0.62 | 1.0 |
n | 1 | 2 | 2 | 2 | 2 | 2 | 2 |
Length F1 | Length F2 | Length F3 | Length F4 | Length F5 | Length F6 | ||
Range | 43 | 43 | 49 | 49 | 52–55 | 49–54 | |
Mean | 43 | 43 | 49 | 49 | 54 | 51 | |
n | 2 | 2 | 2 | 2 | 2 | 2 |
Confirmed records of O. telenomicida are from Romania, Russia, Spain and Ukraine; those from other countries in the Palearctic and Oriental regions were summarized by
Scutelleridae (Hemiptera): Eurygaster integriceps Puton (
Ooencyrtus telenomicida is a facultative hyperparasitoid of Eurygaster integriceps, being either a primary egg parasitoid (more so earlier in the season when unparasitized eggs of the host are readily available and prevalent) or a secondary parasitoid via the telenomine primary egg parasitoids, particularly later in the season when many of the host eggs are parasitized (
According to V. A. Trjapitzin (personal communication), the entire type series of O. telenomicida, if such ever existed, has never been located and is certainly lost. The dire necessity of a proper recognition of this nominal species, which has been impossible with any confidence from some other members of the O. telenomicida species complex (e.g., according to
Based on this information, a genetic library of other members of the complex can be constructed, and their identity determined.
Multivariate ratio analysis for Ooencyrtus mirus sp. nov. and O. telenomicida A scatterplot of isosize against first shape PC B shape PCA, scatterplot of first against second shape PC C PCA ratio spectrum for PC1, bars represent 68% confidence intervals D allometry ratio spectrum; bars represent 68% confidence intervals.
COI fragment sequences of O. lucidus, O. mirus, and O. telenomicida from Romania were trimmed for alignment and analysis with sequences of O. telenomicida, O. pistaciae Hayat & Mehmejad, O. pityocampae (García Mercet), O. mevalbelus Guerrieri & Samra, O. zoeae Guerrieri & Samra, and O. kuvanae (Howard) from
First five best ratios found by the LDA ratio extractor for separating O. mirus sp. nov. and O. telenomicida. Standard distance indicates how well one ratio discriminates compared to another; δ indicates how well shape discriminates compared to size (values close to 0 indicate no influence of size and those close to 1 indicate separation based mainly on size). Ranges were calculated on all available measurements, not only on those from the complete dataset used in the analysis. The ratio marked with * has very little overlap.
Ratio | Ranges | Standard distance | δ | |
---|---|---|---|---|
O. telenomicida | O. mirus | |||
L.mesotibia/L.clava | 7.56–12.36 | 7.29–9.66 | 11.9 | 0.18 |
W.scape/L.F5* | 0.44–0.63 | 0.61–0.74 | 11.73 | 0.18 |
L.F4/L.scutel | 0.22–0.31 | 0.25–0.28 | 11.5 | 0.18 |
W.clava/L.pedicel | 0.46–0.70 | 0.53–0.67 | 11.11 | 0.19 |
L.F2/L.F3 | 0.75–0.92 | 0.78–1.00 | 10.7 | 0.19 |
COI alignment and p-distance calculations among the Ooencyrtus species revealed at least 5.9% and 7.3% genetic divergence in O. mirus and O. lucidus, respectively, from O. telenomicida and other analyzed Ooencyrtus species (Table
Analysis of the ITS2 region further demonstrated genetic separation of these species. Intraspecific variation in this region is absent to extremely low, while interspecific variation is expected to be high. Our analysis was based on a partial fragment of the ITS2 region because the full sequence was not obtained for every specimen; however, the region analyzed was flanked by regions of congruence (16 bases at the 5’ end and 22 bases at the 3’ end; average 385 bp region analyzed for each species). The lowest p-distance between O. mirus and all compared species in this region was 0.069 (6.9% pairwise distance), which was demonstrated with O. pistaciae (Table
Uncorrected pairwise-distances between Ooencyrtus lucidus sp. nov., O. mirus sp. nov., O. telenomicida, and other congeneric species. Proportions were determined for a fragment of the mitochondrial cytochrome c oxidase I (COI) gene and the nuclear internal transcribed spacer 2 region (ITS2). Values to the left are the p-distances observed based on the COI gene region, while values to the right are p-distances observed based on the ITS2 region. Values on the diagonal element within the parentheses represent the intraspecific variation observed.
1 | 2 | 3 | |
---|---|---|---|
1. O. lucidus | (0.000) / (0.000) | – | – |
2. O. mirus | 0.087 / 0.227 | (0.000) / (0.000) | – |
3. O. telenomicida Romanian | 0.096 – 0.104 / 0.216 | 0.067 – 0.074 / 0.072 | (0.031) / - |
4. O. telenomicida East Mediterranean | 0.080 – 0.086 / 0.224 | 0.060 – 0.070 / 0.077 | 0.056 – 0.076 / 0.062 |
5. O. pistaciae | 0.073 – 0.078 / 0.223 | 0.059 – 0.065 / 0.069 | 0.063 – 0.079 / 0.064 |
6. O. pityocampae | 0.082 – 0.085 / 0.226 | 0.062 – 0.066 / 0.144 | 0.073 – 0.079 / 0.134 |
7. O. mevalbelus | 0.091 – 0.094 / 0.205 | 0.070 – 0.074 / 0.091 | 0.075 – 0.093 / 0.075 |
8. O. zoeae | 0.078 – 0.084 / 0.202 | 0.062 – 0.066 / 0.096 | 0.074 – 0.087 / 0.083 |
9. O. kuvanae | 0.097 / 0.442 | 0.091 / 0.428 | 0.098 – 0.109 / 0.425 |
Phylogenetic analysis of Ooencyrtus species, inferred using concatenated COI and ITS2 genetic regions, supported O. mirus as a sister taxon to O. telenomicida from Romania (Fig.
Relationship of Ooencyrtus lucidus sp. nov., O. mirus sp. nov., and O. telenomicida with other congeneric species based on concatenated partial regions of the mitochondrial cytochrome c oxidase I (COI) gene and the nuclear internal transcribed spacer 2 region (ITS2). Optimal maximum likelihood phylogenetic tree based on the Tamura-Nei model. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches (values over 50 are shown), and the tree is drawn to scale with branch lengths indicating uncorrected p-distance.
Members of the speciose genus Ooencyrtus, in which more than 300 currently valid species are known, are notoriously difficult to identify morphologically. That is particularly true for the taxa within the O. telenomicida species complex in the Old World. In the New World, identification keys exist only for some Neotropical species (
Traditionally, the standard DNA barcode region of the COI gene described in
We are very grateful to John S. Noyes (
Measurements used in the multivariate ratio analysis for Ooencyrtus mirus Triapitsyn & Power and O. telenomicida (Vassiliev) (Hymenoptera: Encyrtidae)
Data type: measurement
Explanation note: The complete set of measurements used in the multivariate ratio analysis for Ooencyrtus mirus Triapitsyn & Power and O. telenomicida (Vassiliev).