Research Article |
Corresponding author: Y. Miles Zhang ( yuanmeng.zhang@gmail.com ) Academic editor: Petr Janšta
© 2017 Y. Miles Zhang, Michael W. Gates, Joseph D. Shorthouse.
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:
Zhang YM, Gates MW, Shorthouse JD (2017) Revision of Canadian Eurytomidae (Hymenoptera, Chalcidoidea) associated with galls induced by cynipid wasps of the genus Diplolepis Geoffroy (Hymenoptera, Cynipidae) and description of a new species. Journal of Hymenoptera Research 61: 1-29. https://doi.org/10.3897/jhr.61.13466
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Eurytomids are small parasitic wasps associated with many communities of phytophagous insects. In most cases, the accurate identification of eurytomids is impeded by inadequate species descriptions that do not include figures of diagnostic features, and keys that are difficult to use. Here, diagnostic features and redescriptions are provided for both sexes of the eurytomids associated with galls induced by cynipid wasps of the genus Diplolepis Geoffroy found on shrub roses across Canada. Consequently, six species of Eurytoma Illiger, along with Tenuipetiolus ruber Bugbee, are dealt with. One new species, Eurytoma shorthousei Zhang & Gates, sp. n., is described. Two species are synonymized, E. hebes Bugbee, 1973 and E. spina Bugbee, 1951 under E. longavena Bugbee, 1951, syn. n. Several new host and distribution records are reported. A dichotomous key is provided for both sexes of all seven species using photographs and scanning electron microscopy images.
Eurytomidae , Diplolepis , Eurytoma , Tenuipetiolus , Canada
The interaction between insect herbivores and their associated natural enemies is one of the key factors in understanding the origin and evolution of multi-trophic systems. One particularly species-rich, ecologically-closed model system for studies of host-parasitoid relationships is the community of gall wasps (Hymenoptera: Cynipidae) and their associated inquilines (e.g. Periclistus spp., Cynipidae: Diastrophini) and parasitoids (primarily Hymenoptera: Ichneumonoidea, Chalcidoidea) on oaks and roses (
Members of the family Eurytomidae (Hymenoptera: Chalcidoidea) are one of the most common parasitoids associated with cynipid galls on roses in Canada, often comprising up to 40% of the component community (
Recent phylogenetic analyses redefined Eurytomidae as a monophyletic group (
All species with a carinate gena and showing no other outstanding characters were redefined as Eurytomasensu stricto (s.s.) with the following derived states: 1) Postgenal lamina present and raised ventrally over the surface of the postgena; 2) Postgena with a ventral depression between the posterior margin of the gena and the hypostomal fossa, with the depression delimited dorsally by a ridge or a step; 3) Gena with posterior margin slightly angulate above oral fossa (
Most eurytomids associated with galls induced by Diplolepis are univoltine. They feed throughout the summer on larvae of the gall inducer, inquilines, or on other parasitoids, overwinter as larvae within gall chambers, pupate in the spring and turn into adults (
Eurytomid larvae in gall chambers with immature Diplolepis feed as koinobionts, keeping the inducer alive until the larva is fully grown and then consume it. This is necessary since the eurytomid larva grows to the same size as its single host. Eurytomids commonly feed on gall tissues along the inside surface of galls after the inducer is consumed (Fig.
Eurtyoma longavena 1 Female ovipositing into immature gall 2 Egg deposited on the inside surface of gall chamber 3 Mature larva inside a gall showing frass as a result of feeding on gall tissue 4 Pupa overwintering inside the gall before exiting the following year. Tenuipetiolus ruber 5 Propodeum + petiole. Photos 1–4 credit Brandy L. Fenwick.
Fully grown eurytomid larvae can be distinguished from larvae of other parasitoids in Diplolepis galls by their cylindrical body shape and the presence of dorsal protuberances (
The objective of this study is to describe both male and female eurytomids associated with rose galls in Canada, as well as updating morphological characters, hosts, and distributional records following the molecular study using COI (
The eurytomids used for this study were from the collection of J. D. Shorthouse (JDS), previously deposited at Laurentian University in Sudbury, Ontario. Upon JDS’s retirement, pin-mounted specimens were deposited in the Canadian National Collections of Insects, Arachnids, and Nematodes (
The specimens were photographed using a Canon 7D Mark II with either a Canon MP-E 65mm F/2.8 Macro Photo Lens, or with a Mitutoyo M Plan Apo 10x objective mounted onto the Canon EF Telephoto 70–200 mm zoom lens, and the Canon MT-24EX Macro Twin Lite Flash with custom made diffusers to minimize hot spots. Scanning electron microscopy (SEM) micrographs were taken using methods described by
1 | Female. Gt1 and Gt2 fused dorsally. Petiole longer than metacoxa (Fig. |
Tenuipetiolus ruber |
– | Female. Gt1 and Gt2 not fused dorsally. Petiole subequal in length to metacoxa (Fig. |
Eurytoma Illiger 2 |
2 | Tegula, scape and pedicel yellow (Figs |
E. shorthousei sp. n. |
– | Tegula black to brown, scape and pedicel black with yellow restricted to basal region (Fig. |
3 |
3 | Pro- and mesocoxa yellow to brown, never entirely black (Fig. |
E. iniquus |
– | Pro- and mesocoxa entirely black (Fig. |
4 |
4 | Female. Gaster dorsal outline S-curve shaped in lateral view, longer than head plus mesosoma, ovipositor sheath upturned (Fig. |
E. discordans |
– | Female. Gaster not S-curve shaped (Fig. |
5 |
5 | Scape entirely black (Fig. |
E. longavena |
– | Scape black with yellow at extreme base or along entire anterior surface | 6 |
6 | Female metasoma small, oval shaped (Fig. |
E. imminuta |
– | Female metasoma large, elongate (Fig. |
E. spongiosa |
Tenuipetiolus ruber 6 Female habitus. Eurytoma iniquus 7 Female habitus. E. longavena 8 Female habitus. E. discordans 9 Female habitus. E. imminuta 10 Female habitus (length 2.0 mm). E. spongiosa 11 Female habitus (length 3.2 mm), arrow pointing to precoxal tooth formed by the adscrobal carina.
Tenuipetiolus
rubra
Bugbee, 1951a: 39–42. Holotype female (
Body length 2.0–3.6 mm. Color: Black except yellow to brown on basal half of scape, pedicel, and funicular segments, apices of all femora, pro-, meso- and metatibia, tip of ovipositor sheath, tegula, wing venation; all tarsomeres 1–4 white (Fig.
Head. Head 1.2× as broad as high, umbilicate punctured with small tentorial pits. Genal carina present. Malar space 0.8× eye height, clypeus emarginate and supraclypeal area superficially rugose. Toruli positioned dorsad lower ocular line. Antenna with funicular segments subequal in length; pedicel chalice-shaped; funiculars fusiform with one row longitudinal sensilla and two whorls of setae; F1 slightly narrowed basally. Ratio LOL:OOL:POL as 1:1:2.5. Head posteriorly without postgenal lamina or postgenal depression. Postgena sparsely setose.
Mesosoma. About 1.2× as long as broad; notauli incomplete, shallow. Epicnemium imbricate, flattened. Mesepisternum anterior to femoral depression umbilicate; mesepimeron reticulate ventrally, striolate or smooth dorsally, with longitudinal rugae originating from the posterior margin. Propodeum concave, superficially punctate, bordered mediolaterally by numerous carinae forming irregular setose cells, median furrow not delimited (Fig.
Metasoma. Gaster 1.5× as long as mesosoma in lateral view; smooth, anterior edge of gastral tergites microreticulate. Petiole 2× length of metacoxa (Fig.
Body length: 1.4–2.5 mm. Color as described for female. Sculpture as described for female. Antennae with funicular segments pedunculate, F2–F5 each with 2 rows of erect setae and 1 row of longitudinal sensilla; scape without ventral plaque. Petiole in lateral view cylindrical, in dorsal view about 3× as long as greatest width, 2× as long as metacoxa; strigose laterally.
This species is likely a generalist that is not restricted only to Diplolepis galls. Rearing records reported in the original description include cynipids of the genus Diastrophus.
Reared from field populations of galls induced by Diplolepis bassetti on Rosa woodsii Lindl.; D. polita, D. nodulosa, and D. triforma on Rosa acicularis Lindl.
(27 females, 12 males). CANADA: British Columbia: Osoyoos, 14.V.2003, J.D. & M.R. Shorthouse, ex Diplolepis bassetti on Rosa woodsii (3F, 3M,
Disjunctive populations have been found in Western Canada in British Columbia and Eastern Canada in Ontario and Québec (Fig.
This species is named for Joseph D. Shorthouse, honoring his contribution to the understanding of Diplolepis galls and their associated inhabitants, as well as the collector of the type specimens.
This species differs from other eurytomids studied in the yellow or brown scape and tegula, with supraclypeal area strigose (Fig.
Body length 3.2 mm. Color: Black except brown funicular segments, apices of procoxa and metafemur, metatibia excluding apex, and yellow scape, pedicel, pro- and mesotibia, mesofemur, apices of metatibia and metafemur, all tarsomeres 1–4, tip of ovipositor sheath, tegula, wing venation (Fig.
Head. 1.3× as broad as high, 2.5× as broad as long in dorsal view, umbilicate punctured. Malar space 0.5× eye height, malar carina present, raised in ventral half, becoming impressed line in dorsal half (Fig.
Mesosoma. About 1.2× as long as broad; notauli impressed, shallow. Epicnemium imbricate, flattened. Mesepisternum anterior to femoral depression, umbilicate; mesepimeron reticulate ventrally, striolate or smooth dorsally, with longitudinal rugae originating from the posterior margin. Precoxal tooth formed by raised adscrobal carina present in lateral view. Procoxa imbricate, lacking setation proximally, with oblique groove and S-like basal ridge. Metacoxa sparsely setose anteriorly and one row of setae on the posterior apical margin. Mesocoxal lamella absent. Lateral panels of propodeum and callus with umbilicate punctures distinctly delimited from median area by carinae forming irregular asetose cells, median furrow delimited, forming 1–2 rows of irregular foveae. Propodeal spiracle with raised rim anteriorly (Fig.
Metasoma. Gaster 1.5× as long as mesosoma in lateral view. Length 81 (valvulae excluded), height 55, relative lengths of Gt1–4 measured along dorsomedial line: 8:9:20:25; syntergum 7. Smooth, anterior edge of gastral tergites microreticulate. Petiole with three separate protuberances, one dorsomedial and two anterolateral (Fig.
Body length 3.0 mm. Color: Black, yellow and brown areas as described for female. Sculpture as described for female. Antennal segment ratios as: 52:14:3:36:27:31:27:27:42; funicular segments longer than wide, pedunculate, F2–F5 each with 3 irregular rows of appressed setae and two irregular rows of longitudinal sensilla; scape with ventral plaque in apical half (Fig.
Body length ranges from 2.5–3.2 mm in females, 1.7–3.0 mm for males. Occasionally, brownish area on anterior pronotum extends laterally onto collar.
This species was originally mistakenly identified as Eurytoma obtusilobae, described by Ashmead in 1885 based on four specimens, “bred from an unidentified cynips gall on Quercus obtusiloba [now stellata; post oak]” from Jacksonville, Florida. The only specimen remaining from this series is a female designated and labeled as a lectotype by
The lectotype of E. obtusilobae is not conspecific with E. shorthousei as noted below although the two species do resemble each other in general habitus. They were confused due because sharing the supraclypeal striae and similar sculpture and coloration. They may be separated as E. shorthousei has medially notched clypeal margin (Fig.
Found at only one site in this study, E. shorthousei’s distribution is wide in North America given the specimens reported by
Reared from field populations of galls induced by Diplolepis radicum on Rosa carolina, R. palustris, and R. woodsii.
Holotype. Female, CANADA: British Columbia: Central Okanagan; Kelowna 2 km S.E. of Kelowna airport 49.952N – 119.381W; 344m; J.D. Shorthouse & R.G. Lalonde; 14/10/1999. ex Diplolepis radicum on Rosa woodsii (
Collected in British Columbia and Manitoba (Fig.
Eurytoma
iniquus
Bugbee, 1951b: 253–254. Holotype female (
This species is similar to E. discordans, it can be distinguished by the yellow infuscation on the inner side of the pro- and mesocoxae (Fig.
Body length 2.2–3.0 mm. Color: Brown to black except for the following yellow to brown: inner faces of procoxa, pro- and mesofemur and tibia, apices of hindleg, protibia laterally, tip of ovipositor sheaths, all tarsomeres 1–4, wing veins (Fig.
Head. 1.3× as broad as high, umbilicate punctured with small tentorial pits. Genal carina present; malar space 0.8× eye height; clypeus truncate and supraclypeal area smooth (Fig.
Mesosoma. Largely umbilicate, 1.4× as long as broad; notauli complete, shallow. Epicnemium imbricate, flattened. Mesepisternum anterior to femoral depression umbilicate; mesepimeron reticulate ventrally, striolate or smooth dorsally, with longitudinal rugae originating from the posterior margin. Precoxal tooth formed by raised adscrobal carina present in lateral view. Lateral panels of propodeum and callus umbilicately punctate, distinctly delimited from median area by carinae forming irregular setose cells, median furrow delimited, forming 2 rows of irregular foveae (Fig.
Metasoma. Gaster 1.8× as long as mesosoma in lateral view; smooth, anterior edge of gastral tergites microreticulate (Fig.
Body length: 1.7–2.8 mm. Color: Black, yellow areas as described for female. Sculpture as described for female. Antennae with funicular segments pedunculate, F2–F5 each with 2 rows of erect setae and 1 row of longitudinal sensilla (Fig.
This species is likely a predator of inquiline Periclistus rather than the gall inducer, as they are reared from hosts that have a high rate of inquilism (
Reared from galls induced by Diplolepis bicolor on Rosa blanda; D. nodulosa on R. virginiana; D. polita, D. rosaefolii on R. acicularis; and D. variabilis on R. woodsii.
(33 females, 20 males). CANADA: Alberta: Peace River, 16.VIII.1970, J.D. & M.R. Shorthouse, ex Diplolepis polita fall/spring emergence (4F, 2M,
Eurytoma
longavena
Bugbee, 1951b: 249–250. Holotype female (
Eurytoma
hebes
Bugbee, 1973: 13–14. Holotype female (
Eurytoma
spina
Bugbee, 1951b: 250–251. Holotype female (
This species differs from other eurytomids in the wholly brown to black scape, legs (except apices of femora and tibiae) (Fig.
Body length 3.0–3.7 mm. Color: Black, except for the following yellow to brown: apices of all legs, protibia laterally, tip of ovipositor sheaths, tarsomeres, wing venation (Fig.
Head. 1.25× as broad as high, umbilicate punctured with small tentorial pits. Genal carina present; malar space 0.8× eye height; clypeus weakly emarginate and supraclypeal area smooth (Fig.
Mesosoma. Largely umbilicate, 1.2× as long as broad; notauli complete, shallow. Epicnemium imbricate, flattened. Mesepisternum anterior to femoral depression umbilicate; mesepimeron mesepimeron reticulate ventrally, striolate or smooth dorsally, with longitudinal rugae originating from the posterior margin. Precoxal tooth formed by raised adscrobal carina present in lateral view. Lateral panels of propodeum and callus umbilicately punctate, distinctly delimited from median area by carinae forming irregular setose cells, median furrow delimited, forming 2 rows of irregular foveae (Fig.
Metasoma. Gaster 1.3× as long as mesosoma in lateral view; smooth, anterior edge of gastral tergites microreticulate (Fig.
Body length: 1.7–2.2 mm. Color: Black, yellow areas as described for female. Sculpture as described for female. Antennae with funicular segments pedunculate, F2–F5 each with 2 rows of erect setae and 1 row of longitudinal sensilla (Fig.
This widespread species is found from galls of 7 native species of Diplolepis that induce galls on leaves. Additionally, it is collected from stem galls of D. fusiformans, a species that is closely related to D. rosaefolii, which induces galls on leaves (
Reared from galls induced by Diplolepis bassetti, D. bicolor, D. fusiformans on R. blanda; D. gracilis on R. woodsii; D. nebulosa on R. blanda; D. polita, D. rosaefolii on R. acicularis and R. woodsii; and D. variabilis on Rosa sp.
(52 females, 22 males). CANADA: Alberta: Coaldale, 24.X.2002, J.D. Shorthouse, ex Diplolepis nebulosa on Rosa woodsii (2F, 1M,
Widespread, from British Columbia, Alberta, Saskatchewan, Ontario, and Québec (Fig.
Eurytoma
discordans
Bugbee, 1951b: 220–223. Holotype female (
Eurytoma
acuta
Bugbee, 1951b: 223–234. Holotype female (
Eurytoma
calcarea
Bugbee, 1951b: 240–249. Holotype female (
Females are distinguished from other species by the S-curved metasoma that is larger than head plus mesosoma (Fig.
Body length 2.1–5.0 mm. Color: Black except for the following yellow – basal half of scape, pro- and mesofemur, basal pro- and mesotibia, apex of metatibia, tip of ovipositor sheaths, tarsomeres 1–4, wing veins (Fig.
Head. 1.2× as broad as high, umbilicate punctured (Fig.
Mesosoma. Largely umbilicate, 1.5× as long as broad; notauli complete, shallow. Epicnemium imbricate, flattened, with superficial submedial, shallow depressions to receive procoxa. Mesepisternum anterior to femoral depression umbilicate; mesepimeron reticulate ventrally, striolate or smooth dorsally, with longitudinal rugae originating from the posterior margin. Precoxal tooth formed by raised adscrobal carina present in lateral view. Lateral panel of propodeum and callus with umbilic punctures, distinctly delimited from median area by carinae forming irregular setose cells, median furrow delimited, forming 2 rows of irregular foveae (Fig.
Metasoma. Gaster 1.8× as long as mesosoma in lateral view; smooth, anterior edge of gastral tergites microreticulate (Fig.
Body length: 1.7–3.1 mm. Color: Black, yellow areas as described for female. Sculpture as described for female (Fig.
This is a widespread and morphologically variable species.
Reared from field populations of galls induced by D. bicolor on R. blanda; D. nodulosa on R. woodsii; D. spinosa on R. blanda and Rosa rugosa Thunb.; D. radicum on R. acicularis; D. tumida on R. woodsii; D. variabilis on R. woodsii. Also reared from galls of Diastrophus nebulosus (Osten Sacken) on Rubus spp..
(197 females, 120 males). CANADA: Alberta: Beaverlodge, 1933 (1F, CNC); Head-Smashed-In Buffalo Jump, 10.V.2011, J.D. & M.R. Shorthouse, ex Diplolepis tumida on Rosa woodsii (3F, 4M,
Eurytoma
imminuta
Bugbee, 1951b: 259–260. Holotype female (
Eurytoma imminuta can be distinguished from most Eurytoma species by black tegula and scape. E. imminuta differs from E. spongiosa by their small, oval metasoma that is not laterally compressed (Fig.
Body length 1.9–4.0 mm. Color: Black except for the following yellow – basal half of scape, apical fifth of pro- and mesofemur, basal pro- and mesotibia, apex of hindlegs, tip of ovipositor sheaths, tarsomeres 1–4, wing veination (Fig.
Head. 1.2× as broad as high, umbilicate punctured with small tentorial pits. Genal carina present; malar space 0.8× eye height, supraclypeal area smooth (Fig.
Mesosoma. Largely umbilicate, 1.5× as long as broad; notauli complete, shallow. Epicnemium imbricate, flattened. Mesepisternum anterior to femoral depression umbilicate; mesepimeron mesepimeron reticulate ventrally, striolate or smooth dorsally, with longitudinal rugae originating from the posterior margin. Precoxal tooth formed by raised adscrobal carina present in lateral view. Lateral panel of propodeum and callus with umbilicate punctures, distinctly delimited from median area by carinae forming irregular setose cells, median furrow delimited, forming 2 rows of irregular foveae (Fig.
Metasoma. Gaster 1.2× as long as mesosoma in lateral view; smooth, anterior edge of gastral tergites microreticulate (Fig.
Body length: 1.7–2.0 mm. Color: Black, yellow areas as described for female. Sculpture as described for female. Antennae with funicular segments pedunculate, F2–F5 each with 2 rows of erect setae and 1 row of longitudinal sensilla (Fig.
E. imminuta in the
Reared from galls induced by Diplolepis ignota on R. woodsii, D. nebulosa, D. polita, D. spinosa on R. blanda, R. rugosa; D. rosae on R. canina, D. triforma on R canina; D. tumida on R. woodsii, and D. variabilis.
(101 females, 50 males): CANADA: Alberta: Coaldale, 12.V.2007, J.D. & M.R. Shorthouse, ex Diplolepis ignota on Rosa woodsii (2F,
Widespread, from British Columbia, Alberta, Manitoba, Ontario, and Québec (Fig.
Eurytoma
spongiosa
Bugbee, 1951b: 254–258. Holotype female (
Similar to E. imminuta, but metasoma larger and more elongated (Fig.
Body length 1.0–4.0 mm. Color: Black except for the following yellow - basal half of scape, posterior half profemur, mesofemur, basal pro- and mesotibia, apex of hindlegs, tip of ovipositor sheaths, tarsomeres 1–4, wing veination (Fig.
Head. 1.3× as broad as high, with umbilicate punctures with small tentorial pits. Genal carina present; malar space 0.8× eye height; supraclypeal area smooth (Fig.
Mesosoma. Largely umbilicate, 1.5× as long as broad; notauli complete, shallow. Epicnemium imbricate, flattened. Mesepisternum anterior to femoral depression umbilicate; mesepimeron reticulate ventrally, striolate or smooth dorsally, with longitudinal rugae originating from the posterior margin. Precoxal tooth formed by raised adscrobal carina present in lateral view. Lateral panels of propodeum and callus with umbilicate punctures, distinctly delimited from median area by carinae forming irregular setose cells, median furrow delimited, forming 2 rows of irregular foveae (Fig.
Metasoma. Gaster 1.2× as long as mesosoma in lateral view; smooth, anterior edge of gastral tergites microreticulate (Fig.
Body length: 1.7–2.2 mm. Color: Black, yellow areas as described for female. Sculpture as described for female. Antennae with funicular segments pedunculate, F2–F5 each with 2 rows of erect setae and 1 row of longitudinal sensillae (Fig.
Few consistent morphological differences were found between E. imminuta and E. spongiosa (identified in
Reared from galls induced by D. fusiformans on R. blanda; Diplolepis ignota on R. arkansana Porter; D. nebulosa on R. blanda; D. polita on R. acicularis; D. triforma on R. acicularis and R. canina; and D. variabilis.
(28 females, 25 males). CANADA: Alberta: Coaldale, 12.V.2007, J.D. & M.R. Shorthouse, ex Diplolepis ignota on Rosa arkansana (4F, 2M,
From Alberta, Saskatchewan, Ontario, and Québec (Fig.
Taxonomic recognition of chalcid wasps of the family Eurytomidae is notoriously difficult, as is the case with members within the genus Eurytoma associated with galls of Diplolepis (
The overall morphological similarities between the Canadian species of Eurytoma with other members of the rosae species group found in Europe suggest that these species shared a common evolutionary line. As the rosae group is most diverse in Europe (
Although eurytomids are known from a wide variety of hosts (
Even without this more extensive analysis, some trends are already apparent. Firstly, the abundance of eurytomids in the galls of all species of Diplolepis from across Canada indicate that eurytomids are so closely associated with galls of Diplolepis that some species, or certain populations of these species, are now restricted to rose galls. Eurytomids attack both galls initiated in the spring (D. polita and D. spinosa) and those initiated later in the season (D. nebulosa and D. ignota) indicating that the emergence periods of eurytomids are lengthy enabling them to track different periods of gall initiation. Some species such as T. ruber and E. discordans attack both leaf and stem galls. Eurytoma iniquus and E. discordans attack both galls inhabited only by an inducer where they feed as koinobionts, along with inquiline-modified galls of the same Diplolepis where they feed as predators on immature Periclistus and then chew into several Periclistus-induced chambers to consume larvae (
Three of the most widely distributed galls in Canada are those induced by D. polita, D. spinosa and D. triforma and all are heavily attacked by eurytomids. These observations suggest that eurytomids are highly plastic in their choice of hosts, ability to locate roses and their galls in all parts of the range of each, feed as predators or koinobionts on all species of gall inhabitants, tolerate cold and dry conditions of northern Canada, and in the case of E. longavena, have two generations per year when populations of the same gall appear both in the spring and mid-summer (
While the distribution of eurytomids in this study only includes localities within Canada, it is likely representative of the Nearctic fauna even though most diversity of wild roses occurs within Canada (
The systematic placement of the Eurytomidae within the superfamily Chalcidoidea has been controversial in past studies (
The authors thank Yves Alarie, Brandy Fenwick, David Lesbarrères, and Alexander Smith for suggestions on improving the manuscript on this and previous versions. This project was supported by a Natural Sciences and Engineering Research Council Discovery Grant, a grant from the Laurentian University Research Fund, and funds from the Northern Scientific Training Program to sample galls along the shore of James Bay, awarded to JDS. USDA is an equal opportunity employer and provider. Any trade names mentioned herein does not imply endorsement by USDA.