A biodiversity hotspot for Microgastrinae (Hymenoptera, Braconidae) in North America: annotated species checklist for Ottawa, Canada

Jose Fernandez-Triana; Caroline Boudreault; Joel Buffam; Ronald Mclean

doi:10.3897/zookeys.633.10480

. 2016 Nov 17;(633):1–93. doi: 10.3897/zookeys.633.10480

A biodiversity hotspot for Microgastrinae (Hymenoptera, Braconidae) in North America: annotated species checklist for Ottawa, Canada

Jose Fernandez-Triana ¹, Caroline Boudreault ¹, Joel Buffam ¹, Ronald Mclean ¹

PMCID: PMC5126526 PMID: 27917045

Abstract Abstract

Microgastrinae wasps (Hymenoptera, Braconidae) from the city of Ottawa and its surroundings (a 50-km radius circle, ~7,800 km²) were studied based on 1,928 specimens collected between 1894 and 2010, and housed in the Canadian National Collection of Insects. A total of 158 species from 21 genera were identified, which is by far the highest number of species ever recorded for a locality in North America. An annotated checklist of species is provided. Choeras parasitellae (Bouché, 1834) and Pholetesor nanus (Reinhard, 1880) are recorded for the first time in the Nearctic (previously only known from the Palearctic region), Cotesia depressa (Viereck, 1912) is recorded for the first time in Canada (previously only known from the United States), and Cotesia hemileucae (Riley, 1881) and Protapanteles phlyctaeniae (Muesebeck, 1929) are recorded for the first time in the province of Ontario. In Ottawa the most diverse genera are Cotesia, Apanteles, Microplitis, Pholetesor, Microgaster, and Dolichogenidea, altogether comprising 77% of the species found in the area. A total of 73 species (46%) were represented by only one or two specimens, suggesting that the inventory for Ottawa is still relatively incomplete. Seasonal distribution showed several peaks of activity, in spring, summer, and early fall. That general pattern varied for individual species, with some showing a single peak of abundance either in the summer or towards the end of the season, others species attaining two peaks, in late spring and late summer, or in early summer and early fall, and yet others attaining up to three different peaks, in spring, summer and fall. At least 72 of the Microgastrinae species from Ottawa have been previously associated with 554 species of Lepidoptera as hosts – but those historical literature records are not always reliable and in many cases are based on data from areas beyond Ottawa. Thus, our knowledge of the associations between the 158 species of microgastrine parasitoids and the caterpillars of the 2,064 species of Lepidoptera recorded from Ottawa is still very incomplete.

Keywords: Microgastrinae, diversity, North America, Canada, Ottawa

Introduction

Microgastrinae wasps are the second largest subfamily of Braconidae (Hymenoptera) (Yu et al. 2016), and evidence suggests they may eventually prove to be the largest subfamily (e.g., Rodriguez et al. 2013). The number of described species has increased significantly within the past 35 years: in 1980 there were about 1,500 (Papp 1976, Mason 1981), by 2012 there were more than 2,200 (Yu et al. 2012), and currently the total surpasses 2,700 (Yu et al. 2016). The actual diversity worldwide is estimated to be 20,000–46,000 species (Rodriguez et al. 2013), meaning that most likely 10% or even less of the extant species have been described.

At the regional or local level our knowledge about Microgastrinae is also very incomplete, with few biodiversity inventories available and most published information not being comprehensive enough to capture the actual diversity of species. Examples in North America include Lewis and Whitfield (1999), Whitfield and Lewis (2001), Shaw (2002), and Fernandez-Triana et al. (2009, 2011).

Besides its extraordinary diversity, microgastrine wasps are very important in biocontrol efforts against Lepidoptera pests, as they represent the single most important group of caterpillar parasitoids in the world (Whitfield 1997).

This paper analyzes the diversity of Microgastrinae of Ottawa (Canada) and the surrounding areas, discusses the significance of these results for future studies of the group in the Nearctic region, and provides an initial reference point for the Ottawa fauna (with a dynamic species checklist to be available online as well).

Methods

Since 1895, the Ottawa Field-Naturalists’ Club (http://www.ofnc.ca/) has considered a circle with a 50 km radius (approximately 7,800 km²) centered on the Peace Tower in downtown Ottawa as its study area. This human-defined region (variously named as ‘National Capital Region’, ‘Ottawa-Gatineau Region’, ‘Ottawa Region’, ‘Ottawa District’) has been widely adopted and used in many scientific papers and conservation efforts conducted in the city over the past 120 years. We follow the same concept, henceforth calling it simply ‘Ottawa’ for brevity. Figure 1 shows the localities within this 50-km radius where specimens of Microgastrinae had been collected and were available to us for study. For consistency, we do not include data from a few additional species collected in localities slightly out of this 100 km diameter circle even though, from a natural perspective, those species are very likely to be found in Ottawa as well.

Figure 1. — Localities within the city of Ottawa and surroundings where specimens of *Microgastrinae* were collected (1894–2010, data based on *CNC* holdings only).

This paper is based on the study of 1,928 specimens, housed in the (CNC); they were all databased and assigned to species following the most recent taxonomic information available for Canada (Fernandez-Triana 2010, 2014, 2015, Fernandez-Triana et al. 2013, 2014a, 2014b, 2015). Some specimens could only be identified to genus but in all cases they had unique morphological characteristics and/or DNA barcodes that clearly identified them as distinct species–in those cases we use an alphanumeric species identifier e.g., ‘Apanteles jft09’. In order to allow these provisional species to be recognized and studied further in the future we also provide DNA (BINs) (Ratnasingham and Hebert 2013) for them in the annotated species checklist.

Pictures of 36 species are provided to illustrate the diversity of microgastrine wasps in Ottawa. Photos were taken either with a Leica M165 C or a Keyence VHX-1000 Digital Microscope, using a lens with a range of 10–130 ×. Multiple images were taken of a structure through the focal plane and then combined to produce a single in-focus image. For the images taken with the Leica camera, the Zerene Stacker program (http://zerenesystems.com/cms/stacker) was used; software associated with the Keyence System produced focused images taken with that camera. Images were corrected using Adobe Photoshop CS4 and the plates were prepared using Microsoft PowerPoint 2010.

A species checklist was generated using the CNC database (http://www.cnc-ottawa.ca/taxonomy/TaxonMain.php). The list is organized alphabetically by genus and species within a given genus. For every taxon we detail general distribution (outside Ottawa), specimens examined, and notes on species where relevant. For zoogeographic regions we used the following acronyms: NEA, NEO, OTL, and PAL.

Using the Scratchpad platform and infrastructure (Smith et al. 2011), the species checklist given here as the initial reference point for the Ottawa fauna of Microgastrinae will be made available online (http://microgastrinae.myspecies.info/content/microgastrinae-ottawa-canada), where updates will be maintained as and when changes occur.

Results

A total of 158 species from 21 genera of Microgastrinae are recorded from Ottawa. Choeras parasitellae (Bouché, 1834) and Pholetesor nanus (Reinhard, 1880) are new records for the Nearctic (previously only known from the Palearctic region). Cotesia depressa (Viereck, 1912) is a new record for Canada (previously only known from the United States). Cotesia hemileucae (Riley, 1881) and Protapanteles phlyctaeniae (Muesebeck, 1929) are new records for Ontario.

The most diverse genera were Cotesia (32 species), Apanteles (31), Microplitis (23), Pholetesor (13), Microgaster (11), and Dolichogenidea (11). These six genera together comprised 77% of the species found in the area. This pattern is similar to that found in both the whole Nearctic region (Whitfield 1995, Yu et al. 2012, 2016) as well as in specific North American localities that have been the focus of biodiversity inventories (Lewis and Whitfield 1999, Whitfield and Lewis 2001, Shaw 2002, Fernandez-Triana et al. 2009, 2011). A notable exception is Glyptapanteles, one of the most diverse genera in North America and elsewhere, but currently with only three species recorded from Ottawa. However, many species of that genus still remain unidentified and further study will certainly reveal a much higher diversity for Glyptapanteles in the area. Five genera of Microgastrinae reached their northernmost known distribution in Ottawa: Alphomelon, Clarkinella, Distatrix, Protomicroplitis and Pseudapanteles (Fernandez-Triana 2010, 2014, 2015, Fernandez-Triana et al. 2014c).

At species level, the most common were Glyptapanteles militaris (Walsh, 1861) (322 specimens), Pholetesor ornigis (Weed, 1887) (157), Glyptapanteles pallipes (Reinhard, 1880) (87), Apanteles nephoptericis (Packard, 1864) (82), Cotesia atalantae (Packard, 1881) (77), Microplitis varicolor Viereck, 1917 (72), Hypomicrogaster zonaria (Say, 1836) (65), Dolichogenidea cacoeciae (Riley, 1881) (59), Hygroplitis melligaster (Provancher, 1886) (47), and Cotesia laeviceps (Ashmead, 1890) (45). Those ten species together represented 53% of all Microgastrinae specimens collected in Ottawa.

There were 50 species (31.4%) represented by only one specimen, and 23 (14.4%) represented by two specimens. The high proportion (45.9%) of singletons and doubletons shows how incomplete the Ottawa species inventory still is. The Chao-1 non-parametric estimator of species richness (Rarefaction Calculator at http://www.biology.ualberta.ca/jbrzusto/rarefact.php#Calculator) estimates 213.35 ± 16.29 species for Ottawa, thus our present knowledge represents less than 75% of the actual total of species to be found there.

Among all listed species, 73 were only identified to genus and have been assigned interim alphanumeric identifiers. Some of them certainly represent new taxa to be described in future papers. Others may represent species already described in Europe and for the present are given interim identifiers until they are compared with Palearctic material.

Regarding zoogeographical affinities, 132 species (83%) found in Ottawa are strictly Nearctic, 16 species (10%) are distributed within the Holarctic, 5 (3%) are recorded from the New World (Nearctic and Neotropics), and 10 (6%) are either truly cosmopolitan or present in at least three different regions (Nearctic/Neotropics/Palearctic or Nearctic/Oriental/Palearctic).

Some of the localities sampled contain special, sometimes unique habitats/ecosystems. Gatineau Park, with a rich biodiversity and a wide range of protected habitats and ecosystems within its 36,000 ha (http://www.ncc-ccn.gc.ca/places-to-visit/gatineau-park/conservation-gatineau-park) contains five species so far found nowhere else within the Ottawa area: Alphomelon winniewertzae Deans, 2003, Cotesia depressa (Viereck, 1912), Cotesia diacrisiae (Gahan, 1917), Distatrix carolinae Fernandez-Triana, 2010, and Microplitis impressus (Wesmael, 1837).

Mer Bleue, a 3,500 ha conservation area with a northern, boreal-like ecosystem more typical of the Subarctic than the Ottawa Valley (http://www.ncc-ccn.gc.ca/places-to-visit/greenbelt/mer-bleue) harbours three species that have not been found elsewhere in the Ottawa area: Cotesia clisiocampae (Ashmead, 1903), Dolichogenidea absona (Muesebeck, 1965), and Pholetesor rhygoplitoides Whitfield, 2006. Similarly, the approximately 1,500 ha of alvar ecosystem near Almonte (Belcher et al. 1992) is the only known Ottawa-area locality for Pholetesor viminetorum (Wesmael, 1837). Further studies on the fauna of Microgastrinae may show that some of those species are more widely distributed within Ottawa or beyond, though some are likely to remain restricted to particular habitats or ecosystems where their hosts occur.

The diversity of Microgastrinae revealed for Ottawa is extraordinary: in spite of being a relatively small area (7,800 km²) its species total would rank 17^th among countries of the world (Table 1). And, when placed within the context of what has been published for other, similarly-sized localities in North America, Ottawa has the highest number of species, double the second most diverse locality (Table 2). Even when accounting for differences in collecting efforts and taxonomic coverage (e.g., it is clear that the relatively low diversity in the Yellowstone National Park is due to insufficient study of its Microgastrinae fauna), the total recorded in Ottawa may not be surpassed by any North American locality at a comparable latitude. The high diversity found in Ottawa likely relates to being a transition from an eastern deciduous forest biome to a boreal biome, with small areas of unusual habitats like dunes, alvars, floodplains, and bogs.

Table 1.

Microgastrinae diversity by country with over 100 species recorded. Data from Taxapad (Yu et al. 2012), Fauna Europaea (http://www.fauna-eu.org/) and the present paper (for Canada and Ottawa). For Costa Rica the total is a very conservative estimate based on numerous papers published after 2012 on the fauna of Area de Conservación Guanacaste (http://janzen.sas.upenn.edu/caterpillars/database.lasso).

Costa Rica	400+	Finland	163
Hungary	328	Ottawa	158
China	316	Mongolia	157
Russia	293	Italy	150
U.S.A.	284	Ukraine	149
Germany	249	Yugoslavia	139
United Kingdom	234	Democratic Republic of Congo	134
India	210	Bulgaria	124
Canada	196	Korea	124
Czech Republic	190	France	123
Romania	173	Sweden	117
Poland	170	Moldova	113
Switzerland	168	Slovakia	113
Turkey	167	Australia	112
Netherlands	176	Kazakhstan	112

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Table 2.

Microgastrinae diversity in selected North American localities. Data from Lewis and Whitfield (1999), Whitfield and Lewis (2001), Shaw (2002), Fernandez-Triana et al. (2009, 2011), and the present paper.

Locality/ecosystem	Latitude	Species recorded
Yellowstone National Park, Montana/forests	44°N	35
Quebec/apple orchards	45°N	36
Midwestern USA/tall grass prairies	39°N	55
Arkansas/forests	34°N	65
Churchill, Manitoba/boreal forest/tundra	59°N	79
Ottawa, Ontario/diverse habitats	45°N	158

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We are not aware of published information for more southern localities, although based on specimens seen in collections (Fernandez-Triana, unpublished), it is clear that southern localities in the United States, when thoroughly sampled and studied, should have higher species totals. But Ottawa presently is the biodiversity hotspot for Microgastrinae in North America, a result of its habitat diversity and the relatively comprehensive taxonomic studies done on its fauna.

The Ottawa microgastrines we studied were collected from 1894–2010 (Figure 2), with most of the specimens collected either from 1945–1975 or 2007–2008. More recent material (2012–2016) is presently being prepared and will be included in future updates of the current species list.

Seasonal distribution of the specimens in general (Figure 3) shows several activity peaks: 1) spring (second half of May to second half of June), 2) a larger peak in summer (late July to early August), and 3) a smaller peak in early fall (September). This pattern is somewhat similar to that found in another intensively studied Canadian locality (Churchill, Manitoba, at 59°N), although there were only two peaks in that more northern area, due to its shorter season (Fernandez-Triana et al. 2011).

The general pattern varies depending on the species. Among the eight most common species, five show only a single peak of abundance, three in summer (Glyptapanteles militaris, Cotesia atalantae and Hygroplitis melligaster), and two in the fall (Apanteles nephoptericis and Glyptapanteles pallipes). Two species have two peaks, Pholetesor ornigis in late spring and late summer, and Hypomicrogaster zonaria in early summer and early fall. Microplitis varicolor has three peaks in spring, summer and fall (Fig. 4). As more collected material becomes available, a better picture of species seasonality will be obtained.

Figure 4. — Bi-weekly (March-November) abundance of the eight most common species of *Microgastrinae* collected in Ottawa, based on *CNC* holdings only (1894–2010).

Species of Microgastrinae are parasitoids exclusively of Lepidoptera (Whitfield 1997). There are at least 2,064 species of Lepidoptera already recorded from Ottawa (D. Lafontaine, in lit. 2016, Lafontaine 1997; http://www.acleris.com/dls/habitat-diversity.html), with the actual number probably approaching 2,200 species (D. Lafontaine, pers. com.). A literature search shows that 72 of the Microgastrinae species found in Ottawa have been, at some point, recorded parasitizing at least 554 Lepidoptera species (based on data compiled by Yu et al. 2012).

However, it must be pointed that some of those lepidopterans do not actually occur in Ottawa, and some of the reported host/parasitoid associations are likely to be incorrect (see Shaw et al. 2009 for a discussion and examples that demonstrate the pitfalls of using compilations of host/parasitoid abstracted uncritically from the literature). Our knowledge of the association between lepidopteran caterpillars and their microgastrine parasitoids at the local and/or regional level is still very incomplete, and many more studies are needed before some patterns can be reliably established. Thus, in this paper we do not analyze further the relationships between Microgastrinae and Lepidoptera in Ottawa.

Evidence from recent studies in (ACG), Costa Rica, comprising 11,000+ Lepidoptera and 1,100+ Microgastrinae species (e.g., Janzen and Hallwachs 2016) shows that microgastrine wasps are more specialized (=host specific) than previously thought. Most species have been found parasitizing one/few species of Lepidoptera which are usually phylogenetically related or, alternatively, related ecologically in the niche they occupy (e.g., Fernandez-Triana et al. 2014d). At present there is no comprehensively enough information in North America to compare, but the available (more limited) data suggests that it might well be the same situation as in the tropics. Based on the currently verified and available data, the ratio between species of Lepidoptera (2,064) and Microgastrinae (158) in Ottawa stands at 13.1, very similar to the ratio found in ACG and other regions of world (Fernandez-Triana 2010, Rodriguez et al. 2013, Janzen and Hallwachs 2016). The significance of the Lepidoptera/Microgastrinae ratio has been discussed further in Rodriguez et al. (2013).

Annotated checklist of Microgastrinae from Ottawa, Canada

Alphomelon winniewertzae

Deans, 2003

Fig. 5

Viereck, 1912

Fig. 11

Figure 11. — *Apanteles* *polychrosidis*. A Habitus, lateral B Head, lateral C Wings D Metasoma, dorsal E Head and mesosoma (partially), dorsal F Metasoma, lateral.

Distribution.

NEA.

Material examined.

Quebec, Aylmer, 45.4 -75.85, 10.vii.2004, S. Laplante, Voucher Code: HYM00001646.

Apanteles jft01

Distribution.

NEA.

Notes.

This species corresponds in BOLD to BIN BOLD:AAA6373, with specimens found across Canada and US.

Material examined.

Ontario, 5 km NW of Almonte, Hwy 49, Burnt Land, Alvar Prov. Park, Almonte, 45.2549 -76.14, 29.v.2008, Goulet & Fernandez, Voucher Code: CAM0353, CAM0357, CAM0361, CAM0364; Ottawa, city garden, 45.3561 -75.707, 2.vii.2007, H. Goulet, Voucher Code: CAM0128; 30.v.2007, H. Goulet, Voucher Code: CAM0012, CAM0017; Woodlawn, 45.375 -76.083, 6.viii.2008, L. Masner, Voucher Code: MIC000599, MIC000601.

NEA.

Notes.

Material examined.

Ontario, 5 km NW of Almonte, Hwy 49, Burnt Land, Alvar Prov. Park, Almonte, 45.255 -76.14, 29.v.2008, Goulet & Fernandez, Voucher Code: CAM0340, CAM0341, CAM0342, CAM0344, CAM0345, CAM0346, CAM0347, CAM0349, CAM0350, CAM0351, CAM0352, CAM0356, CAM0360, MIC000666; Ottawa, city garden, 45.356 -75.707, 1.ix.2007, H. Goulet, Voucher Code: CAM0146, CAM0151, CAM0163, CAM0166; 10.viii.2007, H. Goulet, Voucher Code: CAM0039, CAM0113, CAM0115; 19.ix.2007, H. Goulet, Voucher Code: CAM0007, CAM0008; 23.vii.2007, H. Goulet, Voucher Code: CAM0054; 26.vi.2007, H. Goulet, Voucher Code: CAM0062, CAM0072, CAM0076; 30.v.2007, H. Goulet, Voucher Code: CAM0011, CAM0013; 30.vii.2007, H. Goulet, Voucher Code: CAM0120; 6.vii.2009, L. Masner, Voucher Code: CNCH1025; 8.ix.2007, H. Goulet, Voucher Code: CAM0099, CAM0103, CAM0106; 45.356000 -75.707000, 8.ix.2007, H. Goulet, Voucher Code: CAM0101.

Choeras consimilis

(Viereck, 1911)

Fig. 12

Figure 12. — *Choeras* *consimilis*. A Habitus, lateral B Wings C Head, frontal D Metasoma dorsal F Head and mesosoma, dorsal.

Distribution.

NEA.

Material examined.

Ontario, Ottawa, 45.3825 -75.7137, 1.ix.1952, J. F. McAlpine, Voucher Code: CNCHYM00278; Quebec, Gatineau Park, 45.600555 -76.042647, 13.vi.1966, D.P. Pielou, Voucher Code: CNC474797; 14.vii.1966, D.P. Pielou, Voucher Code: CNC474794; 15.vi.1965, W.G. Mathewman, Voucher Code: CNC474795; 23.vi.1966, D.P. Pielou, Voucher Code: CNC474793; 4.vii.1966, D.P. Pielou, Voucher Code: CNC474796; 45.60057 -76.042647, 16.vi.1967, W. G. Matthewman, Voucher Code: CNCHYM00272; 22.vi.1966, D. P. Pielou, Voucher Code: CNCHYM00277; 4.vii.1967, W. G. Matthewman, Voucher Code: CNCHYM00279.

Choeras parasitellae

Clarkinella canadensis

Mason, 1981

Fig. 13

Figure 13. — *Clarkinella* *canadensis*. A Habitus, lateral B Head, frontal C Wings D Head dorsal E Metasoma, dorsal F Head and mesosoma, dorsal.

Distribution.

NEA.

Notes.

This species is only known from the type locality (Ottawa), where it has been rarely collected. The status of this species as a potential member of the Species Candidate Lists of COSEWIC was assessed by Fernandez Triana (2014).

Material examined.

Ontario, Ottawa, city garden, 45.356100 -75.707000, 30.vii.2007, H. Goulet, Voucher Code: CAM0263; 8.ix.2007, H. Goulet, Voucher Code: CAM0262; Ottawa, 45.356083 -75.706933, 28.vii.1959, S.M. Clark, 45.406631 -75.701407, 28.vii.1959, S.M. Clark, Voucher Code: CNC15769.

Cotesia acronyctae

(Riley, 1871)

Fig. 14

Figure 14. — *Cotesia* *acronyctae*. A Habitus, lateral B Head, frontal C Wings D Metasoma, dorsal E Head and mesosoma, dorsal.

Distribution.

NEA.

Material examined.

Ontario, Ottawa, 45.406631 -75.701407, 4.x.1941, F.I.S., Voucher Code: CNC474798, CNC474799.

Cotesia atalantae

(Packard, 1881)

Fig. 15

(Ratzeburg, 1844)

Fig. 16

Distatrix carolinae

Fernandez-Triana, 2010

Fig. 18

Figure 18. — *Distatrix* *carolinae*. A Habitus, lateral B Head, frontal C Wings D Metasoma, dorsal E Head and mesosoma, dorsal.

Distribution.

NEA.

Notes.

Distribution.

NEA.

Notes.

This species corresponds in BOLD to BIN BOLD:AAA4784, with all specimens collected in North America.

Material examined.

Ontario, mixed forest, 45.2347 -75.624, 19-29.vi.2007, A. Bennett, Voucher Code: CAM0554; 7-19.vi.2007, A. Bennett, Voucher Code: CAM0555, CAM0556, CAM0557, CAM0558; Ottawa, city garden, 45.3561 -75.707, 30.vii.2007, H. Goulet, Voucher Code: CAM0264, CAM0265, CAM0274; Woodlawn, 45.375 -76.083, 17.viii.2008, L. Masner, Voucher Code: MIC000613; 6.viii.2008, L. Masner, Voucher Code: MIC000607, MIC000608, MIC000609, MIC000610, MIC000611, MIC000612; 8.ix.2008, L. Masner, Voucher Code: MIC000614, MIC000615, MIC000616, MIC000617

Hygroplitis melligaster

(Provancher, 1886)

Fig. 26

Lathrapanteles heleios

Williams, 1985

Fig. 27

Ontario, Constance Bay, 45.486218 -76.073461, 21.vii.1933, G. S. Walley, Voucher Code: cnc482347; Corkery, 45.284686 -76.102742, 3.vii.1948, F.I.S., Voucher Code: CNC482348.

Microgaster gelechiae

Riley, 1869

Fig. 28

Figure 28. — *Microgaster* *gelechiae*. A Habitus, lateral B Head, frontal C Wings D Antenna E Mesosoma and metasoma, dorsal.

Distribution.

NEA.

Material examined.

Ontario, Jockvale, 45.266494 -75.74418, 8.v.1943, J. McDunmough, Voucher Code: CNCHYM01616; 45.266524 -75.744180, 8.v.1943, McDunnough, J., Voucher Code: CNC281031; Ottawa, 45.382500 -75.713700, 1.v.1975, Voucher Code: CNCHYM01615.

Microgaster leechi

Walley, 1935

Fig. 29

Fig. 31

Figure 31. — *Pholetesor* *bedelliae*. A Habitus, lateral B Head, frontal C Wings D Head and mesosoma, dorsal E Metasoma, dorsal F Mesosoma and metasoma, lateral.

Distribution.

NEA, NEO.

Material examined.

Whitfield, 2006

Fig. 33

Figure 33. — *Pholetesor* *rhygoplitoides*. A Habitus, lateral B Head, frontal C Wings D Metasoma, dorsal E Head and mesosoma, dorsal.

Distribution.

NEA.

Material examined.

Ontario, Mer Bleue, 45.393578 -75.512127, 19.vii.1963, Chillcott, J.G, Voucher Code: CNC309878; 45.393593 -75.512138, 18.vii.1963, J. G. Chillcott, Voucher Code: CNCHYM03189.

Pholetesor salicifoliellae

Mason, 1959

Fig. 34

Figure 34. — *Pholetesor* *salicifoliellae*. A Habitus, lateral B Head, frontal C Wings D Metasoma, dorsal E Head and mesosoma, dorsal.

Distribution.

NEA.

Material examined.

Protapanteles paleacritae

(Riley, 1881)

Fig. 35

Figure 35. — *Protapanteles* *paleacritae*. A Habitus, lateral B Head, frontal C Wings D Glued specimen and cocoon E Metasoma, dorsal F Head and mesosoma, dorsal.

Distribution.

NEA.

Material examined.

Ontario, Carp, 45.349117 -76.041225, 23.vii.1942, Voucher Code: CNC483585; Greely, 45.259544 -75.568696, 25.vi.1946, Voucher Code: CNC483586.

Protapanteles phlyctaeniae

(Muesebeck, 1929)

Fig. 36

Figure 36. — *Protapanteles* *phlyctaeniae*. A Habitus, lateral B Head, frontal C Wings D Head and mesosoma, dorsal E Mesosoma (partially) and metasoma, dorsal F Glued specimen and cocoon.

Distribution.

Distribution.

NEA.

Notes.

This species corresponds in BOLD to BIN BOLD:AAH2147, with all specimens collected in southern Ontario.

Material examined.

Ontario, Ottawa, city garden, 45.356100 -75.706900, 10.viii-1.ix.2007, H. Goulet, Voucher Code: WMIC0214; 30.vii-10.viii.2007, H. Goulet, Voucher Code: CAM1011.

Sathon cinctiformis

(Viereck, 1911)

Fig. 40

Figure 40. — *Sathon* *cinctiformis*. A Habitus, lateral B Head, frontal C Wings D Metasoma, dorsal E Head and mesosoma, dorsal.

Distribution.

NEA.

Material examined.

Ontario, Ottawa, Dow’s swamp , 45.419164 -75.709650, 9.vii.1946, G.S. Walley, Voucher Code: CNC309918; Ottawa, Dow’s swamp, 45.394302 -75.704544, 9.vii.1946, G. S. Walley, Voucher Code: CNCHYM03476, CNCHYM03477; Ottawa, 45.406631 -75.701407, 20.vii.1947, W.R.M. Mason, Voucher Code: CNC483601; 20.viii.1947, W.R.M. Mason, Voucher Code: CNC483612; 21.vi.1947, W.R.M. Mason, Voucher Code: CNC483590, CNC483591, CNC483592, CNC483593, CNC483594, CNC483595; 28.vi.1940, O. Peck, Voucher Code: CNC483599; 5.vii.1947, W.R.M. Mason, Voucher Code: CNC483596, CNC483597, CNC483598; 45.406633 -75.701408, 19.vii.1939, O. Peck, Voucher Code: CNC483600; Quebec, Hull, 45.428550 -75.714554, 11.vi.1957, C.D. Miller, Voucher Code: CNC483602, CNC483603, CNC483604, CNC483605, CNC483606, CNC483607, CNC483608, CNC483609; 18.vi.1957, J.G. Chillcott, Voucher Code: CNC483610; 2.viii.1947, W.R.M. Mason, Voucher Code: CNC483611.

Sathon neomexicanus

(Muesebeck, 1921)

Distribution.

NEA.

Material examined.

Ontario, Bells Corners, 45.322133 -75.833303, 7.vii.1943, G.S. Walley, Voucher Code: CNC309924.

Acknowledgements

Many collectors over the past 120 years have contributed Ottawa specimens of Microgastrinae to the CNC, without their efforts this paper would not be possible. We especially thank Henri Goulet and Lubomir Masner (CNC) for collecting most of the recent material (2007-2010). The reviews of John Huber and Donald Lafontaine (CNC) greatly improved the final version of this manuscript. Donald Lafontaine kindly provided the senior author with a list of all Lepidoptera collected in Ottawa as well as comments on its diversity in the region. Ana Fernandez Galliano helped checking the accuracy of labels for some older records. The Biodiversity Institute of Ontario, University of Guelph, has been instrumental in the DNA barcoding of thousands of microgastrine specimens, which has been of great help in taxonomic studies of the Ottawa fauna and many other areas. Two reviewers (Juliano Nunez and James Whitfield) and the editor (Kees van Achterberg) are gratefully acknowledged for helping to improve the final version of the manuscript. This research was supported by project AAFC-STB-1558 'Arthropod systematics research in support of Canadian Agriculture'.

Citation

Fernandez-Triana J, Boudreault C, Buffam J, Mclean R (2016) A biodiversity hotspot for Microgastrinae (Hymenoptera, Braconidae) in North America: annotated species checklist for Ottawa, Canada. ZooKeys 633: 1–93. doi: 10.3897/zookeys.633.10480

References

Belcher J, Keddy PA, Catling PFC. (1992) Alvar vegetation in Canada: a multivariate description at two scales. Canadian Journal of Botany 70: 1279–1291. doi: 10.1139/b92-161 [Google Scholar]
Fernández-Triana J. (2010) Eight new species and an annotated checklist of Microgastrinae (Hymenoptera: Braconidae) from Canada and Alaska. Zookeys 63: 1–53. doi: 10.3897/zookeys.63.565 [DOI] [PMC free article] [PubMed] [Google Scholar]
Fernandez-Triana J. (2014) Towards the conservation of parasitoid wasp species in Canada: Preliminary assessment of Microgastrinae (Hymenoptera: Braconidae). Biodiversity Data Journal 2: e1067. doi: 10.3897/BDJ.2.e1067 [DOI] [PMC free article] [PubMed] [Google Scholar]
Fernandez-Triana JL. (2015) A revision of the genus Protomicroplitis Ashmead (Hymenoptera, Braconidae, Microgastrinae), with the description of a new species. Zootaxa 4039(4): 522–542. doi: 10.11646/zootaxa.4039.4.3 [DOI] [PubMed] [Google Scholar]
Fernández-Triana J, Goulet H, Bostanian N, Boudreault C. (2009) Diversity of Microgastrinae (Hymenoptera: Braconidae) in apple orchards of southern Quebec, Canada. Biocontrol Science and Technology 19: 237–248. doi: 10.1080/09583150802684406 [Google Scholar]
Fernandez-Triana J, Smith MA, Boudreault C, Goulet H, Hebert PDN, Smith AC, et al. (2011) A Poorly Known High-Latitude Parasitoid Wasp Community: Unexpected Diversity and Dramatic Changes through Time. PLoS ONE 6(8): e23719. doi: 10.1371/journal.pone.0023719 [DOI] [PMC free article] [PubMed] [Google Scholar]
Fernandez-Triana J, Cardinal S, Whitfield J, Smith M, Janzen D. (2013) A review of the New World species of the parasitoid wasp Iconella (Hymenoptera, Braconidae, Microgastrinae). ZooKeys 321: 65–87. doi: 10.3897/zookeys.321.5160 [DOI] [PMC free article] [PubMed] [Google Scholar]
Fernandez-Triana J, Shaw M, Cardinal S, Mason P. (2014a) Contributions to the study of the Holarctic fauna of Microgastrinae (Hymenoptera, Braconidae). I. Introduction and first results of transatlantic comparisons. Journal of Hymenoptera Research 37: 61–76. doi: 10.3897/jhr.37.7186 [Google Scholar]
Fernandez-Triana J, Penev L, Ratnasingham S, Smith M, Sones J, Telfer A, deWaard J, Hebert P. (2014b) Streamlining the use of BOLD specimen data to record species distributions: a case study with ten Nearctic species of Microgastrinae (Hymenoptera: Braconidae). Biodiversity Data Journal 2: e4153. doi: 10.3897/BDJ.2.e4153 [DOI] [PMC free article] [PubMed] [Google Scholar]
Fernandez-Triana J, Janzen D, Hallwachs W, Whitfield J, Smith M, Kula R. (2014c) Revision of the genus Pseudapanteles (Hymenoptera, Braconidae, Microgastrinae), with emphasis on the species in Area de Conservación Guanacaste, northwestern Costa Rica. ZooKeys 446: 1–82. doi: 10.3897/zookeys.446.8195 [DOI] [PMC free article] [PubMed] [Google Scholar]
Fernández-Triana J, Whitfield JB, Rodriguez JJ, Smith MA, Janzen DH, Hallwachs W, Hajibabaei M, Burns JM, Solis MA, Brown J, Cardinal S, Goulet H, Hebert PDN. (2014d) Review of Apanteles (Hymenoptera: Braconidae, Microgastrinae) from Area de Conservación Guanacaste, northwestern Costa Rica, with keys to all described species from Mesoamerica. ZooKeys 383: 1–565. doi: 10.3897/zookeys.383.6418 [DOI] [PMC free article] [PubMed] [Google Scholar]
Janzen DH, Hallwachs W. (2016) DNA barcoding the Lepidoptera inventory of a large complex tropical conserved wildland, Area de Conservacion Guanacaste, northwestern Costa Rica. Genome 59: 641–660. doi: 10.1139/gen-2016-0005 [DOI] [PubMed] [Google Scholar]
Lafontaine JD. (1997) Butterflies and Moths (Lepidoptera). In: Smith IM. (Ed.) Assessment of Species Diversity in the Mixedwood Plains Ecozone. Ecological Monitoring and Assessment Network; http://www.naturewatch.ca/mixedwood/lep/intro.htm#toc [accessed 1.VIII.2010] [Google Scholar]
Lewis CN, Whitfield JB. (1999) Braconid wasp (Hymenoptera: Braconidae) diversity in forest plots under different silvicultural methods. Environmental Entomology 28: 986–997. doi: 10.1093/ee/28.6.986 [Google Scholar]
Mason WRM. (1981) The polyphyletic nature of Apanteles Foerster (Hymenoptera: Braconidae): A phylogeny and reclassification of Microgastrinae. Memoirs of the Entomological Society of Canada, Ottawa, Canada, 147 pp. [Google Scholar]
Papp J. (1976) A survey of the European species of Apanteles Först. (Hymenoptera, Braconidae: Microgasterinae), I. The species groups. Annales Historico-Naturales Musei Nationalis Hungarici 68: 251–274. [Google Scholar]
Ratnasingham S, Hebert PDN. (2007) BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7: 355–364. doi: 10.1111/j.1471-8286.2007.01678.x [DOI] [PMC free article] [PubMed] [Google Scholar]
Rodriguez JJ, Fernández-Triana J, Smith MA, Janzen DH, Hallwachs W, Erwin TL, Whitfield JB. (2013) Extrapolations from field studies and known faunas converge on dramatically increased estimates of global microgastrine parasitoid wasp species richness (Hymenoptera: Braconidae). Insect Conservation and Diversity 6: 530–536. doi: 10.1111/icad.12003 [Google Scholar]
Shaw SR. (2002) Studies of parasitic wasps (Braconidae) in Grand Teton National Park. University of Wyoming National Park Service Research Center Annual Report 26(1): 47–59. [Google Scholar]
Shaw MR, Stefanescu C, Van Nouhuys S. (2009) Parasitoids of European butterflies. In: Settele J, Shreeve T, Konvicka M, Van Dyck H. (Eds) Ecology of Butterflies in Europe. Cambridge University Press, 130–156. [Google Scholar]
Smith V, Rycroft S, Brake I, Scott B, Baker E, Livermore L, Blagoderov V, Roberts D. (2011) Scratchpads 2.0: a Virtual Research Environment supporting scholarly collaboration, communication and data publication in biodiversity science. ZooKeys 150: 53–70. doi: 10.3897/zookeys.150.2193 [DOI] [PMC free article] [PubMed] [Google Scholar]
Whitfield JB. (1995) Checklist of the Microgastrinae (Hymenoptera: Braconidae) in America north of Mexico. Journal of the Kansas Entomological Society 68: 245–262. [Google Scholar]
Whitfield JB. (1997) Subfamily Microgastrinae. In: Wharton RA, Marsh PM, Sharkey MJ. (Eds) Manual of the New World genera of the family Braconidae (Hymenoptera). Special Publication No. 1, International Society of Hymenopterists, Washington, D.C., 333–364. [Google Scholar]
Whitfield JB, Lewis CN. (2001) Analytical survey of the braconid wasp fauna (Hymenoptera: Braconidae) on six midwestern US tallgrass prairies. Annals of the Entomological society of America 94(2): 230–238. doi: 10.1603/0013-8746(2001)094[0230:ASOTBW]2.0.CO;2 [Google Scholar]
Whitfield JB. (2006) Revision of the Nearctic species of the genus Pholetesor Mason (Hymenoptera: Braconidae). Zootaxa 1144: 1–94. [Google Scholar]
Yu DSK, van Achterberg C, Horstmann K. (2012) Taxapad 2012, Ichneumonoidea 2011. Database on flash-drive. Ottawa, Ontario, Canada: http://www.taxapad.com [Google Scholar]
Yu DSK, van Achterberg C, Horstmann K. (2016) Taxapad 2016, Ichneumonoidea 2015. Database on flash-drive. Nepean, Ontario, Canada: http://www.taxapad.com [Google Scholar]

[B1] Belcher J, Keddy PA, Catling PFC. (1992) Alvar vegetation in Canada: a multivariate description at two scales. Canadian Journal of Botany 70: 1279–1291. doi: 10.1139/b92-161 [Google Scholar]

[B2] Fernández-Triana J. (2010) Eight new species and an annotated checklist of Microgastrinae (Hymenoptera: Braconidae) from Canada and Alaska. Zookeys 63: 1–53. doi: 10.3897/zookeys.63.565 [DOI] [PMC free article] [PubMed] [Google Scholar]

[B3] Fernandez-Triana J. (2014) Towards the conservation of parasitoid wasp species in Canada: Preliminary assessment of Microgastrinae (Hymenoptera: Braconidae). Biodiversity Data Journal 2: e1067. doi: 10.3897/BDJ.2.e1067 [DOI] [PMC free article] [PubMed] [Google Scholar]

[B4] Fernandez-Triana JL. (2015) A revision of the genus Protomicroplitis Ashmead (Hymenoptera, Braconidae, Microgastrinae), with the description of a new species. Zootaxa 4039(4): 522–542. doi: 10.11646/zootaxa.4039.4.3 [DOI] [PubMed] [Google Scholar]

[B5] Fernández-Triana J, Goulet H, Bostanian N, Boudreault C. (2009) Diversity of Microgastrinae (Hymenoptera: Braconidae) in apple orchards of southern Quebec, Canada. Biocontrol Science and Technology 19: 237–248. doi: 10.1080/09583150802684406 [Google Scholar]

[B6] Fernandez-Triana J, Smith MA, Boudreault C, Goulet H, Hebert PDN, Smith AC, et al. (2011) A Poorly Known High-Latitude Parasitoid Wasp Community: Unexpected Diversity and Dramatic Changes through Time. PLoS ONE 6(8): e23719. doi: 10.1371/journal.pone.0023719 [DOI] [PMC free article] [PubMed] [Google Scholar]

[B7] Fernandez-Triana J, Cardinal S, Whitfield J, Smith M, Janzen D. (2013) A review of the New World species of the parasitoid wasp Iconella (Hymenoptera, Braconidae, Microgastrinae). ZooKeys 321: 65–87. doi: 10.3897/zookeys.321.5160 [DOI] [PMC free article] [PubMed] [Google Scholar]

[B8] Fernandez-Triana J, Shaw M, Cardinal S, Mason P. (2014a) Contributions to the study of the Holarctic fauna of Microgastrinae (Hymenoptera, Braconidae). I. Introduction and first results of transatlantic comparisons. Journal of Hymenoptera Research 37: 61–76. doi: 10.3897/jhr.37.7186 [Google Scholar]

[B9] Fernandez-Triana J, Penev L, Ratnasingham S, Smith M, Sones J, Telfer A, deWaard J, Hebert P. (2014b) Streamlining the use of BOLD specimen data to record species distributions: a case study with ten Nearctic species of Microgastrinae (Hymenoptera: Braconidae). Biodiversity Data Journal 2: e4153. doi: 10.3897/BDJ.2.e4153 [DOI] [PMC free article] [PubMed] [Google Scholar]

[B10] Fernandez-Triana J, Janzen D, Hallwachs W, Whitfield J, Smith M, Kula R. (2014c) Revision of the genus Pseudapanteles (Hymenoptera, Braconidae, Microgastrinae), with emphasis on the species in Area de Conservación Guanacaste, northwestern Costa Rica. ZooKeys 446: 1–82. doi: 10.3897/zookeys.446.8195 [DOI] [PMC free article] [PubMed] [Google Scholar]

[B11] Fernández-Triana J, Whitfield JB, Rodriguez JJ, Smith MA, Janzen DH, Hallwachs W, Hajibabaei M, Burns JM, Solis MA, Brown J, Cardinal S, Goulet H, Hebert PDN. (2014d) Review of Apanteles (Hymenoptera: Braconidae, Microgastrinae) from Area de Conservación Guanacaste, northwestern Costa Rica, with keys to all described species from Mesoamerica. ZooKeys 383: 1–565. doi: 10.3897/zookeys.383.6418 [DOI] [PMC free article] [PubMed] [Google Scholar]

[B12] Janzen DH, Hallwachs W. (2016) DNA barcoding the Lepidoptera inventory of a large complex tropical conserved wildland, Area de Conservacion Guanacaste, northwestern Costa Rica. Genome 59: 641–660. doi: 10.1139/gen-2016-0005 [DOI] [PubMed] [Google Scholar]

[B13] Lafontaine JD. (1997) Butterflies and Moths (Lepidoptera). In: Smith IM. (Ed.) Assessment of Species Diversity in the Mixedwood Plains Ecozone. Ecological Monitoring and Assessment Network; http://www.naturewatch.ca/mixedwood/lep/intro.htm#toc [accessed 1.VIII.2010] [Google Scholar]

[B14] Lewis CN, Whitfield JB. (1999) Braconid wasp (Hymenoptera: Braconidae) diversity in forest plots under different silvicultural methods. Environmental Entomology 28: 986–997. doi: 10.1093/ee/28.6.986 [Google Scholar]

[B15] Mason WRM. (1981) The polyphyletic nature of Apanteles Foerster (Hymenoptera: Braconidae): A phylogeny and reclassification of Microgastrinae. Memoirs of the Entomological Society of Canada, Ottawa, Canada, 147 pp. [Google Scholar]

[B16] Papp J. (1976) A survey of the European species of Apanteles Först. (Hymenoptera, Braconidae: Microgasterinae), I. The species groups. Annales Historico-Naturales Musei Nationalis Hungarici 68: 251–274. [Google Scholar]

[B17] Ratnasingham S, Hebert PDN. (2007) BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7: 355–364. doi: 10.1111/j.1471-8286.2007.01678.x [DOI] [PMC free article] [PubMed] [Google Scholar]

[B18] Rodriguez JJ, Fernández-Triana J, Smith MA, Janzen DH, Hallwachs W, Erwin TL, Whitfield JB. (2013) Extrapolations from field studies and known faunas converge on dramatically increased estimates of global microgastrine parasitoid wasp species richness (Hymenoptera: Braconidae). Insect Conservation and Diversity 6: 530–536. doi: 10.1111/icad.12003 [Google Scholar]

[B19] Shaw SR. (2002) Studies of parasitic wasps (Braconidae) in Grand Teton National Park. University of Wyoming National Park Service Research Center Annual Report 26(1): 47–59. [Google Scholar]

[B20] Shaw MR, Stefanescu C, Van Nouhuys S. (2009) Parasitoids of European butterflies. In: Settele J, Shreeve T, Konvicka M, Van Dyck H. (Eds) Ecology of Butterflies in Europe. Cambridge University Press, 130–156. [Google Scholar]

[B21] Smith V, Rycroft S, Brake I, Scott B, Baker E, Livermore L, Blagoderov V, Roberts D. (2011) Scratchpads 2.0: a Virtual Research Environment supporting scholarly collaboration, communication and data publication in biodiversity science. ZooKeys 150: 53–70. doi: 10.3897/zookeys.150.2193 [DOI] [PMC free article] [PubMed] [Google Scholar]

[B22] Whitfield JB. (1995) Checklist of the Microgastrinae (Hymenoptera: Braconidae) in America north of Mexico. Journal of the Kansas Entomological Society 68: 245–262. [Google Scholar]

[B23] Whitfield JB. (1997) Subfamily Microgastrinae. In: Wharton RA, Marsh PM, Sharkey MJ. (Eds) Manual of the New World genera of the family Braconidae (Hymenoptera). Special Publication No. 1, International Society of Hymenopterists, Washington, D.C., 333–364. [Google Scholar]

[B24] Whitfield JB, Lewis CN. (2001) Analytical survey of the braconid wasp fauna (Hymenoptera: Braconidae) on six midwestern US tallgrass prairies. Annals of the Entomological society of America 94(2): 230–238. doi: 10.1603/0013-8746(2001)094[0230:ASOTBW]2.0.CO;2 [Google Scholar]

[B25] Whitfield JB. (2006) Revision of the Nearctic species of the genus Pholetesor Mason (Hymenoptera: Braconidae). Zootaxa 1144: 1–94. [Google Scholar]

[B26] Yu DSK, van Achterberg C, Horstmann K. (2012) Taxapad 2012, Ichneumonoidea 2011. Database on flash-drive. Ottawa, Ontario, Canada: http://www.taxapad.com [Google Scholar]

[B27] Yu DSK, van Achterberg C, Horstmann K. (2016) Taxapad 2016, Ichneumonoidea 2015. Database on flash-drive. Nepean, Ontario, Canada: http://www.taxapad.com [Google Scholar]

PERMALINK

A biodiversity hotspot for Microgastrinae (Hymenoptera, Braconidae) in North America: annotated species checklist for Ottawa, Canada

Jose Fernandez-Triana

Caroline Boudreault

Joel Buffam

Ronald Mclean

Abstract Abstract

Introduction

Methods

Figure 1.

Results

Table 1.

Table 2.

Figure 2.

Figure 3.

Figure 4.

Annotated checklist of Microgastrinae from Ottawa, Canada

Alphomelon winniewertzae

Figure 5.

Distribution.

Notes.

Material examined.

Apanteles baldufi

Distribution.

Material examined.

Apanteles canarsiae

Distribution.

Material examined.

Apanteles carpatus

Distribution.

Material examined.

Apanteles conanchetorum

Distribution.

Material examined.

Apanteles crassicornis

Figure 6.

Distribution.

Material examined.

Apanteles depressariae

Distribution.

Material examined.

Apanteles epinotiae

Distribution.

Material examined.

Apanteles forbesi

Distribution.

Material examined.

Apanteles fumiferanae

Distribution.

Material examined.

Apanteles jenniferae

Figure 7.

Distribution.

Material examined.

Apanteles laricellae

Figure 8.

Distribution.

Material examined.

Apanteles morrisi

Figure 9.

Distribution.

Material examined.

Apanteles nephoptericis

Distribution.

Material examined.

Apanteles petrovae

Figure 10.

Distribution.

Material examined.

Apanteles polychrosidis

Figure 11.

Distribution.

Material examined.

Apanteles jft01

Distribution.

Notes.

Material examined.

Apanteles jft04

Distribution.

Material examined.