The family Ismaridae Thomson ( Hymenoptera , Diaprioidea ) : first record for the Afrotropical region with description of fourteen new species

The family Ismaridae Thomson, 1858 is reported from the Afrotropical region for the first time. A total of 15 species are recognised, 14 of which are described as new: Ismarus africanus sp. n. from Cameroon, Kenya, Malawi, South Africa; I. apertus sp. n. from Kenya; I. bicolor sp. n. from Cameroon, Kenya; I.  goodrichi sp. n. from Kenya; I. kakamegensis sp. n. from Kenya; I. kenyensis sp. n. from Kenya; I.  laevigatus sp. n. from South Africa; I. madagascariensis sp. n. from Madagascar; I. minutus sp. n. from Kenya, Malawi, Zimbabwe; I. nigrofasciatus sp. n. from Malawi, Uganda; I. notaulicus sp. n. from Kenya; I. rawlinsi sp. n. from Kenya, Malawi; I. steineri sp. n. from Madagascar; I. watshami sp. n. from Botswana, Malawi, South Africa, Zimbabwe. Ismarus halidayi Förster is reported for continental Africa from South Africa (new record). We provide an identification key to all species in Afrotropical region.


Introduction
The family Ismaridae is currently classified as a monotypic family in the Diaprioidea (Sharkey et al. 2012).Prior to this study, the family included 43 described species, distributed worldwide except for the Afrotropical region (Masner 1976;Johnson 1992;Liu et al. 2011;Kolyada and Chemyreva 2016;Comério et al. 2016;Hymenoptera Online 2016;Kim et al. 2018).
Information on the habitats and biology of the species of Ismarus is limited; however, they are known to prefer wooded areas at higher elevations in warmer climatic zones and at low elevations in cooler climatic zones and they are hyperparasitoids of plant hoppers (Cicadellidae) via Dryinidae (Hymenoptera, Chrysidoidea) (Chambers 1955(Chambers , 1981;;Nixon 1957;Wall 1967;Kozlov 1971;Masner 1976;Jervis 1979;Tussac and Tussac 1991;Olmi 2000;Kim et al. 2018).
In 2015-2016, the authors examined some unidentified African Ismaridae provided by Lubomír Masner (Canadian National Collection, Ottawa, Canada), David G. Notton (Natural History Museum, London, United Kingdom) and Robert Copeland (International Centre of Insect Physiology and Ecology, Nairobi, Kenya).This study resulted in the discovery of 15 species of Ismarus from the Afrotropical region, the first Afrotropical representatives of the family (Table 1).Hosts are unknown for all the new species.

Material and methods
The terminology used in the present study follows that of Masner (1976) and Masner and García (2002).The images were captured with a Leica DFC 495 camera through a Leica M205A Stereozoom stereomicroscope (Leica, Microsystems, Solms, Germany) and were produced with LAS software (version 4.1.0.,Leica Microsystems,Switzerland). Final plates were prepared in Adobe Photoshop CS6 (Adobe Systems Incorporated, San Jose, United States of America).
Abbreviations.Morphology.LOL: distance between the inner edges of lateral ocellus and median ocellus; OOL: distance from the outer edge of lateral ocellus to the compound eye; POL: distance between the inner edges of the two lateral ocelli.Collecting methods.MT: Malaise trap; YPT: yellow pan trap.
Diagnosis.Ismarus can be easily separated from other diapriids by the combination of the following characters: low insertion of antennae; transverse head; reduced notauli.For a detailed generic description, see Masner (1976).
Mesosoma.Pronotum in dorsal view smooth with whitish long setae along posterior margin; pronotal shoulders angled; lateral pronotum strongly punctate with whitish long setae upper margin except smooth and concave medially; mesoscutum smooth and convex, with very long setae along posterior margin; notauli present anteriorly, pits merged with the curved notauli (Fig. 1C); humeral sulcus deep and long, longer than length of tegula (3:2); scutellum coarsely rugose, distinctly raised and convex, straight lateral rims, posterior rim truncate with strongly prominent posterolateral corners (Fig. 1C); anterior scutellar pit large and deep, as long as remaining scutellar disc, crenulate at bottom, median keel distinct (Fig. 1C); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron rugose and covered with dense whitish long setae.
Variation.Body length 1.76-3.46mm, in both sexes.Body colour black, dark brown to brown; colour of female antenna yellowish-brown except segments 8-15 to 10-15 brown, male antenna brown except A1-A2 or A1-A3 yellowish; head weakly or strongly rugulose in both sexes; mesoscutum smooth to weakly rugulose in both sexes; blade-like carina on A4, extending 0.6-1.0×length of A4; posterior rim of scutellum truncated to slightly emarginated in both sexes; median furrow extending to 0.15−0.60×length of second tergite in both sexes.

Ismarus apertus
Mesosoma.Pronotum in dorsal view punctate with whitish long setae along posterior margin; pronotal shoulders angled; lateral pronotum predominantly punctate except smooth and slightly concave in the middle; mesoscutum smooth and convex with pairs of long setae in front of scutellar pit; notauli present anteriorly, pits merged with the curved notauli (Fig. 2C); humeral sulcus deep and long, much longer than length of tegula (11:5); scutellum smooth and distinctly convex, lateral rims straight, posterior rim slightly emarginate with strongly prominent posterolateral corners (Fig. 2C); anterior scutellar pit small and deep, much shorter than remaining scutellar disc, crenulate at bottom, median keel weakly present (Fig. 2C); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron punctate-rugose and covered with dense whitish long setae.
Colour.Body black; antennae yellowish-brown except A9−A15 brown, tegulae dark brown and legs uniformly yellow; wings hyaline, covered with brown setae.
Mesosoma.Pronotum in dorsal view punctate-rugose with whitish long setae; pronotal shoulders angled; upper part of lateral pronotum smooth, bare and broadly convex medially; lower part of lateral pronotum with setigerous punctures; mesoscutum smooth and convex; notauli present with 5 small pits on anterior margin (Fig. 3D); humeral sulcus deep and long, as long as length of tegula; scutellum smooth and slightly convex, posterior rim rounded (Fig. 3D); anterior scutellar pit small and deep, much shorter than remaining scutellar disc, distinctly crenulate at bottom, median keel absent (Fig. 3D); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron reticulate and covered with dense whitish long setae.
Wings.Radial cell completely closed, 1.6× as long as wide and 0.55× as long as marginal vein (Fig. 3A).
Metasoma.Petiole subquadrate, with strong costae dorsally; base of second tergite with several short costae basally and very short median furrow, extending 0.15× length of second tergite; suture between T2 and T3 obsolete but the following sutures between tergites distinctly impressed (Fig. 3E).
Colour.Head yellow to yellowish-brown except frons, around the ocelli and median part of vertex brown, mandibles whitish-yellow with reddish tips; mesosoma black except lower half of lateral pronotum yellow; metasoma brown except petiole black; tegulae yellowish-brown; antennae brown except A1-A3 yellow; legs yellow except hind tibiae and tarsi brown; wings hyaline, covered with brown setae.
Mesosoma.Pronotum in dorsal view rugose with whitish long setae; lateral pronotum predominantly rugose punctate except smooth and slightly concave in the middle; mesoscutum smooth and convex with pairs of long setae in front of scutellar pit; notauli present anteriorly, pits merged with the curved notauli (Fig. 4C); humeral sulcus deep and long, much longer than length of tegula (16:11); anterior scutellar pit small and deep, much shorter than remaining scutellar disc, slightly crenulate at bottom, median keel weakly present; scutellum smooth with punctures and slightly convex, posterior rim truncate (Fig. 4C); mesopleuron smooth with deep crenulate line along posterior margin (Fig. 4C); metapleuron rugose and covered with dense whitish long setae.
Wings.Radial cell completely closed, 1.75× as long as wide and 0.95× as long as marginal vein (Fig. 4A).

Distribution. Kenya.
Etymology.This species is named after Gerry Goodrich, a close friend of RSC and an old Kenya hand.
Remarks.This species, widely distributed in the Nearctic, Palaearctic and Oriental regions, is here reported for the first time from the Afrotropical region (South Africa).Masner, 1976 from the Nearctic region.It differs mainly in the antenna colour, A1/A3/A4 ratio and metasomal sutures: in I. clarkae antenna yellow with whitish ventral side of scape, A1 much longer than A3 and A4, metasoma after T2 mostly obsolete or incomplete; in I. kakamegensis sp.n. antenna brown with yellow scape and pedicel, A1 almost equal length to A3 and A4, metasoma after T2 with 4 distinct sutures.
Wings.Radial cell completely closed, 1.6× as long as wide and 0.55× as long as marginal vein (Fig. 5C).
Colour.Body yellow except face whitish-yellow, mesoscutum and scutellum blackish, dorsal part of petiole and basal part of T1 darkened; antennae brown except scape and pedicel yellow, tegulae and legs uniformly yellow; wings hyaline, covered with brown setae.
Ismarus kenyensis sp.n. http://zoobank.org/8E3E41C6-254E-4B0F-8917-BB58AD9A9E30Figure 6A−E Diagnosis.Ismarus kenyensis sp.n. is similar to I. minutus sp.n.It differs mainly in the antennal segments A1/A3/A4 ratio, radial cell/marginal vein ratio and length of median longitudinal furrow on T2: in I. minutus sp.n.A1 much longer than A3 and A4, radial cell shorter than half length of marginal vein, T2 with median furrow extending to 0.10× of segment; in I. kenyensis sp.n., A1 slightly longer than A3 and equal length to A4, radial cell longer than half length of marginal vein, T2 with median furrow extending to ⅓ of segment.
Mesosoma.Pronotum in dorsal view rugose with whitish long setae; lateral pronotum predominantly rugose-punctate except smooth and concave in the middle; mesoscutum smooth and convex; notauli present with 4 small pits on anterior margin (Fig. 6E); humeral sulcus deep and long, much longer than length of tegula (12:7); anterior scutellar pit small and deep, much shorter than remaining scutellar disc, distinctly crenulate at bottom, median keel absent; scutellum smooth and slightly convex, posterior rim rounded (Fig. 6E); mesopleuron smooth with deep crenulate line along posterior margin (Fig. 6E); metapleuron rugose and covered with dense whitish long setae.
Wings.Radial cell completely closed, 1.8× as long as wide and 0.6× as long as marginal vein (Fig. 6A).
Colour.Head and mesosoma dark brown except antennae yellow with A12-A15 brown, tegulae brown, legs yellow with hind coxae and femora brown; metasoma brown except petiole dark brown; wings hyaline, covered with brown setae.

Ismarus laevigatus
Mesosoma.Pronotum in dorsal view punctate-rugose with whitish long setae; pronotal shoulders angled; upper part of lateral pronotum smooth and concave in the middle, lower part of lateral pronotum punctate-rugose; mesoscutum smooth and convex with pairs of long setae in front of scutellar pit; notauli present anteriorly as large pits (Fig. 7D); humeral sulcus deep and short, as long as length of tegula; scutellum smooth and slightly convex, posterior rim rounded (Fig. 7D); anterior scutellar pit large and deep, shorter than remaining scutellar disc, slightly crenulate at bottom, median keel present (Fig. 7D); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron punctate to rugose and covered with dense whitish long setae.
Wings.Radial cell completely closed, 2.1× as long as wide and as long as marginal vein (Fig. 7A).
Metasoma.Petiole subquadrate, rugose dorsally; tergites smooth, with scattered setigerous punctures; base of second tergite with several short costae basally and very long median furrow, 0.90× length of second; sutures between tergites complete and deeply impressed.
Colour.Body black; antennae, tegulae and legs uniformly yellow except inner part of tibiae brown; wings hyaline, covered with brown setae.
Variation.Body length 1.88-2.63mm in both sexes.Median furrow very long extending 0.8−0.9×length of second tergite in both sexes.
Distribution.South Africa.
Mesosoma.Pronotum in dorsal view smooth with deep punctures and whitish long setae along the posterior margin; pronotal shoulders angled; lateral pronotum rugose except smooth and concave in the middle; mesoscutum smooth and convex, with long setae along posterior margin; notauli present anteriorly as large pits (Fig. 8C); humeral sulcus deep and long, longer than length of tegula (15:9); scutellum coarsely punctate and distinctly convex, posterior rim truncate with whitish long setae and prominent posterolateral corners (Fig. 8C); anterior scutellar pit large and deep, as long as rest of scutellar disc, strongly punctate at bottom, median keel distinct (Fig. 8C); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron rugose and covered with dense whitish long setae.
Wings.Radial cell completely closed, 1.5× as long as wide and 0.6× as long as marginal vein (Fig. 8A).
Colour.Body black; antennae yellow except for A12−A15 segment brown; legs and tegulae yellowish-brown to brown; wings hyaline, covered with brown setae.

Ismarus minutus
Variation.Body length 1.83-2.03mm in both sexes.Male body blackish-brown to dark brown, antenna yellowish-brown basally gradually darkened towards apex to uniformly brown.
Wings.Radial cell completely closed, 1.75× as long as wide and 0.7× as long as marginal vein (Fig. 10A).
Colour.Body whitish-yellow to yellow except median longitudinal band of mesoscutum and scutellum blackish (Fig. 10C); antennae, tegulae and legs uniformly yellow; wings hyaline, covered with brown setae.
Etymology.The specific name is an adjective derived from the Latin words nigrum for black and fasciatus meaning with stripe or band.(Haliday, 1831).It differs mainly in the notauli and mesosoma colour pattern: in I. dorsiger notauli completely absent, dorsal part of pronotum yellow, mesopleuron completely yellow; in I. notaulicus sp.n. notauli present with 7 very small pits, dorsal part of pronotum black, mesopleuron brown except upper margin darkened.
Mesosoma.Pronotum in dorsal view punctate with whitish long setae; pronotal shoulders angled; lateral pronotum predominantly smooth and concave except upper and lower margins with whitish long setae; mesoscutum smooth and convex with pairs of long setae in front of scutellar pit; notauli present with 7 very small pits on anterior margin (Fig. 11C); humeral sulcus deep and short, as long as length of tegula; scutellum smooth and slightly convex, posterior rim rounded (Fig. 11C); anterior scutellar pit small and deep, much shorter than remaining scutellar disc, distinctly crenulate at bottom, median keel absent (Fig. 11C); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron rugose and covered with dense whitish long setae.
Wings.Radial cell completely closed, 2.0× as long as wide and 0.6× as long as marginal vein (Fig. 11A).
Metasoma.Petiole subquadrate, with strong costae dorsally; base of second tergite with several short costae basally and very short median furrow, extending 0.20× length of second tergite; suture between T2 and T3 obsolete but the following sutures between tergites distinctly impressed.

Ismarus rawlinsi
Mesosoma.Pronotum in dorsal view punctate with whitish long setae; pronotal shoulders angled; upper part of lateral pronotum smooth and concave in the middle, lower part of lateral pronotum punctate; mesoscutum smooth and convex with pairs of long setae in front of scutellar pit; notauli present with 6 very small pits on anterior margin (Fig. 12E); humeral sulcus deep and short, as long as length of tegula; scutellum smooth and slightly convex, posterior rim rounded (Fig. 12E); anterior scutellar pit small and deep, much shorter than remaining scutellar disc, distinctly crenulate at bottom, median keel absent (Fig. 12E); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron rugose and covered with dense whitish long setae.
Wings.Radial cell completely closed, 1.6× as long as wide and 0.6× as long as marginal vein (Fig. 12A).
Colour.Head dark brown except mandibles yellow with reddish tips and antennae yellowish-brown basally gradually darkened towards apex; mesosoma dark brown except tegulae yellow and lower margin of lateral pronotum brown; metasoma brown except petiole dark brown, apical margin of S2 to S6 yellow and T7 and T8 yellowish-brown; legs yellow except hind tibiae and tarsi brown; wings hyaline, covered with brown setae.
Mesosoma.Pronotum in dorsal view smooth to slightly rugose with whitish long setae; pronotal shoulders angled; upper part of lateral pronotum smooth, bare and broadly convex medially; lower part of lateral pronotum rugose with strong carina along anterior margin; mesoscutum smooth and convex with pairs of long setae in front of scutellar pit; notauli present anteriorly as large pits (Fig. 13E); humeral sulcus deep and long, much longer than length of tegula (19:12); scutellum smooth and slightly convex, straight lateral rims, posterior rim truncate with slightly prominent posterolateral corners (Fig. 13E); anterior scutellar pit large and deep, slightly shorter than remaining scutellar disc, slightly crenulate at bottom, median keel distinct (Fig. 13E); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron reticulate and covered with dense whitish long setae.
Wings.Radial cell completely closed, 2.1× as long as wide and 1.05× as long as marginal vein (Fig. 13A).
Colour.Body black; mandibles brown with reddish tips; antennae dark brown except scape and pedicel yellow; tegulae brown; legs yellow except hind coxae and femora yellowish-brown, tibiae and tarsi brown; wings hyaline, covered with brown setae.

Distribution. Madagascar.
Etymology.This species is named after Warren Steiner, one of the collectors of the holotype specimen.
Ismarus watshami sp.n. http://zoobank.org/116D5CEB-7010-4BFB-9CD5-CF95F758AB2CFigure 14A−E Diagnosis.In antenna colour pattern, Ismarus watshami sp.n. is similar to I. apicalis Kolyada & Chemyreva.The main difference between these two species is length of median longitudinal furrow on T2, radial cell/marginal vein ratio and posterior rim of scutellum shape: T2 with median furrow longer than half of length, radial cell slightly shorter than marginal vein and posterior rim of scutellum rounded in I. apicalis; T2 with median furrow shorter than half of length, radial cell distinctly shorter than marginal vein and posterior rim of scutellum slightly truncated to slightly emarginated in I. watshami.
Mesosoma.Pronotum in dorsal view rugose with whitish long setae; upper part of lateral pronotum distinctly rugose anteriorly, smooth and slightly concave posteriorly, lower part of lateral pronotum distinctly rugose; mesoscutum smooth and convex with pairs of long setae in front of scutellar pit; notauli present anteriorly as large pits (Fig. 14C); humeral sulcus deep and long, longer than length of tegula (17:13); scutellum smooth with sparse puncturation and slightly convex, posterior rim slightly truncated with slightly prominent posterolateral corners (Fig. 14C); anterior scutellar pit large and deep, as long as remaining scutellar disc, slightly crenulate at bottom, median keel distinct (Fig. 14C); mesopleuron smooth with deep crenulate line along posterior margin; metapleuron rugose and covered with dense whitish long setae.
Wings.Radial cell completely closed, 1.6× as long as wide and 0.6× as long as marginal vein (Fig. 14B).
Legs.Fore and mid legs slender; hind tibiae incrassate posteriorly, its maximum width as wide as hind femora.
Variation.Body length 1.74-2.64mm in both sexes.Posterior rim of scutellum slightly truncated to slightly emarginated; median furrow short, extending 0.20−0.35×length of second tergite in both sexes.
Etymology.This species is named after Anthony Watsham, who collected some of the type specimens.

Figure 1 .
Figure 1.Ismarus africanus sp.n. (A-C, E Female D, F Male).A, D Habitus in lateral view B Head in dorsal view C Mesosoma in dorsal view E Metasoma in dorsal view F Antenna (A3-A5).
sp. n. http://zoobank.org/9239A103-7264-45CD-A945-970EBC822808Figure 2A−G Diagnosis.The new species can be differentiated from all Ismarus species by the completely open radial cell.Ismarus apertus sp.n. is similar to I. africanus sp.n.It differs mainly in the radial cell and sculpture of head and scutellum: in I. apertus sp.n., radial cell completely open, radial vein almost absent, head and scutellum smooth; in I. africanus sp.n., radial cell open, as venation becomes weak apically, head and scutellum rugose or rugulose Type material (1♀1♂

Figure 2 .
Figure 2. Ismarus apertus sp.n. (A-C, G Female D-F Male).A, E Habitus in lateral view B Head in dorsal view C Mesosoma in dorsal view D Radial vein of fore wing F Antenna (A3-A5) G Metasoma in dorsal view.

Figure 3 .
Figure 3. Ismarus bicolor sp.n., male.A Habitus in lateral view B Antenna (A3-A5) C Head in dorsal view D Mesosoma in dorsal view E Metasoma in dorsal view.
sp. n. http://zoobank.org/9E8F8A80-A31F-4D15-8BF5-1BB28F9F759CFigure 4A−C Diagnosis.Ismarus goodrichi sp.n. is similar to I. halidayi Förster, 1850.It differs mainly in the posterior rim of scutellum and furrow on base of T2: in I. halidayi, posterior rim of scutellum rounded and base of T2 with long median furrow, at least to half the length of tergite; in I. goodrichi sp.n., posterior rim of scutellum truncated and base of T2 with short median furrow, extending 0.2× length of tergite.

Figure 4 .
Figure 4. Ismarus goodrichi sp.n., female.A Habitus in lateral view B Head in dorsal view C Mesosoma in dorsal view.

Figure 5 .
Figure 5. Ismarus kakamegensis sp.n., female.A Mesosoma in lateral view B Head in dorsal view C Habitus in lateral view D Mesosoma in dorsal view.

Figure 6 .
Figure 6.Ismarus kenyensis sp.n., female.A Fore wing B Head in dorsal view C Habitus in lateral view D Antenna E Mesosoma in dorsal view.

Figure 7 .
Figure 7. Ismarus laevigatus sp.n. (A-B, D Female C, E Male).A, C Habitus in lateral view B Head in dorsal view D Mesosoma in dorsal view E Antenna (A3-A5).

Figure 8 .
Figure 8. Ismarus madagascariensis sp.n., female.A Habitus in lateral view B Head in dorsal view C Mesosoma in dorsal view.

Figure 9 .
Figure 9. Ismarus minutus sp.n. (A-D Female E-F Male).A Antenna B, F Habitus in lateral view C Head in dorsal view D Mesosoma in dorsal view E Antenna (A3-A5).

Figure 10 .
Figure 10.Ismarus nigrofasciatus sp.n., female.A Habitus in lateral view B Head in dorsal view C Mesosoma in dorsal view.

Figure 11 .
Figure 11.Ismarus notaulicus sp.n., female.A Habitus in lateral view B Head in dorsal view C Mesosoma in dorsal view.

Figure 12 .
Figure 12.Ismarus rawlinsi sp.n. (A, D-E Female B-C Male).A, B Habitus in lateral view C Antenna (A2-A5) D Head in dorsal view E Mesosoma in dorsal view.

Figure 14 .
Figure 14.Ismarus watshami sp.n. (A-C Female D-E Male).A Head in dorsal view B, D Habitus in lateral view C Mesosoma in dorsal view E Antenna (A3-A5).