Anagyrus amnestos Rameshkumar, Noyes & Poorani

Rameshkumar, A., Noyes, J. S., Poorani, J. & Chong, J. H., 2013, Description of a new species of Anagyrus Howard (Hymenoptera: Chalcidoidea: Encyrtidae), a promising biological control agent of the invasive Madeira mealybug, Phenacoccus madeirensis Green (Hemiptera: Sternorrhyncha: Pseudococcidae), Zootaxa 3717 (1) : -

Anagyrus amnestos Rameshkumar, Noyes & Poorani , sp. nov.

( Figs 1–13 )

Female ( Figs 1, 2 ). Holotype. Length, 1.3 mm. Head mostly orange with clypeal margin, intertorular space, genal margin dark brown; head with silvery white setae except for a few setae in ocellar area dark brown to black; antenna with radicle dark brown; scape ( Fig. 7 ) dark brown with subapical curved white band in distal third and a white spot at base; pedicel dark brown with apical third whitish (70:30); F1 dark brown, F2 pale brown externally but ventrally white, F3–F6 white with infuscation on dorsal side and darker setae on outer surface; clava yellowish white, basal segment with darker setae; mesosoma orange but neck of pronotum dark brown to dusky, dorsal surface of pronotum medially whitish, laterally orange; tegula whitish with brown suffusion distally; propodeum medially pale orange, brown laterally; prepectus whitish; mesopleuron orange mixed with brown; dorsum of mesothorax covered with dense, short, silvery white setae; scutellum with 3 pairs of sub-apical, semi-erect dark brown setae; fore wing hyaline with venation dark brown; hind wing and its venation hyaline; legs mostly whitish; fore coxa whitish with pale brown suffusion; mid coxa pale brown in basal half, hind coxa fully pale brown; fore and mid femora whitish, but dorsally brownish; hind femur with margins dark brown, remainder with brownish suffusion; all tibiae whitish with dorsal margin brown; tarsi yellowish brown with last segment darker brown; gaster dark brown covered by dense, short silvery white setae.

Head in frontal view ( Fig. 5 ) slightly (1.1×) wider than high; frontovertex 0.4× head width with fine reticulate sculpture; setae on frontovertex as long as diameter of anterior ocellus; posterior ocellus closer to eye margin than occipital margin; eye posteriorly overreaching occipital margin, with dense, dark brown setae, each at least as long as a facet; inner eye margins diverging ventrally; dorsal margin of antennal torulus below ventral eye margin; torulus separated from mouth margin by about 0.4× its height; antennal scrobes moderately deep; malar sulcus distinct; antennal scape ( Fig. 7 ) 2.19× as long as broad; pedicel 2.62× as long as broad, shorter than F1 and F2 combined; all funicle segments longer than broad, F1 to F6 progressively slightly wider; F1 slightly longer than other segments; F3 and F4 equal in length; clava 2.29× as long as broad, longer than preceding three funicle segments combined, with numerous longitudinal sensillae, its apical margin slightly obliquely transverse. Relative measurements: head height, 85; head width, 94; frontovertex width, 40; POL, 13; OOL, 5; OCL, 5: AOL, 7; eye height, 60; malar space, 27; antennal torulus height, 13; torulus width, 7; distance between antennal toruli, 18; distance between lower margin of antennal torulus and mouth margin, 5; radicle length, 12; length and (width) - scape, 57 (26); pedicel, 21 (8); F1, 13 (6); F2, 11 (7); F3, 11 (8); F4, 11 (8); F5, 12 (9); F6, 12 (10); clava, 39 (17).

Mesosoma dorsally with fine reticulate sculpture as on frontovertex; sculpture on scutellum little deeper than that on mesoscutum; posterior margin of pronotum concave; fore wing ( Fig. 10 ) 2.46× as long as broad; linea calva interrupted by 5 rows of setae; costal cell narrow, 25× as long as broad, ventrally with one complete line of setae; marginal vein and stigmal vein equal in length; hind wing 4.4× as long as broad; length of mid tibial spur 0.3× of mid tibia; mid basitarsus longer than mid tibial spur. Relative measurements: fore wing length, 59; fore wing width, 24; longest marginal fringe length, 6; submarginal vein length, 98; marginal vein length, 13; postmarginal vein length, 8; stigmal vein length, 13; hind wing length, 40; width, 9; longest marginal fringe length, 9; mid tibia length, 106; mid tibial spur length, 33; mid basitarsus length, 40.

Metasoma slightly longer than mesosoma, ovipositor ( Fig. 12 ) not exserted, shorter than mid tibia (0.58× of mid tibia), 1.87× as long as mid tibial spur. Relative measurements: ovipositor length, 62; TVII length, 94.

Male ( Fig. 3 ). Length, 1.0 mm. Head dark brown, malar space and region below antennal toruli reddish brown; setae on ocellar region brown, remaining silvery white; radicle dark brown; scape white in basal one-third, remainder dark brown; flagellum pale brown, except F1 little darker; setae on flagellum brown; dorsum of mesosoma dark brown; prepectus whitish; tegula dark brown except base whitish; sides of pronotum and mesopleuron orange brown, anterior side of mesopleuron orange; fore wing hyaline with venation brown; hind wing and its venation hyaline; fore coxa white with dark markings, femur white with dorsal and ventral margins brown, tibia pale brown, tarsus brown; mid and hind coxae brown with white apices, mid femur and tibia white with margins brown, tarsus brownish white; hind femur and tibia brownish with some white markings, tarsus brown; gaster brown.

Head in frontal view ( Fig. 6 ) slightly (1.15×) wider than high; frontovertex 0.57× of head width; antennal scape ( Fig. 8 ) 4.66x as long as wide; pedicel 1.66× as long as wide; all funicle segments longer than broad; F6 shorter than others, others subequal in length; clava solid, shorter than preceding three funicle segments combined; F1 and F2 without longitudinal sensillae; flagellum covered with dark, long and thick setae up to 1.0–1.3× as long as diameter of a funicular segment, F6 with 7 scale-like structures, clava with 4 scale-like structures at its base. Relative measurements: head height, 72; head width, 83; frontovertex width, 47; eye height, 42; malar space, 27; antennal torulus height, 11; torulus width, 7; distance between antennal toruli, 14; radicle length, 7; length and (width)-scape, 28 (6); pedicel, 10 (6); F1, 16 (5); F2, 15 (6); F3, 17 (6); F4, 16 (6); F5, 15 (6); F6, 13 (6); clava, 33 (9).

Mesosoma dorsally with prominent reticulate sculpture; fore wing ( Fig. 11 ) a little more than twice (2.04×) as long as broad; hind wing 3.94× as long as broad; mid tibial spur and mid basitarsus equal in length. Relative measurements: fore wing length, 94; fore wing width, 46; hind wing length, 63; hind wing width, 16; mid tibia length, 89; mid tibial spur length, 24; mid basitarsus length, 24.

Metasoma shorter than mesosoma. Genitalia ( Fig. 13 ) shorter than mid tibia; phallobase with a pair of digiti, each with a pair of apical hooks. Relative measurement (at 20×): genitalia length, 75.

Variation. Female: Length 1.0– 1.3mm; degree of infuscation on dorsal side of F3–F6 sometimes more pronounced ( Fig. 4 ); metasoma in some specimens equal to or shorter than mesosoma. Antennal scape 2.07–2.34× as long as broad; Fore wing 2.40–2.48× as long as broad; ovipositor length 0.54–0.63× of mid tibia; ovipositor 2.15–2.23× as long as mid tibial spur.

Male: Length 0.8–1.0 mm.

Material examined. Holotype, female. “ INDIA: Karnataka: Bangalore, Hebbal, ex. Phenacoccus madeirensis on Hibiscus sp., 15.ii.2013, J. Poorani” (NBAII).

Paratypes: 12 females, 5 males, with same data as holotype; 16 females, 8 males, INDIA, Karnataka, Bangalore, Hessarghatta, ex. Phenacoccus madeirensis on Solanum melongena , 05.ii.2013, A. Rameshkumar (NBAII, NPC, BMNH, NMNH). ITALY, Sicily, Marsala, ex Phenacoccus madeirensis on Brachychiton ?acerifolium, viii.2005 (B. Nijhof), 9 females, 4 males (BMNH).

Additional specimens examined: 13 females, 6 males, INDIA, Karnataka, Bangalore, Hebbal, ex. Phenacoccus madeirensis on weeds, 21.iii.2013, J. Poorani (NBAII, NPC, BMNH); 5 females, 3 males, USA, Georgia, Spalding Co., Georgia Exp. Sta. Ent. Insectary, ex Phenacoccus madeirensis , 13.viii.2003 (J.H. Chong) (PhD adult longevity study gregarious form); 34 females, 10 males, USA, Georgia, Griffin, Georgia Exp. Sta. Ornamental Ent. GH, ex Phenacoccus madeirensis ,?2005 (J.H. Chong) (BMNH); USA: Georgia: Spalding County, University of Georgia, Griffin Campus, 23.v.2005, Ex. Phenacoccus madeirensis Green on coleus, J.H. Chong, 6 females and 1 male (NBAII).

Hosts. Phenacoccus madeirensis (Pseudococcidae) on different host plants including Hibiscus rosasinensis L. ( Malvaceae ), Solanum melongena L., Solanum spp. ( Solanaceae ), and Lantana camara L. (Verbanaceae).

Geographical distribution: USA ( Georgia); Italy (Sicily); India (Karnataka).

Considering its reported host specificity and the distribution and invasive history of its host, P. madeirensis , it is likely that this parasitoid has been fortuitously introduced along with its mealybug host. The disparate geographic distribution known at present seems to support this.

Etymology. The specific epithet is of Greek origin (Gr. “ amnestos ” = ‘forgotten’, ‘neglected’) and is in reference to the long neglected/nameless status of the species despite its proven promise as a highly host-specific biological control agent of the Madeira mealybug.

Comments. This species is similar to two other species in its native range, A. sinope and A. aega Noyes & Menezes (in Noyes 2000). Anagyrus sinope , which is most similar to A. amnestos , differs from it by the following features: antenna with F3–F6 and clava white, scape about 2× as long as broad, pedicel nearly as long as F1 and F2 combined; fore wing with marginal vein 1.5× as long as stigmal, marginal and postmarginal veins combined about 2× as long as stigmal, linea calva interrupted by 3–4 rows of setae; hind wing 4× as long as broad. Anagyrus aega can be separated from A. amnestos as follows: clypeal margin orange, antenna with F1 and F2 dark brown, remainder of flagellum white; fore wing 2.39× as long as broad, marginal and postmarginal veins combined about 2× as long as stigmal vein, linea calva interrupted by 3–4 rows of setae, hind wing 3.8× as long as broad. Anagyrus loecki , introduced to India for the classical biological control of P. marginatus , is also known to parasitize P. madeirensis , but is easily separated from A. amnestos by its almost fully white flagellum except for the dark brown first funicle segment. Anagyrus loecki is not known to have established so far in any of the released sites in southern India (unpublished data).

Two indigenous species in India, A. agraensis Saraswat ( Figs 14–19 ) and A. kamali Moursi ( Figs 20–27 ), have some superficial similarities to A. amnestos in general appearance, particularly in having infuscate/dark setae on the flagellar segments of the female antennae. The antenna in A. agraensis is strikingly similar to that of A. amnestos with the presence of infuscate setae extending as far as the first segment of the clava ( Figs. 14, 17 ), but A. agraensis differs from A. amnestos in having the scape distinctly broader in the middle and F1 and F2 distinctly longer ( Fig. 17 ), a row of dark brown to black setae on the posterior margin of the pronotum ( Fig. 16 ), the ventral surface of the costal cell of the fore wing with two complete lines of setae, and the antennal scape of the male white with the apical third dark brown. The female of A. kamali ( Figs. 20–27 ) has a distinctly more robust body outline compared to A. amnestos , the thoracic setal pattern includes a mixture of black and white setae ( Fig. 26 ), the fore wing lacks marginal setae on the extreme apex ( Fig. 27 ), there are more than two lines of setae on the ventral surface of the costal cell of the fore wing, and the male has the antennal scape whitish with a median dark band, which readily separate it from A. amnestos . The host associations of A. agraensis and A. kamali also are different, with the former being predominantly associated with Nipaecoccus viridis (Newstead) and the latter with Maconellicoccus hirsutus (Green) (Pseudococcidae) in southern India.

In the key to Oriental Anagyrus provided by Noyes & Hayat (1994), A. amnestos appears to run close to A. levis Noyes & Hayat , which is, however, very different and is distinguished by the following: antenna with the first two funicle segments less than twice as long as broad, apical funicle segments darkened externally; ovipositor 0.76× as long as midtibia, and fore wing 2.32× as long as wide.

Biological notes. Anagyrus amnestos was found to parasitize only P. madeirensis , even when simultaneously offered five other mealybug species in addition to P. madeirensis (Chong & Oetting 2007c). Developmental rate of A. amnestos increased with, whereas adult longevity decreased with, increasing temperature between 15 and 30o C (Chong & Oetting 2006a, c). Parasitism rate ranged 17–40% within a 24-hour period, with each female parasitoid producing a range of 58–71 offspring over her lifetime at an average female:male ratio of 2:1 (Chong & Oetting 2006a). Being a koinobiont, gregarious parasitoid, the continuous development of young P. madeirensis after parasitism allowed the parasitoid larvae to accumulate sufficient resources to maximize brood size, survival rate, proportion of females, and body size (Chong & Oetting 2007a). Chong & Oetting (2007b) reported A. amnestos preferred to parasitize third-instar and adult P. madeirensis , which subsequently produced larger and presumably fitter offspring (Chong & Oetting 2006d). Anagyrus amnestos displayed a Type II functional response with the maximum numbers of second-instar and pre-reproductive adults estimated at 28 and 13 individuals, respectively, within a 24-hour period (Chong & Oetting 2007 d). Chong & Oettings (2006b) also found that mutual interference among foraging parasitoids could reduce the estimated maximum numbers of mealybugs parasitized from 10 when foraging alone to 5 when foraging in the presence of 3 other conspecifics.

Figures

FIGURES 1 – 4. Anagyrus amnestos sp. n.: 1. Female, dorsal view; 2. Female, lateral view; 3. Male, dorsal view; 4. Female, dorsal view of head, and antenna.

FIGURES 5 – 13. Anagyrus amnestos sp. n.: 5. Female head, frontal view (slide preparation); 6. Male head, frontal view (slide preparation); 7. Antenna, female; 8. Antenna, male; 9. Head and mesosoma, dorsal view; 10. Fore wing, female; 11. Fore wing, male; 12. Female genitalia; 13. Male genitalia.

FIGURES 14 – 19. Anagyrus agraensis: 14. Female, dorsal view; 15. Female, lateral view; 16. Head and mesosoma, dorsal view; 17. Antenna, female; 18. Antenna, male; 19. Fore wing, female.

FIGURES 20 – 27. Anagyrus kamali: 20. Female, dorsal view; 21. Female, lateral view; 22. Antenna, female; 23. Antenna, male; 24. Male, dorsal view; 25. Male, lateral view; 26. Head and mesosoma, dorsal view; 27. Fore wing, female.