Trichogramma chagres Fursov and Woelke, Trichogramma soberania Fursov and Woelke,

Woelke, Jozef B., Fursov, Viktor N., Gumovsky, Alex V., Rijk, Marjolein de, Estrada, Catalina, Verbaarschot, Patrick, Huigens, M, 2019, Description and biology of two new egg parasitoid species (Hymenoptera: Trichogrammatidae) reared from eggs of Heliconiini butterflies (Lepidoptera: Nymphalidae: Heliconiinae) in Panama, Journal of Natural History 53 (11), pp. 639-657: 647-654

publication ID

http://doi.org/ 10.1080/00222933.2019.1606360

publication LSID

lsid:zoobank.org:pub:941854EE-4A47-4A98-B88E-1EC19D83D074

persistent identifier

http://treatment.plazi.org/id/C70187BE-2F2E-FFAF-FEAC-FEAAFBE8F960

treatment provided by

Valdenar

scientific name

Trichogramma chagres Fursov and Woelke Trichogramma soberania Fursov and Woelke
status

sp. nov.

Trichogramma chagres Fursov and Woelke  , sp. nov.

( Figures 2View Figure 2 and 3View Figure 3)

Diagnosis

Trichogramma chagres  sp. nov. is characterized by a wide GC (about 2.21–2.30 times as long as wide, Figure 2View Figure 2 (b,c)), very wide DLA ( Figure 2View Figure 2 (c)), very long, narrow and apically sharp IVP ( Figure 2View Figure 2 (b)), long and sharp setae of antennae (about 1.92–2.11 times as long as width of clava, Figure 2View Figure 2 (c)). The new species is morphologically close to T. benetti Nagaraja and Nagarkatti  , T. drepanoforum Pinto and Oatman  and T. atopovirilia Oatman and Platner  , but it is distinguishable from them all in the possession of the distinctly long and narrow IVP (about 1.21–1.57 times as long as wide, Figure 2View Figure 2 (c)), which is much shorter and wider in the other species ( Nagaraja and Nagarkatti 1973; Oatman and Platner 1983; Querino and Zucchi 2005). Apart from the shape of IVP, T. chagres  sp. nov. differs from T. bennetti  in having a very narrow base of GC ( Figure 2View Figure 2 (b,c)) (it is widened basally in T. bennetti  ). The new species is distinguishable from both T. drepanoforum  and T. bennetti  in having the wide DLA shaped like a spade with a subtriangular tip ( Figure 2View Figure 2 (c)) (the tip of DLA is evenly acute in both T. drepanoforum  and T. bennetti  ). Also, the tip of DLA is extended beyond the tips of vorsellar digiti in T. chagres  sp. nov. ( Figure 2View Figure 2 (b,c)), unlike in T. bennetti  . Trichogramma chagres  sp. nov. ( Figure 2View Figure 2 (b,c)) is also distinguishable from T. atopovirilia  in having a short vorsellar digiti, whereas they are sharp and much longer in the latter species. IVP of T. atopovirilia  is very short, broadly triangular, with 3 tiny ribs on its tip, whereas IVP is long, narrow and with sharp arrow-like tip in T. chagres  sp. nov. GC is suboval and much broader, with ratio GL/GW about 1.70 in T. atopovirilia  , whereas it is more slender and narrow, with GL/GW = 2.21–2.30 (avg. 2.24) in T. chagres  sp. nov.

Description

Based on holotype and 3 paratype male specimens.

Colour of head and antennae yellow; meso- and metasoma dark brown, except bright yellow axillae, propodeum and base of gaster. All legs yellow, except hind femora and tibiae which are dirty yellow-brown.

Antenna ( Figure 2View Figure 2 (d)) with flagellum 5.26–6.51 (avg. 5.67) times as long as maximum width, 1.92–2.11 (avg. 1.95) times as long as length of scape; SL/FW = 2.85–3.43 (avg. 3.10). Number of flagellar setae 35–38 ( Figure 2View Figure 2 (d)).

GL ( Figure 2View Figure 2 (b,c)) 112.25–137.18 μm (avg. 122.73), GW 50.87–62.11 (avg. 55.50), DA-L 82.15–105.89 (avg. 90.03). DLA-L 23.62–38.29 (avg. 30.85), DLA-W 29.39–33.14 (avg. 31.66); IVP-L 6.97–13.22 (avg. 8.76), IVP-W 4.62–9.90 (avg. 6.18); AD 25.51–38.86 (avg. 31.83); PL 25.81–38.29 (avg. 30.80); AL-B 42.13–44.94 (avg. 44.69); AL 85.63–116.85 (avg. 97.39).

GC wide, with wide DLA, GL/GW = 2.21–2.30 (avg. 2.24), but very narrow at the base ( Figure 2View Figure 2 (b,c)), widest medially or subapically (at distance of 0.53 of GL), then sharply narrowed to the top, with elongated dorsal aperture. DA-L/GL = 0.70–0.78 (avg. 0.74). DLA very wide, spade-shaped, without basal lobes, but with small sharp lateral-apical notches, with nearly parallel lateral sides and with rounded and slightly sharpened apical part ( Figure 2View Figure 2 (c)), extended over apical parts of parameres ( Figure 2View Figure 2 (b,c)). DLA-L/DLA-W = 0.81–1.18 (avg. 0.98). GW/DLA-W = 1.60–1.92 (avg. 1.77). DLA-L/GL = 0.47–0.50 (avg. 0.49). Apex of DLA not extending beyond apical part of parameres, but extending beyond apices of vorsellar digiti ( Figure 2View Figure 2 (b)). IVP sclerotized, large, with wide base and with sharp teeth-like apex ( Figure 2View Figure 2 (b)). IVP-L/IVP-W = 1.21–1.57 (avg. 1.42). AD/IVP-L = 2.58–5.19 (avg. 3.76). AD/GL = 0.23–0.31 (avg. 0.27). Apical part of GC narrowed gradually, without curvature. Parameres extending to the apex of vorsellar digiti at a distance 1.56–2.75 (avg. 2.07) as long as IVP ( Figure 2View Figure 2 (b)). PL/ DLA-L = 0.77–1.28 (avg. 1.04). DA-L/GL = 0.71–0.78 (avg. 0.75). AL/GL = 0.47–0.50 (avg. 0.49). AL-B/AL = 0.73–0.86 (avg. 0.82).

Wings. Fore and hind wings transparent. MV with three large and four small setae ( Figure 2View Figure 2 (e)). Hind wing with 1–2 setae in anterior, 16–21 setae in middle and 5–8 setae in posterior setal track; fringe with 17–20 short anterior and 24–25 long posterior setae; FL/HWW = 1.52–1.68.

Material examined

Holotype male. (SIZK), PANAMA, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, collected 11 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk), specimen on glass slide under 2 small cover slips (genitalia under right side cover slip), circled with black ink, on slide no. 2019 (strain L21) (in Canada balsam).GoogleMaps 

Paratypes. same data (all from strain L21), 1 female on slide no. 2019 (SIZK);  1 male and 1 female on slide no. 2020 (SIZK);  1 male and 1 female on slide no. 2021 (RMNH);  1 male and 1 female on slide no. 2022 (NHMUK) (all in Canada balsam). 

Additional material. (SIZK) same label (strain L23, this parasitized Heliconiini  egg was collected on the same plant, date and location as strain L21), 5 males and 4 females on slide no. 1875;  3 males and 3 females on slide no. 1876; 3 males and 3 females on slide no. 1877; 3 males and 3 females on slide no. 1878 (all in Canada balsam). 

PANAMA, Gamboa, 9°07 ʹ 05.8 ʺ N, 79°41 ʹ 41.1 ʺ W, collected 3 April 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on P. vitifolia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk), strain L31 (SIZK), 3 males and 2 females on slide no. 1871;  3 males and 3 females on slide no. 1872; 3 males and 3 females on slide no. 1873; 5 males and 4 females on slide no. 1874 (all in Canada balsam).

Field records. Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #112, 7 females and 2 males collected 26 February 2008 from egg of Agraulis vanillae vanillae  ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk).

 

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #295 (origin of strain L21) 10 females and 2 males collected 11 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk). 

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #300, 6 females and 1 male collected 11 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J. B. Woelke and M. de Rijk). 

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #301 (origin of strain L23) 10 females and 2 males collected 11 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk). 

Panama, Gamboa, 9°07 ʹ 05.8 ʺ N, 79°41 ʹ 41.1 ʺ W, #1039 (origin of strain L31), unknown number of wasps collected 3 April 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on P. vitifolia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk). 

Host

Wasps were reared from eggs of Agraulis vanillae vanillae  ( Figure 1View Figure 1 (g,h)) and Heliconiini  spp. found on Passiflora foetida  L. var. isthmia Killip  ( Figure 1View Figure 1 (d)) and P. vitifolia Kunth  ( Figure 1View Figure 1 (e)).

Biology

Idiobiont endoparasitoid. All specimens of this species were reared from collected eggs of Heliconiini  butterflies, which were deposited on Passiflora  plants. The collected wasps had an average of 8.25 ± 2.06 SD females and 1.75 ± 0.50 SD males per egg, and a sex-ratio of 21.21%. More specific information about strain L21 ( Figure 3View Figure 3), L23 and L31 ( Figure S1View Figure 1). Females actively oviposit into fresh and relatively mature host eggs (with red bands) ( Figure 3View Figure 3 (a– c), S1a,b). The freshly laid parasitoid egg is 0.08–0.09 mm long ( Figure 3View Figure 3 (d), S1c), developing embryo within the egg (24 h after oviposition) is about 0.15 mm long and 0.05 mm wide (in its widest part) ( Figure S1d,eView Figure 1). The newly hatched larva is about 0.1 mm long, with distinct head capsule bearing mandibles and three thoracic segments separated by deep constrictions, unsegmented abdomen and a caudal formation behind ( Figure 3View Figure 3 (e)). The mature fully fed larva is about 0.7 mm long, 0.4 mm wide, with pulsing mid gut full of consumed host yolk, with remnants of caudal bladder (membranes) behind ( Figure 3View Figure 3 (f– h), S 1g,h). No moults were traced during the larval development, and the mandibles of hatching and mature larvae are of the same size, about 0.01 mm long ( Figure S1fView Figure 1).

Distribution

Panama, tropical lowland rainforest of the Soberania National Park (Parque Nacional Soberanía) ( Figure 1View Figure 1 (c)), and in the town of Gamboa and surroundings.

Etymology

The Chagres (in Spanish: Rio Chagres) is the largest river (193 km) in the Panama Canal watershed. The river that surrounds our research areas, making a sharp bend around the town of Gamboa.

Sequence analysis

MegaBLAST analysis revealed that our Internal Transcribed Spacer 2 (ITS-2) sequences of T. chagres  sp. nov. matched with 40% query cover and 89% identity to T. chilotraeae Nagaraja and Nagarkatti in GenBank. Sequence  ID T. chagres  sp. nov.: MK159692View Materials.

Trichogramma soberania Fursov and Woelke  , sp. nov.

( Figures 4View Figure 4 and 5View Figure 5)

Diagnosis

Trichogramma soberania  sp. nov. is characterized by a narrow shape of phallobase (about 2.5 times as long as wide, Figure 4View Figure 4 (a,b)), very narrow and apically sharp and elongated DLA ( Figure 4View Figure 4 (b)), long and sharp setae of antennae (about 2.5 times as long as width of clava ( Figure 4View Figure 4 (c)). The species is morphologically close to T. exiguum Pinto and Platner  and T. pretiosum Riley  but can be differentiated from both species by the presence of a long and very narrow IVP (2.0–3.62 times as long as wide, Figure 4View Figure 4 (a)). Also, T. soberania  sp. nov. is discernible from T. pretiosum  in the shape of DLA ( Figure 4View Figure 4 (b)), which is notably narrower in the latter species. Trichogramma soberania  sp. nov. is also distinguishable in having a long and thin setae on the male antenna with SL/ FW = 2.71–3.04 (avg. 3.0), whereas they are robust and shorter in T. exiguum  , with SL/ FW = 1.90–2.24 (avg. 2.04). The male antenna of T. pretiosum  is very similar to T. soberania  sp. nov. (with long setae having SL/FW = 2.92–3.30 (avg. 3.11)); however, the two species may be distinguished based on the shape of DLA, as mentioned above. Description

Based on holotype and 8 paratype male specimens.

Colour of head, antennae, meso- and metasoma dark brown, except light yellow scutellum, propodeum and base of metasoma, all legs brown, eyes red.

Antenna ( Figure 4View Figure 4 (c)) with flagellum 5.40–6.19 (avg. 5.83) times as long as its maximum width, and 1.95–2.08 times (avg. 2.02) as long as length of scape; SL/FW = 2.71–3.04 (avg. 3.0). Number of flagellar setae 37–44 ( Figure 4View Figure 4 (a)).

GL 112.60–158.55 (avg. 132.05), GW 35.33–61.02 (avg. 50.96); GW-B 20.46–24.58 (avg. 22.54); DA-L 62.10–95.54 (avg. 76.47).

DLA 36.11–46.03 (avg. 43.50), width 30.08–48.35 (avg. 38.84) ( Figure 4View Figure 4 (b); IVP-L 9.51–18.00 (avg. 14.70); AD 31.20–42.41 (avg. 35.60); PL 29.87–35.08 (avg. 32.82); AL-B 70.58–88.83 (avg. 75.73); AL 126.35–167.28 (avg. 144.22).

GC very narrow basally, widest medially or subapically, and then again sharply narrowed apically; with elongate dorsal aperture. DA-L/GL = 0.56–0.61 (avg. 0.59). GL/ GW = 2.52–3.31 (avg. 2.80). GW/GW-B 1.73–2.49 (avg. 2.26). DLA sharply narrowed medially and smoothly narrowed apically, subtriangular, with distinct basal lobes, small sharp lateral notches, and with smoothly rounded apical part ( Figure 4View Figure 4 (b)). Basal lobes of DLA not extended to lateral sides of GC. Apex of DLA not extended beyond apical part of parameres, but extended beyond the apex of volsellae and volsellar digiti, as well as beyond the apex of IVP ( Figure 4View Figure 4 (a,b)). Apex of DLA narrower than width of aedeagus ( Figure 4View Figure 4 (b)). DLA-L/DLA-W = 0.29–0.40 (avg. 0.34). GW/DLA-W = 1.24–1.75 (avg. 1.41). DLA-L/GL 0.40–0.56 (avg. 0.34). IVP sclerotized on both lateral sides, long, with wide base and with very narrow awl-like sharpened apex ( Figure 4View Figure 4 (a)). IVP not extended beyond the apex of vorsellar digiti, and beyond the apex of DLA. IVP-L/IVP-W = 2.0–3.62 (avg. 2.57). AD/IVP-L = 2.03–3.76 (avg. 2.42). AD/GL = 0.27–0.42 (avg. 0.31). Apical part of GC narrowed gradually, without curvature ( Figure 4View Figure 4 (a,b)). PL/DLA-L 0.63–0.73 (avg. 0.72). AL/GL = 1.04–1.09 (avg. 1.07). AL-B/AL = 0.48–0.56 (avg. 0.53).

Wings. Fore and hind wings transparent, MV with four large and four small setae ( Figure 4View Figure 4 (d)). Hind wing with 1–2 setae in anterior, 26 setae in middle and 5–6 setae in posterior track; fringe with 20 short anterior and 26–27 long posterior setae; FL/ HWW = 1.81–1.94.

Material examined

Holotype male. (SIZK), PANAMA, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, collected 4 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk), specimen on glass slide under 3 small cover slip (genitalia under right left side cover slip), circled with black ink, on slide no. 2023 (strain L20) (in Canada balsam).GoogleMaps 

Paratypes. same label (all from strain L20), 1 male on slide no. 2024 (SIZK);  1 male and 1 female on slide no. 2025 (SIZK);  1 male and 1 female on slide no. 2026 (SIZK);  1 male and 1 female on slide no. 2027 (RMNH);  1 male and 1 female on slide no. 2031 (NHMUK);  1 male on slide no. 2028 (SIZK);  1 male on slide no. 2029 (SIZK);  1 male on slide no. 2030 (SIZK) (all in Canada balsam).

Additional material. (SIZK) same label (strain L20), 3 males and 1 female on slide no. 1867; 3 males and 3 females on slide no. 1868;  3 males and 2 females on slide no. 1869;  3 males and 3 females on slide no. 1870 (all in Canada balsam). 

 

Field records. Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #105, 7 females and 1 male collected 26 February 2008 from egg of Agraulis vanillae vanillae  ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk);

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #168, 10 females and 1 male collected 4 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J. B. Woelke and M. de Rijk);

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #180 (origin of strain L20), 2 females and 1 male collected 4 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk);

Panama, Plantation Road, 9°04 ʹ 32.1 ʺ N, 79°39 ʹ 32.3 ʺ W, #283, 5 females and 2 males collected 6 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora biflora  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk);

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #346, 2 females and 1 male collected 20 March 2008 from egg of Agraulis vanillae vanillae  ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk).

Phoretic wasp record. Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #32, 1 female wasp was collected on a female Heliconius hecale melicerta  butterfly, 12 February 2008 (coll. J.B. Woelke and M. de Rijk).

Host

Wasps were reared from eggs of Agraulis vanillae vanillae  ( Figure 1View Figure 1 (g,h)) and Heliconiini  spp. found on Passiflora biflora Lamarck  ( Figure 1View Figure 1 (f)) and P. foetida  L. var. isthmia Killip  ( Figure 1View Figure 1 (d)).

Biology

Idiobiont endoparasitoid. All specimens of this species were reared from eggs of Heliconiini  butterflies, which were deposited on Passiflora  plants. The collected wasps had an average of 5.20 ± 3.42 SD females and 1.20 ± 0.45 SD males per egg, and a sexratio of 23.08%. Our finding of one female wasp on an adult female Heliconius hecale melicerta  butterfly ( Figure 1View Figure 1 (i,j)) suggests that this species may occasionally be phoretic on adult female butterflies to find suitable host eggs.

More specific information about strain L20. Female wasps oviposit several eggs into a M. brassicae  host of various ages (fresh and mature with red stripes) ( Figure 5View Figure 5 (a,b)). Both winged and brachypterous females oviposit. Freshly laid egg is ovoid, about 0.12 mm long, and ~ 0.06 mm wide ( Figure 5View Figure 5 (c)). About 24 h after, an embryo is traceable within the egg. The freshly hatched larva is about as long as the egg, with poorly sclerotized mandibles. Forty-eight hours later the larva is already 0.4–0.6 mm long, and has a distinct mid gut full of consumed host yolk ( Figure 5View Figure 5 (d)). About 50 h after oviposition the entire egg is consumed, and larvae reach nearly their final size. Up to 14 larvae can develop in same egg of M. brassicae  ( Figure 5View Figure 5 (e)) The fully grown larva is about 0.7–0.8 mm long, swollen, with full mid gut; occasionally it is reddish with white spots ( Figure 5View Figure 5 (f)). No moult or changes in mandible size were traced during the larval development. The male and female pupae differ in size and colour pattern ( Figure 5View Figure 5 (g)). Host eggs turn black after consumption, as in most Trichogramma  species ( Figure 5View Figure 5 (h)).

Distribution

Panama, tropical lowland rainforest of the Soberania National Park (Parque Nacional Soberanía) ( Figure 1View Figure 1 (c)), and in the town of Gamboa and surroundings.

Etymology

Research was conducted in Soberania National Park (in Spanish: Parque Nacion soberanía  ) in Panama, as well in the town of Gamboa, which is located in this park. The park has been protected since 1980, and covers 220 km 2 of tropical lowland rainforest.

Sequence analysis

MegaBLAST analysis revealed that our Internal Transcribed Spacer 2 (ITS-2) sequences of T. soberania  sp. nov. matched with 37% query cover and 93% identity to T. chilotraeae in GenBank. Sequence  ID T. soberania  sp. nov.: MK159692View Materials.

Trichogramma soberania Fursov and Woelke  , sp. nov.

( Figures 4View Figure 4 and 5View Figure 5)

Diagnosis

Trichogramma soberania  sp. nov. is characterized by a narrow shape of phallobase (about 2.5 times as long as wide, Figure 4View Figure 4 (a,b)), very narrow and apically sharp and elongated DLA ( Figure 4View Figure 4 (b)), long and sharp setae of antennae (about 2.5 times as long as width of clava ( Figure 4View Figure 4 (c)). The species is morphologically close to T. exiguum Pinto and Platner  and T. pretiosum Riley  but can be differentiated from both species by the presence of a long and very narrow IVP (2.0–3.62 times as long as wide, Figure 4View Figure 4 (a)). Also, T. soberania  sp. nov. is discernible from T. pretiosum  in the shape of DLA ( Figure 4View Figure 4 (b)), which is notably narrower in the latter species. Trichogramma soberania  sp. nov. is also distinguishable in having a long and thin setae on the male antenna with SL/ FW = 2.71–3.04 (avg. 3.0), whereas they are robust and shorter in T. exiguum  , with SL/ FW = 1.90–2.24 (avg. 2.04). The male antenna of T. pretiosum  is very similar to T. soberania  sp. nov. (with long setae having SL/FW = 2.92–3.30 (avg. 3.11)); however, the two species may be distinguished based on the shape of DLA, as mentioned above. Description

Based on holotype and 8 paratype male specimens.

Colour of head, antennae, meso- and metasoma dark brown, except light yellow scutellum, propodeum and base of metasoma, all legs brown, eyes red.

Antenna ( Figure 4View Figure 4 (c)) with flagellum 5.40–6.19 (avg. 5.83) times as long as its maximum width, and 1.95–2.08 times (avg. 2.02) as long as length of scape; SL/FW = 2.71–3.04 (avg. 3.0). Number of flagellar setae 37–44 ( Figure 4View Figure 4 (a)).

GL 112.60–158.55 (avg. 132.05), GW 35.33–61.02 (avg. 50.96); GW-B 20.46–24.58 (avg. 22.54); DA-L 62.10–95.54 (avg. 76.47).

DLA 36.11–46.03 (avg. 43.50), width 30.08–48.35 (avg. 38.84) ( Figure 4View Figure 4 (b); IVP-L 9.51–18.00 (avg. 14.70); AD 31.20–42.41 (avg. 35.60); PL 29.87–35.08 (avg. 32.82); AL-B 70.58–88.83 (avg. 75.73); AL 126.35–167.28 (avg. 144.22).

GC very narrow basally, widest medially or subapically, and then again sharply narrowed apically; with elongate dorsal aperture. DA-L/GL = 0.56–0.61 (avg. 0.59). GL/ GW = 2.52–3.31 (avg. 2.80). GW/GW-B 1.73–2.49 (avg. 2.26). DLA sharply narrowed medially and smoothly narrowed apically, subtriangular, with distinct basal lobes, small sharp lateral notches, and with smoothly rounded apical part ( Figure 4View Figure 4 (b)). Basal lobes of DLA not extended to lateral sides of GC. Apex of DLA not extended beyond apical part of parameres, but extended beyond the apex of volsellae and volsellar digiti, as well as beyond the apex of IVP ( Figure 4View Figure 4 (a,b)). Apex of DLA narrower than width of aedeagus ( Figure 4View Figure 4 (b)). DLA-L/DLA-W = 0.29–0.40 (avg. 0.34). GW/DLA-W = 1.24–1.75 (avg. 1.41). DLA-L/GL 0.40–0.56 (avg. 0.34). IVP sclerotized on both lateral sides, long, with wide base and with very narrow awl-like sharpened apex ( Figure 4View Figure 4 (a)). IVP not extended beyond the apex of vorsellar digiti, and beyond the apex of DLA. IVP-L/IVP-W = 2.0–3.62 (avg. 2.57). AD/IVP-L = 2.03–3.76 (avg. 2.42). AD/GL = 0.27–0.42 (avg. 0.31). Apical part of GC narrowed gradually, without curvature ( Figure 4View Figure 4 (a,b)). PL/DLA-L 0.63–0.73 (avg. 0.72). AL/GL = 1.04–1.09 (avg. 1.07). AL-B/AL = 0.48–0.56 (avg. 0.53).

Wings. Fore and hind wings transparent, MV with four large and four small setae ( Figure 4View Figure 4 (d)). Hind wing with 1–2 setae in anterior, 26 setae in middle and 5–6 setae in posterior track; fringe with 20 short anterior and 26–27 long posterior setae; FL/ HWW = 1.81–1.94.

Material examined

Holotype male. (SIZK), PANAMA, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, collected 4 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk), specimen on glass slide under 3 small cover slip (genitalia under right left side cover slip), circled with black ink, on slide no. 2023 (strain L20) (in Canada balsam).GoogleMaps 

Paratypes. same label (all from strain L20), 1 male on slide no. 2024 (SIZK);  1 male and 1 female on slide no. 2025 (SIZK);  1 male and 1 female on slide no. 2026 (SIZK);  1 male and 1 female on slide no. 2027 (RMNH);  1 male and 1 female on slide no. 2031 (NHMUK);  1 male on slide no. 2028 (SIZK);  1 male on slide no. 2029 (SIZK);  1 male on slide no. 2030 (SIZK) (all in Canada balsam).

Additional material. (SIZK) same label (strain L20), 3 males and 1 female on slide no. 1867; 3 males and 3 females on slide no. 1868;  3 males and 2 females on slide no. 1869;  3 males and 3 females on slide no. 1870 (all in Canada balsam). 

 

Field records. Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #105, 7 females and 1 male collected 26 February 2008 from egg of Agraulis vanillae vanillae  ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk);

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #168, 10 females and 1 male collected 4 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J. B. Woelke and M. de Rijk);

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #180 (origin of strain L20), 2 females and 1 male collected 4 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk);

Panama, Plantation Road, 9°04 ʹ 32.1 ʺ N, 79°39 ʹ 32.3 ʺ W, #283, 5 females and 2 males collected 6 March 2008 from egg of Heliconiini  butterfly ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora biflora  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk);

Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #346, 2 females and 1 male collected 20 March 2008 from egg of Agraulis vanillae vanillae  ( Lepidoptera  : Nymphalidae  : Heliconiinae  ) found on Passiflora foetida var. isthmia  ( Malpighiales  : Passifloraceae  ) (coll. J.B. Woelke and M. de Rijk).

Phoretic wasp record. Panama, Pipeline Road, 9°08 ʹ 31.8 ʺ N, 79°43 ʹ 30.6 ʺ W, #32, 1 female wasp was collected on a female Heliconius hecale melicerta  butterfly, 12 February 2008 (coll. J.B. Woelke and M. de Rijk).

Host

Wasps were reared from eggs of Agraulis vanillae vanillae  ( Figure 1View Figure 1 (g,h)) and Heliconiini  spp. found on Passiflora biflora Lamarck  ( Figure 1View Figure 1 (f)) and P. foetida  L. var. isthmia Killip  ( Figure 1View Figure 1 (d)).

Biology

Idiobiont endoparasitoid. All specimens of this species were reared from eggs of Heliconiini  butterflies, which were deposited on Passiflora  plants. The collected wasps had an average of 5.20 ± 3.42 SD females and 1.20 ± 0.45 SD males per egg, and a sexratio of 23.08%. Our finding of one female wasp on an adult female Heliconius hecale melicerta  butterfly ( Figure 1View Figure 1 (i,j)) suggests that this species may occasionally be phoretic on adult female butterflies to find suitable host eggs.

More specific information about strain L20. Female wasps oviposit several eggs into a M. brassicae  host of various ages (fresh and mature with red stripes) ( Figure 5View Figure 5 (a,b)). Both winged and brachypterous females oviposit. Freshly laid egg is ovoid, about 0.12 mm long, and ~ 0.06 mm wide ( Figure 5View Figure 5 (c)). About 24 h after, an embryo is traceable within the egg. The freshly hatched larva is about as long as the egg, with poorly sclerotized mandibles. Forty-eight hours later the larva is already 0.4–0.6 mm long, and has a distinct mid gut full of consumed host yolk ( Figure 5View Figure 5 (d)). About 50 h after oviposition the entire egg is consumed, and larvae reach nearly their final size. Up to 14 larvae can develop in same egg of M. brassicae  ( Figure 5View Figure 5 (e)) The fully grown larva is about 0.7–0.8 mm long, swollen, with full mid gut; occasionally it is reddish with white spots ( Figure 5View Figure 5 (f)). No moult or changes in mandible size were traced during the larval development. The male and female pupae differ in size and colour pattern ( Figure 5View Figure 5 (g)). Host eggs turn black after consumption, as in most Trichogramma  species ( Figure 5View Figure 5 (h)).

Distribution

Panama, tropical lowland rainforest of the Soberania National Park (Parque Nacional Soberanía) ( Figure 1View Figure 1 (c)), and in the town of Gamboa and surroundings.

Etymology

Research was conducted in Soberania National Park (in Spanish: Parque Nacion soberanía  ) in Panama, as well in the town of Gamboa, which is located in this park. The park has been protected since 1980, and covers 220 km 2 of tropical lowland rainforest.

Sequence analysis

MegaBLAST analysis revealed that our Internal Transcribed Spacer 2 (ITS-2) sequences of T. soberania  sp. nov. matched with 37% query cover and 93% identity to T. chilotraeae in GenBank. Sequence  ID T. soberania  sp. nov.: MK159692View Materials.