Graptocleptes bicolor (Burmeister 1838)

Gil-Santana, Hélcio R., Davranoglou, Leonidas-Romanos & Neves, Juliana A., 2013, A new synonymy of Graptocleptes bicolor (Burmeister), with taxonomical notes (Hemiptera: Heteroptera: Reduviidae: Harpactorinae: Harpactorini), Zootaxa 3700 (3), pp. 348-360 : 349-359

Graptocleptes bicolor (Burmeister 1838)

Myocoris bicolor Burmeister, 1838: 107 [description]; Walker, 1873b: 131 [catalog]; [description].

Eccagoras [sic] nigricornis Stål, 1855: 189 [description].

Evagoras nigricornis ; Stål, 1866: 295 [as synonym of Myocoris bicolor Burm. ].

Amaurosphodrus bicolor ; Stål, 1866: 295 [as a species of the genus].

Hiranetis bicolor ; Stål, 1859: 371 [citation]; Stål, 1860: 77 [citation].

Euagoras nigricornis ; Stål, 1872: 82 [as synonym of Graptocleptes bicolor Burm. ]; Walker, 1873b: 118 [citation as a valid species]; Lethierry & Severin, 1896: 179 [catalog as var. of Graptocleptes bicolor ].

Graptocleptes bicolor ; Stål, 1872: 82 [redescription]; Berg, 1879: 148 [citation from Uruguay]; Lethierry & Severin, 1896: 179 [catalog]; Wygodzinsky, 1949: 39 [catalog]; Maldonado, 1990: 204 [catalog].

Reduvius coleopteroides Walker, 1873a: 203 [description]; Lethierry & Severin, 1896: 118 [catalog, as species incerti generis], NEW SYNONYM

Hiranetis coleopteroides ; Distant, 1903: 246 [new combination]; Wygodzinsky, 1949: 40 [catalog]; Maldonado, 1990: 218 [catalog], NEW SYNONYM

PLATE 2. Figs. 7–14, Graptocleptes bicolor (Burmeister) , male, 7–13, specimens from São Paulo state, Brazil, 7, dorsal view, 8–9, head, 8, dorsal view, 9, lateral view, 10, second antennal segment, detail, lateral view, 11–12, head and pronotum, dorsal view, 13, right hemelytra and hind wing, 14, specimen from Paraguay, head and pronotum, dorsal view.

PLATE 3. Figs. 15–21, Graptocleptes bicolor , male genitalia, 15–16, pygophore, 15, ventral view, 16, lateral view, 17, paramere, 18–21, phallus, 18, latero-ventral view, 19, dorsal view, 20–21, with endosoma completely inflated, lateral view, the arrow points to an expansion of conjunctiva, 20, specimen from São Paulo state, Brazil, 21, specimen from Paraguay.

RedescrIptIon. Male (Figs. 2–3, 7–35): Dimensions, Tables 1 and 2. ColoratIon: General coloration black (Figs. 2– 3, 7); head, including eyes and antennae black (Figs. 2–3, 7–9, 11–12); neck entirely red (Figs. 8–9, 12) or darkened at sides; anterior pronotal lobe reddish, somewhat darkened to brownish red in a few specimens (Figs. 2–3, 7, 11–12); posterior pronotal lobe black or with reddish suffusion of varying extent (Figs. 2–3, 7, 11–12); scutellum red or variably darkened to entirely blackish (Figs. 11–12, 14); meso- and metasternum brownish-red or blackish; the latter usually brighter, when not all black. In the male from Paraguay, the head, excluding eyes, ocellar bases and antennae, and thorax are almost completely red (Fig. 14), with distal segments of rostrum somewhat brownish. Hemelytra black or dark brown, with a yellow spot on external and mid-distal portions of corium, reaching adjacent part of membrane, mainly in basal portion of distal cell of membrane (Figs. 1–2, 7, 13); hind wing mostly brownish-black, with bright areas at basal third and in lines parallel to veins (Fig. 13); fore femur black, brown, and with a faint incomplete yellowish middle annulus in the specimen from Paraguay; mid and hind femora black, brownish in the specimen from Paraguay, with a yellowish annulus, this is narrower, sometimes almost imperceptible and median in mid femur and larger, much brighter and somewhat distal to median portion of the segment in hind femur (Fig. 7); tibia and tarsi black, brownish in the specimen from Paraguay; sternites mostly reddish, with two or three distal segments variably darker to blackish, including spots or darkened markings in the more proximal reddish segments; connexivum almost completely reddish, variably darkened in the distal segments as well.

HEAD (Figs. 8–12, 14): elongate, integument shiny, with sparse long and several short and straight blackish hairs, denser in posterior lobe of head; gula strongly curved, covered with dense, moderately long pubescence; clypeus straight; postantennal spines blunt, tuberculiform; eyes globose, projecting laterally; transverse sulcus well marked; ocelli elevated, much closer to eyes than to each other; labium with shiny integument, with sparse straight blackish hairs and setae, the latter denser and brighter on apical portion of last segment; segment II (first apparent), thickest, straight, reaching posterior margin of eyes; segment III somewhat curved; segment IV triangular, tapering, almost reaching fore coxae; neck shiny, glabrous. Antennal segments blackish, first two segments shiny and straight; segment I the longest segment with sparse moderately long blackish hairs; segment II with sparse moderately long and several shorter straight blackish hairs, as well as trichobothria, numbering ten in a specimen examined after clarification (Fig. 10); segments III and IV opaque, covered with short adpressed hairs, and some sparse moderately longer curved ones; segment III somewhat thicker in first third and somewhat curved to distal middle; segment IV straight, with blunt apex.

THORAX (Figs. 7, 11–14): pronotum: anterolateral angles pronounced, rounded, diverging laterally; midlongitudinal sulcus shallow anteriorly, deep distally; transverse sulcus well defined; pronotum with shiny integument, margins of anterior lobe covered by dense, short blackish setae; in the disc, these setae sparser; anterior portion of posterior lobe with sparse, short setae, forming a midlongitudinal line in the hind lobe, where these setae are brighter, yellowish to whitish; disc smooth, with faint horizontal depression across humerus; humeral angles rounded, their margins slightly raised; humeral angles rounded; propleurae with acetabula produced laterally; stridulitrum attaining fore coxa; pleurae with blackish hairs, and small groups of adpressed whitish large setae on superior portion of mesopleura in some individuals; meso- and metasternum with patches of white wax, with whitish setae between coxae in few specimens; meso- and metaepisternum with whitish hairs. Scutellum subtriangular, apex blunt; acute in one specimen, with a few hairs in the central portion, reddish-brown or more darkened; sometimes with midlongitudinal line of whitish setae on approximately the first third, this is a continuation of the line of whitish setae on hind lobe. Legs: slender and elongate; coxae globose, slightly constricted apically; trochanters almost quadrangular; coxae and trochanters ventral with fine whitish hairs; femora thickened basally, mostly in fore and mid pairs, with sparse long straight blackish hairs; fore and mid femora with dense erect brush-like whitish setae ventrally; fore tibia with dense erect brush-like whitish setae ventrally, and small apical spur on anterior side of segment; all tibiae with sparse long straight blackish hairs too, and numerous erect setae, denser towards apex and in fore and mid tibiae. Tarsi three-segmented, densely setose, mainly on ventral surface. Hemelytra long, surpassing abdomen by about half length of membrane; corium covered with dense darkened bristle-like setae; cells and nervures of hemelytra and hind wing as Fig. 13. Abdomen: elongate; sternites with integument shiny with long whitish hairs; small patches, with variable dimensions, of whitish short setae on midlateral portions of first sternites in some specimens.

MALE GENITALIA (Figs. 15–35): Pygophore blackish or brownish, with blackish hairs, longer in lateral portions, subpentagonal in ventral view (Figs. 15–16); with a rounded basal protuberance and subtriangular rounded apex (Figs. 15–16). Parameres blackish, symmetrical, elongated, with elongated blackish hairs on lateral margin and apex, where three or four elements are longer (Fig. 17). Phallus simple (Figs. 18–21); articulatory apparatus moderately short; with somewhat rounded arms (Figs. 19, 22, 25), or subsquared arms, these are more sclerotized (Fig. 23); dorsal phallothecal sclerite variably sclerotized, struts simple (Figs. 19, 26–27). After endosoma expansion, in two males, a conical projection of conjunctiva was observed at the apex (Fig. 20), whereas in the specimen from Paraguay, a similar conical projection of the conjunctiva is dorsal between endosoma processes and the apex of the phallothecal sclerite (Fig. 21); conjunctiva finely spiculose (Fig. 31). Among endosoma processes, in addition to diffuse basal thickening, a small, ventral, curved, and somewhat sclerotized process (Fig. 28) was followed, just above it, by another pair of small few sclerotized subrectangular processes (Fig. 28). These latter were subapical in one male (Fig. 28), apical in the male from Paraguay (Fig. 29), and apico-dorsal in another two males, in which these processes were dorsally located in relation to a group of numerous triangular, sclerotized processes (Fig. 30). These triangular processes could be better observed, after full endosoma expansion in the specimen in which they are located alone in the apex (Figs. 32–35). In the specimen from Paraguay, this group of triangular sclerotized processes was subapical.

PLATE 4. Figs. 22–29, Graptocleptes bicolor , male genitalia, 22–25, articulatory apparatus, dorsal view, 24–25, details, 26– 27, dorsal phallothecal sclerite and struts, 28–29, endosoma, dorsal view, 28, middle portion with paired processes, 29, apical paired processes in the specimen from Paraguay.

PLATE 5. Figs. 30–35, Graptocleptes bicolor , male genitalia, 30, paired processes in other specimen, 31, conjunctiva, detail, 32– 35, apex, dorsal view, 33–34, endosoma expanded, 35, triangular, sclerotized processes.

Female (Figs. 5–6, 36–39): Dimensions (in mm): Tables 3 and 4 .

Generally, like the male albeit somewhat bigger, including the variation with head coloration (excluding eyes, ocellar basis, and antennas), and thorax orange-red to reddish (Figs. 6, 36–38); antennal segment III somewhat thinner in portion of maximum width of segment. Abdomen also somewhat more enlarged.

MaterIal examIned: Reduvius coleopteroides Walker, TYPE , [no geographic data], 1 female, “69. Reduvius coleopteroides ,” “ Type ” [green circle label], “521” [BMNH]. Graptocleptes bicolor (Burmeister) : BRAZIL, [no locality data], 1 female, “Royal Brazil,” handwritten, “ Amaurosphodrus,” handwritten, Distant Coll., 1911-383, printed [BMNH]; [no locality data], 1 female, 20.II. [1]927, “Museu Nacional,” “ Brasil,” A. M. Parko [leg.], “ Hiranetis coleopteroides Walker ”, N. C. E. Miller det. 1951 [MNRJ]; São Paulo, PIracIcaba, 7 females, 7 males, 2012, reared by J. A. Neves, in “Laboratório de Ecologia de Insetos” [ESALQ], descendants from a female specimen collected in a corn field at the experimental “Areão Farm”, ESALQ, 22° 41, 716’ S – 47° 38, 478’ W, 520–600 m, III. 2011 [MNRJ]; PARAGUAY, Choré, 1 male, 25.II.2009, Cotton Plantation, Pierre Silvie leg.[MNRJ].

NOTES ON DISTRIBUTION: G. bicolor has been recorded from Brazil (Burmeister, 1838). However, the only detailed geographical data were given by Stål (1855, 1860, 1872), for the states of Minas Gerais and Rio de Janeiro. Berg (1879) collected this species in eastern Uruguay.

NEW RECORD: Paraguay.

NOTES ON ECOLOGY - BIOLOGY: Under natural conditions, a female of G. bicolor was found inside a corn field without information on the prey of this species. The offspring and adults were reared in the laboratory and fed with larvae of Spodoptera frugiperda (Smith, 1797) ( Lepidoptera : Noctuidae ) (Fig. 39), at different stages of development, as well as with larvae of other unidentified lepidopteran species. The only observed copula occurred in a dorsoventral position. Fertile eggs were laid together, displaying a round-shaped clutch. On the other hand, it was observed that females of G. bicolor also laid eggs without fertilization, but these latter were laid in a scattered manner, without showing a normal clutch shape. Five instars were observed before emergence of the adults. These are preliminary observations, and a complete description of the immature forms and biological data will be the subject of a future paper.

Burmeister (1838) described Myocoris bicolor based on specimens from Brazil (Figs. 1–4). After some taxonomical changes as recorded above, and its inclusion in Graptocleptes by Stål (1872), the species has remained included in this genus ever since (Lethierry & Severin, 1896, Wygodzinsky 1949, Maldonado 1990).

Eccagoras [= Euagoras ] nigricornis Stål, 1855 , described as from “Minas Geraes” [now the state of Minas Gerais], Brazil, was recognized as a junior synonym of G. bicolor by C. Stål himself (Stål 1866, 1872). The description (Stål 1855) and photos of the holotype of E. nigricornis are concordant with the idea that these two taxa are identical. The photos of the syntype of E. nigricornis have been made available by the Swedish Royal Natural Museum (Naturhistoriska Riksmuseet, NHRS), and can be freely accessed at http://www2.nrm.se/en/het_nrm/n/ graptocleptes _ nigricornis .html.

Walker (1873a) based his description of R. coleopteroides on a single female specimen, erroneously thought to be male, without any reference to geographical data, which is also missing from the labels attached to the holotype (Fig. 5). This author, in the next part of his catalogue (Walker 1873b), cited Myocoris bicolor Burmeister as a valid species, but as a “desiderata,” or species that it would be “desirable to procure for the collection” as can be inferred by the convention of absence of letters, as explained in the preface, thus denoting that he was unaware that they were conspecific.

PLATE 6. Figs 36–39, Graptocleptes bicolor , female, 36–37, head, 36, dorsal view, 37, lateral view, 38, specimen determined as “ Amaurosphrodus ” by W. L. Distant deposited in BMNH, head and prothorax lateral view, 39, alive, feeding on a caterpillar.

Hiranetis Spinola, 1840 and Graptocleptes Stål, 1866 are two closely related genera (Champion 1898), which together with certain other Harpactorini have been recognized as Müllerian wasp mimics, using various Ichneumonidae and Braconidae as models (Champion 1898, Haviland 1931, Hogue 1993, Maldonado & Lozada 1992). The resemblance resulting from this mimicry has led to misidentification of these two genera, as shown in the present case.

In G. bicolor , variable extent of reddish coloration on the pronotum was recorded here (Figs. 2–3, 6, 7, 11–12, 14, 38–39). Reddish coloration in the sternal area of the thorax and trochanters was recorded in the original description (Burmeister 1838), but the coloration of the thoracic sterna in the specimens examined here was variable, going from entirely reddish to brownish-red and to black in the other specimens. The variation of the extent of the reddish to blackish coloration was also noticed in the head (except for the ocellar bases, eyes, and antennae) (Figs. 6, 8–9, 14, 36–38) and thorax, including the scutellum, distal sternites, and connexivum. Significant color variation has been recorded in other Graptocleptes species as well (Champion 1898).

Stål (1872) recorded a variation of the coloration of the corium of hemelytra, describing it as either paler (“Var. b. - pallidior ”) or completely blackish (“bb. Corio toto nigricante ”)

Males of Graptocleptes can be recognized by their large prominent eyes and the thickened third antennal joint (Champion 1898). Otherwise, regarding G. bicolor , no sexual dimorphism of eyes size was described by Stål (1872) - “ oculis (…) in utroque sexus aeque prominulis. ”

Although more specimens should be examined in order to confirm these results, the sexual dimorphism of G.

bicolor was shown in the specimens examined here to be subtle. Thus, it possibly might go unnoticed in a rapid viewing of specimens. The third antennal segment is slightly thicker in males, whose maximum width of this segment measured 0.18–0.21 mm (min. – max.); in females, it was 0.13 – 0.15 mm ( Tables 1–2 , 3 ). The eyes may seem somewhat larger in males, when comparing separately some specimens of each sex (Figs. 8–9, 36–37). In fact, the measurements of the transverse width of the right eye in dorsal view showed higher values in males (0.35– 0.75 mm: min. – max.) than in females (0.30–0.45 mm), but the range of 0.35–0.45 mm was found in both sexes, so no differences in the respective specimens could be seen, as observed by Stål (1872). In the specimens from the state of São Paulo ( Tables 1 , 3 ), the antennal segments I and II were longer in females, with minimum lengths greater than the maximum lengths of the same segments in males; whereas the antennal segments III and IV are longer in males than in females. However, in the other two females from the BMNH, the lengths of the antennal segments I and II are within the range of those of males from São Paulo; the other segments are missing, thus not allowing further comparison. On the other hand, in the male from Paraguay, the third antennal segment was shorter than in all other specimens. Therefore, more specimens need to be examined, in order to clarify these possible sexual differences.

Lent & Jurberg (1985) studied the male genitalia of specimens of Triatoma dimidiata (Latreille, 1811) (Triatominae) from diverse origins, and pointed out that the same variability noticed in its external color characters and in the relationship between the head and pronotum was demonstrated by structures of the phallus such as the endosoma processes, struts, phallosoma, and vesica. On the other hand, in Triatoma infestans (Klug, 1834) , a species with “stable external characters” (Lent & Jurberg 1985), the dissection of the male genitalia of specimens from different regions or populations showed only a small variability in struts and endosoma processes (Lent & Jurberg 1985; Pires et al. 1998).

Because the dissection of the male genitalia is usually carried out on only one specimen of each species (Lent & Jurberg 1985), the variability of these structures may remain unrecorded. Therefore, in future studies, and particularly in relation to species in which a color or morphological variation is evident, dissection should be performed on more than one specimen of each species, in order to ascertain the possible male genitalia variability, as recorded in the phallic structures of G. bicolor in the present study (Figs. 20–23, 26–30).

The main characteristics that separate Hiranetis and Graptocleptes , according to Stål (1872) and Maldonado & Lozada (1992), are the following:

1— Hiranetis : Head gibbous, densely pilose; postantennal spine absent; legs elongated, slender; fore femur subequally longer than head and pronotum together and clearly thicker basally than apically. 2— Graptocleptes : Head 1.3 times as long as wide across eyes, sparsely pilose; postantennal spine straight, semivertical; legs less elongated, thicker; fore femur shorter than head and pronotum together and of uniform thickness.

Although the characteristics considered by these authors seem to be concordant with the inclusion of Myocoris bicolor Burmeister in Graptocleptes , a revision of Hiranetis , Graptocleptes , and other allied genera and their species needs to be done taking a phylogenetic approach in order to clarify the systematics of the entire group.

Tables

TABLE 1. Measurements (mm) of male specimens (N = 7) of G. bicolor from São Paulo State.

	Mean	SD	Maximum Minimum
Length to tip of abdomen	11.4	0.57	12.1 10.6
Length to tip of hemelytra	14.5	0.75	15.3 13.1
Head length	1.78	0.08	1.90 1.70
Anteocular portion	0.67	0.08	0.80 0.55
Postocular portion	0.48	0.05	0.55 0.40
Head width across eyes	1.52	0.09	1.65 1.40
Interocular distance	0.79	0.05	0.85 0.70
Transverse width of right eye	0.55	0.19	0.75 0.35
Antennal segment I	3.80	0.17	4.00 3.50
Antennal segment II (n=6)	1.08	0.09	1.20 1.00
Antennal segment III (n=5)	5.96	0.27	6.40 5.70
Antennal segment IV (n=2)	1.62	0.11	1.70 1.54
Max. width ant. seg. III (n=6)	0.19	0.015	0.21 0.18
Labium segment II	1.28	0.08	1.45 1.20
Labium segment III	0.76	0.05	0.85 0.70
Labium segment IV	0.38	0.02	0.40 0.35
Pronotum fore lobe length	0.82	0.07	0.90 0.70
Pronotum hind lobe length	1.59	0.07	1.70 1.50
Pronotum maximum width	2.72	0.12	2.90 2.50
Scutellum length	1.20	0.17	1.50 1.00
Forefemur	3.76	0.12	3.90 3.60
Foretibia	4.15	0.12	4.30 4.00
Foretarsus (n=6)	0.62	0.05	0.70 0.60
Midfemur	2.94	0.15	3.10 2.70
Midtibia	3.85	0.12	4.00 3.60
Midtarsus	0.59	0.06	0.70 0.50
Hindfemur	4.30	0.12	4.10 4.50
Hindtibia	5.84	0.42	6.20 5.00
Hindtarsus	0.65	0.04	0.70 0.60
Abdomen length	6.06	0.28	6.40 5.70
Abdomen max. width	3.01	0.38	3.50 2.50

TABLE 3. Measurements (mm) of female specimens (N = 7) of G. bicolor from São Paulo State.

	Mean	SD	Maximum Minimum
Length to tip of abdomen	13.5	0.65	14.3 12.7
Length to tip of hemelytra	16.5	0.87	17.5 15.3
Head length	1.91	0,0 7	2.02 1.80
Anteocular portion	0.77	0.08	0.90 0.66
Postocular portion	0.49	0.09	0.60 0.30
Head width across eyes	1.62	0.09	1.75 1.45
Interocular distance	0.84	0.04	0.90 0.80
Transverse width of right eye	0.39	0.04	0.45 0.30
Antennal segment I	4.42	0.16	4.60 4.20
Antennal segment II	1.46	0.07	1.60 1.40
Antennal segment III (n=5)	5.77	0.23	6.00 5.45
Antennal segment IV (n=5)	1.38	0.17	1.50 1.10
Max. width ant. seg. III (n=5)	0.14	0.008	0.15 0.13
Labium segment II	1.37	0.08	1.50 1.30
Labium segment III	0.85	0.09	1.00 0.70
Labium segment IV	0.42	0.06	0.50 0.35
Pronotum fore lobe length	0.90	0.03	0.95 0.85
Pronotum hind lobe length	1.85	0.07	2.00 1.80
Pronotum maximum width	3.25	0.16	3.50 3.00
Scutellum length	1.47	0.09	1.60 1.30
Forefemur	4.02	0.23	4.50 3.80
Foretibia	4.55	0.20	4.80 4.20
Foretarsus (n=5)	0.60	0.06	0.65 0.50
Midfemur	3.22	0.18	3.60 3.10
Midtibia	4.21	0.29	4.80 3.90
Midtarsus	0.60	0.07	0.65 0.50
Hindfemur	4.75	0.09	4.90 4.65
Hindtibia	6.67	0.36	6.95 6.10
Hindtarsus	0.67	0.07	0.80 0.60
Abdomen length	7.48	0.48	7.90 6.70
Abdomen max. width	3.93	0.25	4.35 3.60

TABLE 4. Measurements (mm) of female specimens.

Length to tip of abdomen	Female deposited in MNRJ 11.5	Reduvius coleopteroides Typus 13.28	Specimen identified as “ Amaurosphrodus ” by W. L. Distant 12.45
Length to tip of hemelytra Head length Head width across eyes	14.0 1.80 1.45	14.94 1.83 1.48	14.94 1.66 1.32
Interocular distance Antennal segment I Antennal segment II	0.70 Abs. Abs.	0.72 3.8 1.2	0.72 3.8 1.12
Antennal segment III Antennal segment IV Labium segment II	Abs. Abs. 1.3	Abs. Abs. 1.3	Abs. Abs. 1.2
Labium segment III Labium segment IV Pronotum fore lobe length	0.8 0.35 0.90	0.84 0.4 0.96	0.8 0.38 0.92
Pronotum hind lobe length Pronotum maximum width Forefemur	1.65 2.75 3.70	1.80 2.96 3.5	1.8 2.88 3.32
Foretibia Foretarsus Midfemur	3.95 Abs. 2.80	4.0 0.68 Abs.	3.74 0.45 2.8
Midtibia Midtarsus Hindfemur	3.80 Abs. Abs.	Abs. Abs. 4.15	3.32 0.4 4.10
Hindtibia Hindtarsus Abdomen length	Abs. Abs. 6.70	5.15 0.6 6.23	5.0 0.5 6.6
Abdomen max. width	2.70	3.32	3.16
DIscussIon