The present report, the second part of a study of the external morphology of Preponini, compares the thorax and thoracic appendages of Archaeoprepona demophon demophon (Linnaeus, 1758), Archaeoprepona licomedes licomedes (Cramer, 1777) and Prepona pylene pylene Hewitson, [1854], through descriptions and illustrations. The results are compared with three other species, Prepona claudina annetta (Gray, 1832), Memphis moruus stheno Hübner, [1819] and Zaretis itys itylus (Westwood, 1850), revealing previously unrecognized similarities among species of Charaxinae.
INTRODUCTION
This is the second contribution to a series of detailed studies on the exoskeletons of Archaeoprepona demophon demophon (Linnaeus, 1758), Archaeoprepona licomedes licomedes (Cramer, 1777), and Prepona pylene pylene Hewitson [1854], The first part consisted of the comparative morphology and analysis of the head, cephalic appendages and cervical sclerite (Bonfantti et al., 2015).
MATERIALS AND METHODS
The material analyzed in this study was the same as that used in the first contribution, as well as for the preparation of body structures and illustrations (Bonfantti et al., 2015). However, the methodology for preparing the wings differs. These were removed and cleared by immersion first in 70% ethanol, then in a sodium hypochlorite (NaOCI) solution until completely cleared, and then again in 70% ethanol to neutralize the action of the sodium hypochlorite, after which they were dried on absorbent paper.
The characters compared are presented in Table 1, together with characters of the other three species: Prepona claudina annetta (Gray, 1832) (Mielke et al., 2004) as a representative of Preponini; and Memphis moruus stheno Hübner, [1819] (Dias et al., 2010) and Zaretis itys itylus (Westwood, 1850) (Mielke et al., 2004), as representatives of Anaeini.
The terminology used follows other morphological studies, such as those of Ehrlich (1958), Casagrande (1979), Mielke et al. (2004), Dias et al. (2010), and Kawahara et al. (2012).
RESULTS
Archaeoprepona demophon demophon (Linnaeus, 1758)
Prothorax. In dorsal view (Fig. 1A), subtriangular pronotum visible. Patagia globular, internally articulated with pronotum; parapatagium sclerotized, elongated, about four times as long as wide, and inserted between membranes.
In lateral view (Fig. 2A), episternum reduced; proepisternum with slight anterior projection. Coxa occupying most of space in lateroventral part of prothorax.
In ventral view (Fig. 3A), proepisternum bilobate. Episternum laterally delimited by patagium between proepisternum and coxal alveolus. Furca originating at base of prothoracic coxae, articulating with spinasternum forming inverted “Y” shape.
Mesothorax. In dorsal view (Fig. 1A), prescutum wide, triangular, occupying whole anterior margin of scutum; latter being subrectangular, medially divided by mesoscutal line. Externally, suralare triangular with apical projection. Scutellum projected, lozenge-shaped with median and anterolateral projections, situated posterior to scutum and separated by mesoscutoscutellar sulcus. In lateral view (Fig. 2A), prealar process elongated and anteroventral to subtegula. Ventrally, basalare subtriangular. Adnotal projecting as long ventral lobe of postalar plate, situated posterior to suralare, and fused to scutum. Subalare narrow and irregularly shaped. Posteriorly, axillary cord originating from postnotum, and projecting over laterophragma. Anepisternum situated ventral to subalare, articulating ventrally to proepisternum; latter being completely separated from katepisternum by preepisternal suture. Epimeron divided into three different parts by dorsal and ventral sutures; anterior sclerite called proepimeron. Basisternum located ventral to proepimeron, articulating with eucoxa and meron.
In ventral view (Fig. 3A), proepisternum narrow. Spinasternum I articulating with basisternum; the latter in turn articulating with proepimeron. In ventral view, meron being the largest of mesothoracic sclerites, separated from eucoxa by coxal suture, delimiting alveolus of trochanter. Discrimen extending longitudinally to basisternum.
Table 1.
Morphological differences among species of neotropical Charaxinae.
Metathorax. In dorsal view (Fig. 1A), metathorax divided into scutum and scutellum, separated by scutoscutellar suture. Scutum medially divided by scutellum, forming two subtriangular areas. Scutellum subtriangular.
Fig. 1.
Thorax, dorsal view; (A) Archaeoprepona demophon demophon (Linnaeus, 1758); (B) Archaeoprepona licomedes licomedes (Cramer, 1777); (C) Prepona pylene pylene Hewitson, [1854], Scale bars: 1 mm.
In lateral view (Fig. 2A), cordate scutum completely separated from suralare by scutal suture; scutellum extending ventrolaterally to form axillary cord, which extends out over notal process of hindwing. Postnotum projected posteroventrally to scutellum. Subalare narrow, located in center of pleural membrane. Sternopleura divided by pleural suture into episternum and epimeron. Episternum divided into three regions, anepisternum, katepisternun, and basisternum. Anepisternum subcircular, lightly sclerotized, and having long setae. Katepisternum elongate, approximately four times as long as wide, and being separated from epimeron by pleural suture. Epimeron divided by dorsal suture.
In ventral view (Fig. 3A), basisternum appearing as subtriangular plate, anterior to metathoracic coxae. Meron separated from eucoxa by coxal suture.
Thoracic appendages. Tegula (Fig. 4A), being protruded, mobile projection of mesothorax, projected at height of subtegula; latter being subtriangular in shape, having laterodorsal projections covering suralare II.
Axillary sclerites (Fig. 5A) articulating wings with thorax through three sclerites. In mesothorax, first axillary II articulating distally with sclerites of second axillary II; latter in turn articulating distally with basal process of subcostal II; third axillary II being in contact with base of anal veins. In metathorax, first axillary III articulating distally with second axillary III; latter in turn articulating with basal process of subcostal vein; third axillary III being in contact with anal veins.
Fig. 2.
Thorax, lateral view; (A) Archaeoprepona demophon demophon (Linnaeus, 1758); (B) Archaeoprepona licomedes licomedes (Cramer, 1777); (C) Prepona pylene pylene Hewitson, [1854], Scale bars: 1 mm.
Forewing (Fig. 6A) subtriangular in both sexes. Outer margin straight, but concave along median third; costal margin convex throughout its length, and inner margin straight; subcostal (Sc) initiating in axillary region, thicker at base, ending along distal third of costal margin; narrow radial (R) appearing along and parallel to Sc; upon reaching end of distal third of discal cell, R forking into R1 and Rs (R2, R3, R4 and R5); R2, R3, and branch of R4 + R5 bifurcating at apex of discal cell soon after this, R3 bifurcating from branch of R4 + R5; R2 ending on costal margin of wing, R3 at apex, and R4 and R5 on outer margin. Final third of R4 curving downward. Veins des and dcm tiny, while dci appearing as nontubular vein. M1 and M2 running separately from upper region of discal cell; M3 separated from M1 and M2 by inferior region of discal cell, together with inferior end of dci. CuA1 and CUA2 being parallel to outer margin, CuA1 originating near base of M3, and CuA2 originating from median third of cubital vein; 2A, only anal vein, being parallel to inner margin, having slight curve at base, leaving axillary region, running separately from discal cell, and reaching anal angle of wing.
Fig. 3.
Thorax, in ventral view; (A) Archaeoprepona demophon demophon (Linnaeus, 1758); (B) Archaeoprepona licomedes licomedes (Cramer, 1777); (C) Prepona pylene pylene Hewitson, [1854], Scale bars: 1 mm.
Fig. 4.
Tegula; (A) Archaeoprepona demophon demophon (Linnaeus, 1758); (B) Archaeoprepona licomedes licomedes (Cramer, 1777); (C) Prepona pylene pylene Hewitson, [1854], Scale bars: 1 mm.
Fig. 5.
Wing sclerites; (A) Archaeoprepona demophon demophon (Linnaeus, 1758); (B) Archaeoprepona licomedes licomedes (Cramer, 1777); (C) Prepona pylene pylene Hewitson, [1854], Scale bars: 1 mm.
In both sexes, hindwing (Fig. 6B) having convex costal margin and straight outer margin; latter having prominent convexity along its median third. Sc + R1 extending from axillary region to apex of wing. Humeral vein (h) curving toward proximal region of costal margin, arising close to separation of Sc + R1 and Rs. Discal cell closed, while dci being nontubular. M1 and M2 arising independently in upper region of discal cell, and M3 being separate from M1 and M2, initiating in lower region of discal cell, with proximal third curved upward. Conformation of veins CuA1 and CuA2 similar to forewing. Anal veins separated from discal cell at their bases, with 2A ending at anal angle of wing; 3A ending in median third of anal margin. In males, odoriferous scales long and projected parallel to veins, originating between CuA2 and 2A.
Prothoracic leg (Fig. 7A, B) atrophied and smallest in relation to others. Tarsus unisegmented in males and pentasegmented in females, both without terminal claw. Coxa elongated, wider at base and gradually narrowing distally. Trochanter subrectangular, and smallest of leg sclerites. Femur and tibia elongated, with approximately the same length. In females, tarsus composed of five tarsomeres, of which proximal longer than others, which have similar lengths and spines at their distal end. Male having single tarsus, which is thin and lacks spines or setae.
Meso- and metathoracic legs (Fig. 7C, D) having similar conformation. Coxae II and III longitudinally divided into eucoxa and meron by coxal suture. Eucoxa and meron II similar in size, whereas meron III about four times larger than eucoxa III. Trochanters II and III irregular in shape. Femurs II and III elongated. Meso- and metathoracic tibiae covered with setae, featuring pair of spurs articulated at inner distal end. Tarsi II and III pentamerous; proximal tarsomere larger than others. Distal portion of distitarsus (Fig. 7E, F) having membranous projected area that contains tarsal claws, pulvilli, and medially placed, rounded, and cushion-like arolium.
Archaeoprepona licomedes licomedes (Cramer, 1777)
Prothorax. In dorsal (Fig. 1B), lateral (Fig. 2B), and ventral (Fig. 3B) views, prothorax having morphological pattern similar to that of A. d. demophon. In A. I. licomedes, parapatagium longer, approximately three times as long as wide; spinasternum subtriangular.
Mesothorax. In dorsal view (Fig. 1B), prescutum broad and lozengeshaped, occupying median portion of anterior margin of hourglass-shaped scutum. Scutellum lozenge-shaped, with median anterolateral projections. Other structures similar to those of A. d. demophon.
Fig. 6.
Wings; (A), (B) Archaeoprepona demophon demophon (Linnaeus, 1758); (C), (D) Archaeoprepona licomedes licomedes (Cramer, 1777); (E), (F) Prepona pylene pylene Hewitson, [1854]; (A, C, E) forewing, (B, D, F) hindwing. Scale bar: 1 mm.
Fig. 7.
Archaeoprepona demophon demophon (Linnaeus, 1758); (A) prothoracic leg, males; (B) prothoracic leg, female; (C) mesothoracic leg; (D) metathoracic leg; (E), (F) distitarsus; (E) lateral view, (F) ventral view. Scale bars: 1 mm.
In lateral (Fig. 2B) and ventral (Fig. 3B) views, mesothorax having same morphological pattern as in A. d. demophon, except for subquadrangular basalare, proepisternum being partially divided from katepisternum by pre-episternal suture, and discrimen extending to furcal pit.
Metathorax. In dorsal (Fig. 1B), lateral (Fig. 2B), and ventral (Fig. 3B) views, conformation being virtually identical to that of A. d. demophon, although only scutellum III having trapezoidal shape and katepisternum being longer, about five times as long as wide.
Thoracic appendages. Tegula (Fig. 4B), axillary sclerites (Fig. 5B), and legs (Fig. 8A–F) having morphological characteristics similar to those of A. d. demophon. In thoracic appendages, these two species differing in venation of forowing (Fig. 6C), such as the bifurcation of R1 and Rs (R2, R3, R4 and R5) at the end of the median third of the discal cell, and the bifurcation of R2 and R3, R4 + R5 at the distal third of the discal cell; although hindwing (Fig. 6D) similar to that of A. d. demophon.
Prepona pylene pylene Hewitson, [1854]
Prothorax. In dorsal (Fig. 1C), lateral (Fig. 2C), and ventral (Fig. 3C) views, prothorax having morphological pattern similar to that of A. d. demophon and A. I. licomedes, although parapatagium being narrow, about seven times as long as wide, and spinasternum being subtriangular.
Mesothorax. In dorsal view (Fig. 1C), prescutum small, triangular, occupying median portion of anterior margin of scutum; latter being subrectangular, having bulged outer margin; scutellum semicircular, having anteromedian salience. Other structures similar to those of A. d. demophon and A. I. licomedes.
In lateral (Fig. 2C) and ventral (Fig. 3C) views, mesothorax having the same morphological pattern as A. d. demophon and A. I. licomedes, except for basalare being elongated; proepisternum completely separated from katepisternum by preepisternal suture; epimeron with laterally projected lobe; and discrimen extending to furcal pit.
Metathorax. In dorsal view (Fig. 1C), morphological pattern similar to that of A. d. demophon and A. I. licomedes, except for medially narrowed scutum and elongated scutellum.
In lateral (Fig. 2C) and ventral (Fig. 3C) views, metathorax similar to that of A. d. demophon and A. I. licomedes, except for subtriangular scutum; elongated scutellum and katepisternum being twice as long as wide; epimeron as single sclerite, therefore without divisions; and transverse inclination of coxal suture.
Thoracic appendages. Tegula (Fig. 4C), axillary sclerites (Fig. 5C), and legs (Fig. 8G–L) having morphology similar to A. I. licomedes. Forewing (Fig. 6E) similar to that of
Fig. 8.
Archaeoprepona licomedes licomedes (Cramer, 1777); (A) prothoracic leg, males; (B) prothoracic leg, female; (C) mesothoracic leg; (D) metathoracic leg; (E), (F) distitarsus; (E) lateral view, (F) ventral view. Prepona pylene pylene Hewitson, [1854]; (G) prothoracic leg, males; (H) prothoracic leg, female; (I) mesothoracic leg; (J) metathoracic leg; (K), (L) distitarsus; (K) lateral view; (L) ventral view. Scale bars: 1 mm.
A. d. demophon. Among thoracic appendages, differences include hindwing (Fig. 6F) in form and arrangement of odoriferous scales, latter being short and perpendicular to venation.
DISCUSSION
As expected, the thorax and appendages have several interesting features. Among these is the mesothoracic prescutum, which is well developed in Archaeoprepona, occupying at least half of the anterior margin of the scutum II, in addition to the metathoracic epimeron divided into two distinct sclerites, and the shape of the scutum III. All these characters can be easily observed and are useful in the diagnosis of this genus. This contrasts with the head and appendages, which in the first part of this study (Bonfantti et al., 2015) proved to show no morphological patterns useful in distinguishing as the thorax.
The two genera, Archaeoprepona and Prepona, showed quite similar morphological patterns for this tagma. As in the first part of this study (Bonfantti et al., 2015), the individual species with the most distinct morphological pattern was Prepona p. pylene. This species differs in having the semicircular scutellum II, a medially narrowed scutum III, and a lobe on the epimeron II, which can easily be observed with the specimen in ventral view, without the need for specimen dissection or damage.
Even with so many similarities, the odoriferous scales have different conformations among the species of Archaeoprepona Fruhstorfer, 1915 and Prepona Boisduval, 1836, and can be widely used as a diagnostic character for the genera. Although these scales are located in the same region, on the dorsal surface of the posterior wing of males between veins CuA1 and 2A, Archaeoprepona has long scales oriented parallel to the venation, while Prepona has short scales oriented perpendicular to the venation.
The thorax in Lepidoptera is relatively unexplored for use in higher-level taxonomy, although it has great importance in the characterization of species (Leite et al., 2010). For Charaxinae, this tagma deserves attention considering that it is where most synapomorphies among adults are concentrated, all of which were corroborated in this study. Moreover, this tagma may show some very interesting characters for diagnosis of Preponini, which should be analyzed in the future in a phylogenetic context to test whether they are synapomorphies for this group, as besides being easily observable, they are well established among other species of this tribe that were not analyzed in this study. One of these characters, the dci vein of the forewing, was shown to be of a nontubular type, differing from what was previously reported for Charaxinae, where only the dci vein of the hindwing was nontubular. Further important characters include the divisions of the mesothoracic epimeron into three distinct sclerites, by the dorsal and ventral sutures; the wing venation, which is generally similar; and the consistent presence of odoriferous scales on the wings of males. The thorax and appendages in general showed several characters that are important for the diagnoses of genera and tribes. Use of these characters will aid in advancing understanding of the phylogeny of these groups. The abdomen, examined in the third and last part of this study, will provide further important characters for understanding the morphological pattern as a whole.
ACKNOWLEDGMENTS
We thank the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (Capes) and the Brazilian Research Council-CNPq for financial support. Dr. Janet W. Reid edited the English text.
