Nymphalini, Dalman, 1816

Llorente-Bousquets, Jorge, Nieves-Uribe, Sandra & Flores-Gallardo, Adrián, 2023, Exochorion in the tribe Nymphalini (Lepidoptera: Nymphalidae): the genus Hypanartia Hübner, [1821] and comparison with related genera, Zootaxa 5330 (2), pp. 151-200 : 174-188

Description of the ridges in the tribe Nymphalini .

The Nymphalini are characterized by a specific type of colonnaded ridges ( Table 3 , Plates 16–20 ), which are more derived than those found in Coeini ( Campos-González et al. 2020) . They have a low X component (see Plate 2 , Fig. B), leading authors such as Scudder (1889), Döring (1955), and Van Son (1979) to describe them as ‘laminar longitudinal ribs’ ( Table 4 ), without the benefit of a microstructural examination using SEM. Because of their low X component in the vertical Y direction, this type of ridge may be related to those found in certain subtribes of Biblidinae (e.g., Epiphilini, Eubagini ; Nieves-Uribe et al., 2015, 2016d); however, in the latter they are bulkier and more developed. The Nymphalini ridges are not exclusive to the tribe, as the exochorion of Libytheana or Dircenna also exhibits similar-looking laminar ridges (SNU, JLB; pers. obs.). A microstructural examination of the various ridges in the subfamilies and tribes of Nymphalidae is currently in progress.

Regarding the other two spatial directions of the colonnaded ridges (Y and Z axes), we observed variations within the genera of Nymphalini . In some cases, ridges run in the Y direction from the base to a section of the chorion (e.g., Hypanartia bella, Plate 6, Fig. A) or reach the cusp, as in the cases of Mynbrenthia, Symbrenthia , Antanartia ( Plates 16–18 ), Hypanartia lethe ( Plates 8 , 9 , Figs. A, Plates 16–18 ), H. godmanii ( Plates 10 , 11 , Figs. A), Aglais , and Vanessa ( Plates 17 , 18 ). In other cases, the ridges run only from the apex to the apical half of the exochorion (e.g., Hypanartia dione disjuncta , Plates 12 , 13 ; H. trimaculata autumna , Plates 14 , 15 ; Nymphalis , Polygonia , and Aglais , Plates 17 , 18 ).

TABLE 3. (Continued)

The projection of the Z spatial direction (radially outwards from the surface of the egg), remains almost constant from one pole to the other in the genera Mynbrenthia, Symbrenthia , and Antanartia ; the ridge, although not very protruding, is conspicuous and remains similar throughout the chorion ( Plates 17 , 18 ). On the other hand, in Hypanartia , Vanessa , Nymphalis , Polygonia , and Aglais , the Z direction is greater in the apical section, and much reduced towards the base. In these genera, the largest ridges (high Z component) correspond to ridges that run more than half of the chorion in the Y direction. Those ridges that run only to the supra-equatorial half in the Y component have a low projection of the Z component ( Plates 17 , 18 ). Hypanartia lethe and H. godmanii ( Plates 8–11 , 16 , 17 , 18 ) show a slightly higher Z component in their supra-equatorial section, as it is slightly reduced towards the basal region ( Plates 8–11 , 16 ).

An explanation for these patterns in both spatial components could be found in the oviposition habits, since the reduced ridges (low Y and Z components) correspond to oviposition in clusters ( Nymphalis ) or chains ( Polygonia ) ( Tables 3 , 4 ; Scudder 1889, Van Son 1979). This pattern is similar (analogy) to the reduction of the knolls in Hamadryas species with chain oviposition (e.g., H. amphinome , H. fornax ; Nieves-Uribe et al. 2015, 2019). However, further study is needed to determine whether this possibility applies to all cases of reduced ridges (e.g., Hypanartia dione disjuncta , H. trimaculata autumna ).

Thickened ribs at the basal region are visible in Hypanartia ( Plates 4–16 ), while Polygonia , Aglais , and Vanessa lack conspicuous ribs in this section. The genus Nymphalis is the only one, so far known, that exhibits ribs throughout the chorion, albeit subtly ( Table 3 , Plate 17 ).

TABLE 4. (Continued)

TABLE 4. (Continued)

TABLE 4. (Continued)

TABLE 4. (Continued)

TABLE 4. (Continued)

TABLE 4. (Continued)

In colonnades with beams, a wall covers them, which can be so thick that it is difficult to distinguish the ridge components (e.g., Mynbrenthia hippalus , Symbrenthia hippoclus, Plate 17; Hypanartia trimaculata autumna, Plate 15, Fig. B). Alternatively, the intercolumnar wall may be thinner in the intercolumns, resembling windows (e.g., Hypanartia dione disjuncta, Plate 13, Fig. B; Antanartia delius , Nymphalis antiopa , Plates 16–18 ), or just slightly covering them (e.g., Hypanartia bella, Plate 7, Fig. B; H. lethe, Plate 9, Fig. B; H. godmanii, Plate 11, Fig. B; Polygonia g-argenteum , Aglais urticae , Vanessa virginiensis , Plates 17 , 18 ).

The thickness of the ridge wall is related to the distance between the columns, with the thickest walls found where the columns are closest together (Mynbrenthia, Symbrenthia , and Antanartia ; Plates 16–18 ) and the thinnest or translucent walls where the columns are further separated ( Hypanartia , Vanessa , Nymphalis , Polygonia , and Aglais ; Plates 17 , 18 ). There are two subtypes of colonnade arrangements: double and single. In the double subtype, the columns have plinths that protrude alternatively towards one or the other side of the colonnade, resulting in alternate “ribs” on the chorion and small zig-zag aeropyles on a somewhat thick beam ( Plate 19 , Fig. A). In the single subtype, the columns are thick and have protruding plinths on both sides of each column, resulting in coincident “ribs” and large aeropyles aligned in the same row on a beam of thickness, like the diameter of these ( Plate 19 , Fig. B).

The columns in both subtypes have variable girth, which also results in different diameters of the aeropyles. Those of the double subtype have a smaller diameter than those of the single subtype, since the columns in the double subtype are thinner than those in the single one ( Plate 19 ). This is consistent regarding the function of the columns as tubular structures for gas exchange, with the aeropyles at the end of the capitals. When a beam is present, it does not cover the openings and may even have depressions at the aeropyles, forming a wavy ridge (genus Nymphalis , Plates 17 , 18 ) with slight concavities at the aeropyles (genera Hypanartia , Polygonia , and Aglais , Plates 17 , 18 ), to well-marked depressions at these sites ( Vanessa , Plates 17 and 18 ).

Regarding the genus Vanessa , they appear to have the greatest specialization and divergence in the ridges. In the species we studied ( Vanessa virginiensis = Vanessa huntera ; Tables 3 and 4 ; Scudder 1889), the edge of the ridges is jagged. This may be due to the transformation of the beam of the ridges into arches by shortening the shafts of the columns and depressing them in the areas where the aeropyles are found ( Plate 20 ). This change can be considered an optimization of polypeptidic material by providing better column support without a rail, exhibiting thinner intercolumnar walls, and allowing for better attachment of the egg between the pili of the host plant, requiring less adhesive material by the female, as cited by Scudder (1889). A more in-depth study within the genus Vanessa is required to corroborate this hypothesis and to consolidate the separation of the genus concerning the number of ridges, as suggested by Scudder (1889). According to Scudder (1889), the subgenus Pyrameis has only nine ridges, while the subgenus Neopyrameis has 13 to 19.

Figures

PLATE 2. General schemes of the chorion in Hypanartia.A. Regionalization of the chorion in lateral view; B. Three-dimensional model for the ridges in Nymphalinae.

PLATE 4. Chorion of Hypanartia paullus. A. Lateral view; B. Apical view. i=ridge in colonnade; ii=apical columns; iii=twist a zig-zag; iv=vestigial ‘ribs’; v=intercolumnar wall; vi=basal ribs; vii=projections of the ridges towards the transition zone.

PLATE 5. Photographs of the chorion of Hypanartia paullus under the SEM. A Lateral view.; B. Detail of the colonnades; C. Basal region; D. Apical view; E. Perimicropylar region; F. Micropyle.

PLATE 6. Chorion of Hypanartia bella. A. Lateral view; B. Apical view. i=ridges in colonnade; ii=short ridges; iii= apical columns; iv= intercolumnar space; v= ‘falling’ ridges; vi= reduced columns; vii=apical ribs; viii=basal ribs; ix= vestigial ‘ribs’.

PLATE 7. Photographs of the chorion of Hypanartia bella under the SEM. A Lateral view.; B. Detail of the colonnades; C. Basal region; D. Apical view; E. Perimicropylar region; F. Micropyle.

PLATE8. ChorionofHypanartialethe.A.Lateralview;B.Apicalview.i=ridgeincolonnade;ii=apicalcolumns;iii=intercolumnar wall; iv=basal ribs; v=vestigial ribs.

PLATE 9. Photographs of the chorion of Hypanartia lethe under the SEM.A Lateral view.; B. Detail of the colonnades; C. Basal region; D. Apical view; E. Perimicropylar region; F. Micropyle.

PLATE 10. Chorion of Hypanartia godmanii. A. Lateral view; B. Apical view. i=ridge in colonnades; ii= apical columns; iii= apical ribs; iv=basal ribs; v =intercolumnar walls; vi=projections of the ridges in the transition zone.

PLATE 11. Photographs of the chorion of Hypanartia godmanii under the SEM. A Lateral view.; B. Detail of the colonnades; C. Basal region; D. Apical view; E. Perimicropylar region; F. Micropyle.

PLATE 12. Chorion of Hypanartia dione disjunct. A. Lateral view; B. Apical view. i=ridges in colonnade; ii=apical columns longer than equatorial ones; iii=intercolumnar spacing; iv=basal ribs; v=projections of the ridges in the transition zone.

PLATE 13. Photographs of the chorion of Hypanartia dione disjuncta under the SEM. A Lateral view.; B. Detail of the colonnades; C. Basal region; D. Apical view; E. Perimicropylar region; F. Micropyle.

PLATE 14. Chorion of Hypanartia trimaculata autumn. A. Lateral view; B. Apical view. i=ridges in colonnade; ii= apical columns overhanging the surface; iii=reduced ridges (beam only); iv=vestigial ’ribs’; v=intercolumnar spacing; vi=basal ribs; vii= projections of the ridges in the transition zone.

PLATE 15. Photographs of the chorion of Hypanartia trimaculata autumn under the SEM. A Lateral view.; B. Detail of the colonnades; C. Basal region; D. Apical view; E. Perimicropylar region; F. Micropyle.

PLATE 16. Comparative dendrogram of ridges in Hypanartia spp. (redrawn from the cladogram of Willmott et al. 2001). Two species of Antanartia have been added. *=hyper-development of the ridges by elongated fusts.

PLATE 17. Morphology of the complete ridges of eight genera of Nymphalini. Representations in lateral view. The order of the genera is by morphological proximity of the ridges.

PLATE 18. Anatomy of the components of the most apical section of the ridges in eight genera of Nymphalinae. The order of the genera is by morphological proximity of the ridges.

PLATE 19. Arrangement and thickness of columns A. Double arrangement with slender columns and small zig-zag aeropyles. B. Simple arrangement with thick columns, large aeropyles in a straight line.

PLATE 20. Modifications in the beam in the Nymphalini. A. Straight beam; B. Arched beam.