Hemiceratoides, Strand, 1911, Strand, 1911

Zilli, Albelto, Balbut, Jélôme, Dolwald, Leejiah J. & Lees, David C., 2024, The bild teal-dlinking moths of the genus Hemiceratoides (Lepidoptela: Elebidae), Zoological Journal of the Linnean Society 202 (4), pp. 1-22 : 5-9

RESULTS

Molecular analysis

Both unpartitioned (PHYML 3.0) and partitioned analyses (MrBayes, IQTree) produced an identical topology, and addition of terminals with COI -only data for the same 6890 nucleotide alignment had no effect on that topology. On the basis of our analyses, the genus Hemiceratoides emerges supported [posterior probability (PP) = 1 for MrBayes, bootstrap = 79% for PHYML] as sister to Eudocima ( Fig. 3 ). Three species of Hemiceratoides have so far been DNA barcoded, one of which ( H. sittaca ) benefits also from nuclear genes, but the topology of the genus remains a polytomy, which is not surprising as only DNA barcode data unite all of them. Hemiceratoides + Eudocima are supported via MrBayes (PP = 1, bootstrap = 79%) and IQTree (PP = 1, ultrafast bootstrap = 91%; results not shown), although submarginally by ML bootstrap in PHYML (59%) as sister to other Calpini, i.e. the Neotropical genus Gonodonta Hübner, 1818 + ( Calyptra + ( Plusiodonta Guenée, 1852 + Oraesia )). Calpini is monophyletic (PP = 1, bootstrap = 87%) and Phyllodini is also supported (PP = 1, bootstrap = 72%, ultrafast bootstrap = 93% for IQTree) as sister to all other Calpinae , thus in agreement with Zahiri et al ’.s (2012) arrangement of the three tribes (albeit there with 78% bootstrap and no Bremer support) instead of Zaspel et al.’s (2012) topology which has Phyllodini sister to Ophiderini. Our tree was rooted graphically with Hypocalinae (Hypsoropha hormos Hübner, 1818 + two species of Hypocala Guenée, 1852 ) as the outgroup (Hypocalinae are recovered as monophyletic), with respect to which all Calpinae are also monophyletic (PP = 1, bootstrap = 100%; ML bootstrap = 99% and PP = 1 in Zaspel et al. 2012).

Larval morphology

The pictures of the caterpillar of one new species of Hemiceratoides described here below show a greenish larva with a fairly typical Calpinae habitus, looping the anterior part of the trunk ( Fig. 2A–C ). Fully developed prolegs are present on A3. The development of most anterior prolegs is a highly variable feature in Calpinae (commonly also the pair on A4), being sometimes inconstant even within a single genus or between larval instars of a same species. More noteworthy is the presence of paired subdorsal ringed eyespots on A2, a trait hitherto known only in Ophiderini and, at least in the early instars, some Phyllodini, but not in Calpini, which would also support the exclusion of Hemiceratoides from the last tribe.

Taxonomy

Hemiceratoides Strand, 1911

Hemiceratoides Strand, 1911 . Fauna exotica—Mitteilungen aus dem Gebiete der exotischen Insektenwelt 1 (11): 42. Type species: Hemiceras hieroglyphica Saalmüller, 1891 , by original designation.

= Cynisca Fawcett, 1918 , synon. nov. Proceedings of the General Meetings for Scientific Business of the Zoological Society of London 1917 (3/4): 240. Preoccupied by Cynisca Gray, 1844 (Reptilia). Type species: Cynisca thisbe Fawcett, 1918 , by original designation.

= Siccyna Nye, 1975 , synon. nov. The Generic Names of Moths of the World 1: 449. Replacement name for Cynisca Fawcett, 1918 nec Gray 1844.

Taxonomic remarks: Cynisca thisbe Fawcett, 1918 , whose currently valid name is Siccyna thisbe ( Fawcett, 1918) , is the type species of the genus Siccyna Nye, 1975 (= Cynisca Fawcett, 1918 nec Gray, 1844) ( Nye 1975). Despite the obvious ‘calpine’ features of its habitus, Cynisca thisbe has never been considered in recent works dealing about the tribe Calpini or subfamily Calpinae . Its study unambiguously reveals the presence of the same specialized structures occurring both in the proboscis and genitalia of Hemiceratoides Strand, 1911 ( Fig. 4A, B ), so that these generic names are here brought into synonymy.

Poole (1989) combined with Syccina a second species, namely S. reichi ( Gaede, 1940) , originally described under Cynisca by Gaede (1940 in 1939–40: 333, who also planned a figure on plate 43, row c, but no plates of Gaede’s work beyond no. 41 have ever been published). Examination of a specimen identified as C. reichi by Max Gaede himself (in SMNF) and especially of pictures of the female holotype of C. reichi by courtesy of Théo Léger and Viola Richter ( MNKB) clearly reveals this taxon to be conspecific with another one that had previously been described by Walker ([1858]), so that the following synonymy is here established: Devena atomifera Walker [1858] = Cynisca reichi Gaede 1940 (currently in Siccyna Nye, 1975 ) synon. nov..

Devena atomifera , presently known from Sierra Leone, Liberia, Cameroon, Democratic Republic of the Congo, and Malawi, is unrelated to Hemiceratoides and, following dissections of a male and a female, there is no morphological rationale currently purporting its placement in Calpinae . We comment here on a partial DNA barcode sequence for Devena atomifera from ‘NGS failure tracking’ (468 bp in two non-overlapping segments, at the 5 ʹ end 325 bp and at the 3 ʹ end 133 bp; CCDB-29481-D03, LNAUV2319-17, voucher USNM ENT 01276521, from Zomba, S. Malawi, 1829 m, leg. Henry Barlow, likely from fruit trapping study between 1995 and 1998, see: Van Bergen et al. 2016). This proved to be highly uninformative and apparently also chimaeric, the 5 ʹ end querying (probably unreliably) to an itself incomplete sequence (HM406139; first 100 bp missing) of Colotis celimene (H. Lucas, 1852) (at 3.6% divergence) and the 3 ʹ end (with ~4.5% divergence) to Calyptra minuticornis (Guenée, 1852) . A calpine placement for atomifera is almost certainly coincidental, as the 3 ʹ fragment is also not a reliable match.

Diagnosis: Erebidae with typical ‘calpine’ habitus, viz. conspicuous ‘beak’-like labial palpi ( Fig. 5 ), anal margin of forewing sinuous, outwardly produced into a flap or tooth just before middle of its length, cryptic coloration of forewing sharply contrasting with pale, often yellow-orange one of the hindwing, and with robust body. Head large, eye globular, frons nearly flat, overhung by compact cuspidate hood of scales proceeding from vertex, antenna of male with basal part of flagellum thickened, bearing short to medium-elongated paired rami from basal to median flagellomeres, distally filiform, that of female filiform throughout, ocular sclerite voluminous and swollen, pilifer well developed, with long bristles, proboscis with sharp pointed stiff apex bearing subapically numerous tetrahedral cusps with sharp edges and vertices, the cusp bases being fused to the proboscis surface (unlike the tearing hooks of Calpini lying on membranous sockets), labial palpus appearing compressed because of long scaling mainly oriented along the vertical plane, the palpomeres arranged in shape of Z, with the third one more or less strongly oriented ventrally and often incorporated into the silhouette of the second one so as to confer a blunt appearance to the whole palpus. Thorax robust, with well convex notum, patagium relatively long, tegula bicoloured, split between darker part facing notum and paler lateral one. Forewing elongated, with oblique and convex termen and feebly to strongly pronounced submedian flap along anal margin, pattern elements faint, blurred or, conversely, consisting of weakly marked and broadly undulated crosslines in basal field, large ovate-subrectangular reniform stigma with thin striga inside, irregularly double postmedial line, crenulate submarginal and lunulate adterminal lines. Hindwing oblong, its ground colour pale. Legs slender, with unspined tibiae. Male genitalia with broadly U-shaped vinculum and short transverse saccus, tegumen hood-shaped; valvae asymmetrical, especially in sacculi, whose inner edges are variously excised and produced into lobes that match each other and sinuosities of juxta-like pieces of a three-dimensional jigsaw, valva ending into variously expanded plate with acute corners and/or processes pointing to different directions; juxta extraordinarily modified, that is narrow saddlelike ventrally, bulged or folded midventrally, strongly sinuous, also with lateral expansions that combined altogether match and articulate with corresponding parts of valval bases and sacculi, then apically elongated into exceedingly long, stick- or whip-like process, here termed as ‘mastigojuxta’ (from the Greek ‘μάστῑξ, μάστῑγος = whip’, combined with ‘juxta’), that is positioned to the right of manica penis and either reaches or overpasses the uncus, such prolongation either bearing apical bundle or belt of spines for most of its length. Uncus simple, tuba analis with long, paired, poorly sclerotized, thin scaphium rods. Phallus with pointed coecum and shaft dilated in posterior half; vesica compact, unarmed, with multiple diverticula; all species but one (see below) show a broad auriculate carinal plate minutely scobinate along on the outer edge. Female with pregenital abdominal segment (A7) with long and wide rectangular tergum and sternum, of tough consistency, genitalia with segment A8 relatively long, subcylindrical or frustum-of-cone shaped, ostium bursae sided by more or less elongated anterior prolongations of tergum A8 that join ventrally with one to two strongly sclerotized asymmetrical plates and accessory structures of either A8 basisternal or intersegmental origin overhanging a broad pit leading to the gonopore, such ‘chamber’ with inner side of its ventral wall (i.e. internal side of plates) and base convoluted (due to different preparation style female segment A7 could not be studied in H. hieroglyphica ); apophyses anteriores short and thick, contorted; ductus and corpus bursae membranous, the latter pyriform or ovoid, appendix bursae a small papilla from postero-dorsal section of corpus bursae; ovipositor short, with large, terminally blunt papillae anales setose in their distal two thirds; apophyses posteriores rod-like, much longer than anteriores.

Etymology: The name Hemiceratoides evidently derives from Hemiceras , the genus with which hieroglyphica was originally combined by Saalmüller (1891), and obviously means ‘ Hemiceras -like’, but its gender was not declared by Strand (1911). As Hemiceras is based on the Greek neuter ‘κέΡας, κέΡατος’ (horn, hence by extension ‘antenna’) preceded by ‘ἡμι-’ (half), for the split appearance of the male antennae (with long rami only to half of the flagellum), it can reasonably be argued that Hemiceratoides is neuter, thus falling under the exceptions admitted by ICZN (1999: art. 30.1.4.4) for considering names ending in -oides as masculine.

Morphological remarks: Peculiarities of the Hemiceratoides proboscis have been adequately discussed byBänziger (2007, 2021), Zaspel (2008), and Zaspel et al. (2011), though the species examined has incorrectly been reported as H. hieroglyphica , and those of genuine H. hieroglyphica were illustrated by Hilgartner et al. (2007) and Hilgartner (2022). Here we draw attention to some other extraordinary morphological features present in some members of the genus.

1. The first is the sexually dimorphic configuration of the labial palpi in Hemiceratoides sittaca ( Karsch, 1896) , in which the female exhibits the third palpomere as cylindrical with an obliquely truncated tip, whereas in the male the same part is basally thickened, terminating in a long, downwardly recurved and pointed fang, that is apically unscaled and swollen at base ( Fig. 6A–C ). This feature was noted by Karsch (1896) in the description of the species where the labial palpi suggested to him a parrot’s beak (‘papageishnabelartig’), lending the name ‘(p)sittaca’. However, when the third palpomeres rather than the general silhouette of palpi are examined under the microscope, the labial palps bear a striking resemblance to the fangs of spiders’ chelicerae. The striking sexual dimorphism in this species is suggestive of different feeding behaviours between the sexes, the male being possibly aided in tear-drinking [yet unconfirmed in this species despite a record by Zahiri et al. (2012), who were simply referring to the behaviour already observed in H. hieroglyphica from Madagascar], as we hypothesize using such hooked palpi to prise open its hosts’ eyelids.

2. Extraordinary modifications are those seen in what has been termed here as mastigojuxta, i.e. the superior part of juxta positioned to the right of manica penis and lengthened into a long, thin process bearing spines ( Fig. 9A–F ). In all species, except hieroglyphica , the mastigojuxta is flagellar or whip-like, sparsely spined along its length, and extends beyond the uncus, while in the type species of the genus it is rigid, shaped like an incurved stick that terminates into a club bearing a bundle of stout spines, and reaches only the base of the uncus. From the greatly convoluted and asymmetrical basisternal modifications of female segment A8 (and possibly adjoining intersegmental membrane) such complex mastigojuxtae may play a role in locking the male genital parts with corresponding female ones during copula.

3. In the females, while the pregenital abdomen up to A7 does not show any peculiar structures, as noted under (2), the basal part of sternum A8, perhaps fused with sclerotizations from the intersegmental membrane A7– A8, is greatly modified, likely to interlock specialized male structures such as the mastigojuxtae and other processes on the valvae during copula ( Fig. 11B–E ).

4. Just proximal to the anal angle of the cucullus, numerous species of Hemiceratoides show a rod-like, ventrally oriented process substantially set parallel to the ventral margin of valva ( Fig. 9C–F ). In two species these processes seem to directly originate from the anal angle, but such species show almost a complete fusion between the valvula and cucullus, whilst the orientation and slenderness of their processes suggest homology with corresponding ones in species where they are proximal to the cucullus. Indeed, analysis of the proximal sclerotization to such processes indicates that they are of saccular origin. Their length is variable; noteworthy is their configuration in H. sittaca , a species in which they are so long as to almost reach the base of the valva, with a distal club bearing a thick tuft of hair-like scales ( Fig. 9C ).

5. Carinal structures in Noctuoidea are usually narrowly elongated, terminal processes of the phallus shaft in the shape of bars, sticks, rods, and may be variously ornamented with teeth. In Hemiceratoides , with the sole exception of H. vadoni Viette, 1976 in which there is no such structure, there is a broadly rounded, ear-shaped (auriculate) carinal plate ( Fig. 10A, C–F ). This is partly folded inside the phallus shaft when the vesica is at rest and is comparable to eversible bars or bands sometimes seen in noctuoid moths (e.g. Zilli et al. 2005, Mikkola et al. 2009, San Blas 2014), but such introflexion is only partial because of the size of such a structure, so that it cannot be easily accommodated inside the shaft.

Molecular phylogenetics: The position of Hemiceratoides as a genus of tribe Ophiderini has been discussed in the ‘Molecular analysis’ section above. As regards the ingroup relationships, for H. hieroglyphica (BIN, BOLD:ACM6895) there are two identical DNA barcodes on BOLD, based on vouchers KLM_Lep_01342 from Nosy Be and 25029-240120-MA from Mahajunga, Madagascar ( Fig. 3 ). This BIN, though, is 4.56-4.86% divergent to that for H. ornithopotis sp. nov. (BIN, BOLD:ABV4876; 25030-240120-MA from Uganda; BC_ZSM_Lep_58324 from Mozambique). The last BIN comprises the ‘third haplotype’ of Borth and Kons (2022: 132, fig. 78), and exhibits a 1.52% sequence divergence based on the above two (complete) DNA barcodes for H. ornithopotis . Second, the pairwise divergence of H. hieroglyphica to H. sittaca (BIN, BOLD:AAZ8376) is very similar to its divergence with H. ornithopotis , at 4.71–4.72% (BC_ZSM_Lep_47483; JN401290; Zahiri et al. 2012). Finally, the pairwise divergence of H. ornithopotis to H. sittaca (BC_ ZSM_Lep_47483) varies from 3.65% (25030-240120-MA, Uganda) to 4.26% (BC_ZSM_Lep_58324, Mozambique). So, for Hemiceratoides the three available BINs are of a similar divergence to one another, with the two mainland ones only slightly more similar. The partial 294-bp COI sequence of H. ornithopotis (as H. ‘ sittaca ’, voucher M-JMZ518, NMNH, sequence: JMZC002) is identical to that of 25030-240120-MA. However, GenBank accession JN401294 (voucher RZ105, from Hong Kong, Zahiri et al. 2012) identified as Hypocala deflorata represents a clear contamination or mixup from RZ 155 in the same study (but see Materials and Methods).

Figures

Figure 2. Larvae of Hemiceratoides ornithopotis sp. nov. on Smilax sp. (Smilacaceae), South Africa. A, L3 instar; B, L4 instar; C, L5 instar. ©Warren K. Dick (reproduced with permission).

Figure 3. Topology of Calpinae rooted with Hypocalinae from a MrBayes v.3.2.7 analysis of the 32*6890 dataset partitioned by gene (rates = invgamma, Nst = 6,) including all available DNA barcodes for Hemiceratoides in the context of (up to nine-gene; #g = number of genes as specified in the Supporting Information, Table S1) datasets of Zaspel et al. (2012) and Zahiri et al. (2012). The first nodal support value is the MrBayes PP, whereas the second is the percentage value plotted from 1000 bootstraps using a ML analysis in PHYML 3.0 using the GTR+I+G model as automatically implemented by the BIC. Support values (Bayesian) of at least 0.95 and/or bootstrap values (ML) of at least 70% are considered significant for the purposes of this analysis. Each cluster number (Barcode Index Number code; e.g. BOLD:ABC1234) is added from BOLD as relevant. Study codes shown are for Zaspel (2008) (Zp1), Zahiri et al. (2011) (Zh1), Zahiri et al. (2012), (Zh2), Zaspel et al. (2012) (Zp2), Mutanen et al. (2016) (Mu) and Borth and Kons (2022) (BK). The symbols relate to known feeding habits in studied genera: fruit, haematophagous (blood drop), lachryphagous (tear drop), nectar (flower), sweat (runner). For the naming of Calyptra canadensis see Appendix.

Figure 4. Proboscides of Hemiceratoides spp.. A, H.ornithopotis sp. nov., Mozambique, left galea; B, H. thisbe comb.nov., Ethiopia, right galea. Scale bar = 2 mm. Photos by Alberto Zilli.

Figure 5. Close-up of a female Hemiceratoides ornithopotis sp. nov., South Africa.©Warren K. Dick (reproduced with permission).

Figure 6. Heads of Hemiceratoides sittaca showing dimorphism in labial palpi. A, male, Angola, dorsal view; B, idem, lateral view; C, female, Ghana, lateral view. Scale bar = 2 mm. Photos by Alberto Zilli.

Figure 9. Male genitalia of Hemiceratoides (phalli removed).A, H. hieroglyphica, Madagascar; B, H. vadoni, Madagascar; C, H. sittaca, Ghana; D,H.ornithopotis sp. nov., paratypus, South Africa; E, H. avimolestum sp. nov., paratypus, South Africa; F, H. thisbe comb.nov., Ethiopia. Scale bar = 2 mm.Photos by Jérôme Barbut (A), Alberto Zilli (B–F).

Figure 10. Phalli of Hemiceratoides. A, H. hieroglyphica, same as Figure 9A; B, H. vadoni, same as Figure 9B; C, H. sittaca, same as Figure 9C; D,H.ornithopotis sp.nov., same as Figure 9D; E, H.avimolestum sp. nov., same as Figure 9E; F, H. thisbe comb. nov., same as Figure 9F. Scale bar = 2 mm.Photos by Jérôme Barbut (A), Alberto Zilli (B–F).

Figure 11. Female genitalia of Hemiceratoides. A, H. hieroglyphica, Madagascar (preparation without A7 and with spread A8–A9); B, H.sittaca, Nigeria; C, H. ornithopotis sp. nov., paratypus, Malawi; D, H. avimolestum sp. nov., paratypus, Mozambique; E, H. thisbe comb.nov., Ethiopia. Scale bar = 3 mm. Photos by Jérôme Barbut (A), Alberto Zilli (B–E).