Science (2012) 19, 153–158, DOI 10.1111/j.1744-7917.2011.01468.x

ORIGINAL ARTICLE A new Upper stem-orthopteran (Insecta) from Ningxia (China)

Olivier Bethoux´ 1,2, Jun-Jie Gu1 and Dong Ren1 1College of Life Sciences, Capital Normal University, Beijing, China, 240 rue d’Aveillans, 38770 La Motte d’Aveillans, France

Abstract During the Upper Carboniferous, orthopteran (grasshoppers, katydids, and crickets) were represented by numerous species distantly related to crown-orthopterans, such as lobeattid and cnemidolestodean insects. The panorthopterans, including total- orthopterans and their closest relatives, are represented by comparatively rarer species in localities of this period. Here we describe Heterologus duyiwuer sp. nov., an infrequent panorthopteran from the Late Carboniferous locality of Xiaheyan Village (Zhongwei City, Ningxia Hui Autonomous Region, China). The only available specimen is composed of an isolated forewing exhibiting a combination of character states previously unknown, in particular the lack of posterior radius (RP) / anterior Media (MA) connection, late branchings of the media (M) and anterior cubitus (CuA), and a branched posterior branch of the posterior cubitus (CuPb). Based on its unusual branching pattern, the composite stem resulting from the fusion of CuA and CuPaα (second anterior branch of CuP) is assumed to be composed of a branched CuA and a simple CuPaα. Key words Archaeorthoptera, homology, Namurian, stem-orthopterans, Tupo Formation

Introduction initially conceptualized as including orthopterans and their closest stem-relatives (Bethoux´ & Nel, 2002a) has The systematics of stem-orthopterans received renewed been altered by Rafael et al. (2008). According to these attention in the last decade, in particular at the species authors this taxon is a synonym of Orthopterida, and en- level. A number of revisions of Upper Carboniferous his- compasses not only total-orthopterans but also the or- torical material led to the identification of a series of ders Grylloblattodea and Mantophasmatodea (among oth- successive stem-representatives of the orthopteran lin- ers). This case exemplifies the excessive plasticity of eage (grasshoppers, katydids and crickets). A new tax- Linnaean-based taxon names, resulting in ambiguity that onomic and nomenclatural framework is currently de- impedes optimal communication (Bethoux,´ 2010). Under veloped under the cladotypic nomenclatural approach the cladotypic nomenclature such volatility is prevented (Bethoux,´ 2007b, 2007c, 2010; see practical introduc- by the association of taxon names together with a defini- tioninBethoux´ & Herd, 2009). Under this scheme the tion. Only those species exhibiting the defining character taxon Archaeorthoptera nom. Bethoux´ and Nel, 2002a, state of a taxon belong to it. With regard to this context, dis.-typ. Bethoux,´ 2007d includes these stem-orthopterans the presumed superiority of this nomenclatural procedure together with crown-orthopterans (Fig. 1). Notice that un- will continue to be tested on the systematics of stem- der the Linnaean approach, the ‘Archaeorthoptera’ taxon, orthopterans. A few species might be sister-representatives of all other Archaeorthoptera (Bethoux,´ 2003, 2006). Two nu- Correspondence: D. Ren, College of Life Sciences, Cap- merically important groups of Upper Carboniferous basal ital Normal University, Beijing 100048, China. email: Archaeorthoptera have been outlined and reported from [email protected] many deposits, namely lobeattid insects (Bethoux,´ 2008a;

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daeans are characterized by a highly variable wing vena- tion (Bethoux´ & Nel, 2003). A few other relevant species are known from Mazon Creek, IL, USA (Carpenter, 1944) and the Piesberg locality, Germany (Brauckmann & Herd, 2006), but they are represented by a limited sample, and frequently by incomplete wings only. Herein we describe a new and rare species based on an isolated forewing from the Upper Carboniferous local- ity near Xiaheyan village. Its preservation is exquisite, and its combination of character states unknown to date.

Material and methods

The material investigated in this contribution is housed at the College of Life Science, Capital Normal University, Beijing (China). Drawings were produced with a Leica MZ7 equipped with a 1.0 planachromatic lens and a draw- ing tube. The specimen was photographed with a Canon EOS 450D coupled with a Canon 50 mm macro lens and a 12 mm elongation tube. The photograph reproduced in Figure 2 is a dry-ethanol composite (see Bethoux´ & Briggs, 2008). The specimen was prepared by O. Bethoux´ in January 2010. Primary homologies for wing venation of total- orthopterans developed by Bethoux´ and Nel (2001, 2002a) are followed. Comments regarding these conjectures Fig. 1 Current phylogenetic framework for stem-orthopterans (Gorochov,2005) and their implications (Rasnitsyn, 2007) (dumasii Brongniart, 1879 and spilopterus Handlirsch, 1911 have been addressed elsewhere (Bethoux, 2007a, 2008b). are assigned to the genera Protophasma Brongniart, 1879 and ´ Cacurgus Handlirsch, 1911 under the Linnaean procedure, The corresponding nomenclature is: ScP, posterior sub- respectively). costa; RA, anterior radius; RP, posterior radius; M, me- dia; CuA, anterior cubitus; CuP, posterior cubitus; CuPa, Bethoux´ & Nel, 2004, 2005; Bethoux´ & Poschmann, anterior branch of CuP; CuPaα, anterior branch of CuPa; 2009; Bethoux´ & Jarzembowski, 2010; Prokop & Ren, CuPaβ, posterior branch of CuPa; CuPb, posterior branch 2007, among others), and cnemidolestodeans (Bethoux,´ of CuP; AA: anterior analis. 2005, among others). These groups abound in the Upper Throughout this contribution we use a nomenclatural Carboniferous locality of Xiaheyan Village (Zhongwei procedure predominantly cladotypic. However, regarding City, Ningxia Hui Autonomous Region, China; O. species names, a binominal name is provided for the new Bethoux´ & J.-J.Gu, pers. obs.) and will be the focus of species by assigning it to a pre-existing , so that the future detailed descriptions. The monophyly of these two name is made available under the International Code of groups is uncertain yet. Zoological Nomenclature (ICZN). Genera of previously According to Bethoux´ and Nel (2002a) a more derived described species are indicated at the first mention of the taxon, the panorthopteran insects, includes jumping or- species. Later on Lanham’s species names are used (else- thopterans (saltatorians) and their closest fossil relatives. where referred to as uninominal names; Lanham, 1965; Panorthopterans exhibit, in forewings, a branched anterior and see Dayrat et al., 2004). Under the cladotypic nomen- branch of the posterior cubitus (basal to its fusion with the clature taxa are referred to by names written in italics anterior cubitus), a character state pointed out as a putative with a capital letter. Linnaean taxon names are avoided autapomorphy of the group by these authors. Inference re- and ‘vernacularized’ names are preferred (e.g., orthopter- garding the panorthopteran plesiomorphic character states ans rather than ). The choice of the nomen- combination (i.e., ground-plan) is made difficult by the clatural procedure is based on the decision of one of us lack of appropriate data. Among panorthopterans, gerari- (OB; see also Bethoux,´ 2010) and does not imply the

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Fig. 2 Heterologus duyiwuer sp. nov. (holotype CNU-NX1–266, left forewing), drawing and photograph (positive imprint, composite, reversed). support of other authors (JJG, DR) to all aspects of this Description Holotype CNU-NX1–266: incomplete procedure. negative imprint and complete positive imprint of a right forewing, very well preserved; length 27.6 mm, width (op- Systematics posite the end of CuPaα) 10.3 mm; area between anterior wing margin and ScP broad, filled with ScP veinlets, with Taxon Archaeorthoptera nom. Bethoux´ and Nel, 2002a few cross-veins between them; ScP reaching RA; ScP+ dis.-typ. Bethoux,´ 2007d RA with weak distal anterior veinlets (cross-veins?); R Genus Heterologus Carpenter, 1944 simple for 8.8 mm; RP simple for 6.1 mm, with 8 branches Heterologus duyiwuer sp.nov. reaching wing apex, without clear branching pattern; RP Diagnosis ScP reaching RA; RP and M without any preserved as tube basal to its first branching, branches of connection; M weak, concave, simple for a long dis- RP preserved as depressions; M + CuA convex, branching tance; fusion CuA + CuPaα short; CuA branched dis- into M and CuA 7.7 mm distal to wing base; M (diverg- tally; CuPaα and CuPaβ simple; CuPb branched; cross- ing from M + CuA) weakly sclerotized, concave, simple veins rarely reticulated, often forming cells broader than for 8.2 mm, with 3 distal branches, branches of M im- long. printed as depressions; CuA (diverging from M + CuA)

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0.9 mm long before its fusion with CuPaα;CuA+ CuPaα raphyletic basal saltatorians) chiefly after the branching short (1.2 mm long; see Comments for homologization of pattern of CuA + CuPaα, with a long distance between CuA+ CuPaα); distal to the divergence of CuPaα (from the first basal branch (itself homologized as CuPaα,see CuA+ CuPaα), CuA simple for 5.5 mm, posteriorly pecti- below) and the next fork (giving rise to branches of CuA, nate, with 4 branches reaching posterior wing margin; see below). In oedischioideans, whichever conjecture of imprint of CuA turns from a tube-like structure to a primary homology is followed for CuA + CuPaα (CuA depression basal to the first branching of CuA; CuP simple + branched CuPaα vs. CuA branched + simple branched 3.2 mm distal to wing base; CuPa simple for CuPaα vs. CuA branched + CuPaα branched), branches 4.0 mm; CuPaα 1.3 mm long before fusion with CuA; are emitted at a regular pace (Bethoux´ and Nel, 2002b; CuPaα and CuPaβ simple; CuPb simple for 7.3 mm, pos- Bethoux´ et al., 2002; Carpenter, 1992; Gorochov, 1987; teriorly pectinate, with 3 branches reaching posterior wing Sharov, 1968, 1971, among others). In addition all stem- margin; CuPaα,CuPaβ and CuPb preserved as tubular saltatorians exhibit a first branching of M near the point of imprints in their basal part, then as depressions; first AA divergence of CuA from M + CuA, while M is simple for vein branched distally; 2 additional convex AA veins oc- a long distance in the specimen CNU-NX1–266. Lastly, cur; cross-veins convex, strong, especially in the middle most of these basal saltatorians exhibit a connection of of their course, straight, rarely reticulated, often forming RP with an anterior branch of M. cells broader than long; in areas between CuA and CuPaβ, The species to which the specimen CNU-NX1–266 the most distal cross-vein (convex) reaches the posterior belongs differs from trecwithiensis Kukalova-Peck´ & margin obliquely, forming a main-vein-like fork pattern Brauckmann, 1992 (genus Osnogerarus Kukalova-Peck´ (main vein concave); wing overall dark, darker coloration & Brauckmann, 1992; see Brauckmann & Herd, 2006: along cross-veins (observed in the middle part). fig. 3) after its simple CuPaβ (branched in trecwithien- sis), the lack of connection between RP and the anterior Material examined Holotype CNU-NX1–266, com- branch of M, a lower number of branches of M, the lack of posed of negative (fragment) and positive (complete) im- strong branches from ScP and the cross-venation (densely prints of an isolated left forewing. reticulated in trecwithiensis). After its late branching of M and its cross-venation, the locality and horizon Tupo Formation (Ningxia new material resembles langfordorum Carpenter, 1944 Hui Autonomous region, China); Namurian, Upper (genus Heterologus Carpenter, 1944). However, langfor- Carboniferous (Lu et al., 2002). dorum has a simple CuPb, while this vein is branched in Etymology ‘In a class by oneself’ [duyiwuer] in the specimen CNU-NX1–266. In addition langfordorum ´ ¯ ´ ` + α Chinese. has more numerous branches of RP,M and CuA CuPa . The erection of a new species is therefore justified. The species is provisionally assigned to the genus Discussion Heterologus Carpenter, 1944 in order to make the species name available under the ICZN. The genus was composed The new material belongs to a species that can be as- of langfordorum Carpenter, 1944 only. As newly delim- signed to Archaeorthoptera as it exhibits the defining ited, the genus is probably paraphyletic but this does not character state of this taxon, namely in forewings, a fu- prevent the name Heterologus duyiwuer to be valid under sion of CuA (diverging from M + CuA) with a branch the ICZN. Notice that under the cladotypic nomenclat- of CuP (Bethoux,´ 2007d). This species is considered as ural procedure the species can be referred to as duyiwer a panorthopteran insect as it exhibits one of the diagnos- Bethoux,´ Gu & Ren, 2011, or Archaeorthoptera duyiwuer tic character states of the group pointed out by Bethoux´ Bethoux,´ Gu & Ren, 2011. and Nel (2002a), namely the branching of CuPa basal to Except for ScP, RA and the most basal AA veins, im- the fusion of its anterior branch (CuPaα) with CuA (the prints of all main veins turn suddenly from a tube-like to taxon name ‘Panorthoptera’ is not yet associated with a a depression-like preservation, from the forewing base to definition under cladotypic nomenclature). the apex and posterior wing margin. The origin of this Among panorthopterans, the new material differs from switch is unknown, but clearly, vein elevation cannot be species of geraridaeans after its more distal branching of considered as relevant for discussion regarding vein ho- M, the lack of strong and oblique anterior branches of mologies in the distal part. RA, and the lack of connection of RP with the anterior The branching pattern of CuA + CuPaα in duyiwuer branch of M (see Bethoux´ and Nel, 2003; among oth- is not usual. In lobeattid insects and oedischioideans, ers). It differs from Late Palaeozoic oedischioideans (pa- among others, CuA + CuPaα emit posterior branches at a

C 2012 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 19, 153–158 A new stem-orthopteran 157 regular pace (Bethoux,´ 2008a; Bethoux´ & Nel, 2004; Bethoux,´ O. (2007c) Cladotypic revisited. Sharov, 1968, among others). In duyiwuer a basal branch Systematics & Phylogeny, 65(2), 127–133. diverges near the fusion of CuA with CuPaα, while others Bethoux,´ O. (2007d) Cladotypic taxonomy applied: titanopter- branch off more distally. This pattern suggests that the ans are orthopterans. Arthropod Systematics & Phylogeny, first posterior branch is CuPaα, while distal branches be- 65(2), 135–156. long to CuA. The composite vein CuA + CuPaα would Bethoux,´ O. (2008a) Revision and phylogenetic affinities of therefore be composed of a branched CuA and a simple the lobeattid species bronsoni Dana, 1864 and silvatica Lau- CuPaα. rentiaux & Laurentiaux-Vieira, 1980 (Pennsylvanian; Ar- chaeorthoptera). Arthropod Systematics & Phylogeny, 66(2), Conclusion 145–163. Bethoux,´ O. (2008b) Groundplan, nomenclature, homology, Recent progress in the systematics of Upper Carbonifer- phylogeny, and the question of the insect wing venation pat- ous Archaeorthoptera allowed us to identify a species of tern. Alavesia, 2, 219–232. phylogenetic importance among the large sample assem- Bethoux,´ O. (2010) Optimality of phylogenetic nomenclatural bled by DR’s the research team. Indeed the new material procedures. Organisms Diversity & Evolution, 10, 173–191. allowed a new primary homology for the branches of Bethoux,´ O. and Briggs, D.E.G. (2008) How Gerarus lost its CuA + CuPaα to be conjectured in a stem-orthoptean. head: stem-group Orthoptera and revisited. Sys- In addition the new species exhibits a combination of tematic Entomology, 33, 529–547. character states previously unknown. It will likely be Bethoux,´ O. and Herd, K.J. (2009) Discovery of an enigmatic a key taxon in future phylogenetic analysis of basal and gigantic Pennsylvanian Archaeorthoptera. Journal of Or- Archaeorthoptera. thoptera Research, 18, 23–28. Bethoux,´ O. and Jarzembowski, E.A. (2010) New basal neopter- Acknowledgements ans from Writhlington (UK, Pennsylvanian). Alavesia,3, 87–96. We thank an anonymous reviewer for constructive com- Bethoux,´ O. and Nel, A. (2001) Venation pattern of Orthoptera. ments. The first author was a recipient of an Endeavour Journal of Orthoptera Research, 10, 195–198. postdoctoral Award at the time of writing. This research Bethoux,´ O. and Nel, A. (2002a). Venation pattern and revi- is supported by the National Natural Science Founda- sion of Orthoptera sensu nov. and sister groups. Phylogeny of tion of China (No. 40872022, 31071964, 31172143), Na- Palaeozoic and Mesozoic Orthoptera sensu nov. Zootaxa, 96, tional Basic Research Program of China (973 Program) 1–88. (2012CB821906), Nature Science Foundation of Beijing Bethoux,´ O. and Nel, A. (2002b) New data on Tcholmanvissiidae (No. 5082002), the Scientific Research Key Program (Orthoptera; ). Journal of Orthoptera Research, 11, (KZ200910028005) and PHR Project of Beijing Munici- 223–235. pal Commission of Education (20090509, 201107120). Bethoux,´ O. and Nel, A. (2003) Wing venation morphology and variability of Gerarus fischeri (Brongniart, 1885) sensu References Burnham (Panorthoptera; Upper Carboniferous, Commentry, France), with inferences on flight performances. Organisms Bethoux,´ O. (2003) Protophasma dumasii Brongniart, 1879, Diversity & Evolution, 3, 173–183. a link between Orthoptera and the ‘dictyopterid’ orders? Bethoux,´ O. and Nel, A. (2004) Some Palaeozoic ‘Pro- Journal of Orthoptera Research, 12(1), 57–62. torthoptera’ are ‘ancestral’ orthopteroids: major wing braces Bethoux,´ O. (2005) Cnemidolestodea (Insecta): an ancient or- as clues to a new split among the ‘’. Journal of der reinstated. Journal of Systematic Palaeontology, 3(4), Systematic Palaeontology, 2, 285–309. 403–408. Bethoux,´ O. and Nel, A. (2005) Some Palaeozoic ‘Pro- Bethoux,´ O. (2006) Revision of Cacurgus Handlirsch, 1911, torthoptera’ are ‘ancestral’ orthopteroids: major wing braces a basal Pennsylvanian Archaeorthoptera (Insecta: Neoptera). as clues to a new split among the ‘Protorthoptera’: corrigen- Bulletin of the Peabody Museum of Natural History, 47(1–2), dum. Journal of Systematic Palaeontology, 3, 223. 29–35. Bethoux,´ O. and Poschmann, M. (2009) A new lobeattid in- Bethoux,´ O. (2007a) Archaeorthoptera wing venation nomen- sect from the Permo-Carboniferous of Niedermoschel, south- clature: a reply to Gorokhov. Paleontological Journal, 41(3), western Germany (Archaeorthoptera). Journal of Orthoptera 338–340. Research, 18, 139–143. Bethoux,´ O. (2007b). Propositions for a character-state-based Bethoux,´ O., Nel, A., Gand, G., Lapeyrie, J. and Gatier J. biological taxonomy. Zoologica Scripta, 36(4), 409–416. (2002) Discovery of the genus Iasvia Zalessky, 1934 in the

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