Ann. Mus. civ. St. nat. Ferrara Vol. 8 2005 [2007] pp.55-58 ISSN 1127-4476

Morphology of the female terminalia of Nymphes myrmeleonoides Leach, 1814 (Neuroptera Nymphidae) and phylogenetic implications

Verena Feuerstein

Georg-August-University Gottingen. Johann-Friedrich-Blumenbach-Institute of Zoology and Anthropology, De­ partment of Morphology and Systematics, Berliner Str. 28, 0-37073 Gottingen, Germany, e-mail: [email protected]

The female terminal structures of Nymphes myrme/eonoides Leach, 1814 (Nymphidae) are de­ scribed in detail. Within Neuroptera the genitalia of Nymphidae are considered to be highly derived. However, all elements of the "orthopteroid" ovipositor are obviously present in N. myrme/eonoides. The ovipositor is short and is composed basically of the gonocoxites IX (+ valvulae III). A pair of scierites (valvulae II) is present along the inner membranous sides. This pair of sclerites interlocks with a structure often called "subgenitale" (fused valvulae I). Similar structures exist in Chrysopidae and the arrangement may even be homologous with the olistheter of Raphidioptera. The valvulae I and II are missing in some other Neuroptera (e.g. Osmylidae). The interpretation of the subgenitale and the corresponding sclerites of Nymphes (and chrysopids) as ovipositor derivates sheds new light on the evolution of the ovipositor in Neuroptera and provides new views of their phylogeny.

Key words - Neuroptera, Nymphidae, Nymphes myrme/eonoides, ovipositor, morphology, phylo­ geny.

Introduction the internal and external genitalia of Neu­ ropterida was performed by Stitz (1909). Nymphidae is a small taxon consisting Principi (1949) and Philippe (1972) de­ of approximately 35 extant species restric­ scribed the morphology of the female ge­ ted to Australia, New Guinea and adjacent nitalia of Chrysopa, that is characterized islands. It is considered to be the sister­ by a very short ovipositor. Investigations group of Myrmeleontidae + Ascalaphidae of taxa with a long ovipositor similar to that + Nemopteridae (New, 1984; Oswald, of the Raphidioptera are restricted to the 1998) or of Myrmeleontidae + Ascalaphi­ external morphology. Ferris (1940) exami­ dae (Mansell, 1992; Aspock et al., 2001) ned the ovipositor of Plega signata (Ha­ within the Myrmeleontiformia (Myrmeleon­ gen, 1877) (Mantispidae) and Tjeder toidea sensu Mansell, 1992), one of the (1937) that of Dilaridae. more species rich subtaxa within Neuro­ The overall similarity of the female ge­ ptera. nital structures of Neuroptera, Megalopte­ Contradictory interpretations of the ra and Raphidioptera was demonstrated neuropteran ovipositor structures exist in by Mickoleit (1973a). He hypothesized a the literature and much controversy sur­ short ovipositor for the ground plan of rounds the homology of female genitalia. Neuropterida and complete loss of the go­ Morphological investigations of the ovipo­ napophyses IX (valvulae II). The gonapo­ sitor have been carried out predominantly physes VIII (valvulae I) are assumed to for taxonomic reasons. Detailed morpho­ have been lost in the ground plan of Neu­ logical examinations exist only for a few roptera as well as that of Megaloptera. Al­ neuropteran taxa. The first examination of ternatively, Mickoleit (1973a) discussed a

55 Proceedings of the IX International Symposium on Neuropter%gy long raphidiopteran-like ovipositor with present along the inner membranous si­ valvulae I and valvulae II for the ground des of gonocoxites IX. This pair of scleri­ plan of Neuropterida. Although Mickoleit tes interlocks with an unpaired sclerotized abandoned this theory for functional rea­ projection of the segment VIII, the so­ sons, Achtelig (1978) supported the hypo­ called "subgenitale" (Figs 1 C and 2 A) - a theses after further investigations of Ra­ structure invariably present in all nym­ phidioptera. phids (New, 1984). The short ovipositor of Nymphidae and Comparable structures exist in Heme­ other Myrmeleontiformia was assumed to robiidae (e.g. Wesmaelius, Aspock et al., be highly derived and for this reason con­ 1980) and Chrysopidae (e.g, Chrysopa, sidered to be less important for the under­ Principi, 1949; Philippe, 1972; Chrysoper­ standing of the ground pattern of female la: Fig. 2 B). In Chrysopidae the "subgeni­ genitalia in Neuroptera. However, exami­ tale" is a pair of lobes which articulate with nation of Nymphes myrmeleonoides Le­ a pair of sclerotized pockets like a snap­ ach, 1814 (Nymphidae) showed that obvi­ press button ("button-pression", Philippe. ously all elements of an "orthopteroid" ovi­ 1972). positor are present and that it is not as de­ Achtelig (1978) compared the arrange­ rived as previously assumed. ment of the sclerites found in Chrysopidae with the interlock of the long ovipositor of Material and methods Raphidioptera (Fig. 3 C). In contrast to Smith (1969) and Mickoleit (1973a) he The ovipositor morphology of N. myrmeleo­ noides was examined based on alcohol fixed material (70%) and macerated specimens that were studied in glycerine. Histological sections of N. myrmeleonoides and Chrysoper/a carnea (Stephens, 1836) were made. For this purpose specimens were fixed in Bouin's solution, sec­ tioned serially at 10l-lm and stained with "Nu­ clear Fast Red" and "Aniline Blue-Orange G" (Azan stain). Females of N. myrmeleonoides were col­ lected at Rocksberg near Brisbane (Queens­ land, Australia) in October 1997 by Ulrike Nol­ te. Specimens of C. carnea were collected at s VII B G6ttingen (Germany) in February 2004 by Ve­ rena Feuerstein.

Results and discussion

The female external genitalia of N. myrmeleonoides (Figs 1 A and 1 B) con­ sist primarily of a pair of so-called "gona­ pophyses laterales", a structure of segment IX present in all Neuropterida. It is inter­ preted as the gonocoxites IX + gonostyli Fig. 1 - Female of Nymphes myrmeleonoides: A. IX (valvulae III) (Mickoleit, 1973a; Achte­ lateral view of terminalia; B, ventral view of termina­ lig, 1978). In N. myrme/eonoides the go­ lia; C, fused valvulae I ("subgenitale") and valvulae II. nocoxites IX + valvulae III are relatively a ::: anus; cat::: cataprocessus; epr = ectoproct; gx = gonocoxite; i = interlock; vv = valvula; s ::: sternite; t = short and joined to the sternum along al­ tergite. most the entire length. A pair of sclerites is

56 V. Feuerstein - Female terminalia of Nymphes myrmeleonoides Leach, 1814

fused unpaired valvulae I. Extrapolating the situation of the oviposi­ tor found in Raphidioptera to that of Chrysopidae Achtelig came to the conclu­ sion that the lobes (subgenitale) of Chryso­ pidae are the reduced valvulae I and the snappress button interlock is a reduced oli­ stheter (Fig. 3 8). As a consequence the subgenitale of Nymphidae and Hemerobiidae may also be interpreted as the fused valvulae I. The sclerites along the inner sides of the gono­ coxites IX are the valvulae II (gonapo­ physes IX) with the primary olistheter as the interlock between them and the valvu­ lae I (Fig. 3). This leads to the conclusion that all elements of the orthopteroid ovipo­ sitor are not only present in the ground plan of Neuropterida, but also in the ground plan of Neuroptera. The question as to the characteristic of the ovipositor in the neuropteran ground plan still remains unanswered. Assuming a primary olistheter a long raphidiopteran-like ovipositor seems probable for the ground plan of Neuropterida. Taxa with a long ovi­ Fig. 2 - Cross section of the ovipositor through the pOSitor must be examined in order to deter­ region of the fused valvulae I: A, Nymphes myrme­ leonoides; B, Chrysoperla carnea. mine whether this also applies to Neuropte­ ra. Tjeder (1937) described an unpaired considered the interlock (= olistheter) of the subgenitale and a pair of rod-like appenda­ raphidiopteran ovipositor to be primary. His ges for Dilaridae which he homologized with examinations of prothetelic larvae showed the valvulae I and valvulae II. Mickoleit that the dorsal part of the ovipositor of Ra­ (1973a), who pointed out the similarity of the phidioptera, consisting mainly of the gono­ ovipositor of Dilaridae and Raphidioptera, coxites IX + valvulae III, also contains the discussed the rod-like appendages of Dilari­ valvulae II along their inner sides (Fig. 3 C). dae as the valvulae I. Similar structures of The valvulae II, which have the function of the segment VIII have not been described a rail, interlock on each side with the long for the long ovipositor of Plega signata

8 c

vv I 200 Ilm

Fig. 3 - Schematic cross section of the ovipositor of (A) Nymphes myrmeleonoides, (B) Chrysoperla carnea, (C) Raphidioptera (after Mickoleit, 1973b). Emphasized structures show sci erotized part.

57 Proceedings of the IX International Symposium on Neuropterology

(Mantispidae) (Ferris, 1940). In accor­ Aspock U., Plant, J. D. & Nemeschkal H., 2001 - Cla­ dance with Achtelig (1978) the presence distic analysis of Neuroptera and their systematic position within the Neuropterida (Insecta: Holometa­ of valvulae I and valvulae II in Neuropte­ bola: Neuropterida: Neuroptera). Systematic Entomo­ ra is considered to be plesiomorphic and logy, 26: 73-86. can be found at least in Nymphidae and Ferris G.F., 1940 - The morphology of Plega signata within Hemerobiiformia in Hemerobiidae (Hagen) (Neuroptera: Mantispidae). Microentomo­ logy, 5: 33-56. and Chrysopidae. The structures dis­ Mansell M.W., 1992 - The systematic position of the cussed are apparently lacking in other Nemopteridae (Insecta: Neuroptera: Myrmeleontoi­ Neuroptera, for example in Myrmeleon­ dea). In: Canard, M., Aspock, H. & Mansell, M.W. - tidae, Ascalaphidae and Coniopterygi­ Current Research in Neuropterology. Proceedings of the 4th Int. Symposium on Neuropterology. Bagneres­ dae. They also seem to be absent in de-Luchon, 223-241. Osmylidae - a taxon which is supposed Mickoleit G., 1973a - Uber den Ovipositor der Neuro­ to have a plesiomorphic ovipositor with pteroidea und Coleoptera und seine phylogenetische respect to the articulation of the gonoco­ Bedeutung (Insecta, Holometabola). Zeitschrift fOr Morphologie der Tiere, 74: 37-64. xites IX with the tergite IX. Mickoleit G., 1973b - Zur Anatomie und Funktion des Additional investigation of the ovipo­ Raphidiopteren-Ovipositors (Insecta, Neuropteroidea). sitor is imperative and will certainly pro­ Zeitschrift fOr Morphologie der Tiere, 76: 145-171. vide new information about its evolution New T, 1984 - Intergeneric relationships in recent Nymphidae. In: Gepp J., Aspock H. & Holzel H. - and lead to new ideas concerning the Progress in World's Neuropterology. Proceedings of the phylogeny of Neuroptera. 1st Int. Symposium on Neuropterology. Graz, 125-131. Oswald J., 1998 - Osmylops Banks (Neuroptera: Nymphidae): generic review and revision of the ar­ Acknowledgements matus species group. Journal of Neuropterology, 1: 79-108. I wish to thank Prof. Dr. Rainer Willmann Philippe R., 1972 - Les appareil genitaux male et fe­ as my advisor, Dr. Gert Troster for critical melle de Chrysopa perla (Neuroptera) etude anato­ comments and Oliver Eikel for very helpful mique et fonctionelle. Anna/es de la Societe entomo­ logique de France (N.S.), 8: 693-705. discussions. I am grateful to Christina Forster Principi M.M., 1949 - Contributi allo studio dei Neurot­ for technical support. My very special thanks teri italiani. VIII. Morfologia, anatomia e funzionamen­ go to Dr. Ulrike Nolte (Queensland, Australia) to degli apparati genitali nel gen. Chrysopa Leach who provided many specimens of N. myrme­ (Chrysopa septempunctata Wesm. e C. formosa leonoides. Brauer). Bol/ettino dell"lstituto di Entomologia della Universita di Bologna, 17: 316-362. Smith E.L., 1969 - Evolutionary morphology of external Bibliography insect genitalia. 1. Origin and relationship to other appendages. Annals of the Entomological Society of Achtelig M., 1978 - Entwicklung und Morphologie America, 62: 1051-1079. der inneren und aul1eren weiblichen Genitalor­ Stitz H., 1909 - Zur Kenntnis des Genitalapparats der gane der Kamelhalsfliegen (Neuropteroidea: Neuropteren. Zoologische JahrbOeher, Abteilung Ana­ Raphidioptera). Entomologiea Germanica, 4: tomie und Ontogenie der Tiere, 27: 377-448. 140-163. Tjeder B., 1937 - A contribution to the phylogeny of the ASpOck H., ASpOck U. & Holzel H., 1980 - Die Neuro­ Dilaridae and the Raphidiidae (Neuroptera). Opuscu­ pteren Europas. Goecke & Evers, Krefeld, 855 pp. la entomologica, 2: 138-148.

58 Bibliography of the Neuropterida

Bibliography of the Neuropterida Reference number (r#): 11952

Reference Citation: Feuerstein, V. 2005 [2007.??.??]. Morphology of the female terminalia of Nymphes myrmeleonoides Leach, 1814 (Neuroptera Nymphidae) and phylogenetic implications. in Pantaleoni, R. A.; Letardi, A.; Corazza, C. (eds.). Proceedings of the Ninth International Symposium on Neuropterology (20-23 June 2005, Ferrara, Italy). Annali del Museo Civico di Storia Naturale di Ferrara 8:55-58.

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File: File produced for the Bibliography of the Neuropterida (BotN) component of the Lacewing Digital Library (LDL) Project, 2012.