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From Chewing to Sucking Via Phylogeny—From Sucking to Chewing Via Ontogeny: Mouthparts of Neuroptera

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From Chewing to Sucking Via Phylogeny—From Sucking to Chewing Via Ontogeny: Mouthparts of Neuroptera Chapter 11 From Chewing to Sucking via Phylogeny—From Sucking to Chewing via Ontogeny: Mouthparts of Neuroptera Dominique Zimmermann, Susanne Randolf, and Ulrike Aspöck Abstract The Neuroptera are highly heterogeneous endopterygote insects. While their relatives Megaloptera and Raphidioptera have biting mouthparts also in their larval stage, the larvae of Neuroptera are characterized by conspicuous sucking jaws that are used to imbibe fluids, mostly the haemolymph of prey. They comprise a mandibular and a maxillary part and can be curved or straight, long or short. In the pupal stages, a transformation from the larval sucking to adult biting and chewing mouthparts takes place. The development during metamorphosis indicates that the larval maxillary stylet contains the Anlagen of different parts of the adult maxilla and that the larval mandibular stylet is a lateral outgrowth of the mandible. The mouth- parts of extant adult Neuroptera are of the biting and chewing functional type, whereas from the Mesozoic era forms with siphonate mouthparts are also known. Various food sources are used in larvae and in particular in adult Neuroptera. Morphological adaptations of the mouthparts of adult Neuroptera to the feeding on honeydew, pollen and arthropods are described in several examples. New hypoth- eses on the diet of adult Nevrorthidae and Dilaridae are presented. 11.1 Introduction The order Neuroptera, comprising about 5820 species (Oswald and Machado 2018), constitutes together with its sister group, the order Megaloptera (about 370 species), and their joint sister group Raphidioptera (about 250 species) the superorder Neuropterida. Neuroptera, formerly called Planipennia, are distributed worldwide and comprise 16 families of extremely heterogeneous insects. Their adults are D. Zimmermann (*) · S. Randolf 2nd Zoological Department, Natural History Museum Vienna, Vienna, Austria e-mail: [email protected]; [email protected] U. Aspöck 2nd Zoological Department, Natural History Museum Vienna, Vienna, Austria Department of Integrative Zoology, University of Vienna, Vienna, Austria e-mail: [email protected] © Springer Nature Switzerland AG 2019 361 H. W. Krenn (ed.), Insect Mouthparts, Zoological Monographs 5, https://doi.org/10.1007/978-3-030-29654-4_11 [email protected] 362 D. Zimmermann et al. terrestrial, as are the larvae of most families; only two families have aquatic larvae (Aspöck et al. 1980, 2001; New 1989; Aspöck and Aspöck 2007). Biting and chewing mouthparts of adults and larvae are hypothesized for ances- tors of the Neuropterida, at present comprising Raphidioptera, Megaloptera and Neuroptera. The ancestors of Neuroptera evolved larval sucking tubes. As a conse- quence, a change from larval sucking to adult biting and chewing mouthparts takes place in the pupal stage of each individual neuropteran life cycle. This chapter compares the morphology of larval and adult mouthparts, presents data to the transformation in the pupal stage and discusses feeding preferences and morpholog- ical adaptations of adult Neuroptera. 11.2 The Mouthparts of the Larvae Already in the 1850s, the Austrian biologist Friedrich Moritz Brauer (1832–1904)— he was about 20 years old—recognized the evolutionary relevance of the larvae of the Neuroptera. He detected, studied and illustrated the larval sucking mouthparts, e.g., of Osmylidae, Chrysopidae, Mantispidae, and he established the Neuroptera as a monophylum based on the sucking feeding apparatus of the larvae (Brauer 1851a, b, 1852a, b; Brauer and Löw 1857). The larval sucking tubes of Neuroptera are the most spectacular and most powerful autapomorphy of the order and they are highly relevant phylogenetically. Moreover, they have a high diagnostic value. Primarily and predominately, they are uniquely effective and dangerous weapons (Figs. 11.1 and 11.2). 11.2.1 Composition of the Sucking Tubes The sucking tubes—either jaws, stylets, needles, or short suckers—comprise a mandibular part which may bear teeth and a maxillary part lacking teeth. The mandible and the distal part of the maxilla are functionally connected in different ways of coaptations, thus forming a food canal (Fig. 11.3). A venom canal runs within the maxilla of most taxa with the exception of Sisyridae (their sucking needles are used to feed on bryozoans and sponges) and with a possible exception of phytophagous Ithonidae, but detailed studies are still lacking in the latter (Wundt 1961; MacLeod 1964; Zwick 1967; Gaumont 1976; Minter 1990; Möller 2003; Grebennikov 2004; Beutel et al. 2010a; Jandausch et al. 2018). [email protected] 11 From Chewing to Sucking via Phylogeny—From Sucking to Chewing... 363 Fig. 11.1 Larva of Chrysoperla plorabunda (Chrysopidae) sucking on the aphid Acyrtosiphon pisum; photo: Peter Duelli Fig. 11.2 Larva of Euroleon nostras (Myrmeleontidae) sitting in its funnel, ambushing prey; photo: Heiko Bellmann Fig. 11.3 Cross section of larval sucking stylet of Osmylus fulvicephalus (Osmylidae). The mandible (md) is seamed with the maxilla (mx), thus forming a nutrition canal (nc). A venom canal (vc) runs within the maxilla; redrawn from Gaumont (1976) [email protected] 364 D. Zimmermann et al. 11.2.2 The Various Types—Shapes and Functions—Of the Sucking Tubes: Pragmatic and Phylogenetic Aspects Shape and function of the mouthparts can be categorized into various types. “Pierc- ing” jaws are stylets of different length, e.g. needle-like in Sisyridae and Osmylidae, or short in Coniopterygidae, Dilaridae and Berothidae in relation to the head (Fig. 11.4a–c). The representatives of all these families are special feeders preferring more or less sessile or “non-running away” prey. Apically curved jaws are weapons appropriate for catching and holding movable prey, preventing it from escaping. They are very impressive in Hemerobiidae and Chrysopidae (Fig. 11.1), and they may even be spectacular in certain Myrmeleontiformia (Figs. 11.2 and 11.4e). The larvae of Ithonidae are grub-like with corresponding stout sucking tubes hypothesized for sucking roots (Fig. 11.4f). Curved sucking tubes are interpreted as a plesiomorphic character state and straight stylets as apomorphic adaptations to diverse feeding conditions (Aspöck 1993). This conforms with the phylogenetic results in Aspöck and Aspöck (2008). Nonetheless, this character polarity continues to be discussed controversially (Winterton et al. 2018; Engel et al. 2018). MacLeod (1964) presents a very thorough study and discussion of larval heads and mouthparts; Aspöck and Aspöck (2007) give an overview. 11.2.3 The Maxillary Head The larval heads of all three orders of Neuropterida are prognathous, in contrast to the orthognathous heads of adult Neuroptera. While larvae of Raphidioptera and Megaloptera have biting mouthparts, Neuroptera feature the above-described extremely complex and diverse sucking tubes or sucking stylets. The mandible, though co-adapted with the maxilla to yield a curved or straight shape, remains simple. Not so the maxilla: only the distal part joins the mandible for the functional sucking tube. The basal parts of the maxillae, however, are immersed into the ventral side of the head capsule and comprise two closely connected sclerites. In Nevrorthidae, the ventral side of the compact head capsule is dominated by a large oval sclerite which is interpreted as the gula (Fig. 11.4d; Aspöck and Aspöck 2007; Beutel et al. 2010a). In the Myrmeleontiformia clade, the basal parts of the maxillae are reduced and shifted terminally; the same process occurred in the gula which, in addition, became extremely reduced (Fig. 11.4e) or completely lost (Fig. 11.4a, b, c, and f; MacLeod 1964; Aspöck and Aspöck 2007). The basal maxillary sclerites are integrated into the ventral side of the head, constituting the “maxillary head”, and can be present in two different specifications: either the “bow maxillary“ type (“Bogenmaxillen”-Typ, Aspöck 1993), e.g. in Osmylidae (Fig. 11.4a) and in Chrysopidae, or the “parallel maxillary“ type [email protected] 11 From Chewing to Sucking via Phylogeny—From Sucking to Chewing... 365 Fig. 11.4 Larval heads of Neuroptera, ventral view; (a) Osmylus fulvicephalus (Osmylidae), (b) Helicoconis sp. (Coniopterygidae), (c) Nallachius krooni (Dilaridae), (d) Nevrorthus fallax (Nevrorthidae), (e) Osmylops sp. (Nymphidae), (f) Polystoechotes punctata (Ithonidae). Redrawn from (a) Wundt (1961), (b, e, f) MacLeod (1964), (c) Minter (1992), (d) Zwick (1967). Schematic drawings: red—mandible, blue—maxilla, dark green—labium, light green—labial palpus, orange—gula [email protected] 366 D. Zimmermann et al. (“Parallelmaxillen”-Typ, Aspöck 1993), e.g. in Hemerobiidae, Berothidae, Dilaridae (Fig. 11.4c). 11.2.4 The Gula The presence of a gula (Fig. 11.4d, e) is traditionally considered a plesiomorphic character state that is homologous in Coleoptera and Neuropterida (e.g. Aspöck 1992; Beutel et al. 2010a). The gula “entered” neuropterology with the discovery of the larva of Nevrorthidae (Zwick 1967). The first treatment of the gula of Nevrorthidae as being homologous to the gula of Raphidioptera and Megaloptera started in the 1990s (Aspöck 1992). The compact head capsule of larval Nevrorthidae, with its large gula, represents the most archaic head type in Neuroptera. Nonetheless, recent interpretations (Winterton et al. 2018; Engel et al. 2018) treat the gula of Nevrorthidae and other Neuroptera as a “new adaptation”
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