Handbook of Zoology: Nannomecoptera and Neomecoptera 9783110272543, 9783110249040

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Handbook of Zoology Nannomecoptera and Neomecoptera

Handbook of Zoology Founded by Willy Kükenthal continued by M. Beier, M. Fischer, J.-G. Helmcke, D. Starck, H. Wermuth Editor-in-chief Andreas Schmidt-Rhaesa

Insecta Edited by Rolf G. Beutel and Frank Friedrich

DE GRUYTER

Nannomecoptera and Neomecoptera

Edited by Rolf G. Beutel and Frank Friedrich

DE GRUYTER

Scientific Editors Prof. Dr. Rolf G. Beutel Friedrich-Schiller-Universität Jena Institut für Zoologie und Evolutionsforschung Ebertstr. 1 07743 Jena Dr. Frank Friedrich Universität Hamburg Institut für Zoologie Martin-Luther-King-Platz 3 20146 Hamburg

ISBN 978-3-11-024904-0 e-ISBN (PDF) 978-3-11-027254-3 e-ISBN (EPUB) 978-3-11-038553-3 ISSN 2193-2824 Library of Congress Control Number: 2019938957 Bibliographic information published by the Deutsche Nationalbibliothek The Deutsche Nationalbibliothek lists this publication in the Deutsche Nationalbibliografie; detailed bibliographic data are available in the Internet at http://dnb.dnb.de. © 2019 Walter de Gruyter GmbH & Co. KG, Berlin/Boston Typesetting: Compuscript Ltd. Shannon, Ireland Printing and Binding: CPI books GmbH, Leck www.degruyter.com

We dedicate this volume to our friend and mentor Niels Peder Kristensen (1943–2014), former editor of the Insecta volumes of the Handbook of Zoology.

Preface The idea to work on a Handbook of Zoology volume on two small and obscure groups of holometabolous insects emerged at the 8th European Congress of Entomology held in 2006 in Izmir (Kuşadası). This international meeting was an excellent opportunity for inspiring discussions with Prof. Dr. Niels Peder Kristensen (1943–2014), out­ standing Danish entomologist, editor of the insect section of the Handbook of Zoology series (De Gruyter), and volume editor of two brilliant and comprehensive tomes on Lepi­ doptera (moths and butterflies). By that time, we were cooperating in a joint research project on the phylogeny of the megadiverse Holometabola. In his typical skepti­ cal manner, Niels Peder, mentor and friend of both of us, pointed out that not only will we be “confused on a higher level” at the end of our holometabolan investigations, but also that crucial problems in the phylogeny of the group will be linked with the two small taxa treated here. Conse­ quently, as editor of the Handbook series, he encouraged us to dedicate a separate volume to these two intriguing taxa. Nannomecoptera (Nannochoristidae) and Neomeco­ ptera (Boreidae) are very small holometabolous groups, together comprising fewer than 50 described species assigned to four presently recognized genera. Tradition­ ally, they were assigned to Mecoptera (scorpionflies, hang­ ingflies etc.), with ca. 600 described species, by far the smallest order of Antliophora, one of the major subunits of Holometabola, which also includes the ectopara­sitic Siphonaptera (fleas) and the megadiverse Diptera (true flies). The two groups treated in this volume were raised to ordinal rank by the eminent British entomologist Howard Everest Hinton (1912–1977), Nannomecoptera in 1958 in an important and often cited study “On the Phylogeny of Pan­ orpoid Orders” (=Mecopterida) and Neomecoptera in 1981, somewhat misplaced in a comprehensive work on “The Insect Eggs.” Both differ very distinctly from what may be casually addressed as “normal Mecoptera.” Nannomeco­ ptera resemble crane flies in their habitus, with thin and long legs and a seemingly fragile body. The very slender larvae are aquatic and differ strikingly in their morphol­ ogy from the terrestrial eruciform immature stages of Boreidae and Mecoptera in the narrower sense (=Pistil­ lifera). The adults completely lack the elongated rostrum, which is found in “typical” mecopterans like Bittacidae (hanging flies) or Panorpidae (scorpion flies) and also in the majority of Neomecoptera (Boreinae). The mouthparts, which are highly modified and only suitable for the uptake of liquid food, resemble those of some extinct groups

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found in Mesozoic deposits, including Burmese amber (Pseudopolycentropodidae). The sperm pump, a typical and epo­nymous feature of Antliophora (=pump bearers), differs distinctly from the condition in scorpionflies and related mecopteran taxa. Unlike Nannomecoptera and the vast majority of Pistillifera, all known species of Neomeco­ ptera are flightless, with wing rudiments transformed to claspers in males. The sperm pump is lacking completely. Unlike all other immature stages of Antliophora, the larvae of Neomecoptera possess well-developed stemmata. Species of Nannomecoptera and Neomecoptera belong to the insects considered as rare or extremely rare. Nannochorista, distributed in Chile, Australia, and New Zealand, is notoriously difficult to collect, and great efforts were necessary to obtain suitably fixed material of one species for a recent transcriptomic project (1KITE). Species of Boreus (Boreinae) are regularly found in suitable habi­ tats in the winter months. Caurinus dectes was considered as one of the rarest insects for a long time. Larger numbers were only collected in recent years by Loren Russell, who described the genus and species in 1979. A second species was discovered in 2010 in Alaska by Derek S. Sikes. We want to emphasize here that the constant support by Loren K. Russell was essential in different ways. Without his enormous contribution, the completion of this volume would have been greatly impeded, if not impossible. One of the most intriguing features of Nannomecop­ tera and Neomecoptera is the extreme difficulty in placing them reliably in the phylogenetic tree of Antliophora. Recent strong efforts to resolve the relationships of Mecop­ tera (in the widest sense), based on either detailed mor­ phological data, single genes, or transcriptomes, did not yield a robust solution. Ongoing efforts in the 1KITE Antli­ ophora subproject are based on very extensive transcrip­ tomic data sets with an extensive taxon sampling. Nev­ ertheless, the relationships of fleas, Nannomeco­ptera, Neomecoptera, and Pistillifera could not be resolved. Even though our own morphological investigations tenta­ tively suggested an inclusion of both taxa in monophyletic Mecoptera (in a broad sense), the most recent phyloge­ netic investigations suggest caution and a phylogeneti­ cally neutral retention of ordinal ranks for both groups. Even though Nannomecoptera and Neomecoptera are two comparatively well-studied groups with a very low diversity, this project turned out as very demanding and dragged on for over a decade. We want to emphasize and acknowledge gratefully at this point that this long-term

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 Preface

endeavor was very efficiently and patiently accompanied by several employees of De Gruyter publishing house, among them, for instance, Simone Witzel and Simone Pfitzner. The deplorable delay is due to different circum­ stances. One of them is increasing pressure in academia, leaving very little space for activities not directly related to research topics yielding high-ranking publications and funding. Another reason is the dwindling number of experts dealing with detailed anatomical studies of insect. Even though morphological investigations are obviously not the main focus of current research in entomology or

zoology, it is evident that understanding the evolution of any group on the phenotypic level is not possible without reliable and well-documented morphological data. This and the apparent phylogenetic key role of Nannomeco­ ptera and Neomecoptera encouraged us to undertake this endeavor. The results we present in this volume may con­ tribute to a better understanding of the early evolution of Antliophora, with more than 160,000 species, one of the most successful lineages of the entire insects. Rolf G. Beutel and Frank Friedrich

Contents Preface

vii

Rolf G. Beutel Pregenital abdomen 1.3.3

Nannomecoptera and Neomecoptera – an overview List of contributing authors

xiii

xv

1 Nannomecoptera, Nannochoristidae, Nannochorista 1

Phillip Suter & Rolf G. Beutel 1.2 Biology 1 Morphology of adults

Bożena Simiczyjew & Rolf G. Beutel 1.3.6 Ovaries 41

5

Rolf G. Beutel & Frank Friedrich 1.3.1 Head 5 1.3.1.1 Head capsule 5 1.3.1.2 Tentorium 6 1.3.1.3 Labrum 7 1.3.1.4 Antenna 7 1.3.1.5 Mandible 8 1.3.1.6 Maxilla 9 1.3.1.7 Labium 10 1.3.1.8 Epipharynx 13 1.3.1.9 Hypopharynx 13 1.3.1.10 Pharynx and esophagus 13 1.3.1.11 Salivarium 16 1.3.1.12 Cerebrum, suboesophageal complex, and stomatogastric nervous system 1.3.1.13 Glands 18 1.3.1.14 Circulatory system 18 1.3.1.15 Tracheal system 18 1.3.1.16 Fat body 18 Frank Friedrich & Rolf G. Beutel 1.3.2 Thorax 19 1.3.2.1 General appearance 19 1.3.2.2 Cervical region and prothorax 1.3.2.3 Mesothorax 22 1.3.2.4 Metathorax 25 1.3.2.5 Legs 29 1.3.2.6 Wings 30

Frank Hünefeld & Rolf G. Beutel Female postabdomen 1.3.4 31 External morphology 1.3.4.1 31 Internal parts of the genital system 1.3.4.2 Gerhard Mickoleit & Rolf G. Beutel 1.3.5 Male postabdomen 34 Segment VIII and genital capsule of 1.3.5.1 segment IX 34 Copulatory apparatus 1.3.5.2 34 1.3.5.3 Function 39

Rolf G. Beutel, Phillip Sutter & Frank Friedrich Taxonomy and distribution 1.1 1

1.3

31

19

1.4

16

Morphology of larvae

43

Rolf G. Beutel, Frank Friedrich, Hans Pohl & Niels P. Kristensen 1.4.1 Head 43 1.4.1.1 Head capsule, external features 43 1.4.1.2 Internal skeletal structures 45 1.4.1.3 Eyes 48 1.4.1.4 Labrum 49 1.4.1.5 Antenna 50 1.4.1.6 Mandible 50 1.4.1.7 Maxilla 51 1.4.1.8 Labium 53 1.4.1.9 Epipharynx 54 1.4.1.10 Hypopharynx 54 1.4.1.11 Cephalic digestive tract 55 1.4.1.12 Labial glands and salivarium 57 Nervous system 1.4.1.13 58 1.4.1.14 Aorta and retrocerebral organs 59 Fat body 1.4.1.15 59 Rolf G. Beutel & Frank Friedrich 1.4.2 Thorax 59 Maximilian Fraulob, Frank Hünefeld & Rolf G. Beutel 1.4.3 Abdomen 61 1.4.3.1 Abdominal segments I–IX 61

34

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 Contents

1.4.3.2 1.4.3.3 1.4.3.4

Abdominal segment X Anal papillae 65 Digestive tract 66

61

Frank Friedrich, Loren K. Russell & Rolf G. Beutel 2.3.2 Thorax 85 Cervical region and prothorax 2.3.2.1 85 2.3.2.2 Pterothorax 87 2.3.2.3 Legs 89 2.3.2.4 Wings 89

Rolf G. Beutel & Margarita Yavorskaya 1.5 Morphology of pupae 66 1.6 References

68

Frank Hünefeld & Rolf G. Beutel Pregenital abdomen 2.3.3

2 Neomecoptera, Boreidae, Caurininae, Caurinus 71 Loren K. Russell & Rolf G. Beutel 2.1 Taxonomy and distribution

71

Loren K. Russel 2.2 Biology 71 2.2.1 Climatic factors 71 2.2.2 Feeding 72 2.2.2.1 Adult feeding behavior 72 2.2.2.2 Larval feeding behavior 72 2.2.3 Host relations and ecology 73 2.2.4 Host phytochemicals 73 2.2.5 Parasites and predation 75 2.2.6 Locomotion 75 2.3

Morphology of adults

75

Frank Friedrich & Rolf G. Beutel 2.3.1 Head 76 2.3.1.1 Head capsule 76 2.3.1.2 Tentorium 77 2.3.1.3 Labrum 77 2.3.1.4 Antenna 78 2.3.1.5 Mandible 79 2.3.1.6 Maxillolabial complex 79 2.3.1.7 Epipharynx 81 2.3.1.8 Hypopharynx 82 2.3.1.9 Pharynx and oesophagus 84 2.3.1.10 Salivarium 84 2.3.1.11 Cerebrum, suboesophageal complex, and stomatogastric nervous system 84 2.3.1.12 Glands 85 2.3.1.13 Circulatory system 85 2.3.1.14 Tracheal system 85 2.3.1.15 Fat body 85

Frank Hünefeld & Rolf G. Beutel Female postabdomen 2.3.4 Frank Hünefeld & Rolf G. Beutel Male postabdomen 2.3.5

90

91

92

Bożena Simiczyjew & Rolf G. Beutel 2.3.6 Ovaries 93 Loren K. Russell & Rolf G. Beutel 2.3.7 Eggs 95 Romano Dallai, Loren K. Russell & Rolf G. Beutel 2.3.8 Spermatophore and spermatozoa

97

Loren K. Russell & Rolf G. Beutel 2.3.9 Organ systems 99 The digestive system and associated 2.3.9.1 organs 99 The nervous system 2.3.9.2 101 Rolf G. Beutel, Benjamin Fabian, Hans Pohl & Frank Friedrich 2.4 Morphology of larvae 101 2.4.1 Head 101 2.4.1.1 Head capsule 101 2.4.1.2 Tentorium 103 2.4.1.3 Eyes 104 2.4.1.4 Labrum 104 2.4.1.5 Antennae 104 2.4.1.6 Mandibles 104 2.4.1.7 Maxillolabial complex 104 2.4.1.8 Preoral cavity and mouth opening 106 2.4.1.9 Pharynx 106 2.4.1.10 Salivary system 107 2.4.1.11 Brain and suboesophageal ganglion 109

Contents 

2.4.2 Thorax 109 2.4.3 Abdomen 109 2.5 References

110

3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus 113 Rolf G. Beutel & Loren K. Russell Taxonomy and distribution 3.1

113

Loren K. Russell 3.2 Biology 114 3.2.1 Habitats 114 Life cycle 3.2.2 114 Mating and oviposition 3.2.3 115 Oviposition and fecundity 3.2.4 116 3.2.5 Egg development and eclosion 117 3.2.6 Larval biology 117 3.2.7 Pupation 118 3.2.8 Adult behavior 118 3.2.8.1 Activity 118 3.2.8.2 Adult feeding behavior 119 3.2.8.3 Predators and parasites 119 3.3

Adult morphology

120

Frank Friedrich & Rolf G. Beutel 3.3.1 Head 120 3.3.1.1 Head capsule 120 3.3.1.2 Tentorium 122 3.3.1.3 Labrum 122 3.3.1.4 Antenna 122 3.3.1.5 Mandible 122 3.3.1.6 Maxillolabial complex 124 3.3.1.7 Epipharynx 126 3.3.1.8 Hypopharynx 126 3.3.1.9 Pharynx and oesophagus 126 3.3.1.10 Salivarium 129 3.3.1.11 Cerebrum, suboesophageal complex, and stomatogastric nervous system 129 3.3.1.12 Glands and neurosecretory organs 129 3.3.1.13 Circulatory system 130 3.3.1.14 Tracheal system 130 3.3.1.15 Fat body 130

Frank Friedrich & Rolf G. Beutel 3.3.2 Thorax 130 General appearance 3.3.2.1 130 Prothorax and cervical region 3.3.2.2 3.3.2.3 Mesothorax 132 3.3.2.4 Metathorax 135 3.3.2.5 Legs 137 3.3.2.6 Wings 138 Rolf G. Beutel Pregenital segments I–VII 3.3.3 Frank Hünefeld & Rolf G. Beutel Female postabdomen 3.3.4 Rolf G. Beutel 3.3.5 Male genital segments

 xi

130

139

139

142

Bożena Simiczyjew & Rolf G. Beutel 3.3.6 Ovaries 143 Nobuo Suzuki, Loren K. Russell & Rolf G. Beutel 3.3.7 Eggs 146 Romano Dallai & Rolf G. Beutel 3.3.8 Spermatophores and Spermatozoa

146

Rolf G. Beutel & Kenny Jandausch 3.3.9 Digestive system 148 Rolf G. Beutel, Hans Pohl & Frank Friedrich 3.4 Morphology of larvae 149 3.4.1 Head 150 3.4.1.1 Head capsule 150 3.4.1.2 Tentorium 151 3.4.1.3 Light sense organs 151 3.4.1.4 Chaetotaxy 151 3.4.1.5 Labrum 151 3.4.1.6 Antennae 151 3.4.1.7 Mandibles 151 3.4.1.8 Maxillolabial complex 152 3.4.1.9 Preoral cavity and pharynx 152 3.4.1.10 Salivary ducts and glands 152 3.4.1.11 Brain, suboesophageal ganglion, and stomatogastric nervous system 3.4.2 Thorax 153

152

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 Contents

3.4.3 Abdomen 153 3.4.4 Postcephalic internal organs 153 Fat body 3.4.4.1 153 3.4.4.2 Postcephalic digestive tract and Malpighian tubules 153 Postcephalic nervous system 3.4.4.3 153 Tracheal system 3.4.4.4 154 Circulatory system 3.4.4.5 154 Rolf G. Beutel & Frank Friedrich 3.5 Morphology of pupae

154

Nobuo Suzuki & Rolf G. Beutel 3.6 Development 155 3.7 References

156

Rolf G. Beutel & Frank Friedrich 4 Phylogeny 159 4.1 References Index

163

160

Nannomecoptera and Neomecoptera – an overview Nannochoristidae (=Nannomecoptera) and Boreidae (=Neomecoptera) are traditionally assigned to the holo­ metabolan order Mecoptera. Both are presently in the focus of insect systematists. They differ strikingly from the “typical” mecopteran pattern, not only in their larval and adult morphology but also in their lifestyle and reproduc­ tive biology. Even recent analyses of extensive molecular data sets in the 1KITE project (www.1kite.org) could not clarify the phylogenetic affinities of the two taxa. Both of them display fascinating features, such as preferred

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temperatures of around 0°C in the case of Boreidae and extremely slender larvae adapted to running water in the case of Nannochoristidae. Despite the very low number of known species, there is no doubt that both groups are key taxa and in their own way highlights in the evolution of the extremely successful Holometabola. This and an impressive number of recent studies on various aspects of Nannochoristidae and Boreidae more than justify a new volume in the Handbook of Zoology series (De Gruyter) dedicated to these highly unusual taxa.

List of contributing authors Prof. Dr. Rolf G. Beutel Institut für Zoologie und Evolutionsforschung Friedrich-Schiller-Universität Jena Erbertstraße 1, 07743 Jena, Germany [email protected]

Dr. Gerhard Mickoleit Zoologische Schausammlung Universität Tübingen Sigwartstraße 3, 72076 Tübingen, Germany [email protected]

Prof. Dr. Romano Dallai Department of Evolutionary Biology University of Siena, Via A. Moro 2, I-53100 Siena, Italy [email protected]

PD. Dr. Hans Pohl Institut für Zoologie und Evolutionsforschung Friedrich-Schiller-Universität Jena Erbertstraße 1, 07743 Jena, Germany [email protected]

Benjamin Fabian, MSc Max Planck Institute for Chemical Ecology Beutenberg Campus, Hans-Knöll-Strasse 8, 07745 Jena, Germany [email protected]

Dr. Loren K. Russell 3420 SW Willamette Avenue, Corvallis, OR 97333, USA [email protected]

Maximilian Fraulob, MSc Südstraße 21, 07548 Gera, Germany [email protected] Dr. Frank Friedrich Institut für Zoologie Universität Hamburg Martin-Luther-King-Platz 3, 20146 Hamburg, Germany [email protected] Dr. Frank Hünefeld Am Anger 26, 07743 Jena [email protected] Kenny Jandausch, MSc Institut für Zoologie und Evolutionsforschung Friedrich-Schiller-Universität Jena Erbertstraße 1, 07743 Jena, Germany [email protected] Prof. Dr. Niels P. Kristensen Natural History Museum of Denmark University of Copenhagen Universitetsparken 15, DK-2100-Copenhagen, Denmark

Dr. hab. Bożena Simiczyjew Department of Animal Developmental Biology Institute of Experimental Biology University of Wroclaw Sienkiewicza 21, 50-335 Wroczlaw, Poland [email protected] Dr. Phillip Sutter Ecology, Environment and Ecology La Trobe University University Drive, Wodonga 3690, Australia [email protected] Prof. Dr. Nobuo Suzuki Department of Movement Sciences Japan Women’s College of Physical Education Kitakarasuyama 8-19-1, Setagaya-ku, Tokyo 157-8565, Japan [email protected] Dr. Margarita Yavorskaya Department of Biology II Functional Morphology Group, Ludwig-Maximillians-Universität München Großhaderner Straße 2, 82152 Planegg-Martinsried, Germany [email protected]

1 Nannomecoptera, Nannochoristidae, Nannochorista Rolf G. Beutel, Phillip Sutter & Frank Friedrich

1.1 Taxonomy and distribution Nannomecoptera was introduced as an independent order in the second volume of H.E. Hinton’s Biology of Insect Eggs (as “Nonnomecoptera”; Hinton 1981: p. 722), as pointed out in Engel and Kristensen (2013), a “most unlikely place for a taxonomic action of that kind.” Hinton (1981) noted that the larvae “are in nearly every way more primitive than any other known larvae of the whole assembly.” After examining immature stages, he was convinced that the group has “nothing to do with Mecoptera” (N.P. Kristensen, personal communication; see Engel & Kristensen 2013). Whiting (2002), even though assuming the non-monophyly of Mecoptera with Nannochoristidae and Boreidae forming a clade with fleas, emphasized that the ordinal status suggested by Hinton (1981) was based on “phenetic differences” rather than on a phylogenetic scheme of argumentation. Nannomecoptera was treated as a suborder by Willmann (1987), who also used this name in a later publication but without assigning a formal rank to the group (Willmann 1989). As pointed out by Kristensen (1989) (see also Engel & Kristensen 2013), the treatment as a separate order did not win general acceptance. Nevertheless, it is still phylogenetically ­ justified considering the apparent isolation of Nannochoristidae (and Boreidae) from the bulk of Mecoptera, i.e. the monophyletic Pistillifera (e.g. Whiting 2002, Beutel et  al. 2011, Friedrich et al. 2013). The precise position of the group is still uncertain, even after thorough analyses of extensive molecular data sets (e.g. Misof et al. 2014; see also Fabian et al. 2015). The family Nannochoristidae was already introduced by Tillyard (1917), who described four species occurring in southeastern Australia and Tasmania: Nannochorista ­dipteroides Tillyard 1917 (Tasmania), N. eboraca Tillyard 1917 (New South Wales), N. holostigma Tillyard 1917 (Tasmania), and N. maculipennis Tillyard 1917 (Tasmania). Three species are known from South America (Byers 1989), N. andina Byers 1989 (western Argentina, Neuquén), N. edwardsi Kimmins 1929 (western Argentina, Chile), and N. neotropica Navás 1929 (western Argentina, Neuquén, Chile, Arauco, LLanquihue, Chiloe, Magellanes [Tierra de Fuego]). Nannochorista philpotti (Tillyard 1917), the only described species from New  Zealand, was first placed https://doi.org/10.1515/9783110272543-001

in a separate genus ­Choristella (Tillyard 1917), and later renamed Microchorista (Byers 1974). Finally, ­Microchorista was synonymized with Nannochorista by Kristensen (1989), leaving only one extant genus.

Phillip Suter & Rolf G. Beutel

1.2 Biology

The biology of Nannochoristidae is still insufficiently known. Information on the small and fragile adults is very limited (e.g. Byers 1987), and direct observations on feeding habits are still lacking. Tillyard (1917) described in detail the mating behavior of the insects collected at Cradle Mountain, but the species is not recorded. “We also noticed the peculiar method of copulation, which resembles that of the Asilidae very closely. If a male and a female be put alive into a glass tube, the male at once seizes the female fiercely with his anal forceps, taking hold of her in any position haphazard. He then quickly moves his appendages to the posterior end of the body of the female, opening the forceps to a great width, and then closing them quickly upon the tip of her abdomen. The result is a lock-grip, the two insects facing in opposite directions. When once the male has got his correct hold, no amount of annoyance will persuade him to let go” (Tillyard 1917: p. 288). In contrast to all other mecopteran groups, the larvae, at least the first three of four instars, are fully aquatic (e.g. Pilgrim 1962, 1972, Williams 1968: p. 198, Riek 1970a, b, Byers 1991, Winterbourn 1982, Ferrington 2008). The first detailed account of larvae and pupae was presented by Pilgrim (1972). He collected immature stages of Nanno­ chorista philpotti Tillyard (as Choristella philpotti) (see Kristensen 1989) over a period of 14 years from a wide distribution in the South Island of New Zealand, but with a main focus on a small, slowly meandering stream in the Hawdon River valley (ca. 1 m wide, 25–30 cm deep, altitude ca. 550 m) (Pilgrim 1972). Nannochoristid larvae in New Zealand apparently have a preference for pools and quiet stretches of small woodland rivers (Fig. 1.2.1; Pilgrim 1972; D. Craig, personal communication) but also occur in springs on the Bogong High Plains (Victoria) in the Australian Alps at altitudes above 1700 m. Ferrington (2008) noted that a Tasmanian

2 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

Fig. 1.2.1: Collecting site of Nannochorista larvae. New Zealand, South Island, Banks Peninsula, Okuti Valley, Okuti Scenic Reserve, Okuti Creek (GPS. S43.78274 E172.83427, alt. 153 mabs, water 5.2°C, pH 8.9). Larvae of Nannochorista collected in sample of muddy sand from the side of the pool upper in the photo. It contained a very rich mayfly fauna and also tanyderid larvae. © D. Craig.

species (probably Nannochorista dipteroides Tillyard) occurred at the margins of riffle habitats in fast flowing streams. Systematic collections of macroinvertebrates for the Australian Monitoring River Health Initiative recorded occasional specimens from near sea-level to above the tree line, but numbers were low and certainly not in the abundances recorded in New Zealand streams (Winterbourne 1982). At the site intensively collected by Pilgrim (1972), much of the stream bed was covered with silt, apparently a typical condition, with large amounts of organic debris with abundant chironomid larvae. Other organisms collected with nannochoristid larvae by Pilgrim (1972) were aquatic nymphs and larvae of other groups of insects, nematodes, oligochaetes, mollusks, and hydrozoans. Winterbourn (1982) collected 3 years with grooved wooden sampling blocks in Middle Stream at Cass in the South Island of New Zealand. The collecting site at the small mountain river was located in a stand of Nothofagus ­solandri

(mountain beech). The average gradient of the stream was 1 in 3.5, and the stony, boulder-strewn bed was less than 2 m wide (Winterbourn 1982; see also Winterbourn 1976 for more details). Immature stages of Ephemeroptera, Plecoptera, Trichoptera, Coleoptera (Scirtidae), and Diptera (Tipulidae, Limoniidae, Chironomidae, ­Ceratopogonidae, Empididae, and Muscidae) were collected, and also ostracods, oligochaetes, planarians, nematomorphs, and nematodes (Winterbourn 1982). Larvae of Paucispinigera midae) were by far the approximate Freeman (Chirono­ most abundant species, with a  frequency of 30.7% compared to 2.2% for N. philpotti (­Winterbourn 1982). On the Bogong High Plains in Australia, the nannochoristid larvae were associated with groundwater-­ spring-fed pools, which had high fine particulate organic material overlying organic rich mud, and where the dominant vegetation was bryophytes, including Blindia robusta and Bartramia subsymmetrica. The ionic content of the pools was low, with conductivity below 10 μS cm−1, pH was below 5.6, and temperature varied little, ranging from 5.6 to 6.3°C. In these pools, the dominant macroinvertebrates were amphipods, with insects accounting for only 6.8% of the animals collected (Clements et al. 2016). Of the insects, the chironomid larvae Paralimnophyes (3.8%) and Paramerina (1.56%) and the marsh beetle larvae (­Scirtidae) (3%) were the most abundant taxa (Clements et al. 2016). The larvae observed by Pilgrim (1972) and one of us (PS) were very active and wriggling violently when disturbed. They progress with eel-like movements through the substrate with sinuous movements of the very elongate body, assisted by the short legs (Pilgrim 1972). Like in some other groups with aquatic larvae (Trichoptera, Corydalidae [Megaloptera], and Hydraenidae [Coleoptera, Staphylinoidea]), terminal abdominal hooks are present and are probably used for temporary anchorage in the substrate. Larvae suspended in water sink, but sinuations of the body allow some progress. They have never been observed to ascend toward the water surface (Pilgrim 1972). The campodeiform and prognathous larvae appear to have a varied diet, with those in New Zealand streams, and possibly also Australian rivers, being predaceous, although those found in the Alpine mountain pools in the Australian Alps feed mainly on fine organic material, and may be omnivorous. Pilgrim (1972) noted that they are very sensitive to movements of prey disturbing the silt and attack swiftly, and although detailed observations on the feeding process are not available, Pilgrim (1972) and Winterbourn (1982) confirmed that the main food source of N. philpotti larvae was the immatures of Chironomidae. Eighteen out of 20 prey items were chironomid larvae in guts of six specimens dissected by Winterbourn (1982).

1.2 Biology 

Ephemeropteran nymphs and larvae of other groups of Diptera apparently also belong to the prey spectrum and possibly also other aquatic organisms occurring in the same habitat (Winterbourn 1982). Tubificid worms have been recorded in larvae collected from Tasmanian streams. The postembryonic development comprises four larval stages and the pupa (for measurements for N. ­philpotti, see Pilgrim 1972: p. 160). The first three instars are completely aquatic and apneustic, with spiracles only visible as very small (ca. 5 µm diameter) stigmatic scars on the pro- and mesothorax and abdominal segments I–VII (Pilgrim 1972). Gas exchange apparently takes place at the surface of the extremely slender body. The two finger-like eversible anal papillae are very likely not involved. They are not differentiated as tracheal gills and contain only fine tracheal branches. The lumen of each of them is filled with hemolymph and blood cells and contains a Malpighian tubule (Pilgrim 1972, Fraulob et al. 2012). It was suggested by Pilgrim (1972) that the very thin-walled appendages serve as sites for the exchange of solutes like anal papillae occurring in aquatic nematoceran larvae (Wigglesworth 1950). The early fourth instar larvae are generally similar to the earlier stages but differ in size and proportion and also in coloration, which is paler overall (Pilgrim 1972). The most notable difference is the presence of open and functional spiracles. The later fourth larval instar is called prepupa and differs distinctly morphologically and in its behavior (Pilgrim 1972). The coloration of the body changes due to underlying fatty material, with the spiracles now standing out conspicuously. Dark brown areas form on the dorsal side of the meso- and metathorax and abdominal segments I–IX. The meso- and metathorax appear swollen due to the developing anlagen of the adult legs and wings. The larval legs appear strongly swollen at their base but are still functional. The fourth instars leave the silt substrate of the water and the prepupae are

 3

found in very damp vegetation (e.g. moss) or sometimes also under bark of partly submerged logs, always above the water level, but usually within 10–20 cm. The body of the prepupae appears C-shaped and they wriggle actively when disturbed. Those placed in soil or under a bark produce a specific cell by excavating the underlying substrate, whereas this is apparently not the case in prepupae lying in moss (Pilgrim 1972). The pupae (not recorded in Australia yet) are pale in the earlier stages of pupation, and the dark coloration in  the later stadium is due to the pigmentation of the pharate adults below the transparent pupal cuticle (Pilgrim 1972). Movability increases due to the activity of the pharate adults. Vigorous wriggling movements occur more and more frequently and finally lead to the rupture of the pupal cuticle on the dorsal side from the posterior metathorax to the head, along the median line on the thoracic segments and along the coronal and one of the frontal sutures on the head. After this, the adults emerge from the pupal skin (Pilgrim 1972). The small (ca. 7–10 mm body length) and rather fragile adults occur close to open water (Byers 1991), where larval development takes place. Species of Nan­ nochorista can be quite common in riparian vegetation in south-eastern Australia, according to Byers (1991). They may congregate in high numbers (Tillyard 1917), but considering there are only 52 records of adults in the Australian museums and National Insect Collection, the term “common” may be an exaggeration. They have two periods of emergence in late spring and in autumn, with two generations per year as in many species of Panorpa in North America (Byers 1991). No observations are available on the feeding habits. However, morphological features of the head described in detail by Beutel and Baum (2008) (see Section 1.3.1) clearly indicate that they exclusively feed on fluids, probably mainly nectar. The females deposit up to 25 eggs end-to-end on moist leaf litter at the river edges.



1.3 Morphology of adults 

1.3 Morphology of adults Adults of Nannochorista (Fig. 1.3.1) are very slender and long-legged, resembling a crane fly in their habitus. In contrast to most mecopterans, they lack a rostrum. Wings are normally developed in both sexes. A distinctly developed genital capsule is present in males. Rolf G. Beutel & Frank Friedrich

1.3.1 Head (based on Beutel & Baum 2008) 1.3.1.1 Head capsule The head is orthognathous. The posterior region is fully exposed and the foramen occipitale is strongly narrowed (Figs. 1.3.1.1 C and 1.3.1.10 B). The head capsule is well ­sclerotized (Fig. 1.3.1.9). Most parts are densely covered with thin and very short setae, but the vestiture is sparse or almost absent in the area ventrally of the paired ocelli, the postgenal region, and the dorsal part of the posterior plate (see Labium), which forms the ventral closure of the head pts

fw hw nt1

ant

mxp fem gst tibs

tib tar

Fig. 1.3.1: Nannochorista sp., female, lateral view. Abbreviations: ant – antenna, fem – femur, fw – forewing, gst – gonostylus, hw – hindwing, mxp – maxillary palp, nt1 – pronotum, pts – pterostigma, tar – tarsus, tib – tibia, tibs – tibial spur. © Frank Hünefeld.

 5

(Fig. 1.3.1.1). More widely spaced long setae are present on the latter two areas, on the vertex, on the clypeus, and on the preocular part of the gena (Figs. 1.3.1.1 and 1.3.1.2 A). In frontal view, the head capsule is broadly oval. The very large, nearly round, multifaceted compound eyes occupy approximately half of the entire surface of the head (Figs. 1.3.1.1, 1.3.1.7 and 1.3.1.10). They are very slightly emarginated above the antennal bases and internally enclosed by a high circumocular ridge (Figs. 1.3.1.9 A–E, 1.3.1.10, and 1.3.1.11 A,C). Three large ocelli with distinctly convex cuticular lenses are arranged as an equilateral triangle on the anterior head region (Figs. 1.3.1.1 A,B, 1.3.1.9 C,E, 1.3.1.10 A, and 1.3.1.11 A). The pigmentation between them is darker than on the other areas. The single median ocellus is slightly smaller than the others. The lateral ocelli are separated by a very indistinct coronal suture, which reaches the postocciput posteriorly (Fig. 1.3.1.1 A). The vestigial frontal sutures meet with each other and with the coronal suture within the ocellar triangle (Fig.  1.3.1.1  A). They are obliterated ventrally. A well-developed ­internal median frontal apodeme reaches the frontoclypeal suture anteriorly (Figs. 1.3.1.1 A, 1.3.1.4 C, 1.3.1.5, and 1.3.1.11  C). It is Y-shaped in cross section ventrally but a simple ridge above the interantennal frontal constriction (Figs. 1.3.1.8 F and 1.3.1.9 A,B). The triangular frontal area below the antennal bases is very small. The large and strongly convex clypeus is posteriorly delimited by a deep inverse U-shaped furrow representing the transverse epistomal strengthening ridge (=frontoclypeal ridge; Fig.  1.3.1.2 A). A short, transverse anteclypeus is separated from the postclypeus by a medially interrupted transverse fold (Fig. 1.3.1.2 A). The following trapezoid element likely represents a separate proximal part of the labrum (Figs. 1.3.1.1 A, 1.3.1.2 A, and 1.3.1.3 C). It cannot be fully excluded that this is also a part of the anteclypeus (Beutel & Baum 2008). However, considering the sclerotization of the cuticle and the absence of a subdivided anteclypeus in other insects, this interpretation appears unlikely. The genal region posterior to the secondary mandibular articulation forms an apically pointed process (Figs. 1.3.1.1 B,C, 1.3.1.2 A, 1.3.1.3 A, and 1.3.1.10). A subgenal suture is not recognizable. The subgenal region is likely represented by a small area between the anterior tentorial groove and the genal process. A postgenal bridge is probably not developed. An undivided posterior plate with unclear homology is adjacent with the foramen occipitale. It is distinctly separated from the postgenal region by lateral ridges and folds (Figs. 1.3.1.1 C, 1.3.1.2 C, 1.3.1.10 B, and 1.3.1.11), and any traces of a median connecting line or zone of weakness are absent. The posterior tentorial grooves are fissure shaped and very distinct (Figs. 1.3.1.1 C,

6 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

mxp ped

foc

ptg

pger

loc

pp

sca

cd

cs lap lbr

lac

ant

pore

cly fap

A

fs

ant ped

moc

mt

st

cpe loc

pmt

gp

sca

ped

mxp cly

mxp

pore

lac lap

B

lbr lap

pmt

gp

C

lac lbr

ant

Fig. 1.3.1.1: Nannochorista neotropica, head, SEM. A, Frontal view; B, lateral view; C, posterior view. Abbreviations: ant – antenna, cd – cardo, cly – clypeus, cpe – compound eye, cs – coronal suture, fap – frontal apodeme, foc – foramen occipitale, fs – frontal suture, gp – genal process, lac – lacinia, lap – labial palp, lbr – labrum, loc – lateral ocellus, moc – median ocellus, mt – mentum, mxp – maxillary palp, ped – pedicellus, pger – postgenal region, pmt – prementum, pore – postoccipital region, pp – posterior plate, ptg – posterior tentorial groove, sca – scapus, st – stipes. Scale bars: 200 µm. Reprinted with modifications from Beutel and Baum (2008) with permission from John Wiley and Sons.

1.3.1.2 B, and 1.3.1.10 B). They enclose the caudal part of the posterior plate. The tentorial bridge divides the narrow foramen occipitale into an upper spindle-shaped ­alaforamen and a round lower neuroforamen (Fig. 1.3.1.10 B). The postoccipital region forms a roof-like extension above the alaforamen (Fig. 1.3.1.1 A,B). A separating line or suture between the occiput and postocciput is not present.

1.3.1.2 Tentorium The tentorium is formed by nearly straight, strongly developed rods connecting the large, round anterior pits with the fissure shaped posterior grooves (Figs. 1.3.1.2 A–C, 1.3.1.8 F, 1.3.1.10 A, and 1.3.1.11 A,C). The anterior part, i.e.

the section comprising the anterior arms and the corpora tentorii, is hollow and nearly round in cross section (Figs. 1.3.1.2 C, 1.3.1.8 F, 1.3.1.9 A,B, and 1.3.1.11 A,C). The lumen is narrowing posteriorly and the posterior arms are solid and flattened (Figs. 1.3.1.2 C, 1.3.1.9 C, and 1.3.1.11 C). The dorsal arms are very thin, ligament-like, and obliterated in macerated specimens (Figs. 1.3.1.10 A and 1.3.1.11 A,C). They originate at minute triangular processes on the dorsal side of the middle section of the tentorial rods (Fig. 1.3.1.2 D), run dorsad close to the brain (in front of the base of the optic lobes) and are attached to the head capsule just mediad the compound eyes by fibrillae. The well-developed tentorial bridge separates the alaforamen from the neuroforamen. It is completely separated from the base of the well-developed posterior arms (Figs. 1.3.1.10 B and 1.3.1.11 B,C).



1.3 Morphology of adults 

cpe

 7

cor

sca pcl

hc

fcs

cpe

atp

acl

cls

A

lbr

gp

lac

ata

C

pta ata

pger

ptg

pp

foc

B

D

Fig. 1.3.1.2: N. neotropica, tentorium, SEM. A, Ventrolateral view of head with clypeus and anterior tentorial pit; B, posterior view of head capsule with posterior tentorial groove; C, D, internal view on macerated specimen: C, sagittal section, overview; D, median view, detail of insertion site of dorsal tentorial arm (arrow). Abbreviations: acl – anteclypeus, ata – anterior tentorial arm, atp – anterior tentorial pit, cls – clypeolabral suture, cpe – compound eye, cor – circumocular ridge, fcs – frontoclypeal suture, foc – foramen occipitale, gp – genal process, hc – head capsule, lac – lacinia, lbr – labrum, pcl – postclypeus, pger – postgenal region, pp – posterior plate, pta – posterior tentorial arm, ptg – posterior tentorial groove, sca – scapus. Scale bars: 25 µm. Reprinted with modifications from Beutel and Baum (2008) with permission from John Wiley and Sons.

1.3.1.3 Labrum The labrum is divided into a trapezoid posterior part, which is connected with the anterior margin of the anteclypeus (see above; Fig. 1.3.1.2 A) and a narrow, tongue-like elongated anterior part (Fig. 1.3.1.3 A,C). The anterior part is distinctly higher than wide. On its ventral side, a halfpipe structure forms the labral food channel (Figs. 1.3.1.3 D, 1.3.1.5, and 1.3.1.8 A,B; see also Epipharynx). Musculature: absent.

1.3.1.4 Antenna The antenna is composed of 34 segments with a moderately dense vestiture of short and longer setae (Figs. 1.3.1

and 1.3.1.1). The insertion areas between the compound eye and the transverse epistomal ridge are almost contiguous (Figs. 1.3.1.1 A,B and 1.3.1.4 C). Two inconspicuous protuberances are present on the base of the scapus dorsomesally and ventrolaterally. They form a loose ­ articulation with corresponding indistinct notches of the antennal ring (Fig. 1.3.1.10 A). The connecting axis is oblique. A similar articulation is formed between the scapus and pedicellus, with projections on the lateral and mesal side of the pedicellus. Both basal antennal segments are about equally long, but the scapus is distinctly larger (Fig. 1.3.1.7). Scapus and pedicellus display a field of sensory hairs on the lateral base (Fig. 1.3.1.4 C). The first flagellomere is approximately one third longer than the cylindrical pedicellus, but only half as wide. The second flagellomere is half as long as the first. The following

8 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

lap

cly

mxp

lac

smj

lbr

ant

cpe

lbr

A

lap

md gp

pmt

C

lac lap lap lbr

fch

B

D

ppg

Fig. 1.3.1.3: N. neotropica, mouthparts, SEM. A, Lateral view; B, anterior view, details; C, dorsal view; D, posterior view. Abbreviations: ant – antenna, cpe – compound eye, cly – clypeus, fch – labral food channel, gp – genal process, lac – lacinia, lap – labial palp, lbr – labrum, md – mandible, mxp – maxillary palp, ppg – palpiger, pmt – prementum, smj – second mandibular joint. Scale bars: 50 µm. Reprinted with modifications from Beutel and Baum (2008) with permission from John Wiley and Sons.

22 antennomeres are of approximately equal size (Fig. 1.3.1.1 B). The distal eight flagellomeres are slightly smaller than the preceding segments. Musculature (Figs. 1.3.1.5, 1.3.1.8 F, 1.3.1.9 A,B, 1.3.1.10 A, and 1.3.1.11): M. tentorioscapalis anterior (M. 1), well-­ developed and fan shaped, without tendon, O (=origin): dorsal side of the anterior tentorial arm, I (=insertion): mesal margin of the scapal base; M. tentorioscapalis posterior (M. 2), well-developed, with a short tendon, O: dorsolaterally on the anterior tentorial arm (posterolaterally of M. 1), I: dorsolateral edge of the scapal base; M. tentorioscapalis lateralis (M. 3), absent; M. tentorio­ capalis medialis (M. 4), cranial rotator, short and flattened, O: frons, above the antennal opening, I: mesolateral edge of the scapal base (close to M. 2); M. scapopedicellaris lateralis (M. 5), compact, well-developed muscle, O: ventral part of the scapal base (dorsad the insertion of M. 1), I: ventrally on the base of the pedicellus; M. scapopedicellaris medialis (M. 6), well-developed, composed of

a larger dorsal and a smaller bundle, M. 6a, O: mesal part of the scapal base, I: mesally on the base of the pedicellus, M. 6b, O: dorsal face of the scapus, I: ventromesal edge of the pedicellus.

1.3.1.5 Mandible The symmetrical mandibles are visible in the lateral view as a narrow triangle between the clypeus and the lacinia (Fig. 1.3.1.3 A). A shallow concavity on the anterior side of the mandibular base is part of a modified secondary mandibular joint. It corresponds with a convexity on the ventral side of the anterior clypeus, close to its lateral margin and anterad the anterior tentorial grooves (Fig. 1.3.1.3 A). The ventral, primary mandibular joint is reduced. The basal part of the mandible is sclerotized. A mola is not developed. The distal parts cover the ventral opening of the epipharyngeal food channel (Figs. 1.3.1.5



1.3 Morphology of adults 

A

B

lap1

 9

lap1

lap2 pmt

lap2

mxp3

cly

fap

lbr

sen

ped

C

sca gp

cpe

D

Fig. 1.3.1.4: N. neotropica, details of labial palp and sensory fields, SEM. A, B, Labial palp: A, lateral view; B, mesal view; C, antennal base, dorsal view. Fields of sensilla marked by dotted circles; D, sensorium of third maxillary palpomere. Abbreviations: cly – clypeus, cpe – compound eye, fap – frontal apodeme, gp – genal process, lap1/2 – labial palpomere 1/2, lbr – labrum, mxp3 – maxillary palpomere 3, ped – pedicellus, pmt – prementum, sca – scapus, sen – sensorium. Scale bars: 50 µm. Reprinted with modifications from Beutel and Baum (2008) with permission from John Wiley and Sons.

and 1.3.1.8 A–C; see below). They are strongly flattened and unsclerotized. Incisivi are absent. Musculature: Mm. craniomandibulares internus/ externus (M. 11/M. 12), absent; M. hypopharyngomandi­ bularis (M. 13), absent; M. tentoriomandibularis (M. 14), represented by two extremely thin fibers accompanied by a nerve, O: ventral face of the anterior tentorial arm (close to anterior tentorial pit), I: inner surface of the ventral mandibular side.

1.3.1.6 Maxilla The maxillae are closely connected with the labium. Both elements together form a maxillolabial complex (Figs. 1.3.1.1 C, 1.3.1.6 B, and 1.3.1.10 B). The small cardo is recognizable as a convexity laterad the base of the mentum (Figs. 1.3.1.1 C, 1.3.1.6, and 1.3.1.10 B). Cardo

and stipes are almost completely fused with each other (Fig.  1.3.1.6). The stipes is composed of a narrow and elongate lateral basistipes and a broader mesal mediostipes, which is covered with short hairs and longer setae, and mesally connected with the lacinia (Fig. 1.3.1.6). The main part of the lacinia is a flattened vertical lamella (Figs. 1.3.1.1 B,C and 1.3.1.6) with a deep, narrow longitudinal furrow on the mesal site (Fig. 1.3.1.8 A,B). The galea is absent. The well-developed five-­segmented palp is inserted on the distal margin of the mediostipes (Figs.  1.3.1.1, 1.3.1.3 A, and 1.3.1.6). It is densely covered with setae. The large proximal segment is approximately half as long as the second. Palpomere 1 is one third longer than 2 and has an irregularly annulated surface structure. A deep cavity with sensilla and a ventrally directed round opening is present at about midlength of the segment (Fig. 1.3.1.4  D). Palpomeres 4 and 5 are about as long as the second segment.

10 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

loc

moc

as 51a fb ceao

pcer

fb

fb 4 cor 41a sca

pch

2

52

1 fap

lm

ata 41b

ph 18

44 43

fg

lbr fch mxp

lac 35

soeg 29

sald

pph 33 37

md

Musculature (Figs. 1.3.1.5, 1.3.1.6, 1.3.1.8 C–F, 1.3.1.9 A,B, 1.3.1.10, and 1.3.1.11): M. craniocardinalis (M. 15), absent; M. tentoriocardinalis (M. 17), compact, O: anterior tentorial arm (close to anterior tentorial pit, opposite to M. 1), I: apodeme of the sclerotized part of the mesal cardinal base; M. tentoriostipitalis (M. 18), laterally flattened, O: ventral face of the anterior tentorial arm, laterad M. 17, I: broadly on ridge between the prementum and stipes; M. craniolacinialis (M. 19), long and very thin, composed of only three thin fibers, O: posterolateral genal region, I: membranous base of the lacinia with a thin tendon; M. stipitolacinialis (M. 20), absent; M. stipitogalealis (M.  21), absent; M. stipitopalpalis externus (M. 22), strongly developed, O: stipital base, I: basal margin of palpomere 1 (opposite to M. 24a); M. stipitopalpalis internus (M. 23), absent; M. palpopalpalis maxillae primus (M. 24), composed of a larger and a very small subcomponent, O: ventrolaterally (M. 24a) and ventromesally (M. 24b)

Fig. 1.3.1.5: N. neotropica, head, sagittal section. Abbreviations: as – airsac, ata – anterior tentorial arm, ceao – cephalic aorta, cor – circumocular ridge, fap – frontal apodeme, fb – fat body, fch – labral food channel, fg – frontal ganglion, lac – lacinia, lbr – labrum, lm – longitudinal muscle of pharynx, loc – lateral ocellus, md – mandible, moc – median ocellus, mxp – maxillary palp, pcer – protocerebrum, pch – postcerebral pharyngeal pumping chamber, ph – pharynx, pph – prepharynx, sald – salivary duct, sca – scapus, soeg – suboesophageal ganglion, 1 – M. tentorioscapalis anterior, 2 – M. tentorioscapalis posterior, 4 – M. tentorioscapalis medialis, 18 – M. tentoriostipitalis, 29 – M. tentoriopraementalis inferior, 33 – M. praementopalpalis externus, 35 – M. palpopalpalis primus, 37 – M. hypopharyngosalivarialis, 41 – M. frontohypopharyngalis, 43 – M. clypeopalatalis, 44 – M. clypeobuccalis, 51 – M. verticopharyngalis, 52 – M. tentoriopharyngalis. Reprinted with modifications from Beutel and Baum (2008) with permission from John Wiley and Sons.

on the base of palpomere 1, I: laterally on the base of palpomere 2 with a common tendon; M. palpopalpalis secundus (M. 25), absent; M. palpopalpalis tertius (M. 26), O: mesal wall of palpomere 3, close to the round sensory organ, I: mesally on the base of palpomere 4; M. palpopalpalis quartus (M. 27), O: mesal wall of palpomere 4, I: mesally on the base of palpomere 5.

1.3.1.7 Labium Most parts of the labium are weakly sclerotized. It cannot be fully excluded that the submentum is represented by the posterior plate (see above); however, considering the articulation of the cardines, this interpretation appears unlikely. The submentum is probably not present as a separate structure; the usually associated M. submentopraementalis is absent (see below). The strongly elongated



1.3 Morphology of adults 

9F

A

9E

mxp

9D

sen

st

lac

18

17

9C

9A

B

 11

pmt

lap

lac

33

st

22

9B

cd

8F 8E

17

8D

18

8C 8B

sen

8A mxp Fig. 1.3.1.7: N. neotropica, head, 3D reconstruction, lateral view. Positions of cross sections presented in Figs. 1.3.1.8 and 1.3.1.9 are indicated by dotted lines. Fig. 1.3.1.6: N. neotropica, maxillolabial complex. A, Lateral view; B, inner view. Abbreviations: cd – cardo, lac – lacinia, lap – labial palp, mxp – maxillary palp, pmt – prementum, sen – sensorium of maxillary palp, st – stipes, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 22 – M. stipitopalpalis externus, 33 – M. praementopalpalis externus. Scale bar: 200 µm. Reprinted with modifications from Beutel and Baum (2008) with permission from John Wiley and Sons.

narrow element between the maxillae contains the indistinctly separated mentum (or postmentum) and prementum (Fig. 1.3.1.1 C). It is separated from the posterior plate by a very deep membranous fold. The posterior part is closely connected with the basal parts of the maxilla. The parallel-sided prementum is medially cleft at its apex. The inner surfaces of this divided apical region are membranous and hold the apical vertical parts of the lacinia in their position. Paraglossae and glossae are not  developed. The two-segmented palp (Figs. 1.3.1.3, 1.3.1.4 A,B, and 1.3.1.6) is inserted on a membranous bilobed palpiger (Fig. 1.3.1.3 D, ppg). Palpomere 1 is about three times as long as wide and slightly widening distally (Fig. 1.3.1.4 A,B). Its mesal side is unsclerotized (Fig. 1.3.1.8 A). Palpomere 2 is approximately three times

as long as the basal segment and is covered with hairs on the medial side. Its proximal half is sclerotized, whereas the distal part is membranous (Fig. 1.3.1.4 A,B). In its distal third, palpomere 2 forms a spoon-like structure with a separate sclerite at its base and a medially oriented concavity (Figs. 1.3.1.3 D and 1.3.1.4 A,B). The surface of this area is densely covered with minute scales (Figs. 1.3.1.3 B, lap, and 1.3.1.4 B). The convex outer side is set with sort setae (Fig. 1.3.1.4 A). Musculature (Figs. 1.3.1.5, 1.3.1.8, and 1.3.1.9 A–C): M. submentopraementalis (M. 28), absent; M. tentoriopraementalis inferior (M. 29), a long and slender muscle, O: mesally on the posterior tentorial arm, I: apodeme of the posterolateral premental edge (between M. 22 and M. 33); M. tentoriopraementalis superior (M. 30), absent or completely merged with M. 29; M. praementoparaglossalis (M. 31), absent; M. praementoglossalis (M. 32), absent; M. praementopalpalis internus (M. 33), strongly developed, O: paramedially on the posterior labial element comprising the mentum and prementum, I: dorsomesally on the base of palpomere 1; M. praementopalpalis externus (M. 34), compact, O: paramedially on the distal part

12 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

mxp

fch

nlbr

lbr md

nmx

lbr

fch md

mxp

nmx

salch

lac 33/34

lac

salch 33

lap

A

B

pmt

nla

34

nlbr nmx

nla

md

gp

24a

lac

hy

33

C

cly

md

24a

24b

43

cly

fb

D

pmt

nmx

37 33

sald

34

cd

pmt

6b

ped

6b

sca

nan

6a

6a fap

5

nan

5 sca

41b

44

eph

nmd

43

atp

43

cly

ata

14

17

eph

19 22

E

18

cd

18 33

mt

sald

F

19 22 33

mt

sald

cd



of the labium, I: dorsolaterally on the base of palpomere 1; M. palpopalpalis labii primus (M. 35), well-developed, O: laterally on the base of palpomere 1, I: laterally on the base of palpomere 2; M. palpopalpalis labii secundus (M. 36), absent.

1.3.1.8 Epipharynx The entire epipharynx is completely devoid of microtrichia and most parts are sclerotized. Its distal part forms a ­cylindrical, ventrally open food channel on the ventral side of the narrow distal part of the labrum (Fig. 1.3.1.8 E,F). The opening of the channel widens toward the cibarium and it is divided by a low median ridge in its posterior sections. It is continuous with the concave roof of the open preoral chamber. Like the anterior part, this inter­ mediate section of the epipharynx is also sclerotized except for the membranous lateral margins. The thin but sclerotized posterior part is laterally connected with the posterior hypopharynx by a narrow semimembranous band. It forms the roof of the closed prepharyngeal tube. The walls of the tube are sclerotized. It is moderately long and U-shaped in cross section, and the lumen is very narrow (Fig. 1.3.1.8 A,B). Musculature (Figs. 1.3.1.5, 1.3.1.8 D–F, and 1.3.1.9 A, B): M. clypeopalatalis (M. 43), strongly developed, composed of many bundles and two major subcomponents, M. 43a, O: broadly on the anterior clypeus, I: roof of the anterior cibarium, M. 43b, composed of fewer individual bundles, but ca. three times as broad as M. 43a, O: posterior part of the clypeus, posterad M. 43a, I: roof of the prepharyngeal tube; M. clypeobuccalis (M. 44), O: immediately dorsad the last bundle of M. 43b, I: dorsal side of bucca, below M. transversalis buccae (see below) and the frontal ganglion.

1.3.1.9 Hypopharynx The hypopharynx is not present as a distinct individual structure but composed of three subunits, which are

1.3 Morphology of adults 

 13

more or less extensively fused with other structures. The distal part is fused with the anterior labium. The terminal section of the salivary duct lies within this combined structure. The intermediate part forms a flat lamella below the mandibles. Its anteromedian part is sclerotized (distal part of sitophore plate) and trapezoid in cross section and fits with the sclerotized mesal edges of the basal part of the mandible. The strongly sclerotized proximal part of the hypopharynx (proximal part of sitophore plate; Fig. 1.3.1.8 E,F) is laterally fused with the posterior ­epipharynx (see above). Both parts together form the closed prepharyngeal tube. The tube is approximately U-shaped in cross section and the walls are sclerotized (Fig. 1.3.1.9 A,B). The sclerotized upper edges may be ­considered as a derivative of the hypopharyngeal suspensorium. However, a typical suspensorial sclerite is not developed. Musculature (Figs. 1.3.1.5, 1.3.1.8 F, 1.3.1.9 A,B, 1.3.1.10 A, and 1.3.1.11 A,B): M. frontohypopharyngalis (M. 41), composed of three subcomponents, M. 41a, fan shaped, O: frontal apodeme, I: sclerotized upper edge of the posterior prepharyngeal tube, anterior to the anatomical mouth, M. 41b, strongly flattened, O: between the frontal apodeme and anterior tentorial pit, I: broadly on the lateral face of the prepharyngeal tube, M. 41c, extremely thin, O: distally on the anterior tentorial arm (mediad M. 1), I: prepharyngeal tube, close to M. 41b; M. tentoriohypopharyngalis (M. 42), absent. The muscle referred to as M. tentoriohypopharyngalis (M. 42) in studies on the head morphology of beetles and other insects (see e.g. Beutel et  al. 2009) functions as a tentorial retractor of the hypopharynx but is homologous to von Kéler’s M. tentoriobuccalis anterior (M. 48) (von Kéler 1963). M. tentoriobuccalis anterior lies within the circumoesophageal connectives, whereas M. tentoriohypopharyngalis lies laterally of them.

1.3.1.10 Pharynx and oesophagus The anterior part of the pharynx is strongly narrowed between the brain and the suboesophageal complex (Figs. 1.3.1.5 and 1.3.1.11 B) and approximately quadran­gular

◂ Fig. 1.3.1.8: N. neotropica, head, histological cross sections. See Fig. 1.3.1.7 for positions. Abbreviations: ata – anterior tentorial arm, atp – anterior tentorial pit, cd – cardo, cly – clypeus, eph – epipharynx, fap – frontal apodeme, fb – fat body, fch – labral food channel, gp – genal process, hy – hypopharynx, lac – lacinia, lap – labial palp, lbr – labrum, md – mandible, mt – mentum, mxp – maxillary palp, nan – nervus antennalis, nla – nervus labialis, nlbr – nervus labralis, nmd – nervus mandibularis, nmx – nervus maxillaris, ped – pedicellus, pmt – prementum, salch – salivary channel, sald – salivary duct, sca – scapus, 5 – M. scapopedicellaris lateralis, 6 – M. scapopedicellaris medialis, 14 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 19 – M. craniolacinialis, 22 – M. stipitopalpalis externus, 24 – M. palpopalpalis primus, 33 – M. praementopalpalis externus, 34 – M. praementopalpalis internus, 37 – M. hypopharyngosalivarialis, 41 – M. frontohypopharyngalis, 43 – M. clypeopalatalis, 44 – M. clypeobuccalis. Scale bars: 50 µm.

14 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

fap ah ahm 1

6a nan

A

2

41b

43

ata

4

41b

41a

fap ahm

43

44

fg

2

cpe

1

17 18

fb nrec

19

33 ahm

sald

29 22 moc pcer

pph

B

ata soeg

pph

sald 29 pcer

ceao

cor

cor

19

17

nrec

cpe

onp lm pta

ceao

C

ph nrec

cor

pch

51a

sald

loc

D

29 ceao

soeg ptg

nret

52b

cm

sald

fb

cpe

52a

as

51b

pcer cm

lm

E

fb

52a sald

cco

51a

tra

pch

F

foc

51c

Fig. 1.3.1.9: N. neotropica, head, histological cross sections. See Fig. 1.3.1.7 for positions. Abbreviations: ah – antennal heart, ahm – antennal heart muscle, as – airsac, ata – anterior tentorial arm, cco – cervical connective, ceao – cephalic aorta, cm – circular muscle fibers, cor – circumocular ridge, cpe – compound eye, fap – frontal apodeme, fb – fat body, fg – frontal ganglion, foc – foramen occipitale, lm – longitudinal muscle fibers, loc – lateral ocellus, moc – median ocellus, nan – nervus antennalis, nrec – nervus recurrens, nret – nervus retrocerebralis, onp – optic neuropils, pcer – protocerebrum, pch – postcerebral pumping chamber, ph – pharynx, pph – prepharynx, pta – posterior tentorial arm, ptg – posterior tentorial groove, sald – salivary duct, soeg – suboesophageal ganglion, tra – trachea, 1 – M. tentorioscapalis anterior, 2 – M. tentorioscapalis posterior, 4 – M. tentorioscapalis medialis, 6 – M. scapopedicellaris medialis, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 19 – M. craniolacinialis, 22 – M. stipitopalpalis externus, 29 – M. tentoriopraementalis inferior, 33 – M. praementopalpalis externus, 41 – M. frontohypopharyngalis, 43 – M. clypeopalatalis, 44 – M. clypeobuccalis, 51 – M. verticopharyngalis, 52 – M. tentoriopharyngalis. Scale bars: 100 µm.



1.3 Morphology of adults 

A

6b loc

4

cor

ah

41a

dta

cpe

19

nan 5

atp

14

fco 43 44 lap

mxp 51b

ata

41b

md

B

 15

lbr 51c

51a

52b

oes cco

52c

cpe

52a tb sald dta

ptg

29 19

pp

ata

cd

17

22

gp

24a

33

24b

pmt

mxp

34 lac

in cross section, without distinct folds, which usually serve for muscle attachment (Fig. 1.3.1.9 C). The inner surface is densely covered with minute tubercles bearing fine spines. The pharynx strongly widens in the posterior head region, where it forms a well-defined, thick-walled

Fig. 1.3.1.10: N. neotropica, head, 3D reconstructions (sclerotized skeleton – blue, eyes – light blue, musculature – orange, nervous system – yellow, digestive tract – green, circulatory system – red, salivary duct – pink). A, anterior view; B, posterior view. Abbreviations: ah – antennal heart, ata – anterior tentorial arm, atp – anterior tentorial pit, cco – cervical connective, cd – cardo, cor – circumocular ridge, cpe – compound eye, dta – dorsal tentorial arm, fco – frontal connective, gp – genal process, lac – lacinia, lap – labial palp, lbr – labrum, loc – lateral ocellus, md – mandible, mxp – maxillary palp, nan – nervus antennalis, oes – oesophagus, pmt – prementum, pp – posterior plate, ptg – posterior tentorial groove, sald – salivary duct, tb – tentorial bridge, 4 – M. tentorioscapalis medialis, 5 – M. scapopedicellaris lateralis, 6 – M. scapopedicellaris medialis, 14 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 19 – M. craniolacinialis, 22 – M. stipitopalpalis externus, 24 – M. palpopalpalis primus, 29 – M. tentoriopraementalis inferior, 33 – M. praementopalpalis internus, 34 – M. praementopalpalis externus, 41 – M. frontohypopharyngalis, 43 – M. clypeopalatalis, 44 – M. clypeobuccalis, 51 – M. verticopharyngalis, 52 – M. tentoriopharyngalis. Scale bars: 200 µm.

postcerebral pumping chamber, which is also quadrangular in cross section and densely covered with spiniferous tubercles (Figs. 1.3.1.5, 1.3.1.9 D,E, and 1.3.1.11). Distinct dorsolateral and ventrolateral folds serve as attachment areas for postcerebral dilators. The anteriormost

16 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

oesophagus, which enters the cervical region, is U-shaped in cross section. Musculature of the precerebral pharynx: Mm. frontobuccales anterior, posterior, and lateralis (M. 45/46/47), absent. Musculature of the postcerebral pharynx (Figs. 1.3.1.5, 1.3.1.9 D–F, 1.3.1.10 B, and 1.3.1.11): M. verticopharyngalis (M. 51), a strongly developed muscle complex composed of three subcomponents, M. 51a, three well-developed bundles, O: vertex, I: dorsolateral fold of the postcerebral pharynx, M. 51b, strongly developed, O: posterior genal region, I: postcerebral pharynx, together with the anteriormost bundle of M. 51a, M. 51c, posteriormost bundle of muscle complex, O: postoccipital region, rooflike extension above the alaforamen, I: dorsolaterally on the postcerebral pharynx, posterad M. 51a; M. tentorio­ pharyngalis (M. 52), strongly developed, composed of three subcomponents, M. 52a, very strongly developed, composed of a series of parallel bundles, O: postgenal region, lateral margin of the neuroforamen, I: ventrolateral fold of the postcerebral pharyngeal pumping apparatus, opposite to insertions of M. 51a and b, M. 52b, two well-developed bundles, O: lateral margin of the alaforamen, above the tentorial bridge, I: ventrolateral fold of the postcerebral pharyngeal pumping apparatus, opposite to insertion of M. 51c, M. 52c, few slender bundles, O: laterally on the postoccipital ridge, between the origins of the posterior tentorial arm and tentorial bridge, I: ventrally on the postcerebral pharynx (mediad M. 52a). Intrinsic musculature (Fig. 1.3.1.9 D,E): M. transversalis buccae (M. 67), a thin transverse muscle band extends over the dorsal wall of the anterior pharynx, immediately posterior to the anatomical mouth opening, above the insertion of M. 44; M. annularis stomodaei (M. 68), a typical ring musculature is not developed; very thin muscle bands attached to the upper edges of the anterior pharynx enclose only the lateral and ventral sides; the intrinsic musculature of the postcerebral pumping apparatus is similar in its attachment to the pharyngeal wall, but strongly developed; M. longitudinalis stomodaei (M. 69), a median longitudinal muscle is present on the dorsal side of the anterior pharynx; well-developed dorsal, ventral, and lateral longitudinal muscle bands are present below the ring musculature of the postcerebral pumping apparatus.

1.3.1.11 Salivarium The anterior part of the salivarium is represented by a narrow, moderately flattened tube with a sclerotized

ventral wall. It opens on the unsclerotized dorsal surface of the complex formed by the anterior hypopharynx and labium, below the posterior opening of the salivary channel formed by the mesal edges of the laciniae (Fig.  1.3.1.8 D). The salivary tube widens at the level of the mandibular articulation (Fig. 1.3.1.11 B). The posterior part is oval in cross section and nearly as broad as the prepharynx (Figs. 1.3.1.8 E,F, 1.3.1.9 A–E, and 1.3.1.10 B). The wall is thick and its inner surface is covered with minute tubercles carrying very fine spines. In the ­cervical region, the salivary tube splits into paired ducts, which form the connection with the salivary glands in the prothorax. Musculature (Figs. 1.3.1.5, 1.3.1.8 D, and 1.3.1.11 B): M. hypopharyngosalivarialis (M. 37), well-developed, O: ventral face of anterior labiohypopharyngeal complex, I: unsclerotized dorsal wall of anterior salivary duct; Mm. praementosalivariales anterior and posterior (M. 38/39), absent; M. annularis salivarii (M. 40), absent.

1.3.1.12 Cerebrum, suboesophageal complex, and stomatogastric nervous system The brain is large in relation to the head capsule. It is located in the anterodorsal area of the head capsule and fills out a large part of this region (Figs. 1.3.1.5, 1.3.1.10, and 1.3.1.11). The protocerebrum is not distinctly separated from the other parts of the brain. The corpora pedunculata, the central body, and the optic neuropils are well-developed (Fig. 1.3.1.9 C–E). The posterior face of the protocerebrum releases a pair of posteriorly directed nerves (nervus retrocerebralis) close to the midline (Figs. 1.3.1.9 E, 1.3.1.11 B, and 1.3.1.12 B). They extend posteriorly above the foregut and accompany the nervus recurrens (see below) toward the cervical region. The antennal nerves originating from the deutocerebrum are unusually large (Figs. 1.3.1.8 E,F, 1.3.1.10 A, 1.3.1.11 A,B, and 1.3.1.12 A). The tritocerebral commissure is not present as a separate structure. It is fused with the suboesophageal ganglion, which nearly fills out the entire space between the posterior salivarium, the posterior tentorial arms, and the pharynx. From the ventral side of the suboesophageal complex emerge four pairs of nerves of similar diameter; they innervate the labium, maxilla, mandible, and labrum, respectively (Fig. 1.3.1.12). The circumoesophageal connectives are very broad and short. The brain and the suboesophageal complex form a compact structure around the pharynx (Figs. 1.3.1.9 C, 1.3.1.11 B, and 1.3.1.12). The posterior part of the suboesophageal complex is continuous with a pair of strongly developed cervical



1.3 Morphology of adults 

loc

moc

2

cor

4

6b

51a

6a

51b

nan

51c

ped

pch

5 1

52b

41b

52a

43

cco

24a ata 19

17

A

34

loc

6a

33

14

cor 51a

51b

ph

pcer

51b 51c

4

52b

52a

fap cpe

sca

tb

soeg ped

41b

pp la

43

2

52c

1

sald

pta

eph 18

37

B

33

29

17

18 hy

pch

ata

5

44

51a

nret 51c

fg

ahm

dta

4 41a

29

pta

22

18

nrec

ahm

6b

 17

19

C

34

Fig. 1.3.1.11: N. neotropica, head, 3D reconstructions (sclerotized skeleton – blue, eyes – light blue, musculature – orange, nervous system – yellow, digestive tract – green, circulatory system – red, salivary duct – pink). A, lateral view; B, sagittal section; C, sagittal section, nervous system and musculature partly removed. Abbreviations: ahm – antennal heart muscle, ata – anterior tentorial arm, cco – cervical connective, cor – circumocular ridge, cpe – compound eye, dta – dorsal tentorial arm, eph – epipharynx, fap – frontal apodeme, fg – frontal ganglion, hy – hypopharynx, la – labium, loc – lateral ocellus, moc – median ocellus, nan – nervus antennalis, nrec – nervus recurrens, nret – nervus retrocerebralis, pcer – protocerebrum, pch – postcerebral pumping chamber, ped – pedicellus, ph – pharynx, pp – posterior plate, pta – posterior tentorial arm, sca – scapus, sald – salivary duct, soeg – suboesophageal ganglion, tb – tentorial bridge, 1 – M. tentorioscapalis anterior, 2 – M. tentorioscapalis posterior, 4 – M. tentorioscapalis medialis, 5 – M. scapopedicellaris lateralis, 6 – M. scapopedicellaris medialis, 14 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 19 – M. craniolacinialis, 22 – M. stipitopalpalis externus, 24 – M. palpopalpalis primus, 29 – M. tentoriopraementalis inferior, 33 – M. praementopalpalis internus, 34 – M. praementopalpalis externus, 37 – M. hypopharyngosalivarialis, 41 – M. frontohypopharyngalis, 43 – M. clypeopalatalis, 44 – M. clypeobuccalis, 51 – M. verticopharyngalis, 52 – M. tentoriopharyngalis. Scale bars: 200 µm.

18 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

noc

noc

nret

pcer

nrec

onp

fg

nlbr eph

A

pch

fco

nan npr

nla nmd nmx

nlbr

cco soeg

nmd nla

B

nmx

connectives (Figs. 1.3.1.9 D,E, 1.3.1.10 B, 1.3.1.11 A,B, and 1.3.1.12 B). The large frontal ganglion is connected with the tritocerebrum by very short and thick frontal connectives, which also release a second thin labral nerve (Figs. 1.3.1.5, 1.3.1.9 B, 1.3.1.10 A, 1.3.1.11 B, and 1.3.1.12 A). Anteriorly, a primarily unpaired nervus procurrens originates from the frontal ganglion (Figs. 1.3.1.11 B and 1.3.1.12 A). Distally, it divides into two branches, which are closely associated with the thin second pair of labral nerves (Figs. 1.3.1.11 B and 1.3.1.12 A). The unpaired nervus recurrens originates from the posterior end of the frontal ganglion and is enclosed by the cephalic aorta (Figs. 1.3.1.9 C–E, 1.3.1.11 B, and 1.3.1.12 B).

hy

Fig. 1.3.1.12: N. neotropica, central nervous system and gut, 3D reconstruction (nervous system – yellow, digestive tract – green). A, Anterolateral view; B, posterolateral view. Abbreviations: cco – cervical connective, eph – epipharynx, fco – frontal connective, fg – frontal ganglion, hy – hypopharynx, nan – nervus antennalis, nla – nervus labialis, nlbr – nervus labralis, nmd – nervus mandibularis, nmx – nervus maxillaris, noc – ocellar nerve, npr – nervus procurrens, nrec – nervus recurrens, nret – nervus retrocerebralis, onp – optic neuropils, pcer – protocerebrum, pch – postcerebral pumping chamber, soeg – suboesophageal ganglion. Scale bars: 100 µm.

these structures and are very distinctly narrowing posteriorly (Figs. 1.3.1.9 A–E and 1.3.1.11 C). The flattened posterior half of the muscle is adjacent to the lateral wall of the cephalic aorta and seemingly disintegrates as a structural unit between the strongly developed circular and longitudinal muscles of the postcerebral pharyngeal pumping chamber.

1.3.1.15 Tracheal system

The well-developed paired salivary glands are located in the prothorax.

A large trachea enters the head capsule medially and two pairs of larger and one pair of smaller tracheae laterally. The median trachea divides into two large air sacs posterior to the brain (Figs. 1.3.1.5 and 1.3.1.9 F). Two tracheae are present below the median fat body layer of the anterior surface of the brain, close to the median line. They unite below the paired ocelli and are posteriorly connected with the air sacs.

1.3.1.14 Circulatory system

1.3.1.16 Fat body

The cephalic aorta is wide and approximately quadrangular in cross section in the occipital region but more rounded and narrower below the brain (Figs. 1.3.1.5 and 1.3.1.9 C–E). The ventral wall is extremely delicate and appears attached to the musculature of the dorsal side of the pharynx. Well-developed antennal hearts are located between the antennal insertion area and the frontal apodeme (Figs. 1.3.1.9 A and 1.3.1.10 A). Dilator muscles of the antennal hearts originate broadly on

Smaller lobes of fat body are present between in the basal part of the mandible, between the salivarium and the prepharynx, in the frontal region, anterior to the brain, in the anteroventral and posteroventral head regions, and in the vicinity of the posterior tentorial arms (Figs. 1.3.1.5 and 1.3.1.9). The anteromedian and the anterolateral surface of the protocerebrum are covered by a layer of fat body. The fat body lobes are massively developed posterior to the brain.

1.3.1.13 Glands



Frank Friedrich & Rolf G. Beutel

1.3.2 Thorax (based on Friedrich & Beutel 2010) 1.3.2.1 General appearance The thoracic morphology of the species of Nannochorist­ idae is very uniform, differing only slightly in the proportions of the sclerites. The segments appear high in lateral view and narrow when viewed from above (Fig. 1.3.2.1). The nota, episterna, and coxae are distinctly sclerotized, whereas the remaining parts show a moderate to weak degree of sclerotization and pigmentation; sclerotized elements are often not clearly separated from adjacent membranous regions (Figs. 1.3.2.1 and 1.3.2.2). Externally visible membranous areas are largely constricted to the cervical/prothoracic region and the areas around the wing bases (Figs. 1.3.2.2 and 1.3.2.6); the intersegmental membranes are largely concealed, especially laterally due to the strongly inflected pleural sclerites (Fig. 1.3.2.1 B). 1.3.2.2 Cervical region and prothorax The prothorax and head are connected by an extensive cervical membrane (Figs. 1.3.2.1 B, 1.3.2.2, and 1.3.2.6), laterally stabilized by a pair of large, well-sclerotized lateral cervical sclerites (Figs. 1.3.2.1 B, 1.3.2.2, and 1.3.2.6 D). The tapering anterior half of these pear-shaped structures contacts the lateral part of the occipital ridge. The posterior rim of the expanded posterior half is closely connected with the propleuron (Fig. 1.3.2.6 D). A distinct, slightly sinuate longitudinal ridge along the internal face of the cervical sclerite forms a reinforced muscle attachment area (e.g. Ipcm2, Ivlm1, and Idvm7, see below). Dorsal or ventral cervical sclerites are not present. The distinctly sclerotized, saddle-shaped pronotum covers the dorsal half of the posterior prothorax (Figs. 1.3.2.1 and 1.3.2.2); its bulging anterior and posterior margins are distinctly delimited from the middle region by transverse transnotal lines (Figs. 1.3.2.1 and 1.3.2.2). The posterior transnotal line (Fig. 1.3.2.1 A) is laterally continuous with the posterolateral pronotal process (see below). Only the anterolateral pronotal edge contacts the dorsal propleural rim. Posterolaterally, the pronotum forms a long, horizontally orientated process below the first thoracic spiracle (Fig. 1.3.2.2); this structure is firmly connected to the anterior process of the mesepisternum (see below).

1.3 Morphology of adults 

 19

The propleural sclerite is composed of a quadrangular anterior and a triangular posterior part, externally demarcated by a strong vertical inflection (Fig. 1.3.2.2); the corresponding internal ridge stretches between the dorsal propleural margin and the pleuro-coxal joint; large parts of the ridge are fused with the tip of the profurcal arm (Fig. 1.3.2.3 D). The anterior propleural part is well sclerotized and its anterior and dorsal margins are distinctly thickened; in contrast, the posterior propleural portion is weakly sclerotized and partly semimembranous (Fig. 1.3.2.2); its posterior boundary is weakly defined. The externally visible part of the prosternum is mainly situated between the procoxae and is not connected to any other sclerite (Fig. 1.3.2.6 D). A discrete median longitudinal ridge starts at the anterior end of the internal prosternal surface (Figs. 1.3.2.3 and 1.3.2.5 A,B); between the coxae, it divides into two ridges, which merge with the anterior surface of the profurcal arms posteriorly. The profurca arises at the posterior area of the sternal plate and consists of two simple but strongly developed lateral arms (Figs. 1.3.2.3 and 1.3.2.5). Their tips are attached to the propleural apophyses (Fig. 1.3.2.3 D). The profurcal invaginations are clearly separated from each other. Spinasternum I is indistinguishably fused with the prosternal plate. A well-developed prospina is present immediately posterad the profurca at the posteriormost part of the plate (Figs. 1.3.2.3 and 1.3.2.5 C). The weakly sclerotized and slender protrochantin is embedded in the membranous area in front of the procoxa (Figs. 1.3.2.1 B and 1.3.2.2 A) but does not contact it; a coxo-trochantinal joint is therefore absent. No muscles are associated with the trochantin (see below). Musculature (Figs. 1.3.2.3 and 1.3.2.5): Dorsal longi­ tudinal muscles: Idlm1 M. prophragma-occipitalis, composed of two slender bundles with common insertion, O (=origin): Idlm1a: anterolateral edge of mesoscutum (laterad Idlm5), Idlm1b: anterior mesoscutal margin, close to midline (mediad Idlm5), I (=insertion): cervical membrane, close to dorsolateral edge of occiput. Idlm3 M. prophragma-cervicalis, O: anterolateral rim of the mesoscutum (laterad Idlm1a, mesad Idlm5), I: dorsolateral part of the cervical membrane. Idlm5 M. ­pronoto-phragmalis anterior, strong, broad muscle, O: anterior half of the pronotum, I: anterolateral mesoscutal margin (mediad Idlm1 and 3). Dorsoventral muscles: Idvm2/3 Mm. cervico-­ occipitales medialis/posterior, strongly developed, O: with two separate bundles from the posterior half of the lateral

20 

A pore

he

 1 Nannomecoptera, Nannochoristidae, Nannochorista

cvm

anp2

sclb2

sss2

sclb3

sss3

tns

nt1

sc2 teg2

axc2

scl2

pn2 sc3

scl3

pn3

pn3

tgI

tgII

pab2 aes2

aes3

apc2

em2

pes3

pes2

pl1

em3

apc3

mer3

lcv ti1 cx1

tr1

pcxs2 mer2 cx3

cx2

B

tr2

cervical sclerite, I: dorsolateral part of the postocciput (bundles completely fused). Idvm4 M. pronoto-­cervicalis lateralis, slender, O: dorsal area of the cervical membrane (anterolaterad pronotum), I: anterior process of the lateral

tr3

Fig. 1.3.2.1: Nannochorista neotropica, thorax, SEM. A, Dorsal view; B, lateral view. Abbreviations: aes2/3 – mes-/ metanepisternum, anp2 – anterior mesonotal process, apc2/3 – meso-/ metathoracic anapleural cleft, axc2 – mesothoracic axillary cord, cvm – cervical membrane, cx1/2/3, pro-/meso-/metacoxa, em2/3, mes-/metepimeron, he – head, lcv – lateral cervical sclerite, mer2/3 – meso-/metacoxal meron, nt1 – pronotum, pab2 – mesothoracic postalar bridge, pcxs2 – mesothoracic precoxal suture, pes2/3, meso-/ metathoracic preepisternum, pl1 – propleuron, pn2/3 – meso-/ metapostnotum, pore – postoccipital region, sc2/3 – meso-/metascutum, scl2/3 – meso-/metascutellum, sclb2/3 – lobe of meso-/metascutellum, sss2/3 – meso-/ metathoracic scuto-scutellar suture, teg2 – mesothoracic tegula, tgI/II – abdominal tergum I/II, ti1 – protrochantin, tns – transnotal suture, tr1/2/3, pro-/meso-/metatrochanter. Scale bar: 200 µm. Reprinted from Friedrich and Beutel (2010) with permission from John Wiley and Sons.

cervical sclerite (close to Ipcm2). Idvm7 M. pronoto-­ cervicalis posterior, well-developed, O: posterior part of the pronotum (laterad Idlm5), I: middle region of the longitudinal ridge of the lateral cervical sclerite (posterad



1.3 Morphology of adults 

sc3

scl2 pn2 pab2 pwp2

sa2

ba2 ppp spi1

ba3 pwp3

sa3 scl3

pn3

pab3

sc2 tgI

nt1

aes3

aes2

spiI

cvm apc2

em3

em2

lcv

pls3

apc3

pls2

pes3

pes2

pcxs3

pl1 st1

mer3

ti1

ti3

cx1

A

pcxs2 tr1

tr3

ti2 mer2 cx2

cx3

tr2

pcxr3

fu2

fu3

di3

pcxr2

mer3

mer2 di2 vsp2

vsp3

scj3

scj2

stcx3

stcx2

B

 21

tr2

C

tr3

Idvm4). Idvm10 M. profurca-phragmalis, O: posterior face of the propleural apophysis, I: anterolateral edge of the mesoscutum. Idvm17 or 18 M. pronoto-­coxalis posterior or lateralis, O: posterolateral edge of the pronotum, I: posterolateral part of the procoxal rim (posteroventrad ­pleuro-coxal joint). Tergo-pleural muscles: Itpm1 M. pleurocrista-occipitalis, O: dorsal propleural rim immediately in front of the propleural apophysis, I: lateral part of the occipital ridge (laterad Idvm2/3). Itpm3 M. pronoto-pleuralis ­anterior,

Fig. 1.3.2.2: N. neotropica, thoracic skeleton. A, Thorax, lateral view; B, mesothoracic sterno-coxal articulation, mesal view; C, metathoracic sterno-coxal articulation, mesal view. Abbreviations: aes2/3 – mes-/metanepisternum, apc2/3 – meso-/metathoracic anapleural cleft, ba2/3 – meso-/metabasalare, cvm – cervical membrane, cx1/2/3, pro-/meso-/metacoxa, di2/3 – meso-/ metathoracic discriminal ridge, em2/3 – mes-/metepimeron, fu2/3 – meso-/metafurca, lcv – lateral cervical sclerite, mer2/3 – meso-/metacoxal meron, nt1 – pronotum, pab2/3 – meso-/ metathoracic postalar bridge, pcxr2/3 – meso-/metathoracic precoxal ridge, pcxs2/3 – meso-/metathoracic precoxal suture, pes2/3 – meso-/ metathoracic preepisternum, pl1 – propleuron, pls2/3 – meso-/ metathoracic pleural suture, pn2/3 – meso-/ metapostnotum, ppp – posterior pronotal process, pwp2/3 – meso-/metathoracic pleural wing process, sa2/3 – meso-/ metathoracic subalare, sc2/3 – meso-/ metascutum, scj2/3 – meso-/metathoracic sterno-coxal joint, scl2/3 – meso-/ metascutellum, spi1/I – first thoracic / first abdominal spiracle, st1 – prosternum, stcx2/3 – sternocoxale of meso-/ metacoxa, tgI – first abdominal tergum, ti1/2/3 – pro-/meso-/metatrochantin, tr1/2/3 – pro-/meso-/metatrochanter, vsp2/3 – ventral sternal process of meso-/ metathorax. Scale bars: 200 µm. Reprinted from Friedrich and Beutel (2010) with permission from John Wiley and Sons.

strongly developed, O: lateral part of the pronotum (immediately laterad Idvm7), I: anteriorly on the dorsal propleural margin. Itpm4 or 5 M. pronoto-apodemalis anterior or posterior, moderately sized, O: lateral area of the pronotum (anterolaterad Itpm3), I: propleuron, posterior face of the invaginated apodeme. Sterno-pleural muscles: Ispm1 M. profurca-­apodemalis, absent (propleural apodeme fused with profurcal arm). Pleuro-coxal muscles: Ipcm2 M. procoxa-cervicalis transversalis, O: anterior edge of the procoxa, I: anterior

22 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

indistinct. The posterolateral mesoscutal edge forms the elongate posterior notal process (Fig. 1.3.2.4); its distal part is demarcated by an articulatory line but not separated from the main part as a discrete fourth axillary sclerite (Fig. 1.3.2.4). The scutoscutellar suture separates the posterior mesoscutal rim and the mesoscutellum (Figs. 1.3.2.1 A and 1.3.2.4). The almost rectangular middle part of the latter is well-developed and internally enclosed by a distinct ridge (Fig. 1.3.2.5 B). A thin lateral mesoscutellar process is proximally closely adjacent with the posterior notal process (Figs. 1.3.2.1, 1.3.2.2 A, and 1.3.2.4); distally, it is connected with the anal part of the wing by a strong ligament (=axillary cord). The large, ventrally directed meso­ postnotum is fused with the posterior scutellar margin, except for a median triangular membranous field (Figs. 1.3.2.1 A and 1.3.2.5 A,B). The middle region of the postnotum, which is ventromedially divided by a vertical notch, forms the attachment area of the pterothoracic dorsal longitudinal muscles (Figs. 1.3.2.5 A,B and 1.3.2.6 A,B, see below: II/IIIdlm1). A solid postalar bridge is formed by the connection between the lateropostnotum and the postero­ dorsal mesepimeral edge (Figs. 1.3.2.1 B and 1.3.2.2 A). The exposed position of large parts of the mesopostnotum results in a distinct separation between the pterothoracic segments. A well-developed tegula is located between the anterolateral mesoscutal rim and the anterior margin of the forewing (Figs. 1.3.2.1 B and 1.3.2.4). The arched ellipsoid sclerite is covered with setae of medium length. It interacts with the mesonotum through the small subtegula (Fig. 1.3.2.4). The mesothoracic wing base is formed by three distinct axillary sclerites. The first axillary is composed of a triangular body and an anteriorly directed neck (Fig. 1.3.2.4); the former articulates with the anterior notal process mesally and with the second axillary laterally, whereas the latter is directly adjacent with the wing. The 1.3.2.3 Mesothorax second axillary is a slightly curved, posteriorly broadThe mesonotum is large and of rhombic shape (Fig. ened sclerite articulating ventrally with the pleural wing 1.3.2.1 A). Distinct prescutoscutellar sutures delimit the process and mesally with the first axillary (Fig. 1.3.2.4). anterolateral mesoscutal edges from the prescutal areas; The lateral rim of the elongated, bar-shaped third axilthese strip-like sclerites lack prealar arms but are closely lary sclerite is connected with the anal field of the wing associated with the small subtegula. A distinct pro- (Fig.  1.3.2.4); posteriorly, it articulates with the similarly phragma is not developed; consequently, M. prophragma-­ shaped region equivalent with the fourth axillary, i.e. mesophragmalis is anteriorly attached to the strongly the movable distal part of the posterior notal process protruding part of the mesoscutum. Moderately devel- (see above). The distinct pleural suture is straight and nearly veroped mesoscutal lobes at the anterolateral edges serve as attachment areas for dorsoventral muscles (Fig. 1.3.2.5 tical (Figs. 1.3.2.1 B and 1.3.2.2 A). It separates the anterior A,B). The lateral mesoscutal margin forms a prominent episternal and the posterior epimeral part of the pleura anterior notal wing process (Figs. 1.3.2.1 A and 1.3.2.4). and connects the pleural wing process and the pleuThe tergal fissure (“Tergalspalt” of German authors) is ro-coxal joint. It is distinctly sunk below the external

process of the lateral cervical sclerite of the opposite side. Ipcm4 M. propleura-coxalis superior, composed of two strong bundles, O: anterodorsal and dorsal rim of the propleura, I: anterolateral part of the procoxa, in front of the pleuro-coxal joint. Ipcm8 M. propleura-­trochanteralis, O: ventral and anterior faces of propleural apophysis, I: trochanteral tendon (together with Iscm6). Ventral longitudinal muscles: Ivlm1 M. profurca-­ cervicalis, O: profurcal arm (laterad Ivlm3a), I: middle region of the internal longitudinal ridge of the lateral cervical sclerite. Ivlm3 M. profurca-tentorialis, two distinctly separated bundles, Ivlm3a O: anterior face of the profurcal arm (mediad Ivlm1), I: ventrolateral part of the foramen occipitale (close to the tentorial bridge), Ivlm3b O: profurcal arm (laterad Ivlm1), I: posteroventrally on the head capsule with a short tendon. Ivlm4 M. intrafurcalis, strongly developed, O: medial face of the profurcal arm, I: profurcal arm of the opposite side. Ivlm7 M. profurca-mesofurcalis, O: profurcal arm, I: mesofurcal arm. Ivlm9 M. prospina-mesofurcalis, very slender, O: prospina (immediately posterior of profurca), I: mesofurcal arm (together with Ivlm7). Sterno-coxal muscles: Iscm1 M. profurca-coxalis anterior, dorsoventrally flattened, fan shaped, O: broadly from the internal longitudinal ridge of the prosternum, I: anterior procoxal rim (close to Ipcm2). Iscm2 M. ­profurca-coxalis posterior, large, flattened, O: large parts of posterolateral profurcal surface, I: posterolateral part of the procoxal rim. Iscm3 M. profurca-coxalis medialis, small, short, O: proximal part of the profurca (mediad Iscm2), I: medial part of the procoxal rim. Iscm6 M. profurca-trochanteralis, closely associated with Ipcm8, ­ O: ventral side of the distal profurcal arm, I: trochanteral tendon.



1.3 Morphology of adults 

Idlm1a

A

B

Idlm1b he

cvm

tb

Idvm7

Idlm3

Idlm5

 23

Idvm10

Idvm4

ppp

Ivlm3a

Ivlm3b Ipcm2 Ivlm4

cx1

C pori

Ivlm9

nt2

Itpm3

Ivlm1 Iscm1

D

Itpm1

mr nt1

Itpm4/5

Ivlm7

Idvm 17/18

pl1 pore

spi1

fu1 Idvm2/3 sp1 Ipcm8

Iscm6

lcv Ipcm4a Ipcm4b

Iscm3 Iscm2

Fig. 1.3.2.3: Nannochorista dipteroides, prothoracic and cervical muscles. A–D, Mediosagittal sections, muscles subsequently removed. Abbreviations: cvm – cervical membrane, cx1 – procoxa, fu1 – profurca, he – head, lcv – lateral cervical sclerite, mr – median prosternal ridge, nt1/2, pro-/mesonotum, pl1 – propleuron, pore – postoccipital region, pori – postoccipital ridge, ppp – posterior pronotal process, sp1 – prospina, spi1 – first thoracic spiracle, tb – tentorial bridge. See text for muscle terminology. Scale bars: 100 µm. Reprinted from Friedrich & Beutel (2010) with permission from John Wiley and Sons.

pleural surface, resulting from a flexion of the posterior episternal and the anterior epimeral marginal regions (Fig.  1.3.2.1 B). The corresponding internal pleural ridge is well-developed and bears a long slender pleural arm at half-length (Fig. 1.3.2.6 B). Ventrally, a mesal extension

of the ridge forms the pleurocoxal joint (“ventraler Pleuralarm” of German authors). The anepisternal area is horizontally subdivided by a distinct anapleural cleft between its anterior margin and the pleural ridge (Figs. 1.3.2.1 B and 1.3.2.2 A). The dorsal part represents the

24 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

forms an anteriorly directed process, which is in contact with the elongated posterolateral part of the pronotum teg2 (Figs. 1.3.2.2 A, 1.3.2.5 B, and 1.3.2.6 B). The mesepimeron is 1ax about two thirds as long as the episternal parts; its curved dorsal margin forms the posterior part of the pleural wing process anteriorly but lacks a sclerotized connection with the subalare (Fig. 1.3.2.2 A). The mesally bent posterior epimeral rim forms the posterior closure of the anp2 sc2 lateral mesothorax (Fig. 1.3.2.5 C); the uppermost part of the inflected dorsal margin is elongated mesally and 2ax firmly fused with the mesothoracic lateropostnotum (postalar bridge, Figs. 1.3.2.1 A and 1.3.2.2 A). The ventral 4ax margin of the mesepimeron is strongly curved thus fitting sss2 to the lateral rim of the mesocoxal meron (Fig. 1.3.2.1 B). 3ax The ovoid subalare, embedded in the membrane between the mesepimeron and mesonotum, forms a muscle disc for the extrinsic muscles of the merocoxa (Figs. 1.3.2.2 A and 1.3.2.6 B); it bears anteriorly and dorsally directed scl2 processes. The preepisternal halves form the ventral wall of pnp2 the mesothorax (see e.g. Matsuda 1970). They contact each other ventromedially along the distinct discrimipn2 nal line, which corresponds with a well-developed interFig. 1.3.2.4: N. neotropica, mesothoracic wing base. Abbreviations: nal ­discrimen (Figs. 1.3.2.2 B and 1.3.2.5 A,B). The height 1/2/3/4ax – first/second/third/fourth axillary sclerite, of this median ridge increases posteriorly and it merges anp2 – anterior mesonotal process, pn2 – mesopostnotum, with the mesofurcal stalk at its posterior end. Anteriorly, pnp2 – posterior mesonotal process, sc2 – mesoscutum, the preepisternum is bent dorsad. A distinct triangular scl2 – mesoscutellum, sss2 – mesothoracic scuto-scutellar suture, katepisternum is delimited from the posterolateral preepi­ steg2 – mesothoracic subtegula, teg2 – mesothoracic tegula. sternal margin by the precoxal suture (=paracoxal suture Scale bar: 50 µm. Reprinted from Friedrich and Beutel (2010) with permission from John Wiley and Sons. of Matsuda 1970; Figs. 1.3.2.1 B and 1.3.2.2 A); it corresponds with an internal transverse ridge (=precoxal ridge) anepisternum (following the nomenclature of Matsuda (Fig. 1.3.2.5 A), which originates at the discrimen in front 1970), whereas the posterodorsal edge of this sclerite and of the mesofurcal stalk, runs laterad, and obliterates in the adjacent mesepimeron form the pleural wing process. the lateral preepisternal region (Fig. 1.3.2.2 B). The mesoThe anterior margin of the mesanepisternum is largely furca invaginates at the intersection of the precoxal suture fused with the basalar disc, except for an area delimited and discriminal line. The long and thin furcasternum by a short basalar cleft. The basalare consists of a bulging, between the mesocoxae is continuous with the discrimen slightly elongated disc, which is laterally connected with anteriorly. The ventral part of the furcasternum splits the dorsal part of the anepisternum and reaches down into two rods establishing the sterno-coxal joint with the to the anterior end of the anapleural cleft (Figs. 1.3.2.2 A ­mesothoracic sternocoxale (Figs. 1.3.2.2 B and 1.3.2.5 A). and 1.3.2.6 B). The basalar disc serves as attachment area The laterally flattened furcal stalk forms the largest part for muscles of the wing base and the coxa. The well-­ of the mesofurca; dorsally, it splits into two short, blunt developed basalar stalk arises at the uppermost point of furcal arms (Fig. 1.3.2.5). A mesospina is not developed. Musculature (Figs. 1.3.2.5 and 1.3.2.6 A,B): Dorsal lon­ the disc and is dorsally oriented. The preepisternum ventrad the anapleural cleft gitudinal muscles: IIdlm1 M. prophragma-mesophrag(Figs. 1.3.2.1 B and 1.3.2.2 A) is about twice as high as the malis, largest mesothoracic muscle, O: paramedially on anepisternum. The ventral half of the anterior preepi­ the protruding part of the mesoscutum, I: median region sternal rim (below the mesobalalare) is bent mesad and of the mesophragma. IIdlm2 M. mesonoto-­phragmalis, forms the anterior closure between the i­ntersegmental strongly developed, O: posterior half of mesoscutum membrane and the mesopleura; its dorsomesal edge (laterad IIdlm1), I: lateral part of the mesophragma steg2



1.3 Morphology of adults 

 25

Pleuro-pleural muscles: IIppm2 M. mesobasalare-­ (laterad IIdlm1). IIdlm3 M. mesoscutello-postnotalis, intersegmentalis, short, flattened, O: anteroventral rim of absent. Dorsoventral muscles: IIdvm1 M. mesonoto-sternalis, mesobasalare (ventrolaterad IItpm3), I: anteriormost part well-developed, O: anterolateral edge of the mesoscu- of mesopleuron, probably derivative of interpleurite I. Sterno-pleural muscles: IIspm1 M. mesopleura-­ tum (mesoscutal lobe), I: mesosternum immediately laterad mesosternal ridge and posterad precoxal bridge. sternalis, strongly developed flat muscle, O: anterior and IIdvm2 M. mesonoto-trochantinalis anterior, about lateral mesosternal regions (laterad IIdvm1), I: ventrolateral half the size of IIdvm1, O: lateral part of the mesoscu- rim of the mesobasalare. IIspm2 M. mesofurca-­pleuralis, tum (laterad IIdlm2, posterad IIdvm1), I: anterior well-developed, O: tip of the lateral mesofurcal arm, mesocoxal rim and medial-most part of the mesotro- I: mesopleural arm by means of a short tendon. Pleuro-coxal muscles: IIpcm2 M. mesobasalare-­ chantin. IIdvm4 M. mesonoto-coxalis anterior, modertrochantinalis, O: midpart of the mesobasalar disc ately sized, O: posterolateral area of the mesoscutum (posterad IIdvm7), I: medial part of the mesocoxal meron. (mediad IIspm1, laterad IIpcm5), I: anterior mesocoxal IIdvm5 M. mesonoto-coxalis posterior, absent. IIdvm6 rim (laterad IIdvm4). IIpcm4 M. mesanepisterno-­ M. ­mesocoxa-subalaris, very large muscle, O: large part coxalis posterior, flattened, fan-shaped, O: ventral of the posterolateral mesocoxal meron (ventrolaterad half of the mesanepisternum, I: anterolateral rim of IIdvm4), I: ventral side of the subalar muscle disc. IIdvm7 the mesocoxa (immediately laterad IIpcm3). IIpcm5 mesanepisterno-trochanteralis, slender, O: medial M. mesonoto-trochanteralis, strongly developed, O: central M. ­ part of the mesoscutum (posterad IIdvm2), I: trochanteral rim of the mesobasalare (mediad IIpcm3), I: trochanteral tendon (together with IIdvm7). tendon. IIdvm8 M. mesofurca-phragmalis, absent. Ventral longitudinal muscles: IIvlm3 M. mesofurcaTergo-pleural muscles: IItpm1 M. prophragma-­ mesanepisternalis, well-developed, O: lateral edge of the metafurcalis, moderately sized, O: posterior face of mesoprescutum, I: dorsal face of the mesobasalare. IItpm2 furcal arm, I: anterior face of metafurcal arm. Sterno-coxal muscles: IIscm1 M. mesofurca-coxalis M. mesopleura-praealaris, moderately sized, O: anepisternal face of the mesopleural ridge below the pleural wing anterior, very strongly developed muscle, composed of basalaris, several bundles with common insertion, O: discriminal process, I: subtegula. IItpm3 M. mesonoto-­ O: lateral mesoscutal rim, I: anteromedial edge of the ridge of the mesosternum and anterolateral face of the mesobasalare. IItpm4 M. mesonoto-pleuralis anterior, mesofurcal stalk, I: anteromesal edge of the mesocoxal largely fused with IItpm5, O: base of the mesopleural rim (mediad IIdvm2). IIscm2 M. mesofurca-coxalis posarm (laterad IItpm6) and episternal side of the pleural terior, three distinct bundles, IIscm2a, extremely thin, ridge, I: anterior part of the first axillary sclerite. IItpm5 O: posterior face of the mesofurcal arm (posterad IIscm4), M. ­mesonoto-pleuralis medialis, largely fused with IItpm4, I:  mesocoxal merocosta, IIscm2b, very slender, O: posO: base of the mesopleural arm (laterad IItpm6) and terior face of the mesofurcal arm (posterad IIscm6), episternal side of the pleural ridge, I: lateral mesoscu- I: merocosta (ventrad IIscm2a), IIscm2c, strong bundle, tal rim. IItpm6 M. mesonoto-pleuralis posterior, two O: posterior face of the mesofurcal stalk and proximal arms, bundles, IItpm6a, well-developed, conical, O: tip of I: merocosta (ventrad IIscm2b). IIscm3 M. mesofurca-­ the mesopleural arm (laterad IIspm2), I: fourth axil- coxalis medialis, flattened, O: posterior face of the mesolary sclerite, IItpm6b, very slender, O: posterior side furcal stalk, I: medial mesocoxal rim, posterad mesofurcal of the pleural ridge between the pleural arm and invagination. IIscm4 M. mesofurca-coxalis lateralis, pleural wing process, I: fourth axillary sclerite. IItpm7 O: ventral side of the distal mesofurcal arm, I: ventral M. ­mesanepisterno-axillaris, flattened but strongly devel- process of the pleural ridge. IIscm6 M. mesofurcaoped, O: mesanepisternum above the anapleural cleft, trochanteralis, well-developed, O: ventral face of the I: third axillary sclerite (together with IItpm9). IItpm9 mesofurcal arm (mediad IIscm4), I: trochanteral tendon M. mesepimero-axillaris tertius, small, triangular muscle, (together with IIdvm7 and IIpcm5). O: anterior face of the dorsal mesopleural ridge (opposite to IItpm2), I: third axillary sclerite, posterad IItpm7. IItpm10 M. mesepimero-­ subalaris, distinctly flattened, 1.3.2.4 Metathorax triangular, O: posterodorsal part of the mesepimeron, I: posterior edge of the subalare. IItpm11 M. mesopleura-­ The metathorax is very similar to the mesothorax in its shape and configuration. Therefore, only differences subalaris, absent.

26 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

scl2

sc2

sc3

scl3

IIdlm2 ssr2 IIdvm4 IIIdvm1 IIIdvm7 phr2 IIIdvm2 ssr3

IItpm1

pn3

IIdlm1

gut

IIdvm1

IIIdlm2

IIIdlm1

phr3

IIdvm2

apm IIspm2

prv fu1

fu3

ggl1

mr

ggl2

IIdvm7

mer3

pcxr2

scj3

vsp2

A

IIscm2a

vsp3

mer2

IIvlm3

Ivlm9

pcxr3 di2

IIIspm2

Ivlm7

di3

st1

IIIdvm6

IIspm1

IIIvlm2

ggl3

IIIdvm4

IIscm1

B

cx2

IIIscm2 IIscm3

cx3

IIIpcm2 IIpcm5 em2 IIIspm1 IIpcm2 IIIpcm5 plr2 pes2 IIdvm4 IIpcm4 plr3 IIspm1 pes3

IIIscm3

em3

IIdvm6

fu1

mer3 IIIdvm6

IIdvm7

IIdvm1

IIIdvm7

IIIdvm4

st1 IIIvlm2 ggl2

ggl1

C

Ivlm7

sp1

Ivlm9

IIdvm2 IIspm2 fu2

ggl3

IIIdvm1 IIIdvm2

IIIspm2

fu3

IIvlm3

Fig. 1.3.2.5: N. neotropica, anatomy of pterothorax, 3D reconstruction (sclerotized skeleton – blue, digestive tract – green, musculature – orange, nervous system – yellow). A, Mediosagittal section; B, mediosagittal section, inner muscle layer, gut, and nervous system removed; C, horizontal section below the pleural arms. Abbreviations: apm – anterior mesopleural process, cx2/3 – meso-/metacoxa, di2/3 – meso-/metathoracic discriminal ridge, em2/3 – mes-/metepimeron, fu1/2/3 – pro-/meso-/metafurca, ggl1/2/3 – pro-/meso-/ metathoracic ganglion, mer2/3 – meso-/metacoxal meron, mr – median prosternal ridge, pcxr2/3 – meso-/metathoracic precoxal ridge, pes2/3 – meso-/metathoracic preepisternum, phr2/3 – meso-/metaphragma, plr2/3 – meso-/metathoracic pleural ridge, pn3 – postnotum, prv – proventriculus, sc2/3 – meso-/metascutum, scj3 – metathoracic sterno-coxal joint, scl2/3 – meso-/metascutellum, sp1 – prospina, ssr2/3 – meso-/metathoracic scuto-scutellar ridge, st1 – prosternum, vsp2/3 – ventral sternal process of meso-/metathorax. See text for muscle terminology. Scale bars: 250 µm. Reprinted from Friedrich and Beutel (2010) with permission from John Wiley and Sons.



 27

1.3 Morphology of adults 

A

sc2

IItpm3

IItpm7

IItpm4+5

IIItpm7

C

sc3

IIItpm4+5

IIItpm3 IItpm1

IItpm6b

phr3

phr2 IItpm10 IIppm2

IItpm6a IIdvm6

IIpcm5

em2

pes2 IIspm1

B

IIpcm2 IItpm9

IIItpm1

IIItpm10

IIIpcm5

IIIdvm6 em3

IIIppm2 IIIpcm2

IIspm2

sa2 IItpm6b

IIItpm9

D

scl2

IIItpm2

IItpm2

IIIspm2 sa3

IItpm6a plr3 plr2

IItpm10

ba2 apm IItpm7 IIspm1

IIdvm6 pla2 IIspm2

ba3

IIItpm10

IIIspm1 apc3 pes3

IIIdvm6 pla3

Fig. 1.3.2.6: N. neotropica, wing base musculature, 3D reconstruction (sclerotized skeleton – blue, musculature – orange). A, B, Mesothorax; C, D, metathorax. Abbreviations: apc3 – metathoracic anapleural cleft, apm – anterior mesopleural process, ba2/3 – meso-/ metabasalare, em2/3 – mes-/metepimeron, pes2/3 – meso-/metathoracic preepisternum, phr2/3 – meso-/metaphragma, pla2/3 – meso-/ metathoracic pleural arm, plr2/3 – meso-/metathoracic pleural ridge, sa2/3 – meso-/metathoracic subalare, sc2/3 – meso-/metascutum, scl2 – mesoscutellum. See text for muscle terminology. Scale bars: 100 µm. Reprinted from Friedrich and Beutel (2010) with permission from John Wiley and Sons.

between the pterothoracic segments will be noted in the following. The metanotum is smaller than the mesonotum, but its anterior half is more complex (Fig. 1.3.2.1 A). The scutal lobes are very distinctly delimited from the rest of the metascutum (Fig. 1.3.2.1 A). A slightly curved parapsidal suture extends from the anterior metascutal margin to the scutal lobes posteriorly. The anteromesal part of the metascutum and the scutal lobes are internally separated

by an inflected bulge (Fig. 1.3.2.6 C,D). The prescutal area of the metanotum is comparatively small but bears a short prealar arm laterally. The distal part of the posterior notal process is detached from the proximal part, forming a fourth axillary sclerite. The metapostnotum, including the metaphragma, is shorter than its mesothoracic counterpart (Fig. 1.3.2.5 A,B); it is medially separated from the metascutellum by an extensive triangular membranous zone and posteriorly fused with abdominal tergite I

28 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

(Figs. 1.3.2.1 and 1.3.2.2 A). The metathoracic anepisternum, basalare, and subalare are similar to the corresponding elements of the mesothorax (Figs. 1.3.2.1, 1.3.2.2 A, 1.3.2.5, and 1.3.2.6). The posteroventral part of the metepimeron is comparatively short. The ventral part of the metathoracic preepisternum is also shortened. With its dorsoventral orientation, it reaches the level of the division of the mesofurcal arms; it is closely associated with the meron of the mesocoxa (Fig. 1.3.2.5 B). The distance between both dorsally directed metafurcal arms is about half as long as the distance between the mesofurcal arms (Fig. 1.3.2.5 C). The posterior part of the metacoxal sternocoxale is not distinctly separated from the posterior coxal face (Fig. 1.3.2.2 C). The distance between the meso- and metacoxae is short (Figs. 1.3.2.1 B, 1.3.2.2 A, and 1.3.2.5 A,B). Musculature (Figs. 1.3.2.5 and 1.3.2.6 C,D): Dorsal longi­ tudinal muscles: IIIdlm1 M. mesophragma-metaphragmalis, very strongly developed, O: median region of the mesophragma, I: median region of the metaphragma. IIIdlm2 M. metanoto-phragmalis, well-developed, O: posterior half of the metascutum, I: ventrolateral part of the meta­ phragma (laterad IIIdlm1). IIIdlm3 M. metascutello-­ postnotalis, absent. Dorsoventral muscles: IIIdvm1 M. metanoto-­sternalis, diameter ca. one half of IIdvm1, O: anterolateral edge of the metascutum (metascutal lobe), I: metasternum, in front of the precoxal bridge (mediad IIIspm1). IIIdvm2 M. metanoto-trochantinalis anterior, slender muscle, O: metascutum (posteromediad IIIdvm1), I: anterior rim of the metacoxa and mesal edge of the ­metatrochantin. IIIdvm4 M. metanoto-coxalis anterior, moderately sized, O: posterolateral area of the mesoscutum (posterad IIIdvm7), I: mesocoxal meron (mediad IIIdvm6). IIIdvm5 M. metanoto-coxalis posterior, absent. IIIdvm6 M. metacoxa-subalaris, strongly developed, O: posterolateral part of the metacoxal meron (ventrolaterad IIIdvm4), I: complete ventral surface of the subalare. IIIdvm7 M. metanoto-trochanteralis, strongly developed, O: lateral area of the metascutum (between IIIdvm1 and IIdvm4), I: trochanteral tendon. IIIdvm8 M. metafurca-phragmalis, absent. Tergo-pleural muscles: IIItpm1 M. mesophragmametanepisternalis, fan shaped but only moderately widening, O: anterolateral edge of the prescutum (close to mesophragma), I: dorsal surface of the metabasalare. IIItpm2 M. metapleura-praealaris, O: anterior face of the metapleural ridge below the pleural wing process, I: subtegula. IIItpm3 M. metanoto-basalaris, O: anterolateral edge of the metascutum, I: anterior part of the

medial metabasalar rim. IIItpm4 M. metanoto-pleuralis anterior, only insertion distinctly separated from IIItpm5, O: base of the metapleural arm (laterad IItpm6), I: first axillary sclerite by means of short tendon. IIItpm5 M. metanoto-pleuralis medialis, largely fused with IIItpm4, O: base of the metapleural arm, I: lateral metascutal rim. IIItpm6 M. metanoto-­pleuralis posterior, absent. IIItpm7 M. metanepisterno-axillaris, O: metanepisternum above the anapleural cleft, I: third axillary sclerite (together with IItpm9). IIItpm9 M. metepimero-axillaris tertius, fan-shaped, O: dorsalmost part of the mesopleural ridge, I: third axillary sclerite, posterad IIItpm7. IIItpm10 M. metepimero-subalaris, moderately sized, flattened, O: dorsal rim of the posteriormost metepimeron, I: posterior edge of the subalare. IIItpm11 M. metapleura-subalaris, absent. Pleuro-pleural muscles: IIIppm2 M. metabasalare-­ intersegmentalis, short, O: anteroventral metabasalar rim, I: anterior edge of the metanepisternum, above the anapleural cleft (probably derivative of interpleurite I). Sterno-pleural muscles: IIIspm1 M. metapleurasternalis, well-developed, O: posterolateral edge of the metasternum, I: lateral rim of the metabasalare. IIIspm2 M. metafurca-pleuralis, fan-shaped, O: broadly on the lateral face of the metafurcal arm, I: dorsal metapleural arm with a tendon. Pleuro-coxal muscles: IIIpcm2 M. metabasalaretrochantinalis, O: metabasalar disc (between IIIspm1 and IIIpcm5), I: anterolateral face of the metacoxal rim (laterad IIdvm4). IIIpcm4 M. metanepisterno-­ coxalis posterior, fan-shaped, O: ventral part of the metan­ episternum immediately in front of the pleural ridge, I: lateral metacoxal rim (close to IIIpcm3). IIIpcm5 M. metanepisterno-trochanteralis, O: medial rim of the ­ metabasalare (mediad IIIpcm3), I: trochanteral tendon (together with IIIdvm7 and IIIscm6). Ventral longitudinal muscles: IIIvlm2 M. metafurcaabdominosternalis, strongly developed, O: posterior face of the metafurcal arm, I: abdominal sternite II. Sterno-coxal muscles: IIIscm1 M. metafurca-coxalis anterior, conical, O: discriminal ridge of the metasternum (behind precoxal bridge), I: anterior metacoxal rim. IIIscm2 M. metafurca-coxalis posterior, well-developed, O: posterior face of the metafurcal stalk (dorsad IIIscm3), I: merocostal ridge of the metacoxa. IIIscm3 M. metafurca-coxalis medialis, flattened, O: posterior face of the proximal metafurcal stalk, I: medial rim of the metacoxa. IIIscm4 M. ­ metafurca-coxalis lateralis, O: lateral face of the metafurcal arm, I: tip of the ventral metapleural process. IIscm6 M. metafurca-­ trochanteralis, strongly



1.3 Morphology of adults 

A

tar

C

tibs

 29

cl

C cl

B

aro

aro

untp pulv

fem

tar tib

Fig. 1.3.2.7: N. neotropica, female, metathoracic leg, SEM. A, Leg (cut of proximally of femur-tibial joint); B, distal tarsomere, ventral view; C, distal tarsomere, anteroventral view. Abbreviations: aro – arolium, cl – claw, fem – femur, pulv – pulvilli, tar – tarsus, tib – tibia, tibs – tibial spur, untp – unguitractor plate. Scale bars: A, 500 µm; B, C, 50 µm.

developed, O: ventral part of the metafurcal arm and lateral face of the discriminal ridge, I: trochanteral tendon (together with IIIdvm7 and IIIpcm5).

1.3.2.5 Legs The legs are elongated and exceptionally slender (Fig.  1.3.1; Evans 1942: fig. 7; Grimaldi & Engel 2005: fig. 12.9). The cone-shaped coxae are distinctly elongated, almost adjacent with each other medially. Like the rest of the legs and most parts of the body, they bear a dense ­vestiture of short and thin setae (Fig. 1.3.2.1). The procoxae are shorter than the meso- and metacoxae and, in contrast to them, uniformly sclerotized, lacking a separate posterior meron. Laterally, they articulate with a ventral process of the small propleural sclerite. They are apparently freely movable in all directions. A distinct meral suture and a corresponding internal ridge divide the elongated mesocoxae into the anterior eucoxa and the posterior merocoxa (meron) (Figs. 1.3.2.1 B and 1.3.2.2). The meron does not reach the base of the trochanter. The

mesal face of the eucoxa forms the sternocoxale, which is broadly continuous with the anterior coxal surface (Fig. 1.3.2.2 B). The posteriorly tapering, well-­sclerotized sternocoxale articulates with the posterior end of the eucoxa. The distance between the mesocoxae and metacoxae is very short (Figs. 1.3.2.1 B and 1.3.2.2 B); they are similar in their general shape and configuration, even though the metacoxae are slightly larger. The distal elements of all three legs are similar. The trochanters are small and roughly triangular, with rounded edges. The femora are elongated and cylindrical. The slender tibiae are longer than the femora. They are slightly wider proximally and distally than in their middle region. The apical tibial spurs bear a fine vestiture of short setae like the remaining parts of the legs (Fig. 1.3.2.7 A). Several pairs of more distinct setae are present along the anterior meso- and metatibial edges (Fig. 1.3.2.7 A). The proximal tarsomere is elongate and slender, about half as long as the tibia (Fig. 1.3.2.7 A). The four distal tarsomeres are less than half as long. The slender apical tarsomere 5 is slightly widening distad. The paired curved and equal claws bear three additional teeth with fine riffles on the surface

30 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

(Fig. 1.3.2.7 B,C). A complex arolium is inserted between the claws, with a straight apical edge, lateral margins curved upward, and several fields of very fine hairs; the convex ventral surface appears lightly sclerotized, whereas the concave dorsal part is membranous or semi­ membranous. Paired hairy pulvilli are inserted below the claws, and a trapezoid unguitractor plate with a scaly surface and a pair of distinct setae is present between them (Fig. 1.3.2.7 B). Euplantulae and tarsal soles with tenent hairs are missing.

A

Sc2 pts

Sc1

R

Rs1+2 Rs3 Rs4

jub

A3

B

A2

A1

CuP CuA M4 pts

M3

Sc

M1

M2 R

Rs1+2 Rs3

1.3.2.6 Wings (Fig. 1.3.2.8) The following description is mainly based on a study on the wing morphology of Nannochorista philpotti Tillyard 1917 (Microchorista philpotti, Choristella philpotti), the only known species from New Zealand (Kristensen 1989). The wing of N. maculipennis is shown in Fig. 1.3.2.8. With functional dipterism, Nannochoristidae are considered the strongest fliers among scorpionflies in the widest sense (Kristensen 1989). The two pairs of wings are held in a roof-like position in repose (Tillyard 1917, ­ Kristensen 1989). The corresponding vestiture of ­microtrichia on the underside of the forewings distad the jugal fold and on the paramedian metanotal surface likely holds the wings in their position (Kristensen 1989). The overall shape and venation of both wing pairs are similar (Evans 1942, Kristensen 1989), but the forewings are about 15% longer and differ in vestiture and pigmentation. Both pairs bear a dense cover of slender microtrichia. True setae are restricted to the well-­ developed longitudinal veins and the marginal vein, as well as the adjacent anterior parts of the pterostigma. The  setae on the hindwing are less distinctly developed and less densely arranged; they are entirely missing on the  subcosta (Sc) and cubitus posterior (CuP). All apical cells and most of the central cells of the forewing bear patches of microtrichia, more densely arranged and less upright than those on the remaining wing surface. The membrane below the patches is unmelanized. The patches reflect light differently from the other wing areas; viewed from some angles, they appear as opaque whitish spots (Kristensen 1989). A wing coupling apparatus is probably generally present in Nannochoristidae (Tillyard 1917, Evans 1942, Kristensen 1989). It is formed by a single strong jugal bristle on the forewing margin, a short distance proxi­ mad the end of the jugal fold, and two corresponding strongly developed frenulum bristles on the slightly

A3 A 2

A1

CuP CuA M 4

M3 M2

M1

Rs4

Fig. 1.3.2.8: Nannochorista maculipennis, wings. A, Forewing; B, hindwing. Abbreviations: A – anal vein, CuA – anterior cubital vein, CuP – posterior cubital vein, jub – jugal bristle, M – medial vein, pts – pterostigma, R / Rs – radial vein, Sc – subcostal vein. Scale bar: 500 µm. Redrawn from Evans (1942), nomenclature based on Kristensen (1989).

produced basal margin of the hindwing. According to Tillyard (1917), the frenulum bristles pass under the forewing jugal lobe, whereas the jugal bristles pass above the base of the frenulum bristle and press down upon the ­hindwing. According to Willmann (1987) and Kristensen (1989), the transverse vein of the forewing connecting Sc with the costa is branch Sc1 of a bifurcate Sc; it contains a branch of the Sc nerve and a single seta may be present or absent on its posterior part. As in most species of the group, Sc2 of N. philpotti anastomoses with the radial vein R well proximad the pterostigma; a variably developed oblique distal part of Sc2 extends from Sc + R toward the costa along the inner pterostigmal margin (not shown in Tillyard 1917). The first Rs-branch (designated as Rs1+2 in Kristensen 1989: fig. 1) is simple, and the second branch of the medial vein (M) has a simple bifurcation like the first one. A Rs3-Rs4 crossvein is usually present but lacking in N. philpotti. In contrast to species described and illustrated by Tillyard (1917), specimens of N. philpotti examined by Kristensen (1989) displayed an outer CuA-CuP crossvein more or ­ ranching-off point of the med less distinctly distad the b ­ iffered by CuP-A unmelanized on the M-stem; they also d anterior part and the presence of a basal A2-A3 crossvein. On the hindwing, in contrast to Tillyard’s (1917) observations, only the proximal one of two crossveins between R and the first principal Rs branch (Rs1+2) could be identified in N. philpotti (Kristensen 1989). A crossvein



between CuP and A1 was shown in line with the lower arm of the basal cubital Y-vein; it is placed distinctly distad the lower Y-arm in N. philpotti, and its course was observed as backward/inward rather than backward/ outward (Kristensen 1989). As in the forewing, the distal CuA-CuP crossvein is placed distad the base of the M stem; except for its anterior base, this crossvein is unpigmented and almost indiscernible. Longitudinal vein CuP is also weakly melanized. A well-defined pterostigmata is present on both wings. Its melanized cuticle lacks particular sculpturing, and ample hemolymph lacunae are present in the lumen. Like in other groups of scorpionflies, three nygmata are generally present in Nannochorista: two are located in the Rs-M interspace, proximad and distad the proximal crossvein, respectively, and one proximad the distal CuA-CuP crossvein (Kristensen 1989). The lumen of the nygma areas is filled with large cells, probably with secretory function (Kristensen 1989). A thyridium is present as an unmelanized area in the vicinity of the basal M-fork like in other mecopterans and in other groups of holometabolous insects (Kristensen 1989). Rolf G. Beutel

1.3.3 Pregenital abdomen The pregenital abdomen of Nannochorista was never studied in detail. Sparse data on the abdominal segments were provided in the original description of the family (Tillyard 1917), and the posterior metathorax and abdominal base were depicted and briefly discussed by Crampton (1931). Tergites and sternites are distinctly separated by pleural membranes. A habitus illustration also showing the pregenital abdomen was presented in the textbook of Grimaldi and Engel (2005: fig. 129). The 11-segmented abdomen is slender and elongated, nearly parallel sided in males and somewhat extended in the middle region in females. Tergite I is firmly connected to the metapostnotum (Fig. 1.3.2.2 A). Sternite I is free but distinctly reduced (see Crampton 1931). Tergites and ­sternites I–VII are clearly delimited and widely separated by pleural membranes (Mickoleit 1975, Byers 1991: fig. 37.3C), which bear the spiracles I–VII. Tergites I–VII are distinctly wider than the corresponding sternites. Abdominal tergal processes (Kaltenbach 1978: “Notalorgane”), and finger-shaped processes of tergites V–VII (present in Nothiothauma and some species of Panorpa and Neopanorpa; Kaltenbach 1978) are missing. A dense vestiture of setae is present on the tergites and sternites.

1.3 Morphology of adults 

 31

Frank Hünefeld & Rolf G. Beutel (largely based on Hünefeld & Beutel 2012)

1.3.4 Female postabdomen 1.3.4.1 External morphology The female postabdomen (Fig. 1.3.4.1) is distinctly tapering posteriorly. The terminal segments are retractable into each other in a telescope-like manner. Segment VII is largely unmodified, with the tergum and the sternal plate normally developed. Tergum VIII is also normally developed and saddle shaped as the preceding tergal plates. Venter VIII bears a pair of broad lateral sclerotized stripes, which are probably largely (if not entirely) derived from appendages rather than of sternal origin (­Mickoleit 1975: “Gonocoxosternite”); their posterior parts are strongly converging but are clearly separated from each other over their entire length. Laterotergites of segment VIII are absent (see Mickoleit 1975). The gonopore opens ventromedially behind the posterior margin of segment VIII (Figs. 1.3.4.1 and 1.3.4.2). Tergum IX is shortened and only half as long as tergum VIII. As on segment VIII, paired ventrolateral sclerites represent the genital appendages IX; they are less wide than the appendages VIII and slightly elongated caudally (approximately 1.2× as long as tergum IX). The exoskeleton of segment X forms a closed ring. Segment XI is distinctly separated from X; the epiproct and the subanal plate are well-developed. A pair of long, three-segmented cerci arises laterally from the intersegmental area between segments X and XI. All sclerotized parts of the postabdomen, including the cerci, bear a rather dense vestiture of short setae; longer setae are present on the posterior margin of the sclerites. The genital opening lies ventromedially behind the posterior margin of segment VIII. The rectum opens in a subapical position on segment XI. Musculature (Fig. 1.3.4.2 B): the muscle set of the female postabdomen of N. neotropica comprises 23 muscles (Hünefeld & Beutel 2012). The muscle numbers used in this volume for this body region is based on Hünefeld et al. (2012). Segment VII. 01 isVII-01, O (=origin): anterior margin of tergum VII, I (=insertion): dorsally on the anterior margin of tergum VIII and adjacent intersegmental ­membrane; F (=function): retractor of segment VIII; 02 isVII-02, O: tergum VII, near the anterolateral corner of the tergum, I: anterolateral corner of tergum VIII and

32 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

A

tgVII

tgVIII

tgIX ept cer

geo

B

stVII

geapVIII

geapIX

seX

sap

geo reo

cer

Fig. 1.3.4.1: Nannochorista neotropica, female postabdomen, external morphology. A, Lateral view; B, ventral view. Abbreviations: cer – cercus, ept – epiproct, geapVIII/IX – genital appendage of abdominal segment VIII/IX, geo – genital opening, reo – rectal opening, sap – subanal plate, seX – abdominal segment X, stVII – abdominal sternite VII, tgVII-IX – abdominal tergite VII-IX. Scale bar: 500 µm. Reprinted from Hünefeld and Beutel (2012) with permission from John Wiley and Sons.

adjacent intersegmental membrane, F: retractor of segment VIII; 03 isVII-03, O: paralaterally on tergum VII, I: paramedially on the anterior margin of tergum VIII and adjacent intersegmental membrane, F: retractor of segment VIII; 04 isVII-04, O: close to the lateral margin of tergum VII, below isVII-01, I: anterior margin of tergum VIII and adjacent intersegmental membrane, laterad isVII-01, F: retractor of segment VIII; 08 isVII-08, O: sternum VII, midlength, I: in front of the genital ­appendages VIII, F: retractor of segment VIII; 09 isVII09, O: anterior half of sternum VII, I: in front of genital appendages VIII, laterad isVII-08, F: retractor of segment VIII; 17 dvVII-02, connecting tergum VII and sternum VII, irregularly arranged thin fibers, F: dorsoventral compressor of segment VII. Segment VIII. 23 isVIII-01, O: paramedially on anterior half of tergum VIII, I: anterior margin of tergum IX, F: retractor of segment IX; 24 isVIII-02, O: anterior half of tergum VIII, two nearly parallel bundles, I: anterior margin

of tergum IX, laterad isVIII-01, F: retractor of segment IX; 36 dvVIII-01, connecting tergum VIII and genital appendages VIII, scattered fibers, F: dorsoventral compressor of segment VIII; 37 dvVIII-02, O: near the anterolateral corner of tergum VIII, I: in front of genital appendages VIII; 39 tVIII-01, connecting right and left genital appendages VIII. Segment IX. 45 isIX-01, O: paramedially on the anterior half of tergum IX, I: paramedially on the anterior margin of tergum X and adjacent membranous areas, F: retractor of segment X; 46 isIX-02, O: anterior half of tergum IX, laterad isIX-01, with two bundles, I: close to the lateral margin of anterior margin of tergum X and adjacent membranes, F: retractor of segment X; 50 dvIX-01, connecting tergum IX and genital appendage IX, irregularly arranged thin fibers, F: dorsoventral compressor of segment IX; 51 dvIX-02, O: near the anterolateral edge of tergum IX, I: anterior apex of genital appendage IX. Segment X. 59 isX-01, O: anterior part of tergum X, I: paramedially on the anterior margin of epiproct, F:



 33

1.3 Morphology of adults 

retractor of segment XI; 60 isX-02, O: anterior part of tergum X, above isX-01, I: anterior margin of the subanal plate, F: retractor of segment XI. Cercal muscle. 67 ce-01, O: tergum X, between isX-01 and isX-02, I: base of the cercus, F: movements of the cercus. Muscles of the genital chamber. 71 gc-02, O: anterior part of genital appendage VIII, I: lateral area of

A

tgVII

agl

tgVIII

sped

genital chamber in segments VII/VIII, F: dilator of genital chamber; 74 gc-05, O: anterior margin of tergum VIII, three bundles, I: laterally on the genital chamber in segment VIII, F: dilator of genital chamber; 75 gc-06, O: laterally on the anterior margin of tergum IX, I: laterally on the genital chamber in segments VIII/IX, F: dilator of the genital chamber; 76 gc-07, O: laterally on segment IX, I: roof of genital chamber.

agd tgIX

seX ept

cer reo sap geapIX

geo geapVIII

gec spe

B

tgVII

cov

stVII 04

02

03

01

57

14

15

37

tgVIII

58

tgIX

25

30

seX ept

cer

40 48 55 36

stVII

05

06

38

59

41

26

28

29

sap

reo

geapIX

geapVIII

Fig. 1.3.4.2: N. neotropica, female postabdomen, sagittal section; external sclerotizations and membranes of the left body half and soft tissues omitted, except the internal parts of the genital system and musculature. A, Internal parts of the genital system. B, Skeleto-muscular arrangement. Abbreviations: agd – duct of accessory gland, agl – accessory gland, cer – cercus, cov – common oviduct, ept – epiproct, geapVIII/IX – genital appendage of abdominal segment VIII/IX, gec – genital chamber, geo – genital opening, reo – rectal opening, sap – subanal plate, seX – abdominal segment X, spe – spermatheca, sped – spermathecal duct, stVII – abdominal sternite VII, tgVII-IX – abdominal tergite VII-IX, muscle numbers following Hünefeld et al. (2012); see text for details. Scale bar: 500 µm. Reprinted from Hünefeld and Beutel (2012) with permission from John Wiley and Sons.

34 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

1.3.4.2 Internal parts of the genital system The roof of the genital chamber was described in detail by Mickoleit (1976). In N. neotropica, the chamber forms a sac-like extension in the middle region of segment VIII, into which the spermathecal duct opens dorsomedially. The duct opening lies on the tip of a massive and conspicuously sclerotized papilla, which almost completely fills out the lumen of the extension (Fig. 1.3.4.3 B). The epithelium of the chamber is mostly formed by cubic cells, but the cells in the region of the spermathecal papilla are enlarged and prismatic (Fig. 1.3.4.3 B). A distinctly developed cuticular intima is present (Fig. 1.3.4.3 A,B). The genital chamber is enclosed by a muscularis mainly composed of longitudinal fibers. A distinct bursa copulatrix is not developed. The slender spermathecal duct (Fig. 1.3.4.3 B) reaches the middle region of segment VII anteriorly. The epithelium is formed of large cubic cells with vesicles visible in the cytoplasm. An intima is present and also a weak muscularis composed of single longitudinal fibers. The spermatheca (Fig. 1.3.4.3 C) is roughly ovoid and its epithelium is composed of very large cubic cells with numerous vesicles and very large storage vacuoles in the cytoplasm. It is likely that the spermatheca and the spermathecal duct also function as glands. The spermatheca is surrounded by a loosely arranged muscularis, which is particularly dense on the ventral half. A distinct spermathecal gland is lacking. The short accessory gland duct (Fig. 1.3.4.3 B) ­originates from the genital chamber a short distance posterior to the spermathecal duct. The epithelium is squamose. The intima is well-developed, and the duct is surrounded by single longitudinal muscle fibers. The accessory glands (Fig. 1.3.4.3 D,E) are paired, but their posterior regions are fused. The epithelium of the posterior region is formed by small cells with an irregular shape, whereas the cells of the anterior (paired) region are strongly enlarged, with vesicles and storage vacuoles visible in the cytoplasm. It is uncertain whether the glands belong to Noirot and Quennedey’s type 1 or type 3 (Noirot & Quennedey 1974). A muscularis associated with the glands is apparently absent. The common oviduct (Fig. 1.3.4.3 F) originates ventromedially from the genital chamber, in opposite ­position to the gland duct; it is Y-shaped in cross section. The common oviduct splits off into the paired lateral oviducts (Fig. 1.3.4.3 C) in the boundary region of segments VII and VIII. The epithelium of both the common oviduct and the paired oviducts is unspecialized; a cuticular lining of their strongly compressed lumina is not recognizable. The

oviducts are surrounded by a loose meshwork of scattered muscle fibers. Gerhard Mickoleit & Rolf G. Beutel

1.3.5 Male postabdomen (based on Willmann 1981a and Mickoleit 2008) 1.3.5.1 Segment VIII and genital capsule of segment IX Segment VIII is normally developed, with distinctly defined and separated tergite and sternite. The basistyli of segment IX form an ovoid genital capsule (Fig. 1.3.5.1). The ventral region of this structure (Willmann 1981a: “intercoxal area”: fig. 15a) is completely closed. In contrast to Bittacidae, neither weakly sclerotized regions nor margins of a former “intercoxal area” are visible (­Willmann 1981a). On the dorsal side of the segment, the basistyli are largely fused (Willmann 1981a: fig. 15b), and the genital foramen is consequently almost completely closed. According to Willmann (1981a), this is due to an extension of the genital jugum. The cranial genital foramen is a moderately sized upright-oval opening. The mesal surfaces of the basistyli are reduced to a narrow bridge (Willmann 1981a). The genital jugum forms the extensive cranial wall of the capsule. The elongate-­ triangular, pincer-shaped dististyli are relatively broad at their base and adjacent over almost their entire length in the flexed position (Willmann 1981a: fig. 15); their mesal edges are set with short and thick, strongly pigmented microtrichia. The stylar organ is placed in an almost circular, relatively large foramen. A short process is present at the dorsocranial base of the dististylus of N. ­maculipennis, possibly homologous to the “Basituberculus” of other mecopterans (Willmann 1981a). This ­structure is scarcely recognizable in N. dipteroides (­Willmann 1981a).

1.3.5.2 Copulatory apparatus The elements of the male copulatory apparatus of Nan­ nochorista are essentially equivalent to the corresponding structures occurring in other antliophoran groups (­ Mickoleit 2008). Consequently, the entire copulatory organ will be referred to as phallus or phallosome in the following, and its terminal external component, as aedeagus. Grell (1942) considered the aedeagus as absent in Mecoptera and the entire sperm pump complex as a secondary formation. However, he exclusively examined the highly modified postabdomen of males of Panorpa



1.3 Morphology of adults 

24

hg

 35

hg

36 agd

75 gec

sped

geapVIII gec

A

spe

lov

geapVIII

B agl lov

C

D agl

E

cov

F

Fig. 1.3.4.3: N. neotropica, female postabdomen, histological cross sections. A, Segment VIII, posterior half; B, segment VIII, anterior half; C, segment VII, midlength, spermatheca; D, boundary region of segments VII and VIII, fused posterior parts of the accessory glands; E, accessory gland, anterior part; F, common oviduct. Abbreviations: agd – duct of accessory gland, agl – accessory gland, cov – common oviduct, geapVIII – genital appendage of abdominal segment VIII, gec – genital chamber, hg – hindgut, lov – lateral oviduct, spe – spermatheca, sped – spermathecal duct; muscle numbers following Hünefeld et al. (2012); see text for details. Scale bars: 50 µm. Reprinted from Hünefeld and Beutel (2012) with permission from John Wiley and Sons.

36 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

cer tgVIII tgVII tgIX

spp? gst aed

stVII

stVIII

gb

Fig. 1.3.5.1: Nannochorista holostigma, male postabdomen, lateral view, right gonostylus removed to expose aedeagus. Abbreviations: aed – aedeagus, cer – cercus, gb – gonobasis, gst – gonostylus, spp? – potential spermatophore, stVII/VIII – abdominal sternites VII/VIII, tgVII-IX – abdominal tergites VII-IX. Modified and redrawn from Mickoleit (2008) with permission of Schweizerbart Science Publishers (www.schweizerbart.de/journals/entomologia).

communis L., and his misinterpretation was apparently induced by the highly modified male apparatus of this species and its close relatives: the copulatory organ is distinctly reduced, whereas the pumping organ has undergone progressive evolution. From this resulted very distinct differences from the corresponding structures of a more generalized mecopterid male postabdomen. In contrast to Grell (1942), the copulatory organ of Meco­ ptera was described as penis or aedeagus in the taxonomic literature (e.g. Byers 1989). Likewise, Evans (1942), in a study on the external morphology of N. maculipen­ nis, designated the median part of the copulatory apparatus as aedeagus without further comments. Ferris & Rees (1939), who examined the skeletal parts of Panorpa nuptialis Gerstaecker, also considered the pumping apparatus as parts of a modified aedeagus. The exoskeleton of the phallosome of Nannochorista comprises three elements, the free aedeagus, the phallobase, and the aedeagus apodeme. The aedeagus apodeme, which is larger than the free aedeagus, is a ventrally open trough-like structure. It is subdivided over its entire length by a median septum. Its walls, the lateral lamellae, are continuous with the lateral walls of the aedeagus; at the level of the phallobase, they are drawn out as pointed, wing-like structures and articulate with the median plate. The median septum (median lamella) is caudally continuous with the phallobase. The aedeagus apodeme is entirely located within the lumen of the genital bulb (Mickoleit 2008). Willmann (1981a, b), who used a merely descriptive terminology, referred to the aedeagus apodeme as capsule (“Kapsel”) and to the aedeagus (following Grell 1942) as posterior genital field complex (“hinterer Genitalfeldkomplex”). The phallobase, which corresponds with the aedeagus

complex in its construction, is inserted as a deep pouch in an excavation designated as posterior genital foramen by Willmann (1981a) (Fig. 1.3.5.3 C,D). A nodule with sensorial bristles is present on both sides of the phallobase above the articulation of the aedeagus in all species of Nannochorista. Distinct elements of the aedeagus of all examined species are a dorsal cap sclerite (Mickoleit 2008: “Haubensklerit”), a ventral median plate, and a dorsal and ventral apical lobe (Figs. 1.3.5.2 and 1.3.5.3 A). The proximal part of the cap sclerite is continuous with the phallobase; distally, it forms the dorsal surface of a duplicature, which forms a hood-like cover above the apex of the aedeagus and extends lateroventrally as a small cusp. Where the dorsal and ventral lobes fuse, paired membranous bulges are present, flanking the apical lobes on both sides. The median plate forms the floor of the aedeagus in its proximal half. Recent investigations and graphical reconstructions based on microtome section series (Mickoleit 2008) confirmed earlier findings (Mickoleit 1971): the structures inside the aedeagus could be confirmed as a sperm propulsion organ (Mickoleit 2008: “Sperma-­ Auspreßvorrichtung”) and as derivatives of the endophallus. The sperm propulsion apparatus is formed by an elongate dorsal structure that fits within a ventral trough-like structure. Both elements are movable against each other. In the following, they will be referred to as tegmen and chamber sclerite (Mickoleit 2008: tegimen, “Kammersklerit”) (Figs. 1.3.5.3 C and 1.3.5.4). As mentioned above, the distal end of the aedeagus is divided into a dorsal and a ventral lobe. Consequently, the endophallus also covers the lower side of the dorsal lobe and the upper side of the ventral lobe. The incision between the lobes is laterally covered by the membranous bulge. The tegmen forms the roof of the endophallus-tube and at the apical part of the aedeagus the lower surface of the dorsal lobe (Fig. 1.3.5.3 A–C) (for comments on Willmann’s 1981a interpretation of the tegmen and ­ dorsal lobe, see Mickoleit 2008). At the level of the phallobase, the tegmen articulates with a fulcrum-like structure, which forms the median septum of the aedeagus apodeme. The side of the tegmen confronting the lumen of the endophallus tube is formed by a massive, only partly sclerotized, cuticle. Ridges formed by the lateral parts are continuous with a sharp edge; they enclose a trough-like concavity on the side of the tegmen opposite to the lumen of the endophallus. The central part of the tegmen and the flanks, which project as flat ridges into the interior of the aedeagus, are strongly sclerotized (Fig. 1.3.5.3 C); cranially, the flanks are extended as a short muscle apodeme (Figs. 1.3.5.2 B and



1.3 Morphology of adults 

M.add.gst

aaed

M.p.ph

M.d.chs

dlo

M.d.dej gst vlo lmba j‘

mpl

A

vdej

dej

M.r.ph M.l.chs

aaed

ful

mla

caed tegm dlo

lM.teg mM.teg

dej

achs

rchs

lmba

M.d.chs

j j‘ mpl

B

M.r.ph

lpch

chs lphb

Fig. 1.3.5.2: N. holostigma, male genitalia. A, Distal part of aedeagus; B, proximal part of aedeagus. Abbreviations: aaed – apodeme of aedeagus, achs – apodeme of chamber sclerite, caed – cap of aedeagus, chs – chamber sclerite, dej – ductus ejaculatorius, dlo – dorsal lobe, ful – fulcrum, gst – gonostylus, j – joint between lateral plate of chamber and median plate, j’ – joint between lateral wing of phallobase and median plate, lmba – lateral membranous bulge of aedeagus, l/mM.teg – lateral/mesal portion of tegmen muscle, lpch – lateral plate of chamber, lphb – lateral wing of phallobase, M.add.gst – adductor of gonostylus, M.d.chs – depressor of chamber sclerite, M.d.dej – depressor of ductus ejaculatorius, M.l.chs – levator of chamber sclerite, M.p.ph – protractor of phallosome, M.r.ph – retractor of phallosome, mla – median lamella, mpl – median plate, rchs – lateral ridge of chamber sclerite, tegm – tegmen, vdej – vesicula ductus ejaculatorii, vlo – ventral lobe. Scale bars: 200 µm. Modified and redrawn from Mickoleit (2008) with permission of Schweizerbart Science Publishers (www.schweizerbart.de/journals/entomologia).

1.3.5.3 D). Craniad its middle section, the tegmen has its greatest diameter. Caudally, its height and width decrease, but the general shape does not change distinctly; cranially, the tegmen is slightly bent upward, resulting in a flat curvature of the abovementioned ridges in lateral view of

 37

the aedeagus (Fig. 1.3.5.2 B). Toward the anterior end of the tegmen, the ridges obliterate and the trough-like part tegmen continues as a flat furrow. The anterior apical part of the tegmen appears clot-like (Mickoleit 2008: “Propfenartig”) in cross section and is already located within the lumen of the ductus ejaculatorius, whose flat, membranous wall is closely adjacent with the tegmen. A flat ventromedian cuticular thickening of the floor of the ductus ejaculatorius fits within the aforementioned furrow of the cranial part of the tegmen (Fig. 1.3.5.3 D). It can be assumed that these elements form a valve mechanism; it is opened by the M. dilatator ductus ejaculatorii, whose fibers attach to the lateral membranous walls of the duct and also to the ventromedian cuticular thickening. At the level of the phallobase, the strengthened upper edges of the flanks of the tegmen connect with the arms of the fulcrum of the phallobase (see above, Figs.  1.3.5.3 C and 1.3.5.4 C,D). The tegmen can pivot around the fulcrum toward the phallobase. As the ventral sclerotized element, the chamber sclerite forms a trough-like structure (U-shaped in cross section) extending over the entire length of the ­aedeagus (Figs.  1.3.5.3  C and 1.3.5.4 A–D). Cranially, the aedeagus chamber is directly continuous with the ductus ­ejaculatorius. A small membranous section of it protrudes into the floor of the chamber sclerite; thus, the chamber sclerite appears bipartite on cross sections of this region. At the apex of the aedeagus, the sclerotized trough forms the upper side of the ventral lobe (Figs. 1.3.5.2 B and 1.3.5.3 A). Cranially, the lateral walls of the ventral lobe of the aedeagus form triangular sclerotized plates; their upper margins, like those of the caudal unsclerotized elements of the lateral walls, are continuous with the trough-shaped chamber sclerite (Fig. 1.3.5.2 B). These parasagitally oriented strengthening elements, referred to here as lateral plates of the chamber sclerite, lie within a pouch invaginated cranially between the lateral membranous bulges of the aedeagus and the ventral lobe (Figs. 1.3.5.3 B and 1.3.5.4 A,B). The ventrally oriented apex of the lateral plates forms a rigid articulation with the reinforced margins of the median plate at its posterior apex (Figs. 1.3.5.2 B and 1.3.5.4 A,B). The ventral tip forming the joint is visible in lateral view below the membranous bulge, which overlaps with the anterior edge of the lateral plate. The cranial margin of the lateral plate is slightly emarginated dorsally Starting from its ventral tip, it forms a strengthened edge, which increases in thickness and enters the apodeme of the chamber sclerite; the apodeme overtops the anterior end of the chamber sclerite and rests medially of the lateral lamella of the aedeagus apodeme (Fig. 1.3.5.3 D). Resulting from

38 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

ful

phb

M.add.gst dlo

n

apMag

cla tegm

M.d.chs

C

lmba

chs

vlo

ch

mpl mla

phb

lla

M.abd.gst

M.add.gst M.teg

A

M.l.chs gb

aed

M.p.ph apMag

D ch

tegm

lpch

chs

achs

M.d.chs

M.add.gst

M.d.dej lla

M.r.mpl mpl M.l.chs

mla

M.abd.gst

M.p.ph

M.teg

M.d.chs

vdej mpl

B

gb

E

apMag M.add.gst

M.r.mpl

dej

M.d.dej

Fig. 1.3.5.3: N. holostigma, drawings based on histological cross sections. A, Distal part of aedeagus; B, proximal part of aedeagus; C, at level of fused gonobases, showing aedeagus and sperm pumping device; D, boundary region of segments VII and VIII, fused posterior parts of the accessory glands; E, accessory gland, anterior part. Abbreviations: aed – aedeagus, achs – apodeme of chamber sclerite, apMag – apodeme of gonostylus adductor, ch – chamber, chs – chamber sclerite, cla – clasp sclerite, dej – ductus ejaculatorius, dlo – dorsal lobe, ful – fulcrum, gb – gonobasis, lla – lateral lamella, lmba – lateral membranous bulge of aedeagus, lpch – lateral plate of chamber, M.abd.gst – abductor of gonostylus, M.add.gst – adductor of gonostylus, M.d.chs – depressor of chamber sclerite, M.d.dej – depressor of ductus ejaculatorius, M.l.chs – levator of chamber sclerite, M.p.ph – protractor of phallosome, M.r.mpl – retractor of median plate, M.teg – muscle of tegmen, mla – median lamella, mpl – median plate, n – nerve, phb – phallobase, tegm – tegmen, vdej – vesicula ductus ejaculatorii, vlo – ventral lobe. Scale bars: 100 µm. Modified and redrawn from Mickoleit (2008) with permission of Schweizerbart Science Publishers (www.schweizerbart.de/journals/entomologia).



its specific constructional properties, the chamber sclerite is a stiff element along its longitudinal axis. The abovementioned pouch is laterally delimited by a thin ­membrane, which is ventrally continuous with the strengthened margin of the lateral plate and dorsally with the upper margin of the tegmen flanks (Figs. 1.3.5.3 B,C and 1.3.5.4 A–D). Caudally, the membrane forms the mesal wall of the lateral membranous bulge; due to its width, the chamber sclerite is quite flexible in the dorsoventral direction. The median plate extends cranially into the body lumen as apodemal plate and ends with two short processes (Figs. 1.3.5.3 C,D and 1.3.5.4 A–D). It is slightly concave in the longitudinal and transverse direction over its entire length The distal end appears truncated. The lateral margins are strengthened and appear bulgelike (Figs. 1.3.5.3 B and 1.3.5.4 A,B). More cranially, these bulges diverge from the lateral edges and form a flat inner ridge (Fig. 1.3.5.4 C,D), which lies mesad of the membrane connecting the lateral wings of the phallobase with the median plate. Together with the apex of the lateral wing, it forms the articulation. The inner ridge obliterates directly craniad the articulation, curving outward and fusing with the lateral margin of the apodeme of the median plate. Musculature of the phallosome. Two strongly developed, antagonistic paired muscles move the chamber sclerite. The levator (M.l.chs) originates on the entire inner surface of the aedeagus apodeme, including the median septum, and inserts on the upper side of the chamber apodeme (Figs. 1.3.5.3 D and 1.3.5.4 C,D). Its pinnate proximal part almost completely fills out the trough of the aedeagus apodeme; it is the largest muscle of the aedeagus. The origin of the depressor of the chamber sclerite (M.d.chs) lies on the median plate. Due to the articulation between the lateral wings of the phallobase and the median plate, both the phallobase and the aedeagus apodeme can pivot around the median plate but cannot be shifted against each other in caudo-cranial direction. Thus, the median plate forms a relatively stable base for the depressor of the chamber sclerite. This muscle inserts on the ventral side of the chamber apodeme opposite to the insertion of the levator and more caudally on the lower edge of the lateral strengthening plates (Figs. 1.3.5.3 C,D and 1.3.5.4). The tegmen is moved by a pair of muscles, which originates with one branch on the lower edge of the median lamella (mM.teg) and with a second branch (lM.teg) craniad the lateral lamella of the aedeagus apodeme. It extends caudoventrally and inserts with a tendon at the muscle apodeme of the tegmen (Figs. 1.3.5.2 B, 1.3.5.3 D,E, and 1.3.5.4 E,F). Its contraction likely results in a ventrally

1.3 Morphology of adults 

 39

directed swaying movement of the part of the tegmen caudad the fulcrum, and it pushes the tegmen in the aedeagus chamber. As the fulcrum articulates with the tegmen, it is likely that only a minimal retraction is caused by the muscle, if at all. It is noteworthy that the tegmen is equipped with only one muscle on either side. The antagonistic effect can only be caused by the intrinsic elasticity of the cuticular elements or indirectly by the lifting of the chamber sclerite. That hemolymph pressure plays a role is highly unlikely. The entire phallosome is moved against the genital bulb by two muscle pairs. The protractors (M.p.ph) originate at the mesal wall of the adductor apodeme of the gonostylus and insert cranially on the external wall of the aedeagus apodeme (Figs. 1.3.5.2 A and 1.3.5.3 E) with a caudoventral-craniomedial orientation. The closely adjacent two retractors (M.r.ph) appear like an unpaired muscle. They have a common area of origin on the floor of the cranial half of the genital bulb (Figs. 1.3.5.2 and 1.3.5.3 D,E) and ascend slightly and insert on the ventral side of the apodeme of the median plate. As the phallobase articulates with the median plate, the retractor is able to retract the entire phallus complex. Due to the obliquely ascending course of the fibers, the retractors can also turn the floor of the aedeagus dorsad; as ­mentioned above, it is cranially continuous with the median plate. The dilator of the ductus ejaculatorius (Grell 1942: Panorpa) originates cranially on the gonocoxites. It extends along the entire length of the ductus ejaculatorius and is closely adjacent to it. It reaches its anterior end, where it is continuous with the vasa deferentia, and it is enclosed in a tube-like cover, which is attached to the walls of the duct on both sides. In the region of the vesiculae ductus ejaculatorii, the muscle lies between these structures and the ductus ejaculatorius; anterior to this position, its fibers lie below the duct. It inserts with its lateral parts ventrolaterally on the duct, at the opening site of the vesiculae ductus ejaculatorii (see above). Immediately posterad, the fibers of its middle region attach to the ventromedian cuticular thickening of the duct.

1.3.5.3 Function Two main elements articulate with the median plate in the joints j’ and j: the phallobase with its lateral wing and the chamber sclerite with its lateral plate. It can be assumed that the phallobase, median plate, and chamber sclerite form a tripartite lever system. Its elements are distinctly sclerotized, relatively rigid structures.

40 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

ful

caed dlo

tegm tegm

lmba

rchs ch

ch chs

chs j

M.d.chs

M.d.chs

mpl

A

rchs

lpch

B

phb ful

C

mpl

mpl

mM.teg

mla

mla

j'

lla M.l.chs

lM.teg

dej tegm

rchs vdej

ch

chs

E dej

D

mpl

M.d.chs

M.d.dej

M.p.ph

F M.d.dej

sdej

Fig. 1.3.5.4: N. holostigma, graphical reconstructions based on histological cross sections. A, B, Transition area with lateral bulges and dorsal lobe entering aedeagus, lateral wall of aedeagus partly removed to expose the chamber sclerite with its lateral plates; C, D, aedeagus at the level of the sperm propulsion organ, connection of fulcrum and tegimen, levator of chamber sclerite shown transparent, lateral wall of phallobase and aedeagus apodeme removed; E, ductus ejaculatorius, anterior part; F, aedeagus apodeme. Abbreviations: caed – cap of aedeagus, ch – chamber, chs – chamber sclerite, dej – ductus ejaculatorius, dlo – dorsal lobe, ful – fulcrum, j – joint between lateral plate of chamber and median plate, j’ – joint between lateral wing of phallobase and median plate, lla – lateral lamella, lmba – lateral membranous bulge of aedeagus, l/mM.teg – lateral/mesal portion of tegmen muscle, lpch – lateral plate of chamber, M.d.chs – depressor of chamber sclerite, M.d.dej – depressor of ductus ejaculatorius, M.l.chs – levator of chamber sclerite, M.p.ph – protractor of phallosome, mla – median lamella, mpl – median plate, phb – phallobase, rchs – lateral ridge of chamber sclerite, tegm – tegmen, sdej – sheath of ductus ejaculatorius, vdej – vesicula ductus ejaculatorii. Scale bars: 50 µm. Modified and redrawn from Mickoleit (2008) with permission of Schweizerbart Science Publishers (www.schweizerbart.de/journals/entomologia).



Adjustments within this system are achieved by the levator and depressor of the chamber sclerite and the retractor of the median plate. The lifting of the chamber sclerite is probably caused by contraction of its levator, supported by the retractor. By the concerted activity of these muscles, the chamber sclerite is likely shifted dorsad, combined with a slight movement in craniocaudal direction. Thereby, the median plate rotates with its apodeme in the joint j and functions at the same time as guiding device for the lateral plate of the chamber sclerite and as bilateral lever. The lowering of the trough of the chamber is likely achieved by the depressor. The turn of the median plate around the pivot j’, which is coupled with this movement, requires the relaxation of the retractor. The constellation of the skeletal and muscular elements described above and the deduced suite of movements indicate clearly that the structural complex within the aedeagus functions as sperm propulsion organ during copulation. Other functions of the closely fitting movable elements of the tegmen and chamber sclerite can be excluded with reasonable certainty. It is very likely that sperm propulsion is mainly effected by the lifting of the chamber sclerite. This is also suggested by the strong equipment of this element with muscles and specifically the very large size of its levator (largest muscle of the entire copulatory apparatus). It is conceivable that the lowering of the tegmen supports sperm propulsion. However, it is very likely that the muscles of the chamber sclerite play the main role. The longitudinal shape of the tegmen, which extends over the entire length of the aedeagus, suggests that the male apparatus of Nannochorista does not function as propulsion organ of liquid sperms but rather of a lump of sperm enclosed by a secretion layer or a defined spermatophore. This interpretation is strongly supported by the finding of a structure likely representing a spermatophore cover in the aedeagus of a dissected male specimen of Nannochorista philpotti (Mickoleit 2008) (Fig. 1.3.5.1). The copulatory apparatus of N. philpotti (New Zealand) is very similar to that of the other species of the family. The spermatophore (in contrast to that of Boreus) is a spindle-­ shaped structure tapering toward the apex and devoid of a median wall. The wall is transparent. Mickoleit (2008) recognized traces of the propulsion process on the cover in a microtome section series. Apparently, the tegmen and chamber sclerite left imprints on the upper and lower side of the spermatophore reflecting their own profile. The putative spermatophore is filled with granular secretions. Spermatozoa could not be identified.

1.3 Morphology of adults 

 41

Bożena Simiczyjew & Rolf G. Beutel

1.3.6 Ovaries (mainly based on Simiczyjew 2002) Two basic types of ovaries occur in insects: panoistic and meroistic. In the panoistic ovary, which is likely ancestral, all oogonia transform into oocytes. In the meroistic type, oocytes and nurse cells are generated. The location of nurse cells within the ovarian tube is the criterion for distinguishing two subtypes: telotrophic and polytrophic. In the former, nurse cells are confined to the apical part of the ovariole (tropharium), whereas in the latter, they are placed next to the oocyte, with which they form the egg chamber. Primary panoistic ovaries occur in basal groups of insects (e.g. Archaeo­ gnatha, Zygentoma, Ephemeroptera, Plecoptera, and Dictyoptera), whereas the polytrophic type occurs in the majority of holometabolan groups (Diptera, Hymeno­ ptera, Trichoptera, Lepidoptera, Coleoptera-Adephaga, and Mecoptera [major part]). Telotrophic ovaries are characteristic for Hemiptera, Coleoptera-Polyphaga, Raphidioptera, Megaloptera (Sialidae), and Ephemero­ ptera. Secondary panoistic ovaries have evolved several times from the meroistic type by reducing the nurse cells. This type, designated as neopanoistic by Štys and Biliński (1990), occurs in Nannochoristidae and Boreidae and also in Siphonaptera (except for Hystrichopsyll­ inae), Thysanoptera, and Megaloptera (Corydalidae) (Büning 1994, Biliński 1998, Simiczyjew 2005). Comparative studies of insect ovaries indicate that ovariole structure and oogenesis are stable characters at the family level and therefore can be used in a phylogenetic context (Štys & Biliński 1990, Büning 1994). In Nannochorista neotropica, each of the paired ovaries is composed of numerous, segmentally arranged ovarian tubes or ovarioles (Fig. 1.3.6.1 A). Each individual ovariole comprises a terminal filament, an elongated vitellarium (Fig. 1.3.6.1 B,D,G), and the ovariole stalk connecting the ovarian tube with the lateral oviduct (not shown). In adult females, germaria, the anterior part of the ovariole where the differentiation of germ cells takes place, are absent. This indicates that the initial stages of oogenesis (germ cell divisions and oocyte differentiation) take place in the larva or pupa, before the individual enters the reproductive phase. The vitellarium, the region where oocytes develop, is composed of a few linearly arranged ovarian follicles, each of which is formed by an oocyte surrounded by somatic follicular cells (Fig. 1.3.6.1 B,D,G). As ovarian follicles do not develop synchronously, previtellogenic, vitellogenic, and choriogenic ovarian

42 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

tf

tf

tf

g n

ov

oo

v

of fe

of

A

v

n tf

B

oo

G

ec

of

nc

nc

fe

n

H

C

oo oo

fe n

mvo

D fe

fe

oo oo n

J

oo

oo oo

K

fe

n

*

lvo

E

oo

I

F

L

follicles can be distinguished. Previtellogenic follicles are located in the apical region of the vitellarium, whereas the largest and most advanced follicles occur at the base of the ovarian tube (Fig. 1.3.6.1 B,D,G). Relatively small early previtellogenic oocytes contain large, roughly spherical, centrally located nuclei (germinal vesicles) (Fig. 1.3.6.1 B,D,G). In the karyoplasm, numerous dense multiple nucleoli occur (Fig. 1.3.6.1 D), which suggests that the extrachromosomal amplification of ribosomal genes (rDNA) takes place in the oocytes of Nannochorista. In meroistic ovaries, very large numbers of ribosomes are produced by nurse cells. The lack of these cells in the neopanoistic ovary of N. neotropica is compensated for

Fig. 1.3.6.1: Ovarioles of nannochoristids and pistilliferans. A–G, J–L, Nannochorista neotropica. H, Bittacus hageni (Bittacidae). A–C, Whole mount preparation; D–F, J–L, semithin sections (stained with methylene blue). A, Ovary with segmentally arranged ovarioles. B, individual ovariole differentiated into terminal filament and vitellarium, containing linearly arranged ovarian follicles. C, individual ovariole composed of four ovarian follicles in different stages of oogenesis. D, part of previtellogenic ovarian follicle (note very large oocyte nucleus). E, early vitellogenic ovarian follicle. F, details of neighboring ovarian follicles in the mid and late vitellogenic stage. g, Schematic representation of ovariole. H, egg chamber of polytrophic ovariole (semithin histocryl section stained with DAPI [4′,6-Diamidin-2phenylindol]), polyploid nuclei of the nurse cells are visible (arrow indicates follicular epithelium). I, Schematic representation of polytrophic ovariole characteristic for Apteropanorpidae, Bittacidae, Choristidae, Eomeropidae, Meropeidae, Panorpidae, and Panorpodidae, note the presence of huge, polyploid nurse cells. J, part of early vitellogenic ovarian follicle. K, contact zone of two choriogenic ovarian follicles (arrows indicate thin egg envelopes of oocytes). L, late vitellogenic oocyte filled with large lipid droplets (asterisk) and yolk spheres (arrow). Abbreviations: ec – egg chamber, fe – follicular epithelium, g – germarium, lvo – late vitellogenic ovarian follicle, mvo – mid vitellogenic ovarian follicle, n – oocyte nucleus, nc – nurse cells, of – ovarian follicles, oo – oocyte, ov – ovariole, tf – terminal filament, v – vitellarium. Scale bars: A–C, 200 µm; D–F, H, J, K, 20 µm; L: 50 µm. © Bożena Simiczyjew.

by the amplification of rDNA in the oocyte nucleus, which enables massive production of ribosomes by the oocyte itself. Ribosomes are needed in very large numbers in the early embryo. This explains that in the panoistic ovaries without nurse cells, the production of ribosomes is enhanced by extrachromosomal amplification of rDNA genes. Multiple nucleoli are visible until an advanced stage of vitellogenesis is reached. During the vitellogenic stage, the volume of the oocytes of N. neotropica increases because of deposition of yolk spheres and lipid droplets (materials required for the growth of the embryo), like in other insects (Fig. 1.3.6.1 F,J,L). In the late vitellogenic stage, the multiple nucleoli in the oocyte nucleus decrease



in size and disperse within the karyoplasm. In the terminal ovarian follicles, apart from yolk accumulation, deposition of eggshell material takes place in the perivitellar space (between the oocyte and the follicular epithelium). Therefore, oocytes in the most advanced follicles are covered by a thin layer of chorionic material (Fig. 1.3.6.1 K). Choriogenic follicles are roughly oval with a slightly flattened anterior pole (Simiczyjew 2002). Ovaries of N. neotropica show a close resemblance to those of boreids, where nurse cells are also absent and the ovarioles display a neopanoistic organization. In both cases, only a terminal filament, vitellarium, and ovariole pedicle can be distinguished in a fully developed ovariole. In adult females of the snow fleas, functional germaria are also absent, although in the apical part of the ovariole, one or two degenerating germ cells occur between the terminal filament and the oocyte in the earliest stage. In both groups, the presence of multiple nucleoli resulting from amplification of rDNA has been demonstrated in the germinal vesicles (Biliński & Büning 1998). The neopanoistic organization is also characteristic of the majority of the studied siphonapterans, a group apparently closely related to Mecoptera (Simiczyjew & Margas 2001). Except for Hystrichopsylinae, flea ovarioles are also neopanoistic, with a similar organization and func­ istilliferan tion. In contrast, all examined females of the p Mecoptera (Apteropanorpidae, Bittacidae, Choristidae, Eomeropidae, Meropeidae, Panorpidae, and Panorpod­ idae) possess ovaries of the meroistic-polytrophic type, with a very similar organization of the ovariole, which are differentiated into terminal filament, germarium, and vitellarium (Fig. 1.3.6.1 I). In each case, a cluster of germ cells is composed of four cystocytes and formed as a result of two mitotic divisions of the cytoblast and cystocytes, which end with incomplete cytokinesis. As a result, the cystocytes of a cluster are connected with one another by intercellular bridges. Within a cluster, one cell differentiates into an oocyte, whereas the remaining three develop into large nurse cells, which are highly polyploid (Fig. 1.3.6.1 H) and show high synthetic activity, producing various macromolecules. In advanced stages of oogenesis, macromolecules and some organelles (ribosomes, mitochondria) and cytoplasm are transported to the oocyte via the cytoplasmic bridges. The oocyte, in turn, remains transcriptionally inactive. Its nucleus is relatively small, while the condensed meiotic chromosomes form a polymorphic karyosphere. Active nucleolus or multiple nucleoli in germinal vesicles are absent, although in representatives of some families, nuclear bodies occur similar to nucleoli (Biliński et al. 1998, Simiczyjew 2005). Studies of the female gonad organization and oogenesis indicate that nannochoristids, similarly to boreids,

1.4 Morphology of larvae 

 43

have ovaries entirely different (neopanoistic) from those of other mecopteran families (meroistic-polytrophic). At the same time, the female gonads of the representatives of Nannochoristidae and Boreidae exhibit a remarkable resemblance to neopanoistic ovaries of Siphonaptera (except for Hystrichopsyllinae) (Simiczyjew 2005).

1.4 Morphology of larvae The aquatic larvae are prognathous and extremely elongate and slender (Fig. 1.4.1; Pilgrim 1972: figs. 1–3). The total length of the final instar of N. philpotti ranges between 12.5 and 14.5 mm (n = 7). The integument in active larvae has a speckled brown-and-whitish pigmentation pattern (Pilgrim 1972: figs. 1 and 2), which rapidly disappears after fixation and also in living larvae in the “prepupal” stage. Rolf G. Beutel, Frank Friedrich, Hans Pohl & Niels P. Kristensen

1.4.1 Head 1.4.1.1 Head capsule, external features (Figs. 1.4.1.1–1.4.1.4) The position of the distinctly prognathous head in the living larvae is evidently somewhat variable (since the immediately following soft-walled trunk region permits ample movement) but is, at most, moderately inclined relative to the long axis of the body (Fig. 1.4.1). For convenience, our descriptive account uses a strictly prognathous orientation, i.e. with “dorsal” and “ventral” being relative to a horizontal longitudinal axis of the head. The head capsule is almost completely exposed (Fig. 1.4.1). Only a trapezoid posteromedian extension is partly covered by prothoracic trunk integument, and its posterior part is internalized and apodemal; it is separated from the posterolateral head regions by distinct angular notches and bears a strongly darkened patch on each side. The cranial cuticle is smooth and shiny and of a light brown to dark brown coloration. The distance from the posterodorsal margin of the head to the frontoclypeal sulcus is slightly longer than the maximum width. The head capsule is slightly rounded laterally, moderately widening posteriorly, and rather abruptly narrowed close to the foramen occipitale, with rounded posterolateral edges. The foramen is lined by a strongly sclerotized dark postoccipital sulcus. Dorsomedially, this sulcus, which is depigmented medially, runs in front of the apodemal part of the trapezoid extension and is contiguous with

44 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

Fig. 1.4.1: Nannochorista philpotti, final instar, habitus, microphotography. © Hans Pohl.

prominently darkened areas on the latter. On the dorsal cranial surface, a short branch extends forward from the postoccipital sulcus, but soon obliterates. Anteriorly, the postoccipital sulcus is continuous with the subgenal sulcus that lines the ventral and anterolateral margins of the head capsule. Posteriorly, this sulcus borders on the postgenal bridge, and anteriorly, it forms the articulatory areas of the maxillae and mandibles. Adjacent to the posterior mandibular articulation, the anteroventral corner of the head capsule is strengthened by an additional short sulcus extending between two points of the subgenal sulcus, which is strongly angled in this area. The subgenal sulcus eventually becomes indistinct in the vicinity of the anterior (topographically dorsal) mandibular articulation, but the entire anterior corner of the head capsule is thick-walled and darkened. On the dorsal surface, the darkening is continuous, with a straight transverse trans­ clypeal strengthening line (sulcus) between the medial corners of the anterior tentorial invaginations (see Beutel et al. 2009). The cranial sclerotization extends a short distance beyond the transverse sulcus, but the anteriormost part of the head capsule – the anteclypeus – is unpigmented and weakly sclerotized. The clypeal area in front of the transverse line is distinctly narrowing toward the labrum and shorter than the width of the anterior margin. A near-­triangular anteromedian “frontoclypeal apotome” (­morphologically belonging to the frons except for the anteriormost zone) is delimited by the weakly curved arms of the Y-shaped ecdysial cleavage line, the stem of the “Y” (“coronal suture” auct.) being ca. one third as long as the entire head on this side. The cleavage lines extend to the lateral corners of the transclypeal sulcus. The maxillolabial complex is located in a deep semicircular concavity in the strongly darkened sclerite (postgenal bridge) (see Beutel et al. 2009), which lies between the postoccipital sulci and forms the ventral closure of the head capsule.

It is strongly darkened but medially divided by a ventral ecdysial cleavage line. It widens anteriorly and posteriorly, and its posterior part is laterally lined by the elongate posterior tentorial fissures but does not extend backward beyond them. A gula is absent.

Setation (Figs. 1.4.1.2–1.4.1.4) Only 13 pairs of cranial setae have been identified. They are tentatively assigned to the groups for which a ­ Lepidoptera-based nomenclature is available (see Hasenfuss & Kristensen 2003: pp. 143–144, figs. 5.3 and 5.10). Most setae of the head capsule and mouthparts are long and slender, and some of them are split into two or more branches. The two pairs of clypeal setae are located on the depigmented anteclypeus, one on the anterior third in the middle between the median line and the lateral margin (C2) and one very close to the posterolateral margin (C1). The frontoclypeal apotome bears the so-called frontal seta F1 on the hind border of the trans­ clypeal sulcus and the adfrontal AF1 (split) in a more posterior position. A branched seta located in front of the eye is tentatively denoted here as A1 since it may pertain to the anterior group rather than to the eye group (S, for stemma; previously termed O, for ocellus). Eye setae apparently have no counterparts in Nannochorista. One additional anterior split seta (possibly A3), a lateral seta (L1, much smaller than other setae on the head surface), and two parietal setae (P1 and P2) are arranged in a row on the dorsolateral region of the head capsule. All three lepidopteran substemmatan setae likely have Nanno­ chorista counterparts: SS1 below A1, SS2 (usually split, but apparently not in one examined specimen) laterad the subgenal sulcus, and SS3 above and posterior to SS2. A long genal seta (G) is located on the posterolateral region of the head capsule. It is noteworthy that the



1.4 Morphology of larvae 

 45

ant ant acl lbr lbr acl

ore

md

pmex

tcl

mxp mxlc

A

B ant

lbr ant

md lap pgeb

lbr md mxp

mxlc

mxp

C

lap

D

Fig. 1.4.1.1: N. philpotti, larval head, SEM. A, Dorsal view; B, lateral view; C, anterior view; D, ventral view. Transverse fold across anteclypeus not generally present (Figs. 1.4.1.4 A and 1.4.1.11), likely caused by excessive contraction of strong muscles 8 and 9 upon fixation; maxillolabium markedly bent downward in the specimen illustrated in C and D, hence appearing shortened. Abbreviations: acl – anteclypeus, ant – antenna, lap – labial palp, lbr – labrum, md – mandible, mxlc – maxillolabial complex, mxp – maxillary palp, ore – ocular region, pgeb – postgenal bridge, pmex – posteromedian trapezoid extension, tcl – transverse anteclypeal fold. Scale bars: 100 µm. Reprinted from Beutel et al. (2009) with permission from Elsevier.

complement of “microsetae” on the posterior cranium (proprioreceptors registering the position of the head relative to the overlapping cervical integument) comprises just a single microdorsal seta; no ventral (“microgenal”) setae have been identified. Small translucent spots (counterparts of “punctures,” “pits,” or “pores” in Lepidoptera) are assigned to seta groups and denoted by lower-case letters. One frontal (Fa), one adfrontal (Afa), three parietal (Pa-c), two substemmatan (SSa-b), and one genal (Ga) have been identified, and in addition, one sensillum is present in the subgenal sulcus above the mandibular articulation. What appears in surface view of whole mount preparations as the “translucent spot” is a central

cavity in a prominent endocuticular thickening. These organs are likely modified campaniform sensilla; they are not accompanied by any externally identifiable cuticle modification and cannot with certainty be located by SEM observation.

1.4.1.2 Internal skeletal structures (Figs. 1.4.1.5 and 1.4.1.7) The tentorium is well-developed, with short and strong posterior arms, a rather long, straight tentorial bridge, and anteriorly diverging anterior arms. Toward the

46 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

A3 L

A1 C1 C2 lbr

acl

F Fa

AF

AFa

Pa P1 P2

Pb

Pc MD

fcl ecl

tcs md eye ant

anterior invagination site, each arm is anteriorly markedly widened into a dorsally concave plate with a slightly thickened medial margin. Each anterior invagination is therefore unusually broad; it is located immediately adjacent to a short antenna-bearing protuberance and the tentorial wall is continuous with the lower and lateral walls of this elevation. The position of the invagination area is not externally visible on the dorsal and lateral cranial surfaces as the tentorial arm is completely solid throughout. The mesal margin of the invagination is located immediately laterad the site where the transclypeal sulcus is interrupted by the anterior cleavage line. The lateral margin of the invagination has the form of a high internal

Fig. 1.4.1.2: N. philpotti, larval head, diagrammatic dorsal view. Abbreviations: acl – anteclypeus, ant – antenna, ecl – ecdysial cleavage line, fcl – frontoclypeus, lbr – labrum, md – mandible, tcs – transclypeal sulcus. For chaetotaxy terms (abbreviations starting with capital letter), see subchapter Setation. Reprinted from Beutel et al. (2009) with permission from Elsevier.

crest on the cranial wall above/behind the (morphologically) anterior mandibular articulations (Figs. 1.4.1.3 B and 1.4.1.4 C–G). The posterior tentorial grooves are ­elongate fissures in the transition region between the postoccipital and subgenal sulci; they extend along the posterior parts of the “postgenal bridge.” Typical dorsal tentorial arms are absent, but a vestige is present in the form of a slender tissue strand (of epithelial cells continuous with those enveloping the tentorium). It arises from each anterior tentorial arm just behind the origin of the antennal muscle; it extends toward the dorsal cranial wall, initially pressed against the anterior surface of the brain/circumoesophageal connective. Curving slightly

▸ Fig. 1.4.1.3: N. philpotti, larval head, diagrammatic views. A, Ventral view of specimen with maxillolabium ventrally bent, hence

appearing shortened (as in Figs. 1.4.1.1, 1.4.1.6 B, and 1.4.1.7 B). Inset at right: maxillary apex in dorsal view; B, transverse section of another specimen, approximately at level X in panel A; C, thick transverse section (reconstructed from three consecutive 7-µm sections), approximately at level Y in panel A. Abbreviations: aph – anterior pharynx, ata – anterior tentorial arm, cbs – cardo + basistipes, dmp – “dorsomedial plate” on distal maxilla, dmpv – ventral apex of dorsomedial plate, dst – dististipes, ecl – ecdysial cleavage line, fco – frontal connective, ga – galea, hy – hypopharynx (apex in A forward/downward bent), lac – lacinia, lap – labial palp, lcm – lacinia mobilis, lm – longitudinal muscles on roof of cibariopharyngeal chamber, md – mandible, mp – “median plate” on cardo + basistipes, mxp – maxillary palp, nan – nervus antennalis, nfr – nervus frontalis, nla – nervus labialis, nmd – nervus mandibularis, nmx – nervus maxillaris, ora – oral arm of hypopharyngeal suspensorium, pgeb – postgenal bridge, ppl – produced prelabial area, pmp – “posteromedial plate” on cardo + basistipes, poc – preoral cavity, ptg – posterior tentorial grove, sal – salivarium, sald – salivary duct, sgs – subgenal sulcus, te11 – tendon of M. 11, te12 – tendon of M. 12, to – torma, tp – “transverse plate” on cardo + basistipes, 1-4 – M. tentorioscapalis, 8+9 – M. frontolabralis + M. frontoepipharyngalis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 18 (-1, -2, -3) – M. tentoriostipitalis, 19 – M. craniolacinialis, 19a – craniodististipitalis, 22 – M. stipitopalpalis externus, 23 – M. stipitopalpalis internus, 37 – M. hypopharyngosalivarialis, 41 – M. frontohypopharyngalis, 42 – M. tentoriohypopharyngalis, 45 – “M. frontobuccalis anterior,” 46 – “M. frontobuccalis posterior,” 47 – M. frontobuccalis lateralis, 48 – M. tentoriobuccalis anterior, 49 – M. tentoriobuccalis lateralis. For chaetotaxy terms, see text. Reprinted from Beutel et al. (2009) with permission from Elsevier.



 47

1.4 Morphology of larvae 

A to

lcm mxp md

ga lac

dst dmpv X

tp cbs

Y

hy ppl

dst

dmp lap

ss1

mp ss2

pmp

ssa

ss3

ssb

sgs

pgeb

G

Ga

ptg nfr ecl

B

ecl

C

nan

8+9 fco 1-4

ata

nan

poc

nmd

37 te12

lm

19a nmx 23 18-2

ata

mp dmp

lm aph

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11 12

sal

nmx 42

18-2 18-3

19 nla

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48

18-1

19a

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te11

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eye

lm

46 45

41

23

sald

48 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

B

G P2

AF

A

F

A3

L

P1

A1

acl ant

ss1

md

lbr

sgs cbs mxp

ss2 ssa

Ga ssb pgeb

tp

dst

G

ss3

lap

B

C

8+9

D 43-2

nlbr nan

43-1

1-4 ati

ant

E

44

F

43-2

44 43-2

G nan 1-4

nlbr 44

43-2 fg

md

Fig. 1.4.1.4: N. philpotti, larval head. A, Diagrammatic lateral view of specimen with clypeolabrum and maxillolabium in position often encountered in fixed specimens (compare with Fig. 1.4.1.1); B–G, successively more posterior transverse sections (at nonuniform intervals) of the head capsule and mandible in the region indicated in A. Abbreviations: acl – anteclypeus, ant – antenna, ati – (ventral) anterior tentorial invagination, cbs – cardo + basistipes, dst – dististipes, fg – ganglion frontal, lap – labial palp, lbr – labrum, md – mandible, mxp – maxillary palp, nan – antennary nerve(s), nlbr – labral nerve, pgeb – postgenal bridge, sgs – subgenal sulcus, tp – “transverse plate” on cardo + basistipes, 1-4 – M. tentorioscapalis, 8+9 – M. frontolabralis + M. frontoepipharyngalis, 43 (-1, -2) – M. clypeopalatalis, 44 – M. clypeobuccalis. For chaetotaxy terms see text. Reprinted from Beutel et al. (2009) with permission from Elsevier.

forward, the strand eventually becomes anchored to the head capsule (just behind the eye and laterad the ­ecdysial-line “Y-leg”) by a delicate conical tissue mass (green-stained in the trichrome-stained sections), which comprises fibrillar material.

1.4.1.3 Eyes The position of the eyes is indicated by conspicuous pigmented spots on the anterodorsal surface of the head (Figs. 1.4.1.2, 1.4.1.3 C, and 1.4.1.4 A). These visual organs



1.4 Morphology of larvae 

A

 49

B 23

ata

sgs

49 18 17 52-1 50 48

dta

tb

1-4 13

22

18-2 18-1

18-3

42 19

17-1

52-2

tvn

19

17-2

19a Fig. 1.4.1.5: N. philpotti, larval head. A, Diagram of tentorium, dorsal view showing muscle origins (right); B, diagram of maxillary musculature, dorsal view; filled circles, insertions on maxilla; filled squares, origins on maxilla; open squares, origin on tentorium or cranium. Abbreviations: ata – anterior tentorial arm, dta – vestigial dorsal tentorial arm, sgs – subgenal sulcus, tb – tentorial bridge, tvn – tendon of ventral neck muscle, 1-4 – M. tentorioscapalis, 13 – M. tentoriomandibularis, 17(-1, -2) – M. tentoriocardinalis, 18(-1, -2, -3) – M. tentoriostipitalis, 19 – M. craniolacinialis, 19a – M. craniodististipitalis, 22 – M. stipitopalpalis externus, 23 – M. stipitopalpalis internus, 42 – M. tentoriohypopharyngalis, 48 – M. tentoriobuccalis anterior, 49 – M. tentoriobuccalis lateralis, 50 – M. tentoriobuccalis posterior, 52(-1, -2) – M. tentoriopharyngalis. Reprinted from Beutel et al. (2009) with permission from Elsevier.

were described in by Melzer et al. (1994) as compound eyes with 10 or more ommatidia, but without corneal lenses. The overlying cranial cuticle is completely smooth. In one specimen, an aberrant stemma unit was observed by Melzer et al. (1994) at the posterior edge of the lateral eyes; it lacks a dioptric apparatus. The rhabdom is star shaped and composed of at least six retinula cells (Melzer et al. 1994). Ocelli are absent.

1.4.1.4 Labrum The well-developed labrum is movable and connected with the anterior clypeal margin by a membrane (Figs. 1.4.1.1, 1.4.1.2, 1.4.1.6, and 1.4.1.9). It is conspicuously protruding and rounded laterally and anterolaterally, with a distinct, rounded anteromedian concavity. The dorsal side is smooth, moderately convex, and devoid of setae. The dorsal and lateral labral walls are sclerotized, and the lower anterior corners of this sclerotization are extended inward/backward as a pair of plate-like tormae in the epipharyngeal wall. One long seta is inserted at the lateral edge of a transverse tripartite field of sensilla and microtrichia, which covers a large part of the anterior labral margin. The upper margin of this field is sinuate. Groups of small microtrichia and papillary sensilla are evenly

distributed, and a pair of longer, articulated sensorial pegs is present laterally. A pair of similar sensorial pegs is inserted on the anteroventral part of the labrum close to the median line (Fig. 1.4.1.6 C,D). It is followed by a small ­ icrotrichia. median field of posteriorly directed coarse m Long and finely barbed, mesally directed acanthae originate in and around a fold along the oblique anterior margin of each torma. Setation (Figs. 1.4.1.2, 1.4.1.3 A, and 1.4.1.6 C): a pair of long setae is present on the anterolateral margin. An elaborate sensillum complement is located on the distal margin, along the transition to the epipharynx (see below). Musculature (Figs. 1.4.1.3 B,C and 1.4.1.11): M. 7: M. labroepipharyngalis, a well-developed oblique muscle, O: laterally on the posterodorsal labral wall, I: postero­ ventral labral wall, close to the median line. M. 8 and M. 9: M. frontolabralis and M. frontoepipharyngalis, these long and strongly developed muscles have an unusual configuration, originating together (O: central area of the frons, above the brain) and appearing as only one pair until a short distance before their insertions, I 8: medially on the posterior margin of dorsal labral wall, I 9: with a short tendon paramedially on the epipharynx in front of, and mediad from, the tormal sclerotization. Despite its very medial insertion and unusual near-complete fusion

50 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

spl

A

B

Fig. 1.4.1.6: N. philpotti, larval head. Details, SEM. A, Base of the right anterior tentorial arm, posterodorsal view; B, sensillum placodeum (spl) on second antennomere. Scale bars: 10 µm. Reprinted from Beutel et al. (2009) with permission from Elsevier.

with M. 8, this muscle is here tentatively interpreted as M. frontoepipharyngalis rather than as a neoformation.

1.4.1.5 Antenna (Figs. 1.4.1.1, 1.4.1.2, and 1.4.1.7 B) The three-segmented antenna is about as long as the ­anterior clypeal margin and almost completely devoid of setae. It is inserted on an anterolateral protuberance of the head, which extends beyond the subgenal sulcus. The protuberance is bordered below and medially by the broad margins (here fused into a solid formation) of the anterior tentorial invagination. Antennomere 1 is about as long as wide. Antennomere 2 is slightly narrower and just more than three times as long as wide. One round sensillum (campaniformium?) accompanied by an internal procuticular thickening is present laterally near mid-length, and there are two round plate-like sensilla (Fig. 1.4.1.7 B) and a short socketed “hair” (sensillum basiconicum?) close to the apex. Antennomere 3 is slender, cylindrical, and about as long as antennomere 1; minute hair-like sensilla and a cupuliform sensillum are present on its apex. Clusters of sensory neuron bodies pertaining to these apical sensilla are located in the second antennomere. Chordotonal organs are absent (see Beutel et al. 2009). Setation: The antenna is almost completely glabrous. A short seta is inserted laterally on the apical part of antennomere 2. Musculature: M. 1–4: M. tentorioscapalis, represented by a single flat bundle (Figs. 1.4.1.3 B,C and 1.4.1.5), O: over a considerable length of the dorsal surface of the anterior part of the anterior tentorial arm, I: ventrally on the base of the basal antennomere.

1.4.1.6 Mandible (Fig. 1.4.1.8 A,B) The symmetrical, slender, and elongate mandibles bear a prominent lacinia mobilis. Two long setae are inserted on the lateral side close to the base. The narrow and acuminate apical part forms a “pars incisivus” comprising four aligned teeth of which the apical and the most proximal/dorsal are the largest; the bases of the subapical teeth are delimited on the ventral side by a curved impression, which extends toward the base of the lacinia mobilis. The lacinia mobilis itself is a sizable, well-­ sclerotized process, the apical edge of which bears five close-set, aligned teeth, of which the apical one may be more or less distinctly larger than the others; the outer base of the latter bears a small group of short acanthae (absent in N. dipteroides). On the mesal base, a softwalled protuberance bears tufts of long acanthae, those of the most proximal/dorsal tuft being the longest, while some of those composing the more anterior/ventral tuft are remarkably widened. A row of short, anteriorly directed microtrichia is present on the dorsal side close to the mandibular base. A mola is not developed. The basal parts of the mandibles are widely separated and do not interact. The mandible articulates with the head capsule in the typical dicondylic manner. The ventral condyle is strongly developed. Pilgrim (1972) noted that the lacinia mobilis is deciduous, becoming shed at the transition to the prepupal phase of the fourth larval instar, leaving a darkened scar. Musculature (Figs. 1.4.1.3 B,C, 1.4.1.5, and 1.4.1.11): M. 11: M. craniomandibularis internus, very large, O: posterodorsally and posterolaterally from the head capsule, I: adductor tendon. M. 12: M. craniomandibularis externus, O: ventrolaterally from the posterior part of ­



 51

1.4 Morphology of larvae 

ga

mxp

pla

dst

pgeb

lac

vml

B

A

bst

lap pmt

lbr

eph

C

D

Fig. 1.4.1.7: N. philpotti, larval head. Postgenal bridge and mouthparts; specimen as in Fig. 1.4.1.1, SEM. A, Postgenal bridge and adjacent regions, ventral view; B, maxillolabium and hypopharynx anteroventral view; C, labrum with sensorial fields, anterior view; D, labral sensilla at higher magnification. Abbreviations: bst – basistipes, dst – dististipes, eph – epipharynx, ga – galea, lac – lacinia, lap – labial palp, lbr – labrum, mxp – maxillary palp, pgeb – postgenal bridge, pla – postlabium, pmt – prementum, vml – ventromedial line. Scale bars: A, B, 50 µm; C, 20 µm; D, 5 µm. Reprinted from Beutel et al. (2009) with permission from Elsevier.

the head capsule, I: abductor tendon. M. 13: M. tentorio­ mandibularis (von Kéler’s M. zygomaticus mandibulae) comprises a few extremely thin fibers, which closely follow the mandibular nerve for a considerable distance, O: anterior tentorial arm, I: two discrete sites on the mandibular base, near the dorsal and ventral margin, respectively. A short distance from its origin, the fiber bundle is associated with an aggregation of sensory neurons (Fig. 1.4.1.8 C), and it is straightforward to assume that both the dorsal and ventral groups are proprioreceptors as it is usually the case in insects (see ­Honomichl 2008). Setation: two long setae are inserted laterally close to the base; the anterior one is split into two branches. A short seta is present in the middle region of the lateral side of the mandible.

1.4.1.7 Maxilla (Figs. 1.4.1.3 A, 1.4.1.4 A, and 1.4.1.5) The maxillae form a structural and functional complex with the labium and hypopharynx. They border on the subgenal sulci but have no specialized articulation points with them. The posterior part of the exposed external and (topographically) lower maxillary surface is mostly weakly sclerotized; an exocuticular layer is present but thin. The boundaries between the cardinal and stipital territories are not evident as in other groups of Meco­ pterida (Hinton 1958). Several more strongly pigmented areas are present (Fig. 1.4.1.5) (somewhat different in N. philpotti and N. dipteroides). One is a narrow, medially tapering marginal thickening of the posterior apex of the maxilla. It is partly almost vertically posed, and

52 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

C

B

A

1-4 ata

lcm lcm nmd

psb

11

pmj te11

smj te12

md

te11 te12

Fig. 1.4.1.8: N. philpotti, larval head. A, B, Mandible, SEM. A, Dorsal view; B, ventral view; C, transverse histological section. Mandibular nerve anchored to the anterior tentorial arm, branch extending into mandible contiguous with proprioreceptor and closely associated with delicate fibers of M. tentoriomandibularis (arrows). Abbreviations: ata – anterior tentorial arm, lcm – lacinia mobilis, md – mandible, nmd – mandibular nerve, pmj – primary mandibular joint, psb – prosthecal brush, smj – secondary mandibular joint, te11/12 – tendons of Mm. craniomandibularis internus/externus, 1-4 – M. tentorioscapalis, 11 – M. craniomandibularis internus. Scale bars: 50 µm. Reprinted from Beutel et al. (2009) with permission from Elsevier.

anteromediad from its inner apex, a narrow ribbon-like “posteromedial plate” lines the posterior inner margin of the maxilla in N. dipteroides, while in N. philpotti, only the posterior part of this ribbon is well-developed. In both, the posterior apex is particularly conspicuously thickened. A prominent, broad, and apically tapering thickening, the “medial plate,” extends inward/forward from the medial margin before maxillary mid-length. It is more pronouncedly darkened in N. dipteroides than in N. philpotti. In the latter, a distinct, thickened “­transverse band” extends inward from the lateral maxillary corner at the same level; its inner margin is very narrowly separated from the “medial plate.” In N. dipteroides, this band is only very faintly indicated. The free dorsal maxillary surface bears a “dorsomedial plate,” the anteromedian arm of which extends to the galea/lacinia ­boundary. Posteromedially, the plate is extended into a thick band, which curves around the maxilla basad from the lacinia lobe; its tapering ventral end almost reaches the apex of the medial plate and bears a small seta, likely a proprio­ receptor registering the position relative to the adjacent palp-bearing labial part. The apical part of the maxilla (Fig. 1.4.1.5) is laterally set off from the proximal part by

a transverse fold. It bears the palp and the apically discrete endite lobes. The small apical part of the lacinia is separated from the mesal side of the galea by a deep cleft and a narrow but distinct extension of the “dorsomedial plate.” It is set with short posteriorly directed, nonarti­ culated spines with acuminate apices and with groups of mesally directed hairs. In contrast, the proximal part of the lacinia is set with small flattened, near-pentagonal teeth (Fig. 1.4.1.9 A), which are arranged in several rows. The galea is a moderately sized and a mostly soft-walled prominence with a sclerotized ribbon curving around its inner and dorsal surface. Tufts of long thin “hairs” (acanthae and some socketed setae) are present on the ventral and dorsal side of the apical part and mesally directed, apically curved spines along the anteromesal margin. The palp comprises three palpomeres with a complete ring-shaped sclerotization. The first of these is slightly shorter than wide, and the following is about 2 times as long as the first. The distal palpomere is distinctly narrower, cylindrical, and apically set with a group of densely arranged short sensilla. The cylindrical palpomeres are borne on a protuberance that appears like a medially incomplete palpomere. Laterally, this



protuberance is well-sclerotized and particularly thickened along the proximal margin. On the ventral maxillary surface, the sclerotization embraces the base of the galea and becomes indistinct mesally (in N. dipteroides less pronouncedly so than in N. philpotti). This distal maxillary region bearing the cylindrical palpomeres and the galea is equivalent to Hinton’s (1958) “dististipes.” The dististipital sclerotization is thin and slightly darkened and difficult to observe (see Beutel et al. 2009). Setation: one long seta is present close to the lateral corner of the stipes, behind the “transverse plate,” and two in front of this plate. One seta is located on the medio­ proximal part of the galea, and at least one near the apex of the galea, close to the tuft of acanthae. One ventral seta is present just beyond the sclerotized half-ring on the dististipes, and two are located in the membrane between the penultimate and distal palpomeres. Musculature (Figs. 1.4.1.10 A, 1.4.1.5, and 1.4.1.11): M. 15: M. craniocardinalis, absent. M. 17: M. tentoriocardinalis, two bundles, O: anterior tentorial arm, I: close to the postero­medial margin of the maxilla, M. 17-1 on and around the thickened posterior apex of the “posteromedial plate,” 17-2 slightly more laterally. M. 18: M. tentoriostipitalis is represented by a group of three bundles, O: anterior tentorial arm, in front of M. 17, I: on the “medial plate,” M. 18-1 near its anteromedian corner, M. 18-2 on a large part of the surface, M. 18-3 near the lateral edge of the plate, partly posterad the preceding. M. 19: M. craniolacinialis is likely represented by a muscle that is fairly slender, O: anteriorly on the base of the posterior tentorial arm, together with the tentorio-hypopharyngeal muscle M. 42 (the two run close together for some distance), I: close to the mesal margin of the “medial plate” but laterad the most medial tentoriostipital (M. 18) bundle (Fig. 1.4.1.10 A) and also proximad the lacinia lobe; for the interpretation, see below. M. 19a: M. craniodististipitalis (not listed by von Kéler 1963), a rather large bundle, O: on the lower/posterior wall of the head capsule just laterad the corpoten­torium and in front of the mandibular abductor M. 12; it runs together with the latter for a considerable distance, I: on the upper wall of the maxilla, just behind the “dorsomedial plate.” M. 20: M. stipitolacinialis, absent. M. 21: M. stipitogalealis, absent. M. 22: M. ­stipitopalpalis externus, O: on the posterior (partly near-vertical) maxillary margin laterad from M. 17, I: on the ventrolateral base of the dististipital sclerotization, hence in the furrow proximally demarcating the latter. M. 23: M. stipitopalpalis internus, O: on the “posteromedial plate” immediately in front of the antero­medial bundle of M. 17 and mediad M. 22, I: with a very short

1.4 Morphology of larvae 

 53

tendon on the medial base of the first fully cylindrical palpomere (putatively the morphologically second). Mm. 24–27: Mm. palpopalpales primus-tertius, absent. For a detailed interpretation of maxillary muscles see Beutel et al. (2009).

1.4.1.8 Labium (Figs. 1.4.1.1 D, 1.4.1.3 A,B, and 1.4.1.6 B) The labium (or its anterior part; see below) is located between the maxillae. There is no recognizable border between the pre- and postlabium. The wall of this composite anterior labial region consists of thick and presumably pliable procuticle and is contiguous with the mesal edge of the maxillary base. The presence of a pair of (split) setae some distance behind the palp bases indicates that this region includes the mentum (see Hinton 1958). As mentioned above, the strongly sclerotized and medially divided sclerite that forms the ventromedian closure of the head capsule is referred to here as the postgenal bridge. It may, however, actually be a composite formation including also a postlabial (submental) component; but in the absence of labial muscles, this question remains open. Setae are absent from this sclerite. The palp is re­presented at least by a near-cylindrical segment which is about 3–4 times as long as wide. It bears a round ­sensillum (placodeum?) close to the base on the lateral side and another (campaniformium?) on the lower side beyond mid-length. A group of densely arranged short sensilla basiconica is present at the apex. This segment is borne on a low semi-annular (medially open) sclerotization, which represents either a basal ­palpomere or a “palpiger,” i.e. a remnant of a medially divided prementum. Conditions in N. dipteroides, where the two sclerotizations, unlike in N. philpotti, are near-contiguous, are particularly suggestive of the latter possibility; but due to the absence of ex- and intrinsic palp muscles in larval Mecopterida also, this question must be left open. Discrete paraglossae and glossae are lacking. The smooth membranous distal part of the prelabium (likely including a ligula homologue) extends pronouncedly beyond the palp bases and then ascends toward the opening of the salivarium. Proximad the salivarium, the dorsal prelabium is fused with the hypopharynx (Figs. 1.4.1.6 B and 1.4.1.11). Setation: a pair of long split setae is present on the anterior third of the prelabium close to the lateral margin, and a pair of minute setae is situated on the prelabial extension just beyond the palps. Musculature: absent (see M. 42)

54 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

lbr

md

lcm eph

ga

A

mxp

B

Fig. 1.4.1.9: N. philpotti, larval head. Ventral view on mouthparts, SEM. A, Lacinia, details of toothed surface; B, epipharynx. Abbreviations: eph – epipharynx, ga – galea, lbr – labrum, lcm – lacinia mobilis, md – mandible, mxp – maxillary palp. Scale bars: A, 10 µm; B, 50 µm. Reprinted from Beutel et al. (2009) with permission from Elsevier.

1.4.1.9 Epipharynx (Figs. 1.4.1.3 A and 1.4.1.9) A large part of the epipharynx is exposed. The bulging region behind the ventral side of the labrum is clearly delimited by a transverse groove. A pair of sensorial pegs is present at the anterior margin close to the median line, a group of extremely small and short spine-like microtrichia in the central area, and a dense transverse row of longer/coarser acanthae (and a couple of socketed ­sensilla) along the posterior margin. The lateral hairs are directed mesally and the longer mesal hairs posteriorly. The surface of this immediately postlabral area is smooth and lightly sclerotized. The membranous areas, which are adjacent laterally, are set with very long and thin hairs. The fairly long following intermediate epipharyngeal section is membranous with a corrugated surface; it is devoid of hairs except for scattered very short microtrichia on its anterolateral part. The posteriormost region of the externally exposed epipharynx is densely covered with rows of short, posteriorly directed microtrichia. The following part forms a very short voluminous preoral chamber together with the mouthparts. The posterior epipharynx forms the anterior part of the “roof” of the morphologically composite closed cibario-pharyngeal part of the anterior food tract. Musculature (Figs. 1.4.1.4 C–G and 1.4.1.11): M. 43: M. clypeopalatalis, very strongly developed, composed of two major subcomponents, M. 43-1, O: anterolaterally on the

clypeus, I: laterally on the anterior transverse epipharyngeal area, M. 43-2, composed of several bundles, O: clypeus, behind M. 43a, I: successively on the posterior epipharynx. M. 44: M. clypeobuccalis, a thin muscle passing around the frontolabral muscles (Mm. 8+9) anterad the frontal connectives, O: on and close to the midline of the anteriormost part of the frontoclypeal apotome, just behind the transclypeal sulcus, I:  on the lateral edge of the roof of the preoral chamber; the insertions of the two components of this muscle pair may be so close that the muscles appear to constitute together a single, semicircular bundle. However, no individual fibers have been observed to cross the midline. The dorsolateral edges of the pharynx are connected by a very strong transverse muscle below the frontal ganglion. A very strong transverse muscle is also present on the ventral side.

1.4.1.10 Hypopharynx (Figs. 1.4.1.3 B and 1.4.1.11) The hypopharynx is closely associated with the antero­ dorsal part of the labium, but its apex is separated from the apical edge of the prelabium by a cleft into which the sali­ vary duct opens (see below). Its anteriormost, protruding part is rather densely set with short, proximad-­pointing microtrichia, while more basally, the dorsal surface of the hypopharyngeal lobe is smooth and lightly sclerotized. Behind the produced lobe, the hypopharyngeal wall again



1.4 Morphology of larvae 

18-1

 55

42 sald

trc

18-2

50

23

ata 48

22

A

B

Fig. 1.4.1.10: N. philpotti, larval head. Transverse sections. A, Maxilla at level between Fig. 1.4.1.3 B and C, showing insertion of the craniolacinial muscle (M. 19) (arrow) between two bundles of the tentoriostipital muscle; B, central nervous system in postgenal-bridge region, showing position of tritocerebral commissure close to suboesophageal ganglion. Abbreviations: ata – anterior tentorial arm, sald – salivary duct, trc – tritocerebral commissure, 18(-1, -2) – M. tentoriostipitalis, 22 – M. stipitopalpalis externus, 23 – M. stipitopalpalis internus, 42 – M. tentoriohypopharyngalis, 48 – M. tentoriobuccalis anterior, 50 – M. tentoriobuccalis posterior. Scale bars: 50 µm. Reprinted from Beutel et al. (2009) with permission from Elsevier.

becomes membranous and ascends steeply toward the anatomical mouth; this region is framed by a ribbon-like sclerotization, which is a derivative of the suspensorium, but is unconnected to the sclerotization on the subapical lobe surface. The left and right proximal ends of the ribbon extend into the lateral walls of the sucking pump; they are obviously counterparts of the “oral” arms of the suspensorium in more ­generalized insects and bear corresponding muscle attachments. Musculature (Figs. 1.4.1.3 B,C and 1.4.1.11): M. 41: M. frontohypopharyngalis, O: central area of the frons, posterolaterad M. frontopharyngalis anterior (M. 45), I: laterally on the cibario-pharyngeal chamber, on the apex of the “oral arm” of the hypopharyngeal suspensorium, laterad the attachment of M. 45 and immediately above the insertion of M. 49. M. 42: M. t­ entoriohypopharyngalis, one well-developed bundle, located laterad the circumoesophageal connectives, O: anteriorly on the base of the posterior tentorial arm, together with M. 19, I: on the soft-walled integument immediately proximad and laterad the opening of the salivary duct; the insertion site, together with the small size of the hypopharynx, and ­regression of its lateral sclerites indicate that this muscle

is a hypopharyngeal retractor and not a muscle of the ­prelabium. M. 49: M. tentoriobuccalis lateralis, moderately sized, inserting laterally on the cibario-­pharyngeal tube with a short tendon between the insertion of the anterior subcomponent of M. 41 and the attachment area of the strong ventral transverse muscle (Fig. 1.4.1.3 C); originates on the anterior tentorial arm, immediately adjacent to the origin of the anteromesal fibers of M. tentoriostipitalis (M. 18); the basal parts of both muscles are closely adjacent. The ventral cibarial dilator is listed in the following section.

1.4.1.11 Cephalic digestive tract (Figs. 1.4.1.3 B,C, 1.4.1.10 B, and 1.4.1.11 A) The position of the anatomical mouth is demarcated by the frontal ganglion. The anterior pharynx is a closed tube with the shape of a flattened U in cross section, with distinct dorsolateral folds for muscle attachment (Mm. 41 and 46) and very indistinct ventral and ventrolateral folds. The pharyngeal section below the cerebrum is almost quadrangular in cross section. The lumen is still

56 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

A

51-1 11

br

46

53

nrec

8+9

ceao lm

44

ph

fg

tcs

50

ora

11

8

acl 7

52

48

9

tb

trc lcm

md

lac

soeg

42

37

19 slp

mxp

54

vn

pgeb

17

lap

sald

B 51-1

46-2

11

46-1 45 44

41

49

47

51-2 dta

1-4

52-1

43-2

52-2

ata 43-1 7

18-1

md

tb

50

18-2

vn

17

lcm

42

19a

19

23 mxp 22

pgeb 18-3

54



wide and the folds are moderately distinct. The posteriormost pharynx and the posteriorly adjacent oesophagus are characterized by very deep longitudinal folds and a strongly narrowed lumen. Musculature (Figs. 1.4.1.3 C and 1.4.1.11): M. 45: “M. frontobuccalis anterior” (von Kéler’s 1963 terms for Mm. 45, 46, 47, and 50 are misnomers as the insertions lie posterad the anatomical mouth; s. Beutel et al. 2009), moderately sized, with a very oblique (backward/inward) course, O: dorsolaterally on the frons above the eye, close to (in front of) the origin of M. 41, I: dorsally on the pharynx, close to the midline. M. 46: “M. ­frontobuccalis posterior” (dorsal pharynx dilator of Denis & Bitsch 1973), a large bipartite muscle, M. 46-1, a long series of bundles, O: posterior frons, anterolaterad the origin of Mm. 8+9 and close to the anteromedial surface of the brain, I: dorsolateral fold of the precerebral pharynx, M. 46-2, a somewhat shorter series of bundles, O: frons, mediad M. 46-1 (but still laterad Mm. 8+9), just in front of the brain, I: dorsomedially on the precerebral pharynx (course of fibers less oblique than those of M. 46-1, almost perpendicular to head capsule). M. 47: “M. frontobuccalis lateralis” (lateral pharynx dilator of Denis & Bitsch 1973), O: frons adjacent to M. 41, I: laterally on the pharynx, below the attachment of the anterolateral bundles of M. 46. M. 48: M. tentoriobuccalis anterior, a pair of thin bundles, immediately adjacent to the dorsal surface of the suboesophageal complex over more than half of their length, O: laterally on the tentorial bridge, I: floor of the sucking pump, at the anatomical mouth. M. 50: “M. tentoriobuccalis posterior” (ventral pharynx dilator of Denis & Bitsch 1973); the fibers pertaining to this set are separated from the preceding muscle by the tritocerebral commissure, O: paramedially on the tentorial bridge, adjacent to M. 48, I: ventrally on the anterior pharynx. M. 51: M. verticopharyngalis, comprising at least two components, M. 51-1, a well-developed bundle, O: dorsally on the anterior vertex, I: dorsal wall of the pharynx and dorsal and dorsolateral folds, immediately posterad the

1.4 Morphology of larvae 

 57

brain; M. 51-2, an oblique muscle, O: dorsolaterally on the vertex, I: laterally on the pharynx, very close to the attachment of M. 51-1. The posteriormost dorsal dilator may be considered derived from the preceding (and could hence be referred to as “M. 51-3”), but it is apparently what was referred to as a separate muscle, M. 53 (“M. postoccipitooesophagalis”) in von Kéler’s (1963) scheme (the meaningfulness of this distinction appears ­questionable), O: dorsolaterally on the apodemal posterior vertex (arguably a postoccipital phragma), I: dorsolateral fold of the posteriormost pharynx. M. 52: M. t­entoriopharyngalis, composed of a series of oblique bundles, of which the most anterior has the origin separate from the rest, M. 52-1, O: on top of the posterior part of the anterior tentorial arm, a short distance behind the dorsal arm vestige, I: ventrolateral fold of the pharynx, M.52-2, O: lateral side of the base of the posterior tentorial arm, I: ventral and ventrolateral fold of the posterior pharynx, below the insertion of M. 51-1 and -2. M. 54: M. tentoriooesophagalis (one of the “dilatateurs ventraux du pharynx” of Denis & Bitsch 1973; origin secondarily shifted to head capsule; see Beutel et al. 2009), O: ventrolaterally from the postoccipital ridge, I: ventrolateral fold of the posteriormost pharynx, below the insertion of M. 53. The ring musculature is well-developed over the entire length of the pharynx (Figs. 1.4.1.10 B and 1.4.1.11 A). The muscles of the posterior part are slightly thinner. ­Longitudinal muscles are present but very thin on the lateral sides of the pharynx. They are more distinctly developed between the dorsal and ventral folds, especially the dorsal muscles of the cibario-pharyngeal region.

1.4.1.12 Labial glands and salivarium (Figs. 1.4.1.11 and 1.4.1.12) The salivary glands are simple paired tubes, the secretory sections of which are located in the first abdominal segment, adjacent to the foregut (Fig. 1.4.1.12). These

◂ Fig. 1.4.1.11: N. philpotti, larval head. Right part reconstructed from serial sections and whole mount preparations. A, Sagittal section,

slightly oblique, posteriorly just laterad from median weakness line in postgenal bridge; B, parasagittal section, central nervous system and lateral portion of M. 8 and 9 omitted, stomodaeum indicated in outline (dashed) only. Abbreviations: acl – anteclypeus, ata – anterior tentorial arm, br – brain, ceao – cephalic aorta, dta – dorsal tentorial arm, fg – frontal ganglion, lac – lacinia, lap – labial palp, lcm – lacinia mobilis, lm – longitudinal muscle fibers, md – mandible, mxp – maxillary palp, nrec – nervus recurrens, ora – oral arm of hypopharyngeal suspensorium, pgeb – postgenal bridge, ph – pharynx, sald – salivary duct, slp – sensory neuron bodies of labial palp sensilla, soeg – suboesophageal ganglion, tb – tentorial bridge, tcs – transclypeal sulcus, trc – tritocerebral commissure, vn – ventral neck muscles, 1-4 – M. tentorioscapalis, 7 – M. labroepipharyngalis, 8 – M. frontolabralis, 9 – M. frontoepipharyngalis, 11 – M. craniomandibularis internus, 17 – M. tentoriocardinalis, 18(-1, -2, -3) – M. tentoriostipitalis, 19 – M. craniolacinialis, 19a – M. craniodististipitalis, 22 – M. stipitopalpalis externus, 23 – M. stipitopalpalis internus, 37 – M. hypopharyngosalivarialis, 41 – M. frontohypopharyngalis, 42 – M. tentoriohypopharyngalis, 43(-1, -2) – M. clypeopalatalis, 44 – M. clypeobuccalis, 45 – “M. frontobuccalis anterior,” 46(-1, -2) – “M. frontobuccalis posterior,” 47 – M. frontobuccalis lateralis, 48 – M. tentoriobuccalis anterior, 49 – M. tentoriobuccalis lateralis, 50 – M. tentoriobuccalis posterior, 51(-1, -2) – M. verticopharyngalis, 52(-1, -2) – M. tentoriopharyngalis, 53 – M. postoccipitooesophagalis, 54 – M. “tentoriooesophagalis.” Reprinted from Beutel et al. (2009) with permission from Elsevier.

58 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

br nrec ncc

aow cm

aos oes

taw

C 11

aow nrec

A

cm

oes ca

B

D

sections are club-like swellings of the terminal parts of the two tubes. Their secretory epithelial cells are greatly enlarged. Toward the anterior ends of the secretory sections, the cytoplasm of the epithelial cells become denser, and the transition into the non-secretory gland duct is characterized by a marked decrease in cell size (Fig. 1.4.1.12 A). The cuticular intima of the thin-walled ducts is strengthened by taenidium-like thickenings, which are somewhat stouter and more widely spaced than their counterparts on equidimensional tracheae. In the cervical region, the two gland ducts fuse into a common duct, which extends forward close to the suboesophageal ganglion. The topographical relations between duct and ganglion varies between individuals: there may be space enough for the duct to be located between the ganglion and the head (postgenal bridge) wall, but alternatively, the ganglion may be pressed against the wall, in which case the duct either runs to one side of it or is lodged in a ventral furrow of the ganglion. The salivarium is fairly narrow and opens medially between the upper edge of the prementum and the anteroventral margin of the hypopharynx.

Fig. 1.4.1.12: N. philpotti, larval head, details of internal structure, histological sections. A, Salivary gland: secretory terminal region in abdominal segment I, horizontal section; B, salivary gland, transition between secretory and nonsecretory regions, horizontal section; C, anterior aorta region, parasagittal section; D, ventrally open aorta sinus and corpus allatum, transverse section. Abbreviations: aos – sinus of cephalic aorta, aow – wall of cephalic aorta, br – brain, ca – corpus allatum, cm – circular muscle fibers of oesophagus, ncc – nervus corporis cardiaci, nrec – nervus recurrens, oes – oesophagus, taw – thickened ventral margin of aorta sinus wall, 11 – M. craniomandibularis internus. Scale bars: A–C, 100 µm; D, 50 µm. Reprinted from Beutel et al. (2009) with permission from Elsevier.

Musculature (Figs. 1.4.1.3 B and 1.4.1.11): M. 37: M. hypopharyngosalivarialis, a well-developed oblique muscle, O: dorsal wall of the posterior hypopharynx, floor of the preoral chamber, I: dorsal wall of the anterior salivary duct. M. 38: M. praementosalivarialis anterior, absent. M. 39: M. praementosalivarialis posterior, absent. M. 40: M. annularis salivarii, absent.

1.4.1.13 Nervous system (Figs. 1.4.1.11 and 1.4.1.13) The cephalic central nervous system takes up a relatively large part of the head lumen. The protocerebral lobes are anteriorly united for less than half of their lengths; their posterior parts taper markedly as they extend toward the foramen occipitale. The protocerebral optic nerve and the deutocerebral antennal nerve are both slender. A sensory “nervus tegumentalis” (of tritocerebral origin?) arises on the posterior side of the brain; it is forked immediately at its base. The frontal ganglion connective (“ventral root of the frontal ganglion”) and the labral nerve separate at the level of the frontal ganglion, where the former turns



1.4 Morphology of larvae 

abruptly mediad. The circumoesophageal connectives are almost vertically oriented and fairly short and thick. The tritocerebral commissure is situated in a remarkably low position between the connectives, being separated from the upper surface of the suboesophageal ganglion only by the very thin bundles of M. tentoriohypopharyngalis (M. 48). The frontal ganglion is small and flattened and the procurrent nerve is minute. The nervus recurrens is pressed against the ventral surface of the brain in two of the sectioned specimens, while in a third, it runs close to the brain, but clearly separated from it. It is noteworthy that a nervus connectivus (“dorsal root of the frontal ganglion”) is absent. The suboesophageal ganglion is large and occupies most of the space between the corpotentorium (and posterior parts of the anterior tentorial arms) and the ventral wall of the head capsule, against which it is pressed in some specimens (Figs. 1.4.1.10 B, 1.4.1.11 A, and 1.4.1.12). The mandibular, maxillary, and labial nerves all arise from the topographically anterior surface of the suboesophageal ganglion, the maxillary nerve giving off a sizable branch (which, on its course into the maxillary base, extends between the tentorio-cardinal and tentorio-­stipital muscles) already at its very exit from the ganglion. Small globular structures in the clypeal region apparently represent aggregates of sensory neuron bodies.

ncc

br nrec fg

nlbr

nteg nan

nrec

nop

nmd

soeg nmx nla

cco

Fig. 1.4.1.13: N. philpotti, cephalic central nervous system, reconstruction from serial sections, lateral view. Abbreviations: br – brain, cco – cervical connective, fg – frontal ganglion, nan – nervus antennalis, ncc – nervus corporis cardiaci, nla – nervus labialis, nlbr – nervus labralis, nmd – nervus mandibularis, nmx – nervus maxillaris, nop – optic nerve, nrec – nervus recurrens, nteg – nervus tegumentalis, soeg – suboesophageal ganglion. Reprinted from Beutel et al. (2009) with permission from Elsevier.

 59

Similar aggregations occur at the bases of the labial palps (Fig. 1.4.1.11 A).

1.4.1.14 Aorta and retrocerebral organs (Fig. 1.4.1.12 C,D) The ventral wall of the aorta opens some distance behind the brain. At this level, the ventral margins of the lateral aorta walls become thickened and comprise more cell layers. These thickened aorta margins represent the corpora cardiaca and they are contiguous with the terminal fork of the recurrent nerve and with the small, near-spherical corpora allata. In each side, they receive only a single (not two as more usual) brain nerve (“nervus corporis cardiaci”), which extends backward adjacent to the lateral aorta wall. An innervation of the retrocerebral complex from the suboesophageal ganglion is apparently missing. The simple lower margins of the lateral aorta wall in front of the thickenings become attached to the stomodaeal muscularis, and the recurrent nerve is located in the closed space thereby formed. The aorta sinus terminates at the posterior surface of the brain, to which its dorsal/lateral walls become attached.

1.4.1.15 Fat body No fat body tissue was found in the head of the specimens examined. Rolf G. Beutel & Frank Friedrich

1.4.2 Thorax (mainly based on Pilgrim 1972) The thorax is very short compared to the rest of the postcephalic body (ca. 3 mm in the largest final instar specimen) (Fig. 1.4.1). The segments are shorter than wide and the prothorax smaller than each of the pterothoracic segments, which are about equally sized (Fig. 1.4.2.1). Two small cervical sclerites are present ventrolaterally on each side; like the pronotum and some parts of the legs, they are sclerotized. The anterior sclerite is slender and Y-shaped, the posterior one oval, vertically oriented, and close to the procoxa (Kluge 2003: fig. 1). A fairly broad, lightly sclerotized anterior collar of the prothorax is present. The distinctly sclerotized pronotal shield is distinctly narrowing anteriorly. Its brown coloration is medially interrupted by a thin, unpigmented ecdysial line and a pattern with areas of lighter pigmentation is recognizable. The hind margin is darker than the remaining parts (as in the case of the head, the pigmentation develops from the posterior aspect after each moult but

60 

cvm

 1 Nannomecoptera, Nannochoristidae, Nannochorista

nt1

spi

nt2

nt3

he

leg1

leg2

leg3

precedes that of the head capsule; Pilgrim 1972). The meso­ thorax and metathorax are of a grayish color and resemble the abdominal segments, but with a different pattern of translucent areas (Fig. 1.4.1). Few very fine setae are present on all three segments (Fig. 1.4.1.1). A spiracular opening lies dorsolaterally in an unpigmented notch of the pronotal shield at the posterior 1/6. It is circular or slightly oval, 35–40 µm in diameter, and consists of a well-sclerotized central scar with 12–16 openings and a narrow peritreme. A minute (7 µm) stigmatic scar of a nonfunctional spiracle is present on the metathorax, about midlaterally close to the anterior margin of the segment. All legs are similar in shape, size, and composition (we do not follow the interpretation of Kluge 2003, see below), and inserted ventrolaterally on the anterior third of their segment, projecting forward and outward (Figs. 1.4.2.1 and 1.4.2.2). The prolegs are slightly longer than those of the meso- and metathorax. In contrast to Kluge (2003), who examined a single “immature larva,” each leg consists of five distinctly developed segments1 (Fig. 1.4.2.2). The coxa is short and broad and bears few long setae. The following element, probably comprising the trochanter and femur, is by far the largest part of the leg. It is more than twice as long as the coxa and conical, gradually narrowing toward its apex, and it bears a few long setae, five stout lanceolate setae, and a patch of very short, fine ventrally. A moderately distinct transverse setae mid-­ furrow on all the legs is possibly an obliterated trochantero-femoral border. The approximately cylindrical tibia is much smaller than the preceding segment and about twice as long as wide. It bears a long apodeme extending

1 The homologization of the elements is problematic. We largely rely on Pilgrim’s (1972) interpretation here.

Fig. 1.4.2.1: Nannochorista philpotti, thorax, lateral view, line drawing. Abbreviations: abdI – abdominal segment I, cvm – cervical membrane, he – head, nt1/2/3 – pro-/meso-/metanotum, spi – spiracle. Scale bar: 250 µm.

abdI

well into the femur. At its distal end on the ventral side, it forms a solid blunt process, which bears a group of very short setae. Dorsolaterally, a short comb of curved, medium-sized setae is present, possibly functioning as a cleaning device. The tarsus is slightly longer than the tibia. Interestingly, it is subdivided into two segments by a fairly distinct furrow. The proximal subunit is cylindrical and shorter than wide, and it bears a few very short and fine setae, one of them laterally, immediately close to the distal margin. The distal tarsal subunit is about twice as long and slightly narrowing toward its apex. Its strongly developed single claw is equipped with four articulated curved setae, which are as long as the claw itself; one of them arises on the convex surface near the base, two are symmetrically placed on the sides, and the fourth is on the posterior surface. The dorsal surfaces of the leg are sclerotized, as well as the tibial apodeme and the claw. The coloration of these regions is brown. Musculature: leg muscles were illustrated by Kluge (2003: figs. 1 and 2). However, as only one “immature” specimen was examined (without dissections or microtome cx

tar

cl

tib

fem

tr

Fig. 1.4.2.2: N. philpotti, middle leg, lateral view, line drawing. Abbreviations: cl – claw, cx – coxa, fem – femur, tar – tarsus, tib – tibia, tr – trochanter. Scale bar: 50 µm.



1.4 Morphology of larvae 

sectioning) and the interpretation of the sclerites appears uncertain (see above), we do not reproduce these results here. Maximilian Fraulob, Frank Hünefeld & Rolf G. Beutel

1.4.3 Abdomen (mainly based on Fraulob et al. 2012)

 61

the lateral ventral internal muscle consist of numerous fiber bundles. One pair of oblique dorsoventral muscles connects the ventrolateral segmental border of each segment with the dorsolateral wall of the anterior third of the same segment. No lateral muscles were identified.

1.4.3.2 Abdominal segment X

1.4.3.1 Abdominal segments I–IX The 10-segmented abdomen is strongly elongated, slender, and round in cross section. Like most other parts of the larva, it is almost completely unpigmented, with the exception of the terminal hooks (Fig. 1.4.1). The cuticle is thin, smooth, and largely glabrous. The anterior segments are about 2 mm long in N. philpotti. The length decreases toward the abdominal apex. The terminal segment X is approximately 1 mm long. Segments I–IX are largely unmodified and very similar in size and shape (Fig. 1.4.3.1). They completely lack prolegs or other appendages. Clearly defined sclerites are not present. Several scattered setae are inserted laterally (Fig. 1.4.3.1). On the dorsal side of segment IX, two setae are inserted on a line perpendicular to the longitudinal body axis, both approximately 100 µm below the dorsal midline. Musculature of segments I–IX: two pairs of ­external dorsal muscles, one pair of internal dorsal muscles, two pairs of external ventral muscles, and two pairs of internal ventral muscles are present in segments I–VIII. All of them except for the mesal dorsal external and

The terminal segment differs distinctly from the preceding ones. A pair of ovoid fields of microtrichia is present on the anterior third. The microtrichia (Fig. 1.4.3.3 C) are arranged in approximately 60 circular groups of ca. 15 microtrichia in each of them. Close to the caudal end of the segment on the dorsal side, a pair of setae is inserted approximately 60 µm below the dorsal midline. Approximately 50 µm below these setae, two additional paired setae are inserted. A third pair is present approximately 50 µm anterior to the second pair. Approximately 50 µm below the third pair and slightly shifted caudally, a fourth pair is inserted. Accordingly, the setae of the second, third, and fourth pair are arranged in a triangle. A fifth pair is present approximately 70 µm below the second pair. All setae are approximately 100–150 µm long and ovoid in cross section. An unpaired seta lies immediately above the left seta of the first pair. It is approximately 50 µm shorter than the others. A pair of three-segmented lobes is inserted at the posterior end of the segment (Figs. 1.4.3.1 A, 1.4.3.2, and 1.4.3.3 B), each with a terminal hook. They are curved ventrally with the apices pointing anteriorly. The slightly elevated basal segment (Fig. 1.4.3.3 A,B,E) is connected with

lo

abdsX abdsX mtf

abdsIX

abdsIX

abdsVIII

A

abdsVIII

B

C

Fig. 1.4.3.1: N. philpotti, larval postabdomen, SEM. A, Dorsal view; B, lateral view; C, ventral view. Abbreviations: abdsVIII-X – abdominal segments VIII-X, lo – lobe, mtf – field of microtrichia. Scale bar: 500 µm. Modified from Fraulob et al. (2012).

62 

 1 Nannomecoptera, Nannochoristidae, Nannochorista

abdsIX

abdsX

db csm

lo

lo mpo vb

go Fig. 1.4.3.2: N. philpotti, larval postabdomen, caudal view, SEM. Abbreviations: abdsIX-X – abdominal segments IX-X, csm – cuticular surface modification, db – dorsal bulge, go – gland opening, lo – lobe, mpo – membranous pouch opening, vb – ventral bulge. Scale bar: 100 µm. Modified from Fraulob et al. (2012).

a cone-shaped intermediate segment (Fig. 1.4.3.3 A,B,E), which is slightly bent ventrally. The intermediate segment bears the slightly sclerotized curved hook apically (Fig. 1.4.3.3 A,B,E). Ventrolaterally on the basal segment, two setae are inserted in a line perpendicular to the longitudinal body axis and separated by approximately 20 µm. Another seta is inserted ventrolaterally on the intermediate segment. Both setae are about as long as those on the proximal main part of segment X. Ventrolaterally on the basal segment lies the opening of a gland (Fig. 1.4.3.2), which is placed inside the proximal part of the lobes. As the cell limits of the epithelium are not recognizable on semithin sections, it remains unclear whether the glands belong to type 1 or type 3 of Noirot & Quennedy (1974). The slit-like, vertical opening of the unpaired membranous pouch lies between the lobes (Figs. 1.4.3.2 and 1.4.3.3 A,B,D). Dorsally and ventrally, it is enclosed by a bulge immediately below and above the basal element of the lobes (Figs. 1.4.3.2 and 1.4.3.3 A,B,E). There, the opening divides into two branches. The entire surrounding area of the opening is covered with scale-like, apically

fringed cuticular surface modifications (Figs. 1.4.3.2 and 1.4.3.3 B,D) of approximately 20 µm length. Musculature of segments IX and X (Figs. 1.4.3.4 and 1.4.3.5). M1, O (=origin): paramedially and dorsally on anterior half of segment IX, I (=insertion): dorsally and paramedially on border between segments IX and X, F (=hypothesized function): contraction of segment IX, retractor of segment X. M2, O: dorsally and paramedially on border between segments VIII and IX, I: dorsally and paramedially on border between segments IX and X, ventrolaterad M1, F: contraction of segment IX, retractor of segment X. M3, O: dorsolaterally on border between segments VIII and IX, I: dorsolaterally on border between segments IX and X, ventrad M2, F: contraction of segment IX, retractor of segment X. M4, O: dorsolaterally, close to the anterior margin of segment IX, I: dorsolaterally on border between segments IX and X, ventrolaterad M3, F: contraction of segment IX, retractor of segment X. M5, O: ventrally and paramedially close to anterior margin of segment IX, I: ventrally and paramedially on border between segments IX and X, F: contraction of segment IX, retractor of segment X. M6, O: ventrally and paramedially on border between segments VIII and IX, I: ventrally and paramedially on border between segments IX and X, dorsolaterad M5, F: contraction of segment IX, retractor of segment X. M7, O: ventrolaterally on border between segments VIII and IX, I: ventrolaterally on border between segments IX and X, dorsolaterad M6, F: contraction of segment IX, retractor of segment X. M8, O: ventrolaterally on border between segments VIII and IX, I: ventrolaterally on border between segments IX and X, dorsad M7, F: contraction of segment IX, retractor of segment X. M9, O: dorsolaterally on border between segments VIII and IX, I: dorsally and paramedially on membranous pouch, anterior apex of the dorsal papilla, F: retractor of the dorsal papilla. M10, O: dorsolaterally on border between segments VIII and IX, I: dorsally and paramedially on membranous pouch, anterior apex of dorsal papilla, ventrad M9, F: retractor of dorsal papilla. M11, O: ventrolaterally on border between segments VIII and IX, I: ventrally and paramedially on membranous pouch, anterior apex of ventral papilla, F: retractor of dorsal papilla. M12, O: ventrolaterally on border between segments VIII and IX, I: ventrally and paramedially on anterior third of the membranous pouch, anterolaterad proximal opening of ventral papillary pouch, F: retractor of membranous pouch. M13, O: ventrally on border between segments VIII and IX, I: ventrally on anterior third of membranous pouch, anterolaterad the ventral papillary pouch, paramedially and dorsomedially of M12, F: retractor of



 63

1.4 Morphology of larvae 

A

B

abdsX

abdsX

vb

db bs

bs

ho

is

ho

bs

is

is

is mpo

mpo

C

D

E

csm

ho

bs

csm

db

mpo

bs

is lo

abdsX

ho vb is Fig. 1.4.3.3: N. philpotti, larval postabdomen, details of segment X, SEM. A, Ventral view; B, dorsal view; C, field of microtrichia; D, caudal view; E, lateral view. Abbreviations: abdsX – abdominal segment X, bs – basal segment, csm – cuticular surface modification, db – dorsal bulge, ho – hook, is – intermediate segment, lo – lobe, mpo – membranous pouch opening, vb – ventral bulge. Scale bars: A, B, D, 50 µm; C, D, 20 µm. Modified from Fraulob et al. (2012).

membranous pouch. M14, O: ventrolaterally on border between segments VIII and IX, I: ventrally on membranous pouch, anterior apex of ventral papillary pouch, dorsolaterad M11, F: retractor of ventral papilla. M15, O: ventrolaterally on border between segments IX and X, posterior to M8, I: dorsally on membranous pouch, anterior end of dorsal papillary pouch, ventrolaterad M9, F: retractor of membranous pouch. M16, O: ventrally and paramedially on segment X, laterally on hindgut with few fibers, I: ventrally and paramedially on segment X, merges posteriorly with M15, F: retractor of membranous pouch. M17, O: ventrolaterally, close to antesegmental margin, I: ventrally and paramedially rior ­ on membranous pouch, anterior end of ventral papilla, ventrad M11, F: retractor of ventral papilla. M18, O: ­ventrolaterally, close to anterior margin of segment X, posterior to M17, I: ventrally and paramedially on

membranous pouch, anterior apex of ventral papilla, laterad M14, F: retractor of ventral papilla. M19, O: ­ventrolaterally, close to anterior margin of segment X, posterior to M18, I: ventrally and paramedially on membranous pouch, anterior third of ventral papillary pouch, F: retractor of ventral papilla. M20, O: ventrolaterally, close to anterior margin of segment X, posterad M19, I: ventrally and paramedially on membranous pouch, anteriorly dorsal papilla, ventrad M10, F: r­ etractor of dorsal papilla. M21, O: ventrolaterally, close to anterior margin of segment X, ventrad M19, I: ventrolaterally, close to anterior margin of segment X, terminal hook at junction of basal and intermediate segment, F: retractor of terminal hook. M22, O: ventrolaterally, anterior half of segment X, I: ventrally and paramedially on middle region of membranous pouch (ventrolateral invagination), F: retractor of membranous pouch. M23, O: ventrolaterally, anterior half of segment X,

64 

A

 1 Nannomecoptera, Nannochoristidae, Nannochorista

M10

dtra M15

M18 M20 i M17 M19

dap

M9 dMt hg M1 M2 M3

B

M25

M4

M5 M6

M26 M27

M16 M33 M7 M8 M13 vMt M12 vtra M21

dpo M29 M28

mep

vpo

M11

M14

C

i

dMt

vap M24 M31 M30 M23 dap dpo a mep

M22 dtra

hg

M32

lo

lo vMt vtra

vap

vpo

dorsad M22, I: ventrally and paramedially on middle region of membranous pouch, dorsad M22, F: retractor of membranous pouch. M24, O: ventrolaterally, anterior half of segment X, posterodorsad M23, I: ventrolaterally, close to posterior margin of segment X, terminal hook at junction of basal and intermediate segment, laterad M21, F: retractor of terminal hook. M25, O: dorsolaterally on anterior half of segment X, I: ventrolaterally on posterior third of membranous pouch, F: retractor of membranous pouch. M26, O: dorsolaterally on anterior half of segment X, posterodorsad M25, I: dorsally and paramedially on middle region of membranous pouch (dorsolateral invagination), F: retractor of membranous pouch. M27, O: dorsolaterally on anterior half of segment X, ventrolaterad M26, I: dorsally and paramedially on middle region of membranous

Fig. 1.4.3.4: N. philpotti, larval postabdomen, segments IX–X, 3D reconstruction based on semithin sections. A, Dorsal view; B, ventral view; C, mesal view (muscles removed, gut and membranous pouch transparent). Abbreviations: a – anus, dap – dorsal anal papilla, dMt – dorsal Malpighian tubule, dpo – dorsal papillary pouch, dtra – dorsal trachea, hg – hindgut, i – integument, lo – lobe, mep – membranous pouch, vap – ventral anal papilla, vMt – ventral Malpighian tubule, vpo – ventral papillary pouch, vtra – ventral trachea. See text for muscle details. Scale bars: 250 µm. Modified from Fraulob et al. (2012).

pouch (dorsolateral invagination), ventrolaterad M26, F: retractor of membranous pouch. M28, O: dorsolaterally on anterior half of segment X, I: dorsally and paramedially on anterior third of membranous pouch (dorsolateral invagination), F: retractor of membranous pouch. M29, O: dorsolaterally on anterior half of segment X, ventrolaterad M28, I: ventrolaterally, close to posterior margin of segment X, terminal hook at junction of basal and intermediate segment, dorsad M21, F: retractor of terminal hook. M30, O: ventrolaterally, posterior half of segment X, I: ventrally and paramedially on posterior third of membranous pouch (ventrolateral invagination), F: retractor of membranous pouch. M31, O: ventrolaterally on posterior half of segment X, posterior to M30, I: ventrally and paramedially on membranous



1.4 Morphology of larvae 

A

hg

i

dtra

dMt dap dpo

vpo

vap

C

M2 M3

M6

M15 M16

M12

M14

M13

M22

B

mep

lo M28

M31

D M29

M23

M9

M10

M25 M26 M27

M11

M8 M4

M17

M20

M1

M5

 65

M19 M21

M7

M18

M24

M30

M32

Fig. 1.4.3.5: Nannochorista sp., larval postabdomen, segments IX–X, 3D reconstruction, right body side, mesal view, cuticle transparent. A, Ventral Malpighian tubule und trachea removed; gut, membranous pouch and anal papillae transparent; B, gut, membranous pouch and anal papillae removed; C, muscles 9, 10, 11, 25, and 27 removed; D, muscles 2, 6, 8, 12, 13, 14, 15, 16, 22, 23, 26, 28, 29, and 31 removed. Abbreviations: dap – dorsal anal papilla, dMt – dorsal Malpighian tubule, dpo – dorsal papillary pouch, dtra – dorsal trachea, hg – hindgut, i – integument, lo – lobe, mep – membranous pouch, vap – ventral anal papilla, vpo – ventral papillary pouch. See text for muscle details. Scale bar: 250 µm. Modified from Fraulob et al. (2012).

pouch, anterior end of ventral papillary pouch, dorsad M14, F: retractor of membranous pouch. M32, O: ventrolaterally on posterior half of segment X, posterior to M30, I: ventrally and paramedially on posterior third of membranous pouch (ventrolateral invagination), ventrad M25, F: retractor of membranous pouch. M33, O: ventrolaterally, close to anterior margin of segment X, ventrad M20, I: ventrally and paramedially on membranous pouch, anteriorly on dorsal papilla, dorsad M20, F: retractor of dorsal papilla.

1.4.3.3 Anal papillae Two finger-like retractile anal papillae are present between the terminal lobes (Pilgrim 1972) ventrally (Figs. 1.4.3.4 B,C, 1.4.3.5 A, and 1.4.3.6) and dorsally (Figs. 1.4.3.4 A,C, 1.4.3.5 A, and 1.4.3.6), respectively. They are separately placed in anteriorly oriented ventral and dorsal invaginations of the membranous pouch (Figs. 1.4.3.4 A,C, 1.4.3.5 A, and 1.4.3.6 A), referred to as papillary pouches in the following (Figs. 1.4.3.4, 1.4.3.5 A,B, and 1.4.3.6 B; ­Kaltenbach 1978: “Hauttaschen”). Anteriorly, they reach

the anterior third of segment X. The anal papillae are seamlessly connected with the anterior end of the respective papillary pouch. Accordingly, the anal papillae can be interpreted as posteriorly directed evaginations of the invaginated unit formed by the membranous pouch and the papillary pouches. The hypodermal cells of the membranous pouch and the paired papillary pouches form a very thin squamose epithelium. The nuclei are located in extensions of the cell bodies. The endocuticle produced by the hypodermis lines the inner wall of the membranous pouch and the papillary pouches. When fully extruded, the papillae are approximately half as long as segment X (Pilgrim 1972). They are unpigmented and transparent (Pilgrim 1972), the surface is smooth, and they are triangular in cross section. Below their cuticle, a single layer of flattened hypodermal cells is present (Pilgrim 1972). Between these cells are some larger cells with a very large granular nucleus. Numerous small cubic cells are also present in the hypodermis of the anal papillae. They appear white and shiny in cross sections, obviously due to large vacuoles. The lumen of the anal papillae is filled with hemolymph (Pilgrim 1972) and appears granular.

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dap

dtra dap dMt dpo

mep

hg vpo

vap vap

A

B

vMt

vtra

Fig. 1.4.3.6: Nannochorista sp., larval postabdomen, histological cross sections. A, Posterior third of segment X; B, transitional region of papillary pouches and anal papillae. Abbreviations: dap – dorsal anal papilla, dMt – dorsal Malpighian tubule, dpo – dorsal papillary pouch, dtra – dorsal trachea, hg – hindgut, mep – membranous pouch, vap – ventral anal papilla, vMt – ventral Malpighian tubule, vpo – ventral papillary pouch, vtra – ventral trachea. Scale bars: 50 µm. Modified from Fraulob et al. (2012).

The lumen of each anal papilla contains the terminal portion of one Malpighian tubule (Figs. 1.4.3.4, 1.4.3.5 A, and 1.4.3.6 B). They are round in cross section and a central lumen is recognizable. In histological cross sections, they appear darker than the surrounding hemolymph. Together with the other four Malpighian tubules, they originate at the midgut-hindgut border in segment VI. The four free tubules end in segment VIII (Pilgrim 1972). The other two form a loop, which reaches segment X, where they enter the anal papillae at the anterior end of the membranous pouch. The tubules extend toward the posterior end of the anal papillae. They become narrower toward their apex and reach about half-length of the papillae (Fig. 1.4.3.5 C). A trachea is also present inside each anal papilla, directly below the ventral Malpighian tubule and above the dorsal tubule (Figs. 1.4.3.4 B,C, 1.4.3.5 A, and 1.4.3.6 B). These structures are in close contact. The tracheae originate on a branch connected with a dorsolateral trachea shortly before the segmental border IX–X. They run below the dorsolateral muscles, the ventral trachea in the left body half, and the dorsal one on the right side. Within segment X, they extend toward the anterior end of the pouch, where they enter the anal papillae together with the Malpighian tubules. They end at approximately the same region as the tubules (Fig. 1.4.3.5 A).

1.4.3.4 Digestive tract The hindgut (Fig. 1.4.3.5 A) enters the membranous pouch in the middle region of segment X. The anal opening (Fig. 1.4.3.4 C) lies within a posteriorly directed evagination of the pouch between the dorsal and ventral papillary pouches.

Rolf G. Beutel & Margarita Yavorskaya

1.5 Morphology of pupae (based on Pilgrim 1972) The only description of a pupa of Nannochoristidae was provided by Pilgrim (1972). The pupal stage (Fig. 1.5.1 A) is preceded by a prepupa, which is not equivalent with the pharate pupa developing later. The prepupa leaves the stream and can be found in damp vegetation such as moss. It is an active but non-feeding larva in the later phase of the fourth stage, with distinctive morphological features and also differing in the behavior. In its appearance, it differs from the early fourth instar in its coloration and usually C-shaped body. The unsclerotized body parts are opaque cream due to underlying fat body material, with the spiracles standing out conspicuously. The mesothorax develops



paired, broad longitudinal areas, and the metathorax, a broad U-shaped region. A single median longitudinal stripe becomes visible on abdominal segments I–IX, broad anteriorly but narrowing toward the abdominal apex. All these areas have diffuse edges and a dark brown coloration. They remain on the larval (prepupal) exuviae after the next ecdysis. The head remains unchanged except for the loss of the lacinia mobilis, which leaves a dark brown scar on the mesal mandibular surface. The thoracic segments become opaque and swollen, especially the meso- and metathorax, correlated with the developing anlagen of the wings and adult legs. The larval legs also appear very swollen and stubby but are still functional. The abdomen remains largely unchanged externally and retains the terminal hooks and anal papillae. In contrast to the larva, the general appearance of the pupa dectica exarata (Fig. 1.5.1 A) is quite similar to that of other described mecopteran pupae (e.g. Byers 1963: Panorpa; Setty 1940: Bittacus; Russell 1979, 1982: Cauri­ nus dectes). The body is strongly C-shaped, with a total length of approximately 5 mm. As in the adult males, the terminal abdominal segments of the pupae of either sex were never observed upturned (Pilgrim 1972), in contrast to other mecopteran pupae, especially males. The color is pale fawn in the early phase of pupation. The developing dark brown coloration is entirely due to the enclosed pharate adult. The pupal exuvia is completely colorless when shed. The antennae are extended over the compound eyes to about midlength of the wings. The large mandibles with sharp edges are placed between the wing bases. The free wings extend to about abdominal segment III. The long legs bear a pair of minute recurved hooks on their apex. They are doubled up and partly held between the wings but extend further along the ventral side of the abdomen. Large setae, mostly inserted on small protuberances, are sparsely distributed on the head and all thoracic and abdominal segments. Few setae are also inserted on the pedicellus, on the distal ends of all tibiae and of the fore and midfemora, and also on the forewing base. These setae probably prevent the pupa from making extensive body contact with the moist surroundings. The hindlegs, which are mostly concealed between the wings and abdomen, lack the femoral seta and its tibial seta is short and sometimes absent. Spiracles are present on the prothorax and abdominal segments I–VII, similarly placed than those of the larvae. A metathoracic stigmatic scar is visible anterior to the hindwing base. Sexual dimorphism is visible in the terminal segment of the abdomen from an early stage of the pupation and even in pharate pupae in the prepupal phase (Fig. 1.5.1).

 67

1.5 Morphology of pupae (based on Pilgrim 1972) 

A

ts1 ts2

ts3 ant

abdsI

abdsII

fw

abdsIII

hw abdsIV

abdsV abdsIX abdsVI

abdsVIII abdsVII

B

spi

abdsIX abdsVIII

abdsVII

Fig. 1.5.1: Nannochorista philpotti, pupa. A, Male, lateral view; B, female, end of abdomen, lateral view. Abbreviations: abdsI-IX – abdominal segments, ant – antenna, fw – forewing, hw – hindwing, spi – spiracle, ts1/2/3 – pro-/meso-/metathorax. Scale bar: 1 mm. Redrawn from Pilgrim (1972).

The pupa is active when disturbed, especially toward the end of the pupal period due to movements of the pharate adult. Spontaneous, vigorous wriggling occurs more and more frequently, finally leading to rupture of the pupal exuviae and to emergence. The exuvia is split from the Y-shaped cephalic frontal and coronal ecdysial sutures

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to the end of the metathorax, along the midline from the posterior head capsule to the posterior end.

1.6 References Beutel, R.G. & Baum, E. (2008): A longstanding entomological problem finally solved? Head morphology of Nannochorista (Mecoptera, Insecta) and possible phylogenetic implications. Journal of Zoological Systematics and Evolutionary Research 46(4): 346–367. Beutel, R.G., Friedrich, F., Hörnschemeyer, T., Pohl, H., Hünefeld, F., Beckmann, F., Meier, R., Misof, B., Whiting, M.F. & Vilhelmsen, L. (2011): Morphological and molecular evidence converging upon a robust phylogeny of the megadiverse Holometabola. Cladistics 27(4): 341–355. Beutel, R.G., Kristensen, N.P. & Pohl, H. (2009): Resolving insect phylogeny: the significance of cephalic structures of the Nannomecoptera in understanding endopterygote relationships. Arthropod Structure and Development 38(5): 427–460. Biliński, S.M. (1998): Introductory remarks. Folia Histochemica et Cytobiologica 36(4): 143–145. Biliński, S.M. & Büning, J. (1998): Structure of ovaries and oogenesis in the snow scorpionfly Boreus hyemalis (Linne) (Mecoptera: Boreidae). International Journal of Insect Morphology and Embryology 27(4): 333–340. Biliński, S.M., Büning, J. & Simiczyjew, B. (1998): The ovaries of Mecoptera: basic similarities and one exception to the rule. Folia Histochemica et Cytobiologica 36(4): 189–195. Büning, J. (1994): The Insect Ovary. Ultrastructure. Previtellogenic Growth and Evolution. Chapman & Hall, London. Byers, G.W. (1963): The life history of Panorpa nuptialis (Mecoptera: Panorpidae). Annals of the Entomological Society of America 56(2): 142–149. Byers, G.W. (1974): New generic names for Mecoptera of Australia and New Zealand. Journal of the Australian Entomological Society 13(2): 165–167. Byers, G.W. (1987): Order Mecoptera. In: Stehr, F.W. (ed.) Immature Insects, Vol. I. Kendall/Hunt Publishing Company, Dubuque, Iowa: 246–252. Byers, G.W. (1989): The Nannochoristidae of South America (Mecoptera). The University of Kansas Science Bulletin 54(2): 25–34. Byers, G.W. (1991): Mecoptera (Scorpion-flies, hanging flies). In: CSIRO (ed.) The Insects of Australia, Vol. 2. Melbourne University Press, Carlton, Victoria: 696–704. Clements, A.R., Suter, P.J., Fussell, M.S. & Silvester, E. (2016): Macroinvertebrate communities in spring-fed alpine source pools. Hydrobiologia 777(1): 119–138. Crampton, G.C. (1931): A phylogenetic study of the posterior metathoracic and basal abdominal structures of insects, with particular reference to the Holometabola. Journal of the New York Entomological Society 39(3): 323–357. Denis, J.R. & Bitsch, J. (1973): Morphologie de la tête des insectes. In: Grassé, P.P. (ed.) Traité de Zoologie, Vol. VIII (1). Masson et Cie, Paris: 1–593.

Engel, M.S. & Kristensen, N.P. (2013): A history of entomological classification. Annual Review of Entomology 58(1): 585–607. Evans, J.W. (1942): The morphology of Nannochorista maculipennis Tillyard (Mecoptera). Transactions of the Royal Society of South Australia 66(2): 218–225. Fabian, B., Russell, L., Friedrich, F. & Beutel, R.G. (2015): The morphology of the larval head of the enigmatic boreid Caurinus dectes (Mecoptera). Arthropod Systematics and Phylogeny 73(3): 385–399. Ferrington, L.C., Jr. (2008): Global biodiversity of Scorpionflies and Hangingflies (Mecoptera) in freshwater. Hydrobiologia 595(1): 443–445. Ferris, G.F. & Rees, B.E. (1939): The morphology of Panorpa nuptialis Gerstaecker (Mecoptera: Panorpidae). Microentomology 4: 79–108. Fraulob, M., Wipfler, B., Hünefeld, F., Pohl, H. & Beutel, R.G. (2012): The larval abdomen of the enigmatic Nannochoristidae (Mecoptera, Insecta). Arthropod Structure & Development 41(2): 187–198. Friedrich, F. & Beutel, R.G. (2010): The thoracic morphology of Nannochorista (Nannochoristidae) and its implications for the phylogeny of Mecoptera and Antliophora. Journal of Zoological Systematics and Evolutionary Research 48(1): 50–74. Friedrich, F., Pohl, H., Beckmann, F. & Beutel, R.G. (2013): The head of Merope tuber (Meropeidae) and the phylogeny of Mecoptera (Hexapoda). Arthropod Structure & Development 42(1): 69–88. Grell, K.G. (1942): Der Genitalapparat von Panorpa communis L. Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 67: 513–588. Grimaldi, D.A. & Engel, M.S. (2005): Evolution of the Insects. Cambridge University Press, Cambridge. 755 pp. Hasenfuss, I. & Kristensen, N.P. (2003): Skeleton and muscles: Immatures. In: Kristensen, N.P. (ed.) Lepidoptera, Moths and Butterflies. Vol. 2: Morphology, Physiology, and Development. Handbook of Zoology. IV Insecta. Vol. 36. Walter de Gruyter, Berlin, New York: 133–164. Hinton, H.E. (1958): The phylogeny of the panorpoid Orders. Annual Review of Entomology 3: 181–206. Hinton, H.E. (1981): Biology of Insect Eggs. Vol. II. Pergamon Press, Oxford, New York, Toronto, Sydney Paris, Frankfurt. 778 pp. Honomichl, K. (2008): Muskelrezeptoren an der Mandibel der Insekten. Entomologia Generalis 31(2): 173–191. Hünefeld, F. & Beutel, R.G. (2012): The female postabdomen of the enigmatic Nannochoristidae (Insecta: Mecopterida) and its phylogenetic significance. Acta Zoologica 93(2): 231–238. Hünefeld, F., Mißbach, C. & Beutel, R.G. (2012): The morphology and evolution of the female postabdomen of Holometabola (Insecta). Arthropod Structure and Development 41(4): 361–371. Kaltenbach, A. (1978): Mecoptera (Schnabelhafte, Schnabelfliegen). In: Helmcke J.-G., Starck, D. & Wermuth, G. (eds.) Handbuch der Zoologie IV Arthropoda. Insecta. Inst. 25. De Gruyter, Berlin, New York: 1–111. Kluge, N.J. (2003): Larval leg structure of Nannochorista Tillyard, 1917 and characteristics of Mecoptera. Russian Entomological Journal 12(4): 1–6.

1.6 References 

Kristensen, N.P. (1989): The New Zealand scorpionfly (Nannochorista philpotti comb. n.): wing morphology and its phylogenetic significance. Journal of Zoological Systematics and Evolutionary Research 27(2): 106–114. Kristensen, N.P. (1989): The New Zealand scorpionfly (Nannochorista philpotti comb. n.): wing morphology and its phylogenetic significance. Zeitschrift für zoologische Systematik und Evolutionsforschung 27(2): 106–114. Matsuda, R. (1970): Morphology and evolution of the insect thorax. Memoirs of the Entomological Society of Canada 76:1–431. Melzer, R.R., Paulus, H.F. & Kristensen, N.P. (1994): The larval eye of nannochoristid scorpionflies (Insecta, Mecoptera). Acta Zoologica 75(3): 201–208. Mickoleit, G. (1971): Das Exoskelet von Notiothauma reedi MacLachlan, ein Beitrag zur Morphologie und Phylogenie der Mecoptera (Insecta). Zeitschrift für Morphologie der Tiere 69(4): 318–362. Mickoleit, G. (1975): Die Genital-und Postgenitalsegmente der Mecoptera-Weibchen (Insecta, Holometabola). I. Das Exoskelet. Zeitschrift für Morphologie der Tiere 80(2): 97–135. Mickoleit, G. (1976): The genital and postgenital segments of the Mecoptera females (Insecta, Holometabola). Zoomorphology 85(2): 133–156. Mickoleit, G. (2008): Die Sperma-Auspreßvorrichtung der Nannochoristidae (Insecta: Mecoptera). Entomologia Generalis 31(2): 193–226. Misof, B., Liu, Sh., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A.J., Aspöck, U., Aspöck, H., Bartel, D., Blanke, A., Berger, S., Böhm, A., Buckley, T., Calcott, B., Chen, J. Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, G., Gu, Sh., Huang, Y., Jermiin, L.S., Kawahara, A.Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y., Li, Zh., Li, J., Lu, H., Machida, R., Mashimo, Y., Kapli, P., McKenna, D.D., Meng, G., Nakagaki, Y., Navarrete-Heredia, J.L., Ott, M., Ou, Y., Pass, G., Podsiadlowski, L., Pohl, H., von Reumont, B.M., Schütte, K., Sekiya, K., Shimizu, Sh., Slipinski, A., Stamatakis, A., Song, W., Su, X., Szucsich, N.U., Tan, M., Tan, X., Tang, M., Tang, J., Timelthaler, G., Tomizuka, Sh., Trautwein, M., Tong, X., Uchifune, T., Walzl, M.G., Wiegmann, B.M., Wilbrandt, J., Wipfler, B., Wong, T.K.F., Wu, Q., Wu, G., Xie, Y., Yang, Sh., Yang, Q., Yeates, D.K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W., Zhang, Y., Zhao, J., Zhou, Ch., Zhou, L., Ziesmann, T., Zou, Sh., Li, Y., Xu, X., Zhang, Y., Yang, H., Wang, J., Wang, J., Kjer, K.M. & Zhou, X. (2014): Phylogenomics resolves the timing and pattern of insect evolution. Science 346: 763–767. Noirot, C. & Quennedey, A. (1974): Fine structure of insect epidermal glands. Annual Review of Entomology 19(1): 61–80. Pilgrim, R.L.C. (1962): The late larva and pupa of Choristella philpotti Tillyard, 1917 (Mecoptera: Nannochoristidae). Proceedings of the Entomological Society of New Zealand, in New Zealand Entomologist 3(1): 2. Pilgrim, R.L.C. (1972): The aquatic larva and the pupa of Choristella philpotti Tillyard, 1917 (Mecoptera: Nannochoristidae). Pacific Insects 14(1): 151–168.

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Riek, E.F. (1970a): Mecoptera. In: CSIRO (ed.) The Insects of Australia. Melbourne University Press, Melbourne: 636–646. Riek, E.F. (1970b): Endemism in the Australian insect fauna. Proceedings of the Royal Entomological Society of London 39(5): 17. Russell, L.K. (1979): A study of the armored boreid Caurinus dectes (Mecoptera). Unpublished PhD thesis, Oregon State University. Russell, L.K. (1982): The life history of Caurinus dectes Russell, with a description of the immature stages (Mecoptera: Boreidae). Entomologica Scandinavica 13(2): 225–235. Setty, L.R. (1940): Biology and morphology of some North American Bittacidae (Order Mecoptera). American Midland Naturalist 23(2): 257–353. Simiczyjew, B. & Margas W. (2001): Ovary structure in the bat flea Ischnopsyllus spp. (Siphonaptera: Ischnopsyllidae). Phylogenetic implications. Zoologica Poloniae 46: 5–14. Simiczyjew, B. (2002): Structure of the ovary in Nannochorista neotropica Navás (Insecta: Mecoptera: Nannochoristidae) with remarks on mecopteran phylogeny. Acta Zoologica 83(1): 61–66. Simiczyjew, B. (2005): Ovary structure, oogenesis and phylogeny of Mecoptera. Zoologica Poloniae 50: 5–52. Štys, P. & Biliński S. (1990): Ovariole types and the phylogeny of hexapods. Biological Reviews 65(4): 401–429. Tillyard, R.J. (1917): Studies in Australian Mecoptera. No 1. The new family Nannochoristidae, with descriptions of a new genus and four new species: and an appendix descriptive of a new genus and species from New Zealand. Proceedings of the Linnean Society of New South Wales 42: 284–301, 2 pls. von Kéler, S. (1963): Entomologisches Wörterbuch mit besonderer Berücksichtigung der morphologischen Terminologie, 3rd ed. Akademie-Verlag, Berlin. 774 pp. Whiting, M.F. (2002): Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31(1): 93–104. Wigglesworth, V.B. (1950): The Principles of Insect Physiology. 4th ed. Methuen, London. 544 pp. Williams, W.D. (1968): Australian Freshwater Life. Sun Books, Melbourne. x + 262 pp. Willmann, R. (1981a): Das Exoskelett der männlichen Genitalien der Mecoptera (Insecta). I. Morphologie. Zeitschrift für zoologische Systematik und Evolutionsforschung 19(2): 96–150. Willmann, R. (1981b): Das Exoskelett der männlichen Genitalien der Mecoptera (Insecta). II. Die phylogenetischen Beziehungen der Schnabelfliegen-Familien. Zeitschrift für zoologische Systematik und Evolutionsforschung 19(3): 153–174. Willmann, R. (1987): The phylogenetic system of Mecoptera. Systematic Entomology 12(4): 519–524. Willmann, R. (1989): Evolution und phylogenetisches System der Mecoptera (Insecta: Holometabola). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 544: 1–153. Winterbourn, M.J. (1976): Fluxes of litter falling in a small beech forest stream. New Zealand Journal of Marine and Freshwater Research 10(3): 399–416. Winterbourn, M.J. (1982): The invertebrate fauna of a forest stream and its association with fine particulate matter. New Zealand Journal of Marine and Freshwater Research 16(3–4): 271–281.

2 Neomecoptera, Boreidae, Caurininae, Caurinus Loren K. Russell & Rolf G. Beutel

2.1 Taxonomy and distribution The genus Caurinus presently comprises two species, Caurinus dectes Russell 1979b and Caurinus tlagu Sikes & Stockbridge 2013, both distributed in northwestern North America. The status of C. tlagu as a separate species was confirmed by differences in external morphological features and sequences of the mitochondrial gene cytochrome oxidase II (Sikes & Stockbridge 2013). The number of ommatidia in males of C. tlagu is lower than in its congener (31–35 versus 38–39, n = 3), and sternum VIII of females lacks a deep notch or only a shallow concavity is present (shallow or pronounced in C. dectes). Caurinus dectes often cooccurs with Hesperoboreus brevicaudatus. It is known from 57 localities in Washington and Oregon (see Russell 1979b: map 1, table 4; Rood et al. 2015). The type locality in Oregon became known as the “funny bug notch” (Rood et al. 2015). It is likely that the species also occurs in north coastal California, but eggshell remains and feeding damage on liverworts growing on redwood logs did not allow definite association with Caurinus. In Oregon, most sites are near the coast. Caurinus populations are numerous and probably continuously distributed near the central and north coast, fragmented and restricted to moist sites at moderate elevations in the eastern Coast Range, and rare if occurring at all in the Cascades and the southern Coast Range. In Washington, Caurinus dectes was collected in the coastal forest zone on the west and northwest sides of the Olympic Peninsula and southwest of Mount Rainier National Park in the Nisqually and Chehalis River drainage. In Oregon, the species occurs from sea level to about 650 m at Mary’s Peak. At distances of more than 20 km inland, most populations occur above 150 m, while the lower elevational limit at Mary’s Peak is about 500 m. Rood et al. (2015) extended the range of C. dectes in both states, with new county records in both of them. The most important macroclimatic factor determining the range limit of Caurinus dectes and other coastally distributed invertebrates and cryptogams is probably the availability of moisture during the summer drought. Near the coast, total evaporation is reduced and moisture is increased by fog capture along ridgelines. Caurinus adults can survive in epiphytes exposed to continuous

https://doi.org/10.1515/9783110272543-002

freezing temperatures for several days. The generally mild temperatures near the coast (January mean minimum 0°C–+2.5°C) increase the scope for activity on the exposed host plants. The comparatively mild temperatures in early spring are likely favorable for the completion of larval feeding prior to seasonal drying of suitable substrates. C. tlagu was discovered on Prince of Wales Island in the Alexander Archipelago, Alaska. It was collected at 16 sites close to the northern end of the island (Sikes & Stockbridge 2013: fig. 1). Most specimens were collected in alpine perhumid rainforest dominated by Sitka spruce (Picea sitchensis), Western hemlock (Tsuga heterophylla), lodgepole pine (Pinus contorta var. contorta), Alaska yellow cedar (Chamaecyparis nootkatensis), red cedar (Thuja plicata), and red alder (Alnus rubra) (Sikes & Stockbridge 2013: fig. 2). Specimens were more or less evenly collected from mid-May to mid-August (Sikes & Stockbridge 2013: table 1).

Loren K. Russel

2.2 Biology 2.2.1 Climatic factors Caurinus dectes is univoltine, as confirmed by rearing and by the regular succession of larvae, pupae, and adults through the year (Russell 1979a, b, 1982). It thus differs from boreines, all of which appear to spend 2 years as larvae. The life cycle is less well known for C. tlagu and for the undescribed British Columbia populations. While Sikes and Stockbridge (2013) suggested that C. tlagu has a primarily summer-active life cycle, his field data extended only from May through August. Based on the collection of nearly mature C. tlagu larvae in May, as well as the preponderance of teneral adults in early September in the British Columbia populations (L. K. Russell, personal observation), it seems likely that all Caurinus share a common life history pattern: larval development through late winter and spring, pupation in late summer, and emergence of long-lived adults in autumn. The adults remain active in cool or cold weather, which extends through the spring and summer in coastal Alaska. All Caurinus then share with boreines a pattern of adult emergence in autumn, with both adults and larvae feeding through the

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winter and early spring, and pupation occurring in early summer. It appears that the upper thermal tolerance is higher in Caurinus than in most or all boreines. Adults and larvae of C. dectes were maintained for over 60 days at 17–20°C, while C. tlagu adults and larvae survived in bulk bryophyte samples for 48 hours stored in a room with temperatures near 28°C. Caurinus differ from Boreus in completing their life cycle in 1 year. Therefore, no larval estivation takes place.

2.2.2 Feeding Caurinus adults and larvae are both specialized to feed on liverwort gametophytes, utilizing different liverworts over a range of habitats and seral stages in the coastal rain forest. Hosts include a number of species of leafy liverworts (Jungermanniales in the broad sense, including the order Porellales). Some “simple thalloid” liverworts (e.g. Pelliales and Metzgeriales) may also be fed on by adult Caurinus when preferred hosts are not available. Adult Caurinus feed on the unistratose (one cell layer) liverwort “leaves” and occasionally on the tissues of the central axis (“stem”). The larvae are internal feeders, primarily mining the central axis of the liverwort, but in later instars also incorporating leaf tissues into their closed galleries.

2.2.2.1 Adult feeding behavior The following account is typical for adult Caurinus feeding on either of the two predominant (but very distantly related) hosts: Porella navicularis (Porellaceae) and Scapania navicularis (Scapaniaceae). Both liverworts are confirmed hosts for all studied populations of Caurinus. They are both relatively large, with dorsal leaves about 2–2.5 mm × 1.5 mm, and are extremely abundant throughout the range of Caurinus. When introduced to either liverwort, adult Caurinus explore the surface of the liverwort with antennae and maxillary palps before selecting a feeding site on a leaf near the growth apex. Feeding is initiated with the insect in a head-down position with the mandibles abducted. The Caurinus first thrusts its head from side to side until the mandibular apical teeth achieve a puncture or laceration of the leaf. The laceration is enlarged further with the teeth of both mandibles, until the Caurinus pushes forward into the incision and begins to macerate the leaf

tissue using the scissor-like mandibular molae. Rhythmic mastication usually continues for 5 to 20 minutes, interrupted by occasional lateral thrusts of the apical mandibular teeth. In wet conditions, clear droplets of water are expressed from the anus during feeding. In most cases, feeding proceeds until half or more of the leaf is consumed, often leaving intact leaf margins. Over several hours, a single Caurinus may feed on several leaves on a shoot. The resulting damage, with linear or arcuate incisions in the leaves and particularly the presence of abundant white cell wall debris and intact leaf margins, is distinctive and has been useful for locating new populations of Caurinus in the field. Russell (1979b) noted frequent grooming of the antennae, eyes, rostrum, and legs and less frequently of the abdomen. Aside from wet individuals (the consequence of extraction by means of wet screening), most grooming followed feeding. Antennal grooming sometimes resembled that common among the mecopteroid orders, pulling an antenna between the front tarsi. Generally, grooming consisted of simple, repeated, wiping with one tarsus or tarsus and tibia.

2.2.2.2 Larval feeding behavior Larvae are able to creep over liverwort surfaces, using their thoracic pedal lobes and their pygopod for attachment as they climb from one leaf to another. Shortly after hatching, the first-instar larva initiates a feeding gallery in the central axis of a liverwort (robust liverworts, like Scapania bolanderi and Porella navicularis) or (in Calypogeia fissa and other smaller liverworts) it constructs a gallery from fragments of several adjacent shoots. The feeding pattern varies in detail for different hosts, in response to host growth form. This gallery is gradually extended to 3 to 5 mm and is kept open at one or both ends. Feeding debris (comprising coarse cell wall debris and feces) is pushed out these openings and may be used to seal them. The first and second larval molts occur inside the gallery and the exuviae are pushed out one of the openings. By the end of the second instar, a larva will either extend its gallery basad on the liverwort into older growth or may abscond to the apical growth of another shoot and begin to construct a new gallery. Mature larvae leave their feeding galleries to construct pupal cells. Depending on the architecture of the liverworts, cells are constructed among shoots (in cushion-forming hosts, e.g. Gyrothrya underwoodiana),

2.2 Biology 

directly under the bryophyte mat (e.g. epiphytes like Porella navicularis), within rotted wood (frequent for Scapania navicularis) or in soil, where these are in contact with the host. A parchment-like silk cocoon is constructed in the pupal cell. The pupal and adult molts occur within the pupal cell in late summer and early autumn (Russell 1982: fig. 11).

2.2.3 Host relations and ecology Porella navicularis and Scapania bolanderi have been identified as the most important hosts of Caurinus, but some populations have been found where neither of these liverworts is common or present at all. In a survey by Russell (1982), 46 species of liverworts, which included 38 species of Jungermanniales (s.l.), were collected at Caurinus sites in Oregon and Washington. These include most of the liverwort species occurring in lower-elevation forests within the range of C. dectes. Feeding trials, 44 species of liverworts presented to adults and 13 species to the larvae of C. dectes, as well as field associations, are summarized in Tabs. 2.2.3.1, 2.2.3.2, 2.2.3.3 and 2.2.3.4.1 The trials showed that both adults and larvae readily accept alternative hosts, even in the presence of the one they were collected from. Thirteen liverworts (all Jungermanniales s.l.) were identified as “highly accepted” hosts, while another 18 species, including several species of Metzgeriales, were accepted under deprivation in the study. Taken together, the “highly accepted” liverworts are present in most seral stages and habitat types in lowland forests within the range of C. dectes. Porella navicularis is an extremely abundant epiphyte on deciduous trees and shrubs, including Alnus rubra, dominant in many secondary forests and Acer circinatum, common along streams and coniferous understory. Scapania bolanderi is very common as an epiphyte on large conifers and on stumps and logs. It may persist on the latter for decades but is usually replaced by an assemblage including Calypogeia spp., which tolerate shade. Finally, a number of mat-forming liverworts, including Gyrothyra underwoodiana, Nardia scalaris, and Diplophyllum spp., are found on shaded soil, often along roads and trails but also at the base of windthrown trees and along game trails. Caurinus dectes is

1  Liverwort taxonomy is updated following Stotler & CrandallStotler (2017) (see also Söderström et al. 2016).

 73

rarely found in very dense, dry shade in dense secondary forest, where liverworts are scarce. Sikes and Stockbridge (2013) found that C. tlagu also “is not a habitat specialist“ like C. dectes but occurs in all seral stages from clear-cut to secondary and primary forest. The northern Caurinus (C. tlagu and the Vancouver Island population) occupy the range of forest associations described for C. dectes, but they also occur in open habitats and at higher elevations. Sikes found C. tlagu at a 917-m elevation in tundra-alpine-heath vegetation, dominated by Harrimanella stelleriana, Luetkea pectinata, and Rhytidiadelphus loreus, and also in sea-level “muskeg,” a subarctic hydric community with Sphagnum hummocks and isolated shore pines (P. contorta). The Vancouver Island form has been found from sea level to the subalpine, where it occurs both in open heath and in wet meadows above 1000 m. Leafy liverworts are diverse and abundant in these alpine and subarctic habitats. Since few of the common coastal forest species are present, it is likely that there are additional host species in these associations.

2.2.4 Host phytochemicals Liverworts are notable for the presence and diversity of isoprenoid (also referred to as “terpenoid”) essential oils, sequestered in intracellular oil bodies surrounded by a single membrane (Asakawa et al. 2013). The oil bodies are unique to the Marchantiophyta and are present in almost all contemporary species. Labandeira et al. (2014) reported the presence of both oil bodies and several arthropodan herbivore damage types (both external foliage-feeding and gall-forming) in the Middle Devonian (388 mya) liverwort Metzgeriothallus sharonae. The authors suggest that “oil body cells, similar to the terpenoid-containing oil bodies of liverworts, were probably involved in the chemical defense of M. sharonae against arthropod herbivores.” The Devonian herbivores were not identified but very likely included Acari and probably Collembola or other entognathous hexapods. There is tremendous diversity of the oil body terpenoids even within genera, which may account for the odd pattern of host preferences in C. dectes (Tab. 2.2.3.4), where widely divergent genera (e.g. Scapania and Porella) contain equally highly accepted and also unacceptable species (Bungert et al. 1998, Heinrichs et al. 2007). Little is known of present-day arthropodan herbivory of liverworts. In the Pacific Northwest, collembolans and

74 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

Acari (especially stigmaeids, penthaleids, and oribatids) are regularly associated with, and likely to feed on, liverworts. Among pterygote insects, aside from Caurinus, a wide range of leafy liverworts are fed on by larvae of the

chironomid genus Cricotopus. Larvae of the micropterygid Epimartyria pardella usually feed on the large thalloid liverwort Conocephalum conicum but may also feed on several genera of Jungermanniales.

Tab. 2.2.3.1: Summary of liverworts in feeding studies (Caurinus dectes adults and larvae, 1978–1979). Predominant host group in bold. Liverwort taxa Sphaerocarpales Marchantiales Metzgeriales Jungermanniales (incl. Porellales) Anthocerotae Total

# Genera in Oregon

# Genera in study

Percent

1 11 7 29

0 2 4 20

0% 18% 57% 69%

2 49

1 27

50%

#Species in Oregon

#Species in study

Percent

1 17 15 ca.75

0 2 5 34

0% 12% 33% 45%

? ca.110

1 42

– 38%

Tab. 2.2.3.2: Liverworts associated with Caurinus dectes in the field. Liverwort species

Location

Bazzania ambigua B. tricrenata Calyptogeja neogaea Lophocolea heterophylla Plagiochila porelloides Gyrothyra underwoodiana Schistochilopsis incisa Nardia scalaris Diplophyllum albicans D. obtusifolium Scapania umbrosa S. bolanderi Porella navicularis

WA WA OR WA OR OR WA OR OR OR OR OR,WA OR,WA

Adults present, feeding damage

Larvae in situ or larval galleries

+ + + + +

Eggs attached to liverwort + +

+

+

+ + + + + +

+ +

+ + + +

+ +

+ +

Larvae or larval galleries

Eggs attached to liverwort

Tab. 2.2.3.3: Liverworts associated with Caurinus tlagu in the field (L. Russell, unpublished data) Liverwort species

Location

Calypogeia cf. neogaea Scapania bolanderi Porella navicularis

AK AK AK

Adults or adult feeding damage + + +

+

+

Tab. 2.2.3.4: Status of liverworts as hosts for Caurinus dectes, inferred from field observations and from adult and larval feeding trialsa Habitat group

Highly accepted hostsb

Possible secondary hostsc

Not acceptedd

Epiphytic on deciduous trees, shrubs

Porella navicularis

Frullania nisquallensis

Scapania bolanderi Bazzania tricrenata

Ptilidium californicum Bazzania ambigua Lophocolea cuspidata

Radula bolanderi Metzgeria conjugatae Lepidozia reptans Porella roellii

Epiphytic on conifer bark, including recently cut stumps

2.3 Morphology of adults 



 75

Tab. 2.2.3.4 (continued) Habitat group

Highly accepted hostsb

Possible secondary hostsc

Not acceptedd

Decaying conifer logs and stumps, mostly decorticated

Calyptogeia neogaea C. muelleriana C. [cf. azurea?] Scapania bolanderi S. umbrosa Lophocolea heterophylla

Cephalozia lunulifolia Blepharostoma trichophyllum Chiloscyphus pallescens Lepidozia reptans

Terrestrial, on compacted soil

Gyrothyra underwoodiana Nardia scalaris Diplophyllum albicans D. obtusifolium Plagiochila porelloides

Geocalyx graveolens Schistochilopsis incisa Cephalozia bicuspidata C. lunulifolia Syzygiella autumnalis Jungermannia atrovirens Riccardia latifronse Solenostoma rubrum Blasia pusillae

Terrestrial, on loose soil, litter Semiaquatic, in seeps, stream edge

Porella cordeana Scapania americana Chiloscyphus polyanthos Riccardia multifidae Blasia pusillae

Pellia neesianae Clevea hyalinae Conocephalum salebrosume Anthoceros punctatuse Porella roellii Scapania undulata Anthoceros punctatuse

a Data from Russell (1979b); liverwort nomenclature follows Stotler & Crandall-Stotler (2017) (see also Söderström et al. 2016). b “Highly accepted” = feeds freely in the presence of P. navicularis or S. bolanderi. c “Possible secondary hosts” = limited acceptance, only under deprivation. d “Not accepted” = no feeding, even under deprivation. e “Thalloid” liverworts, these are not in Jungermanniales.

2.2.5 Parasites and predation No parasites of Caurinus adults or larvae have been observed, although a single isolated abdomen of a female C. dectes was recovered with a dipteran puparium inside it. In the absence of further evidence, it is likely that the dipteran was a scavenger. Predation has not been observed, but Caurinus adults and larvae exist in very predator-rich substrates, with a wide range of spiders and other arachnids, centipedes and staphylinoid larvae particularly common. The population curve of Caurinus larvae suggests significant mortality, likely from predation, while the high survival of the adults suggests that they are largely immune from predation.

2.2.6 Locomotion Caurinus adults are active, and their relatively short legs allow agile movement over the host plants. They are also capable of dispersing a significance distance from their host plants, as shown by their relative abundance in pitfall trap surveys in Alaska (Sikes & Stockbridge 2013) and in British Columbia (D. Blades, personal communication). In Oregon, C. dectes usually leave exposed epiphytes during very cold (below 0°C) or very warm, dry periods – presumably

by dropping to the forest floor. When mild, moist weather returns, they soon return to the epiphytes, often covering a distance of 5 m or more within 2 or 3 days. Unlike Boreus and Hesperoboreus, Caurinus are rarely active on the surface of snow. Like boreines, Caurinus are able to hop when disturbed but do not jump during normal locomotion. The disturbance hop typically covers a horizontal distance of 50 to 60 mm (e.g. about 25 body lengths). Upon landing, the Caurinus pull in their appendages and remain still for some time. The disturbance hop is presumed to involve resilin pads in the pleura, as in boreines (Burrows 2011).

2.3 Morphology of adults The small and sexually dimorphic adults (size ca. 1.5–2.5 mm) are strongly sclerotized; the body has a brown coloration and a sparse pubescence of short setae (Fig. 2.3.1; Sikes & Stockbridge 2013: figs. 5 and 6). The forewings are transformed into curved claspers in males and only pad-like vestiges are present in females; the hindwings are missing in both sexes. An elongated rostrum of the head is missing. The thorax and abdominal segments I–VI form a compact functional and structural unit. The entire abdomen appears roundish in dorsal view. The legs

76 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

A

B

ant

fem2

ant

abdsI cpe

fw

fw

dps

nt1

nt3

nt2

nt3

nt2 abdsIV

abdsI

C

fw

nt3

abdsVII

nt3

D

nt1

fw

abdsIV

tgVIII

vps hypa

abdsI

nt2 nt1

stVIII

mxp

tr3 cx3

mxp

fem3 tib3

Fig. 2.3.1: Caurinus dectes, adults, SEM. A, C, Female; B, D, male; A, B dorsal view; C, D, lateral view. Abbreviations: abdsI/IV/VII – abdominal segment I/IV/VII, ant – antenna, cpe – compound eye, cx3 – metacoxa, dps – dorsal penis sclerite, fem2/3 – meso-/metafemur, fw – forewing, hypa – hypandrium, mxp – maxillary palp, nt1/2/3 – pro-/meso-/metanotum, stVIII – abdominal sternum VIII, tgVIII – abdominal tergum VIII, tib3 – metatibia, tr3 – metatrochanter, vps – ventral penis sclerite. Scale bars: 200 µm.

are elongate and slender; the jumping hind legs are longer than the other two pairs. Frank Friedrich & Rolf G. Beutel

2.3.1 Head (mainly based on Beutel et al. 2008) 2.3.1.1 Head capsule (Figs. 2.3.1.1, 2.3.1.2 A,B, and 2.3.1.3) The head is orthognathous. The posterior region is not exposed. A narrow occipital collar shaped like a very shallow triangle overlaps the anterior margin of the narrow pronotum. The largest part of the posterior side of the head fits tightly with the flattened anterior side of the procoxae. The foramen occipitale is narrow and keyhole-shaped (Fig. 2.3.1.1); its ventral margin is reinforced by a low internal ridge. The head capsule is well sclerotized and light brown

except for the nearly black eyes. A regularly arranged vestiture of medium-length setae is present on the anterior side, whereas the shiny posterior side is smooth; a pair of longer setae is inserted on the clypeus, close to its dorsal margin (see arrows in Fig. 2.3.1.2 B). In frontal view, the head capsule is about as broad as long. The maximum width (between external margins of compound eyes) is slightly less than 0.6 mm. The frontal side is distinctly convex. The well-developed compound eyes are strongly convex and multifaceted, slightly emarginated mesad the antennal bases, and internally enclosed by a high circumocular ridge (Fig. 2.3.1.3 A,B). Ocelli are lacking (Figs. 2.3.1.2 A and 2.3.1.3 A). The coronal and fontal sutures (=epicranial suture) are absent; a fairly low dorsolateral ridge is present between the antennal socket and the mesal margin of the eyes (Fig. 2.3.1.2 A). The transverse, trapezoid clypeus is very distinctly divided into a smooth and even anterior anteclypeus and a slightly convex and uneven postclypeus. The clypeolabral suture and the transverse intraclypeal

2.3 Morphology of adults 



A

afo

ext

tb cpe nfo ped

pgeb ori mxpl mxl

pmt

lap

mxp

ga

md

B cpe

foc

Fig. 2.3.1.1: Caurinus dectes, head of adult. A, Posterior view; B, posterodorsal view, with foramen occipitale. Abbreviations: afo – alaforamen, cpe – compound eye, ext – extrinsic head muscles, foc – foramen occipitale, ga – galea, lap – labial palp, md – mandible, mxl – maxillary lobe, mxp – maxillary palp, mxpl – maxillolabial plate, nfo – neuroforamen, ori – oblique ridge, ped – pedicellus, pgeb – postgenal bridge, pmt – prementum, tb – tentorial bridge. Scale bars: 100 µm. Reprinted from Beutel et al. (2008) with permission from Elsevier.

line are slightly curved, whereas the frontoclypeal transverse strengthening ridge is externally represented by an almost straight, deep furrow, which reaches the lateral margin of the head capsule (Fig. 2.3.1.2 A). The anterior tentorial grooves are distinctly curved fissures posterad the long

 77

postclypeal setae; a narrow, curved fissure with unknown homology is present between their posterior margin and the lateral margin of the head (Fig. 2.3.1.2 B). An elongated rostrum is not developed; the genal region between the secondary mandibular articulation and the ventral margin of the eye is not distinctly elongated. A postgenal bridge is present (Figs. 2.3.1.1 A and 2.3.1.2 C); it is possibly fused with the submental region. The sclerotized area dorsad the fossa containing the maxillolabial complex is about half as long as the elongate foramen occipitale. The posterior tentorial grooves are not recognizable externally. Sharp and high longitudinal ridges are present posterolaterally, connecting a triangular genal projection with a semicircular ridge above the foramen occipitale; a shorter ridge laterad the upper part of the foramen joins the semicircular ridge dorsally (Fig. 2.3.1.1).

2.3.1.2 Tentorium (Figs. 2.3.1.1 A, 2.3.1.2 A, 2.3.1.3, 2.3.1.4 C,D, and 2.3.1.5 D–F) The main part of the tentorium is x-shaped (Fig. 2.3.1.4 C). The connecting elements between the posterior and anterior parts are very delicate and hardly visible in serial sections (Fig. 2.3.1.5 E,F). The tentorial bridge separates a small ventral part of the foramen occipitale (neuroforamen) from the much larger dorsal part (anteforamen) (Figs. 2.3.1.1 A and 2.3.1.3 D). It is continuous with fused corpora tentorii (Fig. 2.3.1.4 C), which form a plate-like structure. The following separate sections of the corpora tentorii are strongly flattened and weakly sclerotized. Dorsal arms are present but very thin (Figs. 2.3.1.3 A, 2.3.1.4 C,D, and 2.3.1.5 F). They are attached to the head capsule anteriorly, just dorsad the antennal sockets (Fig. 2.3.1.3 A). The anterior tentorial arms are strongly developed, massive structures. A mesally directed flat process below the precerebral pharyngeal pumping chamber serves as attachment area of extrinsic maxillary muscles and a very short pharyngeal muscle (Fig. 2.3.1.5 D).

2.3.1.3 Labrum (Figs. 2.3.1.2 B and 2.3.1.3 A) The distinctly flattened labrum is almost as long as the entire clypeus and separated from its anterior margin by a fold. Both parts are internally connected by a membrane. The rounded lateral edges diverge anteriorly but are covered by the maxillary lobes, when the maxillolabial complex is in its protracted position. The ventral edge is concave and irregular, appearing almost serrate. A few pairs of short setae are inserted on the upper surface of

78 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

pcl acl

cpe ped

ant

lbr

mxl sca atp

D

fcs

mxp

E

ga

md

B

B

mxp

mdf

md

C

A ped mxpl

ori

mxl

pmt sen

D

mxp

lap

mdf

E

C

Fig. 2.3.1.2: C. dectes, head of adult, SEM. A, Anterior view; B, clypeal and labral region, anterior view (postclypeal setae marked by arrows); C, mouthparts, posterior view; D, antenna, basal segments, posterior view; E, antenna, distal segments, anterior view. Abbreviations: acl – anteclypeus, ant – antenna, atp – anterior tentorial pit, cpe – compound eye, fcs – frontoclypeal suture, ga – galea, lap – labial palp, lbr – labrum, md – mandible, mdf – mandibular furrow, mxl – maxillary lobe, mxp – maxillary palp, mxpl – maxillolabial plate, ori – oblique ridge, pcl – postclypeus, ped – pedicellus, pmt – prementum, sca – scapus, sen – sensilla. Scale bars: 500 µm. Reprinted from Beutel et al. (2008) with permission from Elsevier.

the labrum; a row of 10 two-segmented sensilla is present close to the ventral margin and a row of short, fine setae ventrolaterally. Musculature: absent. 2.3.1.4 Antenna (Fig. 2.3.1.2 A,D,E) The antenna is composed of 16 segments with a vestiture of medium-length setae. They are inserted in large, widely

separated antennal sockets with a strongly pronounced antennal ring, between the mesal emarginations of the compound eye and the anterolateral ridge. The cylindrical scapus is about as wide as long. The pedicellus is the largest segment; its middle part is distinctly widened and it contains a well-developed Johnston’s organ. The first flagellomere is distinctly narrower than the apical part of the pedicellus, about twice as long as wide, and constricted in its middle section; an annular ridge is present



but very indistinct (Fig. 2.3.1.2 D). The following nine flagellomeres are widening apically but are distinctly smaller and decreasing in size toward the antennal apex. Antennomeres 14 and 15 are cylindrical and slightly longer than the preceding ones. The apical segment is conical and rounded apically. A pair of sensilla, composed of one sensillum coeloconicum and one sensillum basiconum, is present on the ventral side of the distal part of flagellomeres 1 and 2 (Fig. 2.3.1.2 D). Musculature (Figs. 2.3.1.3 A,B and 2.3.1.4 E): M. tentorioscapalis anterior (M. 1), origin (=O): with two bundles from the posterior and middle regions of the anterior tentorial arm (close to the dorsal arm), insertion (=I): ventrally on the scapal base; M. tentorioscapalis posterior (M. 2), O: middle region of the anterior tentorial arm (laterad second bundle of M. 1, posterad M. 3), I: dorsally on the scapal base; M. tentorioscapalis lateralis (M. 3), O: anterior tentorial arm, anterior to both other tentorio-antennal muscles; I: laterally on the inner surface of the scapus; M. scapopedicellaris lateralis (M. 5), O: ventral part of scapal base; I: ventrally on the base of the pedicellus; M. scapopedicellaris medialis (M. 6), O: mesal face of the scapal base; I: dorsally on the base of the pedicellus. A cranial muscle attached to the scapus is not present. 2.3.1.5 Mandible (Figs. 2.3.1.2 B,C, 2.3.1.3, and 2.3.1.5 A,B) The primary and secondary mandibular joints are welldeveloped. The mandibles are symmetrical and falciform. Large parts of them are exposed anterad and laterad the clypeus and labrum in the extended position, but the base is covered by the maxillary lobe and galea (see below) in the flexed position (Fig. 2.3.1.2 B). The elongate apical tooth is slender and acuminate. Two slender subapical teeth on the mesal side are slightly less pointed at their apex. Narrow furrows or canals on the anterior and posterior side are recognizable on the scanning electron microscopy (SEM) pictures and serial sections (Figs. 2.3.1.2 B,C and 2.3.1.5 A); the dorsal furrow splits into two branches distally. A prostheca is not developed. The basal part of the mandibles is distinctly extended, thus forming prominent molae with a tuberculate dorsal surface. The molar areas are separated in the extended position (Fig. 2.3.1.3 A) but interact with each other and probably with the epipharyngeal protrusion in the flexed position. Musculature (Figs. 2.3.1.3 and 2.3.1.5): M. craniomandibularis internus (M. 11), the largest muscle of the head, O: anterolateral, posterolateral and extensive dorsal areas of the head capsule (anterad and posterad the compound eyes), anterior part of the circumocular ridge, I: adductor tendon; M. craniomandibularis externus (M. 12),

2.3 Morphology of adults 

 79

O: posterolateral wall of the head capsule and posterodorsal part of the circumocular ridge, I: abductor tendon; M. hypopharyngomandibularis (M. 13), two parallel bundles, O: ventrolateral part of the prepharyngeal clasps (base of oral arms), I: anterior part of the basal mandibular rim; M. tentoriomandibularis (M. 14), very large, O: base of the anterior tentorial arm, I: inner surface of the posterior side of the mandibular base. 2.3.1.6 Maxillolabial complex (Figs. 2.3.1.1 A, 2.3.1.2 C, 2.3.1.3, and 2.3.1.5 A–D) The maxillae and the labium form a closely connected functional and morphological unit inserted in a deep semicircular emargination of the posterior head capsule. A distinct articulatory membrane is visible posterior to the maxillolabial complex, and a pair of short, closely adjacent processus is present at the posteromedian margin of the complex. The proximal parts of the maxilla and labium are fused and form a triangular glabrous, plate-like structure (maxillolabial plate; Figs. 2.3.1.1 A and 2.3.1.2 C). Cardines are not present as separate structures (Fig. 2.3.1.2 C). The basal maxillary region does likely include this element and the proximal stipes (Russell 1979a: zygostipes). The presumptive basal part of the stipes is firmly connected with the anterior postmentum, but both elements are separated by a short, indistinct oblique furrow corresponding with an internal ridge (maxillolabial ridge). The main distal element of the maxilla (maxillary lobe; Figs. 2.3.1.1 A and 2.3.1.2 B,C) is separated from the proximal part by an indistinct transverse line (Fig. 2.3.1.2 C). Its mesal margin is not connected with the prementum but bears the flat, unsclerotized lacinia; the lateral margin is strongly curved and bears a single, short seta. The inflected laterodistal part and a flat, membranous, setiferous lobe probably representing the galea enclose the lateral parts of the mandible and labrum (Fig. 2.3.1.2 B; see above). A short, fixed tooth is present apicomesally. The maxillary palp is inserted laterad the maxillary lobe. Its proximal segment is possibly represented by a very small semicircular sclerite at its lateral base. The first distinct palpomere is elongate and distinctly widened distally. The following shorter segment is widening distally and curved, with a distinctly longer lateral margin. Setae are inserted dorsally and laterally on both segments. The penultimate palpomere is large and club-shaped, with a shallow furrow on its posterior side. Approximately 20 medium-sized and longer setae are inserted on it and it bears the slender, conical terminal segment on its widened apex. Only few very short setae are present on the apical palpomere.

80 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

11

51a

51b

11 dta

cor

cpe

12 onp

sca

pcer

5 pcgl

6 3

nan tdm 46a nrec

3

46a 46b

17

2

19

41

atp

22

45b

fg

18

45a

14

43

lbr t11 ccc 11

43

t12

B

44

mxp

29

44

26

cly

A

1

md 51b

md ph

52

cpe

11

51a

12

52

ceao

tb

tb pcer

cten

nrec

29

tdm

soeg

pgeb

19 17

mxpl

18 mxl

22

soeg

pch

46a

17

41

22

45a,b fg

26

C

md

lap

18 37

44

34

mxp

34

29 sald

43a,b

D

lap md



The well-developed prementum is attached to the anterior margin of the prominent anteromedian part of the maxillolabial plate (Figs. 2.3.1.1 A and 2.3.1.2 C). It is slightly narrowed basally and the lateral margins are rounded. A strongly developed median apodeme is present at its posterior margin. A pair of long setae is inserted on the sclerotized main element of the prementum. The anterolateral articulation areas of the two-segmented labial palps are membranous. A distinct median sclerotization is present between them. The proximal palpomere is distinctly inflated. Its lateral margin is strongly rounded. One long seta is present on the ventral surface, one long seta distolaterally, and several setae along the slightly concave mesal margin. The distal palpomere is slender and conical, similar to the apical maxillary palpomere. Maxillary musculature (Figs. 2.3.1.3 and 2.3.1.5 B–D): M. craniocardinalis (M. 15), absent; M. tentoriocardinalis (M. 17), two slender bundles, O: mesally directed process of the anterior tentorial arm, I: cardinal region of the maxillolabial plate, close to the median line (dorsad M. 22); M. tentoriostipitalis (M. 18), slender, O: process of the anterior tentorial arm (laterad M. 17), I: maxillolabial ridge; M. craniolacinialis (M. 19), well developed, O: posterolaterally on the head capsule, at the level of the anterior margin of the compound eye, I: ridge on the dorsal side of the stipital part of the maxillolabial complex, with a thin tendon; M. stipitolacinialis (M. 20), absent; M. stipitogalealis (M. 21), absent; M. stipitopalpalis externus (M. 22), well-developed posterior bundle and two slender anterior bundles, O: posterior two bundles medially on the posterior part of the maxillolabial plate, anterior bundle laterally on the maxillolabial ridge; M. stipitopalpalis internus (M. 23), absent; M. palpopalpalis maxillae primus (M. 24), absent; M. palpopalpalis maxillae secundus (M. 25), absent; M. palpopalpalis maxillae tertius (M. 26), O: lateral wall of short second palpomere, I: mesally on the base of the penultimate palpomere; M. palpopalpalis maxillae quartus (M. 27), absent.

2.3 Morphology of adults 

 81

A very thin fibrillar structure connects the ridge between the proximal maxillary and labial elements with the lateral wall of the proximal maxilla. The homology is unclear. Labial musculature (Figs. 2.3.1.3 and 2.3.1.5): M. submentopraementalis (M. 28), absent; M. tentoriopraementalis inferior (M. 29), O: medially on postgenal bridge (close to occipital foramen), I: median premental apodeme; M. tentoriopraementalis superior (M. 30), absent; M. praementoparaglossalis (M. 31), absent; M. praementoglossalis (M. 32), absent; M. praementopalpalis externus (M. 34), moderately sized, two closely adjacent bundles, O: median premental apodeme, I: ventrolaterally on the base of palpomere 1; Mm. palpopalpales labii primus/ secundus (Mm. 35, 36), absent.

2.3.1.7 Epipharynx (Figs. 2.3.1.4 A,B and 2.3.1.5 A–C) The distal part of the epipharynx, i.e. the ventral side of the labrum, is flat and semimembranous. Its lateral area is equipped with minute tubercles, spines, hairs, and a low longitudinal ridge. These structures interact with the edges of the dorsal mandibular furrows (Fig. 2.3.1.5 A). The epipharyngeal section below the anterior clypeus is concave and also set with tubercles. A sclerotized, median pistil-like protrusion is formed by the epipharynx at the level of the secondary mandibular joint (epipharyngeal protrusion). Spiniferous tubercles are present on the semi­ membranous area laterad this structure. The middle section of the epipharynx is sclerotized and convex and forms an x-shaped preoral chamber together with the membranous area at the mesal mandibular base and the strongly sclerotized and convex part of the hypopharynx proximad to the hypopharyngeal projection (see below). It is completely devoid of microtrichia. The epipharyngeal part close to the anatomical mouth opening is narrow and laterally connected with the posterior

◂ Fig. 2.3.1.3: C. dectes, head, three-dimensional reconstructions (skeleton – blue, musculature – orange, nervous system – yellow,

digestive tract – green, salivary duct – pink). A, Anterior view; B, lateral view; C, posterior view; D, sagittal section. Abbreviations: atp – anterior tentorial pit, ccc – corpora cardiaca-corpora allata complex, ceao – cephalic aorta, cly – clypeus, cor – circumocular ridge, cpe – compound eye, cten – corpora tentorii, dta – dorsal tentorial arm, fg – frontal ganglion, lap – labial palp, lbr – labrum, md – mandible, mxl – maxillary lobe, mxp – maxillary palp, mxpl – maxillolabial plate, nan – nervus antennalis, nrec – nervus recurrens, onp – optic neuropils, pcer – protocerebrum, pcgl – protocerebral genal lobe, pch – precerebral pumping chamber, pgeb – postgenal bridge, ph – pharynx, sald – salivary duct, sca – scapus, soeg – suboesophageal ganglion, tb – tentorial bridge, tdm – transverse dilator muscle, t11 – adductor tendon, t12 – abductor tendon, 1 – M. tentorioscapalis anterior, 2 – M. tentorioscapalis posterior, 3 – M. tentorioscapalis lateralis, 5 – M. scapopedicellaris lateralis, 6 – M. scapopedicellaris medialis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 14 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 19 – M. craniolacinialis, 22 – M. stipitopalpalis externus, 26 – M. palpopalpalis maxillae tertius, 29 – M. tentoriopraementalis inferior, 34 – M. praementopalpalis externus, 37 – M. hypopharyngosalivarialis, 41 – M. frontohypopharyngalis, 43 – M. clypeopalatalis, 44 – M. clypeobuccalis, 45a, b – M. frontobuccalis anterior, 46a, b – M. frontobuccalis posterior, 51a, b – M. verticopharyngalis, 52 – M. tentoriopharyngalis. Scale bar: 100 µm.

82 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

51a

51a

nrec

pcer

51b

nan dta ata

46a

ceao

ldm

ph

tdm

fg

coe

cten

52

C

46a 46b

41

onp

45b

tb

soeg

pcer

dta tb

onp

cla 45b

45a 44 pep

43c

cla

45a nan 44

43b

A

43a eph

hyr

B

hyr

eph

dcer nrec

D

ata

fco

pcgl

fg

Fig. 2.3.1.4: C. dectes, head of adult, three-dimensional reconstructions (skeleton – blue, musculature – orange, nervous system – yellow, digestive tract – green). A, B, Digestive tract with muscles: A, Anterolateral view; B, posterior view. C, D, Central nervous system and tentorium: C, dorsal view; D, anterolateral view. Abbreviations: ata – anterior tentorial arm, ceao – cephalic aorta, cla – clasps of pumping chamber, coe– circumoesophageal connective, cten – corpora tentorii, dcer – deutocerebrum, dta – dorsal tentorial arm, eph – epipharynx, fco – frontal connective, fg – frontal ganglion, hyr – hypopharyngeal roof, ldm – longitudinal dilator muscle, nan – antennal nerve, nrec – nervus recurrens, onp – optic neuropils, pcer – protocerebrum, pcgl – protocerebral genal lobe, pep – posterior epipharynx, ph – pharynx, soeg – suboesophageal ganglion, tb – tentorial bridge, tdm – transverse dilator muscle, 41 – M. frontohypopharyngalis, 43a, b, c – M. clypeopalatalis, 44 – M. clypeobuccalis, 45a, b – M. frontobuccalis anterior, 46a, b – M. frontobuccalis posterior, 51a, b – M. verticopharyngalis, 52 – M. tentoriopharyngalis. Scale bars: 100 µm. Reprinted from Beutel et al. (2008) with permission from Elsevier.

hypopharynx, thus forming a narrow prepharyngeal tube (Fig. 2.3.1.5 C). The upper edges of the tube are reinforced by distinct sclerotizations representing the suspensorium. They are continuous with a ventromedian sclerotization of the anterior pharynx, which divides and forms a strongly sclerotized clasp enclosing the precerebral phar-

yngeal pumping chambers (=oral arms) (Figs. 2.3.1.4 A,B and 2.3.1.5 D). Musculature (Figs. 2.3.1.3, 2.3.1.4 A,B, and 2.3.1.5 B,C): M. clypeopalatalis (M. 43), well-developed, composed of three subcomponents, M. 43a, medially on the anterior margin of the postclypeus, I: ventrolaterally on

▸ Fig. 2.3.1.5: C. dectes, head of adult, histological cross sections. A, Anteclypeal region; B, distal postclypeal region; C, proximal postclypeal region; D, anterior pharyngeal region, precerebral pumping chamber; E, antennal base; F, posterior of antennal base. Abbreviations: acl – anteclypeus, ah – ampulla of antennal heart, ata – anterior tentorial arm, cla – clasps of pumping chamber, coe – circumoesophageal connective, cor – circumocular ridge, cpe – compound eye, dta – dorsal tentorial arm, eph –epipharynx, hyf – hypopharyngeal fold, hyr – hypopharyngeal roof, lac – lacinia, ldm – longitudinal dilator muscle, md – mandible, mdf – mandibular furrow, mxl – maxillary lobe, mxp – maxillary palp, mxpl – maxillolabial plate, nfr – nervus frontalis, nmd – nervus mandibularis, nrec – nervus recurrens, ori – oblique ridge, pcer – protocerebrum, pcgl – protocerebral genal lobe, pch – precerebral pumping chamber, pcl – postclypeus, ped – pedicellus, ph – pharynx, pmt – prementum, pmtap – premental apophysis, sald – salivary duct, sca – scapus, smj – second mandibular joint, soeg – suboesophageal ganglion, t11 – adductor tendon, t12 – abductor tendon, tdm – transverse dilator muscle, 1 – M. tentorioscapalis anterior, 6 – M. scapopedicellaris medialis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 13 – M. hypopharyngomandibularis, 14 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 19 – M. craniolacinialis, 22 – M. stipitopalpalis externus, 29 – M. tentoriopraementalis inferior, 34 – M. praementopalpalis externus, 37 – M. hypopharyngosalivarialis, 41 – M. frontohypopharyngalis, 43a, b, c – M. clypeopalatalis, 44 – M. clypeobuccalis, 45b – M. frontobuccalis anterior, 46b – M. frontobuccalis posterior, 47 – M. tentoriooralis. Scale bar: 100 µm.

2.3 Morphology of adults 



mxp

mdf

eph

pcl

acl

 83

43a smj

hyr

13

md

md

14

lac

mdf mxl

pmt

A

44

mxp

34

nfr

43c

eph

B

t11

pmt

cla 43b nmd

t12

45b

34

hyf 41 47

46b

13

14

pmtap

ata

14

pch

pcgl

hyr 37

t11

soeg 22

C

sald

sca

29

mxpl

ldm

ah

6

ori

t12

D

tdm

11

19 17

22

29 sald

mxpl pcer

ldm

ped

1 dta

nrec ph pcgl coe ata soeg cor

E

sald cpe 12

11

29

F

cpe 29

11

12

84 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

the median epipharyngeal projection; M. 43b, medially, close to the posterior margin of postclypeus, I: dorsolaterally on the median projection; M. 43c, O: postclypeus, dorsolaterad M. 43b, I: medially on the roof of the preoral chamber; M. clypeobuccalis (M. 44), O: immediately dorsolaterad M. 43c, I: anatomical mouth opening, below the frontal ganglion.

2.3.1.8 Hypopharynx (Figs. 2.3.1.4 A,B and 2.3.1.5 B,C) The anterior hypopharynx is represented by a membranous fold anterad the opening of the salivary duct and a separate projection above it (hypopharyngeal projection), between the mandibles and the median epipharyngeal projection (Fig. 2.3.1.5 B,C); the latter is triangular in cross section and continuous, with a strongly convex and strongly sclerotized median part of the preoral chamber. The posterior hypopharynx forms the sclerotized floor of the prepharyngeal tube, i.e. the sitophore plate. It is strongly sclerotized and convex opposite to the attachment of M. 43c (see above). Sclerotized ventral and lateral elements of the posterior hypopharynx form part of the anteriormost digestive tract dorsad the frontal ganglion, including the precerebral pharyngeal pumping chamber. Musculature (Figs. 2.3.1.3 A,B,D, 2.3.1.4 A, and 2.3.1.5 D): M. frontohypopharyngalis (M. 41), small muscle, O: frons, I: apical part of the pharyngeal clasp (oral arm); M. tentoriohypopharyngalis (M. 42), absent. M. tentorio­ oralis (M. 47), extremely short, O: mesal projection of the anterior tentorial arm, I: laterally on the prepharyngeal clasp (oral arm).

2.3.1.9 Pharynx and oesophagus (Figs. 2.3.1.3 D, 2.3.1.4 A,B, and 2.3.1.5 D–F) The anatomical mouth is narrow and flattened. It is followed by the short and narrow anteriormost pharyngeal section, which abruptly widens to form a very large pumping chamber. The chamber has a triangular shape in cross section. It is reinforced by sclerotizations connected with the suspensorium (pharyngeal clasp), which are equivalent to the oral arms of other insects. The postcerebral pharynx is narrow. The dorsolateral, lateral, and ventrolateral folds for attachment of dilator muscles are indistinctly developed. The oesophagus is slightly wider than the posterior pharynx and is round in cross section.

Musculature of the precerebral pharynx (Figs. 2.3.1.3, 2.3.1.4 A,B, and 2.3.1.5 D): M. frontobuccalis anterior (M. 45), strongly developed set of three bundles, M. 45a, two parallel bundles, O: frons (mesad the anterior tentorial pit), I: ventral wall of the precerebral pumping chamber; M. 45b, O: frons (dorsomesad M. 45a), I: anteroventrally on precerebral pumping chamber; M. frontobuccalis posterior (M. 46), composed of two muscle groups with distinctly different sites of origin, M. 46a, two parallel bundles, O: central region of frons (between antennal sockets), I: dorsal side of the pumping chamber; M. 46b, two strong bundles, O: lateral part of frons (ventrad antennal sockets), I: dorsolaterally on the pumping chamber. M. tentoriobuccalis anterior (M. 48), absent. A well-developed ring muscle is present around the anatomical mouth. Musculature of the postcerebral pharynx (Figs. 2.3.1.3 and 2.3.1.4 A,B): M. verticopharyngalis (M. 51), composed of two subcomponents, M. 51a, two bundles, O: dorsally on the vertex, posterad the brain, I: dorsolaterally on the postcerebral pharynx; M. 51b, a pair of very thin bundles, O: posterad, M. 51b, dorsolateral margin of the foramen occipitale, I: dorsolaterally on the postcerebral pharynx, above the attachment of the posterior bundles of M. 52; M tentoriopharyngalis (M. 52), a series of moderately sized bundles, O: laterad the alaforamen, close to the origin of the tentorial bridge, I: ventrally and ventrolaterally on the postcerebral pharynx.

2.3.1.10 Salivarium (Figs. 2.3.1.3 D and 2.3.1.5 C–F) The salivarium is strongly flattened at its opening and U-shaped and sclerotized on its posterior side in the following section (Fig. 2.3.1.5 C). The proximal part is thin walled and round in cross section. Musculature (Figs. 2.3.1.3 D and 2.3.1.5 C): M. hypopharyngosalivarialis (M. 37), represented by a highly modified intrinsic muscle of the unsclerotized anterior wall of the distal part of the salivary duct; Mm. praementosalivariales anterior/posterior (M. 38, 39), absent; M. annularis salivarii (M. 40), absent.

2.3.1.11 Cerebrum, suboesophageal complex, and stomatogastric nervous system (Figs. 2.3.1.3, 2.3.1.4 C,D, and 2.3.1.5 C–F) The brain is located in the central part of the head capsule and is not distinctly enlarged in relation to the head size.

2.3 Morphology of adults 



 85

It appears roughly quadrangular in dorsal view. The upper margin of the protocerebrum is extended toward the foramen occipitale. The upper edge is slightly sinuate. Distinct concavities are present on the posterior side of the upper part of the protocerebrum, allowing the passage of bundles of Mm. craniomandibulares internus/externus (Figs. 2.3.1.3, 2.3.1.4 C,D, and 2.3.1.5 E,F). A nervus connectivus originating from the frontal part of the protocerebrum is absent. The optic neuropils are strongly curved due to the spatial arrangement of the brain, the bundles of M. craniomandibularis internus, and the opening of the circumocular ridges. The deutocerebrum is not distinctly separated from the protocerebrum. The antennal nerves originating from it laterally are flattened basally and thin and cylindrically in their distal part. The tritocerebrum is represented by distinct paired lobes directed toward the ventral cranial margin. It is connected with the frontal ganglion by thick frontal connectives (Fig. 2.3.1.4 D). Anteriorly, a thin frontal nerve originates from the frontal ganglion (Fig. 2.3.1.5 C). A separate tritocerebral commissure is absent. A very broad and short circumoesophageal connective connects the brain with the suboesophageal complex (Fig. 2.3.1.5 E,F), which is located in the posterior head region (Figs. 2.3.1.3 C,D and 2.3.1.4 D). Its rostral part is roughly quadrangular in cross section and laterally enclosed by the mesal edges of M. craniomandibularis internus. The caudal part is heart shaped in cross section, with the paired lobes directed toward the pharynx.

divisions occur within the head capsule. Large air sacs are absent.

2.3.1.12 Glands

The cervical membrane is concealed by the pronotum dorsally, and laterally by the postorbital ridges, which fit closely with the prothorax when the head is retracted (Fig. 2.3.1). The lateral cervical sclerites are well-sclerotized, but less wide in Caurinus than in boreine species. The cervicalia articulate with the middle anterior margin of the propleuron, while they are more vertically disposed in boreines, where they insert on the proepisternum near the procoxal articulation. The dorsal cervical sclerites, which are usually inconspicuous in Boreinae, are absent in Caurinus. The prothorax of Caurinus (Fig. 2.3.2.1) is shorter and more transverse than in Boreus but is larger than in most groups of Mecoptera (but see Mickoleit 1967: large prothorax of Merope). The pronotum of Boreidae is arguably secondarily enlarged by a sclerotization of the intersegmental membrane, as suggested by the pronotal location of the mesothoracic spiracle. The pronotum of Caurinus is immovably joined to the mesonotum, whereas a ventral process of the pronotum articulates on each side with a

Glands are not present within the head capsule.

2.3.1.13 Circulatory system (Figs. 2.3.1.3 D and 2.3.1.4 A) The cephalic aorta is approximately triangular in cross section; it opens posterior to the central part of the brain. Musculature: An unpaired transverse dilator (Figs. 2.3.1.3 A,D, 2.3.1.4 A, and 2.3.1.5 E) interconnects the antennal hearts of both body sides. Paired longitudinal dilator muscles (Figs. 2.3.1.4 A and 2.3.1.5 E) are attached to the cephalic aorta immediately close to its opening.

2.3.1.14 Tracheal system One pair of tracheae enters the head capsule and divides into sub-branches within the foramen occipitale. Further

2.3.1.15 Fat body Fat body lobes are absent in the head. Frank Friedrich, Loren K. Russell & Rolf G. Beutel

2.3.2 Thorax The thoracic skeleton of Caurinus is similar to that of Boreus and Hesperoboreus in its basic structure. Like the species of Boreinae (see Section 3.3.2), Caurinus is brachypterous and has a large prothorax, and the sclerites of the pterothoracic pleura and sterna are fused into a single sclerotized structure. Similar pterothoracic fusions have independently evolved in the nonrelated apterous Apteropanorpa (Hepburn 1970). The process of reduction of membranes and fusion of sclerites has proceeded further in Caurinus than in the Boreinae. Most of the postcephalic body, from the prothorax to abdominal segment VI, is essentially a single mechanical unit, with little or no freedom of movement between segmental areas and hardly any exposed membrane.

2.3.2.1 Cervical region and prothorax

86 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

A cpe

B

nt1

nt1

scl2

fw fw

scl2

scl3

scl3 abdsI

abdsII

abdsI

abdsII

Fig. 2.3.2.1: Caurinus dectes, thorax of adults, SEM. A, Female, dorsal view; B, male, dorsal view (right side wings removed). Abbreviations: abdsI/II – abdominal segment I/II, cpe – compound eye, fw – forewing, nt1 – pronotum, scl2/3 – meso-/metascutellum. Scale bars: 100 µm.

mesepisternal fovea in boreines. The remaining prothoracic structures except for the procoxae are similar to the condition found in Boreinae (see Section 3.2.3). The procoxae (and pterothoracic coxae) are much shorter and more cylindrical than those of Boreus. Musculature (Fig. 2.3.2.2 A,B) Dorsal longitudinal muscles: Idlm1 M. prophragmaoccipitalis, two parallel portions, O (=origin): midline of the anterior mesoscutal margin (laterad Idlm5), I (=insertion): dorsolateral region of the postocciput. Idlm2 M. pronoto-occipitalis, slender, O: posteromesally on the pronotum (in front of Idlm1), I: dorsolateral region of the postocciput (together with Idlm1 and Idvm9). Idlm3 M. prophragma-cervicalis, laterally adjacent to Idlm5, O: anterior region of pronotum, I: lateral area of prophragma. Idlm5 M. pronoto-phragmalis, thin bundle, mesally adjacent to Idlm3, O: central region of the pronotum, I: lateral area of the prophragma. Dorsoventral muscles: Idvm2/3 M. cervicooccipitalis, strongly developed, O: large parts of the lateral cervical sclerite, I: dorsally on the postocciput. Idvm4 M. pronoto-cervicalis lateralis, absent. Idvm5 M. pronoto-cervicalis anterior, three bundles, O: anterolaterally on pronotum, I: posterior region of lateral cervical sclerite. Idvm7 M. pronoto-cervicalis posterior, moderately sized, O: posterior margin of the pronotum (in front of Idvm10), I: anterior third of the lateral cervical sclerite. Idvm9 M. profurca-occipitalis, O: tip of the profurcal arm (close to propleural transition), I: dorsolateral region of the postoccipital ridge (together with Idlm1 and Idlm2).

Idvm10 M. profurca-phragmalis, slender bundle, O: distal region of the profurcal arm (behind Idvm9), I: laterally on the prophragma. Idvm17 or 18 M. pronoto-coxalis, O: posterolaterally on the pronotum, I: posterior margin of the procoxa (laterad Iscm2). Tergo-pleural muscles: Itpm1 M. pleurocristaoccipitalis, absent. Itpm3 M. pronoto-pleuralis anterior, O: anterolateral region of the pronotum, I: dorsal margin of the propleuron. Itpm4 M. pronoto-pleuralis posterior, broad, flattened, O: lateral area of the pronotum, I: laterally on the propleuron. Sterno-pleural muscles: Ispm1 M. profurcaapodemalis, absent (profurcal arm continuous with propleural apodeme). Pleuro-coxal muscles: Ipcm2 M. procoxa-cervicalis, slender transverse muscle, O: anterior edge of the procoxa (lateral of Iscm1), I: anterior tip of the lateral cervical sclerite of the opposite body side. Ipcm4 M. propleuracoxalis, O: anterodorsal part of the propleuron, I: anterolateral part of the procoxa (lateral of Ipcm2). Ipcm8 M. propleura-trochanteralis, O: anteroventral area of the propleuron, I: trochanteral abductor tendon (together with Iscm6). Ventral longitudinal muscles: Ivlm1 M. profurcacervicalis, O: anterior face of the profurcal arm, I: middle region of the lateral cervical sclerite. Ivlm3 M. profurcaoccipitalis ventralis, two main bundles, O: profurcal arm (below and above the insertion site of Ivlm4), I: ventrally on the foramen occipitale. Ivlm4 M. intraprofurcalis, O: mesal face of the profurcal arm, I: profurcal arm of the



opposite side. Ivlm7 M. profurca-mesofurcalis, O: posterior face of the profurcal arm, I: anteriorly on the mesofurcal arm. Ivlm9 M. prospina-mesofurcalis, absent. Sterno-coxal muscles: Iscm1 M. prosterno-coxalis anterior, O: medially on the prosternal ridge (anterior of profurca), I: anterior procoxal rim. Iscm2 M. profurcacoxalis posterior, strongly flattened, O: ventral side of the profurcal arm, I: posteriorly and posterolaterally on the procoxal rim. Iscm3 M. profurca-coxalis medialis, absent. Iscm6 M. profurca-trochanteralis, O: base of profurcal arm, I: trochanteral abductor tendon.

2.3.2.2 Pterothorax The pterothorax is also more compact than in Boreinae. Apomorphic conditions in Caurinus include reductions of the pleural and intersegmental sutures, as well as of the hindwing of the male (Fig. 2.3.1.1 B) and abdominal spiracle I (Fig. 2.3.1 C,D). The line of fusion of the first abdominal tergite to the metathorax is effaced. A free apical tergite of segment I as it is present in Boreinae is missing in Caurinus. The mesothoracic and metathoracic coxae are deeply set in coxal cavities and partly immobilized. The mesonotum and metanotum of males are also derived compared to conditions found in Boreinae; they are partly membranous and the sclerites are thinner than the cuticle of the pleurosternal region. The scutellum is well developed and the scutum reduced to a narrow band in both pterothoracic segments. The forewing of the male extends only to abdominal segment II; the hindwing is represented by a minute peg-like sclerite (Fig. 2.3.1.1 B). Musculature (males; largely identical to that of females in Fig. 2.3.1.2) Mesothorax: Dorsal longitudinal muscles: IIdlm1 M. prophragma-mesophragmalis, dorsoventrally flattened, weakly developed, O: prophragma, close to midline, I: mesophragma (in front of IIdvm7). IIdlm2 M. mesonotophragmalis, absent. IIdlm3 M. mesoscutello-postnotalis, absent. Dorsoventral muscles: IIdvm1 M. mesonoto-sternalis, absent. IIdvm2 M. mesonoto-trochantinalis anterior, absent. IIdvm4 M. mesonoto-coxalis anterior, slender, O: mesonotum, directly posterior of IIdvm7, I: posterolaterally on mesocoxal rim (mediad IIdvm6). IIdvm6 M. mesocoxa-subalaris, slender, O: posterior edge of the mesocoxa with short, strong tendon, I: remnant of subalare at the wing base. IIdvm7 M. mesonoto-trochanteralis, welldeveloped, O: mesonotum (in front of IIdvm4), I: trochanteral abductor tendon. IIdvm8 M. mesofurca-phragmalis, absent.

2.3 Morphology of adults 

 87

Tergo-pleural muscles: IItpm1 M. prophragmamesanepisternalis, well-developed, O: prophragma/anterior margin of mesoscutum (close to Idvm10), I: anterior face of the basalar apodeme (close to IIpcm2/3). IItpm2 M. mesopleura-praealaris, absent. IItpm3 M. mesonoto-basalaris, absent. IItpm4/5/6 Mm. mesonoto-pleurales anterior/medialis/posterior, absent. IItpm7 M. mesan­ episterno-axillaris, absent. IItpm9 M. mesepimero-axillaris, fan-shaped, O: extensively from the central part of the mesepimeron, I: wing base (likely third axillary sclerite) by a long tendon. IItpm10 M. mesepimero-subalaris, absent. Pleuro-pleural muscles: IIppm2 M. mesobasalareintersegmentalis, absent. Sterno-pleural muscles: IIspm1 M. mesopleurasternalis, absent. IIspm2 M. mesofurca-pleuralis, absent. Pleuro-coxal muscles: IIpcm2/3 M. mesobasalarecoxalis, O: basalar invagination of the mesanepisternum, I: antero-laterally on mesocoxal rim by the long tendon. IIpcm4 M. mesanepisterno-coxalis, flattened, O: anteroventral area of the mesanepisternum, I: anterolateral rim of the mesocoxa (together with IIpcm2/3). IIpcm5 M. mesanepisterno-trochanteralis, absent. Ventral longitudinal muscles: IIvlm3 M. mesofurcametafurcalis, two moderately sized portions, O: dorsal face of the mesofurcal arms, I: anteriorly on metafurca by two thin tendons. Sterno-coxal muscles: IIscm1 M. mesofurca-coxalis anterior, O: mesosternal discrimen and proximal part of mesofurcal arm, I: anterior mesocoxal rim. IIscm2 M. mesofurca-coxalis posterior, broad, flattened, O: ventral side of the mesofurca (mesally of IIscm6), I: posterior mesocoxal rim. IIscm3 M. mesofurca-coxalis medialis, very thin, O: base of mesofurcal arm (mesally of IIscm2), I: mesal mesocoxal rim. IIscm4 M. mesofurca-coxalis lateralis, short, O: laterally from the mesofurca, I: ventral part of the mesopleuron above the coxo-pleural joint. IIscm6 M. mesofurca-trochanteralis, well-developed, O: ventral side of mesofurca, I: trochanteral abductor tendon (together with IIdvm7). The following muscles are absent in females: IIdlm1 M. prophragma-mesophragmalis, IItpm1 M. prophragmamesanepisternalis, IItpm9 M. mesepimero-axillaris tertius, IIvlm3 M. mesofurca-metafurcalis, IIscm3 M. mesofurca-coxalis medialis. Metathorax: Dorsal longitudinal muscles: absent. Dorsoventral muscles: IIIdvm1 M. metanoto-sternalis, absent. IIIdvm2 M. metanoto-trochantinalis anterior, absent. IIIdvm4/5 Mm. metanoto-coxales anterior/ posterior, absent. IIIdvm6 M. metacoxa-subalaris, well-developed, O: posterior margin of the metacoxa, I:

88 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

Idvm7

IIIdvm7

nt3

abdsII

tgI

Idlm3&5

nt2

Idvm2/3

Itpm4

nt1 atI-atII hc

Idvm10 Idvm2/3

pori Idvm5

Ivlm3b

fu1

Ivlm1

tb Ipcm2

IIpcm4 asI-asII

Ipcm4 st1

IIIvlm2

Iscm1 Ivlm4

A

C

Ivlm7

IIpcm2/3

Idlm2

Idlm1

IIdvm7

nt2

IIIpcm2/3

nt1 ph1 IIIdvm6 IIdvm6

Idvm2/3

spi1

Itpm3

Idvm4? Idvm17/18

Idvm9 IIIscm4?

Ivlm3a

IIIpcm4 st1

B

stI

cx1 cx2

fu1 fu2

IIIscm6a

Ipcm8

cx1

cx3 cxtr

st3

D

cx2

Fig. 2.3.2.2: C. dectes, thorax of female, reconstruction based on histological sections. A, Right body half, gut and nervous system removed; B, same as A, median muscles removed; C, D, lateral prothoracic muscles. Abbreviations: abdsII – abdominal segment II, cx1/2/3 – pro-/ meso-/metacoxa, fu1/2 – pro-/mesofurca, hc – head capsule, nt1/2/3 – pro-/meso-/metanotum, ph1 – prophragma, pori – postoccipital ridge, spi1 – prothoracic spiracle, st1/3 – pro-/metasternum, stI – first abdominal sternum, tb – tentorial bridge, tgI – first abdominal tergum. See text for muscle terminology. Scale bars: 100 µm.

2.3 Morphology of adults 



subalare via short, strong tendon. IIIdvm7 M. metanoto-trochanteralis, largest thoracic muscle, O: large areas of anterior metascutum and mesophragma, I: trochanteral abductor tendon. IIIdvm8 M. metafurca-phragmalis; absent. Tergo-pleural muscles: IIItpm1 M. mesophragmametanepisternalis, very thin, slender, O: mesophragma/ anterior margin of the metascutum, I: metabasalar apodeme (dorsally to IIIpcm2/3). IIItpm2 M. metapleurapraealaris, absent. IIItpm3 M. metanoto-basalaris, absent. IIItpm4/5/6 Mm. metanoto-pleurales anterior/ medialis/posterior, absent. IIItpm7 M. metanepisternoaxillaris, absent. IIItpm9 M. metepimero-axillaris, absent. IIItpm10 M. metepimero-subalaris, absent. Pleuro-pleural muscles: IIIppm2 M. metabasalareintersegmentalis, absent. Sterno-pleural muscles: IIIspm1 M. metapleurasternalis, absent. IIIspm2 M. metafurca-pleuralis, absent. Pleuro-coxal muscles: IIIpcm2/3 M. metabasalarecoxalis, spindle shaped, O: invaginated apodeme of the metabasalare, I: anterolateral part of the metacoxa (lateral of IIIpcm4). IIIpcm4 M. metanepisterno-coxalis, short, O: ventral area of the metanepisternum, I: anterolaterally on the metacoxal margin. IIIpcm5 M. metanepisterno-trochanteralis, absent. Ventral longitudinal muscles: IIIvlm2 M. metafurcaabdominosternalis, two bundles; O: posterior face of the metafurcal arm, I: ventrally and ventrolaterally on abdominal sternite II. Sterno-coxal muscles: IIIscm1 M. metafurca-coxalis anterior, flattened, O: metasternal discrimen and proximal parts of the metafurca, I: anterior metacoxal margin. IIIscm2 M. metafurca-coxalis posterior, short, O: base of the metafurcal arm, I: posterior margin of the metacoxa. IIIscm3 M. metafurca-coxalis medialis, absent. IIIscm4 M. metafurca-coxalis lateralis, O: lateral part of the metafurcal arm, I: ventral area of the metapleura (close to pleuro-coxal joint). IIIscm6 M. metafurca-trochanteralis, O: lateral face of the discrimen and base of the metafurcal arms, I: trochanteral abductor tendon (together with IIIdvm7). Females lack IIItpm1 M. mesophragma-metanepisternalis.

2.3.2.3 Legs The distal parts of the three pairs of legs are similar, but the middle legs are slightly longer than the forelegs, and the jumping hind legs are distinctly longer than the other two pairs (Sikes & Stockbridge 2013: fig. 6). A fine pubescence is present like on the other body parts. The trochanter is

 89

well-developed, of parabolic shape, and widening toward the joint with the femoral base (Fig. 2.3.1 C,D). The roughly cylindrical femora are very slightly convex along their dorsal edge and very slightly concave along their ventral margin; the profemur is shortest and the metafemur about 1.5 as long as the mesofemur (Fig. 2.3.1 B,D). The cylindrical tibiae are less wide but slightly longer than the respective femora (Fig. 2.3.1 D); they are very slightly widening distally. Several very short apical spines and tibial spurs are present (Fig. 2.3.2.3 A). Like in the case of the femora, the length increases from the anterior to the posterior. The tarsi are five-segmented (Fig. 2.3.2.3 A), shortest on the fore leg and longest on the hind leg. The basal and distal tarsomere are the longest, the former moderately widening toward its apex, the latter strongly extended distally. The short three intermediate tarsomeres are narrow basally and distinctly widening distally. The size increases slightly from segment 2 to 4. The tarsomeres are quite densely covered with medium length setae, but soles with specialized tenent hairs are missing (Fig. 2.3.2.3 A). The strongly developed equal claws lack additional teeth. Arolium and pulvilli are absent (Fig. 2.3.2.3 B,C). The surface of the proximal part of the strongly developed unguitractor plate displays a scale-like pattern; distolaterally, it bears long, slender and apically curved processes, resembling setae, but without basal articulation. Short bulges between the bases of these structures are continuous with the bases of the claws (Fig. 2.3.2.3 C).

2.3.2.4 Wings Like in Boreus (Mickoleit & Mickoleit 1976), the modified wings of Caurinus males (Fig. 2.3.2.1 B) are apparently used to support the female by grasping one or more appendages during prolonged copulation (Cooper 1940, Crampton 1940). The forewing of the male is used to clasp one of the female’s antennae. Like in Boreus, the forewing of Caurinus is restricted to rotation in a plane nearly parallel to the longitudinal axis of the insect. However, the wing of Caurinus is capable of 180° forward rotations, while the clamping action of Boreus and Hesperoboreus appears to be feasible through only a 40° to 50° arc (Russell 1979a). The extended position of the wings suggests that both wings are frequently moved together and that there are two stable positions: fully closed (the position in repose) and fully extended. The size and shape of the wings, and possibly of a rapid closure with the long spines rotating mesally to interlock, lend this mechanism the appearance of a “snap-trap” (Russell 1979a). The key modifications of permitting

90 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

tib

A

tar

cl

tibs tar

cl

untp

B

C

Fig. 2.3.2.3: C. dectes, female, prothoracic tarsus, SEM. A, Tarsus, lateral view; B, distal tarsomere, ventrolateral view; C, details of distal tarsomere, ventral view. Abbreviations: cl – claw, tar – tarsus, tib – tibia, tibs – tibial spur, untp – unguitractor plate. Scale bars: A: 50 µm, B, C: 10 µm.

a 180° rotation are the loss of the direct articulation of the wing base with the pleural wing process and the free posterior margin of the basalare. As in Boreus, elevation of the wing (abduction) is apparently steered by a single tergo-pleural muscle inserting on the basalare (IItpm1). The basalare is dorsally linked to the expanded lateral wing base and articulates anteriorly with the narrow wall of the anepisternum. Lowering, or adduction, of the wing is apparently guided by a more dorsally inserted pleural muscle (IItpm9) inserted on a small sclerite near the dorsal wing process (the functional pivot). In addition, it is apparent that the wings of Caurinus (like in Boreinae) are “spring-loaded” resisting movement from the position of repose in the absence of muscle tonus (even when the muscles are removed). This elastic joint mechanism is probably the function of the large pad of resilin found in the wing ligament by Rothschild and Schlein (1975), rather than involvement in the hopping mechanism. A third pleural muscle found in Boreus, effecting the rotation of the wing on its longitudinal axis and assisting in adduction, is apparently missing in Caurinus (Russell 1979a). This suggests that wing rotation is enabled by the linkage of the basalare and lateral wing margins.

The forewings of females are transformed into small, pad- or scale-like structures (Fig. 2.3.2.1 A). Wing-moving muscles are present in males but absent in females (see above). Frank Hünefeld & Rolf G. Beutel

2.3.3 Pregenital abdomen The external morphology of the abdomen is described in Russell (1979a). The abdomen is more elongate in males than in females (Figs. 2.3.1 and 2.3.3.1 A,B). Tergite I is fused with the adjacent metathoracic sclerotization but can be distinguished from it by a different vestiture and the presence of nonfunctional spiracle I. Sternite I is represented by a pair of minute sclerites fused to the ring-like sclerotization of segment II. The tergites and sternites II–VI are laterally fused, thus forming sclerotized ringlike structures. The intersegmental membranes between segments II and VI are extremely short, which results in a strongly restricted flexibility of this region. Tergites and sternites VII and VIII are distinctly separated by a lateral pleural membrane in both sexes. Spiracles VII and VIII are located laterally in the tergites.

2.3 Morphology of adults 



A

abdsII

tgVII

tec

hypa cx3

B

stVII tgVII

 91

muscle numbers for the pregenital abdominal segments are taken from von Kéler (1963). M. antecosta-antecostalis uronotum medialis (170), O: tergal region, on or near the antecosta, paramedially, I: antecosta of following tergal region, paramedially. M. antecosta-antecostalis uronotum lateralis (171), O: tergal region, on or near the antecosta, laterad 170, I: antecosta of following tergal region, laterad 170. M. uronotoantecostalis paradorsalis (174), O: tergal region, on or near the antecosta, laterad 171, I: antecosta of following tergal region, laterad 171. M. antecosta-antecostalis urosterni medialis (175), O: sternal region, approximately at half length, I: antecosta of following sternal region. Frank Hünefeld & Rolf G. Beutel

tec

abdsII

C

stVII 170 171

175

174

Fig. 2.3.3.1: Caurinus dectes, abdomen, lateral view. A, Male, terminal segments hyperextended. B; female, terminal segments hyperextended; C, female, lateral view, segments II–VI sagittally sectioned, abdominal musculature, nonmuscular soft tissue removed. Abbreviations: abdsII – abdominal segment II, cx3 – metacoxa, hypa – hypandrium, stVII – abdominal sternite VII, tec – terminal complex (fully retracted in repose), tgVII – abdominal tergite VII. Muscle numbers according to von Kéler (1963). Scale bar: 250 µm.

Musculature (Fig. 2.3.3.1 C): the segmental pregenital musculature comprises four pairs of muscles in females (no data available for males). Dorsoventral or transverse muscles were not found. The muscle nomenclature and

2.3.4 Female postabdomen Tergites VII and VIII of females and the corresponding ventral plates are separated by a pleural membrane (Fig. 2.3.4.1 A). Both segments are about equally long. Segment VIII is the last exposed segment in the inactivated abdomen. Ventral appendages VIII are fused, forming a solid, unpaired plate that does not markedly project beyond the posterior margin of the segment. This is clearly in contrast to the long, paired appendages in Boreinae (see Section 3.3.4). Behind the posterior margin of the ventral plate of segment VIII lies the gonopore (Fig. 2.3.4.1 B). The retracted terminal segments IX–XI can be everted by hemolymph pressure. A secondary ovipositor, as it is found in Boreinae (Section 3.3.4), is not developed, and some minute plates are the only sclerotized elements of the terminal segments. The segmental borders are clearly traceable. On segment IX, the tergal sclerotization is reduced to a pair of small trapezoid lateral plates. Below these plates lie the vestiges of genital appendages IX as minute, slender sclerotized stripes (Fig. 2.3.4.1 A). Tergite X is small and plate like. A ventral sclerotization of segment X is lacking (Fig. 2.3.4.1 A). The epiproct and subanal plate of segment XI are welldeveloped (Fig. 2.3.4.1 B). The unsegmented, slender cerci arise laterad the intersegmental area between segments X and XI (Fig. 2.3.4.1 A). Musculature (Fig. 2.3.4.1 B). Fourteen postabdominal muscles can be identified. Muscle numbers are taken from Hünefeld et al. (2012). Segment VII. 01 isVII-01, O: anterior half of tergite VII, paramedially, I: anterior margin of tergite VIII, paramedially, F: retractor of segment VIII; 02 isVII-02, O: anterior half of tergite VII, laterad M. 01, I: tergite VIII, laterad M. 01, F: segment VIII-retractor; 03 isVII-03, O: posterolaterad

92 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

A

tgVII tgVIII

01

03

02

tgIX

B 24

tgX

23

45

67 ept

cer

reo sap

sap

46 50 geapIX stVII

geapVIII

17

09

36

73

geo

27

Fig. 2.3.4.1: Caurinus dectes, female postabdomen, terminal segments hyperextended. A, Lateral view; B, skeleto-muscular arrangement, mesal view. Abbreviations: cer – cercus, ept – epiproct, geapVIII/IX – genital appendage of segments VIII/IX, geo – genital opening, reo – rectal opening, sap – subanal plate, stVII – abdominal sternite VII, tgVII-X – abdominal tergites VII–X. See text for muscle details. Scale bar: 250 µm.

M. 01, I: laterad M. 02, anterolateral corner of tergite VIII, F: retractor of segment VIII; 09 isVII-09, O: posterior half of sternite VII, paramedially, I: anterior margin of the ventral plate of segment VIII, F: retractor of segment VIII; 17 dvVII02, O: tergite VII, I: sternite VII, F: depressor of segment VII. Segment VIII. 23 isVIII-01, O: posterior part of tergite VIII, paramedially, I: anterior margin of the vestiges of tergite IX, F: retractor of segment IX; 24 isVIII-02, O: midlength of tergite VIII, below M. 23, I: membranous anterior margin of segment IX, F: retractor of segment IX; 27 isVIII-05, O: laterally on the ventral plate of segment VIII, I: anterior apex of the vestige of the genital appendage IX, F: retractor of segment IX; 36 dvVIII-01 (1 compact muscle), O: tergite VIII, I: dorsal margins of the ventral plate of segment VIII. Segment IX. 45 isIX-01, O: dorsally on the membranous cuticle of segment IX, I: in front of tergite X, F: retractor of segment X; 46 isIX-02, O: ventrally on the membranous cuticle of segment IX, I: ventrally on the anterior margin of segment X, F: retractor of segment X; 50 dvIX-01, O: vestiges of tergite IX, I: vestiges of the ventral appendages IX. Cercal muscle. 67 ce-01, O: beside tergite X, I: base of the cercus, F: moves the cercus. Muscles of the genital chamber. 73 gc-04, O: posterior half of the ventral plate of segment VIII, paramedially, I: ventrolaterally on the genital chamber, a short distance in front of the gonopore, F: dilator of the genital chamber.

Frank Hünefeld & Rolf G. Beutel

2.3.5 Male postabdomen The morphology of the male postabdomen and the internal parts of the genital system were described by Russell (1979a). The terminal segments IX–XI are retracted into the pregenital abdomen in repose. They are concealed between sternite IX (“hypandrium”) and tergite VIII. Extrusion during mating is likely effected by hemolymph pressure. Segment IX lacks a distinct tergal sclerotization. Sternite IX is very large and plate-like and slightly curved dorsad. The large gonocoxites originate laterally from the basal part of segment IX (Fig. 2.3.5.1). Anteriorly, their bases are produced as a long lateral and a short mesal apodeme. Distally, they bear the strongly sclerotized gonostyli, each with a curved and elongate external tooth and a short and setose mesal tooth. The large penis, which originates ventrobasally on segment IX between the gonocoxites, is composed of a distinctly developed dorsal and ventral sclerite (Fig. 2.3.5.1). The apex of the dorsal sclerite is spoon-shaped and its internal anterior part is produced into a pair of short apodemes, which articulate with the mesal apodemes of the bases of the gonocoxites. The ventral sclerite is a large, plate-like structure covering the entire ventral surface of the penis. Its posterior margin is conspicuously arched and bears a sparse vestiture of setae. Two minute sclerotized stripes are embedded in the membranous

2.3 Morphology of adults 



A

lps

B

gcxIX

dps

geo

 93

vps lps

vps gstIX dps

gcxIX

prg prg

gstIX

tgVIII hypa

tgVII

stVIII stVII Fig. 2.3.5.1: Caurinus dectes, male postabdomen, external structures, terminal segments hyperextended. A, Lateral view; B, dorsal view. Abbreviations: dps – dorsal penis sclerite, gcxIX – gonocoxite IX, geo – genital opening, gst IX – gonostylus IX, hypa – hypandrium, lps – lateral penis sclerites, prg – proctiger, stVII-VIII – abdominal sternite VII-VIII, tgVII-VIII – abdominal tergite VII-VIII, vps – ventral penis sclerite. Scale bar: 250 µm.

lateral areas of the penis on both sides (Fig. 2.3.5.1). An unpaired small plate lies below the genital opening. Segments X and XI form the proctiger with the rectal opening on its apex. The segmental limits are indistinct. The proctiger is largely membranous, but small unpaired dorsal and ventral plates are present. It is unclear whether these sclerotizations represent tergite and sternite X or the epiproct and the subanal plate belonging to segment XI. Information on the postabdominal musculature of males of Caurinus is presently not available. The internal genitalia of Caurinus (Fig. 2.3.5.2) are similar to those of males of the other boreid genera. The medially fused testes, which contain six follicles, lie in the dorsal midline of the abdomen. The vasa deferentia are long, slender tubes. They are connected with the large accessory glands, which are composed of a balloon-shaped main component and an anterodorsal “cap.” The “cap” contains a multicoiled tube, which is likely a continuation of the vas deferens (see Russell 1979a). A short, wide tube connects the paired structural units formed by the vasa deferentia and the glands with the ejaculatory duct, which is enclosed by a strongly developed muscularis.

Bożena Simiczyjew & Rolf G. Beutel

2.3.6 Ovaries As pointed out in Russell (1979a, b), the female reproductive system is most conveniently studied in teneral adults. Within a few weeks after adult emergence, the reproductive system is greatly distorted by the very large mature oocytes (Russell 1979a). A well-defined genital chamber is not present. The epithelium of the lateral oviducts, which are closely adjacent to abdominal ganglion VI, is composed of extremely flattened cells and surrounded by a single-layered muscularis formed of single fibers. The paired tubes merge into a short unpaired oviduct, with an epithelium of strongly flattened cells with the nuclei located in extensions of the cell bodies; the lumen is wide and the wall is lined with a thin intima. The duct of the accessory glands and the spermathecal duct both open dorsally into the median duct, the latter in front of the former, with some distance between them. The spermathecal duct is about five times as long as the spermatheca and tightly coiled; it is composed of cubic epithelial cells and internally lined with a thick cuticular intima (Fig. 2.3.6.1); a muscularis is lacking (Fig. 2.3.6.2 A).

94 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

ova

tst

sped

spe

vd

agl

agl

dej

Fig. 2.3.5.2: C. dectes, male, internal parts of the genital system, dorsal view. Abbreviations: agl – accessory gland, dej – ejaculatory duct, tst – testes, vd – vas deferens. Scale bar: 250 µm. Redrawn from Russell (1979a).

The rather elongated spermatheca is bilobed, approximately kidney-shaped; its epithelial cells are flattened; and its muscularis consists of single fibers forming a loose meshwork (Fig. 2.3.6.2 A). The accessory gland opens with a very short duct with an intima. The secretory units are “type 1” glands (Noirot & Quennedy 1974) (Fig. 2.3.6.2 B) with prismatic cells with the nuclei close to the basal poles; a muscularis associated with the gland is absent. Each of the paired ovaries is composed of four ovarioles, with closely adjacent openings on the lateral oviducts. A single ovariole is composed of a terminal filament, an elongated vitellarium, and the ovariole pedicle (Fig. 2.3.6.3 A,B). The vitellarium is composed of

lov cov

Fig. 2.3.6.1: Caurinus dectes, female, internal parts of the genital system, dorsal view. Abbreviations: agl – accessory gland, cov – common oviduct, lov – lateral oviduct, ova – ovary, spe – spermatheca, sped – spermathecal duct. Scale bar: 500 µm. Redrawn from Russell (1979a).

linearly arranged ovarian follicles, which are composed of an oocyte surrounded by somatic cells forming a single-layered epithelium (follicular epithelium) (Fig. 2.3.6.3 A,D,E,F). In each ovariole, early previtellogenic, mid previtellogenic, late previtellogenic, vitellogenic, and choriogenic follicles can be observed. Early previtellogenic ovarian follicles are located in the apical part of the vitellarium. The oocytes are relatively small at this stage (Fig. 2.3.6.3 A,C). The germinal vesicle (the oocyte nucleus) is spherical, situated centrally and occupies a considerable proportion of the cell (Fig. 2.3.6.3 D,E). Numerous intensely stained fine structures are regularly distributed in the karyoplasm (Fig. 2.3.6.3 I); they are likely multiple nucleoli resulting from rDNA amplification (selective extrachromosomal amplification of ribosomal genes). During previtellogenesis, the somatic follicular cells form a monolayered epithelium, a compact unit of morphologically uniform cuboidal cells (Fig. 2.3.6.3 D). At the stage of early vitellogenesis, the follicular epithelium differentiates into two subpopulations: follicular cells covering the lateral parts and posterior pole of the oocyte and group of cells encompassing the anterior pole of the oocyte (Fig. 2.3.6.3 F). During vitellogenesis, spaces form between the follicular cells; their large nuclei occupy nearly the entire cell volume. During vitellogenesis, the oocytes increase in size as a result of the deposition of yolk spheres and lipid droplets; the yolk spheres increase in number and size, thus gradually filling out the whole oocyte (Fig. 2.3.6.3 I,J).

2.3 Morphology of adults 



A

spe

sped

B

agl Fig. 2.3.6.2: C. dectes, female abdomen, histological cross sections. A, Spermatheca and spermathecal duct; B, accessory gland. Abbreviations: agl – accessory gland, spe – spermatheca, sped – spermathecal duct. Scale bars: 25 µm.

The shape of the oocyte changes and becomes more irregular in the advanced vitellogenesis. The constant number of four ovarioles in Caurinus is the lowest recorded for Mecoptera. Females of Hespero­ boreus notoperates have 6 ovarioles per ovary, while the number varies from 7 to 10 in Boreus (sometimes within a single species). The ovariole number in other Pistillifera varies from 7 to 10 in the more “ancestral” families (Meropeidae, Choristidae) to as many as 14 in Panorpa and 14 to 19 in Apterobittacus apterus. Ovaries of the neopanoistic type are also present in Boreinae (see Section 3.3.6; Biliński & Büning 1998, Biliński et al. 1998). Štys & Biliński (1990) postulated that this condition has evolved from meroistic ovarioles by a secondary loss of nurse cells. The neopanoistic type is

 95

also found in Nannochoristidae, where the ovarioles are diversified into a terminal filament and vitellarium, the latter comprising a few ovarian follicles built of oocytes surrounded by follicular epithelium (see Section 1.3.6). All ovarioles of Caurinus (and Boreus) are jointly connected with the lateral oviduct, whereas they appear segmentally arranged in Nannochorista, each of them with an individual connection. A panoistic organization is also common in Siphonaptera (except for Hystrichopsyllinae). In contrast, investigations of the ovary structure and the course of oogenesis have revealed an entirely different, polytrophic organization in most families of Mecoptera (Apteropanorpidae, Bittacidae, Choristidae, Eomeropidae, Merope­ idae, Panorpidae, and Panorpod­idae) (Simiczyjew 2005): in all of them, clusters of germ cells are formed, each of them composed of four cells, resulting from two mitotic divisions of a cytoblast and cystocytes, ending with incomplete cytokineses. Within a cluster, one cell differentiates into an oocyte, whereas the remaining three transform into large polyploid nurse cells, characterized by high synthetic activity. In the nurse cells, various macromolecules are synthesized, which are subsequently transported to the oocyte. The nurse cells also provide organelles (e.g. ribosomes and mitochondria) to the ooplasm (Büning 1994). In contrast, the oocyte remains transcriptionally inactive throughout oogenesis. The condensed meiotic chromosomes form a prominent karyosphere in the relatively small nucleus. In Caurinus dectes, the lack of nurse cells is apparently compensated for by the amplification of rDNA genes in the oocyte nucleus. Similar activity occurs in the oocyte nucleus of Boreus and Nannochorista (Simiczyjew 2002) and also in fleas with panoistic ovaries (Büning 1994, Simiczyjew & Margas 2001). The elongate spermatheca and spermathecal duct of Caurinus resemble the condition found in Boreus and most other groups of Mecoptera. In contrast, the spermatheca of Hesperoboreus is almost sessile and multi-chambered. The seemingly unpaired accessory gland of Caurinus is most likely formed by a fusion of paired organs.

Loren K. Russell & Rolf G. Beutel

2.3.7 Eggs (based on Russell 1979a) Newly laid eggs of Caurinus dectes are elongate-oval and almost spindle shaped, with narrowly rounded (parabolic) ends. No noticeable polar or dorsoventral asymmetry is recognizable. The average site is 0.60 × 0.25 mm (length by width) after deposition, but moderate swelling

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 2 Neomecoptera, Boreidae, Caurininae, Caurinus

tf

tf

oo

oo

ovf

fep

oo

nu

fep

C

nu nu

B

D

oo

E

F

poo

fep

poo

nu voo

oo

A

voo voo nu oo

G

poo

H

I

J

Fig 2.3.6.3: C. dectes. Structure of the ovariole. A, Schematic representation of the ovariole, ovarian follicle built of an oocyte surrounded by follicular epithelium; B, apical part of the ovariole with terminal filament; C, early previtellogenic oocytes; D, previtellogenic ovarian follicle; E, part of the vitellarium; previtellogenic oocyte with extremely large nucleus, arrow indicates the follicular epithelium; F, early vitellogenic ovarian follicle; the follicular epithelium that surrounds the lateral parts of the oocyte is different from that forming the anterior pole of the oocyte (arrow); G, cross section through an oocyte covered with a thin egg envelope (arrow) in late stage of oogenesis; H-J, ovarian follicles at various stages of oogenesis in cross-sections, arrows indicate follicular epithelium. Abbreviations: fep – follicular epithelium, nu – oocyte nucleus, ovf – ovarian follicles, oo – oocyte, poo – previtellogenic oocyte, tf – terminal filament, v – vitellarium, voo – vitellogenic oocyte. © Bożena Simiczyjew.

occurs later in development. The eggs appear black, with a micro-reticulation over most of the surface or the entire surface. A few eggs are less pigmented at one pole and show that the chorion itself is cream colored, but covered with a dark cementing material, which usually fills in the angles where the egg joins the substrate. Eggs that are lightly covered with cement show dark spots, where this fills the punctures in the chorion surface, as well as parallel longitudinal streaks. This suggests that this material is

applied during oviposition before the egg leaves the body. The cement layer is usually very thin, suggesting that the microreticulate surface is developed on the chorion. Occasional thicker areas of cement covering appear quite smooth at 250× magnification. Eggs with an incompletely pigmented surface were commonly observed in cultures both early and near the end of the season of activity of adult C. dectes. The cement is probably produced by the colleterial glands of the female and is likely a protein,



which is tanned after secretion. The coating of the colorless egg with dark cement may protect the exposed egg from ultraviolet light damage. Intact eggs remaining on the liverwort substrate become bleached to a dark brown color by late July to August. The chorion is a very tough and leathery layer. This is not a result of the tanning of the cement layer, for the colorless, mature ovarial eggs are frequently found intact in detached, skeletal abdomens recovered in wet-screened samples. Oviposition was never observed during the 2 years adult Caurinus dectes were held for study even though several hundred eggs were laid by captive females. It may have been missed by its being a largely nocturnal activity in this species. However, it is also conceivable that it is more rapid and involves a less conspicuous posture by the female than that occurring in Boreus species (Aubrook 1939). The spindle-shaped eggs are laid singly and are cemented by their sides to the bryophyte leaf. Both in culture and in the field, the eggs were usually attached to the ventral surface of liverwort leaves. Especially in the case of eggs deposition on Porella navicularis, the eggs are frequently inserted between two overlapping leaves, and the egg is sometimes cemented to both leaves in this position. Both in Porella and Scapania bolanderi, where the eggs are usually within the leaf overlap, but adherent only to the underside of the upper leaf, the leaves are sufficiently close and rigid to necessitate considerable extension of membranous segments IX–XI of the female Caurinus dectes for insertion of the egg. Eggs were invariably deposited on bryophytes, usually on leafy liverworts, but occasionally also on mosses. One egg was found in the field on the upper surface of the thallus of Conocephaluri conicum (Marchantiales). The placement of the eggs is normally on leaves of the host liverworts, and adult feeding is usually found on the same shoot. Eggs were also found deposited on moss shoots in the field, but these were always intermingled with liverwort hosts. Although several hundred eggs were obtained in culture (Russell 1979a), and many more from the field, very few have hatched in culture. The hatching process was not observed and the following account is based on observation of many eggs recovered from field samples of liverworts. The opening of eggs by hatching larvae is very different from Boreus and Hesperoboreus. The egg is slit in a neat longitudinal line on the surface directly opposite the cemented surface. This straight slit extends nearly the entire length of the egg and is not widened or frayed at any point. It is unknown whether the chorion is cut along its length or if there is a line of weakness to facilitate hatching. The hatching larva probably cut through the chorion with the very fine, serrate ridge on the frons, which appears to be an eggburster. The chorion is not eaten by the larvae. The eggshell

2.3 Morphology of adults 

 97

retains its normal shape and it is often difficult to distinguish hatched from unhatched eggs without manipulation. Romano Dallai, Loren K. Russell & Rolf G. Beutel

2.3.8 Spermatophore and spermatozoa The spermatozoa of Caurinus dectes were described for the first time by Russell (1979a) and in more detail using transmission electron microscopy (TEM) and other techniques by Russell et al. (2013). For the more recent study, sperm was obtained from males collected in late January and early February 2013, at the type locality for the species on the northeast ridge of Mary’s Peak, 22 km west of Corvallis Oregon, at 650 m elevation. The adults were collected from host liverworts (Scapania bolanderi) growing on the bark of large conifers and on large stumps and fallen logs. Unlike in the pistilliferan groups of Mecoptera, males of Caurinus and Boreinae produce sperm packages. The spermatophores of Caurinus dectes are probably mostly formed by a highly refractive, light blue material produced in the large lumen of the main lobe of the accessory gland. This substance hardens soon after the exposure to air or fixatives (Russell 1979a). The sperm package is a sausage-shaped, hardened gelatinous structure. A bent, finger-like appendage is present at its apex. The main structure is 0.55 × 0.20 mm large and the apical appendage 0.12 mm long. The outer walls are transparent and unpigmented, while much of the internal volume is occupied by two lateral chambers of granular, gray material. An opaque white channel extending to an orifice on the apical appendage is possibly continuous with the two granular chambers, but confirmation is required (Russell 1979a). It was observed by Russell (1979a) that the spermatophore was retained within the male aedeagus until after the pair separated and that only the apical appendage protruded from the everted intromittent organ after copulation was terminated. The spermatozoa are filiform and about 0.9 mm long. Ultrastructural TEM observations revealed a strongly electron-dense cytoplasm obscuring the appearance of all major sperm components. However, cysts occur within the testes with electron-transparent spermatozoa. Within the sperm cysts, scattered electron-transparent spermatozoa can be intermingled with those showing the dense condition. The transparent spermatozoa were used for characterizing the sperm organelles in Russell et al. (2013). The sperm head contains an apical conical acrosome vesicle that is approximately 1 µm long (Fig. 2.3.8.1 A). This is intersected by an axial subacrosomal perforatorium, which extends longitudinally into the anterior

98 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

axo

*

ac

*

nu

ac

A

cam

ac

mid

B

C gly axo

gly lam

mid

mid lam

mid

D

cam

nu

nu

nu

gly

mid

E

gly

F

axo

mid axo

G

2.3 Morphology of adults 



nuclear region over a short distance. The nucleus is elongated and cylindrical, with a diameter of ca. 0.3 µm (Fig. 2.3.8.1 A,B), and a compact electron-dense content. Two opposite lateral shallow infoldings of the nuclear envelope extend along the entire nuclear length. Two crescent-shaped masses of dense centriole adjunct material in the anteriormost part of the flagellum embrace an axoneme with a simple 9 + 2 microtubular pattern and a single large mitochondrial derivative (Fig. 2.3.8.1 C,D,G). Beneath this region, extra-axonemal accessory structures and two mitochondrial derivatives extend along the flagellum. Microtubule doublets of the axoneme bear inner and outer dynein arms and radial spokes, and a central complex is also present. Extra-axonemal accessory structures are present as two electron-dense fibers, ca. 12 nm thick, located on the two opposite lateral sides of the flagellum close to the plasma membrane. Each of them is embedded in a small triangular cluster of material originating from the centriole adjunct. A smaller spot of the same material is often visible in the central region of the flagellum, just beneath the axoneme. In cross section, the two mitochondrial derivatives appear relatively small and equal in size, ca. 0.1 µm in diameter. Longitudinally arranged cristae are present in their peripheral region, with a regular repeat of ca. 45–50 nm, whereas the central region appears distinctly crystallized. Cross sections of the flagellum show a peculiar glycocalyx surrounding the plasma membrane (Fig. 2.3.8.1 D–F), consisting of a series of longitudinal electron-dense ridges projecting from the cell membrane over a distance of ca. 10–15 nm. Each ridge is separated from the adjacent ones by a distance of ca. 15–18 nm. In the posterior portion of the flagellum, the sperm components change their configuration abruptly. A cross section at this level shows the presence of only a single small mitochondrial derivative and a disorganized axonemal structure (Fig. 2.3.8.1 E,F). A dense spot associated with a microtubule doublet is present on both sides of the mitochondrial

 99

derivative. Beneath this structure, two dense laminae of ca. 20 nm thickness are visible (Fig. 2.3.8.1 E,F), each of them carrying a microtubule doublet at their lateral extremities. Additionally, a complex of two microtubule doublets along with a small amount of electron-dense material is visible at the opposite side of the flagellar section. Posterior to this region, the flagellum narrows to a diameter of only 0.1 µm. At this level, the mitochondrial derivative becomes increasingly smaller and an axial cylindrical structure appears. Cross sections processed with the method of Thiéry (1967) revealed that this cylindrical structure at the end of the flagellum appears electron-dense, while glycogen granules were detected in the cytoplasm of the cells of the testes wall (Russell et al. 2013). In the anterior region of the flagellum, no positive reaction was observed, except for the outer leaflet of the plasma membrane. Loren K. Russell & Rolf G. Beutel

2.3.9 Organ systems (mainly based on Russell 1979a)

2.3.9.1 The digestive system and associated organs The salivary glands of Caurinus dectes are simpler in structure compared to those of other mecopterans (Potter 1938). The short common salivary duct opens on the anterior labio-hypopharyngeal surface. It extends from the flattened salivarium almost to the cervical region, where it divides into two lateral ducts placed to either side of the oesophagus (Fig. 2.3.9.1). The distal part of the common duct is characterized by an unusual intrinsic muscle, the secretion former (Fig. 2.3.1.3 D: 37). This compact muscle is also present in Boreinae and Pistillifera (Section 3.3.1), but missing in Nannochoristidae, where instead the usual three salivary muscles (with areas of origin on the hypopharynx and prementum) are present

◂ Fig. 2.3.8.1: Caurinus dectes, sperm ultrastructure, TEM. A, Longitudinal section of the apical sperm region showing acrosome with inner

subacrosomal perforatorium (asterisk); B, cross section of the apical sperm region showing two opposite shallow infoldings of nuclear envelope (arrowheads). Cross sections of acrosome with inner subacrosomal perforatorium (asterisk); C, cross section of proximal region of sperm flagellum showing simple 9 + 2 axoneme, a mitochondrial derivative with crystallized inner content, and two conspicuous dense structures of centriole adjunct material. Note also glycocalyx surrounding the plasma membrane and consisting of series of longitudinal ridges projecting from the plasma membrane; D, cross section of sperm flagellum showing simple 9 + 2 axoneme with two equally sized mitochondrial derivatives; two dense fibers (arrows) and two dense assemblages of centriole adjunct material (arrowheads) visible beneath axoneme (on both flagellar sides); E, F, cross sections of sperm flagellar end, showing disorganization of sperm components; single mitochondrial derivative; few microtubular doublets of axoneme visible, interconnected by dense laminae; glycocalyx still present; G, longitudinal section of sperm flagellum showing axoneme and two mitochondrial derivatives exhibiting regular repeat of inner mitochondrial membrane. Abbreviations: ac – acrosome, axo – axoneme, cam – centriole adjunct material, gly – glycocalyx, lam – laminae, mid – mitochondrial derivate, nu – nucleus. Scale bars: A, B, 0.2 µm; C–F, 0.1 µm; G: 0.5 µm.

100 

oes

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

prv

mg

hg

salg

Mtub

re

Fig. 2.3.9.1: Caurinus dectes, female, alimentary tract with salivary glands and Malpighian tubules. Abbreviations: hg – hindgut, mg – midgut, Mtub – Malpighian tubule, oes – oesophagus, prv – proventriculus, re – rectum, salg – salivary gland. Redrawn from Russell (1979a).

(Section 1.3.1; Beutel & Baum 2008, Beutel et al. 2008). The paired ducts reach abdominal segment II posteriorly, where each divides into three glandular branches. Two branches continue caudad along the lateral wall of the midgut. The dorsal branch of the salivary gland is recurved anteriorly into the thorax and lies alongside the salivary duct. The salivary glands of Caurinus are relatively shorter and thicker than those of Boreus hyemalis and also differ in their irregular branching, the apparent lack of a reservoir on each lateral duct, and the shorter common duct. There is no apparent sexual dimorphism, as occurs in Panorpidae (Mercier 1915). The anterior precerebral part of the pharynx (see Section 2.3.1 for details) of C. dectes is characterized by a large pumping chamber reinforced by a sclerotized clasp (Beutel et al. 2008). The posterior pharynx is narrow. A postcerebral pumping chamber as it is present in Nanno­choristidae, most dipterans, and fleas (Beutel & Baum 2008, Schneeberg & Beutel 2014) is missing. The oesophagus extends from the cervical region to the posterior thorax. It is narrow (external diameter ca. 0.4 mm), approximately round in cross section, and elongate, without forming an extended ingluvies. The proventriculus, located in the metathorax and abdominal segment I, is a rounded, caudally truncated cone, 0.17 mm wide and 0.15 mm long. The walls are thick and muscular, and the interior surface is densely lined with fine cuticular acanthae (Richards & Richards 1969). These spines form an unusual filtration valve which is found in all families of Pistillifera (Hepburn 1969). The shape of the acanthae in C. dectes basically conforms to the type found in three species of Boreus (Hepburn 1969), even though without a distribution of meso- and endocuticle characteristic for Boreinae (Russell 1979a). The proventriculus is joined to the short, broad, and sac-shaped midgut through the

five-lobed cardiac valve, which extends caudally into the midgut lumen. The external surface of the midgut wall has a distinct irregular polygonal pattern formed by a network of pale lines, with a diameter of meshes of ca. 0.1 to 0.15 mm. In males, the midgut, when engorged, is almost spherical (about 0.65 mm in diameter) and occupies most of the anterior half of the abdominal cavity. The midgut of females is usually more elongate, with dimensions ranging from 0.4 mm × 0.6 mm when nearly empty to 0.65 mm × 0.9 mm in a distended condition. The midgut epithelium is a layer of large, cuboidal cells, arranged in a hexagonal pattern. Crypts of regenerative epithelial cells, which are numerous in the midgut of Panorpa communis (Grell 1938), were not observed in C. dectes (Russell 1979a). Regenerative cells were found in a ventral fold near the pyloric valve (Russell 1979a). The musculature of the midgut is principally composed of transverse and oblique fibers. A peritrophic membrane is absent, as in other examined species of Mecoptera (Hepburn 1969). A few cell wall fragments were found in the fluid midgut contents of one specimen of C. dectes, which had fed on the yellow-ladle liverwort Scapania bolanderi. Other specimens that had fed on liverworts had fluid or semisolid gut contents composed entirely of cell contents. Hepburn (1969) reported that Mecoptera form a solidly packed food bolus in the midgut, except for Nannochoristidae, which have reduced mouthparts (Beutel & Baum 2008) and are unable to consume solid food as adults. Such boli were not found in C. dectes (Russell 1979a). The narrow, cylindrical hindgut (proctodaeum) is very clearly separated from the entodermal sac-like midgut. Short, lamellar structures project from the pyloric attachment into the midgut. Even though these resemble a valvular structure, it is uncertain whether the lumen is continuous from midgut to hindgut (Russell 1979a). The pyloric region is short and slightly enlarged where the six Malpighian tubules open into the gut (Fig. 2.3.9.1). The distal ends of the tubules lie along the rectum, and a loop of each of them reaches anteriorly along the posterior wall of the midgut. The color of the Malpighian tubules is reddish-brown for most of their length, but they are unpigmented near their point of origin. The regions of the hindgut are only weakly differentiated. The ilium, about 0.6 mm long, is very narrow (0.3–0.4 mm). The transition to the rectum is marked only by a noticeable increase in diameter (to 0.5 mm–0.7 mm). The rectal glands, which are characteristic of all previously investigated Mecoptera except Boreus, are also absent in C. dectes (Russell 1979a). The entire hindgut is about 1.5 mm long, coiled about twice, and placed with the Malpighian tubules against the dorsal midgut surface. A short

2.4 Morphology of larvae 



terminal section is slightly narrowed as it nears the anus. The solid material in the hindgut resembles the contents of the Malpighian tubules and may be exclusively composed of them (Russell 1979a). Since very little solid, indigestible material reaches the midgut of the adults, there would be little fecal material whether the pyloric connection is, or is not, functional. Any solid substrates entering the gut could be removed by “back-flushing” with selective filtering through the proventriculus, and the production of green stains on the substrate by feeding adults apparently indicates frequent regurgitation (Russell 1979a). The mechanism for the elimination of large quantities of clear liquid from the anus cannot be specified on structural grounds. It can be assumed that the Malpighian tubules, or the hindgut, or both regulate the composition of the hemolymph by production of hypotonic urine, when excess water enters the midgut (Russell 1979a).

2.3.9.2 The nervous system The brain and ventral nerve cord are similar in form to that described for Boreus hyemalis (Potter 1938). The transverse brain is large in relation to the head size (see Section 2.3.1; Beutel & Baum 2008), with well-developed optic lobes and inconspicuous antennal lobes. Together with the large and rather elongate suboesophageal complex, it forms a compact mass around the pharynx, with short and broad circumoesophageal connectives like in other groups of Antliophora (e.g. Beutel & Baum 2008, Schneeberg & Beutel 2010, 2014). The connectives between the suboesophageal and prothoracic ganglia and between the abdominal ganglia are closely appressed and appear fused. The three thoracic ganglia are large and nearly coalesced, especially those of the pterothorax. There are six separate abdominal ganglia in female C. dectes, the first five of equal size, while the sixth (likely equivalent with ganglia VI–VIII) is about twice the size of the others. The first abdominal ganglion is separated from the metathoracic ganglion only by a constriction. The remaining connectives are distinct, but short. In males, the large last abdominal ganglion is teardrop shaped rather than oval and almost fused to the preceding ganglion. The number of separate abdominal ganglia is seven (like in in both sexes of B. hyemalis and most males of Pistillifera) or six in the male. The shortening and fusion of the connectives make the ganglionic chain of Caurinus more concentrated than in any other known mecopterans. This is likely due to the very compact body shape and especially to the very short thorax. Information on the stomadaeal sympathetic nervous system is

 101

scarce, but a well-developed, typical frontal ganglion was described in Beutel et al. 2008) (see Section 2.3.1).

Rolf G. Beutel, Benjamin Fabian, Hans Pohl & Frank Friedrich

2.4 Morphology of larvae

The entire body (Fig. 2.4.1.1 A) of the curculioniform larva (Russell 1979a) is slightly curved in lateral view and has an elongate-ellipsoid shape seen from above, with the largest diameter at the region of the metathorax and abdominal segment I. The posterior abdominal segments are moderately tapering. The average length of stretched third (final) instar larvae is about 2 mm. The cuticle of the head capsule is light brown, whereas the coloration of the rest of the body is whitish or light gray. The postcephalic body is characterized by large oblique and nearly vertical folds, an unsclerotized cuticle with a tuberculate or wart-like surface structure, greatly reduced thoracic legs, and missing abdominal appendages. The postcephalic segments are distinctly separated from each other, even though the segmental pattern appears somewhat obscured by the folds.

2.4.1 Head (mainly based on Russell 1979a and Fabian et al. 2015) 2.4.1.1 Head capsule The sclerotized orthognathous head is almost completely exposed, only a very short posterodorsal region covered by the dorsal cervical membrane (Fig. 2.4.1.1 A; Russell 1979a: figs. 28 and 29). The head capsule is nearly round in the frontal view (Figs. 2.4.1.2 A and 2.4.1.4) and appears oval in the lateral, ventral, and dorsal views (Figs. 2.4.1.2 B and 2.4.1.3 A). A distinct triangular incision in the dorsolateral cephalic region is anteriorly continuous with a relatively short and indistinct occipital furrow. The cuticle is largely smooth and glabrous; a honeycomb-like surface pattern with pentagonal and hexagonal fields is present on the genal area above the field of stemmata (Fig. 2.4.1.1 A); it is still recognizable in adjacent dorsal and ventral areas but obliterates toward the frontal and occipital regions. The coronal and frontal ecdysial sutures (epicranial sutures) are distinctly recognizable (Fig. 2.4.1.2 A). The coronal suture divides the vertex medially and is almost half as long as the dorsal head capsule. The paired frontal sutures originate from it below the AF2 setae (Fig. 2.4.1.2 A); they extend laterad from their origin but

102 

A

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

2

1

6D 6C 6E 6B 6A

3

I

IV

III

II

V

VI

VII VIII

stef

IX X

ant lbr

mx

md

steI fr

cly

ciam

ant

lbr md

ciam

md

lap

cly

cd/bst dst

dst

B

lbr

mxp

C

mxp

cd/bst

mtf lap

Fig. 2.4.1.1: Caurinus dectes, larva, SEM. A, Entire larva, lateral view, postcephalic segmental borders indicated by dotted lines (1–3, thoracic segments; I–X, abdominal segments; 6A–E indicate planes of histological sections in Fig. 2.4.1.6); B, detail of mouthparts, lateral view; C, detail of mouthparts, ventral view. Abbreviations: ant – antenna, ciam – circum-antennal membrane, cd/bst – unseparated cardo and basistipes, cly – clypeus, dst – dististipes, fr – frons, lap – labial palp, lbr – labrum, md – mandible, mtf – field of microtrichia on dististipes, mx – maxilla, mxp – maxillary palp, stef – field of stemmata, steI – stemma I. Scale bars: A, 200 µm; B, C, 20 µm. Modified from Fabian et al. (2015).

turn anterad after a short distance, with an almost right angle between the two sections. The slightly irregular anterior part reaches the level of the dorsal margin of the antennal foramen. The fronto-clypeal ridge (transverse strengthening ridge) is present but weakly developed. The clypeus is distinctly broader than long (Fig. 2.4.1.2 A), with the anteclypeus distinctly separated from the broader postclypeus by a transverse furrow; a small bulge is present at the ventral clypeal edge. A gula and a hypo­ stomal bridge are missing. Cervical sclerites are present. Setation (Fig. 2.4.1.2) The denomination of the setae (labeled with capital letters and Roman numbers in Fig. 2.4.1.2) is based on the topological position and the nomenclature introduced for lepidopteran caterpillars based on the innervation by Hasenfuss & Kristensen (2003) (information on the innervation is not available for Caurinus).

Twenty-eight pairs of cranial setae are present (Fig. 2.4.1.2), all of them short (15–25 µm in 2 mm larvae; Russell 1979a) and not cleft. Three pairs insert in a short row parallel to the coronal suture on the dorsal region of the head capsule (D1–3). D1 and D2 are closer to each other than D2 and D3. Three additional pairs are arranged along a virtual line continuous with this row (AF1, AF2, and F): AF1 is inserted at the level of the dorsal margin of the field of stemmata, AF2 at the ventral end of the coronal suture, and F (frontal seta) at the level of the antennae. A small and strongly curved setae A1 inserts at the ventral margin of antennomere 1. S1 is located within the field of stemmata, between stemmata I and VII; an additional pair (S2) is present at the dorsal margin of the field of stemmata and two other setae (SS1 and SS2) posterior to it, close to the hind margin of the head. Two pairs of parietal setae (P1 and P2) insert posterior to the angle of the frontal

2.4 Morphology of larvae 



suture on the dorsal genal region, and a lateral seta (L), on the posterior genal area posterodorsad the posterior stemma of the upper row (VII). Three pairs are present on the postclypeus (C1–3): C1 is laterally inserted on the ventrolateral clypeal bulge, whereas C2 and C3, close to

A

D1 cs AFb AF2 fs

P1 Pa

AFa

ge

P2

AF1

fr

S2

Lb

Sb

L

Fa

stef

F

ant

cly Ca

ciam

S1

A C3 C2 Cb

SSb

C1

lbr

md

Sa

ML2

mx

mxp

ML1

B

D1

D2

M3

SS2 SS1 M2

M1

D3

AF2

fs

Lc

P2

P1

Lb

Pa AFa

Sb

IV

Fa F

Ca C3 C2

VI

V

III

II

A

SS2

Sa S1 SSc I SSb SSa

SS1

ML2

C1 lbr

C

2.4.1.2 Tentorium

La

VII

M2 M1 Cb

mxp

SSd ML4 ML3 M3

ML1 MXL

Oc Ob Oa cd/bst

ML5 ML3 lap MLg md dst MLf M1 MLd ML2 MLc ML1 MLb MLa ML7 ML6 MLh

the central clypeal region. Three setae on the mandibles (M1–3) are arranged in a triangle. Seven pairs are present on the maxillae (ML1–7): ML3 and ML4 insert ventrolaterally on the basal maxillary sclerite (cardo + basistipes) and ML5 ventrally, ML2 inserts on the posterior part of the dististipes and ML1 on palpomere 1, and ML6 and ML7 are placed in the field of microtrichia on the ventral surface of the dististipes. One pair of setae (MXL) is located ventrally on the membranous area adjacent to the labial palps. Small punctured grooves (labeled with small and capital letters according to their position) are distributed on the head capsule and the mouthparts. They probably also have a sensory function as suggested for similar structures of lepidopteran larvae (Hasenfuss & Kristensen 2003). Punctures Fa and AFa are located dorsomediad the setae F and AF1, respectively, and Pa ventrad P1. Sa lies within the field of stemmata and Sb anterior to it. Four punctures (SSa–d) are distributed around setae SS1. La–c are arranged in a curved row on the posterior genal region, with the seta L inserted between La and Lb. Two punctures Ca and Cb are present on the anteclypeus. Oa–c are arranged in a short line posterodorsad the SS2 setae. Nine pairs (MLa–i) are visible on the ventral side of the maxilla: MLa and MLb are inserted ventrally on palpomere 2, and MLc and MLd, ventrolaterally on the apical membrane of palpomere 1, and adjacent to them MLe on the ventral side of the basal palpomere; MLf is placed laterad ML2, and MLg, within the field of microtrichia on the dististipes; MLh and MLi are arranged in an arcuate series with setae ML3 and ML5.

L

S2

AF1

 103

MLi

S1 SS2 SS1 ML4 M3 M2

The well-developed sclerotized anterior tentorial arms (Fig. 2.4.1.5 A) lack a recognizable lumen (Fig. 2.4.1.6 A,B); they are oval in cross section and distally continuous

◂ Fig. 2.4.1.2: C. dectes, larva, head, chaetotaxy. A, Frontal view;

B, lateral view; C, mouthparts, posterior view. Dotted areas indicate membranous regions. Setae labeled with capital letters or capital letters + numbers, and punctures are labeled with capital letters combined with small letters; I-VII – stemmata. Abbreviations: A – antennal, AF – adfrontal, ant – antenna, C – clypeal, cd/ bst – unseparated cardo and basistipes, ciam – circum-antennal membrane, cly – clypeus, cs – coronal suture, D – dorsal, dst – dististipes, F – frontal, fr – frons, fs – frontal suture, ge – gena, L – lateral, lap – labial palp, lbr – labrum, M – mandibular, md – mandible, ML – maxillary, mx – maxilla, MXL – maxillolabial, mxp – maxillary palp, O – occipital, P – parietal, S – stemmatal, stef – field of stemmata, SS – substemmatal. Scale bar: 50 µm. Modified from Fabian et al. (2015).

104 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

with the mesal rim of the antennal foramen. Externally recognizable anterior tentorial pits are missing (Fig. 2.4.1.1 B). Very thin dorsal arms are attached to the dorsal head capsule by connective tissue (Figs. 2.4.1.3 B, 2.4.1.4, 2.4.1.5 A, and 2.4.1.6 A,B). The tentorial bridge above the maxillolabial complex is massively developed (Figs. 2.4.1.3 C, 2.4.1.5 A, and 2.4.1.6 E); the bases of the anterior tentorial arms form a discrete plate-like corpotentorium (Figs. 2.4.1.5 B and 2.4.1.6 C,D). The posterior arms are short and stout.

2.4.1.3 Eyes Compound eyes and ocelli are missing. A field of welldeveloped stemmata is present laterally above and posterior to the antennal foramen (Figs. 2.4.1.1 A, 2.4.1.2 B,C, 2.4.1.3 A,B, and 2.4.1.4); it appears black due to pigmentation below the cuticle. Seven corneal lenses are recognizable externally (Figs. 2.4.1.2 A and 2.4.1.3 A,B). Four anterior stemmata (SI–SIV) form a rather straight line behind the antennal articulatory area, and the posterior three (SV– SVII) form a shortened semicircle above and posterior to the anterior row. The distances between the stemmata are similar within the two groups (4–5.6 µm), and the shape of the cornea lenses varies from almost circular to slightly oval and the diameter is between 14.4 µm and 19.2 µm.

2.4.1.4 Labrum An internal membranous fold connects the welldeveloped, roughly rectangular labrum with the ventral clypeal margin (Fig. 2.4.1.1 C); it is about half as long as wide, with a basal width of ca. 80 µm (Figs. 2.4.1.1 B,C, 2.4.1.2 B,C, and 2.4.1.3 B). The basal margin is slightly concave and the distal margin medially incised (Fig. 2.4.1.3 B). Paired fields of more than 20 setae are present laterad the incision (Figs. 2.4.1.1 C, 2.4.1.2 A, and 2.4.1.3 B). The labral setae are distinctly longer than those of the head capsule (ca. 19 µm). Musculature (Figs. 2.4.1.3 B, 2.4.1.4, and 2.4.1.5 B): M. labroepipharyngalis (M.7, nomenclature of von Kéler 1963): compact, O (=origin): posteromesal labral region, I (=insertion): distal epipharynx. M. frontolabralis (M.8): well-developed, O: centrally on frons (ventrad M.46), I: median process of dorsal labral margin.

2.4.1.5 Antennae Short, two-segmented antennae (Figs. 2.4.1.1 A,B, 2.4.1.2 A,B, and 2.4.1.3 B) are inserted in a wide antennal foramen

on a nearly round articulatory membrane (Figs. 2.4.1.1 B and 2.4.1.2 A,B) anterior and below the oblique lower row of stemmata and above the anterior mandibular articulation. The extremely short cylinder-shaped antennomere 1 is ca. 6.6  µm long. Three circular to slightly oval discshaped placoid sensilla (diameter ca. 7.5 µm) are inserted on the ventromesal half of its distal surface. The cylindrical antennomere 2 is longer and has only about one third of the diameter of antennomere 1; it tapers toward its apex and bears sensilla on its distal part (Russell 1982: peg-like sensilla). Two longitudinal membranous areas were described by Russell (1982); large apical setae are missing. Musculature: the single antennal muscle (Figs. 2.4.1.4, 2.4.1.5 A, and 2.4.1.6 A), presumably M. tentorioscapalis anterior (M.1?), originates laterally on the proximal half of the anterior tentorial arm and inserts ventromesally on the antennal base.

2.4.1.6 Mandibles The mandibles are covered by the labrum in their resting position. The posterior (primary) and anterior (secondary) joints are well-developed (Figs. 2.4.1.1 B, 2.4.1.2 B, and 2.4.1.3 A). Four distal teeth increase in size toward the apex. A prostheca is not present. The base is broadened but a typical mola with a grinding surface is missing. Setation: Three setae are inserted on the lateral mandibular surface (Fig. 2.4.1.2 A,B). Musculature (Figs. 2.4.1.3 A,B, 2.4.1.4, 2.4.1.5 B, 2.4.1.6 B–E): M. craniomandibularis internus (M.11): largest cephalic muscle filling out about 60% of the lumen of the head, O: dorsal and dorsolateral walls of head capsule, I: mesal rim of the mandible with strongly developed adductor tendon. M. craniomandibularis externus (M.12): about 10% of the volume of M.11, O: lateral wall of the head capsule, I: lateral mandibular margin with a tendon. M. tentoriomandibularis (M.13): extremely thin, composed of few fibers, accompanied by the mandibular nerve, O: anterior tentorial arm, adjacent to the tentorio-antennal muscle, I: posteriorly on the mandibular base.

2.4.1.7 Maxillolabial complex A large transverse basal maxillary sclerite, formed by the completely fused cardo and basistipes, articulates laterally with the postgenal region (Fig. 2.4.1.3 C). Its dorsal margin is strengthened, whereas the anterolateral areas are rather thin. The dorsal margin continues

2.4 Morphology of larvae 



A 12

stef mx

ant

mxp

md

cs

11

fs

B

br

C

tb 11

ph

54

12 dta stef ant 43 md cly

7 mxp

lbr

46 8 45 1? sald pmt hyrd

17 cd/bst dst lap

mxp

mtf md

 105

Fig. 2.4.1.3: C. dectes, larva, CLSM (autofluorescence). A, Entire larva, lateral view; B, head, anterior view; C, ventral half of the head, posterior view. Abbreviations: ant – antenna, br – brain, cd/bst – unseparated cardo and basistipes, cly – clypeus, cs – coronal suture, dst – dististipes, dta – dorsal tentorial arm, fs – frontal suture, hyrd – posterior rods of hypopharynx, lap – labial palp, lbr – labrum, md – mandible, mtf – field of microtrichia on dististipes, mx – maxilla, mxp – maxillary palp, ph – pharynx, pmt – prementum, stef – field of stemmata, sald – salivary duct, tb – tentorial bridge, 1? – M. tentorioscapalis, 7 – M. labroepipharyngalis, 8 – M. frontolabralis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 17 – M. tentoriocardinalis, 43 – M. clypeoepipharyngalis, 45 – M. frontopharyngalis anterior, 46 – M. frontopharyngalis posterior, 54 – M. craniopharyngalis ventralis. Scale bars: A, 100 µm; B, C, 50 µm. Modified from Fabian et al. (2015).

11 8

46 br dta

45

12 fg

44 1?

43

onp

steI

ant

cly md

13 abt 7

pmj 22

18

sald

mxp

lbr

mx

Fig. 2.4.1.4: C. dectes, larva, head, 3D reconstruction based on histological sections (skeleton – blue, stemmata – light blue, musculature – orange, nervous system – yellow, digestive tract – green, salivary duct – pink), anterior view, skeleton of left half semitransparent. Abbreviations: abt – abductor tendon of mandible, ant – antenna, br – brain, cly – clypeus, dta – dorsal tentorial arm, fg – frontal ganglion, lbr – labrum, md – mandible, mx – maxilla, mxp – maxillary palp, onp – optic neuropils, pmj – primary mandibular joint, sald – salivary duct, steI – stemma I, 1? – M. tentorioscapalis, 7 – M. labroepipharyngalis, 8 – M. frontolabralis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 13 – M. tentoriomandibularis, 18 – M. tentoriostipitalis, 22 – M. basistipitodististipitalis lateralis, 43 – M. clypeoepipharyngalis, 44 – M. clypeocibarialis, 45 – M. frontopharyngalis anterior, 46 – M. frontopharyngalis posterior. Scale bar: 50 µm. Modified from Fabian et al. (2015).

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ventromesally and forms an anteriorly directed rod-like extension (Figs. 2.4.1.3 C and 2.4.1.6 C–E), which runs along the inner rim of the maxilla into the endite lobe (Fig. 2.4.1.6 B: mxl); the basal sclerite is connected with the posterior part of the dististipes, which bears the distal maxillary elements; its mesal part is weakly sclerotized and covered with dense fields of microtrichia (Figs. 2.4.1.1 C and 2.4.1.3 C). The palp is short and two-segmented; the broad and short palpomere 1 bears a round sensorium on its distal part, laterad of palpomere 2 (Fig. 2.4.1.3 C), which is slightly longer and less wide. The apical area of palpomere 2 also bears a round sensorium laterally. Ten small sensilla on the mesal side are similar to the apical sensilla of antennomere 2. A pair of small endite lobes is present between the mandibles and hypopharyngeal lobe (visible on histological sections) (Fig. 2.4.1.6 B). The homology is uncertain as no muscles are attached. The distinctly reduced labial elements are mainly formed by an undivided and unsclerotized triangular area mesad the maxillary bases (Figs. 2.4.1.2 C, 2.4.1.3 C, and 2.4.1.3 6 D,E); it is posteriorly not distinctly delimited from the neck membrane. The anterior premental region bears the vestigial palps, the only distinctly sclerotized labial parts; they are composed of an indistinct basal part and a small, rounded single palpomere with sensilla of different shapes and sizes (Figs. 2.4.1.2 C and 2.4.1.3 C). The premental area anterad the palps is a narrow stripe between the maxillae and largely covered by them (only recognizable on histological sections) (Fig. 2.4.1.6 D); this membranous region is laterally flanked by a pair of long, well-sclerotized rods (Fig. 2.4.1.6 D,E), which originate from the posterior end of the main hypopharyngeal element, which bears the opening of the salivary duct and reaches posterad the level of the labial palps. Musculature (Figs. 2.4.1.3 C, 2.4.1.4, and 2.4.1.6 D,E): M. tentoriocardinalis(-basistipitalis) (M.17): two parallel, closely adjacent bundles, O: posterior tentorial arm, I: posterolaterally on basal maxillary sclerite. M. tentorio­ stipitalis (M.18): two parallel, closely adjacent bundles, O: corpotentorium and base of the anterior tentorial arm, I: posteriorly on the mesal edge of the basal sclerite. M. craniolacinialis (M.19): well-developed, I: head capsule below M. craniomandibularis internus and close to the posterior tentorial grooves, I: mesal endite lobe with a thin tendon. M. basistipitodististipitalis lateralis (M.22): O: lateral half of basal sclerite, I: laterally on dististipes. Mm. tentoriopraementales inferior/superior (M.29/30): probably absent (see. M.42). Intrinsic labial muscles absent.

2.4.1.8 Preoral cavity and mouth opening The dorsoventrally compressed preoral cavity is laterally bordered by the mandibular bases. The semimembranous epipharynx forms the roof. Only the insertion sites of the frontal and labral muscles are slightly sclerotized. The inner epipharyngeal surface is smooth without any microtrichia. The hypopharyngeal sclerite is ventrally fused with the anterior labial region forming a slender prelabio-hypopharyngeal lobe, which appears triangular in cross section (Figs. 2.4.1.5 B and 2.4.1.6 B,C). The proximal epipharynx and hypopharynx fuse along their lateral edges, thus forming a short prepharyngeal tube (Fig. 2.4.1.5 B) with a very narrow lumen. The border to the pharynx (anatomical mouth) is indistinct but marked by the position of the frontal ganglion. A sclerotized hypopharyngeal suspensorium (oral arms) was not visible in histological sections. Musculature (Figs. 2.4.1.3 B, 2.4.1.4, 2.4.1.5, and 2.4.1.6 A,C,E): M. tentoriohypopharyngalis (M.42): slender, O: posterior tentorial arm, I: posterior end of the prelabiohypopharyngeal lobe, close to the base of the labial palp. M. clypeoepipharyngalis (M.43): three slender, closely arranged bundles, O: posterior half of the clypeus, below the clypeofrontal ridge, I: mesally on the epipharynx. M. clypeocibarialis (M.44): slender, O: ventral (clypeal) face of the clypeofrontal ridge, above M.43, I: anatomical mouth opening (below frontal ganglion, opposite to insertion of M.48). M. tentoriocibarialis (M.48): slender, O: centrally on the ventral side of the corpotentorium (between paired attachment sites of M.18), I: ventral side of the cibarium (opposite to M.44).

2.4.1.9 Pharynx The lumen of the precerebral pharynx is narrow but widens below the central part of the brain (Fig. 2.4.1.5 B); folds for attachment of dilators are present in this area (Fig. 2.4.1.6 B–E). Muscles of precerebral pharynx (Figs. 2.4.1.3 B, 2.4.1.4, 2.4.1.5, and 2.4.1.6 A): M. frontopharyngalis anterior (M.45): moderately sized, O: frons above clypeofrontal ridge, I: dorsally on the precerebral pharynx (above the frontal ganglion). M. frontopharyngalis posterior (M.46): subdivided into two main sections, O: frons (dorsolaterad M.8), I: dorsally on the precerebral pharynx (anterior part close to M.47, posterior part between the circumoesophageal connectives). M. tentoriopharyngalis lateralis (M.47?): slender, O: anterior tentorial arm, close to the anterior tentorial pit, I: laterally on the precerebral

2.4 Morphology of larvae 



pharynx (laterad M.45). M. tentoriopharyngalis anterior (M.50): O: mesally on the anterior margin of the corpotentorium and proximally on the anterior tentorial arms, I: ventrally on the precerebral pharynx (opposite to M.45). Muscles of postcerebral pharynx (Figs. 2.4.1.3 C, 2.4.1.5, and 2.4.1.6 B–E): M. verticopharyngalis anterior (M.51): two subcomponents, O: wall of the head capsule, between the antero-mesal bundles of M.11, I: dorsolaterally on the anterior postcerebral pharynx (opposite M.52). M. tentoriopharyngalis posterior (M.52): composed of two main portions, M.52a: two very short, parallel bundles, O: anterior tentorial arm and base of the dorsal tentorial arm (Fig. 2.4.1.6 B), I: laterally on the pharynx (between the posterior bundle of M.46 and anterior bundle of M.51), M.52b: strongly developed, O: posterior tentorial arms, I: ventrolaterally on the postcerebral pharynx (opposite to M.51). M. craniopharyngalis posterior (M.53): O: cranium, between the posteriormost bundles of M.11, I: dorsolaterally on the posterior region of the postcerebral pharynx (opposite M.52). M. craniopharyngalis ventralis (M.54): two strong branches, O: cranial regions close to the base of the posterior tentorial arms, I: ventrolaterally on the postcerebral pharynx (behind M.52b, opposite to M.53).

2.4.1.10 Salivary system

suboesophageal ganglion (Fig. 2.4.1.5 B). The thin-walled unpaired anterior duct runs toward the tip of the hypopharyngo-labial lobe (Figs. 2.4.1.3 C, 2.4.1.5 B, and 2.4.1.6 B–E). The U-shaped floor of the duct is well-sclerotized close to the salivary orifice, whereas the roof is mostly membranous (Fig. 2.4.1.6 C). Only the posteriormost part of the roof is slightly sclerotized, forming a defined muscle attachment site (Fig. 2.4.1.6 B).

A

dta

51

53

45

ph ata

52 54

44

adt

19

tb

1?

18 17

43

sald

13 48

histological sections (skeleton – blue, musculature – orange, nervous system – yellow, digestive tract – green, salivary duct – pink). A, Parasagittal section, mesal view (nervous system removed); B, sagittal section, mesal view. Abbreviations: abt – abductor tendon of mandible, adt – adductor tendon of mandible, ata – anterior tentorial arm, br – brain, cten – corpotentorium, dta – dorsal tentorial arm, eph – epipharynx, fg – frontal ganglion, lahyl – prelabio-hypopharyngeal lobe, lbr – labrum, md – mandible, mx – maxilla, oes – oesophagus, ph – pharynx, pmj – posterior mandibular joint, sald – salivary duct, soeg – suboesophageal ganglion, tb – tentorial bridge, trc – tritocerebral commissure, 1? – M. tentorioscapalis, 7 – M. labroepipharyngalis, 8 – M. frontolabralis, 11 – M. craniomandibularis internus, 13 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 19 – M. craniolacinialis, 22 – M. basistipitodististipitalis lateralis, 37 – M. hypopharyngosalivarialis, 42 – M. tentoriohypopharyngalis, 43 – M. clypeoepipharyngalis, 44 – M. clypeocibarialis, 45 – M. frontopharyngalis anterior, 46 – M. frontopharyngalis posterior, 48 – M. tentoriocibarialis, 50 – M. tentoriopharyngalis anterior, 51 – M. craniopharyngalis anterior, 52 – M. tentoriopharyngalis posterior, 53 – M. craniopharyngalis posterior, 54 – M. craniopharyngalis ventralis. Scale bars: 50 µm. Modified from Fabian et al. (2015).

52

46

The large salivary glands in the thorax are continuous with paired salivary ducts, which connect below the

▸ Fig. 2.4.1.5: C. dectes, larva, head, 3D reconstruction based on

 107

B

abt

pmj

51

22

mx

11

52

53

46 br oes

45 8

ph

fg

trc

50 52

cten

44 43

soeg

48 7 lbr

eph

md

37

lahyl

42

sald

108 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

A

C

nel

nep

46

pek

51

nel pek

11

51 ph

dta

47?

45

18

cten

cc

ata

col

48

12

abt

ciam 44

1? md 7

sald

lahyl

nmx

D

43

bst

dst 11

ph

pek

51

B

coe

fg lbr

37

adt

52b

cten 11

19

17

soeg

18 ph

hyrd

sald 52a

onp

bst

col

pic

22

E

dst

54

ph

19

52b

coe

dta

lahyl

ata sald

abt md mxp

mxl

nmx

tb

soeg

42 17 22

dst hyrd sald

bst

Fig. 2.4.1.6: C. dectes, larva, head, histological sections (for location of the section planes, see arrows in Fig. 2.4.1.1 A). Abbreviations: abt – abductor tendon of mandible, adt – adductor tendon of mandible, ata – anterior tentorial arm, bst – basistipes, ciam – circumantennal membrane, cc – crystalline cone cells, coe – circumoesophageal connective, col – corneal lens, cten – corpotentorium, dst – dististipes, dta – dorsal tentorial arm, fg – frontal ganglion, hyrd – posterior rods of hypopharynx, lahyl – prelabio-hypopharyngeal lobe, lbr – labrum, md – mandible, mxl – maxillary endite lobe, mxp – maxillary palp, nel – neurolemma, nmx – nervus maxillaris, onp – optic neuropil, nep – neuropil (brain), pek – perikarya (cell bodies of brain), ph – pharynx, pic – pigment cells, sald – salivary duct, soeg – suboesophageal ganglion, tb – tentorial bridge, 1? – M. tentorioscapalis, 7 – M. labroepipharyngalis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 19 – M. craniolacinialis, 22 – M. basistipitodististipitalis lateralis, 37 – M. hypopharyngosalivarialis, 42 – M. tentoriohypopharyngalis, 43 – M. clypeoepipharyngalis, 44 – M. clypeocibarialis, 45 – M. frontopharyngalis anterior, 46 – M. frontopharyngalis posterior, 47? – M. tentoriopharyngalis lateralis, 48 – M. tentoriocibarialis, 51 – M. craniopharyngalis anterior, 52a/b – M. tentoriopharyngalis posterior, 54 – M. craniopharyngalis ventralis. Scale bars: 50 µm. Modified from Fabian et al. (2015).



Musculature (Figs. 2.4.1.5 B and 2.4.1.6 C): M. hypopharyngosalivarialis (M.37): compact, O: hypopharynx, I: roof of the distal part of the salivary duct.

2.4.1.11 Brain and subeosophageal ganglion The moderately sized brain is mainly located in the anterior half of the head and fills out about 30% of the lumen (Fig. 2.4.1.5 B). The posterior protocerebral face forms one median and two lateral lobes, which fit into gaps between bundles of the mandibular flexor (Figs. 2.4.1.3 B, 2.4.1.4, 2.4.1.5 B, and 2.4.1.6 B). The anterior face is curved around the anterior tentorial arms and fronto-pharyngeal muscles. Two large anterior lobes are folded around the dorsal tentorial arm and in tight contact with each other anterior to this structure, creating the impression that it penetrates the brain (Figs. 2.4.1.4 and 2.4.1.6 A). Large ellipsoid optic lobes are present laterally. The compact frontal ganglion is closely associated with the brain, with thick and very short frontal connectives (Figs. 2.4.1.5 B and 2.4.1.6 A). The nervus recurrens is very thin. Circumoesophageal connectives are thick proximally (Fig. 2.4.1.6 A–C) but taper distinctly below the pharynx before they reach the suboesophageal ganglion below the tentorial bridge (Figs. 2.4.1.5 B and 2.4.1.6 D). A short tritocerebral commissure is present between the tentorio-cibarial and the tentorio-pharyngeal muscles (Mm. 48, 50). The suboesophageal ganglion is completely shifted to the prothorax (Fig. 2.4.1.5 B) and connected with the first thoracic ganglion by very short connectives.

2.4.2 Thorax (based on Russell 1982 and Fabian et al. 2015) Like the abdomen, the thorax is characterized by an unsclerotized, semimembranous cuticle with dorsoventrally oriented very distinct folds (Fig. 2.4.1.1 A). The surface is characterized by wart-like tubercles, referred to as “uniform conical pebbles” by Russell (1982), with a diameter of about 10 µm. These surface structures are arranged in transverse rows on much of the dorsal and ventral surfaces and whorled or irregularly aligned on other regions. A vestiture of setae is missing on the postcephalic body and fleshy protuberances are also absent. The thoracic segments are nearly cylindrical, highly arched dorsally, and only very slightly flattened ventrally. The prothorax is the longest thoracic segment. The semimembranous notum bears two indistinct folds laterally and is drawn

2.4 Morphology of larvae 

 109

out ventrad, reaching about half height of the segment. A defined pronotal sclerite and a dorsomedian ecdysial line are missing. A short semimembranous fold anterior to the cranial pronotal margin slightly overlaps with the occipital region of the head. A large triangular pleural area delimited by two distinct oblique folds is present posterior to the genal region; its lower part is smooth. A small, triangular pleural element with indistinct surface sculpture is present posterolaterally. A small oval, vertically oriented spiracle is inserted between its anterodorsal edge, the anterior triangular pleural area, and the posteroventral edge of the notum. The lower pleural region is distinctly sculptured, ventrally adjacent with the upper rim of the procoxa, and not distinctly separated from the sternal region anteriorly. Defined sclerotized sternal elements are missing; the sternal regions are traversed by grooves extending between and diverging anterior and posterior to the legs. Posteriorly, the prothorax is distinctly separated from the mesothorax by a slightly sinuate, nearly vertical fold. The mesothorax is distinctly shorter than the prothorax, but the surface sculpture and pattern of folds are similar. An anterior dorsomedian region is distinctly separated from the rest of the semimembranous notum, which is also extended ventrad on the lateral side. The triangular anterior pleural area is smaller and lacks a smooth ventral margin. A smooth posterolateral pleural element is recognizable but very small. A spiracle is not visible. The ventral mesopleural region is similar to its prothoracic equivalent but slightly larger. The meso-metathoracic intersegmental fold is similar to that separating the pro- and mesothorax. The metathorax is very similar to the mesothorax, but broader, slightly shorter dorsally and laterally, and slightly longer ventrolaterally. The posterolateral pleural element and a spiracle are not recognizable. The legs are small, conical, and widely separated from the midline; they are frequently retracted and unrecognizable in preserved specimens. The two anterior pairs are more prominent than the hind legs. A distinct subdivision is missing distad the coxae. The apical part is nipple-like. Claws are missing.

2.4.3 Abdomen (based on Russell 1979a and Fabian et al. 2015) The abdomen is composed of 11 segments (Fig. 2.4.1.1 A). Segments I–VI are similar to the meso- and metathorax in their general configuration and surface sculpture, except for the absence of legs. Abdominal prolegs are missing. The abdomen is distinctly tapering from segment VII to

110 

 2 Neomecoptera, Boreidae, Caurininae, Caurinus

the terminal segment XI. An anterior dorsomedian notal region is present and increasing in size on segments I– VI but missing on the posterior ones. Deep transverse ventral folds are present on segments I–V; they are less deep on sternites VI–VIII and distinctly shifted posteriorly on the latter. Broad, smooth areas are present in the dorsal border regions between segments VII and VIII, and VIII and IX. Segment VIII is about as long as VII, and IX is distinctly shorter and oriented ventrad. Segment X is distinctly developed and oriented ventrad but distinctly narrower than IX and almost cylindrical, slightly tapering toward its truncated apical region. Segment XI appears extremely short, apparently withdrawn into segment X in the specimen examined. A four-lobed membranous appendage of the abdominal apex is indistinct but present; it functions as an adhesive device, according to Russell (1979a), as it is the case in Panorpa and other pistilliform larvae.

2.5 References Asakawa, Y., Ludwiczuk, A. & Nagashima, F. (2013): Chemical Constituents of Bryophytes: Bio- and Chemical Diversity, Biological Activity, and Chemosystematics. Springer, Dordrecht, Heidelberg, London, New York. 796 pp. Aubrook, E.W. (1939): A contribution to the biology and distribution in Great Britain of Boreus hyemalis (L.) (Mecoptera: Boreidae). Journal of the Society for British Entomology 2: 13–21. Beutel, R.G. & Baum, E. (2008): A longstanding entomological problem finally solved? Head morphology of Nannochorista (Mecoptera, Insecta) and possible phylogenetic implications. Journal of Zoological Systematics and Evolutionary Research 46(4): 346–367. Beutel, R.G., Friedrich, F. & Whiting, M.F. (2008): Head morphology of Caurinus (Boreidae, Mecoptera) and its phylogenetic implications. Arthropod Structure & Development 37(5): 418–433. Biliński, S.M. & Büning, J. (1998): Structure of ovaries and oogenesis in the snow scorpionfly Boreus hyemalis (Linne) (Mecoptera: Boreidae). International Journal of Insect Morphology and Embryology 27(4): 333–340. Biliński, S.M., Büning, J. & Simiczyjew, B. (1998): The ovaries of Mecoptera: basic similarities and one exception to the rule. Folia Histochemica et Cytobiologica/Polish Academy of Sciences, Polish Histochemical and Cytochemical Society 36(4): 189–195. Bungert, N., Gabler, J., Adan, K.-P., Zapp, J. & Becker, H. (1998): Pinguisane sesquiterpenes from the liverwort Porella navicularis. Phytochemistry 49(4): 1079–1083. Büning, J. (1994): The Insect Ovary. Ultrastructure. Previtellogenic Growth and Evolution. Chapman & Hall, London. 400 pp. Burrows, M. (2011): Jumping mechanisms and performance of snow fleas (Mecoptera, Boreidae). Journal of Experimental Biology 214(14): 2362–2374.

Cooper, K.W. (1940): The genital anatomy and mating behavior of Boreus brumalis Fitch. (Mecoptera). The American Midland Naturalist 23: 354–367. Crampton, G.C. (1940): The mating habits of the winter mecopteran, Boreus brumalis Fitch. Psyche 47(4): 125–128. Fabian, B., Russell, L., Friedrich, F. & Beutel, R.G. (2015): The morphology of the larval head of the enigmatic boreid Caurinus dectes (Mecoptera). Arthropod Systematics and Phylogeny 73(3): 385–399. Grell, K.G. (1938): Der Darmtraktus von Panorpa communis L. und seine Anhänge bei Larve und Imago. Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 64: 1–86. Hasenfuss I. & Kristensen N.P. (2003): Skeleton and muscles: immatures. In: Kristensen N.P. (ed.) Lepidoptera, Moths and Butterflies. Vol. 2: Morphology, Physiology, and Development. Handbook of Zoology. Vol. IV Arthropoda: Insecta. Part 36. Walter de Gruyter, Berlin, New York: 133–164. Heinrichs, J., Hentschel, J., Wilson, R., Feldberg, K. & Schneider, H. (2007): Evolution of leafy liverworts (Jungermaniidae, Marchantiophyta): estimating divergence times from chloroplast DNA sequences using penalized likelihood with integrated fossil evidence. Taxon 56(1): 31–44. Hepburn, H.R. (1969): The proventriculus of Mecoptera. Journal of the Georgia Entomological Society 4: 159–167. Hepburn, H.R. (1970): The skeleto-muscular system of Mecoptera: the thorax. University of Kansas Science Bulletin 48: 721–765. Hünefeld, F., Mißbach, C. & Beutel, R.G. (2012): The morphology and evolution of the female postabdomen of Holometabola (Insecta). Arthropod Structure and Development 41(4): 361–371. Kéler, S. von (1963): Entomologisches Wörterbuch mit besonderer Berücksichtigung der morphologischen Terminologie, 3rd ed. Akademie-Verlag, Berlin. 774 pp. Labandeira, C.C., Tremblay, S.L., Bartowski, K.E. & VanAller Hernick, L. (2014): Middle Devonian liverwort herbivory and antiherbivore defence. New Phytologist 202(1): 247–258. Mercier, L. (1915): Caractere sexuel secondaire chez les Panorpes. Le rôle des glandes salivaires des males. Archives de Zoologie éxperimentale et génerale, Paris 55: 1–5. Mickoleit, G. (1967): Das Thoraxskelet von Merope tuber Newman. (Protomecoptera). Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 84: 313–342. Mickoleit, G. & Mickoleit, E. (1976): Über die funktionelle Bedeutung der Tergalapophysen von Boreus westwoodi (Hagen) (Insecta, Mecoptera). Zoomorphologie 85(2): 157–164. Noirot, C. & Quennedey, A. (1974): Fine structure of insect epidermal glands. Annual Review of Entomology 19(1): 61–80. Potter, E. (1938): The internal anatomy of the order Mecoptera. Ecological Entomology 87(20): 467–501. Richards, P.A. & Richards, A.G. (1969): Acanthae: a new type of cuticular process in the proventriculus of Mecoptera and Siphonaptera. Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 86(2): 158–176. Rood, R.J., Johnson, J.B., Lisowski, E.A., Pike, K.S., & Turner, W.J. (2015): Caurinus dectes Russell (Mecoptera: Boreidae: Caurininae) a range extension in Oregon and a new state record in Washington. Zootaxa 4013(3): 449–450. Rothschild, M. & Schlein, J. (1975): The jumping mechanism of Xenopsylla cheopis. I. Exoskeletal structures and musculature. Philosophical Transactions of the Royal Society London (B) 271(914): 457–490.

2.5 References 

Russell, L.K. (1979a): A study of the armored boreid Caurinus dectes (Mecoptera). Unpublished PhD thesis, Oregon State University. Russell, L.K. (1979b): A new genus and a new species of Boreidae from Oregon (Mecoptera). Proceedings of the Entomological Society of Washington 81: 22–31. Russell, L.K. (1982): The life history of Caurinus dectes Russell, with a description of the immature stages (Mecoptera: Boreidae). Entomologica Scandinavica 13(2): 225–235. Russell, L.K., Dallai, R., Gottardo M. & Beutel, R.G. (2013): The sperm ultrastructure of Caurinus dectes Russell (Mecoptera: Boreidae) and its phylogenetic implications. Tissue and Cell 45(6): 397–401. Schneeberg, K. & Beutel, R.G. (2010): The adult head structures of Tipulomorpha (Diptera, Insecta) and their phylogenetic implications. Acta Zoologica 92(4): 316–343. Schneeberg, K. & Beutel, R.G. (2014): The evolution of head structures in lower Diptera. ScienceOpen Research (DOI: 10.14293/S2199-1006.1.SOR-LIFE.ALTCE1.v2). Sikes D.S. & Stockbridge, J. (2013): Description of Caurinus tlagu, new species, from Prince of Wales Island, Alaska (Mecoptera, Boreidae, Caurininae). ZooKeys 316: 35–53. Simiczyjew, B. (2002): Structure of the ovary in Nannochorista neotropica Navás (Insecta: Mecoptera: Nannochoristidae) with remarks on mecopteran phylogeny. Acta Zoologica 83(1): 61–66.

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Simiczyjew, B. & Margas W. (2001): Ovary structure in the bat flea Ischnopsyllus spp. (Siphonaptera: Ischnopsyllidae). Phylogenetic implications. Zoologica Poloniae 46: 5–14. Simiczyjew, B. & Margas W. (2005): Ovary structure, oogenesis and phylogeny of Mecoptera. Zoologica Poloniae 50 (Suppl.): 5–52. Söderström, L., Hagborg, A., von Konrat, M., Bartholomew-Began, S., Bell, D., Briscoe, L., Brown, E., Cargill, D.Ch., Costa, D.P., Crandall-Stotler, B.J., Cooper, E.D., Dauphin, G., Engel, J.J., Feldberg, K., Glenny, D., Gradstein S.R., He, X., Heinrichs, J., Hentschel, J., Ilkiu-Borges, A.L., Katagiri, T., Konstantinova, N.S., Larraín, J., Long, D.G., Nebel, M., Pócs, T., Puche, F., Reiner-Drehwald, E., Renner, M.A.M., Sass-Gyarmati, A., Schäfer-Verwimp, A., Segarra Moragues, J.G., Stotler, R.E., Sukkharak, Ph., Thiers, B.M., Uribe, J., Váňa, J., Villarreal, J.C., Wigginton, M., Zhang, L., Zhu & R.-L. (2016): World checklist of hornworts and liverworts. Phytokeys 59: 1–826. Stotler, K.E. & Crandall-Stotler, B. (2017): A synopsis of the Liverwort Flora of North America North of Mexico. Annals of the Missouri Botanical Garden 102(4): 574–709. Štys, P. & Biliński S. (1990): Ovariole types and the phylogeny of hexapods. Biological Reviews 65(4): 401–429. Thiéry, J.-P. (1967): Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. Journal of Microscopy 6: 987–1018.

3 Neomecoptera, Boreidae, Boreinae, Boreus and Hesperoboreus Rolf G. Beutel & Loren K. Russell

3.1 Taxonomy and distribution Boreinae are subdivided into two monophyletic genera, Boreus Latreille 1816 and Hesperoboreus Penny 1977 (Penny 1977), the former with 26 species and the latter with 2 species. Hesperoboreus is restricted to western North America, whereas species of Boreus are widely distributed in the Nearctic and Palearctic regions (California Academy of Science World Checklist). The species diversity reaches its maximum along the Pacific Coast of North America (e.g. Penny & Byers 1979, Blades 2002, Penny 2006), where not only both boreine genera occur, but also both species of Caurinus. Boreus hyemalis and B. westwoodi occur in Western Europe. Boreus jezoensis was the first species discovered in Japan (Hori & Moritomo 1996). The diversity in the Russian Far East (e.g. Plutenko 1984, 1985, Gabdullina & Nikolajev 2015) is likely higher than presently known. List of presently recognized species of Boreinae: Boreus Latreille 1816 = Ateleptera Dalman 1823 = Euboreus Lestage 1940

Boreus hyemalis Latreille 1816 (Western Europe) = Panorpa hyemalis Linnaeus 1767 = Gryllus proboscideus Panzer 1796 = Bittacus hiemalis Latreille 1805 = Boreus hiemalis Latreille 1817 = Ateleptera hiemalis Dalman 1823 = Boreus gigas Brauer 1876 (s. Willmann 1977) Boreus insulanus Blades 2002 (Canada, Vancouver Island) Boreus intermedius Lloyd 1934 (Alaska) = Euboreus intermedius Lestage 1940 Boreus jacutensis Plutenko 1984 (Russian Far East) Boreus jezoensis Hori & Moritomo 1996 (Japan) Boreus kratochvili Mayer 1938 (Czech Republic, e.g. area of Brno) Boreus lokayi Klapálek 1901 (Romania) Boreus navasi Pliginsky 1914 (Crimea, type material not preserved) = Boreus aktijari Pliginsky 1914 Boreus nivoriundus Fitch 1847 (Eastern U.S.) = Euboreus nivoriundus Lestage 1940

Boreus altaicus Nikolayev 2015 (Kazhakstan, Altai Mountains)

Boreus nix Carpenter 1935 (Western N.A., Montana) = Euboreus nix Lestage 1940 = Boreus gracilis Carpenter 1935, = Euboreus gracilis Lestage 1940

Boreus beybienkoi Tarbinsky 1962 (Kyrghyzstan, Ala Tau)

Boreus orientalis Martynova 1954 (Russian Far East)

Boreus borealis Banks 1923 (USA, Alaska) = Euboreus borealis Lestage 1940

Boreus pilosus Carpenter 1935 (Western N.A., British Columbia) = Euboreus pilosus Lestage 1940

Boreus brumalis Fitch 1847 (Eastern N.A. [=North America]) = Euboreus brumalis Lestage 1940 Boreus californicus Packard (1870) (Western N.A.) = Boreus unicolor Hine 1901 = Euboreus unicolor Lestage 1940 = Boreus isolatus Carpenter 1935 = Euboreus isolatus Lestage 1940 = Boreus californicus fuscus Carpenter 1935 = Euboreus californicus Lestage 1940 Boreus chagzhigireji Pliginsky 1914 (territory of former U.S.S.R., Crimea) Boreus coloradensis Byers 1955 (Western N.A.) Boreus elegans Carpenter 1935 (Western N.A.) = Euboreus elegans Lestage 1940

https://doi.org/10.1515/9783110272543-003

Boreus reductus Carpenter 1933 (Western N.A., British Columbia, Montana) = Euboreus reductus Lestage 1940 Boreus semenovi Pliginsky 1930 (Siberia, Oijski mountain range) = Euboreus semenovi Lestage 1940 Boreus sjostedti Navás 1926d (Kamchatka) Boreus tardokijanensis Plutenko 1985 (Russian Far East) Boreus vlasovi Martynova 1954 (Turkmenistan, Tajikistan) Boreus westwoodi Hagen 1866= Boreus boldyrevi Navás 1911 = Boreus tarnanii Navás 1911

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Hesperoboreus Penny 1977 Hesperoboreus brevicaudus Penny 1977 (Western N.A.) = Boreus brevicaudus Byers (1961) Hesperoboreus notoperates Penny 1977 (Western N.A.) = Boreus notoperates Cooper (1972)

Loren K. Russell

3.2 Biology 3.2.1 Habitats Boreinae, despite the small number of species and their uniform morphology, are ecologically versatile. As a group, the species of Boreus and Hesperoboreus occupy habitats that range from coniferous rain forest and mesic deciduous woodland to dry pine forest and open habitats that encompass grassland, shrub-steppe, and tundra. Only a few species are very well known, and for these, much of the literature consists of notes reporting the activity of adults during winter, frequently mentioning their occurrence on the surface of snow. Deep snow cover is normally persistent for most of the period of adult activity for B. jezoensis, in central Hokkaido (T. Nakamura, personal communication), for northern populations of B.  brumalis (Shorthouse 1979) and B. nivoriundus in eastern North America (Penny 1977), and for B. hyemalis and B. westwoodi, where the two species occur together in southeastern Norway (Hågvar 2001). The northern populations of the species mentioned above usually are found in coniferous or birch/conifer woodland, and as Hågvar (2001) notes, the adults there are subnivean through most of their active period. Further south, these eastern North American and western European species usually occur in or on the margins of deciduous woodland, often on sandy soil. Boreus hyemalis often occurs in sparsely vegetated patches in sand dunes characterized by the gray hair grass Corynephorus canescens and the moss Polytrichum piliferum (Strübing 1950, Raemakers & Kleukers 1999). Boreus hyemalis is found in association with other mosses, including Polytrichum commune (Fraser 1943) and Mnium hornum. In France, B. hyemalis is most frequently associated with Mnium hornum, Dicranella heteromalla, and Bryum atropurpureum (Tillier & Ledys 2008). In Connecticut, Maier (1984) used sticky plates to capture boreid adults and to determine their patterns of activity. He found B. brumalis and B. nivoriundus occurring together in regrowth forests in mosses growing on disturbed soil. These forests were dominated by Quercus alba, Q. prinus, Q. rubra, and Fagus grandifolia, sometimes

intermixed with small stands of Tsuga canadensis and with thickets of Kalmia latifolia (Maier 1984). Adults of B. brumalis were captured on Dicranella heteromalla and Atrichum spp. growing on mineral soil along woodland paths, at the base of trees, and on eroded hillsides. Adults of B. nivoriundus occurred on Atrichum spp. in these sites, but also were captured on Polytrichum ohioense and P. commune growing at the base of large, upright trees and on rocky ledges. Boreinae are most diverse in western North America. Penny (1977) noted that the two species of Hesperoboreus, as well as B. elegans, live in areas of rather warm climate along the Pacific coast, while the remaining species of Boreus occur east of the Cascade-Sierra crest in mountainous areas with severe winters. This distinction is not as strong as he believed: H. notoperates, H. brevicaudus, B. elegans, and B. insulanus, more recently described from Vancouver Island (Blades 2002), are all now known to occur at elevations above 1000 m, where snow cover is persistent through most of the winter, while B. californicus is found on both sides of the Cascade Mountains in Oregon and Washington. East of the Cascade-Sierra mountain crest, the closely related and nearly allopatric B. coloradensis and B. californicus occur in dry pine forest, grassland, and shrub-steppe, often accompanied by B. reductus, B. nix, B. pilosus, and, in eastern Wyoming, B.  bomari. The annual precipitation in these localities ranges from about 60 cm to as low as 18 cm at the Hanford Reach National Monument in eastern Washington, where B. californicus, B. nix, and B. reductus all occur together in Artemisia shrub-steppe and in adjacent disturbed sites dominated by Bromus tectorum (Looney et al. 2019). West of the Cascade Mountains, B. californicus has been found in coniferous rain forest with annual precipitation exceeding 250 cm, at 1300 m in the Olympic Mountains near Port Angeles (W. Bicha, unpublished data), and with B. elegans at 900 m in the Oregon Coast Range (Russell 1979).

3.2.2 Life cycle Boreines generally share a common phenology that features a 2-year life cycle, with eggs hatching in late winter or early spring, pupation at the end of the second summer, and adults emerging in autumn. This pattern, recognizable by the coexistence of two age classes of larvae, from March or April through August, is known to occur in B. hyemalis, B. brumalis, B. nivoriundus, B. elegans, B. californicus, H. brevicaudus, and H. notoperates. Based on head capsule measurements, four larval instars have been suggested for Boreus hyemalis (Withycombe 1922, Strübing 1950) and for H. notoperates (Cooper 1974).

3.2 Biology 

The adults of most species are active from November through March or April. Populations living in Arctic tundra extend their activity through the spring and summer. The latter include B. borealis, collected on islands in the Bering Sea between May and August, an undescribed species in mainland Alaska (D. Sikes, personal communication), and possibly B. orientalis, which was described from a late August collection in maritime tundra in Kamchatka). However, it is possible or perhaps likely that these Arctic populations retain the basic boreine life history with adult emergence in autumn and then persist through most of the year in the subnival zone. Alpine or subalpine zone populations of other, wide-ranging species (for instance, B. nix, collected in June at Jasper, Alberta) also remain active well into spring, while conforming elsewhere to the typical boreine phenology.

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3.2.3 Mating and oviposition The rapine mating behavior, lacking any evident courtship, seems to be uniform among boreines. Mating is described in detail for Boreus californicus by Cockle (1914), by Steiner (1937) for Boreus hyemalis, and by K.W. Cooper for B. brumalis (Cooper 1940) and H. notoperates (Cooper 1974). The males apparently locate the female visually. Males of B. hyemalis jump at the female and try to grasp a leg with the hooks of the copulatory apparatus. The hookshaped rudimentary wings of the males (see Section 3.3.2) (Steiner 1937: “Kopulationshilfsorgane”; see also Mickoleit & Mickoleit 1976: B. westwoodi) are already extended in this stage. If the male succeeds in holding fast the female at a tarsus or tibia (phase 1), both rest for a few seconds, without attempts of the female to escape. After this short

A

B

C

D

Fig. 3.2.1: Boreus westwoodi, mating behavior (male black dotted, female white). A, Male holds female between wings and abdomen; B, coupling of genitalia; C, male releases hold on female; D, male locks the legs of female with his wings. Reprinted from Mickoleit & Mickoleit (1976) with permission from Springer (Zoomorphologie).

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interlude, the male grasps the female with an abrupt stroke of its abdomen, without releasing the tarsi or tibia. After this, the male uses the transformed wings to grasp the female directly behind the thorax and at the same time releases the legs (phase 2: Fig. 3.2.1 A). The male briefly loses footing during this process but shortly thereafter resumes a normal posture by a quick turn of the body. He carries the female on his back, but usually transversely or obliquely relative to his own longitudinal axis. In this stage, the female is inactive and hardly moves. After this, the copulation is initiated (phase 3: Fig. 3.2.1 B). The male tries to grasp the female postabdomen with the genital hooks and uses them to spread the paired elements of the female ovipositor. As soon as male and female genital segments are firmly interlocked, the grasp of the male wings is released and the body of the female abruptly turns backward, resulting in right angle formed by the body axes of the mating partners (Fig. 3.2.1 C). The female then lowers her antennae and places them between the legs on the ventral side. The legs, which were previously extended, are now drawn up toward the body. The head is lowered and placed between the forelegs. The male then bends its postabdomen upward and uses its wings to grasp the procoxae, profemora, or thoracic trunk of the female, which are not released during the entire process of copulation (Fig. 3.2.1 D). The coupling of the mating partners is very rigid and the male is able to move around freely with the female on his back. Mating partners were frequently observed under leaves, pieces of small branches, or grass stalks (Steiner 1937). Mating in B. brumalis is very similar (Cooper 1940). The male approaches the female to within 1 cm, then rushes or leaps at her and attempts to grasp an appendage with his gonopods. When the male is successful, the female usually becomes quiescent, with her appendages drawn to her body. The male then uses his rudimentary forceps-like wings to position her over his dorsum and parallel to his body. The hypovalves of the female sternite VIII are inserted into pockets in the male endandrium and are held in place by the male gonopods. Mating in H. notoperates differs both in more prolonged resistance by the female and in a final copulatory position in which the female remains vertical and is not held by the male’s wings. Cooper (1974) reported that in this species, the males approach “within some millimeters” (e.g. one or a few body-lengths) before springing at the females. Unlike Boreus spp., female H. notoperates typically continue to resist the males for an extended period, and during mating, the final copulatory position is “female perpendicular.” Unlike Boreus, the male’s wings do not support or clasp the female in this pose.

In all studied species, copulation lasts for one to several hours. The female remains motionless, while the male moves about. When the pair separates, the spermatophore is retained in the female’s spermathecal duct for a short time (observed only in B. hyemalis; Mickoleit 1974). This contrasts with Caurinus, where the sperma­ tophore, which resembles that of B. hyemalis, is retained in the male aedeagus when the couple separates. A spermatophore has not been described for other boreines, but Cooper’s camera lucida drawings of the male B.  brumalis (Cooper 1940) and H. notoperates (Cooper 1974) collected in copula appear to show the apex of a spermatophore protruding from the aedeagi. Mickoleit (1974) suggested that redevelopment of a spermatophore (present in the endopterygote groundplan, but absent in Pistillifera) may be connected to the formation of a secondary ovipositor in Boreus. Since Caurinus lacks the elongate boreine ovipositor, the presence of a spermatophore in that genus may cast doubt on Mickoleit’s interpretation.

3.2.4 Oviposition and fecundity Strübing (1950) failed to observe oviposition either in the field or in culture and suggested that this was a nocturnal activity. However, Aubrook (1939), Svensson (1966), and Cooper (1974) have observed females laying their eggs during the day, each describing the characteristic vertical posture with ovipositor inserted in the moss cushion. Svensson, observing a female (either B. westwoodi or B. hyemalis; the females of these two species are not reliably distinguishable), described the passage of the egg along the tube formed by the gonapophyses and tergite X. When the egg reached the tip, flexion of the cerci forced the egg onto the ventral surface of the gonapophyses and then onto a moss stem. Cooper (1974) described a similar posture for oviposition in H. notoperates. Eggs are usually found singly among the moss stems but occasionally are found in clumps of three to seven (Strübing 1950). Females may also oviposit repeatedly in a small area: Svensson noted that the female he observed laid four eggs separately within a period of 2 hours. The typical number of eggs laid by a female over its life span is poorly known. Cooper (1974) suggested 32 eggs as a minimal number for H. notoperates, based on an average of 1.16 eggs per day per female in culture and a lifespan of 4 weeks. Since free-living females may survive and reproduce for several months, Cooper thought that the potential fecundity in the field was significantly higher. Hågvar (2001) took another approach, dissecting over 1000 females of B. hyemalis and B. westwoodi that he

3.2 Biology 

collected on snow in southeastern Norway between October and April. He found evidence that Boreus lay eggs throughout the winter and concluded that after a first batch of 10–20 eggs (one or two per ovariole) are laid in November, December, and early January, additional batches of eggs are produced. He found that under Norwegian conditions, a large fraction of these eggs is laid on moss in air spaces under the snow.

3.2.5 Egg development and eclosion Strübing (1950) reported that eggs obtained in culture hatched in 3 weeks at 10°C and in 1½ months at 7°C. With warming temperatures in the field, this means that most eggs hatched within a few weeks, regardless of when they were laid. In H. notoperates (Cooper 1974), eggs held at 9°C for 30 days swelled but showed no other sign of development. When moved to 20°C, these eggs hatched 25 to 61  days later. Fifteen days after the move to 20°C, eyes were visible in nearly all eggs, and at 21 days, the head capsule and mandibles were pigmented and the reflexed abdomen was visible. Since boreine larvae lack the frontal egg buster found in first instar Caurinus, eclosion is effected by means of the larval mandibles. This has been observed in H. notoperates (Cooper 1974) and in H. brevicaudus (L. Russell, unpublished observation). Cooper reported that in H. notoperates, the first instar mandible has a sharp, falcate, apical tooth, a sharp subapical tooth, and two successively smaller, sharp denticles, which abrade and cut the chorion. In contrast, later instars have robust, bluntly toothed mandibles. After penetrating the chorion, the larva continues to cut a transverse slit, opening a broad, irregular apical flap allowing the larva to emerge.

3.2.6 Larval biology Boreus larvae are typically found in the rhizoid layer or soil under cushion- or turf-forming mosses, where the larvae form galleries and feed on the rhizoids of the moss, and perhaps also on humus. The mosses are usually the same species frequented by the adults, for instance Dicranella, Mnium, and several species of Polytrichaceae (Polytrichum and Atrichum), all of which are common on disturbed soil in forest-edge habitats. In western Oregon, larvae of B. californicus and B. elegans were found under cushions of the widespread Racomitrium heterostichum, growing on gritty soil at the base of basalt outcrops (Russell 1979). Relatively little is known of the larval hosts of dryland species of Boreus, but the larvae of

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H.  notoperates, living in a dry pine forest in southern California, were found to feed on dwarf saxicolous mosses, ­including Grimmia apocarpa, G.  montana, Racomitrium sudeticum, and Orthotrichum rupestre (Cooper 1974). Exceptionally, Penny (1977) reported a collection of adults and larvae of B. reductus from a club moss, Selaginella. This association with a vascular plant should be confirmed since it is based only on a Berlese funnel extraction of bulk samples that contained the clubmoss. In the arid regions of eastern Washington, many dryland mosses, including species of Bryum, Grimmia, Syntrichia, and Tortula spp., grow in association with Selaginella (Evans et al. 2003). They could have been the hosts for B. reductus in this case. Boreine larvae tolerate rather dry conditions, but during periods of drought, they may descend to moister, cooler soil, as Strübing (1950) reported for B. hyemalis. In some species, including B. californicus and B. elegans, both first-year larvae and prepupal larvae estivate near the rhizoid layer in cells that appear to be lined with a secretion similar to that reported for pupal cells of B. hyemalis (L. Russell, unpublished observation). Larvae of Hesperoboreus also produce estival cells lined with a secretion. H. notoperates are frequently exposed to dry conditions, since they inhabit small lithophilous mosses that desiccate rapidly and repeatedly during the active period of the larvae. The larvae feed during the late winter and spring before the moss turf becomes dry. Later in the year, when the moss cushions are usually very dry, the larvae are active only for short periods when the mosses are wetted by rain showers. Cooper (1974) found that larvae and pupae estivate in small ellipsoidal cells composed of soil and moss particles with smooth inner surfaces. During dry periods, these cells remain intact when the dry mosses are broken up, apparently protecting the larva from desiccation. However, when the mosses are wetted, the cells soften and larvae resume their activity. Although H. brevicaudus occurs in mesic habitats, the larvae inhabit epiphytic mosses that desiccate rapidly and remain dry during long summer droughts. During the summer, when the moss is wetted (as when samples are wet-screened), larvae emerge and begin to feed. Since the larvae do not emerge when similar samples are processed in Berlese funnels, it is likely that this species forms estival cells like those of H. notoperates (Russell 1979; L.  Russell, unpublished observation). Cooper inferred that both the estival and pupal cells formed by H. notoperates and the pupal chambers of B. westwoodi and B. hyemalis (Withycombe 1922) are cemented by a salivary secretion that makes their walls impervious to water loss. Larvae of H. brevicaudus are exceptional

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among boreines in their tendency to feed on the leaves and stems of mosses (Russell 1979). Most frequently, they are found among pleurocarpous mosses growing as epiphytes on understory trees and shrubs, but H. brevicaudus larvae also occur in loose, blanketing mosses on boulders and logs. When placed on shoots of these mosses, the larvae actively move among the stems. On Antitrichia curtipendula, the larvae typically come to rest within a leaf axil with their dorsum against the inner leaf surface and feed on the outer layer of the stem. The larva eventually bores through the base of the leaf and continues its feeding along the stem, eventually forming an open gallery filled with fibrous debris. In Plagiothecium undulatum, an epiphytic moss with thicker terminal shoots than A. curtipendula, the H. brevicaudus larvae bore their galleries within the stem axis, leaving the closely appressed leaves untouched.

3.2.7 Pupation The following account is based on Cooper’s (1974) description of H. notoperates. Cooper follows Hinton (1971) in dating the pupal and adult stages from their apolyses, rather than from their ecdyses. Since the onset of the pupal apolysis is easily recognized by the migration of the pigment of the larval eye, Cooper’s terminology is followed in this discussion. Given this convention, most boreids are very similar in their metamorphosis to pupa and adult. Further, the period between apolysis and ecdysis is similar: Strübing (1950) stated that the duration for the pupa of B. hyemalis of 40 to 59 days is a week later, but not very different in duration from Cooper’s reckoning. Generally, the larval-pupal apolysis occurs in mid-August and in September in H. notoperates and in all the other boreids for which pupation has been recorded. Over a week or so, the eye pigment separates, elongates, and then migrates to the position of the pupal/adult eye. Although feeding does not occur, the larval jaws are functional and the larva will move around if disturbed. By the time the imaginal eye is fully outlined, the larval-pupal apolysis has been completed, and the pharate pupa can no longer move the larval mandibles. During the migration of the components of the developing pupal eye, spermatogenesis occurs in B. brumalis (Cooper 1940) and B. nivoriundus. In H. notoperates, however, only spermatogonial divisions and early prophase stages of the first meiotic division occur in the pharate pupa, and the meiotic divisions and spermatogenesis take place in the late pupa and pharate adult. Within one to several days following the completion of apolysis, the larval-pupal ecdysis ensues. Initially, the pupa is translucent white with the tips of the mandibles brown, and the eyes are a purplish brown. Within

a week, the body yellows, and pigmentation increases in the decticous mandibles and the eyes and setae. Within 2 weeks, the eyes, the ocelli, and Malpighian tubules are all pigmented. At 5 weeks, the jaws and body are still moveable, but pupal-adult apolysis has occurred. The pharate adult stage, during which the entire body, wings, and legs of the imago darken, may last from 10 days to 3 weeks. The pupal to adult ecdysis generally takes place 6 to 8 weeks after the onset of pupation. Boreines vary somewhat in adult pigmentation at eclosion: B. hyemalis (Strübing 1950) and B. westwoodi remain teneral for up to a week after adult eclosion, while B.  brumalis and H. notoperates are fully colored within a half-day following eclosion.

3.2.8 Adult behavior 3.2.8.1 Activity Adults of Boreus and Hesperoboreus are relatively longlived. They remain active throughout the colder winter months, when they are often observed walking or jumping on snow, or feeding on mosses. The physiological cold hardiness is known only for the two northern European species. The hardier of the two, B. westwoodi, may remain active at temperatures as low as −5°C and is able to survive short periods at −6.5°C (Sømme & Østbye 1969). In England, B. hyemalis can be active at temperatures as low as −3°C (Burrows 2011), which also seems to be near the lower limit reported for surface activity of Boreus species in North America. Hesperoboreus may be less tolerant of low temperatures, although H. brevicaudus have been observed walking on snow at −1°C (L. Russell, unpublished observation). Most, if not all, populations of Boreus live in areas where winter temperatures repeatedly fall 10, 20, or more degrees Celsius below the lethal point. As Strübing (1950) commented, observing the effect from a sudden freeze in the absence of snow cover on a population of B. hyemalis, “it is surprising how little resistance B. hyemalis has to low temperatures.” Although reports of the activity of Boreus can seem confusing, if not contradictory (e.g. diurnal vs. crepuscular, sunshine vs. overcast, reported in Penny 1977), most of the cited behavior can be explained in terms of thermal management, especially the avoidance of exposure to lethal temperatures. Not surprisingly, activity increases as temperatures rise from these minima. Walking and jumping are both affected. Burrows (2011) recorded walking/running speeds up to 14 mm/s at 8°C for B. hyemalis, but at 3°C, the maximum walking speed observed fell to 1 mm/s. Burrows regarded the jump as in part an adaptation providing faster

3.2 Biology 

movement both on loose snow and at low temperatures. The distance jumped increased with temperature, reaching a plateau (about 10 cm) at 10°C. Although the maximum distances jumped at 21.5°C and at 10°C were not significantly different, the minimum time interval between jumps dropped (Edwards 1987, Burrows 2011). Jumps may be used in ordinary directional movement (Hågvar 2001) but are most dramatic as a response to disturbance, whether visual, in response to nearby movements, or in response to mechanical stimulus. When disturbed at temperatures near 0°C, Boreus usually execute a single escape jump, the insects coming to rest motionless, with the appendages drawn in. At higher temperatures, Boreus often execute a rapid series of jumps, each with an erratic shift in direction, again ending in a cataleptic posture. When disturbed, H. brevicaudus often adopts a different evasive movement, combining one or more jumps with fast, erratic runs that end in shelter among the loose, tufted mosses they live in (L. Russell, unpublished observation). Continuous jumping is also employed in migration behavior, presumably as an exaptation of the escape jump. Hågvar (2001) reported that in Norway, B. westwoodi and B. hyemalis are mainly subnivean but engage in active dispersal on the snow surface, especially on warmer sunny days. They climb along tree trunks to reach the snow surface, possibly to absorb heat for egg development as well as to disperse. During this “migration,” each insect moves in a fixed direction by continuous jumping, covering a meter or more per minute. Different individuals migrate in different directions, both in relation to the compass direction and in relation to the position of the sun. In Ontario, Canada, Courtin et al. (1984) studied similar dispersive behavior by B. brumalis. Strikingly, they found that these insects, active on the snow surface between 10:00 and 15:00, were able to maintain body temperatures 5–7°C above both the snow surface temperature and that of the air immediately surrounding them. This resulted from the insects’ absorption of shortwave and longwave radiation and their presence in the boundary layer where conductive and convective heat loss is low. Edwards (1987) and Burrows (2011) have studied the biomechanics of jumping in Boreus. Both found that the jump involves a catapult mechanism similar to that in fleas, with energy from the large tergotrochanteral muscles stored in the pleural arch and in a resilin pad at the site of the wing hinge (Sutton & Burrows 2011). Burrows used high-speed microvideography to demonstrate that the jump in B. hyemalis is propelled by simultaneous movements of both the middle and hind pairs of legs. In contrast, fleas power their jump using only the hind legs and have pads of resilin only in the metathorax. Burrows

 119

notes that propulsion by both middle and hind legs is very unusual among jumping insects; aside from boreines, nearly all propel their jump by the metathoracic legs alone.

3.2.8.2 Adult feeding behavior Adult boreines are frequently observed feeding on mosses. The feeding is intermittent, with the insect often moving from one stem to another. The long, slender rostrum allows them to feed selectively and to reach the softest host tissues, e.g. leaf bases within the terminal growth of acrocarpous mosses and the leaf lamellae of haircap mosses (Polytrichum, Atrichum). A group of coarse outward-directed maxillary setae are peculiar to the Boreinae and may anchor the labiomaxillary complex, allowing the mandibles to be driven deeper into the moss tissues. The mouthpart structures vary among the Boreinae; most strikingly, in Hesperoboreus, the three apical teeth form a transverse series, while Boreus species typically have a series of teeth along the mesal margin (see Section 3.3.1). The functional significance is unknown. There is evidence that under deprivation, boreines also may consume dead insects. Strübing (1950) found B. hyemalis, deprived on its host moss, Polytrichum piliferum, would consume dead collembolans but did not attack live insects. Withycombe (1922) fed B. hyemalis dead flies, and dead crickets have also been consumed by an American species of Boreus (J. Abbott, personal communication). The significance of these reports is unclear as saprophagy has not been reported under field conditions. Strübing (1950), describing the consumption of collembolans, also noted the enlarged salivary glands in B. hyemalis and suggested that in boreines, digestion may be, in part, extraoral (see also Bratton 2001).

3.2.8.3 Predators and parasites Despite the frequent occurrence of boreine adults on snow, which would be expected to attract birds and mammals, and their employment of an escape leap, there seem to be few reports of predation. Cooper (1974) cites a single record of Boreus from the stomach contents of trout. Winter-active spiders and other arthropods are likely predators of boreines; but again, observations are lacking. Cooper (1974) found that the larvae of B. brumalis are parasitized by a Cordyceps fungus. A few hymenopterans are known to parasitize boreid larvae. In England, B. hyemalis larvae are parasitized by the braconid Dyscoletes lancifer (Aubrook 1939). According to Withycombe (1922),

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a second, wingless hymenopteran may also parasitize this species. In North America, Cooper (1974) found larvae of a hymenopteran parasitoid on B. brumalis but was not able to rear the parasites for identification. Later, he was able to rear an unidentified species of Conostigmus (Megaspilidae) from parasitized larvae of the Californian H. notoperates.

3.3 Adult morphology Adults of Boreinae (Fig. 3.3.1) appear less compact than those of Caurinus. They are also dimorphic, but the wings are less strongly reduced. An elongate rostrum is present. The legs are long and slender. Males lack a closed genital capsule. A secondary ovipositor is present in females.

ant nt1

fw

tga

hw fem3

cly tib3 mxp

tr3

tar3

Frank Friedrich & Rolf G. Beutel

3.3.1 Head This chapter is mainly based on personal observations (entire and dissected specimens of B. hyemalis, scanning electron microscope [SEM] images, microtome section series, and three-dimensional [3D] reconstructions) and on information presented in Cooper (1972), Hepburn (1969a), Penny (1977), and Russell (1979). The information on Hesperoboreus is mainly taken from the literature (Cooper 1972, Penny 1977, Russell 1979), but additional data were obtained from a microtome section series of H. notopteratus. The head structure is similar in its overall features in both genera. Hesperoboreus differs from Boreus in the undivided foramen occipitale, the lower number of antennomeres, the position of the antennifer opposite the lower margin of the compound eyes, and the shape of the hypostomal bridge, mandibles, and maxillolabial complex (Figs. 3.3.1.4 and 3.3.1.5). Muscles and other internal soft parts of H. notopteratus could not be observed due to insufficient fixation of the available specimen.

3.3.1.1 Head capsule In contrast to Caurinus, the orthognathous head of the species of Boreinae is strongly elongated, about three times as long as the maximum width. Its posterodorsal region is slightly overlapped by the pronotum (Fig. 3.3.1). The foramen occipitale is moderately large and subdivided by the tentorial bridge in species of Boreus (Fig.  3.3.1.1 C), but not in Hesperoboreus according to

Fig. 3.3.1: Boreus hyemalis, male, habitus, anterolateral view, SEM. Abbreviations: ant – antenna, cly – clypeus, fem3 – metafemur, fw – forewing, hw – hindwing, mxp – maxillary palp, nt1 – pronotum, tar3 – metatarsus, tga – tergal apophysis, tib3 – metatibia, tr3 – metatrochanter. Scale bar: 100 µm. Reprinted from Beutel et al. (2008) with permission from Elsevier.

Cooper (1972). In Boreus, the upper part (alaforamen) is roughly pentagonal and narrowing toward the tentorial bridge, whereas the lower neuroforamen is distinctly smaller and quadrangular, with rounded corners. A small triangular projection is present above the alaforamen. The postoccipital ridge is extensive dorsolaterally. The head capsule is sclerotized, with a microreticulate surface structure in B.  hyemalis and probably other species. At least the dorsal regions of the head are distinctly pigmented. The coloration is mostly shining black with a bronze or greenish glint in Hesperoboreus, but with dark reddish brown areas on the lateral, apical, and ventral areas of the rostrum (Cooper 1972). It is brown to almost black and slightly metallic toward the hind margin in Boreus. The brown coloration is less intensive on the posterior side. The ventral parts comprising almost the entire strongly elongated rostrum are of a pale, creamwhite, or yellowish coloration. A vestiture of short setae is present on the anterodorsal parts and slightly longer hairs along the lateral clypeal margin. The posterior side of the head capsule is smooth. The ovoid compound eyes are well-developed, prominent, and composed of

3.3 Adult morphology 



is missing in Hesperoboreus. The ocelli are distinctly reduced in size compared to those of Nannochorista or pistilliferan species (e.g. Hepburn 1969). In Boreus, the median ocellus lies above the median bridge separating the antennal foramina and the lateral ones very close

about 400 ommatidia with hexagonal corneae. Interfacetal setae are absent. The coloration is plum-colored to brownish black in Hesperoboreus. An extensive, curved circumocular ridge is present internally. Three ocelli are present in Boreus (Fig. 3.3.1), but the median ocellus

A

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C

ah

11

51c

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dta 4 sca

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2 1

av atp

12

sald

cpe 12

pgeb cd

11

18

cly

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43 18

46c

t12 41b

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II III

7

mxp lbr

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st 22b I II

67

ata

44

22a

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ga

33

17 IV

46a

fg

41c

nmx

17

t12

41a

45

43

46b

nfr

B

md

III IV V

ga pmt lap mxp

Fig. 3.3.1.1: B. hyemalis, adult, head, three-dimensional reconstructions (skeleton – blue, musculature – orange, nervous system – yellow, digestive tract – green, salivary duct – pink). A, Anterior view; B, detail, anterior view; C, posterior view. Abbreviations: ah – antennal heart, ata – anterior tentorial arm, atp – anterior tentorial pit, av – antennal vessel, br – brain, ccc – corpora cardiac–corpora allata complex, cd – cardo, ceao – cephalic aorta, cly – clypeus, cpe – compound eye, dta – dorsal tentorial arm, fg – frontal ganglion, ga – galea, lap – labial palp, lbr – labrum, loc – lateral ocellus, md – mandible, moc – median ocellus, mxp – maxillary palp, nan – nervus antennalis, nfr – nervus frontalis, nmx – nervus maxillaris, pgeb – postgenal bridge, ph – pharynx, pmt – prementum, sald – salivary duct, sca – scapus, st – stipes, tb – tentorial bridge, tra – trachea, t11 – adductor tendon, t12 – abductor tendon, 1 – M. tentorioscapalis anterior, 2 – M. tentorioscapalis posterior, 4 – M. tentorioscapalis medialis, 7 – M. labroepipharyngalis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 14 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 20 – M. stipitolacinialis, 22 – M. stipitopalpalis externus, 33 – M. praementopalpalis internus, 41 – M. frontohypopharyngalis, 43 – M. clypeopalatalis, 44 – M. clypeobuccalis, 45 – M. frontobuccalis anterior, 46 – M. frontobuccalis posterior, 51 – M. verticopharyngalis, 54 – M. tentoriooesophagalis, 67 – M. transversalis buccae. Scale bars: A, C, 250 µm; B, 50 µm.

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to the upper margin of the compound eyes. The fontal sutures and coronal sutures are absent, and the fronto­ clypeal strengthening ridge is also missing. An indistinct V-shaped frontal suture is present anterior to the antennal articulation area (B. hyemalis), but the border between the frontal and clypeal region is only indicated by the blackish, fissure-shaped anterior tentorial pits. An apodeme separating both areas as described by Hepburn (1969) is not present in B. hyemalis. The clypeus is strongly elongated, comprising about half of the entire head length. It is subparallel, slightly narrowed in its middle region, and not divided into an anteclypeus and postclypeus. The subgena is elongated along the clypeus, thus forming a part of the rostrum. It is separated from it and from the genal region by distinct sutures. A postgenal (hypostomal) bridge is present, broad in Boreus (Fig. 3.3.1.1 C) but strongly elongated in Hesperoboreus (Cooper 1972). A median suture or internal ridge is absent. The posterior tentorial grooves are visible as strongly darkened fissures in B. hyemalis.

3.3.1.2 Tentorium The tentorium is well-developed, with a complete tentorial bridge (Figs. 3.3.1.1 C, 3.3.1.2 A, and 3.3.1.7 A) in Boreus, and posterior and anterior arms are well-developed. The dorsal arm is present, but thin (Figs. 3.3.1.1 A, 3.3.1.2 B, and 3.3.1.7 B).

3.3.1.3 Labrum In contrast to Caurinus, the border between the clypeus and the small ovoid labrum is only indicated by small lateral incisions. Between them, the upper labral surface is fused with the anterior margin of the clypeal region. The dorsal surface is not flattened like in Caurinus. Anteriorly, it is unpigmented, appearing desclerotized. It is densely set with short setae. The lateral and ventral margins are equipped with dense setation (Fig. 3.3.1.3). Musculature (Figs. 3.3.1.1 and 3.3.1.2): in contrast to Caurinus, M. labroepipharyngalis (M. 7) is well-developed in Boreus. The extrinsic labral muscles are missing.

3.3.1.4 Antenna The long and slender antennae reach the posterior abdominal region when directed posteriorly in Boreus,

but only the anterior abdomen in Hesperoboreus (Cooper 1972: figs. 1 and 2). They are composed of 18 segments in H. notopteratus, whereas 23 are present in B. hyemalis (22 in other species; Penny 1977), covered with a dense vestiture of short setae. The large ovoid articulatory openings are medially separated from each other by a fairly narrow chitinous bridge, less than half as wide as each of them, and laterally only narrowly separated from the compound eyes (Fig. 3.3.1.1 A). They are slightly reinforced by a very low cuticular thickening (Fig. 3.3.1.7 A–C) and bear a very small condylar process laterally. The white articulatory membrane is extensive. The scapus is short, dorsoventrally flattened, and trapezoid in ventral or dorsal view, distinctly wider at its base than at its distal margin. The pedicellus is very slightly longer, distinctly narrowed basally, widening distally, and again slightly narrowing at its membranous apical part. The Johnston’s organ is well-developed. The flagellomeres are cylindrical. Flagellomeres 1 and 2 are only slightly longer than wide (B. hyemalis). The intermediate segments are distinctly elongated and the distal ones are moderately decreasing in length toward the apex. The apical segment is slightly longer than the preceding flagellomeres and apically rounded and densely set with setae (B. hyemalis). Musculature (Figs. 3.3.1.1 A, 3.3.1.2 B, 3.3.1.6 D–F, and 3.3.1.7 A,C): M. tentorioscapalis anterior (M. 1), strongly developed, fan-shaped, large part of the anterior tentorial arm, I: ventromesally on the scapal base. M. tentorioscapalis posterior (M. 2), strongly developed, O (=origin): base of the anterior tentorial arm between M. 1 and the tentorial bridge, I (=insertion): dorsolaterally on the scapal base with short tendon. In contrast to Hepburn (1969) (and Caurinus), the cranial rotator of the scape (M. 4) is present in Boreus and H. notopteratus, flat and composed of several thin parallel bundles, O: dorsal frontal region, mesad upper margin of compound eyes, I: dorsolaterally on articulatory scapal membrane.

3.3.1.5 Mandible The primary and secondary mandibular joints are present; a distinctly developed clypeal condyle articulates with a corresponding notch of the mandibular base anteriorly. The symmetrical mandibles are distinctly less massive compared to those of Caurinus. The base has the shape of a flattened triangle in cross section, but the main part is distinctly flattened and blade like, with approximately parallel dorsal and ventral walls. Unlike

3.3 Adult morphology 



11

51a,b

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7 la

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52

67 44

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51a

tb

46 45 fg

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B

la md

20

18 14

22a

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22b

43 33 7 la

C

Fig. 3.3.1.2: B. hyemalis, adult, head, three-dimensional reconstructions (skeleton – blue, musculature – orange, nervous system – yellow, digestive tract – green, salivary duct – pink). A, Sagittally sectioned, mesal view; B, parasagittal sectioned, lateral view; C, lateral view. Abbreviations: ah – antennal heart, ahm – antennal heart muscle, ata – anterior tentorial arm, br – brain, cd – cardo, ceao – cephalic aorta, cla – clasps of pumping chamber, cly – clypeus, dta – dorsal tentorial arm, fg – frontal ganglion, la – labium, loc – lateral ocellus, md – mandible, moc – median ocellus, nfr – nervus frontalis, nla – nervus labialis, nlbr – nervus labralis, nmx – nervus maxillaris, nrec – nervus recurrens, pgeb – postgenal bridge, ph – pharynx, pph – prepharynx, sald – salivary duct, sca – scapus, soeg – suboesophageal ganglion, st – stipes, str – stipital ridge, tb – tentorial bridge, tra – trachea, t11 – adductor tendon, t12 – abductor tendon, 1 – M. tentorioscapalis anterior, 2 – M. tentorioscapalis posterior, 4 – M. tentorioscapalis medialis, 7 – M. labroepipharyngalis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 14 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 20 – M. stipitolacinialis, 22 – M. stipitopalpalis externus, 33 – M. praementopalpalis internus, 37 – M. hypopharyngosalivarialis, 43 – M. clypeopalatalis, 44 – M. clypeobuccalis, 45 – M. frontobuccalis anterior, 46 – M. frontobuccalis posterior, 50 – M. tentoriobuccalis posterior, 51 – M. verticopharyngalis, 52 – M. tentoriopharyngalis, 54 – M. tentoriooesophagalis, 67 – M. transversalis buccae. Scale bars: 250 µm.

in Caurinus, a basal prominent molar projection is completely missing and longitudinal furrows on the dorsal or ventral surface are also absent. A series of five small teeth is present apically. A long and prominent apical tooth (Figs. 3.3.1.3 and 3.3.1.4), as it is present in Caurinus, is missing.

Musculature (Figs. 3.3.1.1, 3.3.1.2, 3.3.1.6, and 3.3.1.7): M. craniomandibularis internus (M. 11), strongly developed, with extensive area of origin, O: dorsal and posterior regions of the head capsule, circumocular ridge and parts of clypeus, I: with tendon on mesal mandibular base, tendon. M. craniomandibularis externus (M. 12),

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st

cly

I

3.3.1.6 Maxillolabial complex

II

III ga IV

lbr

region, laterad M. 43, ventrad M. 12, I: posterolaterally and anterolaterally on the mandibular base. The tendons of the adductor and abductor lie very closely together in the anterior part of the rostrum and even in the median plane at the functional mouth opening (external opening of the prepharynx, see below).

pmt I lac

II

lap

V mxp md

Fig. 3.3.1.3: B. hyemalis, adult, mouthparts, lateral view, SEM. Abbreviations: cly – clypeus, ga – galea, lac – lacinia, lap – labial palp, lbr – labrum, md – mandible, mxp – maxillary palp, pmt – prementum, st – stipes. Scale bar: 500 µm.

less voluminous than M. 11. O: lateral parts of the head capsule, I. with long and strongly developed tendon on the lateral edge of the mandibular base. M. tentoriomandibularis (M. 14), two extremely thin bundles closely associated with the mandibular nerve, O: central clypeal

Like in Caurinus (see Section 2.3.1 and Beutel et al. 2008), the maxillae and the labium form a functional and structural unit (Fig. 3.3.1.5). The length ratio maxillolabial complex versus rostrum is less than 0.6 in H.  notopteratus but more than 0.61 in Boreus (Penny 1977). The entire structure is inserted in a deep rectangular emargination of the posterior head capsule. The elongate, nearly parallel-sided, and transparent maxillolabial complex comprises the fused cardines and stipites, and probably the postmentum (or parts of it; Fig. 3.3.1.5: psm). Laterally, it is connected with the head capsule by a wide, thick membrane; it appears plate like and slightly sinuate in cross section. Posteriorly, it is delimited by a strongly sclerotized, almost vertical unpaired plate (possibly part of the postmentum), which is distinctly separated from the main part and completely devoid of muscle attachments. Internally, the complex is almost completely divided by a longitudinal median ridge, which reaches its greatest height in the middle region and obliterates anteriorly and posteriorly (Figs. 3.3.1.2 A and 3.3.1.6 B,C). Like in Caurinus and other mecopterans (except for Nannochorista), the galea laterally ensheaths the mandible and the clypeolabrum (Figs. 3.3.1.3 and 3.3.1.1 A). The lacinia is blade like, with a sharp and distinctly

A

C

B

D

Fig. 3.3.1.4: Mandibles of adult boreines. A, B, Hesperoboreus notoperates. C, D, Boreus elegans. A, C, Posterior view; B, D lateral view. Scale bars: 50 µm. Redrawn from Russell (1979).

3.3 Adult morphology 



sclerotized mesal edge (Fig. 3.3.1.3). The five-segmented maxillary palp is short in comparison with the length of the head (less than 0.2). Palpomeres 1–4 are of about equal length; the ultimate segment is about twice as long as the others in B. hyemalis and is spindle-shaped (Fig. 3.3.1.3). The spade-shaped prementum is about 0.2 times as long as the entire maxillolabial complex; it is inserted in a deep, rounded anteromedian emargination. Endite lobes are absent. The very short labial palp is two-segmented, with a wide proximal palpomere and small and peg-like distal segment (Fig. 3.3.1.3). Maxillary musculature (Figs. 3.3.1.1, 3.3.1.2, and 3.3.1.6): M. craniocardinalis (M.  15), absent. M. tentoriocardinalis (M.  17), strongly developed series of bundles, oblique, posteriorly directed (Hepburn 1969: ccm), O: middle clypeal region, I: laterally on the basal part of the median ridge and on the flat surface of the posteriormost part of the maxillolabial complex. M. tentoriostipitalis

 125

(M.  18) (Hepburn 1969: tsm), several bundles with distinctly oblique orientation, anteromedially directed, O: proximal clypeal region and from the proximal part of the anterior tentorial arms, immediately close to the origin on the head capsule, I: edge of the median ridge of the maxillary plate. M. craniolacinialis (M.  19), absent (possibly transformed into intrinsic maxillary muscle with origin on internal stipital surface, in this case represented by the following muscle). M. stipitolacinialis (M. 20), moderately sized, with long tendon, O: posterolaterally on the maxillary plate (anterolaterad M. 17), I: base of the lacinia. M. stipitogalealis (M. 21), absent. M. stipitopalpalis externus (M.  22), strongly developed, fan-shaped, composed of several subcomponents, O: posteriormost bundles medially on the posterior part of the maxillolabial plate, anterior bundle laterally on the maxillolabial ridge, I: anterodorsal edge of the maxillary palpomere I. Intrinsic palp muscles are absent.

A

B

ga lap

lap ga pmt pmt mxp mxp psm

st st

cd

cd

Fig. 3.3.1.5: Maxillolabial complex of adult boreines, posterior view. A, H. brevicaudatus. B, Boreus nivoriundus. Abbreviations: cd – cardo, ga – galea, lap – labial palp, mxp – maxillary palp, pmt – prementum, psm – postmentum, st – stipes. Scale bars: A, 100 µm; B, 250 µm. Redrawn from Russell (1979).

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

Labial musculature (Figs. 3.3.1.1 C and 3.3.1.2): M.  submentopraementalis, Mm. tentoriopraementales inferior/superior (Mm.  28-30), M. praementoparaglossalis (M.  31), M. praementoglossalis (M. 32), absent. M. praementopalpalis internus (M.  33), a moderately sized single bundle, O: base of the premental sclerite, I: not precisely identified on available microtome sections. Mm. palpopalpales labii primus/secundus (M. 35, M. 36), absent.

3.3.1.7 Epipharynx The cuticle of the anteriormost part of the ventral wall of the labrum is thin but sclerotized, whereas the following part of the anterior epipharynx is largely membranous or semimembranous. A short, sclerotized median rim is present above the attachment of M. 7. It is posteriorly continuous with the roof of the prepharyngeal tube. The anterolateral area is equipped with minute tubercles, spines, hairs, and a low longitudinal ridge. The epipharyngeal section below the anterior clypeus is concave and also set with tubercles. A sclerotized, median pistil-like protrusion is formed by the epipharynx at the level of the secondary mandibular joint; spiniferous tubercles are present on the semimembranous area laterad this structure. The middle section of the epipharynx is sclerotized and convex and forms an x-shaped preoral chamber together with the membranous area at the mesal mandibular base and the strongly sclerotized and convex part of the hypopharynx proximad the hypopharyngeal projection (see below). It is completely devoid of microtrichia. The epipharyngeal part close to the anatomical mouth opening is narrow and laterally connected with the posterior hypopharynx, thus forming a very narrow, flattened prepharyngeal tube (Figs. 3.3.1.2 A and 3.3.1.6 A–D). The upper edges of the tube are reinforced by distinct sclerotizations representing the suspensorium. They are continuous with a ventromedian sclerotization of the anterior pharynx, which divides and forms a strongly sclerotized clasp

enclosing the ­precerebral pharyngeal pumping chambers (pharyngeal clasp; Fig. 3.3.1.2 A). Musculature (Figs. 3.3.1.1 A,B, 3.3.1.2 A,C, and 3.3.1.6 A,B): M. clypeopalatalis (M. 43), a complex, highly specialized muscle with many successively arranged bundles (very similar to M. 43 of Panorpa, strikingly different from M. 43 of Caurinus; Beutel et al. 2008). M. clypeobuccalis (M. 44), O: immediately dorsolaterad M. 43c, I: anatomical mouth opening, below the frontal ganglion.

3.3.1.8 Hypopharynx In contrast to Caurinus (Beutel et al. 2008), the anterior hypopharynx is not present as a recognizable separate element. The posterior hypopharynx forms the sclerotized floor of the strongly elongated prepharyngeal tube. Musculature (Fig. 3.3.1.1 B and 3.3.1.6 D,E): M. frontohypopharyngalis (M. 41), probably represented by a very small dorsal muscle, O: frons, dorsad M. 46, I: apical part of sclerotized bars. M. tentoriohypopharyngalis (M. 42), absent. An extremely short muscle connects the mesal projection of the anterior tentorial arms with the sclerotized bars of the pumping chamber. It cannot be fully excluded that the very short muscle connecting the anterior tentorial arm with the clasp of the pumping chamber is homologous with M. 48 (see below). However, considering the very atypical shape, origin, and insertion, this interpretation appears unlikely.

3.3.1.9 Pharynx and oesophagus The anatomical mouth is narrow and flattened (Fig. 3.3.1.6 D). The anterior pharynx appears like a horizontal crescent in cross sections, with the anterior edges and the pharyngeal roof between them serving as attachment areas for dorsal (anterior) dilators. A pumping chamber reinforced by sclerotized claspers is present like in Caurinus, but it is much smaller. The posterior pharynx is narrow and

▸ Fig. 3.3.1.6: B. hyemalis, head of adult, histological sections. A, Base of maxillary palp; B, midregion of rostrum; C, proximal stipital region; D, level of frontal ganglion; E, ventrally of foramen occipitale; F, level of foramen occipitale and antennal base. Abbreviations: ah – antennal heart, ata – anterior tentorial arm, br – brain, cla – clasps of pumping chamber, cm – circular pharyngeal muscles, cor – circumocular ridge, cpe – compound eye, cvm – cervical membrane, fg – frontal ganglion, lm – longitudinal pharyngeal muscles, mxp – maxillary palp, nla – nervus labialis, nlbr – nervus labralis, nmd – nervus mandibularis, nmx – nervus maxillaris, nrec – nervus recurrens, onp – optic neuropils, ph – pharynx, pph – prepharynx, sald – salivary duct, sca – scapus, soeg – suboesophageal ganglion, st – stipes, str – stipital ridge, tra – trachea, t11 – adductor tendon, t12 – abductor tendon, 1 – M. tentorioscapalis anterior, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 14 – M. tentoriomandibularis, 17 – M. tentoriocardinalis, 18 – M. tentoriostipitalis, 20 – M. stipitolacinialis, 22 – M. stipitopalpalis externus, 37 – M. hypopharyngosalivarialis, 41 – M. frontohypopharyngalis, 43 – M. clypeopalatalis, 45 – M. frontobuccalis anterior, 46 – M. frontobuccalis posterior, 50 – M. tentoriobuccalis posterior. Scale bars: 50 µm.

3.3 Adult morphology 



A

43

nlbr

B

pph

43

pph

nmd

14b

nmd

t12 37 mxp t11

sald

22b

st

C

st

22a

pph

D

t11 11

nmx

20

sald

nla pph

fg

17

lm

45

sald

str

1 ata

41c

12

cpe

nmd cla cm br tra t12

nmx 17 18

12 20

E

ata

str 1

st 46c

41b

46b

F

ah

11

sald

sca 1

nrec

cpe

onp

46d

cpe

lm ph cm 50 br ata soeg

cor 12

sald 11

tra

cvm

cor tra

11

12

 127

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

sca

sca

ahm

nan

cor

2

cpe

ah

onp

dta

br

cm

ahm nrec ph 52 cm tb cpe

A

54 cor

12 11

50

nmoc

sald

B

soeg

12 cco

ciam ceao

11 51a

sald nloc

4

cor cpe br 11

51a 51b nrec 51c cm ph cpe

C

cor

12

11

54

D

ceao

12

Fig. 3.3.1.7: B. hyemalis, head of adult, histological sections. A, Level of antennal hearts; B, level of tentorial bridge; C, level of median ocellus; D, level of lateral ocelli. Abbreviations: ah – antennal heart, ahm – antennal heart muscle, br – brain, cco – cervical connective, ceao – cephalic aorta, ciam – circum-antennal membrane, cm – circular pharyngeal muscles, cor – circumocular ridge, cpe – compound eye, dta – dorsal tentorial arm, nan – nervus antennalis, nloc – nerve of lateral ocellus, nmoc – nerve of median ocellus, nrec – nervus recurrens, onp – optic neuropils, ph – pharynx, sald – salivary duct, sca – scapus, soeg – suboesophageal ganglion, tb – tentorial bridge, 2 – M. tentorioscapalis posterior, 4 – M. tentorioscapalis medialis, 11 – M. craniomandibularis internus, 12 – M. craniomandibularis externus, 50 – M. tentoriobuccalis posterior, 51 – M. verticopharyngalis, 52 – M. tentoriopharyngalis, 54 – M. tentoriooesophagalis. Scale bars: 100 µm.

l­aterally compressed. Distinct dorsolateral and ventrolateral folds are present for muscle attachment, as well as much shorter folds laterally. The anterior oesophagus is narrow and slightly compressed dorsoventrally. Indistinct internal folds are present.

Musculature of precerebral pharynx (Figs. 3.3.1.1, 3.3.1.2 A, and 3.3.1.6 D–F): M. frontobuccalis anterior (M.  45), probably represented by a pair of strongly developed muscles, O: mesad anterior tentorial groove, I: anterior wall of the precerebral pumping chamber.



frontobuccalis posterior (M. 46), composed of two M. ­ subcomponents, M. 46a, O: central region of the frons, I: anterior side of the pumping chamber; M. 46b, very strongly developed, composed of two parallel bundles, O: frons, dorsad M. 45, I: dorsally on the pumping chamber. M. tentoriobuccalis posterior (M. 50), slender, O: tentorial bridge, I: ventrally on the pharynx, below M. 46. M. transversalis buccae (M. 67), O: lateral corner of the precerebral pharynx (below frontal ganglion), I: lateral corner of the precerebral pharynx of opposite body site. M. tentoriobuccalis anterior (M. 48), absent. Two very strong pairs of muscles originating on the lateral wall of the head capsule below the antennal sockets and inserting on the lateral walls of the pumping chamber are either a separate third subcomponent of M. 46 or homologous with von Kéler’s M. frontobuccalis lateralis (M. 47) (von Kéler 1963). The homologization of all precerebral dilators is impeded by the unusual modification of the anterior pharynx. A well-developed ring muscle is present around the anatomical mouth (Fig. 3.3.1.6 D,E). Musculature of postcerebral pharynx (Figs. 3.3.1.1 A,C, 3.3.1.2, and 3.3.1.7): M. verticopharyngalis (M. 51), composed of two subcomponents, M. 51a, pair of very thin muscles, O: anterodorsally on the head capsule, I: dorsolateral folds of the posterior pharynx, below M. 53; M. 51b, three to four thin parallel muscles, O: anterior wall of the head capsule, ventrolaterad M. 51a, I: dorsolateral folds of the posterior pharynx, below M. 51a. M tentoriopharyngalis (M. 52), represented by several bundles, O: head capsule immediately laterad the alaforamen and laterally on the tentorial bridge close to its base, I: lateral and ventrolateral folds of the posterior pharynx. M. postoccipitooesophagalis (M. 53), a pair of very thin muscles, O: dorsolaterally on the postoccipital ridge, I: posteriormost pharynx (or anteriormost oesophagus), on the dorsolateral fold. M. tentoriooesophagalis (M. 54), several moderately sized bundles, forming a close unit with M. 52, O: head capsule, immediately laterad alaforamen and very close to base of tentorial bridge, I: posteriormost pharynx on the dorsolateral fold.

3.3.1.10 Salivarium The salivary duct is unpaired within the head capsule. It splits into two branches when it enters the cervical region posteriorly. The proximal part in the upper region of the head appears strongly flattened in the available microtome sections, whereas the middle part is almost round in cross section, with a fairly wide lumen. The posterior wall of the distal part is sclerotized. The duct opens on the anterior side of the distal part of the maxillolabial

3.3 Adult morphology 

 129

complex, immediately posterad the posterior mandibular surfaces. Musculature (Figs. 3.3.1.2 A,B and 3.3.1.7 A): M. hypopharyngosalivarialis (M.  37), like in Caurinus (Beutel  et  al. 2008) and Panorpa (Heddergott 1938: “Speichelpumpe”) probably represented by a highly modified intrinsic muscle of the unsclerotized anterior wall of the distal salivary duct. Mm. praementosalivariales anterior/posterior (M. 38, M. 39), M. annularis salivarii (M. 40), absent.

3.3.1.11 Cerebrum, suboesophageal complex, and stomatogastric nervous system The brain is located in the dorsal cephalic region. It is moderately sized in relation to the head size. The central body, the optic neuropils, and other protocerebral elements are well-developed. A distinctly developed, separate tritocerebral commissure is not present. The upper margin of the protocerebrum is extended toward the foramen occipitale. The upper edge is slightly sinuate. Shallow concavities on the posterior side of the upper protocerebral part allow for the passage of bundles of Mm. craniomandibulares internus/externus (Fig. 3.3.1.7). A nervus connectivus originating from the frontal part of the protocerebrum is absent. The optic neuropils are less strongly bent than in Caurinus, but the curvature is still distinct. The spatial arrangement of the brain is adjusted to the bundles of M. craniomandibularis internus and the opening of the circumocular ridges. The well-developed antennal nerves originate laterally from the deutocerebrum; they are flattened basally and split into two branches at the antennal foramen. The trito­ cerebrum is represented by distinct paired lobes directed toward the ventral cranial margin; it is connected with the frontal ganglion by thick frontal connectives (Fig.  3.3.1.2 A). The frontal ganglion appears roughly triangular in the dorsal view and releases a nevus frontalis and a nervus recurrens in ventral and dorsal direction, respectively (Fig. 3.3.1.1 A,B). The latter runs on the upper side of the pharynx posterad (Figs. 3.3.1.2 A, 3.3.1.6 E,F, and 3.3.1.7). A very broad and short circumoesophageal connective connects the brain with the suboesophageal complex, which is located in the posterior head region (Figs. 3.3.1.2 A,B and 3.3.1.6 F). It releases the nerves of the labrum, mandible, maxilla, and labium (Fig. 3.3.1.2 A,B).

3.3.1.12 Glands and neurosecretory organs Gland tissue is present around the base of the paired cephalic tracheae and the transverse connecting branch

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

(see below). The corpora allata-corpora cardiaca complex lies laterad the posteriormost pharynx immediately anterad the attachment of M. 52 (Fig. 3.3.1.1 C).

3.3.1.13 Circulatory system (Figs. 3.3.1.1 A,B and 3.3.1.3 A,C) The thin-walled cephalic aorta is approximately triangular in cross section, where it enters the head capsule, with a maximum diameter of c. 20 µm. Within the alaforamen, it becomes closely attached to the dorsal wall of the posterior pharynx (Figs. 3.3.1.2 B and 3.3.1.7 C,D). It opens approximately at the proto-deutocerebral border. Paired accessory pulsatile organs (Fig. 3.3.1.7 A,B) support the hemolymph flow into the antennae via thin vessels. The ampullae of these antennal hearts are expanded by long muscles attached to the cephalic aorta posteriorly (see Figs. 3.3.1.2 A and 3.3.1.7 A,B).

3.3.1.14 Tracheal system One pair of moderately sized tracheae enters the head capsule. At their base, they are connected by a transverse branch. The paired trachea divides into sub-branches within the head capsule (Figs. 3.3.1.1 C and 3.3.1.2 A). Air sacs are absent.

3.3.1.15 Fat body Fat body lobes are absent in the head. Frank Friedrich & Rolf G. Beutel

3.3.2 Thorax This chapter is largely based on two articles by Füller (1954, 1955) on Boreus westwoodi Hagen, which is sexually dimorphic like all species of Boreidae. In the following, the thoracic structures of males are described in detail. Differences occurring in the females are treated briefly at the end of the chapter.

3.3.2.1 General appearance The habitus of Boreinae is mainly characterized by the specifically modified wings, which form curved, clasper-like structures in males (Fig. 3.3.1) and are vestigial in females.

The thorax is much less compacted than in Caurinus. The coloration is mainly brownish, with some areas with reduced pigmentation and sclerotization. Most parts of the thoracic surface bear a dense vestiture of very short setae. Additionally, longer and very fine setae are inserted on some areas, especially the proximal parts of the legs. The legs are long and slender, increasing in length from the prothorax to the metathorax.

3.3.2.2 Prothorax and cervical region The cervical region is not distinctly constricted; it is membranous except for the small, paired dorsal cervicalia and the large pair of lateral cervical sclerites. The weakly sclerotized and elongate dorsal cervical sclerites are adjacent with the dorsal corners of the foramen occipitale and placed in a transverse fold of the cervical membrane. The spoon-shaped lateral cervical sclerite is nearly vertically orientated (Fig. 3.3.2.1 A,B). It forms a connection between the head and prothorax. Its slender anterior process articulates with the hypostomal spur (Füller 1954: “Kehlsporn”). Its oval posterior end widens and articulates with the anteroventral edge of the proepisternum at an angle of about 90°. The somewhat twisted sclerite is strengthened by a longitudinal ridge. The dorsal side of the well-developed prothorax is about as long and wide as the dorsum of each of the pterothoracic segments. Due to the smaller size of the sternite and the shorter pleura, it is only about two thirds as high as the metathorax (Fig. 3.3.2.1 A,C). The dark brown pronotum is a strongly sclerotized, nearly rectangular plate with two shallow transverse concavities. It nearly covers the entire upper half of the segment. Its surface is characterized by fine transverse wrinkles, and large areas are devoid of setae. The posterior angles are drawn out as apically pointed processes, which articulate with sockets at the anterodorsal edges of the mesanepisterna. The bases of the articulatory processes bear the very large first thoracic spiracles, which are enclosed by a strongly developed chitinous ring. A distinct chitinous ridge extends to the apex of the articulatory process (Fig. 3.3.2.1 A,B). The propleuron comprises the proepisternum and the distinctly smaller proepimeron, both elements separated by a strongly developed propleural ridge. Ventrally, the pleural ridge forms the articulatory process of the pleurocoxal joint, which is in contact with the lateral procoxal rim. The ridge extends distinctly beyond the condyle of the pleurocoxal joint (Fig. 3.3.2.1 B). Anterior to the joint, it is continuous with the strongly developed ventral

3.3 Adult morphology 



The small prosternum is a single wedge-shaped sclerite, anteriorly pointed and forming ventrolaterally oriented wing-shaped plates in front of the procoxae. This area bears a strongly developed median discriminal ridge, which splits up posteriorly to continue on the anterior face

preepisternal margin, which is anteriorly articulated with the lateral cervical sclerite. The well-developed pleural arm originates at the upper third of the pleural ridge; it is broadly fused with the profurcal arm, thus forming a massive endoskeletal arch (Fig. 3.3.2.1 B).

teg3

nt1 spi1

pl1

nt2

teg2

fw

hw pn3 bas3 spiI

cpe

nt1

sc2 em2 aes2

 131

tgII

em3 aes3

scl2

sc3 scl3

fw

stII

lcv

pn3 cx1 tr1

A

nt1

pl1

spi1

tgI

pcj3

pcj1

C

cx3

cx2 pwp2 sa2 spi2 pwp3

sa3 plr3

pn3

nt1

tgI em2

lcv

aes2

pwp2

em3 aes3

scl2

sa2 pcj3

stII

fu1

fu3

teg3

scl3

hw

pn3

sa3

pab2 fw pab3

tgI

st1

fu2 sp1

B

teg2

tgII

vsp2

vsp3 scj3

D

Fig. 3.3.2.1: Boreus westwoodi, thoracic skeleton. A, Male, lateral view; B, male, sagittal sectioned, mesal view; C, male, dorsal view (left wings removed); D, female, dorsal view (left forewing removed). Abbreviations: aes2/3 – mes-/metanepisternum, bas3 – metathoracic basalare, cpe – compound eyes, cx1/2/3 – pro-/meso-/metacoxa, em2/3 – mes-/metepimeron, fu1/2/3 – pro-/meso-/metafurca, fw – forewing, hw – hindwing, lcv – lateral cervical sclerite, nt1/2 – pro-/mesonotum, pab2/3 – meso-/metathoracic postalar bridge, pcj1/3 – pro-/metathoracic pleurocoxal joint, pl1 – propleuron, plr3 – metathoracic pleural ridge, pn3 – metapostnotum, pwp2/3 – meso-/ metathoracic pleural wing process, sa2/3 – meso-/metathoracic subalare, sc2/3 – meso-/metascutum, scj3 – metathoracic sterno-coxal joint, scl2/3 – meso-/metascutellum, sp1 – prospina, spi1/3 – first/second thoracic spiracle, spiI – first abdominal spiracle, st1 – prosternum, stII – abdominal sternum II, teg2/3 – meso-/metathoracic tegula, tgI/II – abdominal tergum I/II, tr1 – protrochanter, vsp2/3 – ventral sternal process of meso-/metathorax. Modified from Füller (1954).

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

of the profurcal arms. The strongly widened postcoxal part of the prosternum bears the strongly developed, slightly curved furcal arms. The paired profurcal pits are distinctly separated. The tips of the profurcal arms are firmly fused with the pleural arms (see above). Anteriorly, both furcal arms are widened as broad lamellae, which serve as muscle attachment areas. A distinct sterno-coxal joint is not developed, but the prosternum and procoxa are separated by a narrow membranous strip. A precoxal bridge interconnecting the sternum and pleurae is absent. The prospina is represented by a minute posteriorly directed process at the posterior end of the prosternum (Fig. 3.3.2.1 B). Musculature (Fig. 3.3.2.2). Dorsal longitudinal muscles: Idlm1 M. prophragma-occipitalis (F.55 [=Füller 1955]: 0dlm1), slightly tapering toward insertion, O [= origin]: anterior mesoscutal margin, close to midline (laterad Idlm5), I [= insertion]: dorsal region of the cephalic postoccipital ridge. Idlm3 M. prophragma-cervicalis (F.55: 0dlm2), O: central region of the pronotum, I: dorsal cervical sclerite. Idlm5 M.  pronoto-phragmalis (F.55: Idlm), comparatively thin, O: central region of the pronotum, I: anterolateral margin of the mesoscutum (mediad Idlm1). Dorsoventral muscles: Idvm2/3 M. cervico-occipitalis (F.55: 0dvm), well-developed, O: broadly on the posterior half of the lateral cervical sclerite, I: dorsolateral part of the postocciput. Idvm4 M. pronoto-cervicalis lateralis (F.55: 0ism2), well-developed, O: anterolaterally on the pronotum, I: anterior process of the lateral cervical sclerite. Idvm9 M. profurca-occipitalis (F.55: 0ism1), well-developed, O: distal part of the profurcal arm (close to the propleural transition), I: dorsal region of the postoccipital ridge (together with Idlm1). Idvm10 M. profurca-phragmalis (F.55: Iism), weakly developed, O: transition zone of the profurcal arm and propleural arm, I: anterolaterally on the mesoscutum. Idvm17 or 18 M. pronoto-coxalis (F.55: Idvm), slender, O: posterolaterally on the pronotum, I: posterolateral part of the procoxal rim (behind the pleuro-coxal joint). Tergo-pleural muscles: Itpm1 M. pleurocrista-occipitalis (F.55: 0ism1?), possibly included in Idvm9. Itpm3 M.  pronoto-pleuralis anterior (F.55: Ipm3), fan-shaped, O: broadly on the anterior region of the pronotum, I: short process on the dorsal margin of propleuron. Itpm4 M. pronoto-pleuralis posterior (F.55: Ipm4), broad, flattened, O: lateral area of the pronotum, I: laterally on the propleuron. Sterno-pleural muscles: Ispm1 M. profurca-apodemalis, absent (propleural apodeme fused with the furcal arm). Pleuro-coxal muscles: Ipcm2 M. procoxa-cervicalis transversalis (F.55: 0ism3), slender, transverse muscle (in contrast to Füller 1955), O: anterior edge of the procoxa, I: anteriormost part of the lateral cervical sclerite of the

opposite side. Ipcm4 M. propleuro-coxalis (F.55: Ipm1), O: broadly on the anterodorsal propleural region, I: anterolateral part of the procoxa (between Ipcm2 and pleuro-coxal joint). Ipcm8 M. propleura-trochanteralis (F.55: Ipm2), O: dorsal margin of the proepisternum, I: trochanteral abductor tendon (together with Iscm6). Ventral longitudinal muscles: Ivlm1 M. profurcacervicalis (F.55: -), O: ventral ridge of the profurcal arm, I: middle region of the lateral cervical sclerite. Ivlm3 M. profurca-occipitalis ventralis (F.55: 0vlm), strongly developed, O: anterior face of the profurcal arm (mediad Ivlm1), I: ventrolateral part of the foramen occipitale. Ivlm4 M. intraprofurcalis (F.55: Iifum), cylindrical, O: medial face of the profurcal arm, I: profurcal arm of the opposite side. Ivlm7 M. profurca-mesofurcalis (F.55: Ivlm), O: posterior face of the profurcal arm, I: anteriorly on the mesofurcal arm. Ivlm9 M. prospina-mesofurcalis (F.55: -), very thin, O: medially at the posterior end of the prosternum, I: mesofurcal arm (mesal of Ivlm7). Sterno-coxal muscles: Iscm1 M. prosterno-coxalis anterior (F.55: Ibm1), dorsoventrally flattened, fan-shaped, O: medially on the prosternum, I: anterior procoxal rim. Iscm2 M. profurca-coxalis posterior (F.55: Ibm3), broad, flattened, O: ventral side of the profurcal arm, I: postero­ laterally on the procoxal rim. Iscm3 M. profurca-coxalis medialis, absent. Iscm6 M. profurca-trochanteralis (F.55: Ibm2), O: ventral side of the profurcal arm, I: trochanteral abductor tendon. Coxo-trochanteral muscles: ctr-ab coxo-trochanteral abductor muscle (F.55: Icxm4), O: posterior face of the procoxa, I: abductor tendon of the trochanter (together with Ipcm8 and Iscm6). ctr-ad coxo-trochanteral adductor muscles (F.55: Icxm1-3), O: lateral half of the procoxal rim, I: laterally on the trochanter.

3.3.2.3 Mesothorax The mesotergum is subdivided into a notum with a complex structure and a simple, transverse band-shaped postnotum (Fig. 3.3.2.1 C). The mesonotum is shorter and narrower than its prothoracic equivalent. The anterior mesoscutum is comparatively well-sclerotized and dark brown; anteriorly, it is indistinguishably fused with the prescutum. A distinct prealar sclerite or a prealar bridge connecting the mesoscutum and mesanepisternum is not present. The lateral scutal region is interrupted by large membranous areas. The strongly sclerotized region posterior to the antecosta is medially divided by the anterior part of the mesoscutellum. Both sides are approximately wing-shaped, concave, and sometimes covered with

3.3 Adult morphology 



Idlm3

Idlm5 Idlm1

Ivlm7

IIIdlm1

Idvm4 Idvm9

Idvm10 IIdvm7

 133

IIIdvm7

atI-atII

Ivlm3 Ipcm2*

A

IIIvlm2

Ivlm1* Ivlm4

IIIscm4

Ivlm9*

Itpm4 Idvm17? Idvm2/3

IIdvm6

Ipcm8

Iscm6

ctr-ab

B

IIIdvm6

ctr-ab

ctr-ab

trt

trt Itpm3

stim

IItpm9

IIItpm9 IIItpm9

asI-asII

Ipcm4 ctr-ad

IIpcm4

ctr-ad ctr-ad

C

ctr-ad

IIIpcm4

IIpcm2/3

IIIpcm2/3

D

Fig. 3.3.2.2: B. westwoodi, male, thoracic musculature. A–D, Subsequent preparation of sagittal sectioned specimen. Muscles marked by an asterisk are modified from or added to the original figures based on own investigations. Abbreviations: ctr-ab – coxo-trochanteral abductor muscle, ctr-ad – coxo-trochanteral adductor muscle, trt – trochanteral abductor tendon. See Fig. 3.3.2.1 for skeletal details and text for muscle terminology. Modified from Füller (1955).

numerous wrinkles. Two parallel strengthening lines of the scutum start at the anterior edge of the scutellum, diverge at the antecosta, and obliterate laterally. The anterior scutal margin runs parallel to the posterior pronotal margin and meets on both sides with the arched posterior scutal edges at a narrow angle. Anterolaterally, the scutum forms the pointed anterior notal process, which extends over large parts of the lateral scutal margin. Posteriorly, the process is delimited by an incision (a distinct cleft in some specimens), which represents the tergal

fissure. It accommodates a sclerite (Füller 1954: “vorderes Tergalgelenkstück”), which is likely homologous to the third axillary sclerite. The posterior scutal rim is almost completely separated from the scutellum by membranous areas. The posterior notal process is not distinctly developed (Fig. 3.3.2.1 B). The well-developed mesoscutellum is of a yellowish, light brown coloration and delimited from the scutum by a distinct scuto-scutellar suture. Its pentagonal anterior part is inserted between the hind margins of the mesoscutum, resulting in a shape similar to an

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

inverse T (Fig. 3.3.2.1 C). The anteriorly directed median part is evenly convex and lies distinctly above the level of the scutal area of the notum. The posterior scutellar parts form a transverse bar, which is nearly as wide as the anterior margin of the mesoscutum. Both posterolateral edges of the bar are somewhat narrowing and ventrally directed. The edge of this structure is internally strengthened by a ridge. The clasp-like mesopostnotum is laterally continuous with the dorsal part of the mesepimeron, thus forming a postalar bridge. The sclerite is partly merged with the posterior scutellar section and fused with the median part of the anterior metanotal margin. The mesopleuron is integrated into a large pleural sclerite, which also contains the metapleuron and pleurotergal elements of abdominal segment I. This single structure covers the entire lateral surface of the pterothorax (Fig. 3.3.2.1 A). The intersegmental border is internally marked by a strong ridge in the ventral half of the sclerite, which is externally represented by a dark brown, scar-like depression. In contrast, no internal or external delimitation is discernable in the dorsal half. The mesopleural region is subdivided by the pleural ridge into the dorsally narrowing mesepisternum and the mesepimeron, which is posteriorly continuous with the metepisternum. Anteriorly, the mesepisternal margin is bent mesad, forming a strongly developed ridge (Füller 1954: “Vorderapodem”), which is slightly emarginated at its upper end. The anterodorsal mesepisternal edge is elongated as a small tongue-like process, which forms the socket of the pronotomesopleural articulation (see above). The upper mes­ episternal margin is bent into the lumen of the segment and serves as a rigid attachment area for a tendon; this part represents the mesobasalare. An anapleural suture or cleft is absent. Ventrally, the mesepisternum is continuous with the ventral elements of the thorax, without any discernable external nor internal dividing lines or sutures. The preepisternal regions of both sides form the ventral mesothoracic closure and contact each other medially, forming an internal discriminal ridge. A short precoxal ridge originates from the anterolateral face of this structure, forming an incomplete division between pre- and katepisternum. At its ventral end, the pleural ridge forms the condyle of the pleurocoxal joint. A hook-shaped ventromedially directed process (ventral pleural arm) originates directly above the joint. The upper end of the pleural ridge forms the pleural wing process. A pleural arm is missing (Fig. 3.3.2.1 B). The mesepimeron is larger than the episternum. Dorsally, the posterior segmental border is only marked by the vestigial mesothoracic spiracle (Fig. 3.3.2.1 B; see above). Ventrally, the epimeral rim is strengthened by a strongly developed ridge, which is anteriorly

continuous with the pleural ridge immediately above the pleurocoxal joint and posteriorly fused with the postcoxal ridge. Posterodorsally, the mesepimeron is gradually narrowing and continuous with the mesopostnotum, forming the slender postalar bridge (Fig. 3.3.2.1 A,B). The sternal mesothoracic elements are invaginated to a high degree. Sternites are represented by the longitudinal discriminal ridge (see above) and the furcasternum. The compact mesofurca bears two relatively short lateral arms, divided into a laterally directed external branch and an anterodorsally directed internal arm. The former is short but strongly developed, the latter slightly longer but distinctly narrower. Ventrally, the mesosternum is gradually extended into two long, slender posteroventrally directed processes; they contact the mesal mesocoxal rims, thus forming the sterno-coxal joints. The meso­ sternal region is deeply invaginated medially between the processes. Musculature (Fig. 3.3.2.2). Dorsal longitudinal muscles: IIdlm1 M. prophragma-mesophragmalis, absent. IIdlm2 M. mesonoto-phragmalis, absent. Dorsoventral muscles: IIdvm1 M. mesonoto-sternalis, absent. IIdvm2 M. mesonoto-trochantinalis anterior, absent. IIdvm4 M. mesonoto-coxalis anterior; absent. IIdvm6 M. mesocoxa-subalaris (F.55: IIpm2+5), slender muscle with long tendon, O: posterolateral mesocoxal rim and pleuro-coxal joint, I: subalare via long tendon. IIdvm7 M. mesonoto-trochanteralis (F.55: IIdvm), strongly developed, O: broadly on the mesonotum, I: trochanteral abductor tendon. IIdvm8 M. mesofurca-phragmalis; absent. Tergo-pleural muscles: IItpm1 M. prophragmamesanepisternalis, absent. IItpm2 M. mesopleurapraealaris, absent. IItpm3 M. mesonoto-basalaris, absent. IItpm4/5/6 Mm. mesonoto-pleurales anterior/medialis/ posterior, absent. IItpm7 M. mesanepisterno-axillaris, absent. IItpm9 M. mesepimero-axillaris (F.55: IIpm3), fanshaped, O: extensive area of the mesepimeron (including the posterior side of the pleural ridge), I: wing base (likely third axillary sclerite). IItpm10 M. mesepimero-subalaris, absent. Pleuro-pleural muscles: IIppm2 M. mesobasalareintersegmentalis, absent. Sterno-pleural muscles: IIspm1 M. mesopleurasternalis, absent. IIspm2 M. mesofurca-pleuralis (F.55: “Zwischenmuskel”), absent. Pleuro-coxal muscles: IIpcm2/3 M. mesobasalarecoxalis (F.55: IIpm1), O: basalar tendon of the mesanepisternum, I: anterior mesocoxal rim. IIpcm4 M. mesanepisterno-coxalis (F.55: IIpm4), flattened, O: anteroventral area of the mesanepisternum, I: ­anterolateral



rim of the mesocoxa (close to IIpcm2/3). IIpcm5 M. ­mesanepisterno-trochanteralis, absent. Ventral longitudinal muscles: IIvlm3 M. mesofurcametafurcalis, absent. Sterno-coxal muscles: IIscm1 M. mesofurca-coxalis anterior (F.55: IIbm2), O: discrimen of the mesosternum and anterolateral face of the mesofurcal stalk (in front of IIscm6), I: anteromesal mesocoxal rim. IIscm2 M.  mesofurca-coxalis posterior (F.55: IIbm3), broad, flattened, O: posterior face of the mesofurca (behind IIscm6), I: posterior mesocoxal margin. IIscm3 M. mesofurca-coxalis medialis, absent. IIscm4 M. mesofurca-coxalis lateralis (F.55: -), extremely thin, composed of only two fibers, O: tip of the mesofurcal arm, I: ventral process of the pleural ridge. IIscm6 M. mesofurca-trochanteralis (F.55: IIbm1), well-developed, O: base of the mesofurca, I: trochanteral abductor tendon (together with IIdvm7 and IIpcm5). Coxo-trochanteral muscles: ctr-ab coxo-trochanteral abductor muscles (F.55: IIcxm5-7), O: anterior and posterior face of the mesocoxa, I: abductor tendon of the trochanter (together with IIdvm7 and IIscm6). ctr-ad coxo-trochanteral adductor muscles (F.55: IIcxm1-4), O: interiorly on the lateral half of the mesocoxal rim, I: laterally on the trochanter.

3.3.2.4 Metathorax The metathorax is similar to the mesothorax in its general shape and configuration. The metanotum is also composed of two sections (Fig. 3.3.2.1 C). The scutellum is slightly larger than its mesothoracic equivalent. The prescuto-scutal part is slightly less sclerotized. Its anterior margin reaches below the mesoscutellum, forming a tongue-like process. It is reinforced by a ridge, which extends to the anterior tergal lever (Füller 1954: “vorderer Tergalhebel”) below the metanotum. The tergal cleft is deeper than that of the mesothorax, and the anterior tergal lever, slightly smaller. The mesopostnotum is fused with the anterior metanotal margin on both sides of the tongueshaped process. A faint V-shaped suture delimits the rounded anterior part of the scutellum from the anterior metanotal margin. A distinctly narrowed section connects the anterior metascutellum with the posterior transverse part, which is similar to the corresponding mesoscutellar element at its posterior margin, but not anteroventrally inflected below the mesonotum. It is laterally fused with the postnotum, but separated from it by a small median membranous area. The metapostnotum is a prominent, bulging sclerite. In males, it supports the modified wings in their oblique resting position. Laterally, it is completely

3.3 Adult morphology 

 135

fused with the metepimeron, and at its hind margin, with abdominal tergite I (Fig. 3.3.2.1 A,B). The metapleural region of the lateral pterothoracic plate is very similar to the mesopleural part described above. The largely reduced second thoracic spiracle lies in the upper region of the meso-metapleura. Like in the meso­ thorax, the metepisternum is laterally connected with the metasternum by a broad precoxal bridge. The metepimeron is completely fused with the metapostnotum and the anterior region of abdominal segment I. The epimeral-postnotal border is only indicated by the slightly different convexity of the elements and a faint chitinous ridge. The ventral epimeral margin is continuous with abdominal segment I. A postcoxal bridge is absent (Fig. 3.3.2.1 A). The metathoracic basisternum is anteriorly fused with the mesothoracic postcoxal bridge. The short, bandshaped sclerite is strengthened by its ridge-like upper margin and a well-developed ventromedian discriminal ridge. The ventrally directed sternal processes forming the sternocoxal joints are slightly shorter than those of the mesothorax. The stalk of the metafurca is continuous with the posterior end of the dicriminal ridge, The lateral arms are simple and pointed. The metafurca is distinctly wider than its mesothoracic equivalent. Anterior furcal arms are absent. Musculature (Fig. 3.3.2.2). Dorsal longitudinal muscles: IIIdlm1 M. mesophragma-metaphragmalis (F.55: IIIdlm), weakly developed, O: median region of the mesophragma, I: median region of the metaphragma. IIIdlm2 M. metanoto-phragmalis, absent. Dorsoventral muscles: IIIdvm1 M. metanoto-sternalis, absent. IIIdvm2 M. metanoto-trochantinalis anterior, absent. IIIdvm4 M. metanoto-coxalis anterior, absent. IIIdvm6 M. metacoxa-subalaris (F.55: IIIpm2), moderately sized, O: posterolateral part of the metacoxa, I: subalare via long tendon. IIIdvm7 M. metanoto-trochanteralis (F.55: IIIdvm), strongly developed, O: large areas of the anterior and lateral metascutum, I: trochanteral abductor tendon. IIIdvm8 M. metafurca-phragmalis; absent. Tergo-pleural muscles: IIItpm1 M. mesophragmametanepisternalis, absent. IIItpm2 M. metapleurapraealaris, absent. IIItpm3 M. metanoto-basalaris, absent. IIItpm4/5/6 Mm. metanoto-pleurales anterior/medialis/ posterior, absent. IIItpm7 M. metanepisterno-axillaris, absent. IIItpm9 M. metepimero-axillaris (F.55: IIIpm3), fan-shaped, O: dorsal half of the metepimeron, I: hindwing base. IIItpm10 M. metepimero-subalaris, absent. Pleuro-pleural muscles: IIIppm2 M. metabasalareintersegmentalis, absent. Sterno-pleural muscles: IIIspm1 M. metapleurasternalis, absent. IIIspm2 M. metafurca-pleuralis, absent.

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

Pleuro-coxal muscles: IIIpcm2/3 M. metabasalare-coxalis (F.55: IIIpm1), O: small invaginated area of the dorsal metanepisternum (basalare), I: anteriorly at the metacoxal rim. IIIpcm4 M. metanepisterno-coxalis (F.55: IIIpm4), flattened, O: ventral area of the metanepisternum, I: anterolateral part of the metacoxal rim. IIIpcm5 M. metanepisterno-trochanteralis, absent. Ventral longitudinal muscles: IIIvlm2 M. metafurcaabdominosternalis (F.55: IIIvlm), two bundles, O: posterior face of metafurcal arm, I: ventrally and ventrolaterally on abdominal sternite II.

A

Sterno-coxal muscles: IIIscm1 M. metasternocoxalis anterior (F.55: IIIbm2), flattened, O: metasternal discrimen, I: anterior metacoxal margin. IIIscm2 M. metafurca-coxalis posterior (F.55: IIIbm3), short, flattened, O: ventral face of the metafurcal arm, I: posterior rim of the metacoxa. IIIscm3 M. metafurca-coxalis medialis, absent. IIIscm4 M. metafurca-coxalis lateralis (F.55: IIIbm4), very thin, O: tip of the metafurcal arm, I: tip of the ventral metapleural process. IIIscm6 M. metafurca-trochanteralis (F.55: IIIbm1), well-­developed, O: ventral part of metafurcal arm and lateral face of

tar

cl

tib

B

untp

cl

cl

C tar Fig. 3.3.2.3: B. hyemalis, male, prothoracic tarsus, SEM. A, Tarsus, mesal view; B, details of distal tarsomere, lateral view; C, distal tarsomere, ventral view. Abbreviations: cl – claw, tar – tarsus, tib – tibia, untp – unguitractor plate. Scale bars: A, 100 µm; B, C, 20 µm.



discrimen, I: trochanteral abductor tendon (together with IIIdvm7). Coxo-trochanteral muscles: ctr-ab coxo-trochanteral abductor muscles (F.55: IIIcxm5-7), O: anterior and posterior face of the metacoxa, I: abductor tendon of the trochanter (together with IIIdvm7 and IIIscm6). ctr-ad coxo-trochanteral adductor muscles (F.55: IIIcxm1-4), O: interiorly on lateral half of the metacoxal rim, I: laterally on the trochanter.

3.3.2.5 Legs The legs of the three segments are similar except for the coxae (Fig. 3.3.1). The fore legs are the shortest and the hind legs are the longest and most strongly developed (Fig. 3.3.2.1 A). The procoxa is conical and elongated. Its mesal base is connected with the prosternum by a narrow membrane without a coxal joint. Laterally, the basal margins converge at a narrow angle and form the ventral articulation of the pleurocoxal joint. The proximal coxal margin, especially its lateral section, is strengthened by an externally recognizable internal ridge, which delimits a narrow marginal strip. Thus, a small basicoxale is present anterior to the subcoxal joint, as well as a slightly longer but rather narrow meron posterior to it. A wide lateral emargination at the distal coxal margin allows a strong adduction of the distal parts of the leg. The conical mesocoxae are closely adjacent medially, a condition that is likely correlated with the far-reaching sternal invagination. The distal sclerite of the largely membranous mesal region is restricted to about 20% of the total coxal length. Anteriorly, it widens gradually and is continuous with the sclerotized lateral coxal wall. This is not the case on the posterior side, where the mesal sclerite forms a lamella reaching below the descending posterior coxal margin. A separate meron is not distinctly recognizable on the mesocoxa. An indistinct ridge extending ventrad from the pleurocoxal joint may represent a vestigial merocosta (Füller 1954). The dorsal and posterior margin of the coxa is reinforced by ridgelike thickening, which is bifurcated anteriorly. A short, posteriorly directed lateral branch forms the socket articulating with the ventral mesosternal process. Both parts together form the sternal coxal joint (Fig. 3.3.2.1 B). Another ridge extends over a part of the sclerotized coxal region, parallel to the posterior coxal margin. As on the procoxa, a wide lateral emargination is present on the distal mesocoxal region. Anteriorly and posteriorly, it is continuous, with a groove-like concavity serving as articulation areas of the dicondylic coxo-trochanteral

3.3 Adult morphology 

 137

joint. The ventral part of the coxa bears very long setae, especially on its mesal side. Like the mesocoxae, the metacoxae are closely adjacent medially. They are distinctly larger. The sternal articulatory processes of the metathorax are longer than those of the mesothorax, and consequently, the mesal membranized area is slightly smaller. The ventral sclerite is broader and anteriorly and posteriorly continuous with the sclerotized lateral coxal wall. Thus, in contrast to the mesocoxa, the metacoxa forms an uninterrupted coneshaped sclerotized unit. The merocosta is also vestigial; the mesal margin is only strengthened on its mesal and posterior side. The ridge-like thickening is broadened mesally, where it articulates with the ventral metasternal process. The trochanters of the three segments are similar (Fig. 3.3.1), short, knee-shaped curved tubes with two short processes at their proximal margin. The orientation of the coxo-trochanteral joints is slightly different on the three pairs of legs. The line connecting the two points of articulation is parallel to the body axis in the middle leg, whereas the anterior one of the foreleg is mesally directed and the posterior one laterally, and vice versa in the hind leg. The trochanteral margin mesad the coxal joint is invaginated, thus forming the strongly developed trochanteral tendon, which reaches into the lumen of the coxa. At its distal margin, the trochanter is broadly connected with the femoral base and articulates with it with a condyle (Füller 1954: “kombiniert syndetisch-monokondyles Gelenk”). The connecting articulatory membranes of the middle leg are very narrow laterally but distinctly wider on the mesal side. The distal trochanteral margin is strongly sclerotized and reinforced laterally. Its anterior edge forms a small, protruding process that articulates with the proximal margin of the femur. Posterior to this joint, the femoral margin is strongly thickened and very strongly sclerotized. On the middle and hind legs, corresponding with the orientation of the coxa, the articulatory process is mesally or anterolaterally directed, respectively. The femora of all three legs are elongate, almost straight, cylindrical structures. The distal ends are slightly widened. They are connected with the tibia by a dicondylic joint and a wide articulatory membrane on the mesal side. In the flexed position, the proximal end of the tibia is slightly overlapped by the femur. The femoral apex bears a tooth on both sides of the articulatory membrane, with the sockets of the femuro-tibial joint placed at the base of these projections (Fig. 3.3.1). The proximal margin of the tibia articulates with two horizontal processes with corresponding sockets at the base of the terminal femoral teeth. The proximolateral

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

tibial margin forms a cone-shaped process between the two articulatory processes. The entire tibia is similar to the tarsomeres in its general shape, forming a very slender cylindrical tube, and like the femora, only very slightly widened distally. Several thorns are present on the mesal side of the distal tibial halve; two spurs (Füller 1954: “Calcaria”) and several less strongly developed thorns are present apically. Laterally, the distal end of the tibia is strongly sclerotized and forms a pocket serving as attachment area for a short process of the dorsolateral proximal margin of tarsomere 1. This articulation restricts the dorsal and lateral movability of the tarsus. Similar joints are present between the tarsomeres, even though the articulatory process at the proximal margins of tarsomeres 2, 3, 4, and 5 is less wide and longer compared to that of the proximal tarsomere (Fig. 3.3.2.3). The tibia is longer than the proximal tarsal segment, and the length of tarsomeres 1–4 decreases toward the apex of the leg. Tarsomere 5 is slightly longer and bears two simple, equal claws (Fig. 3.3.2.3). Dorsally, they articulate with the distally bifurcated unguitractor plate. The arolium is greatly reduced and pulvilli are lacking. The unguitractor is internally continuous with a long tendon (Fig. 3.3.2.3). All tarsomeres are covered with numerous well-developed distally directed thorns (Fig. 3.3.2.3).

3.3.2.6 Wings The wings have entirely lost their flight function. In the males, they function as claspers during copulation (see Section 3.2.3). They extend posterodorsad and the inner margins meet immediately posterior to the mesoscutellum. The boat-shaped mesothoracic wing rudiments are externally convex and cover the smaller ones of the metathorax. Their widest part is close to the attachment area. They taper gradually toward their parallel distal regions and terminate with a long apical thorn. The posterior third is bent downward. Both wing margins are set with strongly developed, slightly curved, posteroventrally oriented thorns. The density of the thorns increases toward the apex on the mesal side. The apical thorn is about 4–5 times longer than the other ones. The thorns along the external wing margin are less densely arranged and they are missing on the curved distal end. The total number varies, with a maximum of 35 mesally (including the apical thorn) and 14 laterally (Fig. 3.3.2.1 C; Füller 1954). The forewings are more sclerotized than the hindwings and are densely covered with very fine posteriorly directed hairs on their external surface. Due to the relatively distinct separation of the two lamellae, the wings

appear bloated – especially at their margins. The venation is almost completely reduced; only a single vestigial longitudinal vein is present, extending over half of the length of the wing, close to the keel and parallel to the external margin. The wing articulation is strongly modified (see Füller 1954 for full details). A rotation results in a right angle between the axis of the wing base and the longitudinal body axis. The movability is restricted due to the reduced condition of the articulatory sclerites and the broad connection between the wing base and the main body of the pterothoracic segments. Three sclerites articulate with the forewing base. The small basalare rests directly on the inflected upper edge of the mesepisternum; the lateral edge of the wing base rests on its posterior end. The second sclerite articulates with the anterior and posterior tergal lever. It reaches into the tergal cleft and covers the anterior lever. It is continuous with the external lamella of the wing without a distinct border. The third and largest articulatory sclerite is likely a product of fusion of the well-developed subalare and at least one axillary sclerite of the wing base. The subalar component of this sclerite is easily identifiable by the coxal muscle attached to a small knob-shaped process. As the sickle-shaped anterior margin of the composite sclerite encloses the pleural wing process dorsally and posteriorly, an inclusion of the second axillary sclerite is also likely. The dorsal part, which rests on the pleural wing process, reaches into the wing, where it forms a structural unit with both wing lamellae. An elliptical tegula is present between the posterior pronotal margin and the wing base; it is distinctly sclerotized and bears strongly developed hairs. The articulation and basal part of the hindwing are similar to the conditions described for the forewing. The part posterior to the region resting on the transverse element of the scutellum is strongly narrowed and the distance between the dorsal and ventral lamellae increases. Therefore, the main part of the hindwing is not boat-shaped and rather extensive like the forewing, but a slender, rod-shaped, posteriorly curved structure. The main part is circular in cross section and a distinction between the dorsal and ventral lamella is not possible. The hindwing fits in the cavity formed by the concave inner surface of the forewing. Females differ from males mainly by their largely reduced wings. The forewings are about as long as the pronotum and spoon-shaped (Fig. 3.3.2.1 D; Füller 1954). The short and broad wing base is similar to that of males. The hindwings are small vestiges hidden below the forewings. They are similar to the proximal part of the forewings,

3.3 Adult morphology 



with the wing blade only represented by a short, stubshaped process. The meso- and metanota differ in the proportions and shape of the sclerotized elements. The fused mesonotum and mesopostnotum form a complex sclerite. The region comprising the mesopraescutum and scutum is enlarged in relation to the scutellum. The posterior part of the scutum is broader than in males. A tergal cleft is not recognizable. The pleurotergal metathoracic region is very tightly attached to abdominal segment I. The plate-like quadrangular metanotum appears largely undivided and

A

tgII

tgaII

B

tgII

is laterally continuous with the metepimeron. The scutoscutellar border is only weakly indicated; an emargination is present at the insertion area of the hindwing. The tergal cleft is obsolete. The metapostnotum is flat and narrower than in the males. It is laterally continuous with the metepimera and fused with the scutellum anteriorly and abdominal tergite I posteriorly. The musculature is almost identical. One muscle is missing in each of the pterothoracic segments (IIpm5, IIIpm3; see also Füller 1955). M. mesepimero-axillaris is distinctly smaller in the female. Rolf G. Beutel

tgIII

tgaIII

3.3.3 Pregenital segments I–VII

spi

stII

 139

stIII tgIII

stIV

tgaIII

The abdomen is composed of 11 segments in females and 10 in males. Segment I is closely associated with the metathorax in both sexes (Fig. 3.3.2.1). A vestigial tergum I is visible in males of Boreus coloradensis but not in the female (Penny 1977: figs. 1 and 2). The terga and sterna of segments II–VII are widely separated by membranous pleura and also by distinctly exposed intersegmental membranes from each other (Figs. 3.3.2.1 A,B and 3.3.3.1 A). Tergites I–VII are approximately of equal length and width. The size of the sternites increases slightly posteriorly in females. The entire abdomen of the females appears more bloated, with distinctly widened membranous pleural areas, especially in the middle region (Byers 1961: fig. 2, Penny 1977: fig. 1). Terga II and III bear flattened ridges in species of Boreus (Fig. 3.3.3.1; Penny 1977: B. hyemalis), addressed as tergal apophyses by Mickoleit and Mickoleit (1976). These structures are used to hold the females during the mating process, together with the hook-like male wing rudiments and postabdominal clasping organs (Fig. 3.2.1; Mickoleit 1971, Mickoleit & Mickoleit 1976). They are missing in Hesperoboreus (Cooper 1972). Annular spiracles II–VII are placed close to the lateral edge of the respective tergites (Byers 1961: figs. 1 and 2).

Frank Hünefeld & Rolf Georg Beutel

3.3.4 Female postabdomen tgaII Fig. 3.3.3.1: Boreus westwoodi, male, base of abdomen. A, Lateral view; B, dorsal view. Abbreviations: spi – spiracle, stII-IV – abdominal sternite II-IV, tgII/III – abdominal tergite II/III, tgaII/III – apophysis of abdominal tergite II/III. Reprinted from Mickoleit and Mickoleit (1976) with permission from Springer (Zoomorphologie).

Segment VII is largely unmodified, with a normally developed tergite and a sternite that is moderately extended posteriorly. The small spiracle VII is embedded in the pleural membrane like the spiracles of the anterior segments. A narrow membranous area separates the posterior edge of sternite VII from the ventrolateral parts of tergite VIII (see below). Terminal segments VIII–XI and the cerci form a

140 

 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus tergite VIII on its dorsal side and slightly tapering towards their rounded apex (Fig. 3.3.4.1). Their anterior halves are connected ventromedially by a membrane, whereas their posterior parts are completely separated and moderately curved outward in their resting position. Approximately 60 conspicuous papillae, probably with sensorial function, are present on the ventrolateral surface. The mesal surface of the appendages is membranous and the cuticle on the outer side is flexible at about midlength. This results in a high degree of intrinsic flexibility: the posterior halves can be bent ventrolaterad at an angle of more than 90° during

secondary ovipositor. Tergite VIII is as long as the preceding tergites on its dorsal side, but it is strongly extended toward the ventral and posterior regions of the segment, with the edges almost meeting each other ventromedially (Fig. 3.3.4.1 A,C). Close to its anterolateral corner, it bears spiracle VIII, which appears slightly larger than the anterior spiracles. Sternal plate VIII is completely lacking. The ventromedian membranous area is narrow. Elongate and largely sclerotized paired genital appendages VIII originate ventrolaterally at the posteroventral margins of tergite VIII. They are approximately 3 times as long as

A

tgVII

B tgVIII

cer

C

reo

tgIX tgX

cer

sap

geapVIII

tgVIII

tgIX geapVIII stVII

D

tgVII

23 24

01

36

03

45

46

67

tgX

59

ept

02

cer

26 reo

sped sap geapVIII

04

agd 39

09

36

cov 08

stVII

Fig. 3.3.4.1: Boreus hyemalis, female postabdomen. A–C, External morphology. A, Lateral view; B, dorsal view; C, ventral view. D, skeletomuscular arrangement, sagittal sectioned specimen. Abbreviations: agd – duct of accessory gland, cer – cercus, cov – common oviduct, ept – epiproct, geapVIII – genital appendage VIII, reo – rectal opening, sap – subanal plate, sped – spermathecal duct, stVII – abdominal sternite VII, tgVII-X – abdominal tergite VII–X. Muscle numbers following Hünefeld et al. (2012), see text for details. Scale bars: 500 µm.

3.3 Adult morphology 



copulation (see Mickoleit 1974). The small saddle-shaped tergite IX is the only sclerotized area of this segment. The duct of the accessory glands opens at its membranous ventral surface, which is covered by the basal parts of the paired appendages. The parallel-sided tergite X is strongly elongated, approximately 3 times as long as tergite IX, and slightly narrower. Tergites IX and X together form a rooflike structure, which is the dorsal element of the secondary ovipositor. Tergite XI is absent. The cerci are medially fused and form a relatively small and apically pointed triangular sclerite. This is the apical element of the secondary ovipositor on the dorsal side. A small but distinctly developed subanal plate is present and visible between the apices of the paired appendages VIII. The configuration of the sclerites of the genital and postgenital segments is largely uniform within the genus. Musculature (Fig. 3.3.4.1 D). Fifteen postabdominal muscles are present in females of B. hyemalis (14 paired muscles, one transverse muscle). Muscle nomenclature following Hünefeld et al. (2012). Segment VII. 01 isVII-01, O [= origin]: tergite VII, paramedially, I [= insertion]: anterior margin of tergite VIII, paramedially, F [= function]: retractor of segment VIII; 02 isVII-02, O: tergite VII, laterad M. 01, I: tergite VIII and adjacent intersegmental membrane, laterally, F: retractor of segment VIII; 03 isVII-03, O: a short distance posterolaterad M. 01, I: anterior margin of tergite VIII, between Mm. 01 and 02, F: retractor of segment VIII; 04 isVII-04, O: ventrally on the anterolateral corner of sternite VII (usually on the anterolateral corner of tergite VII), I: anterolateral corner of tergite VIII, F: retractor of segment VIII; 08 isVII08, O: sternite VII, close to the median line, I: in front of the genital appendages VIII, close to the median line, F: retractor of segment VIII, also involved in downward movements

tgVII

A

B

tgVIII tgIX tgX

tgX

cer tgIX

stVII

 141

of appendages VIII; 09 isVII-09, O: directly below M. 04 on sternite VII, I: laterally in front of appendages VIII, F: retractor of segment VIII, like M. 08 involved in downward movements of appendages VIII; 17 dvVII-02, O: tergite VII, I: sternite VII, F: depressor of segment VII. Segment VIII. 23 isVIII-01, O: close to the anterior margin of tergite VIII, close to the median line, I: anterior margin of tergite IX, close to the median line, F: retractor of segment IX; 24 isVIII-02, O: near the anterior margin of tergite VIII, with two large attachment areas, laterad M. 23, I: anterior margin of tergite IX, near the anterolateral corner of the sclerite, F: retractor of segment IX; 26 is VIII-04, O: near the anterolateral corner of tergite VIII, close to the lateral margin, I: anterolateral corner of tergite IX, close to the lateral margin, F: retractor of segment IX; 36 dvVIII-01 (one compact muscle), O: tergite VIII, dorsal region, I: base of the appendages VIII, F: levator of the appendages VIII; 39 tVIII-01, transverse muscle, connects the bases of the right and left appendage VIII. Segment IX. 45 isIX-01, O: close to the anterior margin of tergite IX, close to the median line, I: anterior margin of tergite X, close to the median line, F: retractor of segment X; 46 isIX-02, O: anterior half of tergite IX, laterad M. 45, I: anterolateral corner of tergite X and adjacent membranous area, F: retractor of segment X, possibly also downward movements of segment X during oviposition. Segment X. 59 isX-01, O: mid-length of tergite X, near the ventral margin of the sclerite, I: dorsally on anterior margin of segment XI, close to the median line. Cercal muscle. 67 ce-01 (very large), O: near the anterior margin of tergite X, close to the lateral margin, I: base of the cercus, dorsolaterally, F: movements of the cercus. The female postabdomen of Hesperoboreus (Fig. 3.3.4.2) is generally similar to that of Boreus. Segment VII is

cer

C reo

geapVIII geo tgVIII

geapVIII

Fig. 3.3.4.2: H. brevicaudus, female, postabdomen. A, Lateral view, caudal elongation of tergite X (paired “blades”) indicated by arrowhead; B, dorsal view; C, ventral view. Abbreviations: cer – cercus, geapVIII – genital appendage VIII, geo – genital opening, reo – rectal opening, stVII – abdominal sternite VII, tgVII-X – abdominal tergite VII–X. Scale bars: 250 µm.

142 

 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

unmodified and similar to the pregenital segments. A secondary ovipositor is developed and composed of the same elements as in Boreus, i.e. the genital appendages of segment VIII, segments IX–XI, and the cerci. The ovipositor is distinctly shorter in relation to the total length, particularly in H. brevicaudus. Tergite VIII is as long as the preceding tergites in H. notoperates, whereas in H.  brevicaudus, tergite VIII is markedly shorter than VII and less dark than the sclerites of the pre-genital abdomen. As in Boreus, the ventral margin of tergite VIII is very distinctly prolonged and a sternal plate is lacking in this segment. The ventromedian space between the ventral tergal margins of this segment is wider than in Boreus. The genital appendages VIII arise in this region. Their outer surface is sclerotized. In H. brevicaudus, the sclerotization is less distinct than in H. notoperates. The appendages are moderately prolonged caudally, approximately 2 times as long as tergite VIII. Their anterior thirds are connected ventromedially by a membrane, whereas the posterior parts are separated. On their posterior halves, the ventrolateral surfaces of the appendages bear numerous papillae which likely have a sensory function (innervation; Fig. 3.3.4.3, indicated by arrowheads). Tergite IX is saddle-shaped and approximately as long as tergite VIII. Ventral sclerotized elements of segment IX are lacking. In contrast to Boreus, tergite X is not markedly longer than tergite IX. The posterolateral edges of tergite X are strongly prolonged (Cooper 1972: blades; indicated by arrowhead in Fig. 3.3.4.2 A). The epiproct (Mickoleit 1974: “Circumapikalsklerit”) and the subanal plate are well-developed. The cerci are elongate and extensively sclerotized (less strongly in H. brevicaudus). The apices appear tooth-like. Their proximal parts are medially fused.

n

Fig. 3.3.4.3: H. notoperates, female, postabdomen, longitudinal histological section, genital appendage VIII with sensory papillae (marked by arrowheads). Abbreviations: n – nerve. Scale bar: 10 µm.

Musculature. The muscle set of the female postabdomen of H. notoperates is very similar to what is described for Boreus above, but muscle 23 (isVIII-01) is absent. Rolf G. Beutel

3.3.5 Male genital segments (mainly based on Penny 1977 and Mickoleit 1974) Tergum and sternum VIII are completely fused laterally in B. californicus and B. hyemalis groups, with the annular spiracle placed on the midlateral region. They are unfused in B. nivoriundus and B. reductus groups, as well as in Hesperoboreus (Penny 1977). Tergum IX is raised in Boreus, and a median depression is present for reception of the tips of the dististyli. The medial depression is covered anteriorly by a thin, hood-like structure in Boreus but not in Hesperoboreus. The hood is divided by a median septum in B. californicus and B. hyemalis groups. Numerous peg-like denticles are present caudally and laterally on tergum IX. Sternum IX (hypandrium) is elongate-triangular, with its apex rounded, truncate, slightly emarginated, or deeply notched. Tergum and sternum X are reduced to small, oval sclerites between the basistyles. The aedeagus is membranous, except for a small, thin sclerite along the anterior surface. The basistyles (gonocoxites) are bulbous, with a dorsomedian ridge extending anteriorly as two sclerotized, laterally flattened straps, expanding medially to unite and form a thin, broad plate (Cooper 1974: dorsal gonobase, Penny 1977; see also Cooper 1972: fig. 4). The dististyli are claw-shaped, with an inner basal lobe and many stout denticles present below the apex of the claw. They are normally recurved over the abdomen, with the apex in depressions of tergite IX and the denticles of this tergite in contact with similar structures below the apex of the dististyli (Fig. 3.3.5.1). A well-defined genital capsule and a sperm pump, characteristics of Nannochoristidae and pistilliferan Mecoptera (Mickoleit 2008), are absent in Boreinae (Fig. 3.3.5.1) and also in Caurinus (Mickoleit 1974). A spermatophore is produced in the male genital ducts during copulation. During sperm transfer, the spermatophore remains within a membranous aedeagus with the exception of its tip, which is introduced into the orifice of the female ductus receptaculi (Mickoleit 1974). Mickoleit (1974) interpreted the spermatophore as a functional component of the male copulatory organ, as an elongation of the aedeagus. Additionally, it helps to force out the sperm, guaranteeing efficient sperm transfer without loss.

3.3 Adult morphology 



tgVII

abdsIX

tgVIII

gst

spi

gb stVIII

stVII

hypa

Fig. 3.3.5.1: Boreus vlasovi, male, postabdomen, lateral view. Abbreviations: abdsIX – abdominal segment IX, gb – gonobasis, gst – gonostylus, hypa – hypandrium, spi – spiracle, stVII/VIII – abdominal sternite VII/VIII, tgVII/VIII – abdominal tergite VII/VIII. Redrawn from Penny (1977).

Bożena Simiczyjew & Rolf G. Beutel

3.3.6 Ovaries (based on Biliński & Büning 1998 and Biliński et al. 1998) The ovaries and oogenesis of Boreus hyemalis were described in detail by Biliński and Büning (1998). The ovarioles are of the panoistic (neopanoistic) type (Biliński & Büning 1998: fig. 1A; see also Biliński et al. 1998), and seven or eight of them are combined in each of the paired ovaries (Fig. 3.3.6.1 A). Each of the ovarioles is tightly surrounded by a reticular network of striated muscles and

A

B

tf ova

 143

consists of a terminal filament, an elongated vitellarium, and an ovariole stalk (Biliński & Büning 1998: fig. 1 A,B). Functional germaria are absent in adult females (Biliński & Büning 1998: fig. 1 A). However, two or three degenerating germ cells may be present between the terminal filament and the first (youngest) oocyte in some ovarioles. The vitellarium is composed of 10 to 14 growing oocytes in a linear arrangement (Fig. 3.3.6.2 A). Each follicle is composed of an oocyte surrounded by somatic follicular epithelium (Fig. 3.3.6.2 B,C). The ovarian follicles develop asynchronously; thus, in the same ovariole, previtellogenic, vitellogenic, and choriogenic follicles can be observed (Biliński & Büning 1998). Between the neighboring ovarian follicles, groups of somatic interfollicular cells are present (Fig. 3.3.6.2 C,D). These cells do not make contact with the oocytes and differ significantly in size and shape from the follicular cells surrounding them. Early previtellogenic ovarian follicles are located in the anterior region of the ovariole (Fig. 3.3.6.2 A). In this stage of oogenesis, oocytes are surrounded by squamous follicular cells. The germinal vesicle (oocyte nucleus) is large, roughly spherical, and contains nucleolar mass, endobodies, and chromatin aggregations. During the early previtellogenic stage, the ooplasm is homogeneous. With the progress of oogenesis, the oocyte cytoplasm becomes diversified into peri­ nuclear (transparent) and peripheral (opaque) regions (Fig. 3.3.6.2 E). The latter contains numerous ribosomes, mitochondria, Golgi complexes, elements of endoplasmic reticulum, and clathrin-like cages. During the mid previtellogenic stage, the oocyte nucleus becomes elongated, and its volume increases significantly. Simultaneously,

tf ova

*

agd

*

sped agl cov

cov agd

spe

spe

agl sped

Fig. 3.3.6.1: Females, internal parts of the genital system, dorsal view, right ovary removed (marked with asterisk). A, Boreus hyemalis; B, Hesperoboreus notoperates. Abbreviations: agl – accessory gland, agd – duct of accessory gland, ova – ovary, cov – common oviduct, spe – spermatheca, sped – spermathecal duct, tf – terminal filament. Scale bars: 1 mm. Redrawn from Steiner (1937) and Cooper (1972).

144 

 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

B

A

D

C

oo nu

nu

oo fep

fep fep

nu

ovf

E

G

F nu

fep nu

nu

Fig. 3.3.6.2: B. hyemalis, ovariole structure, semithin Epon sections, methylene blue staining (except for D, semithin histocryl section, DAPI [4′,6-Diamidin-2-phenylindol], and iodide propidium; F, semithin histocryl section, bromophenol blue). A, Individual ovariole (terminal filament not shown) with vitellarium composed of linearly arranged ovarian follicles; B, previtellogenic ovarian follicles; oocytes surrounded by follicular epithelium; C, D, two neighboring ovarian follicles; E, part of late previtellogenic ovarian follicle; note the large oocyte nucleus filled with numerous multiple nucleoli; accumulations of nuage material occur (arrowheads) close to the nuclear envelope; ooplasm differentiated into two clearly recognizable regions: perinuclear (translucent) and peripheral (opaque); F, late previtellogenic ovarian follicle; note accumulations of nuage material close to nuclear envelope (arrowheads); G, part of ovarian follicle in late vitellogenic stage; oocyte nucleus located near follicular epithelium. Abbreviations: fep – follicular epithelium, nu – oocyte nucleus, ovf – ovarian follicles, oo – oocyte. © Bożena Simiczyjew.

in the karyoplasm, numerous multiple nucleoli occur (Biliński & Büning 1998). In close vicinity of the nuclear envelope, large accumulations of nuage material are localized (Fig. 3.3.6.2 E,F). During mid previtellogenesis, the number of follicular cells surrounding the oocytes gradually increases. Consequently, these cells form a one cell thick epithelium, which is composed of prismatic, uniform cells, with large nuclei with a large amount of heterochromatin and prominent nucleoli (Fig. 3.3.6.2  C,D). During vitellogenesis, when the ooplasm becomes filled

with large yolk spheres, the oocyte nucleus changes its position from the central to the peripheral region. As a result, during the final stages of vitellogenesis, the oocyte nucleus is located in close proximity to the follicular epithelium. Multiple nucleoli are still present in the karyo­ plasm, but far fewer than in the previtellogenic stage (Fig. 3.3.6.2 G). During vitellogenesis, the shape of the follicular cells changes. They lose their prismatic character. Among follicular cells encompassing the lateral areas of the oocytes, spaces appear, and consequently,

3.3 Adult morphology 



the epithelium becomes exposed. In the cytoplasm of the follicular cells, very large accumulations of rough endoplasmic reticulum occur (Fig. 3.3.6.3 B,C). The follicular cells at the anterior pole of the oocyte differ from those covering its lateral areas. They remain compact throughout the whole vitellogenesis. During advanced vitellogenesis, prechorional granules are visible in the space between the oocyte and surrounding follicular cells, i.e. in the perivitelline space. Subsequently, these granules fuse with one another, forming a layer on the oocyte surface. Finally, two relatively thin layers of the chorion constitute the egg envelope: a compact internal and a porous external layer covered by granulations (Fig. 3.3.6.3 F,G). The egg capsule of Boreus hyemalis is

 145

oval, and micropyles or other specialized structures on its surface are lacking. The surface sculpture of the egg capsule reflects the shapes of the follicular cells that formed it (Fig. 3.3.6.3 E–G). The ovaries and other elements of the internal genital system of H. notoperates are briefly described in Cooper (1972). Six ovarioles are combined in each of the paired ovaries (Fig. 3.3.6.1 B; Cooper 1972). The common oviduct is longer than in Boreus. It divides into a pair of lateral oviducts (Cooper 1972). The paired accessory glands are tube-shaped. Their duct is short and unpaired (Cooper 1972). Together with the spermathecal duct and the common oviduct, it opens behind segment VIII. The spermathecal duct is reduced to a short stalk; it is connected

oo fc

fep

rer fc

A

E

B

D

C

F

G

Fig. 3.3.6.3: B. hyemalis, follicular epithelium and egg envelopes. A, Part of ovarian follicle in early vitellogenic stage; follicular epithelium formed by prismatic cells; semithin Epon section, methylene blue; B, follicular cells in mid vitellogenic stage; accumulations of rough endoplasmic reticulum in cytoplasm marked by arrows; semithin Epon section, methylene blue; C, accumulations of rough endoplasmic reticulum in the cytoplasm of follicular epithelium cells; TEM; D, late vitellogenesis; oval follicular cells; semithin histocryl section, DAPI; E, ovarian follicle in vitellogenesis; shapes of follicular cells covering oocyte visible (arrows); SEM; F, egg envelopes during advanced choriogenesis; arrows indicate porous external layer of chorion; G, surface of fully developed egg capsule; SEM. Abbreviations: fc – follicular cell, fep – follicular epithelium, oo – oocyte, rer – rough endoplasmic reticulum. © Bożena Simiczyjew.

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

to the spermatheca, which is composed of two hemispheres, each containing 12 separate sperm receptacles (Fig. 3.3.6.1 B; Cooper 1972). The ovaries and oogenesis of boreines are similar to conditions found in Caurinus and also Nannochorista neotropical of Nannochoristidae (Simiczyjew 2002). However, the ovarioles differ significantly from the polytrophic ovaries of other groups of Mecoptera, namely Apteropanorpidae, Bittacidae, Choristidae, Eomeropidae, Meropeidae, Panorpidae, and Panorpodidae (Biliński et  al. 1998, Simiczyjew 2005). Furthermore, the organization of the ovariole and development of the oocytes in Boreidae show some resemblance to those of fleas (except for Hystrichopsyllinae). In both cases, ovarioles are secondarily panoistic (secondary lack of nurse cells). In mature females, the ovarioles are devoid of germaria (germ cell mitoses must occur before the reproductive phase), amplification of rDNA takes place in oocyte nuclei (resulting in multiple nucleoli), the ooplasm is differentiated into two regions, and accumulations of clathrin-like cages occur in the ooplasm (Biliński et al. 1998, Biliński & Büning 1998, Simiczyjew & Margas 2001). Nobuo Suzuki, Loren K. Russell & Rolf G. Beutel

3.3.7 Eggs (based on Suzuki 1990 and Cooper 1972, 1974) The shape of the mature ovarian and newly deposited eggs of Boreus westwoodi (reared by E. Mickoleit and G. Mickoleit; see Section 3.2) is oval and the size range is 0.45–0.5 mm by 0.25–0.3 mm. A chorion is present as a honeycomb network on the surface, which becomes less distinct toward the poles. Two separate micropyles are present on both poles. The chorion is transparent even as the embryogenesis is proceeding (Suzuki 1990). The periplasm occupies ca. 35% of the egg volume. The endoplasmatic reticulum is not strongly developed but is more distinct than in Bittacus laevipes Navás 1909.

The maturating female pronucleus in the cytoplasmic island of the periplasm is located one third of the egg length from the anterior pole. The yolk spherules stain homogenously with eosin and their maximum diameter is ca. 0.02 mm. The spherules occupy ca. 60% of the egg volume. Granules were not observed in B. westwoodi (Suzuki 1990). Mature eggs of Hesperoboreus notoperates were described as buffy-white by Cooper (1972), ranging in size from 0.53 × 0.31 mm to 0.6 × 0.3 mm, slightly narrowed at one end, and with a smooth chorion (the chorion of laid eggs of B. nivoriundus was described as “microscopically vermiculate” in the same study). Egg laying of H. notoperates was described in Cooper (1974). They are deposited singly, vertically, and ordinarily at such a depth that the apex of the egg lies from 0.1 to 0.3 mm below the surface of the sod of the moss, amid the rhizoids. The author located 186 eggs laid by 16 females over a period of 10 days at 21°C. Romano Dallai & Rolf G. Beutel

3.3.8 Spermatophores and Spermatozoa The spermatophore of Boreus westwoodi was described in detail by Mickoleit (1974). The knowledge of the spermatozoa of Neomecoptera (Boreidae) is still very fragmentary. Aside from Caurinus dectes (see Section 2.3.8) the only available detailed description of the ultrastructure is on Boreus hyemalis (Dallai et al. 2003b). The spermatophore of Boreus westwoodi (see Mickoleit 1974) is a robust structure, approximately spindle-shaped, with a rounded and an acuminate apical region, the former slightly curved. The structure is about 1.4 mm long and has a maximum width and height of 0.3 and 0.24 mm, respectively. The wall consists of a though, leathery, transparent material, more robust than in other groups of insects. Internally, it is divided into two s­ eparate chambers, divided by a median septum. A sperm tube

▸ Fig. 3.3.8.1: Boreus hyemalis, ultrastructure of spermatozoa, TEM. A, Sperm cyst, cross section, regular array of sperm flagella with simple 9 + 2 axoneme, cross section of nucleus with two longitudinal grooves marked by arrows; B, apical acrosome, cross section, axial crystallized perforatorium marked by arrowhead; C, nucleus showing two opposite longitudinal grooves (arrows), cross section; D, centriolar region, cross section, derived centriole with nine doublets devoid of dynein arms, surrounded by dense material of centriole adjunct, plasma membrane with unusual glycocalyx consisting of series of orderly arrayed longitudinal ridges (arrows); E, initial part of flagellar 9 + 2 axoneme, cross section, small mitochondrial derivative surrounded by dense and compact material of centriole adjunct; F, sperm flagellum, cross section, two remnants of centriole adjunct material marked by arrows; G, flagellum with 9 + 2 axoneme, cross section, mitochondrial derivatives with crystallized matrix, two dense fibers (arrows) embedded in the material of accessory bodies, glycocalyx with longitudinal dense ridges (arrowheads); H, mitochondrial derivative, longitudinal section, regular array of cristae (arrowheads) in the periphery, corresponding to bottom of each mitochondrion; I, sperm tail ends showing flattened and disorganized axonemes, cross section, note crystallized material on one side of the flagellar section (asterisks). Abbreviations: ab – accessory body, ac – acrosome, axo – axoneme, cam – centriole adjunct material; lam – laminae, mid – mitochondrial derivate, nu – nucleus. Scale bars: A, 0.5 µm; B–I, 0.1 µm.

3.3 Adult morphology 



axo axo

ac

mid

B

nu

A C lam

axo

cam

mid

D

ab ab mid axo mid

cam mid mid

E

G

axo ab

ab mid

F

H

*

mid

I

axo

axo

*

 147

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

connects each of them with the acuminate apex. Only the posterior lumen of the spermatophore is filled with spermatozoa, whereas the remaining part contains granular material. Contact with insect Ringer’s solution immediately liquefies the secretion granules, which are then released as a viscous mass intermingled with sperm. The content of the two spermatophore chambers is produced in the vesiculae seminales (Steiner 1937, Potter 1938a) of a widened section of the ductus deferentes. Initially, sperm is released in the proximal part of the vesiculae seminalis. After this, the accessory glands located produce the granular secretion, which accumulates in the vesiculae. The wall of the spermatophore is probably formed within the ductus deferentes for each chamber separately. The spermatophore is transmitted after males and females are coupled (Mickoleit & Mickoleit 1976). Males extrude a very large, membranous penis-tube. This is inserted in the ovipositor from its apex and reaches the anterior end of the female genital chamber internally. The completed spermatophore is pressed into the penis-tube by peristaltic movements of the abdomen, probably pushed forward by the ring muscles of the tube. It enters the opening of the ductus receptaculi, which opens into the genital chamber on a cushion-like thickening. Specific anchoring devices of the spermatophore were not observed (Mickoleit 1974). The sperm of Boreus hyemalis is a filiform cell with a short, conical, bilayered apical acrosome (0.2 µm in diameter), provided with a crystallized axial perforatorium (Fig. 3.3.8.1). The nucleus is a cylindrical, elongated structure, 0.25 µm in diameter at half of its length. Two longitudinal narrow grooves on its surface are opposed to each other. The posterior nuclear region contains the modified centriole, provided with doublet microtubules, surrounded by conspicuous, compact, electron-dense centriole adjunct material. The two mitochondrial derivatives are also embedded in this material. At this level, they differ in size and have a crystallized matrix. The axoneme has a simple 9 + 2 microtubular pattern with visible outer and inner dynein arms on each doublet, radial spokes, and a central complex (Fig. 3.3.8.1 E). The centriolar adjunct material forms two small, triangular, fibrous extensions placed between the mitochondrial derivatives and the axoneme (Fig. 3.3.8.1). They correspond with the structures usually referred to as accessory bodies, which accompany the axoneme for most of its length beneath the plasma membrane. In the region close to the axoneme, they contain two dense, longitudinal fibers of 10–12 µm thickness. The two mitochondrial derivatives are equally sized for most of their length, with two small cisterns visible on the side facing the axoneme. In the

mitochond­rial matrix, opposite to the axoneme, the remnants of cristae are present, regularly arranged at a distance of about 45 nm. Toward the tail end, the two dense fibers are no longer visible and the two mitochondrial derivatives taper and then disappear (Fig. 3.3.8.1). The axoneme flattens at the posterior tail end and the microtubular doublets appear disorganized. The two central tubules are in contact with the microtubular doublets. A semicircular mass of crystallized material is visible on one side of the axoneme, surrounded by fine granular material. The plasma membrane of the spermatozoa is provided with an unusual glycocalyx. It consists of longitudinal, densely arranged regular ridges (distance ca. 12 nm) projecting ca. 10 nm from the cell membrane. Several of the sperm characters displayed by Boreus hyemalis are symplesiomorphies shared with all or most other groups of insects. This includes the bilayered acrosome, the conspicuous centriolar adjunct material, the presence of two accessory bodies, and the presence of two mitochondrial derivatives (Jamieson et al. 1999). An apomorphic feature shared with Panorpa ssp. (and probably other mecopterans) is a simple 9 + 2 axoneme, due to a secondary loss of the accessory microtubules (groundplan of Diplura + Insecta). Other apomorphies are the presence of two longitudinal opposite grooves all along the nucleus (also present but differently shaped in the dipteran bombyliid Anthrax sp.; Jamieson et al. 1999), the presence of a peculiar glycocalyx organized as longitudinal ridges or filaments (somewhat similar to that of the strepsipteran Xenos vesparum; Dallai et al. 2003a), and the presence of two dense fibers extending along the axoneme and embedded into the centriole adjunct material forming the two accessory bodies. The last mentioned feature is a potential synapomorphy of Boreidae and Pistillifera. The sperm structure of Boreus hyemalis (Dallai et  al. 2003b) and Caurinus (see Section 2.3.8) supports the monophyly of Mecoptera as suggested by Wiegmann et al. (2009) and Beutel et al. (2011), but is in contrast to a sister-group relationship between Boreidae and Siphonaptera as proposed by Whiting (2002). Information on the hitherto unknown sperm ultrastructure of Nannochoristidae is necessary for a reliable phylogenetic interpretation. Rolf G. Beutel & Kenny Jandausch

3.3.9 Digestive system (based on Potter 1938a) Selected internal organs of Boreus hyemalis were treated in a comprehensive study on the anatomy of Mecoptera by Potter (1938a).

3.4 Morphology of larvae  



Mtub

salg

ph

 149

hg

oes

br mg res pph

soeg

re

prv Mtub

sald ros salg

abds reo

Fig. 3.3.9.1: Boreus hyemalis, female, alimentary tract with salivary glands and Malpighian tubules. Abbreviations: abds – abdominal segment, br – brain, hg – hindgut, mg – midgut, Mtub – Malpighian tubule, oes – oesophagus, ph – pharynx, pph – prepharynx, prv – proventriculus, re – rectum, reo – rectal opening, res – salivary reservoir, ros – rostrum, sald – salivary duct, salg – salivary gland, soeg – suboesophageal ganglion. Redrawn and modified from Potter (1938a).

Like in Caurinus and other mecopterans, the unpaired distal part of the salivary duct opens into a salivarium, which is dorsally delimited by the strongly sclerotized ventral wall of the anterior hypopharynx and ventrally by the frontal prelabial surface. The fine salivary duct divides into paired branches in the cervical region. The branches run on either side of the ganglionic chain and very shortly expand into thin-walled reservoirs. The duct leading from the reservoir is strongly wrinkled and its diameter is decreasing posteriorly. In the midgut region, the ducts enter the salivary glands, each dividing into short paired tubes, which again split into two long tubules. Two of the tubes are closely adjacent to the duct and reservoir of their side, whereas the other two lie close to the gut. In contrast to Panorpa, the glands are similar in both sexes (Fig. 3.3.9.1; Potter 1938a). The oesophagus entering the thorax is narrow but expands into a large, bluntly cone-shaped proventriculus before it connects with the midgut (Fig. 3.3.9.1). The midgut is comparable in length to that of Chorista australis Klug and Merope tuber Newman but distinctly shorter than that of Panorpa communis and much shorter than that of Bittacus pilicornis Westwood (Potter 1938a: figs. 1 and 5). Anterior caeca are missing and regenerative crypts are also absent. Posteriorly, the midgut narrows

into a thin tube (Fig. 3.3.9.1). The anteriormost hindgut region, where the six Malpighian tubules originate, is expanded as a pylorus (Fig. 3.3.9.1). The elongate tubules are placed close together on the ventral and lateral surface of the midgut and their distal parts end freely in the body cavity. The hindgut posterior to the pylorus narrows and coils slightly in the abdomen. In the posterior abdominal region, it expands into a rectum with a strongly muscular wall. The posterior rectal part narrows again and opens on segment X in males and XI in females (Potter 1938a).

Rolf G. Beutel, Hans Pohl & Frank Friedrich

3.4 Morphology of larvae

Like in Caurinus (Russell 1979, 1982, Fabian et al. 2015), the larvae of Boreinae (Fig. 3.4.1) are characterized by a distinctly sclerotized orthognathous head and an unsclerotized postcephalic body with a rather irregular surface structure, the former with a brown coloration and the latter largely unpigmented. In contrast to the very slightly curved larvae of Caurinus, the larval abdomen is distinctly curved downward in Boreinae (Cooper 1974: fig. 3 D,F; Russell 1979: C-shaped, scarabaeiform). Deep,

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

nearly vertical folds are present in the thoracic region of Boreus. The legs of boreine larvae are distinctly shortened and simplified, and the insertion of the prothoracic pair shifted mesad. The total length of the first instars of Boreus hyemalis is ca. 0.9 mm but would be slightly above 1 mm with a stretched abdomen. Mature larvae of B. brumalis and B. coloradensis reach a length of 4.8 mm (Byers 1987). The body length of the first instars of H. notoperates is 0.9 mm, and the length of the last instar ranges between 2.6 mm and 3.7 mm (Cooper 1974). The larva of H. notoperates is very similar to the immature stages of Boreus in its general morphology (see Russell

A

stef

fs

hc 1

lbr md

spi

3.4.1 Head

2

3.4.1.1 Head capsule

mx 3

leg1 leg2

I

B

leg3 II

III

IV

V

VI

VII X

IX

1979: table 15) but differs from the larvae of B. hyemalis in the following features according to Cooper (1974): shape of the head capsule, configuration of palps, maxillary brushes, prementum and mandibular teeth, one less seta on the palpifer, presence of a complete frontal suture (also present in some other species of Boreus; Cooper 1974), distinct frontoclypeal strengthening ridge (also present in B. westwoodi and B. brumalis; Cooper 1974) and sclerotized clypeal band, emarginated labrum, and details of the chaetotaxy (Cooper 1974). The dorsal and less so the lateral regions of the postcephalic segments of species of Boreus (B. brumalis and B. westwoodi) display regularly distributed bristles inserted on tubercles (Kaltenbach 1978), whereas the dorsal, transverse patches of denticles are present on abdominal tergites II-V in H. notoperates (Cooper 1974).

VIII

Fig. 3.4.1: Hesperoboreus notoperates, larvae, lateral view. A, Last instar (1–3: thoracic segments; I–X: abdominal segments); B, first instar. Abbreviations: fs – frontal suture, hc – head capsule, lbr – labrum, md – mandible, mx – maxilla, spi – spiracle, stef – field of stemmata. Scale bar: 100 µm. Redrawn from Cooper (1974).

Like in Caurinus the larval head is sclerotized, orthognathous, and nearly completely exposed, with only a very short dorsal and dorsolateral part retracted below the cervical membrane. The head capsule is slightly compressed along the antero-posterior axis; like in Caurinus, it is nearly round in frontal view. A slightly curved distinct occipital furrow originates from a distinct dorsolateral triangular incision and obliterates on the posterior third of the head capsule (ca. 0.1 mm long in first instars of B. hyemalis). The cuticular surface is smooth on all regions of the head. A rather spares vestiture of long, unbranched setae is present. An egg burster is missing in first instars (Russell 1979). The coronal suture is indistinct but present and long. Posteriorly, the frontal sutures are distinct and enclose a V-shaped posterior frontal region; the anterior parts are obliterated. Anterior (adfrontal) cranial strengthening lines are absent like in Caurinus and Nannochorista (Beutel et al. 2009). Externally, the frontoclypeal strengthening ridge is only distinct laterally; internally, it is less prominent than in Nannochorista and Panorpa (Beutel et al. 2009). The trapezoid clypeus, less transverse than in Caurinus, is about half as long as the width at the posterior margin. A division into a postclypeus and an anteclypeus is indistinctly recognizable. The lateral edges converge distinctly anteriorly. The slightly concave anterior margin is directly adjacent with the posterior labral edge, without a visible frontoclypeal membrane. Four setae are arranged in a slightly curved row on the clypeal surface (C2, C3). A gula and a hypostomal bridge are absent. Cervical sclerites appear to be present ventrolaterally but are not distinctly developed in first instar larvae.

3.4 Morphology of larvae  



3.4.1.2 Tentorium The tentorium is very similar to that of Caurinus in its general configuration, but dorsal arms are absent (Beutel et al. 2009).

3.4.1.3 Light sense organs Three stemmata are present on both sides of the head (Fig.  3.4.1), without convex cuticular lenses (not visible on SEM micrographs) but with intensely black pigment aggregations underneath them (Potter 1938b: fig. 6, Byers 1987). A well-organized rhabdom and dioptric apparatus are present according to Melzer et al. (1994), who suggested homology with ommatidia of the “Panorpa-type” (secondary larval compound eyes).

cly

 151

lbr ant

stef pmt

md mxp psm

leg2

leg1

leg3

3.4.1.4 Chaetotaxy The cephalic chaetotaxy is similar to the pattern in Caurinus, but the setae are much longer (0.5–0.6 mm in larvae with a body length of 2–3 mm; Russell 1979). They are unbranched like in Caurinus.

3.4.1.5 Labrum The labrum is about two thirds as long as the clypeus and its lateral edges are nearly parallel sided, only very slightly converging distad (Fig. 3.4.1.1). The frontal surface of the labrum is smooth. The rounded distal margin bears six stout setae and very densely arranged flattened setae are present posterior to them. Musculature: Similar to the condition observed in Caurinus. M. labroepipharyngalis (M.  7) and M. frontolabralis (M.  8) are well-developed, and M. frontoepipharyngalis (M. 9) is absent (Beutel et al. 2009).

3.4.1.6 Antennae Like in Caurinus, the antennae are very short and twosegmented (Fig. 3.4.1.1). The very wide antennomere 1 is inserted in a membranous articulatory area laterad the posterolateral edge of the postclypeus and above the mandibular base. The much narrower cylindrical antennomere 2 bears two elongate sensilla on its apex. Placoid sensilla are missing in the apical membrane of antennomere 1.

Fig. 3.4.1.1: H. brevicaudus, larva, ventral view, SEM. Abbreviations: ant – antenna, cly – clypeus, lbr – labrum, md – mandible, mxp – maxillary palp, pmt – prementum, psm – postmentum, stef – field of stemmata. Scale bar: 100 µm. Modified from Beutel et al. (2014). © Hans Pohl.

Musculature: two extrinsic antennal muscles are present, one of them arising from the anterior t­ entorial arm and one from the hypopharyngeal tentorium (Beutel et al. 2009).

3.4.1.7 Mandibles The stout mandibles are similar to those of Caurinus but are largely exposed in their resting position. They articulate with the head capsule in a typical dicondylic manner, with their relatively broad bases widely separated. A prostheca and mola are not developed and a lacinia mobilis is also missing. The distal part, which is distinctly darkened, bears a blunt apex and subapical teeth, followed by a small and more pointed additional tooth and a shallow convexity (two to three apical teeth according to Russell 1979). A seta is inserted near the lateral mandibular base. Musculature: like in Caurinus.

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

3.4.1.8 Maxillolabial complex

3.4.1.9 Preoral cavity and pharynx

Like in Caurinus, the maxillae and labium form a functional complex, which is retracted and thus widely separated from the mandibular base; posteriorly, the combined structure ends with a posteroventral membranous region adjacent with the ventral cervical membrane. The cardo is present as a distinctly developed, obliquely triangular sclerite, narrowing laterally, with a nearly straight lateral edge and a single seta. A backward directed mesal process is absent (Beutel et al. 2009). A distinct oblique suture separates it from the large basistipes, which has a concave lateral edge and two long setae inserted on its surface, the longer one close to the lateral margin. The dististipes is well-developed, separated from the basistipes by a deep transverse fold and connected with it by an articulatory membrane. Laterally, it bears two-segmented palps (Fig. 3.4.1.1); mesally, it is continuous with the undivided maxillary endite lobe. One seta is inserted on its middle region and one close to the endite lobe. The large basal palpomere is mesally not separated from the disti­ stipes. A seta is inserted close to its lateral edge. The distal palpomere is about as long as the lateral edge of the proximal one, cylindrical, with a rounded apical part densely set with short, apically rounded sensilla. The distal region of the endite lobe, which is not delimited from the apicomesal dististipital region, is densely set with stout setae inserted on densely arranged tubercles. In contrast to Caurinus, the labial elements are well-­ developed (Fig. 3.4.1.1). The postmentum is a fairly large transverse trapezoid sclerite. Two short setae are inserted on it, one of them close to the lateral margin. The convex posterior margin is adjacent with the membranous region at the posterior cephalic margin, the nearly straight anterior edge with the prementum (Fig. 3.4.1.1). The prementum is nearly twice as long as the postmentum. Posteriorly, it is as wide as the postmentum, but it is distinctly narrowing distally, with a concave lateral edge. An internal membrane connects the posterior edge with the postmentum. The straight anterior margin bears the palps. A ligula or labial endite lobes are not developed. The proximal cylindrical proximal palpomeres are separated by a little bit less than their diameter. They are about half as long as the prementum. Palpomere 2 is slightly shorter and very slightly widened distally. Its apical region is set with different sensilla, some similar to those on the distal maxillary palpomere, but one much longer and some of medium length. Musculature: maxillary muscles similar to those of Caurinus, with well-developed M. tentoriocardinalis (-basistipitalis) (M. 17) and M. tentorio-stipitalis (M. 18). Labial muscles are absent like in Caurinus.

No detailed data are presently available on the preoral cavity and pharynx, but the general features of the cephalic digestive tract are similar to the condition described for Caurinus. Musculature: M. clypeopalatalis (M. 43) is composed of several bundles. M. tentoriohypopharyngalis (M. 42) is apparently absent (in contrast to Caurinus; see Beutel et al. 2009). The precerebral and postcerebral pharyngeal dilators are well-developed. M. verticopharyngalis anterior (M.  51) is composed of two bundles, and M. tentoriopharyngalis (M. 52), of several bundles forming one functional unit.

3.4.1.10 Salivary ducts and glands An unpaired cephalic salivary duct opens on the hypopharynx. It divides into paired ducts below the subesophageal ganglion at the anterior prothoracic margin. These run up on either side of the ganglionic chain to the oesophagus, where each of them expands into a small thin-walled reservoir (smaller than in the adults and in larvae of Panorpa; Potter 1938b). The glands open into a long thin duct leaving the reservoir. They consist of four strongly coiled branches or tubules on both sides, but without a chainlike arrangement of gland cells as in larvae of Panorpa (Potter 1938b). The branches join in pairs before entering the duct. With their caudal parts, they reach the posterior end of the midgut, where each of them may fork again irregularly. One pair of tubules of each gland coils around the duct and reservoir (as in the adults; Potter 1938a, b), while the other pair is placed among the Malpighian tubules on the side of the intestine.

3.4.1.11 Brain, suboesophageal ganglion, and stomatogastric nervous system The brain is moderately sized in relation to the head size, apparently not affected by miniaturization. It lies transversely in the anterior region of the head like a dumbbell-shaped structure, with the thin optic lobe (optic nerve) laterally extending to the stemmata. The antennal nerve originates from the anteriorly projecting antennal lobe. The circumoesophageal connectives pass ventrally between the tentorial arms below the antennal lobes; they enter the suboesophageal ganglion below the tentorial bridge after forming a right angle. The large suboesophageal ganglion lies partly in the posterior cephalic region, but its main is shifted to the prothorax. The frontal ganglion

3.4 Morphology of larvae  



is large in relation to the size of the brain. It is less closely connected to it as in Caurinus. The nervus recurrens divides just behind the brain; the paired branches extend along the oesophagus on both sides and reach the midgut posteriorly.

3.4.2 Thorax The thorax is largely unsclerotized like in Caurinus and also subdivided by deep folds. Prominent setose dorsal and lateral lobes are present in Boreus (Figs. 3.4.1 and 3.4.1.1), but the fine microsculpture characteristic of ­Caurinus is missing. The tergal regions of the pro-, meso-, and metathorax, which are not present as well-defined sclerites, bear long setae, like the corresponding sternal areas. The upper pleural regions of the meso- and metathorax are subdivided by pleural ridges, which are externally visible as deep oblique folds. The threesegmented legs are much less reduced than in Caurinus. The insertion of the foreleg is shifted mesad, which results in an unusual vertical orientation (Fig. 3.4.1.1). The middle and hind legs are ventrolaterally directed; a large, fleshy ventral part of the pleura is present above them, separated from the dorsal pleural elements by a deep fold. The very wide and cylindrical coxae bear many small setae, especially at the distal margin, and a long seta is inserted anterodistally. The second leg segment is also large but conical, strongly narrowing toward the apex. The vestiture of short setae is similar to that of the coxa. The third and apical leg segment is much narrower than the proximal ones; it is cylindrical, apically rounded, and lacks claws. The small paired spiracles between the pro- and mesothorax comprise a double peritreme and atrium (elateroid type; Hinton 1947, Russell 1982).

3.4.3 Abdomen The abdomen is composed of 10 distinctly developed segments and an additional very short terminal segment XI. It is weakly sclerotized like the thoracic segments and unpigmented. A scarce vestiture of long setae is present (Fig. 3.4.1). Prolegs are missing on all segments. The tergal sculpture of segments I–III is similar to that of the metathorax, with the size of the setal lobes decreasing from I to III. Lateral setal lobes are present on segments I–IX, more conspicuous on the posterior segments. The curvature of the abdomen starts with segment V and is most pronounced between segments VI and VIII. Segment IX is slightly larger than VIII and forms an angle of about 90° with the longitudinal body axis in the thoracic region.

 153

The large segment X appears rounded and simplified in its structure, ring-like, and lacking folds and setose lobes. The very short, simple, and rounded segment XI is only slightly protruding from segment X. A distinctly fourlobed adhesive device of the abdominal apex is absent, even though the extrusible terminal segment XI can be used for attachment (Kaltenbach 1978). Small functional spiracles are present on segments I–VIII.

3.4.4 Postcephalic internal organs (based on Potter 1938b) 3.4.4.1 Fat body Masses of spongy, white fat body are present in the postcephalic body, covering the main tracheae, surrounding the hindgut and overlying the salivary glands.

3.4.4.2 Postcephalic digestive tract and Malpighian tubules The oesophageal tube is produced into the lumen of the midgut, forming an oesophageal valve (valvula cardiaca). A proventriculus is not developed. The midgut is short and very distensible due to its thin wall (Potter 1938b: “enormously swollen with fragments of moss leaves when the larva is feeding”). The lumen narrows toward the junction with the hindgut. A muscular constriction (valvula pylorica) is present in this region, and six free Malpighian tubules originate immediately close to it. The tubules are equally spaced around the gut; they are of even thickness throughout their length and lie freely in the abdomen, principally in the caudal region, but some of them pass forward before returning to the posterior abdominal area and surrounding the hindgut. The hindgut is coiled and of approximately uniform circumference. The anus is an elongate slit. Before reaching the anus, the hindgut expands slightly and is surrounded by a ring muscle and supported by lateral dilators. It then expands into a small membranous chamber surrounding the anus. A rectal expansion is lacking.

3.4.4.3 Postcephalic nervous system The prothoracic ganglion is distinctly separated from the suboesophageal ganglion and slightly more elongated than the more rounded following two thoracic ganglia. The connectives between the pro- and mesothoracic ganglia

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

are distinctly elongated. The eight abdominal ganglia are of rhomboid shape and only slightly smaller than those of the thorax; they are placed in abdominal segments I–VII. The posterior ganglionic complex VIII is slightly more elongated than the preceding ones. Two paired nerves arise from the meso- and metathoracic ganglia and from the ganglionic complex VIII, respectively, but only one pair from the others (Potter 1938b: fig. 12). It is possible that the nerve of the foreleg is ventrally directed and was therefore not depicted by Potter (1938b). Very fine segmental transverse nerves are connected to the ganglia of the preceding segments by a median nerve (ventral nerve, Leydig’s nerve).

3.4.4.4 Tracheal system The tracheal system (Potter 1938b: fig. 12) consists of two main tracheal trunks on each side, one dorsal and ant 1 fw

2 3

lbr

mxp

The dorsal vessel lies between muscle bundles close to the dorsal surface of the postcephalic body. It is a narrow, transparent-walled median tube extending through the length of the body. The heart lies close to the dorsal body wall in the abdomen, but the aorta in the region of the posterior oesophageal valve descends and runs along the oesophagus adhering closely to its dorsal surface. Anteriorly toward the head, it becomes more and more slender and terminates before the origin of the large pharyngeal dilators. The heart is lined by a single layer of large nephrocytes on either side of its posterior region. Chambers and ostia were not identified by Potter (1938b).

3.5 Morphology of pupae (mainly based on Williams 1916)

II

lap

3.4.4.5 Circulatory system

Rolf G. Beutel & Frank Friedrich

I

md

one ventral, connected by segmental anastomoses (Potter 1938b: fig. 12). Two large tracheae run from the welldeveloped first spiracle into the head. A vestigial stigmatic thread terminates between the meso- and metathorax. The ventral main trunk gives off branches to the salivary glands, the Malpighian tubules, the ganglionic chain, and to the digestive tract. Branches from the dorsal trunk pass to the dorsal regions of the body.

III leg1

IV V VI

leg2

VII VIII IX

leg3 X

Fig. 3.5.1: Boreus brumalis, pupa, female, lateral view. Abbreviations: 1–3 – thoracic segments, I–X – abdominal segments, ant – antenna, fw – forewing, lap – labial palp, lbr – labrum, md – mandible, mxp – maxillary palp. Scale bar: 1 mm. Redrawn from Williams (1916).

The coloration of Boreus brumalis Fitch is whitish in the earlier stages of pupation, but with darkened compound eyes and mandibles. The color of the body of mature pupae is brownish or greenish yellow, and the longer appendages, at first rather closely appressed to the body, show a tendency to move out of position (Williams 1916). A distinct vestiture of setae is present in a pupa tentatively assigned to Boreus elegans Carpenter by Russell (1979), distinctly longer than in Caurinus and Hespero­ boreus, probably forming a suspensory system. Longer setae are inserted on the head and dorsal and dorsolateral areas of the postcephalic body of B. brumalis, and a short transverse row of little thorns is present on either side of the middorsal line on abdominal segments II–V (Fig.  3.5.1;  Williams 1916). The surface of the cuticle is finely pointed-granulated (Williams 1916). In their general shape and size, the pupae are similar to the adult. The body length is 3.2–3.75 mm in pupae of B.  brumalis (Williams 1916) and about 6 mm in the pupa assigned to B. elegans (Russell 1979). The appendages are



free (pupa exarata; Fig. 3.5.1). The head is elongated, with a distinctly developed rostrum. The antennae reach the anterior margin of the abdominal segment IV posteriorly in B. brumalis (Williams 1916). The configuration of the ventral mouthparts is similar to the condition found in adults. However, the four-dentate pupal mandibles of B. brumalis (Williams  1916) are several times as large as the small bidentate mandibles of the adults. They were as long as two thirds the distance from their base to the lower portion of the compound eyes and varied slightly in the specimens (two females, one male) examined by Williams (1916). Two pairs of long, narrow wing cases are present in males, whereas only a single short pair is inserted on the mesothorax in females (Fig. 3.5.1). The pterothoracic notal regions are undifferentiated. The coxae are long and well-developed. The male genitalia are terminal and somewhat reflexed. In an advanced stage, the male pupae exhibit a stout upturned pair of chitinous clasping organs, which are strongly toothed on their concave border. In the female, the 11-segmented abdomen terminates in a more or less conical point, which encloses the inner portion of the secondary ovipositor. The outer blades of the egg-laying apparatus are ensheathed in a pair of ventrally appressed appendages that arise from abdominal segment VIII and do not reach the abdominal apex. The pupa becomes very active when disturbed, moving the head up and down vigorously, opening and shutting the mandibles, and twisting the abdomen (Williams 1916).

Nobuo Suzuki & Rolf G. Beutel

3.6 Development (mainly based on Suzuki 1990) Hatching was observed in laboratory samples of eggs of Boreus hyemalis within 8 to 10 days, at 8.8°C, with about 50% mortality (Withycombe 1922, 1926). In contrast, Strübing (1950) reported a duration from 3 weeks (c. 20°C) to as long as 1½ months at 7°C, and 44 of 46 eggs of the investigated series hatched. A swelling of the egg prior to hatching was described by Strübing (1950) (also described in in other groups of Mecoptera; e.g. Setty 1940, Byers 1963), and the process took 10–12 minutes in B. hyemalis. It was shown by Strübing (1950, 1958) that the rate of development in B. hyemalis is strongly affected by temperature. Eggs and larvae develop only very slowly, if at all, at low temperatures. The eggs remain dormant through the winter months, normally hatching in the period from the end of March to mid-April.

3.6 Development (mainly based on Suzuki 1990) 

 155

The development of Boreus westwoodi and species of Bittacidae, Panorpidae, and Panorpodidae was described in a comprehensive study by Suzuki (1990). The samples of B. westwoodi were obtained in Tübingen (Germany) in December 1979. Eggs were collected from moss and reared and fixed by Drs. G. Mickoleit and E. Mickoleit. As the precise age of the fixed eggs was unknown, only histological features in early and middle embryonic development were described by Suzuki (1990). Stage 1: Maturation of the female pronucleus and fertilization were not observed. When the sixth cleavage occurs, the cleavage cells are located in a zone ca. 0.1 mm distant from the egg surface. After this, cells move toward the egg periphery and increase in number. The cell membranes appear and the blastoderm is completed. Stage 2 (Fig. 3.6.1 A): After completion of the thin cellular blastoderm, an elliptical embryonic area or ventral plate differentiates. It is composed of vacuolated cells, which are much thicker than the extraembryonic cells. The lateral plates and the middle plate, which later forms the mesoderm, are distinguishable in the anterior part of the embryonic area. Stage 3 (Fig. 3.6.1 B,C): A pear-shaped embryo becomes recognizable. Its ventral side is covered by a thick, vacuolated amnion. The embryo elongates and a notch appears in the center of the anterior margin of the forming protocephalon. The middle plate becomes tubular and invaginates along the median line of the embryo. As development proceeds, the tubular form of the median plate breaks down in the anterior embryonic region, whereas it persists in the posterior part, until it obliterates in stage 4. Stage 4 (Fig. 3.6.1 D): The prospective stomodaeum becomes visible in the center of the protocephalon as a shallow invagination. The gnathal and thoracic segments are differentiated. The caudal end of the embryo is located at the posterior egg pole. At the end of this stage, neuroblasts appear in the gnathal and following segments. About 10 pairs of neuroblasts become visible in the thoracic segments. The primary median mesoderm migrates laterad. The segmentation of the mesoderm occurs in the gnathal and thoracic segments before the ectodermal segmentation becomes apparent. At the end of stage 4, about 15 prospective germ cells are found on the mesodermal cell mass of abdominal segment X. The developing proctodaeum sinks into the yolk in the middle of stage 4. Stage 5 (Fig. 3.6.1 E,F): The embryo elongates and its abdomen comprises 10 segments. Segments VII–X are narrower than I–VI. Small paired labral and antennal anlagen appear on the protocephalon, and paired anlagen of the gnathal and thoracic appendages also become recognizable. Neuroblasts appear in the protocephalic ectoderm.

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 3 Neomecoptera, Boreidae, Boreinae, Boreus, and Hesperoboreus

sd eea

mds pcep

mxs

pcep

las

ea

A lbr

ts1

pc

pc

B

C

D md mx

ants

ant

mxp la leg2

mds mxs las leg1

E

abdsX

F

abdsIII

G

H

Fig. 3.6.1: Boreus westwoodi, developmental stages. A, Ventral view of egg in early stage 2; B, embryo in early stage 3; C, embryo in late stage 3; D, embryo in stage 4; E, embryo in stage 5 (dorsal view); F, embryo in stage 5 (ventral view); G, embryo in stage 6 (lateral view); H, embryo in stage 6 (ventral view). Abbreviations: abdsIII/X – abdominal segment III/X, ant – antenna, ants – antennal segment, ea – embryonal area, eea – extraembryonic area, la – labium, las – labial segment, lbr – labrum, md – mandible, mds – mandibular segment, mx – maxilla, mxp – maxillary palp, mxs – maxillary segment, pc – protocorm, pcep – protocephalon, sd – stomodaeum, ts1 – first thoracic segment. Scale bar: 100 µm. Modified from Suzuki (1990). © Nobuo Suzuki.

Stage 6 (Fig. 3.6.1 G,H): Paired spiracles appear on the mesothorax and on abdominal segments I–VIII. The labial anlagen move medioventrad. The developing thoracic appendages are divided into three subunits. Paired small swellings appear on abdominal segments I–VIII, aligned with the anlagen of the thoracic legs. In contrast to Caurinus (Russell 1979), the newly hatched first instars of Boreus and H. notoperates lack a cephalic egg tooth (see Section 3.2.5). They penetrate the chorion with their sharp mandibular teeth (Cooper 1974; L. Russell, personal communication).

3.7 References Aubrook, E.W. (1939): A contribution to the biology and distribution in Great Britain of Boreus hyemalis (L.) (Mecopt., Boreidae). Journal of the Society for British Entomology 2: 13–21.

Beutel, R.G., Friedrich, F. & Whiting, M.F. (2008): Head morphology of Caurinus (Boreidae, Mecoptera) and its phylogenetic implications. Arthropod Structure & Development 37(5): 418–433. Beutel, R.G., Kristensen, N.P. & Pohl, H. (2009): Resolving insect phylogeny: the significance of cephalic structures of the Nannomecoptera in understanding endopterygote relationships. Arthropod Structure and Development 38(5): 427–460. Beutel, R.G., Friedrich, F., Hörnschemeyer, T., Pohl, H., Hünefeld, F., Beckmann, F., Meier, R., Misof, B., Whiting, M.F. & Vilhelmsen, L. (2011): Morphological and molecular evidence converging upon a robust phylogeny of the megadiverse Holometabola. Cladistics 27(4): 341–355. Beutel, R.G., Friedrich, F., Ge, S.-Q. & Yang, X.K. (2014): Insect Morphology and Phylogeny. A Textbook for Students of Entomology. De Gruyter, Berlin, New York, New York. Biliński, S.M. & Büning, J. (1998): Structure of ovaries and oogenesis in the snow scorpionfly Boreus hyemalis (Linne) (Mecoptera: Boreidae). International Journal of Insect Morphology and Embryology 27(4): 333–340. Biliński, S.M., Büning, J. & Simiczyjew, B. (1998): The ovaries of Mecoptera: basic similarities and one exception to the

3.7 References 

rule. Folia Histochemica Et Cytobiologica/Polish Academy of Sciences, Polish Histochemical and Cytochemical Society 36(4): 189–195. Blades, D.C. (2002): A new species of Boreus (Mecoptera: Boreidae) from Vancouver Island, British Columbia. Journal of the Entomological Society of British Columbia 99: 133–140. Bratton, J. (2001): Not quite observations of snow fleas Boreus hyemalis (L.) feeding. Entomologists Record and Journal of Variation 113: 184–186. Burrows, M. (2011): Jumping mechanisms and performance of snow fleas (Mecoptera, Boreidae). Journal of Experimental Biology 214(14): 2362–2374. Byers, G.W. (1961): An unusual new species of Boreus (Mecoptera: Boreidae) from Oregon. Journal of the Kansas Entomological Society 34(2): 73–78. Byers, G.W. (1963): The life history of Panorpa nuptialis (Mecoptera: Panorpidae). Annals of the Entomological Society of America 56(2): 142–149. Byers, G.W. (1987): Order Mecoptera. In Stehr, F.W. (ed.) Immature Insects, Vol. I. Kendall/Hunt Publishing Company, Dubuque, Iowa: 246–252. California Academy of Sciences (Entomology): World checklist of extant Mecoptera species. Boreidae (winter scorpion flies). http://researcharchive.calacademy.org/research/entomology/ Entomology_Resources/mecoptera/boreidae.htm (accessed 16.1.2017). Cockle, J.W. (1914): The mating of Boreus californicus. Proceedings of the British Columbia Entomological Society 4: 52–54. Cooper, K.W. (1940): The genital anatomy and mating behavior of Boreus brumalis Fitch. (Mecoptera). The American Midland Naturalist 23: 354–367. Cooper, K.W. (1972): A southern Californian Boreus, B. notoperates n. sp. I. Comparative morphology and systematics (Mecoptera: Boreidae). Psyche 79(4): 269–283. Cooper, K.W. (1974): Sexual biology, chromosomes, development, life histories and parasites of Boreus, especially of B. notoperates. A Southern California Boreus. II. (Mecoptera: Boreidae). Psyche 81(1): 84–120. Courtin, G.M, Shorthouse, J.D. & West, R.J. (1984): Energy relations of the snow scorpionfly, Boreus brumalis (Mecoptera) on the surface of the snow. Oikos 43: 241–245. Dallai, R., Beani, L., Kathirithamby, J., Lupetti, P., Afzelius, B.A. (2003a): New finding on sperm ultrastructure of Xenos vesparum (Rossi) (Strepsiptera, Insecta). Tissue and Cell 35(1): 19–27. Dallai, R., Lupetti, P., Afzelius, B.A. & Frati, F. (2003b): Sperm structure of Mecoptera and Siphonaptera (Insecta) and the phylogenetic position of Boreus hyemalis. Zoomorphology 122(4): 211–220. Edwards, J.S. (1987): The leap of the snowflea. Proceedings of the Washington State Entomological Society 49: 819–820. Evans, J.R., Lih, M.P. & Dunwiddie, P.W. (eds.) (2003): Biodiversity Studies of the Hanford Site Final Report: 2002–2003. Prepared by The Nature Conservancy of Washington for the U.S Department of Energy and the U.S. Fish and Wildlife Service, Hanford Reach National Monument, in partial fulfillment of federal grant DE-FG-06-02RL14344 (August 29, 2003). Fabian, B., Russell, L., Friedrich, F. & Beutel, R.G. (2015): The morphology of the larval head of the enigmatic boreid

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Caurinus dectes (Mecoptera). Arthropod Systematics and Phylogeny 73(3): 385–399. Fraser, F.C. (1943) Ecological and biological notes on Boreus hyemalis (L.) (Mecoptera, Boreidae). Journal of the Society for British Entomology 2: 125–129. Füller, H. (1954): Das Thorakalskelett von Boreus westwoodi Hag. Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 73(4): 425–449. Füller, H. (1955): Die Muskulatur des Thorax von Boreus westwoodi Hag. Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 74(2): 189–210. Gabdullina, A.U. & Nikolajev, G.V. (2015): A new species of the scorpion-fly of the genus Boreus Latreille (Mecoptera, Boreidae) from Altai mountains, Kazakhstan. Euroasian Entomological Journal 14(1): 32–34. Hågvar, S. (2001): Occurrence and migration on snow, and phenology of egg-laying in the winter-active insect Boreus sp. (Mecoptera). Norwegian Journal of Entomology 48: 51–60. Heddergott, H. (1938): Kopf und Vorderdarm von Panorpa communis L. Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 65: 229–294. Hepburn, H.R. (1969): The skeleto-muscular system of Mecoptera: The head. University of Kansas Science Bulletin 48(17): 721–765. Hinton, H.E. (1947): On reduction of functional spiracles in the aquatic larvae of Holometabola, with notes on the moulting process of spiracles. Transactions of the Royal Entomological Society of London 98(10): 449–473. Hinton, H.E. (1971) Some neglected phases in metamorphosis. Proceedings of the Royal Entomological Society of London (C) 3: 55–56. Hori, S. & Morimoto, K. (1996): Discovery of the Family Boreidae (Mecoptera) from Japan, with description of a new species. Japan Journal of Entomology 64(1): 75–81. Hünefeld, F., Mißbach, C. & Beutel, R.G. (2012): The morphology and evolution of the female postabdomen of Holometabola (Insecta). Arthropod Structure and Development 41(4): 361–371. Jamieson, B.G.M., Dallai, R. & Afzelius, B.A. (1999): Insects. Their Spermatozoa and Phylogeny. IBH Publishing, Oxford. Kaltenbach, A. (1978): Mecoptera (Schnabelhafte, Schnabelfliegen). In: Helmcke J.-G., Starck, D. & Wermuth, G. (eds.) Handbuch der Zoologie IV Arthropoda. Insecta. Inst. 25. De Gruyter, Berlin, New York: 1–111. Looney, C., Freeman, M.M., Asche, M. & Zack, R.S. (2019): Snow Skorpionflies (Mecoptera: Boreidae) of the Hanford Reach National Monument. Pan-Pacific Entomologist 95(1): 1–12. Maier, C.T. (1984): Habitats, distributional records, seasonal activity, abundance, and sex ratios of Boreidae and Meropeidae (Mecoptera) collected in New England. Proceedings of the Entomological Society of Washington 86(3): 608–613. Melzer, R.R., Paulus, H.F. & Kristensen, N.P. (1994): The larval eye of nannochoristid scorpionflies (Insecta, Mecoptera). Acta Zoologica 75(3): 201–208. Mickoleit, G. (1971): Zur phylogenetischen und funktionellen Bedeutung der sogenannten Notalorgane der Mecoptera (Insecta, Mecoptera). Zoomorphology 69(1): 1–8. Mickoleit, G. (1974): Über die Spermatophore von Boreus westwoodi Hagen (Insecta, Mecoptera). Zeitschrift für Morphologie der Tiere 77(4): 271–284.

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Mickoleit, G. (2008): Die Sperma-Auspreßvorrichtung der Nannochoristidae (Insecta: Mecoptera). Entomologia Generalis 31(2): 193–226. Mickoleit, G. & Mickoleit, E. (1976): Über die funktionelle Bedeutung der Tergalapophysen von Boreus westwoodi (Hagen) (Insecta, Mecoptera). Zoomorphologie 85(2): 157–164. Penny, N.D. (1977): A systematic study of the family Boreidae (Mecoptera). University of Kansas Science Bulletin 51(5): 141–217. Penny, N.D. (2006): A review of our knowledge of California Mecoptera. Proceedings of the California Academy of Sciences 57(1/11): 365. Penny, N.D. & Byers, G.W. (1979): A check-list of the Mecoptera of the world. Acta Amazonica 9(2): 365–388. Plutenko, A.V. (1984): A new species of the genus Boreus (Mecoptera: Boreidae) from the Soviet Far East. Zoologicheskii Zhurnal 63: 778–781 (In Russian). Plutenko, A.V. (1985): New and little-known species of Mecoptera from the Soviet Far East. Entomologicheskoe Obozrenie 64: 171–176 (In Russian) (Entomological Review 64: 113–119). Potter, E. (1938a): The internal anatomy of the order Mecoptera. Ecological Entomology 87(20): 467–501. Potter, E. (1938b): The internal anatomy of the larvae of Panorpa and Boreus (Mecoptera). Proceedings of the Royal Entomological Society of London (A) 13(7–9): 117–130. Raemakers, I. & Kleukers, R.M.J.C. (1999): De sneeuwspringer Boreus hyemalis in Nederland (Mecoptera: Boreidae). Nederlandse Faunistiche Mededelingen 8: 1–10. Russell, L.K. (1979): A study of the armored boreid Caurinus dectes (Mecoptera). Unpublished PhD thesis, Oregon State University. Russell, L.K. (1982): The life history of Caurinus dectes Russell, with a description of the immature stages (Mecoptera: Boreidae). Entomologica Scandinavica 13(2): 225–235. Setty, L.R. (1940): Biology and morphology of some North American Bittacidae (Order Mecoptera). American Midland Naturalist 23(2): 257–353. Shorthouse, J.D. (1979): Observations on the snow scorpionfly, Boreus brumalis Fitch (Boreidae: Mecoptera) in Sudbury, Ontario. Quaestiones Entomologicae 15: 341–344. Simiczyjew, B. (2002): Structure of the ovary in Nannochorista neotropica Navás (Insecta: Mecoptera: Nannochoristidae) with remarks on mecopteran phylogeny. Acta Zoologica 83(1): 61–66. Simiczyjew, B. (2005): Ovary structure, oogenesis and phylogeny of Mecoptera. Zoologica Poloniae 50 (Suppl.): 5–52.

Simiczyjew, B. & Margas W. (2001): Ovary structure in the bat flea Ischnopsyllus spp. (Siphonaptera: Ischnopsyllidae). Phylogenetic implications. Zoologica Poloniae 46: 5–14. Sømme, L. & Østbye, E. (1969): Cold-hardiness in some winter active insects. Norsk entomologisk Tidsskrift 16: 45–48. Steiner, P. (1937): Beitrag zur Fortpflanzungsbiologie und Morphologie des Genitalapparates von Boreus hiemalis L. Zeitschrift für Morphologie und Ökologie der Tiere 32(2): 276–288. Strübing, H. (1950): Beiträge zur Biologie von Boreus hyemalis L. Zoologische Beiträge (N.F.) 1: 51–110. Strübing, H. (1958): Schneeinsekten. Die neue Brehm-Bücherei 220. Ziemsen Verlag, Wittemberg Lutherstadt. 47 pp. Sutton, G.P. & Burrows, M. (2011): Biomechanics of jumping in the flea. Journal of Experimental Biology 214: 836–847. Suzuki, N. (1990): Embryology of the Mecoptera (Panorpidae, Panorpodidae, Bittacidae and Boreidae). Bulletin of the Sugadaira Montane Research Center, University of Tsukuba 11: 1–87. Svensson, S.A. (1966): Studier over visa vinteraktiva insekters biologi. Norsk entomologisk Tidsskrift 13: 335–338. Tillier, P. & Ledys, P. (2008): Contribution à l’étude des Mécoptères de France. Quatrième partie: Boreus hyemalis (L.), une espèce commune dans le Val-d’Oise (Île-de-France, France). L’Entomologiste 64(6): 309–317. von Kéler, S. (1963): Entomologisches Wörterbuch mit besonderer Berücksichtigung der morphologischen Terminologie, 3rd ed., Akademie-Verlag, Berlin. Whiting M.F. (2002): Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31(1): 93–104. Wiegmann, B.M., Trautwein, M.D., Kim, J.-W., Cassel, B.K., Bertone, M.A., Winterton, S.L. & Yeates, D.K. (2009): Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biology 7: 34. Williams, F.X. (1916): The pupa of Boreus brumalis Fitch. Psyche 23(2): 36–39. Willmann, R. (1977): Redeskription von Boreus gigas Brauer (Boreidae, Mecoptera), zugleich ein Beitrag zur Variabilität von B. hyemalis (L.). Annalen des Naturhistorischen Museums in Wien 81: 525–532. Withycombe, C.L. (1922): On the life history of Boreus hyemalis L. Transactions of the Entomological Society of London 1921: 312–318. Withycombe, C.L. (1926): Additional remarks upon Boreus hyemalis L. Entomological Monthly Magazine 62: 81–83.

Rolf G. Beutel & Frank Friedrich

4 Phylogeny

The placement of Nannochoristidae and Boreidae is one of the most persistent problems in systematic entomology (e.g. Kristensen 1991, 1995, 1999, Whiting 2002, Willmann 2005, Beutel et al. 2009, 2011, Friedrich et al. 2013, Fabian et al. 2015). Therefore, it is not surprising that both groups were raised to ordinal rank by the eminent zoologist Howard E. Hinton, Boreidae as Neomecoptera (Hinton 1958), and Nannochoristidae as Nannomecoptera (Hinton 1981). Wood & Borkent (1989) suggested a sister group relationship between Nannomecoptera and Diptera (see also Oosterbroek & Theowald 1991), a concept that was tentatively followed by Beutel & Baum (2008) in a study on the cephalic anatomy of adults. Beutel & Baum (2008) proposed a clade (Siphonaptera + (Nannomecoptera + Diptera)), supported by mouthparts specialized on the uptake of liquid food and the presence of a postcerebral pharyngeal pumping apparatus. A clade comprising Boreidae and Siphonaptera was suggested by Whiting (2002) based on analyses of four genes (18S, 28S rDNA, COII, and EF1-α), and Nannochoristidae were placed as its sister group. This concept was supported by Simiczyjew (2002, 2005) based on evaluations of the ovary structure and oogenesis. Potential morphological synapomorphies of Boreidae and Siphonaptera were pointed out in Whiting (2002): a similar process of resilin secretion (pleural arch in fleas and wing case in Boreus) (Rothschild 1975, Schlein 1980), similar proventricular teeth (Richards & Richards 1969), and multiple sex chromosomes (Bayreuther & Bräuning 1971). Recent analyses in the 1KITE project (www.1kite.org) (K. Meusemann, personal communication) yield ambivalent results: either monophyletic Mecoptera with Boreidae as sister to Nannochoristidae + Pistillifera or, alternatively, Siphonaptera nested within mecopteran taxa as sister group of Nannochoristidae. Monophyletic Mecoptera were supported by analyses of six nuclear protein-coding genes (Wiegmann et al. 2009) and also by analyses of an extensive morphological data set (Beutel et al. 2011). Potential synapomorphies of Boreidae, Nannochoristidae, and Pistillifera are the presence of a male postabdominal genital capsule (not entirely closed in Boreidae but in Nannochoristidae and Pistillifera) and a stylar organ on the dististylus. A strong argument for a clade Nannochoristidae + Pistillifera is the absence of stemmata in the larvae of both https://doi.org/10.1515/9783110272543-004

groups and the presence of secondary larval compound eyes (Suzuki & Nagashima 1989, Melzer et al. 1994). Stemmata are arguably a groundplan apomorphy of Holometabola excl. Hymenoptera (=Aparaglossata) (Beutel et al. 2011, Peters et al. 2014). However, it is conceivable that the secondary compound eyes of typical larvae of Pistillifera (e.g. Bierbrodt 1942, Byers 1991, Tan & Hua 2008) and the aberrant light sense organs of larvae of Nannochoristidae (see Section 1.4.1; Melzer et al. 1994) have evolved independently. A basal placement of Boreidae in monophyletic Mecoptera implies that a sperm pump is completely absent in the groundplan of this group (e.g. Mickoleit 2008, Hünefeld & Beutel 2005), with sperm transfer via a spermatophore as in Boreidae (see Sections 2.2 and 3.2) as ancestral condition. Under this scenario, the sperm pump (Mickoleit 2008: “Sperma-Auspreßvorrichtung”) would be a synapomorphy of Mecoptera (in the broad sense) excl. Boreidae, with the relatively simple configuration of male Nannochoristidae as ancestral condition, possibly still with the formation of a spermatophore (Mickoleit 2008). The second scenario with a pattern ((Boreidae + Pistillifera) + (Nannochoristidae + Siphonaptera)) would suggest that slender prognathous larvae (see Section 1.4) are ancestral in Antliophora and the mecopteransiphonapteran clade, with grub-like larvae with postabdominal lobes and a more or less unsclerotized postcephalic body with folds and protuberances as synapomorphy of Boreidae and Pistillifera. The evolution of the larval eyes would remain ambiguous as light sense organs are completely missing in flea larvae. A sperm pump with a pistil chamber moved against a fixed pistil would be a potential synapomorphy of fleas and nannochoristids. Other shared features of the two taxa are the formation of a strongly sclerotized fulcrum as support of the roof of the endophallus by the phallobasis posterad the median septum and the formation of the fixed piston by the fulcrum and the endophallus roof (Mickoleit 2008). However, it was emphasized by Mickoleit (2008) that the entire configuration of the organ differs considerably in the two groups. The chamber consists of a dorsal sclerotized bulge in male fleas, whereas it is formed by a trough-shaped sclerite of the ventral endo­ phallic wall in males of Nannochorista. It is obvious that morphological characters of the mecopteran complex including Nannochoristidae and Boreidae remain ambiguous (e.g. Friedrich et al. 2013).

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 4 Phylogeny

Moreover, the potential to discover new phylogenetically informative features is probably very limited. At the same time, phylogenetic results obtained with very extensive molecular data sets (e.g. Misof et al. 2014; unpublished results of the 1KITE Antliophora subproject) are also ambivalent. Denser taxon sampling in phylogenetic investigations and analyses of the fossil record (e.g. Willmann 1987, Grimaldi et al. 2005, Ren et al. 2010), including anatomical reconstructions of amber material (e.g. Pseudopolycentropodidae) (Grimaldi et al. 2005, Ren et al. 2010), may possibly help to resolve the enigma in the future.

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