Snakes and Lace

The holometabolous insects—that is, the clade containing most insects with a complex life cycle including differentiated larval and pupal stages—is one of the most extensive radiations of animals on this planet. Much of this diversity is assigned to four major orders: wasps, moths, beetles and flies. But there are also a number of smaller lineages making up the holometabolous insects. Among these are the lacewings and their relatives in the clade Neuropterida.

Female snakefly Puncha ratzeburgi, copyright Hectonichus.

Modern members of the Neuropterida are generally recognised as belonging to three orders—the lacewings and ant-lions in the Neuroptera, the snakeflies in the Raphidioptera, and the alderflies and dobsonflies in the Megaloptera—though go back a few decades and you may find texts referring to a single order Neuroptera. A number of authors have advocated for use of the name 'Planipennia' for the lacewing order to avoid confusion with the broader sense of Neuroptera but, while a case could certainly be made for this usage, it's just never really caught on. Most neuropteridans are fairly similar in overall appearance: long-bodied insects with well developed wings with numerous crossveins. Of the living holometabolous insects, they probably bear the greatest overall resemblance to the clade's ancestors and hence they are commonly thought of as 'relicts'. However, they do possess their own specialisations and are not primitive in every regard (for instance, the most primitive egg-laying apparatus among holometabolous insects belong to wasps). Species of Neuropterida are mostly predators as larvae. The larvae of the lacewing family Ithonidae may possibly feed on decaying plant matter though we don't know for certain (Grimaldi & Engel 2005). Adults are predators and/or pollen-feeders, or may not feed at all in some short-lived forms.

Male (above) and female dobsonflies Corydalus cornutus, copyright Didier Descouens.

The exact relationships between the neuropteridan orders have been debated over the years. Though most of their obvious similaities to each other represent shared ancestral features, there is a broad consensus that they do indeed form a clade. There has also been little, if any, question of the monophyly of the Raphidioptera and Neuroptera; the monophyly of Megaloptera has been more debated but seems more likely than not. Most recent studies have suggested that the Raphidioptera are the sister group to a clade of the other two orders (Engel et al. 2018). Raphidioptera are the least diverse of the generally recognised living orders of insects with about 250 known species. They are found in cooler regions of the Northern Hemisphere—in the temperate zone or at higher elevations in lower latitudes—and are completely absent from the Southern Hemisphere (Aspöck & Aspöck, 1991, refer to a failed attempt to introduce them to Australia and New Zealand but provide no details why such a thing was tried in the first place). They are characterised by a notably elongate prothorax (the first segment of the thorax) which explains the vernacular name of 'snakefly'. Larvae live under bark or in litter and moult into pupae with the onset of cold weather. The pupae of Raphidioptera and Megaloptera are primitive in aspect, with legs separate from the body wall, and are highly mobile. Engel et al. (2018) even refer to the pupae of Raphidioptera as 'active predators' but I've not been able to find corroborating details for that remarkable description.

The Megaloptera are often particularly large neuropteridans, reaching up to twenty centimetres in wingspan, and comprise a bit less than 400 species worldwide, mostly found in temperate regions. Larvae are aquatic, living under rocks and debris, and characterised by the presence of filamentous lateral gills on the abdomen. Adults are short-lived and feed little if at all. Male dobsonflies (of the subfamily Corydalinae) possess spectacularly large, curved mandibles of largely unknown purpose; certainly they do not seem to use them for biting.

Mantisfly Mantispa styriaca, a raptorial lacewing, copyright Gilles San Martin.

The largest of the three orders, by a considerable margin, is the Neuroptera with over 5700 known species. Needless to say, this level of species diversity is associated with a high diversity of appearances and lifestyles, too many to cover adequately here. The larvae of two families of Neuroptera, the Nevrorthidae and Sisyridae, are aquatic and there has been a long-running debate whether this aquatic habit is an ancestral feature of the order shared with the Megaloptera (Nevrorthidae larvae are generalist predators, Sisyridae are specialised feeders on freshwater sponges and bryozoans). However, recent phylogenetic studies (e.g. Vasilikopoulos et al. 2020) do not agree with earlier hypotheses that the Nevrorthidae represent the sister taxon of the remaining Neuroptera. Instead, Nevrorthidae and Sisyridae may form a clade with the Osmylidae, a family whose larvae are not aquatic but often inhabit damp stream banks. The aquatic Neuroptera probably entered the water independently of the alderflies. The current favourites for the sister clade of other neuropterans are the dustywings of the Coniopterygidae, a group of small neuropterans with reduced wing venation that have historically been difficult to place owing to their derived features.

An unidentified dustywing, Coniopterygidae, copyright Katja Schulz.

A fourth order has often been associated with the Neuropterida, the extinct Glosselytrodea. Glosselytrodeans are small insects known from the Late Permian to the Jurassic, characterised by wings bearing dense cross-veins of which the fore pair would have had a leathery appearance in life (not dissimilar in texture to the fore wings of grasshoppers and other Orthoptera). Other than the wings, the features of glosselytrodeans are poorly known: they seem to have been hypognathous (i.e. had the head directed downwards) with slender legs (Grimaldi & Engel 2005). Connections to Neuropterida are based on features of the wing venation but cannot be considered strongly supported. Other authors have regarded them as of uncertain position within the broader holometabolous clade, or even as more closely related to the Orthoptera than any Holometabola. Unless more complete remains should come to light, it seems likely that the question will remain open.

REFERENCES

Aspöck, H., & U. Aspöck. 1991. Raphidioptera (snake-flies, camelneck-flies). In: CSIRO. The Insects of Australia: A textbook for students and research workers 2^nd ed. vol. 1 pp. 521–524. Melbourne University Press.

Engel, M. S., S. L. Winterton & L. C. V. Breitkreuz. 2018. Phylogeny and evolution of Neuropterida: where have wings of lace taken us? Annual Review of Entomology 63: 531–551.

Grimaldi, D., & M. S. Engel. 2005. Evolution of the Insects. Cambridge University Press: New York.

Vasilikopoulos, A., B. Misof, K. Meusemann, D. Lieberz, T. Flouri, R. G. Beutel, O. Niehuis, T. Wappler, J. Rust, R. S. Peters, A. Donath, L. Podsiadlowski, C. Mayer, D. Bartel, A. Böhm, S. Liu, P. Kapli, C. Greve, J. E. Jepson, X. Liu, X. Zhou, H. Aspöck & U. Aspöck. 2020. An integrative phylogenomic approach to elucidate the evolutionary history and divergence times of Neuropterida (Insecta: Holometabola). BMC Evolutionary Biology 20: 64.

Ant-lions of Australia

Austrogymnocnemia edwardsi, photographed by Shaun Winterton.
For today's post, I'll be looking at a group of lacewings known as the Periclystina. Earlier posts on lacewings have looked at members of the families Chrysopidae, Kalligrammatidae and Hemerobiidae; the Periclystina belong to a further family, the Myrmeleontidae. Myrmeleontids are commonly known as ant-lions (indeed, Myrmeleon is derived from the Greek words for 'ant' and 'lion'), particularly their larvae which are fat-bodied animals with large mandibles and flip-top heads. Ant-lion larvae dig themselves into soft ground at the bottom of a conical pit; when crawling insects such as ants walk over the edge of the pit, they end up sliding down to the bottom of the cone and into the waiting jaws of the ant-lion. Ant-lions can dig themselves into the ground quite quickly; this video from Wikipedia shows an ant-lion attempting to capture prey and digging itself into the ground.

Ceratoleon brevicornis, photographed by Shaun Winterton (again).
For all their charms, larval ant-lions could not be described as elegant animals. The adults, though, are as attractive as any lacewing, which is very attractive indeed. The Periclystina are a subtribe recognised by Stange (1976) within the tribe Dendroleontini of the subfamily Myrmeleontinae, and were distinguished by Stange from other dendroleontins primarily by features of the female genitalia (such as the absence of anterior gonapophyses). Stange included seven genera in the Periclystina, all of them endemic to Australia (one genus, Periclystus, has since also been found in New Guinea—New 1990). The Australian Dendroleontini were revised by New (1985), who pointed out that some of the features used by Stange (1976) to distinguish his subtribes were not entirely reliable. Though New did not formally dismantle Stange's system, it is telling that he did not make any attempt to place his own new genera within it, and Stange's subtribes may require further examination.

Angular-wing lacewing Periclystus circuiter, from Brisbane Insects.
Many Periclystina are large and eye-catchingly patterned. The species of Periclystus are particularly remarkable with oddly scalloped ends to their wings. The irregular wing shape together with their patchy markings function to camouflage the insect when it sits along a twig. Also remarkable is Ceratoleon brevicornis, with antennae much shorter than those of any other ant-lion. Other than that, I think the pictures I'm sharing with you here largely speak for themselves.

Glenoleon falsus, photographed by Donald Hobern.
REFERENCES

New, T. R. 1985. A revision of the Australian Myrmeleontidae (Insecta: Neuroptera). II. Dendroleontini. Australian Journal of Zoology, Supplementary Series 105: 1-170.

New, T. R. 1990. Myrmeleontidae (Insecta: Neuroptera) from New Guinea. Invertebrate Taxonomy 4: 1-20.

Stange, L. A. 1976. Classificacion y catalogo mundial de la tribu Dendroleontini con la redescripcion del genero Voltor Navas (Neuroptera: Myrmeleontidae). Acta Zoologica Lilloana 31: 261-322.

The Red-lined Wings of South America

So far as I've been able to find, what you see above is the only published illustration of the South American lacewing Belonopteryx arteriosa, from its original description by Gerstaecker (1863) (or very nearly from there: somewhat confusingly, the plate illustrating this animal was published an issue earlier than the article describing it). It is something of a pity that the drawing is not in colour, as Gerstaecker's description indicates a quite handsome animal: about 16 mm long with a ca 20 mm wingspan* with a mostly orange head, golden yellow body and blood red veins on the wings. The first segment of the antenna was yellow, the second darker, and the remainder black. Along the medial and secondary radial veins, the red colour of the veins extended to part of the cells on either side, producing two longitudinal red stripes on each wing.

*Gerstaecker gives the body length as 8 lines, with the front wings 9.5 lines long. A 'line' is a unit of measurement used by a number of 18th and 19th century biologists. The exact length of a line seems to have varied somewhat between countries (see this page for explanations), though it seems to have generally been a little more than 2 mm. Linnaeus apparently defined a line in the introduction to Philosophia Botanica as the length of a lunule (the white half-moon at the base of a fingernail) on any finger other than the thumb.

Despite being the type of the tribe Belonopterygini, Belonopteryx arteriosa seems to have received little attention since its description. Gerstaecker (1863) held only a single female specimen, reporting its collection locality (with a precision not uncommon for his time) as "Brazil". Freitas & Penny (2001) indicated that this species was known only from three specimens from Argentina (whether this indicates that Gerstaecker's locality was mistaken, or whether this is in addition to the original location, I couldn't say). The larva of B. arteriosa has never been identified, though larvae of related genera are associated with ant nests.

REFERENCES

Freitas, S. de, & N. D. Penny. 2001. The green lacewings (Neuroptera: Chrysopidae) of Brazilian agro-ecosystems. Proceedings of the California Academy of Sciences 52 (19): 245-395.

Gerstaecker, A. 1863. Ueber einige neue Planipennien aus den familien der Hemerobiiden und Panorpiden. Entomologische Zeitung 24 (4-6): 168-188 (plate in issue 1-3).

Name the Bug: Psectra diptera

The points for this one go to Kai, who successfully identified this as a flightless hemerobiid lacewing:


Psectra diptera, from MacLachlan (1868).

Psectra diptera is found in both Europe and North America but is apparently nowhere very common (a live photo can be seen here). Gunnar pretty much gave the reasons for identifying this insect as a lacewing in his comment: the high density of veins (particularly cross-veins) in the wings and the long, filamentous antennae (but lost out on the marks by assuming that it must be a fossil).

Of course, lacewings normally have four wings, not two. Many basic references on insects will indicate that the only group of insects with a single pair of developed wings* is the Diptera, the true flies, but diptery is also found among Strepsiptera, mayflies, scale insects, lacewings, Psocodea and snowfleas** (and probably a couple of others that I've forgotten). Different processes seem to have resulted in wing loss in different lineages—among lacewings and psocops, for instance, it is associated with loss of flying ability, but Diptera and mayflies are capable of aerobatics that few other insects can rival.

*Technically, Diptera do still have their hindwings: they've been altered into small knobbed rods called halteres. Hindwing halteres are unique to flies among living insects. Strepsiptera have the forewings altered into halteres; scale insects have knobless filaments called hamulohalteres; and hindwing halteres were present in the Cretaceous lacewing Mantispidiptera.

**Though the appendages of male snowfleas are just so freakishly bizarre (as described in the linked post) that I rather feel calling them wings is a little like calling a whale's flippers 'legs'. It may be correct in an evolutionary sense but it's a little ridiculous by any other measure.

As noted by the commenter 'Reprobus', Strepsiptera are a little different from the other entries in the list in that they have lost the forewings instead of the hindwings. Relatively few groups of insects have larger hindwings than forewings: Orthoptera (crickets and grasshoppers), stick insects, earwigs, some beetles. All of these have the forewings protectively hardened to some degree, and in earwigs and beetles the forewings have become entirely hardened into protective cases called elytra. The evolutionary affinities of Strepsiptera are decidedly contentious (see the post linked to above) but some authors have suggested a relationship to beetles (and one recent molecular study has provided further support for this relationship: Longhorn et al., 2010). If so, strepsipterans may have been derived from ancestors that also had hardened forewings that were no longer functional when flying, potentially explaining why that was the pair that was lost.

REFERENCES

Longhorn, S. J., H. W. Pohl & A. P. Vogler. 2010. Ribosomal protein genes of holometabolan insects reject the Halteria, instead revealing a close affinity of Strepsiptera with Coleoptera. Molecular Phylogenetics and Evolution 55 (3): 846-859.

MacLachlan, R. 1868. A monograph of the British Neuroptera-Planipennia. Transactions of the Royal Entomological Society of London 1868: 145-224.

Name That Bug: Meioneurites spectabilis

Meioneurites (Parameioneurites) spectabilis (from Engel, 2005).

This image wasn't up ten minutes before being identified by Adam Yates. Meioneurites spectabilis is a member of the Jurassic butterfly-like lacewing family Kalligrammatidae. Kalligrammatids have been featured on Catalogue of Organisms previously.

In the fossil above, you can see that kalligrammatids lacked the coiled proboscis of a butterfly (though their mouthparts are much more elongate than other lacewings, and kalligrammatids were probably nectar feeders like butterflies). Also, if you look very closely at the wings (you'd probably have to zoom in), you may be able to make out that there is a higher density of veins in the wings than in butterflies.



For comparison, here's another kalligrammatid, Sophogramma lii, in a figure from Yang et al. (2009). Pretty.

REFERENCES

Engel, M. S. 2005. A remarkable kalligrammatid lacewing from the Upper Jurassic of Kazakhstan (Neuroptera: Kalligrammatidae). Transactions of the Kansas Academy of Science 108 (1-2): 59-62.

Yang Q., Zhao Y.-Y. & Ren D. 2009. An exceptionally well-preserved fossil kalligrammatid from the Jehol Biota. Chinese Science Bulletin 54 (10): 1732-1737.

Butterflies Before there were Butterflies

The giant Jurassic lacewing Kalligramma haeckeli being pursued by the small pterosaur Anurognathus ammoni. Reconstruction by Dmitry Bogdanov.

Lacewings are a remarkable group of insects. Though not an overly large order, they cover a wide diversity of forms, including large narrow-winged forms superficially not dissimilar to dragonflies (previously covered here), minute psocid-like taxa, species with large mantis-like raptorial forelimbs, and large broad-winged forms that might almost be mistaken for moths were it not for the lack of scales on the wings. One living family, the Nemopteridae, includes species in which the hindwings have developed into long ornamental streamers. But it is to the fossil-record that we must turn to see what were perhaps the most spectacular lacewings of all - the giant butterfly-mimics of the Kalligrammatidae.

Though perhaps it is more accurate to say that butterflies are kalligrammatid-mimics, because the kalligrammatids flew through Europe and central Asia in the late Jurassic, at least sixty million years butterflies were even thought of (Grimaldi & Engel, 2005). But while at no time did the two ever share a time-frame, if they could have been brought together the resemblance would have been striking. Kalligrammatids resembled lepidopterans even more than did other broad-winged lacewings because their wings were darkly coloured and densely setose, and their fossils even preserve evidence of bold patterns such as eye-spots. Like butterflies, kalligrammatids would have been slow but aerobatic fliers, and must have been a spectacular sight in the Jurassic forests.


Fossil of Kalligramma haeckeli, showing how the colour-pattern (if not the colour) of the wings remains discernable. Photo from here.

Most lacewings are known for being voracious predators, both as larvae and adults, but kalligrammatids had slender mouthparts that seem to have been developed for sipping nectar, yet another parallel to butterflies. No kalligrammatid larvae have yet been identified (and the extreme morphological differences between larvae and adults of holometabolous insects would make doing so all but impossible), so we have no idea if they shared their parents' genteel habits or whether they remained predatory (either is possible - some modern butterflies have predatory larvae). Specialised nectar-feeders are first recorded from the early Jurassic, though potential nectar production has been inferred from plants as old as the Permian, and many pre-Jurassic insects without obvious specialisations for nectarivory would have still been perfectly capable of feeding on nectar opportunistically if such a resource had been available (Zherikhin, 2002). Nectar is a feature today associated with flowers, and the existence of Jurassic nectarivores has been cited as evidence that angiosperms must have appeared much earlier than the Cretaceous age indicated by fossils (Ren, 1998), but such claims overlook the fact that, even among the modern flora, nectar or nectar-like fluids are also produced by cycads and gnetaleans, both of which (or their stem groups) were present in the Jurassic*. It seems more likely that nectar-feeding insects first evolved in concert with gymnospermous taxa, only to switch to angiosperms as they became the dominant flora.

*Besides, the specific fossils described by Ren (1998) come from the decidedly contentiously-dated Yixian Formation of China, and are quite likely early Cretaceous rather than Jurassic.


A modern thread-winged lacewing of the family Nemopteridae. Thread-wings are among the closest living relatives of the kalligrammatids, but other than that there's not much connection between this photo and the post. I just included it because nemopterids are pretty. Photo by Joaquim Maceira.

REFERENCES

Grimaldi, D., & M. S. Engel. 2005. Evolution of the Insects. Cambridge University Press: New York.

Ren, D. 1998. Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science 280: 85-88.

Zherikhin, V. V. 2002. Ecological history of the terrestrial insects. In History of Insects (A. P. Rasnitsyn & D. L. J. Quicke, eds.) pp. 331-388. Kluwer Academic Publishers.

Of Lions and Lace

The "non-green, green lacewing" (Catanach, 2007) Abachrysa eureka. Photo by M. C. Thomas.

There is a term that bird-spotters use to describe the ability to recognise what species a bird belongs to even if one cannot see the details of its features - they refer to the "jizz" of a bird, derived from the acronym GIS for "general impression and shape". The jizz of a bird species is not something that can be described easily, if at all - it is something that can really only be appreciated with experience. It should hardly come as a surprise that the same concept applies with identifying other organisms just as much as birds. Lacewings (Neuroptera) are a smallish order of insects (only about 5000 species) that include a diversity of forms, but many look at first glance not unlike small dragonflies. Still, a closer look will reveal significant differences to a dragonfly. For a start, lacewings have longer antennae and are able to fold their wings back over their abdomen in a way that no dragonfly can. There is also the feature that gives them their name - the wings of lacewings are particularly densely covered with veins, the little criss-crossing fluid-carrying lines that you can see on any insect wing. While you might need to look very closely indeed to see the individual veins, the cumulative effect of the dense veins is to give lacewing wings a distinctive shimmer, like light off satin, or the glimmer of colour across oil. This week's highlight taxon is a specific group of lacewings - the tribe Belonopterygini.

Lacewings have a complete metamorphosis, meaning they have a distinct larval stage separated by a dormant pupal stage from a very different-looking adult. Most lacewings start out life as formidable predators, and are quite recognisable by their large, protruding jaws. The most famous are the antlions of the family Myrmeleontidae, which dig themselves conical pits at the bottom of which they lie dug into the soil, waiting for any small insects unlucky enough to fall into the pit. While the large jaws are used for capturing and macerating prey, lacewing larvae are actually liquid feeders, injecting digestive saliva into their prey then sucking out the dissolved juices (Canard, 2007). One intriguing (yet kind of disgusting) feature of the order is that the midgut is not actually connected to the hindgut until pupation, meaning that the larva is not capable of defecation. Any indigestible waste products are stored in the gut until the lacewing reaches adulthood and passed after emerging from the pupa. Can you imagine the relief?


The belonopterygin Italochrysa insignis. This photo illustrates very well the distinctive shimmer that neuropteran wings possess in the right light and which I've found is actually one of the quickest ways to recognise an adult lacewing. Photo by Sheila.

Belonopterygini are a cosmopolitan tribe of a different family, the Chrysopidae (green lacewings), whose larvae are active hunters, many of them of economic significance as predators of plant pests such as aphids and thrips. Belonopterygin larvae are specialist associates of ant nests (Freitas & Penny, 2001), feeding on the ants therein. Unfortunately, such specialist habits make Belonopterygini one of the less-studied chrysopid groups, and I have been unable to find how the larvae evade detection by the ants. Like other chrysopids, belonopterygin larvae use small bits of soil and debris to disguise themselves, starting with the shell of the egg they hatched from (Catanach, 2007). Larvae of other chrysopids have been observed to incorporate the husks of drained prey into their trashy disguises so I would be interested to know if belonopterygins do the same, as has been described recently for assassin bugs.

Adult chrysopids may be predacious like the larvae, or they may feed on non-live food such as honeydew. Honeydew-feeding species possess diverticula in the gut that house symbiotic yeasts aiding the lacewing in digestion. Sounds produced by tapping the abdomen on the substrate are used by chrysopids in courtship, and the pattern of sounds produced may differ significantly between closely related species (New, 1991). Eggs are laid perched on the end of long silk threads.

REFERENCES

Canard, M. 2007. Natural food and feeding habits of lacewings. In Lacewings in the Crop Environment (P. McEwen, T. R. New & A. Whittington, eds.) pp. 116-129. Cambridge University Press.

Catanach, T. A. 2007. Abachrysa eureka (Banks) (Neuroptera: Chrysopidae): egg, first instar larva and biological notes. Unpublished thesis, Texas A & M University.

Freitas, S. de, & N. D. Penny. 2001. The green lacewings (Neuroptera: Chrysopidae) of Brazilian agro-ecosystems. Proceedings of the California Academy of Sciences 52: 245-395.

New, T. R. 1991. Neuroptera. In The Insects of Australia (CSIRO, ed.) pp. 525-542. Melbourne University Press.