Tuesday, January 8, 2013

Mantidflies: Chimeras of the Insect World

File:Chimera d'arezzo, fi, 04.JPG
The Chimera of Arezzo, an Etruscan effigy of the monster
Now it's time to post on creatures that I've wanted to discuss for along time: mantidflies. I was immensely gratified when I finally collected one (Dicromantispa sayi) this past June. These insects are uncommon and little-known outside of the entomological community, which is a pity, given their strangeness–both in their chimerical morphology and weirdo ontogeny.

How is a mantidfly akin to the Chimera–a monstrous fire-breathing beast of Greek myth? This fictitious creature had the body (and head) of a lion, a serpentine tail with a snake's head at its tip, and a dorsal goat's head to boot: consequently, the name has become a byword in biology for an organism assembled from unrelated parts. Mantidflies (Mantispidae) certainly look as though they were haphazardly crafted in this fashion: they have the abdomen, wings, and thorax of a lacewing attached to the head, pronotum, and forelegs of a mantis. This confusion of insect bodies is compounded in Climaciella brunnea, a common North American species, since it does a very passable impersonation of a paper wasp (Polistinae), as seen below.

BG2324 E5758 - Climaciella brunnea - male
A Louisianan C. brunnea, photographed by Gayle Strickland
Mantidflies' marked likeness to their namesakes is the result of convergent evolutionthe two insects could not be more unrelated, as one can readily see from mantispid ontogeny (more about that later). But, as one would surmise from those ferocious grabbing chelae, the members of the Mantispidae are predators just as the mantises (although small ones: 2-3.5 cm.). To determine mantidflies' true provenance we must disregard their body-parts from the mesothorax forward. Excluding those, it is obvious that the mantidfly is a member of the order Neuroptera, along with antlions, dustywings, owlflies and all manner of lacewings. Among the other families of this order (collectively called "net-winged insects"), the Mantispidae are most akin to the beaded lacewings (Berothidae) and thorny lacewings (Rhachiberothidaeformerly sunk into the Berothidae; Tjeder, 1959), with which they comprise the Mantispoidea. Both these lacewings are rather more conventional than their mantidfly cousins, although beaded lacewing larvae (or those in the sole North American genus) are odd in that they haunt termitaries, preying on the resident termites with the Fart of Death (actually a blast of deadly gas from anal glands; Johnson & Hagen, 1981). This would be a good place to engage in some middle-school fun at beaded lacewings' expense, but I'll refrain.

Lacewing - Lomamyia
Lomamyia sp., the only genus of beaded lacewing found in the United States; picture by Randy Hardy
Neuropterans are holometabolous: that is, their metamorphosis is complete (proceeding from larva to pupa to adult). That alone establishes the Mantispidae's un-relation to the order Mantodea, the constituents of which are nymphs (not larvae) when young (and thus hemimetabolous), even if a systematist ignored the obvious neuropteran affinity demonstrated by mantidflies' fossil record and wing venation. It is the particular mantispid mode of metamorphosis that completes their surreal persona. Ontogenetically speaking, however, the four mantidfly subfamilies differ substantially; so a description of each would probably be germane before I treat their metamorphoses.

The Symphrasinae are the most plesiomorphic of the foursome (since it's politically incorrect to call them "primitive") (Lambkin, 1986); thorny lacewings were once classified as mantidflies due to a noticeable similarity (Willmann, 1990). In line with their basal status, symphrasines have a short prothorax; they are presently restricted from South America north to the southwestern United States, although they had a presence in Germany in the Paleogene Period (Wedmann & Makarkin, 2007). To continue: the Drepanicinae are roughly as advanced as the Symphrasinae; they range throughout Australia and South America, but are known as fossils from the mid-Cretaceous of Kazakhstan (Makarkin, 1990). Unusually, the genus represented from that locality (Gerstaeckerella) is extant (Enderlein, 1910). The Calomantispinae are known only from Central America (north into the San Fernando Valley) and eastern Australia (all of Queensland, New South Wales, Victoria, and Tasmania), and have no fossil record; whilst the Mantispinae are by far the most widespread and diverse of the subfamilies, found in all the regions in which the other subfamilies are present (except Argentina and Tasmania) plus the rest of the world north to about 50°N (Wedmann & Makarkin, 2007) and lived on the Isle of Wight during the Paleogene Period (Jarzembowski, 1980).

Dicromantispa? - Plega
A Plega sp. (Symphrasinae) making rude tarsal gestures at the photographer (Marcela Freerks)
Now that we've gotten all of that under finger, I'll get on with the interesting stuff. The larvae of Calomantispinaethose that are knownhave a lifestyle typical of net-winged insects: that of mobile predators. Symphrasines and mantispines are the ones that "grow outside of the box", as it were (drepanicines' young remain unknown). The life-cycles of the mantidflies in the Symphrasinae remains poorly-studied; but what we do know shows us that as larvae they are parasitoids of bees and wasps (both solitary and social; Buys, 2008; Hook et al., 2010). Some have also been implicated as attackers of moth, fly, or beetle pupae (Parfin, 1958). How the larvae reach their hosts remains uncertain. They could, of course, be laid as eggs thereupon by their mothers, but the fact that intrusions into beehives by adult Plega hagenella are promptly foiled by the resident (and potential host) stingless bees (Meliponini) suggests that symphrasine larvae may have to seek hosts on their own (Maia-Silva et al., 2012): as do the mantispines (also parasitoids), which are comparatively well-studied.

Life cycle of Mantispidae
The hypermetamorphic stages of Mantispa sp., as shown in Introduction to Entomology (1933); not to scale
Members of the Mantispinae begin life as minuscule (~1 mm.), slender, active larvae termed planidia–from the Greek for "wandering" (Gordh & Headrick, 2003), since that is all a planidium does from the moment of its hatching. The objective of this wandering is a spider: locating and boarding such a creature is vital to the larva. Finding a suitable one is difficult (species differ in preference); at this point Morgan Freeman might solemnly intone that Many Will Not Survive, which would be absolutely true: mantidfly mothers lay something on the order of 1,000 eggs in each batch (Drees & Jackman, 1999), compensating for the tiny odds that any one planidium will reach its hairy eight-eyed destination. But that destination is not in and of itself the larva's prospective host.

Spider Parasite?
A first-instar mantispine situated near a jumping spider's (Salticidae) pedicel; photograph by Jeff Kramer
What, then, is the purpose of a mantispine planidium's quest? Their relationship with the adult spiders is only phoretic*, for it is upon the contents of spiders' egg sacs that they feed. Naturally, only a female spider will produce what the larva requires; but if a planidium has the misfortune to board a male, all is not necessarily lost: like some kind of crawling STD, it can transfer to the male's mate during copulation (or cannibalization). In the meantime, the planidium may conceal itself by coiling around the juncture betwixt cephalothorax and abdomen (as seen above) or, if the spider molts, take shelter in the latter's book lungs, surviving by sucking blood from those organs for the time being (Redborg & MacLeod, 1983). Some species (D. sayi among them) may dispense with the hassle of spider phoresy and simply seek out and penetrate egg sacs directly (Redborg, 1998); but others are obligate spider boarders: they can only enter an egg sac while it is under construction (Redborg & MacLeod, 1983).

Acrocerid - Ocnaea - female
Ocnaea sp. (Acroceridae), female, photographed by Jeff Gruber
Regardless of how it accomplished the feat, a larva that has gained entrance to an egg sac molts, and undergoes a total morphological shift: one from a campodeiform (fast-running, flattened, and in possession of functional antennae) shape (fig. A in the illustration from John Henry Comstock's Introduction to Entomology) to a scarabaeiform (inactive and grub-like) one (B). Immersed in the embryonic spiderlings upon which it will subsist, the mantidfly has no further need for a planidial form (Imms, 1957). Hypermetamorphosis, as this change is termed, is a rarity among the holometabolous insects, appearing in 4 disparate orders aside from the Neuroptera; it is always an adaptation to a parasitoid ecology in situations where it is inconvenient for a mother to directly lay her eggs on the host (as the vast majority of parasitoids do). Mantidflies' fellow hypermetamorphic insects–such as wedge-shaped beetles (Rhipiphoridae) and small-headed flies (Acroceridae)–are nearly as fascinating this post's titular chimeras: but I will have to defer them to another day.

Happy New Year (if it is a happy one–which I doubt).

*That is, hitchhiking, as opposed to parasitic.

Buys, S. C. (2008). Observations on the biology of Anchieta fumosella (Westwood 1867) (Neuroptera: Mantispidae) from Brazil. Tropical Zoology, 21, 91-95.

Drees, B. M. and Jackman, J. (1999). Field Guide to Texas Insects. Houston: Gulf Publishing Company.

Enderlein, G. (1910). Klassifikation der Mantispiden nach dem Material des Stettiner Zoologische Museums. Stettiner Entomologische Zeitung, 71, 341-379.

Gordh, G. and Headrick, D. H. (2003). A Dictionary of Entomology. Wallingford: CABI. 

Hook, A. W.; Oswald, J. D. and Neff, J. L. (2010). Plega hagenella (Neuroptera: Mantispidae) parasitism of Hylaeus (Hylaeopsis sp.) (Hymenoptera: Colletidae) reusing nests of Trypoxylon manni (Hymenoptera: Crabronidae) in Trinidad. J. Hymenopt. Res., 19, 77-83.

Imms, A. D. (1957). A General Textbook of Entomology. London: Methuen.

Jarzembowski, E . A. (1980). Fossil insects from the Bembridge Marls, Palaeogene of the Isle of Wight, southern England. Bulletin of the British Museum of Natural History (Geology), 33, 133-140. 

Johnson, J. B. and Hagen, K. S. (1981). A neuropterous larva uses an allomone to attack termites. Nature, 289, 506-507.

Lambkin, K. J. (1986). A revision of the Australian Mantispidae (Insecta: Neuroptera) with a contribution to the classification of the family I. General and Drepanicinae. Australian Journal of Zoology (Supplementary Series), 116, 1-142.

Maia-Silva, C.; Hrncir, M.; Koedam, D.; Machado, R. J. P. and Imperatriz-Fonseca, V. L. (2012). Out with the garbage: the parasitic strategy of the mantisfly Plega hagenella mass-infesting colonies of the eusocial bee Melipona subnitida in northeastern Brazil [electronic version]. Naturwissenschaften, 100, 101-105. Retrieved 1/6/13 from http://link.springer.com/content/pdf/10.1007%2Fs00114-012-0994-1 

Makarkin, V. N. (1990). Novye setchatokrylye (Neuroptera) iz verkhnego mela Azii. In: I. A. Akimov (ed.), Novosti Faunistiki I Sistematiki (pp. 63-68). Kiev: Naukova Dumka.

Parfin, S. I. (1958). Notes on the bionomics of the Mantispidae (Neuroptera: Planipennia). Entomological News, 69, 203-207. 

Redborg, K. E. (1998). Biology of the Mantispidae. Annual Review of Entomology, 43, 175-194.

Redborg, K. E. and MacLeod, E. G. (1983). Climaciella brunnea (Neuroptera: Mantispidae): a mantispid that obligately boards spiders. Journal of Natural History, 17, 63-73.

Tjeder, B. (1959). Neuroptera-Planipennia. The lace-wings of southern Africa. 2. Family Berothidae. In: Hanström, B.; Brinck, P. and Rudebec, G. (eds.), South African Animal Life Results of the Lund University Expedition in 1950-51 (vol. 6, pp. 256-314). Stockholm: Almqvist and Wiksell.

Wedmann, S. and Makarkin, V. N. (2007). A new genus of Mantispidae (Insecta: Neuroptera) from the Eocene of Germany, with a review of the fossil record and biogeography of the family [electronic version]. Zoological Journal of the Linnaean Society, 149, 701-716. Retrieved 1/6/13 from http://www.biosoil.ru/files/00004954.pdf 

Willmann, R. (1990). The phylogenetic position of the Rhachiberothinae and the basal sister-group relationships within the Mantispidae (Neuroptera). Systematic Entomology, 15, 253-265.