The Feared Mosquito

It's one of those standard pub-quiz "trick" questions. What animal kills the most people? The hope is that contestants will nominate the 'obvious'—snakes, sharks, bears, whatever—before being blind-sided by the revelation that mosquitoes kill over a million people. They don't kill them directly, of course; their victims die from the diseases they spread*. The statistic also glosses over the point that there are many hundreds of species of mosquito that vary significantly in the nature and severity of their role as disease vectors. Nevertheless, for this post I'm considering the group that includes some of the most notorious vectors: the genus Anopheles.

*For the record, if the question was confined to active killings, the most dangerous animal to humans is other humans. Dogs come a distant second.

Anopheles punctipennis feeding, with the long palps extended in front of the head, copyright Nathan D. Burkett-Cadena/University of Florida.

Anopheles is one of the most divergent genera of mosquitoes, being placed in a distinct subfamily Anophelinae (along with a couple of small related genera) from the bulk of mosquitoes in the subfamily Culicinae. Adult Anopheles can be readily distinguished from culicine mosquitoes by their palps which are about as long as the proboscis (in other mosquitoes, the palps are distinctly shorter). Larvae of Anopheles lack the long respiratory siphons at the end of the abdomen found in other mosquito larvae so they rest parallel with the water surface rather than hanging below it. The genus is found around the world; over 450 named species are currently known (Harbach 2013) with many more waiting to be described. The genus is currently divided between seven subgenera though one of the largest of these, the cosmopolitan subgenus Anopheles, is not monophyletic. The remaining subgenera are better supported with the largest of these, Cellia, being found in the Old World. Between them, the subgenera Anopheles and Cellia account for over 400 of the known Anopheles species. The remaining small subgenera are mostly Neotropical with a single Oriental species being awarded its own subgenus.

Anopheles maculipennis, copyright Ryszard.

Anopheles is of most concern to humans, of course, for its role as a disease vector. As with other mosquitoes, the transmission of disease is done entirely by females taking blood meals to provide nutrients for their developing eggs. Males are not blood feeders, instead feeding entirely on sugar sources such as nectar (females also feed on nectar for their own nutrition). The main disease spread by Anopheles is malaria, but they may also spread malaises such as filariasis and arboviruses (Krzywinski & Besansky 2003). As noted above, species may vary significantly in their importance as disease vectors, even between quite closely related taxa. Many historically recognised vector "species" have proved, on close inspection, to represent species complexes of which some may be vectors and others not. For instance, one of the most important transmitters of malaria, the African A. gambiae, has been divided between at least eight different species (Coetzee et al. 2013). Misidentification of vectors can be a significant issue. For instance, mosquito control regimes in central Vietnam during the 1990s focused on two species, A. dirus and A. minimus, that were each active at different times of year. However, Van Bortel et al. (2001) found that A. minimus was in fact very rare in this area, with specimens previously thought to be A. minimus proving to be another species, A. varuna. Anopheles varuna is not a significant malaria vector, feeding almost entirely on animals such as cattle rather than on humans. Large amounts of resources would have been wasted trying to control a mosquito that was of little concern. What is more, the fact that malaria was not being transmitted by A. minimus raises the possibility that it was being spread by yet another species, one that had managed to escape attention. Remember, kids: bad taxonomy kills.

REFERENCES

Coetzee, M., R. H. Hunt, R. Wilkerson, A. Della Torre, M. B. Coulibaly & N. J. Besansky. 2013. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619 (3): 246–274.

Harbach, R. E. 2013. The phylogeny and classification of Anopheles. In: S. Manguin (ed.) Anopheles Mosquitoes: New insights into malaria vectors. InTechOpen.

Krzywinski, J., & N. J. Besansky. 2003. Molecular systematics of Anopheles: from subgenera to subpopulations. Annual Review of Entomology 48: 111–139.

Van Bortel, W., R. E. Harbach, H. D. Trung, P. Roelants, T. Backeljau & M. Coosemans. 2001. Confirmation of Anopheles varuna in Vietnam, previously misidentified and mistargeted as the malaria vector Anopheles minimus. American Journal of Tropical Medicine and Hygiene 65 (6): 729–732.

To Dung and Beyond

When most people think of a fly, odds are that they imagine one of the group of flies known as calyptrates. This is the clade that includes, among others, such animals as house flies, blow flies and flesh flies. Calyptrates are often reasonably large as flies go and they often have life styles (such as larvae feeding on decaying matter) that bring them close to humans and their homes. One of the most recognisable features of this clade, and the inspiration for its name, is enlargement of the lower calypter, a lobe at the base of the wing. This lower calypter can be moved semi-independently of the rest of the wing which is how calyptrate flies are able to fly acrobatically and avoid being swatted. Nevertheless, there is one significant subgroup of 'calyptrate' flies that has foregone the advantages of an enlarged calypter, commonly recognised as the family Scathophagidae.

Yellow dung fly Scathophaga stercoraria, copyright Derek Parker.

The Scathophagidae are a modestly diverse family of flies with about 250 known species, the great majority of which are found in the Holarctic region (Vockeroth 1987). Only a handful of species are found in more southerly regions, mostly at higher altitudes. They are medium-sized flies, ranging between three and eleven millimetres in length, fairly similar to a house fly in overall appearance but generally more slender and bristly. They are commonly referred to as 'dung flies', in reference to the larval diet of one of the most widespread and best known species, Scathophaga stercoraria (whose scientific name broadly and appropriately translates as 'shit-eater, thing of shit'). However, despite the unremarkable number of species, scathophagids are actually more diverse in their larval habits. As far as we know, adult scathophagids are all predators on other insects.

Scathophagids are divided between two subfamilies, distinguished by features of the male terminalia. In Scathophaginae, the sixth abdominal tergite (dorsal plate) of the male is hairy and usually separate from the following fused syntergosternite 7 + 8 (with dorsal and ventral plates of the segments fused to form a ring). In Delininae, the sixth tergite lacks hairs and is always fused to the following syntergosternite. The subfamilies also differ in life history. Larvae of Delininae are leaf-miners on monocots, hatching from eggs laid on the leaf surface. The Scathophaginae are more diverse. As already indicated, some are saprobes. As well as the dung-feeding S. stercoraria, the genus Scathophaga also includes species which specialise on rotting seaweed on the sea-shore (a milieu which, offhand, supports a range of fly species belonging to numerous families). Other species are, like the Delininae, miners in plant tissue though they are found in a wider range of hosts (both monocots and dicots) and their eggs are inserted by the female directly into the plant tissue. A handful are aquatic or semi-aquatic predators, feeding on small invertebrates along lake shores or in sewage, or on the eggs of caddisflies in fast-running streams.

Cordilura pubera, a plant-feeding scathophagid, copyright Aleksandrs Balodis.

Considering the more derived character of the male terminalia in the Delininae, and the more disparate life habits of the Scathophaginae, some authors have suggested that the latter may be paraphyletic to the former. It has also been presumed that the Scathophagidae as a whole is ancestrally saprobic, considering that saprobic habits are also the norm in related fly families such as the Muscidae (house flies). However, a molecular phylogenetic analysis of the Scathophagidae by Kutty et al. (2007) supported monophyly of both subfamilies. Their results indicated that the original scathophagids were plant-feeders with saprobic lineages arising within the family on two separate occasions. Predatory larvae also evolved twice, once as a further development from saprobes and once direct from plant-feeding ancestors. The diet of this family started out fresh but, somewhere along the line, some species decided they'd rather eat muck.

REFERENCES

Kutty, S. N., M. V. Bernasconi, F. Šifner & R. Meier. 2007. Sensitivity analysis, molecular systematics and natural history evolution of Scathophagidae (Diptera: Cyclorrhapha: Calyptratae). Cladistics 23: 64–83.

Vockeroth, J. R. 1987. Scatophagidae. In: McAlpine, J. F. (ed.) Manual of Nearctic Diptera vol. 2 pp. 1085–1097. Biosystematics Research Centre: Ottawa.

Apiocera: Flower-Loving Flies that Don't Particularly Care for Flowers

The insect world is full of animals that may be striking in appearance but about which we know relatively little. Such, for instance, are the flies of the genus Apiocera.

Male Apiocera, copyright Chris Lambkin.

Apiocera is a genus of a bit over 130 known species of relatively large flies, about half an inch to an inch in length, that are found in hot, arid habitats in disparate parts of the world: western North America, southern South America, southernmost Africa and Australia. Records of Apiocera from Borneo and Sri Lanka were regarded by Yeates and Irwin (1996) as probably errors. They are similar in their overall appearance to the robber flies of the family Asilidae, differing lacking the piercing mouthparts of robber flies or the moustache of bristles below the antennae. The venation of their wings is more similar to that of the mydas flies of the Mydidae, but they differ from most mydids in having shorter antennae and the regular triangle of three round ocelli on top of the head (Woodley 2009).

Observations of Apiocera species have been fairly few. A study of North American species by Toft & Kimsey (1982) found them to be restricted to sandy habitats with a fair amount of subsurface moisture, such as the shores of lakes and rivers or among sand dunes. The larvae, so far as we know, are similar to those of robber flies and are probably burrowing predators in the sand. Adults emerge from holes in the ground late in the growing season. In some places (such as Wikipedia), you may find Apiocera referred to as 'flower-loving flies' but visits to flowers are few. Toft & Kimsey (1982) found that the species they observed emerged after most plants had finished flowering and, indeed, questions have been raised historically as to whether adult Apiocera feed at all. Nevertheless, they may take honeydew from plant-sucking insects, and I will direct you to the photo below by Jean & Fred Hort that seems to show at least one Apiocera individual feeding at a flower. Males may congregate at certain locations, seemingly to form leks, though it is unclear whether they maintain territories. Toft & Kimsey (1982) noted that tussels between males of A. hispida were common, observing that "two males would make rapid contact in mid-flight, and stay together in a buzzing, tumbling ball for several seconds".

There seems to be little question that Apiocera and mydas flies are closely related. In fact, an analysis of Apiocera's phylogenetic relationships by Yeates & Irwin (1996) lead to a number of other genera that had previously been classified with Apiocera in the family Apioceridae being reassigned to the Mydidae (I suspect that it is the behaviour of these other 'apiocerids' that is behind the erroneous association of Apiocera with the 'flower-loving' moniker). Apioceridae is still maintained as a distinct family for Apiocera alone but, as noted by Woodley (2009), one could be forgiven for questioning whether Apiocera would be better treated as a very basal mydid. But that, of course, is simply a question of categories.

REFERENCES

Toft, C. A., & L. S. Kimsey. 1982. Habitat and behavior of selected Apiocera and Rhaphiomidas (Diptera, Apioceridae), and descriptions of immature stages of A. hispida. Journal of the Kansas Entomological Society 55 (1): 177–186.

Woodley, N. E. 2009. Apioceridae (apiocerid flies). In: Brown, B. V., A. Borkent, J. M. Cumming, D. M. Wood, N. E. Woodley & M. A. Zumbado (eds) Manual of Central American Diptera vol. 1 pp. 577–578. NRC Research Press: Ottawa.

Yeates, D. K., & M. E. Irwin. 1996. Apioceridae (Insecta: Diptera): cladistic reappraisal and biogeography. Zoological Journal of the Linnean Society 116: 247–301.

Flies on Stilts

Flies deserve a much better rep than they're usually given. They are animals of grace and poise that step lightly through the world. And perhaps few flies have an appearance that conveys that grace better than the stilt-legged flies of the Micropezidae. For today's post, I wanted to look at one particular subfamily of micropezids, the Taeniapterinae.

Scipopus sp., copyright Gail Hampshire.

Stilt-legged flies are found in most parts of the world but are particularly diverse in tropical regions. As their name indicates, they are light-bodied flies with notably long legs, the middle and hind legs being much longer than the fore legs. This legginess perhaps reaches its peak in the Madagascan genus Stiltissima, males of which have the hind femora alone at least 2.5 times the length of their thorax (Barraclough 1991). The adults are predators of small insects but are also attracted to decaying fruit or dung. Larvae of the family are little known but indications are that they feed on the aforementioned ordure or other rotting vegetation. Many of them are mimics of wasps such as ichneumons or ants with their slender figure resembling the narrow-waisted appearance of a wasp. Because micropezids belong to the brachyceran lineage of flies, in which the antennae are few-segmented and usually short, the front pair of legs is instead held out in front to imitate the wasp's antennae.

Habitus of Stiltissima violacea, from Barraclough (1991).

The Taeniapterinae are the most diverse of three subfamilies recognised within the Micropezidae. Distinctive features of this subfamily include ocelli sitting relatively forward on the top of the head, a dense vertical fan of bristles on the sternopleuron (the sclerite on the side of the thorax just between the base of the fore and middle legs) and a vestigial subscutellum (Jackson et al. 2015). Though cosmopolitan in distribution, and the only micropezid subfamily known from sub-Saharan Africa (Barraclough 1991; the only non-taeniapterines known from the Afrotropical region are restricted to the Mascarene islands), taeniapterines are most diverse in the Neotropical region.

Mesoconius dianthus contrasted with its ichneumon model Cryptopteryx, from Marshall (2015).

The Taeniapterinae have been divided into two tribes based on the length of the cup cell near the base of the fore wing, the short-celled Rainieriini and the long-celled Taeniapterini (Jackson et al. 2015). All taeniapterines found outside the Neotropical region belong to the Rainieriini, as well as a number of Neotropical genera. The Taeniapterini are restricted to the New World. Genera of Taeniapterinae are often poorly distinguished with the relationships between species obscured by the evolution of features related to mimicking their wasp models. A phylogenetic analysis of selected Taeniapterinae by Jackson et al. (2015) indicated many recognised genera were non-monophyletic. It also cast doubt on the tribal classification with the Taeniapterini rendering the Rainieriini paraphyletic.

REFERENCES

Barraclough, D. A. 1991. Review of the Madagascan Taeniapterinae (Diptera: Micropezidae), with the description of a remarkably elongate-legged new genus and first record of Rainieria Rondani from the subregion. Annals of the Natal Museum 32: 1–11.

Jackson, M. D., S. A. Marshall & J. H. Skevington. 2015. Molecular phylogeny of the Taeniapterini (Diptera: Micropezidae) using nuclear and mitochondrial DNA, with a reclassification of the genus Taeniaptera Macquart. Insect Systematics and Evolution 46: 411–430.

The Asteiids: Overlooked Flies

Flies are incredibly diverse, but they may be one of the least appreciated of the major insect groups. There are many significant fly lineages whose presence goes all but unnoticed by a small number of afficionados.

Asteia amoena, copyright Mick E. Talbot.

One of the largest clades of flies is the Schizophora, including many such familiar animals as house flies, blowflies, and fruit flies (of both varieties). The most distinctive feature marking this lineage is the ptilinal fold, a groove that runs around the face of the flies along the inner margin of the eyes and across above the antennal insertions. This groove marks the position of a large fold of soft cuticle, the ptilinum, that is used by the fly when it emerges from the hardened case, the puparium, in which it metamorphoses from a larva. The ptilinum expands like a bellows as the fly pumps its head full of liquid until the pressure causes the cap of the puparium to pop open. After this, the excess cuticle is folded away inside the head, never to emerge again, but the mark of its presence remains.

House fly Musca domestica emerging from its puparium, showing the inflated ptilinum. Copyright Alex Wild.

Schizophorans have commonly been divided between two main groups, referred to as the calyptrates and acalyptrates. The basis of this division is the presence (calyptrates) or absence (acalyptrates) of the calypters, lobes at the base of the wings that help in controlling flight. This is not an entirely phylogenetic system: the calyptrates are a single clade but the acalyptrates are not. The most familiar flies belong to the calyptrates (which include house flies and blowflies) despite the fact that acalyptrate flies are considerably more diverse. This is in part because many acalyptrates are very small flies, easily overlooked by the casual observer.

The Asteiidae are one such group of overlooked flies. They are found pretty much world-wide and can be very abundant in some habitats. Nevertheless, they are apparently not common in collections: their soft-bodiedness makes them tricky to preserve, and Grimaldi (2009) noted that tropical species living on rolled leaves of herbs such as bananas and gingers were reluctant fliers and so unlikely to be collected by passive intercept traps. Noteworthy features of asteiids compared to similar flies include a reduced wing venation, and an antennal arista bearing alternating rays (Friedberg 2009). In two genera, Polyarista and Anarista, the arista is reduced or lacking, replaced by a collection of long setae arising from the first flagellomere (Papp 2013).

Diagnostic features of Asteia amoena, from Walker's Insecta Britannica Diptera.

Because of their low collection rates, the natural history of asteiids is poorly known. As already noted, a number of species are found in association with vegetation; others have been raised from fungi. Grimaldi (2009) described Asteia species running "over the surface of a leaf in all directions with uniform effort, including backwards and sideways, which gives them an appearance of floating over the surface". Some species have mating rituals involving trophallaxis, in which a male attempts to entice a female by offering her a regurgitated droplet. If his offering meets her standards, they will collaborate to produce a new generation that will carry on in the same obscurity as the last.

REFERENCES

Freidberg, A. 2009. Asteiidae (asteiid flies). In: Brown, B. V., A. Borkent, J. M. Cumming, D. M. Wood, N. E. Woodley & M. A. Zumbado. Manual of Central American Diptera pp. 1093–1096. NRC Research Press: Ottawa.

Grimaldi, D. A. 2009. The Asteioinea of Fiji (Insecta: Diptera: Periscelididae, Asteiidae, Xenasteiidae). American Museum Novitates 3671: 59 pp.

Papp, L. 2013. A new genus of Asteiidae with a key to the Old World genera (Diptera). Annales Historico-Naturales Musei Nationalis Hungarici 105: 199–205.

Midges of the Macabre

In a recent post, I commented that derived members of an insect 'order' could sometimes be all but unrecognisable as belonging to that order. Take a look at this:

Miastor sp., copyright Charles Olsen.

Believe it or not, sitting in the middle of that photo is a fully reproductively mature insect (I'm not so sure about the maturity of the other individuals). In fact, it's a fully mature fly. Miastor is a genus of midges found living in rotting wood or fungal fruiting bodies. Members of this genus are found worldwide; I believe that several species are recognised, but distinguishing the individual species is extremely difficult. Miastor exhibit what is called paedogenesis: they can become reproductively mature while still in the larval state. They are not the only genus of the family Cecidomyiidae to exhibit this process; another such genus, Oligarces, is found in similar habitats. Miastor is probably the best known such genus, in part because it has been cultured for study in the laboratory, and in part because of the decidedly macabre way in which its paedogenesis plays out.

Each paedogenetic Miastor larva develops several eggs within its ovaries (generally four to ten or more—Harris 1923). No males are involved in this process: the larvae are parthenogenetic as well as paedogenetic. These eggs hatch while still inside their mother, after which the daughter larvae are nourished by the mother's own tissues. Eventually, the daughters are not born so much as they escape. In the words of Quammen (1985), "While the food lasts, while opportunity endures, no Miastor female can live to adulthood without dying of motherhood". But karma still seems to have its place, because by the time the daughter larvae escape they carry their own fate within them: they emerge with their own eggs already developing inside them.

Metamorphosed male Miastor metraloas, copyright John Plakidas.

In this way, a Miastor colony can go through an entire generation in as little time as two weeks, until changing conditions (such as exhaustion of food supplies, or a change in season) induce a change in tack. Larvae are produced that do not reproduce paedogenetically in the way that their mothers did, but instead pupate in the usual way to emerge as more ordinarily formed midges, both males and females. As with another paedogenetic insect that has already been featured on this site, the beetle Micromalthus debilis, these metamorphosing larvae can be readily distinguished from paedogenetic larvae. Not only do they not produce the precocious reproductive organs of their fellows, but they have visible imaginal discs (the clumps of tissue that develop into adult structures during metamorphosis), and have eyes that are clearly separated on top rather than touching as in paedogenetic individuals (Harris 1923). After the mature adult midges emerge from their pupae, they can disperse in search of new habitats, seeking food for their offspring and mates for themselves in order to begin the cycle again.

REFERENCES

Harris, R. G. 1923. Occurrence, life-cycle, and maintenance under artificial conditions, of Miastor. Psyche 30 (3–4): 95–101.

Quammen, D. 1985. Natural Acts. Schocken Books.

Juniper Gall Midges

Sometimes, the evidence of an insect's presence may be much more visible than the insect itself. Imagine passing by a common juniper tree Juniperus communis and seeing a structure like the one in the photo above (copyright Jean-Yves Baugnée). You might think it was some sort of reproductive structure. You would be right, though it is not the tree that is reproducing. This is the gall of a juniper gall midge Oligotrophus juniperinus, and were you to cut the gall in half you would possibly find a single gall midge larva lurking within. Many insects (and other animals) cause the development of galls on their host plants, thus providing themselves with both shelter and food in one convenient location.

Male Oligotrophus betheli, from Simova-Tošić et al. (2010).

The adult gall midge is a minute, very delicate fly, unlikely to be spotted by the casual observer. Gall midges are classified in the family Cecidomyiidae, an extremely diverse group of which not all members cause galls as larvae (some feed on plants without causing galls, others feed on fungi, a few are even predators or parasitoids). Cecidomyiids are divided between a number of subfamilies and tribes, with Oligotrophus belonging to the tribe Oligotrophini. In the past, this tribe has been used to cover a heterogeneous mix of relatively unspecialised cecidomyiids, but the most recent classification of the tribe strips it down to two genera, Oligotrophus and Walshomyia, found in the Holarctic region (Harris et al. 2006). Adults of these genera have legs with simple tarsal claws and long empodia (the soft pads between the claws), and as larvae they all live in galls on trees of the cypress family Cupressaceae. The exact form of the gall produced may differ between species, and it is often (though not always) possible to determine the species responsible for a gall by its form. For instance, three species that cause galls on Juniperus communis in Europe are Oligotrophus juniperinus, O. panteli and O. gemmarum. The first two species have galls formed from whorls of leaves pressed into a vase shape, but whereas in galls of O. juniperinus the leaves splay outwards towards the tip, in galls of O. panteli they remain parallel. The third species, O. gemmarum, has much smaller galls formed from only slightly modified buds; though very different from mature galls of the other two species, they may be confused with young undeveloped galls (Harris et al. 2006).

Despite their diversity, and the fact that some species are economically significant to humans, cecidomyiids are not a widely studied group. Part of the reason for this is that their small size and build makes them difficult to handle; diagnostic work on adults often requires slide-mounting them. I have made one not-very-successful attempt at slide-mounting cecidomyiids, and I can confirm that it is a fiddly process. Because the different body parts often have to be examined from different angles, slide-mounting first requires dissection of the animal into sections (so, for instance, the head can be placed on the slide face-on, the body side-on, and the terminalia top-up). In my experience, instructions for slide-mounting animals requiring such dissections will always tell you to arrange the various bits appropriately on the cover-slip before placing the slide (or the other way around, if you prefer). And if you know how to attach slide to cover-slip without having all your carefully arranged body parts immediately zooming off to a completely different spot on the slide from where you put them, then you're a far more skillful slide preparer than I am.

REFERENCES

Harris, K. M., S. Sato, N. Uechi & J. Yukawa. 2006. Redefinition of Oligotrophus (Diptera: Cecidomyiidae) based on morphological and molecular attributes of species from galls on Juniperus (Cupressaceae) in Britain and Japan. Entomological Science 9: 411–421.

Simova-Tošić, D., D. Graora, R. Spasić & D. Smiljanić. 2010. Oligotrophus betheli Felt (Diptera: Cecidomyiidae), a new species in the fauna of Europe. Arch. Biol. Sci. 62 (4): 1219–1221.