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Diptera

(Mosquitoes, midges, and flies)

Class Insecta

Order Diptera

Number of families 188

Photo: Non-biting midge larvae among stonewort, showing gills and false legs. (Photo by Kim Taylor. Bruce Coleman, Inc. Reproduced by permission.)

Evolution and systematics

Permotipula patricia from the Upper Triassic of the Mesozoic period from Australia, about 225 million years ago, is the earliest known fossil of a true fly. Since that time, flies have diversified to become one of the four largest orders of insects with about 124,000 species described. It is estimated that an equal number of species, mostly from tropical forests, still await description.

Diptera or true flies are the closest relatives to the Mecoptera or scorpionflies within the Panorpoid-complex (including butterflies and moths, scorpionflies, and fleas), with which they share numerous wing venation characters. Flies are distinguished from other insects by several derived characters, the more important of which are: metathoracic wings transformed into clublike halteres, metathorax reduced in size, labium modified as a labellum, and larval spiracles lacking a closing apparatus.

The order Diptera is divided into two suborders, Nematocera and Brachycera. Nematocera includes generally small, delicate insects with long antennae, regarded as more primitive flies, such as mosquitoes, crane flies, midges, punkies, and no-see-ums. Brachycera includes more specialized, compact, robust flies with short antennae. In older classifications, two divisions were recognized within Brachycera: Orthor-

rhapha and Cyclorrhapha. The Orthorrhapha includes brachyceran flies with free pupae (lacking a puparium) and larvae with incomplete head capsule, such as horse flies and robber flies, and the Cyclorrhapha comprises brachyceran flies with pupae enclosed in the hardened skin of the last larval instar (called puparium) and larvae without head capsule. The Cyclorrhapha are further divided into two groups based on the presence or absence of the ptilinum and associated fissure on the head. The ptilinum is a sac that is everted only once during the emergence of the adult fly to assist in breaking free of the puparium. The Aschiza (flower flies and coffin flies) lack the ptilinum, whereas it is present in the Schizophora. Schizophora in turn comprises a group of flies, the Calypteratae (including house, bottle and flesh flies), with basal lobes in the wings called calypters, and a second group without such lobes, the Acalypteratae (including fruit, vinegar, and oil flies).

These traditional groupings of Diptera have been critically reexamined in recent decades, and many of the categories such as the Nematocera, Orthorrhapha, and Aschiza are not considered natural groups. Instead, these categories consist of a collection of basal lineages from which some natural groups (Brachycera, Cyclorrhapha, and Schizophora, respectively) arose. No consensus has been reached to date on a natural classification for the order.

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A male mosquito emerging from pupa skin. (Photo by Dwight R. Kuhn. Bruce Coleman, Inc. Reproduced by permission.)

Physical characteristics

Adults have a mobile head, with large compound eyes that can be contiguous (holoptic condition, found usually in males) or separated (dichoptic condition, most commonly encountered in females) on top. The antennae have six or more segments in nematoceran flies, and five or fewer in brachyceran flies. Mouthparts are adapted for sucking and form a proboscis or rostrum. In predatory species, the mandibles form a pair of piercing stylets, and in cyclorrhaphan flies the labial palps form the labella, membranous sponge-like apical lobes traversed by sclerotized canals called pseudotracheae, through which liquids ascend by capillary action. The major morphological feature that distinguishes flies from other insects is the presence of only one pair of functional wings, hence their scientific name (di = two, pteron = wing). The mesothorax has become greatly enlarged to contain the powerful flight muscles, and the proand metathorax are reduced. The hind wings are modified into halteres, which are small, club-like structures that function as balancing organs during flight. A few other groups of insects have also attained a similar two-winged form, such as males of scale insects (Coccoidea, Hemiptera), and a few flies have lost their wings and halteres as an adaptation to a parasitic life style (e.g., louse-fly families Nyc-

teribiidae and Hypoboscidae) or habitats such as tidal pools (e.g., the midge Pontomyia in the Indopacific), snow fields (e.g., the crane fly Chionea in Europe), islands (e.g., the crane fly Limonia hardyana and the dolichopodid fly Campsicnemus from Hawaii), or coffins (e.g., the phorid fly Conicera). However, those flies are still recognizable by the structure of their mouthparts, greatly enlarged mesothorax, and legs.

There is a large diversity in leg shape and structure, but all species in this order have five tarsomeres (distal segments), which are used as tactile organs. Legs can be adapted as raptorial organs in predatory forms (e.g., the fore legs of some ceratopogonids, empidids, and ephydrids) or for holding onto the female during copulation, as organs of sexual or combative display (e.g., the ornamented tarsi of some African dolichopodid flies), or as grasping organs in ectoparasites, and can bear combs of setae and brushes of hairs for grooming. The abdomen of flies has a basic number of 11 segments, the last one called the proctiger, represented by only the caudal appendages or cerci and the anus. In nematoceran and orthorrhaphan flies, the abdomen is usually longer and slender, whereas it tends to be robust in the Cyclorrhapha. The male aedeagus or intromitent organ is found on the underside between abdominal segments 9 and 10, and the female genital opening is between segments 8 and 9. Female flies do not have an ovipositor formed by valves;

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instead, in the more advanced flies, the terminal segments of the abdomen, from 5 or 6 to the tip, form a “functional ovipositor” in the shape of a tapered telescopic tube. The apical portion of the male abdomen is often flexed—folded ventrally, laterally, or dorsally—and the genitalia is usually twisted 90° to 360° as an adaptation for mating and storing the genitalia when not in use.

Larvae are usually elongated and subcylindrical or fusiform, and often have transverse swollen areas called creeping welts that usually bear a transverse series of microspinules on the ventral surfaces—or on both the ventral and dorsal surfaces—of the first seven abdominal segments. Larvae always lack external wing pads and legs, although some may have fleshy tubercles called prolegs on the prothorax and some abdominal segments. Nematoceran larvae have a sclerotized head capsule and mouthparts that move in a horizontal plane. In Brachyceran larvae, also called maggots, the mandibles move in a vertical plane, the head capsule is reduced (in orthorrhaphan flies) or absent (in cyclorrhaphan flies), and the head possesses an internal cephalo-pharyngeal endoskeleton. Larvae differ in the number of spiracles or openings for their respiratory system. They may be apneustic (without openings); amphipneustic (with an anterior and a posterior pair of spiracles); or metapneustic (with only the posterior pair of spiracles). Aquatic larvae spiracles may be situated at the tip of projections of the body called siphons, which allow them to reach the atmosphere (e.g., in the rattailed maggot, the larva of an Eristalis syrphid fly, which lives in the bottom of bodies of oxygen-poor water and breaths through a very long siphon, the tail) or pierce underwater aircontaining plant tissues (e.g., several mosquito larvae with sawlike siphons).

Diptera pupae have nonfunctional mandibles and one pair of wing pads. The appendages may be free from the body (as in Nematocera) or glued to the body (as in Orthorrhapha brachyceran flies), and the pupa may be free or concealed inside the puparium (as in Cyclorrhapha brachyceran flies).

Distribution

Flies are found on all continents including Antarctica, where two species of midges occur. Most families reach higher species richness in the tropics than in the more temperate areas, although Mycetophilidae, Chironomidae, and Empididae are most diverse at higher latitudes. Some species are very restricted in distribution, such as the wood-boring flies of the family Panthophthalmidae that occur only in Brazilian forests, the wingless fly Mormotomyia hirsuta, which is known only from a single fissure in a rock in Kenya where it feeds on bat dung, and the tabanid Thriambeutes mesembrinoides from the Usambara Mountains in Tanganyika.

Habitat

Larvae occur in aquatic, semiaquatic, and moist terrestrial environments, as endoparasites of other animals or as miners within plant tissues, but because their cuticle is soft and susceptible to desiccation, only a few live in dry environments.

Order: Diptera

Non-biting male midge showing plumed antennae. (Photo by Kim Taylor. Bruce Coleman, Inc. Reproduced by permission.)

Larvae of some shore flies (family Ephydridae) live in unusual habitats that would be lethal for other insects, such as hot springs and geysers where the water temperature exceeds 112°F (44.4°C) (Ephydra brucei), pools of crude oil (Helaeomyia petrolei), and ponds with very high concentrations of salt (the brine fly Ephydra cinera). Some bombyliid larvae live inside the nests of various bees, ants, and wasps, on which brood they feed.

The pupa normally occupies the same habitat as the larva. Pupation of most of the fully aquatic species occurs underwater, while semiaquatic species may pupate above water. The pupa may swim to the surface before the adult emerges, or it may remain on the bottom.

Adults are usually terrestrial, active in the daytime, and almost always free-living, the exception being the ectoparasitic adults of the louse-flies (families Hippoboscidae, Streblidae, and Nycteribiidae).

Behavior

Aggregations occur in many flies. Many Bibionidae and Empididae species as well as numerous nematoceran flies form aerial swarms, in which adults—usually males—hover together around some fixed object, such as a tree or bush, a hill top, a rock on a stream, a patch of sunlight in a forest, a building, or a highway (e.g., the lovebug, a bibionid fly that forms mating swarms on roads from Central America to the southern United States). These swarms usually allow males to be more conspicuous to their prospective mates. Other adults form sedentary aggregations for the purpose of mating or for seeking shelter or warmth, such as on roofs, or as the result of a mass emergence. Larvae can also form aggregations, such as leatherjackets and bibionids in the soil and the armyworms

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A phantom crane fly (Ptychopteridae) resting on underside of leaf in West Virginia, USA. (Photo by L. West. Bruce Coleman, Inc. Reproduced by permission.)

(Sciara militaris), which can be seen marching in long columns across European forests.

Mimicry is known in several flies that imitate ants (e.g., Sepsisoma, richardiid flies that mimic Camponotus ants; Microdon mutabilis, syrphid flies that imitate Formica lemani and Myrmica scabrinodis); bees and wasps (e.g., several conopid and tephritid fruit flies species that mimic vespid wasps); bumblebees (e.g., Laphria asilids that mimic Bombus species); and jumping spiders (e.g., fruit flies with banded wings and/or spotted abdomens). The mimicry can be in shape as well as behavior, either as a strategy to deceive the model in order to feed or lay eggs on its brood, or to deceive potential predators.

Feeding ecology and diet

Larvae are phytophagous (feeding on leaves, fruits, or roots of plants), filter organic matter, or are scrapers of algae, predators, parasitoids and saprophagous feeders of decaying organic matter including vegetables, dead animals, or dung. Endoparasitic larvae include those in the family Tachinidae, which parasitize other insects, particularly centipedes and spiders; those in the family Pipunculidae, which parasitize the larvae of cicadas and leafhoppers; and some species of bee flies (family Bombyliidae), which develop in the eggs or larvae of bees and wasps, other flies, beetles, and butterflies.

Adults typically consume liquid food such as nectar and other plant exudates or decomposing organic matter, or they prey on other insects or mollusks; adults of some species feed on little or nothing at all. Females of some groups may take blood meals from vertebrates (e.g., the “biting” mosquitoes, no-see-ums, black flies, and horse flies) as a prerequisite to oviposition.

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Reproductive biology

Flies undergo complete metamorphosis, passing usually through four life stages: egg, larva, pupa, and adult. The basic number of larval instars is 4 to 9 for the lower Diptera (Nematocera), and only three in many Cyclorrhapha, as the fourth larval stage develops within the puparium. The length of the egg stage is often brief, encompassing a few days or weeks, and that of the larval stage is variable, ranging from a few days in larvae feeding on short-term resources (such as rotting meat) to more than two years in some larvae that develop in cold and moist habitats.

Mating in flies is often preceded by an initial courtship in which the male or both sexes perform a chain of actions involving body movements or vibrations of the wings. In some dance-flies (family Empididae), males offer a nuptial gift to the female as part of the courtship, such as an insect wrapped up in silk, or just a hollow balloon of silk. Mating usually starts with an initial coupling position of both sexes facing in the same direction, and ends in a final mating position with male and female facing in opposite directions, in a tail-to-tail orientation. Some species are parthenogenetic (e.g., some Drosophila, Lonchoptera, Sciara, and Diaphorus flies).

Egg laying is related to the habitat of the larvae. Fruit fly females have a long needle-like ovipositor with which they pierce the skin of the fruit in which the larvae live and feed; parasitic flies show an extraordinary array of strategies to get eggs into their hosts, including laying them on the host’s surface, inserting them into the host with a piercing ovipositor, pasting them close or onto the host’s nest, hiding them among the host’s food, or laying them on another animal that will eventually come in contact with the host, such as a tick or mite. Flies with aquatic larvae oviposit on the water or on rocks or vegetation overlaying the water, and eggs can be laid singly or in the form of rafts.

Conservation status

Several flies are threatened not by direct exploitation but by loss or degradation of their habitats; they are at risk because their ecosystems are at risk. The IUCN Red List includes seven species from this order; three as Extinct, two as Endangered, one as Critically Endangered, and one as Vulnerable. The three Extinct species are the Volutine stoneyian tabanid fly, Stonemyia volutina (Tabanidae), from the continental United States; the Ko’okay spurwing long-legged fly, Campsicnemus mirabilis (family Dolichopodidae), from the Hawaiian Islands; and Lanai pomace fly, Drosophila lanaiensis (Drosophilidae), also from Hawaii. The sugarfoot moth fly, Nemapalpus nearcticus (family Psychodidae), from the United States, and the giant torrent midge, Edwardsina gigantea (family Blepharoceridae), from Australia, are Endangered. The Tasmanian torrent midge, Edwardsina tasmaniensis (family Blepharoceridae), is Critically Endangered due to the establishment of a hydroelectric dam in the Launceston Cataract Gorge at the Dennison River in Australia. Finally, Belkin’s dune tabanid fly, Brennania belkini (Tabanidae), from Mexico and United States, is considered Vulnerable because of the progressive destruction of its habitat by urban development.

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Although not listed by the IUCN, the flower-loving fly, Rhaphiomidas terminatus (family Apioceridae), from California, is at risk of extinction. Rhaphiomidas terminatus consists of two subspecies, the Delhi sands flower-loving fly, R. terminatus abdominalis, and the El Segundo flower-loving fly, R. terminatus terminatus. The latter, confined to the El Segundo sand dunes and portions of the sandy alluvial plain of the Los Angeles River—the last remains of which were eliminated by construction for the Los Angeles International Airport in the 1960s—was thought to be extinct but has recently been rediscovered. The Delhi sands flower-loving fly is a rare endemic subspecies restricted to the Delhi series of sand dunes, 98% of which have been converted to residential, agriculture, and commercial uses. The subspecies is listed as Endangered by the United States Fish and Wildlife Service.

Significance to humans

Flies are the most important arthropod vectors of disease in humans and other animals. For example, malaria is believed to have killed more human beings than any other known disease and is still a major cause of illness in many tropical countries. Also, diseases transmitted to humans and livestock by tsetse flies were the main obstacle to European colonization of North Africa. Deer or horse flies can transmit bacterial diseases such as tularemia and anthrax, filariasis (via the Loa Loa worm), and trypanosomiasis (causing surra in caribou, horses, and camels). Mosquitoes are vectors of filariasis (elephantiasis), malaria (caused by four species of the protozoan Plasmodium), and viruses including yellow fever and dengue fever; black flies can transmit onchocercosis (via worms); tsetse flies are vectors of trypanosomiasis (causing the fatal disease nagana in cattle and sleeping sickness in humans); and sand flies are vectors of leishmaniasis (via the Leishmania protozoan).

In addition to serving as vectors for diseases, flies can cause health problems themselves. Three main dipteran families— Oestridae (bot flies), Sarcophagidae (flesh flies), and Cal-

Order: Diptera

liphoridae (bottle flies) cause economically important myiasis in livestock and also occasionally in humans. Myiasis is the infestation of live vertebrate animals by dipterous larvae, which at least for a certain period feed on the host’s dead or living tissue, liquid body substances, or ingested food.

Still others are nuisance pests or carry filth, such as the eye gnats (genus Hippelates, family Chloropidae) and face flies (Musca autumnalis, family Muscidae), attracted to the secretions of the eyes of vertebrates; or the house flies (Musca domestica, family Muscidae), little-house flies (Fannia, family Muscidae), and latrine flies (Chrysomyia, family Calliphoridae), which breed in excrement and garbage.

Fruit flies (family Tephritidae) are among the most destructive agricultural pests in the world, eating their way through citrus crops and other fruit and vegetable crops at an alarming rate and forcing food and agriculture agencies to spend millions of dollars on control and management measures. Other agricultural pests include the gall gnats (family Cecidomyiidae), leaf miner flies (family Agromyzidae), and root miner flies (family Anthomyiidae).

Besides their essential roles in our ecosystems, including serving as food items for numerous animals and as pollinators, flies are of some direct benefit to humans. Some are important as biological control agents of weeds and other insects; as indicators of water quality (e.g., midge larvae known as blood worms are indicators of polluted environments); as experimental animals (e.g., much of our knowledge of animal genetics and development has been acquired using the fruit fly, Drosophila melanogaster as an experimental subject); and in forensic investigations to establish the time of death, whether the corpse has been moved after death, and the cause of death (e.g., several larvae of families Trichoceridae, Stratiomyidae, Phoridae, Phanidae, Muscidae, Calliphoridae, Sarcophagidae, and others feed on carrion and flesh in different degrees of decomposition, in different situations, and at different times of the year).

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1. New World primary screwworm (Cochliomyia hominivorax); 2. Yellow fever mosquito (Aedes aegypti); 3. Dasypogon diadema; 4. Tsetse fly (Glossina palpalis); 5. Cyrtodiopsis dalmanni; 6. New Zealand glowworm (Arachnocampa luminosa); 7. Petroleum fly (Helaeomyia petrolei). (Illustration by Jonathan Higgins)

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1. Mediterranean fruit fly (Ceratitis capitata); 2. European marsh crane fly (Tipula paludosa); 3. Fire ant decapitating fly (Pseudacteon curvatus); 4. Spider bat fly (Basilia falcozi); 5. Chevroned hover fly (Allograpta obliqua); 6. Big black horse fly (Tabanus punctifer); 7. Horse bot fly (Gasterophilus intestinalis); 8. Dawson River black fly (Austrosimulium pestilens). (Illustration by Jonathan Higgins)

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