Evolutionary Biology Lab

Evolution & Ecology Research Centre and School of Biological, Earth and Environmental Sciences, University of New South Wales

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ANTLER FLIES (Protopiophila litigata)

The antler fly is a small (2-3 mm body length) piophilid that breeds exclusively on the discarded antlers of cervids such as moose and deer (Bonduriansky 1995; Bonduriansky and Brooks 1999). The antler fly's extreme specialization on a rare resource is associated with a remarkable site fidelity, which makes this species an ideal model system for longitudinal field studies.

For scale: male antler flies running past a Canadian penny

Moose antler supporting a population of antler flies.

The known distribution of antler flies extends across the eastern part of Canada, from Newfoundland and Cape Breton, Nova Scotia, to southern Ontario. In Algonquin Park, Ontario, the first adults emerge from pupae in the soil and appear on antlers in late May or early June. The mating season continues until late August.

A technique is available for individual marking and measurement of these tiny live flies without injury (Bonduriansky & Brooks 1997). Flies are marked on the thorax with enamel paint. Here's a video of a marked antler fly male (#11) on a moose antler. Because males tend to spend every day of their lives on the same antler, it is possible to observe them throughout their lives and obtain biographical field data on their behaviour and life history. Their 2-hour long copulations make it possible to estimate mating success in the field.

This unique species has provided the first evidence of ageing (senescence) -- declining survival rate and reproductive rate -- and its fitness costs in an insect population in the wild (Bonduriansky & Brassil 2002). Our analysis also showed that ageing rate is related to body size: large males exhibit faster reproductive ageing than small males (Bonduriansky & Brassil 2005). Research on these tiny flies is continuing through a collaboration between Russell Bonduriansky at UNSW and Howard Rundle and Brian Mautz at the University of Ottawa.

Male antler flies are astonishingly aggressive: litigata translates roughly as 'bellicose'. On antlers, males form complex, highly structured aggregations. Some individuals defend stable territories, while others simply wander in search of females, which arrive on antlers to feed, mate and oviposit (Bonduriansky & Brooks 1998, 1999). In prime areas of the antler, near oviposition sites (cracks in the antler surface), males spend much of their time battling rival males. They even attack insects vastly larger than themselves. This video of an antler fly aggregation was created by Phil Savoie of the BBC-NHU. The photos below show male-male combat.

Antler flies appear to engage in mutual mate choice, with both males and females rejecting some potential mates (Bonduriansky & Brooks 1998). Following copulation, the female expels and ingests much of the male's ejaculate, then inserts her ovipositor into minute cracks or pores in the antler surface and deposits her eggs. During oviposition, the male remains on the female's back and 'guards' her by warding off rival males with his wings (Bonduriansky & Brooks 1998b). Mating and ovipositing pairs are viciously attacked by single males, who attempt to dislodge the male and re-mate with the female (bottom left photo). Sometimes, several single males attack a female simultaneously (bottom right photo). Such wrestling matches can last for several minutes, and females and males can sustain serious injury.

Antler flies face a wide array of predators on antlers, such as the lacewing larva (left) and spider (right) in the photos below. A predatory empidoid fly with raptorial forelelgs (Tachypeza sp.) also attacks antler flies. 

Antler flies are also exploited by mites, which sometimes undergo explosive outbreaks lasting several days. Some antler fly individuals have nematode parasites in their abdomens. The photos below show a male heavily infested by mites and missing part of one fore-leg (left), and a female with mites all over her abdomen being mounted by a male (right).

Antler fly larvae develop in the porous bone matrix inside antlers, and come to the antler surface when ready to pupate. Here, the larvae perform an astonishing leap off the antler surface, as seen in this video. They land on the surrounding leaf-mould, burrow into the soil, and undergo metamorphosis. The photos below, showing an antler fly maggot preparing to leap, were created from footage shot by Phil Savoie, BBC-NHU. The sequence is shown from left to right, and top to bottom: the maggot first raises the anterior part of its body and curves it into a loop, then grasps its posterior end with its mouth-hooks, and tightens its muscles to create tension; finally, the maggot releases its hold abruptly (not shown here), causing its posterior end to recoil against the substrate, and launching itself into flight.

This amazing behaviour (also exhibited by maggots of several other dipteran families) was first described in the 17th century by the Dutch naturalist Jan Swammerdam, who observed maggots of a relative of antler flies -- the 'cheese skipper' fly Piophila casei (which he called 'the Mite') -- leaping off cheeses and cured meats. Swammerdam wrote:

 

'When this creature intends to take a leap, it first erects itself upon its anus... Immediately after this, the creature bends itself into a circle, and having brought its head...towards its tail, it presently stretches out its two black crooked claws, and directs them to the cavities formed between the two last or hindmost tubercles of the body, where it fixes them in the skin... The Mite having thus made itself ready, contracts its body with such force, that from a circular, it becomes of an oblong form...the contraction extending in a manner to every part of its body. This done, it again reduces itself with so prodigious a force to a straight line, that its claws, which are seated in the mouth, make a very perceivable noise on parting from the skin of the last ring of the body: and thus the Mite, by first violently bending, and afterwards stretching out its body, leaps to a most extraordinary height, if compared with the smallness of the creature... I have indeed seen a Mite, whose length did not exceed the fourth part of an inch, leap out of a box six inches deep, that is, to a height twenty-four times greater than the length of its own body; others leap a great deal higher.'

Swammerdam, Jan. 1758. The Book of Nature, or, the History of Insects (translated from the Dutch and Latin by Thomas Flloyd). London: C.G. Seyffert.

Piophila casei infests the popular Sardinian cheese casu marzu, which is eaten together with the leaping maggots.

The ability to leap may facilitate larval movement from the feeding substrate to pupation sites. Because larval creeping locomotion is excruciatingly slow and rather inefficient, maggots may face considerable energetic costs and, more importantly, great risk of being captured by predatory insects on the surfaces of carcasses or antlers. The ability to leap may represent a solution to both of these problems (Bonduriansky 2002).

Piophilid maggots are also able to hear and respond to sound. Final instar maggots respond to the sound of a rattle by coming to the surface of their feeding substrate and leaping off. Moisture elicits a similar response. The timing of pupation appears to be facultative in this species, and final instar maggots may wait inside their food substrates (antlers or carcasses) until they perceive stimuli associated with rain (i.e., rattling sound or moisture) before initiating the hazardous migration to their pupation sites. Observations suggest that rain facilitates larval locomotion, and may reduce risk of predation (Bonduriansky 2002). 

Following metamorphosis (which takes about 12 days), adult antler flies emerge from the puparium and usually return to their natal antler. These photos of an antler fly adult emerging from the puparium were created from footage shot by Phil Savoie of the BBC-NHU. After breaking out of the puparium, the adult (which is still soft) repeatedly inflates the anterior part of its head.