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DR RUSSELL BONDURIANSKY


 
ANTLER FLIES (Protopiophila litigata)
 
Tiny insects with a remarkable specialization
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 and its remarkable site fidelity make it an ideal model system for field research, making it possible to observe the same individuals throughout their lives and obtain longitudinal ('biographical') field data on their behaviour and life history. Their 2-hour long copulations also facilitate estimates of mating success in the field. In order to take advantage of the unique opportunities offered by this system, I developed a technique for marking and measuring tiny live flies without injury (Bonduriansky & Brooks 1997). 
Moose antler
 
This unique species has provided the first convincing evidence of senescence in an insect population in the wild (Bonduriansky & Brassil 2002).
 
Because male antler flies are astonishingly aggressive, I named this species litigata, which translates loosely as 'those who love to pick fights' (Bonduriansky 1995). They readily attack muscid flies vastly larger than themselves, or even the tip of a biologist's pen! On antlers, these 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). 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). 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 (see below). They land on the surrounding leaf-mould, burrow into the soil, and undergo their pupal development.
 
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.
 

ANTLER FLY LIFE CYCLE
 
Leaping Larvae
The final instar larvae of many species of piophilid flies (as well as flies of several other families) have the ability to leap. This amazing behaviour was first described in the 17th century by the Dutch naturalist Jan Swammerdam, who observed maggots of 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.
 
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).
 
As if the ability to leap were not enough, these maggots are also able to hear and respond to sound. I found that 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). 

Antler fly larva Antler fly larva Antler fly larva Antler fly larva
Antler fly larva Antler fly larva Antler fly larva Antler fly larva
Antler fly larva Antler fly larva Antler fly larva Antler fly larva
 
Antler fly maggot preparing to leap off an antler (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.
 
(photos created from film sequence shot by Phil Savoie, BBC Natural History Unit)
 
Pupation
After burrowing into the leaf-litter or soil, the piophilid larva moults into a pupa, and undergoes metamorphosis into the adult stage. Pupal metamorphosis takes about two weeks at room temperature.
 
Antler fly emerging from puparium Antler fly emerging from puparium Antler fly emerging from puparium
Antler fly emerging from puparium Antler fly emerging from puparium Antler fly emerging from puparium
 
An antler fly adult emerging from its puparium: by periodically inflating and deflating the anterior part of its head, the fly breaks off the 'cap' of the puparium (which can be seen just below the fly's head); once completely out of the puparium, the fly burrows through the soil to the surface.
 
(photos created from film sequence shot by Phil Savoie, BBC Natural History Unit)
 
Adults
After reaching the soil surface, newly emerged adults hide in vegetation until their wings have unfolded and their exoskeleton has hardened. After this, they either return to their natal antler, or fly away to seek fresher antlers.
 
Antler fly aggregation on a moose antler Marked male antler fly Male antler fly chasing an opponent Mating antler flies
An antler fly aggregation on a moose antler.
A marked male on an antler.
One male chasing another following a fight.
A mating pair of antler flies (male on top of female).

Ovipositing antler flies Ovipositing antler flies Ovipositing antler flies
Antler fly females (guarded by their mates, who ride on their backs) ovipositing into a crack in the surface of a moose antler. Single males (like the one seen in the middle and right photos) attempt to dislodge guarding males and mate with the females.
 
(photos created from film sequence shot by Phil Savoie, BBC Natural History Unit)
 
[Photographs on this page may not be reproduced without permission.]