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.
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Moose antler
supporting a population of antler flies.
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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 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.
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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 with
Howard Rundle's
lab 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. |
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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. |
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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. |
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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). |
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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. |
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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.
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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. |
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