BrownBrian V.KungGiar-AnnPorrasWendyA new type of ant-decapitation in the Phoridae (Insecta: Diptera)Biodivers Data J02120152015310.3897/BDJ.3.e4299 Dohrniphora Dahl 1898Biology

All species of flies had similar behavior, documented in video clips. Approximately 10 decapitations per species have been observed. Flies arrived shortly after the ants were injured, usually arriving as in copula pairs in flight, cruising back and forth above the ants. After the pair landed, males immediately departed and females approached the injured Odontomachus.

Female flies spent several minutes apparently assessing the degree of incapacitation of the ants. First, a fly would rapidly tap on undergrowth leaves with its body (“drumming”) while circling about 5 cm around the ant. This drumming behavior was observed only with D. oricilla, but might have been overlooked in other species. Next, the fly approached the ant, darting in to touch it occasionally, still circling it. Occasionally, flies would grasp antennae or legs and rapidly pull on them (Fig. 1 at 19 seconds). If ants were too active, flies retreated and approached other, more incapacitated hosts (Fig. 2).

Eventually, flies climbed on the ant body, and began to probe with their mouthparts. Each fly concentrated on the occipital region of the ant body, using their mouthparts to probe deeply through the membrane (Fig. 3). The fly was nearly constantly in motion, probing from several angles. They made in-and-out, as well as rotational head movements, apparently while they were cutting the tissue of gut tract, nerve cord, and intersegmental membrane. On some occasions, flies preceded this stage by pulling the entire ant host out of the observation area, apparently to deal with it in a more secluded location.

Eventually, the ant's head became loosened and after some tugging (Fig. 4), the fly pulled the head off the body. It then would drag the ant head as far as several meters away, by holding onto the head with its forelegs and pulling with its middle and hind legs (Fig. 4). Interactions were followed for up to 45 minutes until the fly was lost in the undergrowth. A minimum of about 8 minutes were required by the fly to decapitate an ant, although such short time periods were rarely observed. Instead, timed sessions varied widely due to interruptions in the decapitation process due to the presence of competing females, other saprophagous phorids, and other insects, especially ants. In one instance, a pair of D. conlanorum females were observed in a 20 s long "fight" during which they flailed each other with their forelegs while rapidly running, flying, and jumping just above the leaf litter surface.

Some flies (n=10) were captured, placed in a plastic tub with injured ants, and observed indoors. Most decapitated their hosts quickly in low light conditions, and fed upon the head capsule contents. On two occasions, flies laid a single egg 1 cm from the ant head. Injured crickets and grasshoppers (Insecta: Orthoptera) placed in the same cages were ignored by flies.

Apparently, healthy ants are not subject to attack by Dohrniphora females. Under laboratory conditions, caged flies were frequently captured and crushed by ants (Fig. 5).

Morphology

Females of the Dohrniphora longirostrata species group are distinctive because of their greatly elongated proboscis, which is almost as long as their entire body (Fig. 6). In our observations, this proboscis is used to separate the ant’s head from the rest of the body. Study of the structure of the apex of the proboscis shows that the epipharynx is extremely modified as a bladed cutting organ that is used in the process of severing the ant's head (Fig. 7).

We rarely observed oviposition in our study, but it originally seemed unlikely that the flies would be engaging in this ant-decapitating behavior for any other reason than to secure food for their larvae. A single ant head appears to be the required size for the development of the single fly larva. In captivity, however, the flies were usually observed feeding on the contents of ant head capsule. More strikingly, we dissected females arriving at the injured ants (n=16) and found no mature eggs in their ovaries. As these non-gravid flies could not possibly have oviposited, we therefore conclude that female Dohrniphora require feeding on the contents of Odontomachus heads in order to mature their eggs.

A female of D. oricilla assessing injured Odontomachus ants at La Cangreja NP, Costa Rica.

A female of D. conlanorum processing and eventually decapitating an injured Odontomachus ant at La Suirre, Costa Rica.

A female of D. oricilla cutting the head off an injured Odontomachus ant at La Cangreja NP, Costa Rica.

A female of D. longirostrata decapitating an Odontomachus ant near Cabo Verde, Brazil.

An Odontomachus ant eating a captured D. conlanorum female (photo by Inna Strazhnik).

A female of D. longirostrata, lateral view.

Tip of female Dohrniphora longirostrata proboscis.