Phorid Flies

Phorid flies are known to parasitize  ants. The common means of parasitism, and until recently thought to be the only method, is as follows. A gravid female phorid fly seeks out foraging ants to parasitize, and most flies appear to specialize on specific species of ants or at least a group of congeners. Once found the female attacks host workers and injects eggs into their head. The egg hatches, feeds from the ant that is hosting it and eventually pupates. In many cases the fly emerges from its pupal case in such a way that it causes the ant's head to pop off.

Recently it was discovered there is another method of ant decapitation. Some adult phorids were observed sawing the heads off of injured Odontomachus ants. Presumably the ant heads are used for food by the adult flies.

Impact on Foraging Activity
Braganca et al. (1998): Females of the parasitic phorid Neodohrniphora sp. were collected in the field and released singly inside an observation chamber placed between a laboratory colony of Atta sexdens and its foraging arena. The number and speed of loaded and unloaded ants returning to the nest, the weight of foragers and their loads, the number of leaf fragments abandoned by ants, and the number of small workers ‘hitchhiking’ on leaf fragments were measured before phorids were released, while they were in the observation chamber, and after they were removed. Relatively fewants were attacked by Neodohrniphora sp., but the presence of flies prompted outbound ants to return to the nest and caused a significant reduction on the number and mass of foragers. Additionally, the weight of leaf fragments transported by ants was reduced and the number of abandoned fragments increased in response to Neodohrniphora sp. Presence of the parasitoid caused no significant changes in the number of hitchhiking ants. The regular ants’ traffic was resumed after phorids were removed, but foraging activity remained below normal for up to three hours. In the field A. sexdens forages mostly at night, but colonies undergo periods of diurnal foraging during which ants are subject to parasitism from several species of phorid flies. Considering that daytime foraging may be necessary for nutritional or metabolical needs, phorids may have a significant impact on their hosts by altering their foraging behavior regardless of the numerical values of parasitism.

Impact on Colony Growth
Kaspari (2000) points out that the risk of parasitism may slow the growth rate of some ant colonies. Recent work on the interactions between phorid flies and ants exemplifies this phenomenon. Phorids are tiny parasitic flies, many of which specialize on a single ant species or genus (Brown and Feener 1991a, 1991b; Brown 1993). Phorid flies search for their host ants (often following the odor plume of the ants themselves), hover, then zoom in to lay an egg somewhere on the worker ant's body (Porter et al. 1995a, 1995b; Feener et al. 1996). The worker falls over, stunned, then eventually returns to the colony and dies when the egg hatches and the ant serves as food for the developing maggot.

However, phorid flies first must catch worker ants. Host ants often run and hide in the presence of their phorid parasite (Porter et al. 1995c). This reaction is so profound as to interfere with foraging, and perhaps swing the competitive balance away from the host ant to its phorid-free competitor (Feener 1981).

Feeding on Odontomachus
The following notes are provided by Brown at al. (2015):

Females of the Dohrniphora longirostrata group decapitate injured Odontomachus ants in tropical Central and South America, both for their larvae but apparently also to feed themselves and allow development of eggs. Such feeding behavior is known for other non-gravid parasitoid flies feeding on their injured host ants (Brown 2000), especially Apocephalus species. For Dohrniphora females, this behavior is laborious and time-consuming, but is apparently a viable way for them to obtain food. The species D. longirostrata is common in Atlantic forests in Brazil, and in other localities D. longirostrata group species are among the commonest Dohrniphora in Malaise trap samples (Brown and Kung 2007). Injured Odontomachus hosts must be common in the environment for flies to reach such densities. Indeed, recent work suggests that injured ants in general are a reliable source of hosts and nutrients for phorid flies (Segura and Brown 2014). Over the last 30 years, the authors have been crushing ants and other arthropods in tropical forests in eight countries of South and Central American, resulting in about 120 distinct collecting records of nearly 2500 specimens (Suppl. material 1). This vast resource of data shows that, in addition to the D. longirostrata species group, at least 70 species of the Apocephalus miricauda group feed and oviposit on injured ants (Brown 2000), as do the 100 known species of the metopinine genera Rhyncophoromyia Malloch, 14 Diocophora Borgmeier (Brown 1999), and some others (Disney and Maschwitz 2000, Brown 2010, Disney and Brown 2003). Milichiid, chloropid and ceratopogonid flies are also frequently attracted, apparently to feed. Possibly, as was postulated for parasitoids of the ant Paraponera clavata (Brown and Feener 1991), frequent inter-colony aggression (Segura and Brown 2014) provides the large number of injured workers necessary for these flies to breed so profusely. Regardless of the source in nature, the specificity of D. longirostrata group species to Odontomachus ants amidst the hundreds of records of phorid flies attracted to injured ants is notable. These flies were similarly never attracted to injured grasshoppers, katydids, or termites, all of which are part of our normal field protocol and attract many other phorids (including other Dohrniphora).

It is common in tropical forests for up to 50-100 species of Dohrniphora to be co-existing (Brown and Kung 2007, Brown and Kung 2010). These flies are often dismissed as scavengers, but if so, the number of sympatric congeners, plus hundreds of other species of phorid “scavengers” pursuing the identical saprophagous lifestyle is difficult to explain. Extremely specialized natural histories, like that of the D. longirostrata species group probably allows such a high diversity of saprophagous flies to co-exist in tropical forests.

Associations with Army Ants
Brown & Fenner (1998) provide the following notes regarding phorids associated with army ants.

In general, there are two types of associations between phorid flies and ants (Borgmeier 1928; Brown 1993):
 * Nest symbionts live in ant colonies as scavengers in refuse piles, as predators of host ants, their brood or other guests, or on food regurgitated directly to them by host ants (Rettenmeyer & Akre 1968). The majority of these symbionts are associated with New World army ants (subfamily Ecitoninae).
 * Aerial parasitoids, in contrast, live independent of ant colonies as adults and are obligate parasitoids of arthropods, mostly sterile worker ants or, more rarely, reproductive females. Many of these parasitoids are extremely host specific, attacking only particular species or castes. Eggs are deposited in the head, thorax or abdomen of host ants and larval development proceeds therein.

Aerial Parasitoids of Army Ants
All previous summaries of the literature on army ant-phorid interactions have assumed that co-occurrence of the ants and flies implies a host-parasite relationship. Actual observations of phorids attacking ants, however, are exceedingly rare, and in their absence such assumptions are highly questionable. Actual host-parasite relationships cannot be gleaned from the literature, as all published records refer to flies “associated with” ants or “flying over” ants. No records of attacks on army ants are available in the literature.

Definitive records of phorids attacking army ants therefore are limited. Only species of Cremersia and Dacnophora are confirmed army ant parasites; these two genera are associated exclusively with non-Eciton army ants. But most of the phorids we have collected in association with army ants were with the commonly observed, above-ground foraging army ant species Eciton burchellii and Eciton hamatum. This leaves open the following question: what are the majority of these flies doing?

Phorids Attacking Victims of Army Ant Raids
Our observations indicate that most of the phorid species associated with raids actually attack victims of army ants rather than the army ants themselves. These victims, usually other ants, are emitting distress pheromones, substances that are known to attract some parasitic phorid flies (Brown & Feener 1991; Feener et al. 1996).

Pseudacteon
Pereira et al. (2015) - The genus Pseudacteon has a worldwide distribution and comprises parasitic myrmecophilous species that decapitate host ants. Seventy three species are known in the genus with 41 of them occurring in the Neotropical Region.