Assessing Host Specificity and Potential of Fire Ant Decapitating Flies tain relationship to fire ants (Porter et al., a). Escape . Phorid decapitating flies of the genus Pseudacteon are the third group of . perhaps Pogonomyrmex harvester ants and Atta leaf-cutter ants would stand out as iconic species. JSTOR is a not-for-profit organization founded in to build trusted digital archives for scholarship. We work with the . between leaf-cutting ants and parasitic phorid flies . relationship between leaf mass and carrier mass was determined. 2The Conservation Land Trust Argentina, Carlos Pellegrini , () Corrientes, Argentina. Relationships among species were established based on their activity Borgmeier, T. Revision of the North American phorid flies. . size on Apocephalus attophilus offspring, a parasitoid of the leaf-cutting ant Atta bisphaerica.
Whilst highlighting how there remains a wealth of hidden biological diversity right under our noses, I became particularly interested in this story for another reason. A quick search demonstrated the many varied life cycles this family possesses from fungus to flesh feedersbut what grabbed my attention were those that act as brain eating, ant-decapitating parasitoids!
These flies were definitely worth a bit of further research. A variety of ways to make a living Phorid flies are a single family within the order Diptera, which contains the true flies. They are small insects, typically between 0. Photo credit Halvard Hatlen, hosted wikicommons. With approximately 4, species known worldwide, most dwelling in tropical latitudes, these flies possess an incredible variety of life styles.
This latter group of phorids are extremely valuable to forensic entomologists. But as fascinating as these life styles are, it is those that consume ants heads from the inside that naturally I was most interested in. The brain-eaters Parasitoid phorid flies are the scourge of many ant species. As the ants forage outside their nests, phorids stalk their hosts, hovering above them menacingly. The march is halted as the ants head falls off, decapitated by the secretion of neck-membrane dissolving enzymes produced by the developing fly.
A grizzly but amazing lifecycle. Pseudacteon curvatus ovipositor used for injecting an egg into its ant hosts. These ants have mass recruiting strategies, following a trail, more or less developed or clear, depending on the species, with 1 to several trails per nest, short or as long as m. In Atta foraging trails are numerous and very conspicuous. Atta a, b and Acromyrmex c morphological differences and exhibiting different body postures.
Acromyrmex colony nests can be completely hypogeous underground, i. The existent literature on the shape of Acromyrmex nests [ 15 — 17 ] is incomplete. Another conspicuous feature that helps identify some species of this genus is the location of refuse dumps. Most Acromyrmex species have internal refuse dumps, although there are few exceptions where this characteristic is very helpful in identification i.
Psyche: A Journal of Entomology
However, distinctions among species require an experienced eye that could also recognize key morphological characteristics of workers.
Unfortunately, we know very little about the natural history of these species and the costs involved in dealing with trash and nest construction. For instances, is it less costly to lose additional workers by carrying the unsanitary trash outside to eliminate possible foci of infection or is it more energy efficient to close a trash filled internal chamber and not to maintain it? If the trash is internal, are these ants taking advantage of the nutrients that mineralize within those trash-decomposition hot spots?
Is the heat produced by internal refuse dumps utilized by the ants for colony or fungal thermoregulation? Phoridae within 8 genera associated with Acromyrmex ants whereas 39 species in 5 genera were recorded on Atta.
Also, he lists 7 cases of the same phorid species seen flying or sitting beside the nests of both genera. However, if only positive-sure cases hosts from which parasitoids emerge or phorids seen pursuing and attacking ants are considered, these numbers decrease for Acromyrmex to 15 species in 4 genera, for Atta to 25 species, and 4 genera with only 2 observations of phorids attacking both genera Apocephalus setitarsus and Myrmosicarius crudelisalthough these could well be mistakes or trials that were seen only once.
Further observations for these two species should be specifically done as one of the references for each record is very old. In fact, Elizalde and Folgarait [ 1219 ] argue that leaf-cutter phorid parasitoids are very specific in the sense that those attacking Acromyrmex ants do not attack Atta and vice versa.
Therefore, these observations could be considered mistakes or tests made by the parasitoids. What really matters is the recurrent attack of a phorid species on the same host and its possibility of emerging from that host.
According to this criterion, phorids that attack Acromyrmex or Atta ants are specific to that ant genus. Recently the subgenus Eisbesfeldtphora was elevated to genus status [ 20 ], and a new genus with a single species has been described Lucianophora folgaraitae Disney [ 23 ].
However, Eibesfeldtphora is present in the largest number of countries [ 9 ]. Among the four most important genera attacking leaf-cutter ants, Apocephalus [ 26 ], Eibesfeldtphora [ 1027 ], Myrmosicarius [ 2829 ], and Neodohrniphora [ 10 ], it is difficult to say which one is most important.
In the case of Apocephalus, the subgenera Apocephalus includes only ant-decapitating flies, and these flies are recognized for lacking tibial setae and possessing abdominal segments 7 to 10 fused to form an ovipositor, with which the eggs are inserted into the host. Segment 7 forms a rigid structure called oviscape.
Another diagnostic character is the presence of a stylet comprised of segments 8 to 10 [ 30 ] Figure 2. The mentioned subgenus has subgroups specializing on different ant subfamilies. These are potentially monophyletic groups. Apocephalus flies attack both ant genera with 8 recorded species attacking Atta and 6 others that use Acromyrmex as hosts [ 9 ]. Neodohrniphora at present has only two species attacking leaf cutters N. This genus is distinctive because the front legs have 5 unusual fore-tarsal segments.
Besides, abdominal segment 6 is either reduced to hairs or has on its sides a transverse row of long hairs. Segment 7 also could be reduced to 2—4 hairy lobes or is basally articulated to form appendages. Beyond the ovipositor and below the tip of the abdomen is found a strongly sclerotized hook [ 31 ] Figure 2. Eibesfeldtphora largely specializes as 9 out of 10 species are known to oviposit or develop on Atta hosts.
It has yellow legs with dorsal enlarged hair palisade in all tibia. Fore leg with tarsomeres 4 and 5 fused, therefore with 4 distinctive tarsomeres. Abdominal segments are yellow ventrally 1—5but segment 6 is mainly dark. Segment 7 has several lateral lobes darkly sclerotized. Segments 8—10 form at the end a pointed stylet [ 27 ] Figure 2. There are 6 Myrmosicarius species that attack Acromyrmex whereas only 3 attack Atta. Females of the latter are recognized because the front tarsus is reduced to two segments; the sternite of the abdominal segment 6 is absent or vestigial and, by the characteristic oviscape tube, relatively nonornamented, that is, formed from abdominal segments 7 and 8 [ 29 ] Figure 2.
Schematic drawings of phorids showing details of the main characters that can be used to easily identify and distinguish among the main genera attacking leaf-cutter ants. Sizes represent real relative differences.
Leaf-Cutter Ant Parasitoids: Current Knowledge
Other features that help to identify among the mentioned genera are related to the pupae. While most Apocephalus species have a free pupae, the other genera have claustral pupation in the dead host head. Apocephalus do not decapitate their host and is unique in that more than one adult can emerge from a single host although this has not been recorded on Acromyrmex hosts. Also Apocephalus vicosae is the single exception for having a pupae coming out from the thorax.
Myrmosicarius pupae are difficult to detect as the pupa is found deep in the head, below the tentorium arms, and the respiratory horns do not come outside of the head capsule; all these parasitoids decapitate their host. The other two genera pupae also develop in the head although they are easily seen and recognized by the exposed respiratory horns and sclerotized operculum Figure 3 ; not all the species induce host decapitation [ 32 ].
Schematic drawings showing different types of pupae according to the parasitoid genus. Dorsal view of a free pupae from Apocephalus, top right: Generalities Atta parasitoids oviposit on workers while transporting leaves in the foraging trail or while potential hosts are cutting leaf fragments [ 33 — 36 ], sometimes using the load transported by the ant as a platform [ 37 ] or not [ 3839 ].
In the case of Acromyrmex parasitoids, not only these also attack ants on the foraging trail, those that are transporting a load or cutting leaves, but also while workers are repairing the nest or attending external refuse piles [ 19 ]. Both Atta and Acromyrmex parasitoids use either an ambush or an actively searching strategy and oviposit on different parts of the ant body such as through on the mandibles, in the head, thorax, legs, and anus [ 323840 ].
Tables summarizing this information at the species level can be found for Acromyrmex [ 19 ] and for Atta [ 20 ]. Eibesfeldtphora females can use an ambush or active searching strategy, can land and oviposit on the head or abdomen, and always attack ants on the foraging trails while pursuing the host; in general they rest close to nest entrances.
On the other hand, Myrmosicarius is mainly an active flyer while searching for its host. Some of them can fly onwards, backwards, or sideward. They also land and oviposit in the head mandible, clypeus, and occiput and abdomen tip and can attack while on the trails, doing nest maintenance, or at refuse dumps.
Apocephalus females attack using an ambush strategy, landing on the leaves carried by the ants, and ovipositing close to the mandible. Neodohrniphora are ambush or active searching parasitoids; there are too few records so as to generalize this genus. The four genera search hosts at foraging trails [ 19 ]. Refuse Dumps Phorids attacking ants at refuse dumps were observed only for Acromyrmex ants [ 19 ].
This behavior was recorded consistently for M. The common factor seems to be the Monte habitat and inconspicuousness of the foraging trails of the mentioned hosts either for being subterraneus or otherwise covered with vegetation and being difficult to find. Therefore, the refuse piles could be a better place to spot the ants by these phorids in microhabitats with dense and high vegetation and low light. In fact, the mean light intensity at this habitat is 1 order of magnitude lower than for species attacking at other microhabitats [ 20 ].
Despite this capacity to oviposit at very low light levels, phorids attacking at refuse piles do not coincide with nocturnal ones M. As nocturnal phorids are also diurnal, therefore an exact agreement between the phorid circadian rhythm and the microhabitat of attack may not be necessary. It is expected that refuse dump and nocturnal phorids rely more on close-range cues not associated with vision. This hypothesis, with the little knowledge that exists, disagrees with the data gathered for Neodohrniphora elongata [ 41 ]; however as it is a diurnal phorid as far as it is knownit is reasonable that uses visual cues in motion for host location and recognition.
On the other hand, another diurnal phorid, Pseudacteon tricuspis, uses short range chemical cues to locate their fire ant hosts [ 42 ]. This topic deserves further attention and research [ 43 ].
Phorid species that consistently attack at refuse piles such as M. These abilities may be important in a small microsite, such as the refuse piles of these hosts, where many ants are together, carrying refuses and walking in a variety of directions in comparison to the bimodal pattern on a foraging trail. Their developmental times are the longest recorded to date, even considering that developmental periods of phorids that attack Acromyrmex ants are longer than those coming from Atta.
Furthermore, considering that these flies attack small ants [ 20 ], these lengthy developments are even more surprising as, in general, phorids attacking smaller ants develop faster than those attacking larger ones [ 254445 ]. Probably, the ants involved in this task, such as carrying refuses plus working on them, are constantly dealing with infectious pathogens and may well be considered disposable ants from the colony point of view either for being old or having a bad health and, in turn, poor hosts from a phorid nutritional perspective.
If this is the case, then a longer developmental time is expected. Leaf-Cutters Defenses against Parasitoids 4.
Generalities Phorids that parasitize leaf-cutting ants affect the ant behavior which translates to a negative effect on their foraging activity. The response behaviors of Atta ants against phorids include dropping their load [ 33 ], retreating to the nest [ 46 ], moving legs, antennae, and mandibles [ 37 ], outrunning the phorid [ 40 ], or adopting particular body postures in order to avoid oviposition such as lowering the tip of the abdomen, having a C posture, or making a ball with their whole body Figure 1 [ 3339 ].
Similar behaviors were observed in Acromyrmex ants [ 19 ]. The presence of phorids was a significant determinant for the display of defensive behaviors by Acromyrmex ants. In fact, this chance was 5 times greater in the presence of phorids than in their absence [ 19 ]. It is particularly intriguing why phorids that attack Atta ants are not the same as those attacking Acromyrmex [ 32 ] considering 1 that, in several cases, the ants are attacked by species from the same genus, 2 that hosts oviposited by different phorid species respond in such similar ways to the attacking flies, and 3 that both host genera could be present in the same habitat as well as their specific parasitoids.
Besides, Atta parasitoids do not attack soldiers, a caste not present in Acromyrmex ants. Although ant species varied in the incidence levels of defensive behaviors like the ones mentioned above, most ant species reacted against different phorids utilizing similar behaviors, as, for example, ants being attacked by an anus ovipositing fly typically lowered their abdomen, whereas ants being attacked by a head ovipositing fly adopted a C or biting posture Figure 1.
In contrast, parasitoids perform different behaviors when presented with multiple hosts [ 19 ]. Furthermore, Acromyrmex ants are generalist hosts in terms of being attacked by several phorid species, whereas phorids are mainly specialists attack only one host species [ 20 ], adding another level of asymmetry in the interaction.
This pattern is not as strong for Atta ants [ 9 ]. As mentioned in Elizalde and Folgarait [ 19 ], parasitoids can choose their hosts whereas leaf cutters cannot easily reject or avoid a specific phorid species. Phylogenetic analyses of phorids that attack each genus may shed some light although immunological capacities could also help explain the lack of overlap. However, it will be more fruitful to first perform specificity tests offering different species of specialist parasitoids to a single host species.
Besides, it will be useful to evaluate, in long-term field studies, new communities where leaf-cutter hosts and nonhosts of several phorids species are present.
Hitchhikers There has been a long standing controversy regarding the role s of hitchhikers, which are small ants riding on leaves that are transported by foraging workers. Despite the initial role proposed as defenders against parasitoids of the ants they ride [ 37 ], other functions are offered such as leaf microbes cleaners or sap ingestion from cut leaves [ 47 — 49 ]. Initially, it was also proposed that hitchhikers needed a flat surface where to ride [ 37 ] and were present only during the day because of the diurnal phorid activity [ 46 ].
However, in Acromyrmex, hitchhikers were found to ride on tips of monocots or pieces of grasses, they were present at night, and it was shown that nocturnal phorids exist [ 1935 ]. At present, hitchhikers are known for each of the 9 Atta species in which this behavior has been studied.
The latter authors have shown that the chance for finding greater proportion of ants exhibiting hitchhikers was 2. Leaf Cutter and Their Parasitoids: Some Relevant Aspects of Their Interaction 5. Parasitism Rates Natural parasitism from the same nests of Atta vary through time [ 2532 ], and these rates may reflect changes in health status of each colony or physiological tolerances of phorids to different weather conditions.
For comparable data, percentages of natural parasitism in Atta are greater than in Acromyrmex in Argentina.Massive Leafcutter ant colony