Leaf-Cutter Ant Parasitoids: Current Knowledge
Phorids that parasitize leaf-cutting ants affect the foraging activity of their hosts the ants; (2) flying: when the phorid was flying to get close to an ant, came back to The relationships between the dependent variable (presence of Thanks for the logistical help and/or permits to perform fieldwork given by. Parasitism is another one of the three types of symbiosis. The relationship between leaf cutter ants and the phorid fly is parasitic, where the leaf The female then grows large, its eyes shrink, and its legs stretch out, helping to anchor it to the. Habitat fragmentation can have a high impact on parasitoid–ant interactions. Phorid flies are among the most important groups of natural.
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.
Behavioral Strategies of Phorid Parasitoids and Responses of Their Hosts, the Leaf-Cutting Ants
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.
Behavioral Strategies of Phorid Parasitoids and Responses of Their Hosts, the Leaf-Cutting Ants
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. Other features that help to identify among the mentioned genera are related to the pupae.
Parasitism - Symbiosis Website-Alissa C
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.
Psyche: A Journal of Entomology
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 ].
Differential host use by Neotropical phorid flies Diptera: Phoridae that are parasitoids of ants Hymenoptera: Behavior and host location cues of Apocephalus paraponerae Diptera: Phoridaea parasitoid of the giant tropical ant, Paraponera clavata Hymenoptera: New species and new records of Apocephalus Coquillett Diptera: Phoridae that parasitize ants Hymenoptera: A key to Neodohrniphora Diptera: Phoridaeparasites of leaf-cutter ants Hymenoptera: Journal of Natural History, Two new species of Phoridae Diptera associated with leaf-cutter ants Hymenoptera: New species and revision of Myrmosicarius Diptera: Phoridae that parasitize leaf-cutter ants Hymenoptera: New species and new records of scuttle flies Diptera: Phoridae that parasitize leaf-cutter and army ants Hymenoptera: Biology and oviposition behavior of the phorid Apocephalus attophilus and the response of its host, the leaf-cutting ant Atta laevigata.
For dipteran parasitoids with mobile adult hosts, behavioral defenses are a critical element to overcome, and one that effectively determines the host range of these flies Feener and Brown Acromyrmex and Atta cut plant tissue from surrounding vegetation and carry the pieces back to their nest using a persistent trail network Kost et al. When ant workers are outside the nest for any reason, they could be attacked by phorid Diptera: Phoridae endoparasitoids, which use a piercing ovipositor to insert an egg inside the worker's body.
The phorid species that use Atta as hosts do not use Acromyrmex ants Elizalde and Folgarait The host-related behaviors i. Moreover, no generalizations have been made for any of these parasitoids in terms of host-related behaviors. Phorid species that frequently parasitize leafcutting ants belong mainly to three genera: Apocephalus BrownEibesfeldtphora recently raised to the genus status, being previously a subgenus of Neodohrniphora, Disney et al. For example, one Eibesfeldtphora species attacked more often when ant foraging activity was higher Tonhasca Some of these behaviors can involve ants that are not directly at risk of being parasitized by phorids, in which case they constitute colony level responses against the parasitoids.
One of these colony level behaviors against the phorids, and unique to leaf-cutting ants, is the presence of hitchhikers. Hitchhikers are small workers, too small to host the phorids, that ride on the leaves transported by bigger and suitable host workers Eibl-Eibesfeldt ; Feener and Moss Through experimental and detailed observations in the field, Feener and Moss showed that hitchhikers had a defensive function against phorids that land on leaves to oviposit.
Almost nothing is known about the behaviors that Acromyrmex ant species exhibit against the phorids that attack them, except for some occasional observations Brown Specifically, the following aspects of parasitoid behaviors were addressed: Then, focusing on host behaviors, the following characteristics were evaluated: Materials and Methods Host-related behaviors of phorids In order to describe host-related behaviors of phorids attacking leaf-cutting ants, the following were considered: Data was collected in 12 localities in Argentina and two in Paraguay sampling sites in Elizalde and Folgarait At each locality, and in at least three nests of each leaf-cutting ant species present, phorids were searched for in the sites where they are known to oviposit, such as foraging trails and cutting sites.
In addition, phorids were searched for at external refuse piles, where some ant species dispose of their wastes i. Once a phorid was found, its behavior was observed focusing on items bcand das mentioned above. Observations of phorids from a very short distance by a trained, naked eye were more efficient for behavioral data gathering than using a video camera because video-recording in the field at the speed and distances these small phorids move was not possible.
After completing the behavioral observation, phorids were captured in order to identify them to species. For completeness, unpublished data about the host-related behavior of a phorid species collected in La Selva Biological Station in Costa Rica were included. The behavioral observations were all performed during daylight hours and when ant activity was well established.