Phorid Species Research Articles

Behavioral Strategies of Phorid Parasitoids and Responses of Their Hosts, the Leaf-Cutting Ants

Host-searching and oviposition behaviors of parasitoids, and defensive responses of the hosts, are fundamental in shaping the ecology of host-parasitoid interactions. In order to uncover key behavioral features for the little known interactions between phorid parasitoids (Diptera: Phoridae) and their leaf-cutting ant hosts (Formicidae: Attini), host-related behavioral strategies (i.e., host searching and oviposition) for 13 phorid species, and host defensive responses (i.e., hitchhikers and particular body postures) for 11 ant species, were studied. Data was collected at 14 localities, one of them characterized by its high species richness for this host-parasitoid system. Phorid species showed both great variation and specificity in attacking behaviors. Some chose their hosts using either an ambush or an actively searching strategy, while some species attacked ants on different body parts, and specialized on ants performing different tasks, such as when ants were foraging, removing wastes to refuse piles, or repairing the nest. Combining all the behaviors recorded, most phorid species differed in performance in at least one, making it possible to recognize species in the field through their behavior. Phorid species that attacked hosts with greater activity levels showed overall higher attack rates, although there was no significant correlation between attack rates by most phorid species and ant activity outside the nest while parasitoids were attacking. The presence of phorids was a significant determinant for the presence of defensive behaviors by the ants. Although ant species varied in the incidence levels of these defensive behaviors, most ant species reacted against different phorids by utilizing similar behaviors, in contrast to what parasitoids do. General features of the observed phorid-ant interactions were parasitoid specialization and corresponding high interspecific variation in their behaviors, while their hosts showed generalized responses to attacks with high intraspecific variation. Behavioral patterns as well as specific features of these ant-parasitoid interactions are described, and their ecological importance discussed.

Environmental and Habitat Drivers of Relative Abundance for a Suite ofAzteca-AttackingPseudacteonPhorid Flies

Phoridae (Diptera) have widespread impacts on insect communities by limiting host ant behavior. However, phorid-ant interactions may vary with habitat or environmental conditions. Three Pseudacteon species parasitize Azteca instabilis Fr. Smith, a common ant in coffee agroecosystems, and limit A. instabilis foraging, indirectly benefiting other insects. However, little is known about how phorid abundance, behavior, and effects change with environmental conditions. In shaded coffee systems, coffee (Coffea arabica L.) grows under a range of shade conditions and management changes affect species interactions. For example, Pseudacteon spp. more strongly limit A. instabilis foraging in low-shade coffee habitats. We sampled relative abundance of three phorid species around A. instabilis nests in three coffee habitats varying in shade management during dry and wet seasons. We measured canopy cover, tree richness, tree density, leaf litter depth, and number of nearby trees with A. instabilis to determine whether these habitat factors correlate with phorid abundance. P. laciniosus Brown was the most abundant phorid in both seasons. Phorid relative abundance did not differ by habitat, but did differ by season. P. laciniosus accounted for a higher proportion of phorids in the wet season (91.4%) than in the dry season (78.9%), and P. planidorsalis Brown accounted for a larger percent in the dry season (21.1%) than in the wet season (7.3%). Phorid composition did not differ with habitat type, and none of the measured environmental variables correlated with changes in phorid composition. Thus, phorids in coffee agroecosystems respond to large seasonal differences, but not differences between coffee habitats.

Parasitoid phorid flies (Diptera: Phoridae) from the threatened leafcutter ant Atta robusta Borgmeier (Hymenoptera: Formicidae)

Phorid flies are well known natural enemies of leafcutter ants, but there is no information on phorid species associatedwith the threatened species Atta robusta Borgmeier. During 2009 and 2010 we collected phorid parasitoids of A. robustaat Guriri Island, Espirito Santo (18o43’S; 39o 45’W) and at Rio de Janeiro city (23°01’S; 43°28’W). Three new specieswere found: Eibesfeldtphora breviloba Brown, E. digitata Brown, and Myrmosicarius exrobusta Brown. These species,the attack behavior of the two species of Eibesfeldtphora, as well as the anti-parasitoid defense behavior of A. robusta, are described.

Biological attributes of Argentinian phorid parasitoids (Insecta: Diptera: Phoridae) of leaf-cutting ants, Acromyrmex and Atta

Little is known about the natural history of phorid parasitoids of leaf-cutting ants, an important pest in the Neotropics. This is particularly so for phorids attacking Acromyrmex species. We searched for phorids ovipositing and reared them from ants collected in the field. We found that these phorids formed a guild. Acromyrmex phorids selected ants from all sizes available outside the nests, whereas Atta phorids did not parasitize the smallest workers and soldiers. Maximum parasitism by phorids was 12% for Acromyrmex and 35% for Atta hosts, percentages higher than any reported previously. Some phorid species coexisting in a site showed differences in developmental times. Only 1.1% of phorids collected over hosts were males; however, as the male : female ratios from parasitoid rearing did not differ from one, mating is suspected to occur elsewhere. Our results helped to increase the knowledge of the phorids of leaf-cutters, and highlighted their potential use for the biocontrol of these ants.

Life-History Traits and Parasitism Rates of Four Phorid Species (Diptera: Phoridae), Parasitoids of Atta vollenweideri (Hymenoptera: Formicidae) in Argentina

Leaf-cutting ants in the genus Atta F. (Formicidae, Attini) are among the most important pest arthropods in Central and South America, consuming more vegetation than any other animal group. Among the organisms attacking ants in nature, flies of the family Phoridae have been proposed as the most promising biocontrol agents for pest ants. Four phorid species, Apocephalus setitarsus Brown, Myrmosicarius brandaoi Disney, Myrmosicarius gonzalezae Disney, and Eibesfeldtphora trilobata Disney, were reared from ants collected at Atta vollenweideri Forel nests and off foraging trails in Santa Fe province in Argentina. E. trilobata attacked larger ants and had bigger adults than the other species, also exhibiting the longest developmental time. Correlations between size of hosts and size of adults, as well as between size of adults and developmental times, could be established only in some cases. No differences were found between the sizes of the hosts from which males and females emerged. The natural percentage of parasitism varied throughout the seasons and seemed to be influenced by the extreme drought affecting the study site. We discuss why all four species would be suitable candidates for integrating an assemblage of biocontrol agents against A. vollenweideri.

Introduction of the fire ant decapitating fly Pseudacteon obtusus in the United States: factors influencing establishment in Texas

The introduction and establishment of Pseudacteon obtusus Borgmeier (Diptera: Phoridae) into the United States is an important milestone in the effort to introduce a suite of parasitoids and pathogens as prospective biocontrol agents of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae).P. obtusus is the fourth species of phorid fly to be established in the US and is now present in at least 11 sites in Texas. This species has a greater propensity for attacking foraging worker ants, and to a lesser degree it will attend mound disturbance events. The effectiveness of alternate field release strategies was evaluated across 28 sites in Texas, with establishment success 35 times more likely when no other phorid species were present at the outset of the releases. This result implies that competition between phorid species may interfere with establishment. Therefore release strategies should be directed to locations lacking other naturalized species or to times when abundances of other species are low.

Host diversity and environmental variables as determinants of the species richness of the parasitoids of leaf‐cutting ants

AbstractAim Because of the obligatory relationship between endoparasitoids and their hosts, we presume that hosts exert strong selection pressure on parasitoids. One prediction is a positive relationship between host diversity and parasitoid richness. This relationship could be the product of resource availability which could lead to more opportunities for speciation, or could represent shared responses to the environment by both groups.Location Argentina and Paraguay.Methods We sampled a 1800‐km transect to test for a correlation between the richness of leaf‐cutting ant hosts and their phorid parasitoids. Regression models were used to assess if host and environmental variables could explain phorid species richness at nest, hectare and locality spatial scales. We used canonical correspondence analysis (CCA) to explore if there were similar responses of phorid species to particular host and environmental variables at different spatial scales, and partial CCA to separate the relative importance of both groups of variables.Results Phorid richness was positively correlated with host richness. Host richness/abundance accounted for 20–53% of the variation in parasitoid richness at the hectare and locality scales of analysis, with most of the variation accounted for by ant abundance. We were not able to assess the prediction at the nest scale as only one phorid species was found at most nests. Climatic variables did not explain phorid species richness once host variables were in the models. Partial CCA showed that host‐related variables accounted for most of the variance associated with phorid species ordination at the nest and hectare scales, but not at the largest grain, the locality, where climatic variables were more important. However, most phorid species did not show particular positions along the climatic gradient.Main conclusions The association between parasitoid richness and host richness and abundance, and the overall weak associations with environmental variables, suggest that these host variables are key factors influencing parasitoid speciation.

Molecular identification of carrion-breeding scuttle flies (Diptera: Phoridae) using COI barcodes

Entomological evidence is often used in forensic cases for post-mortem interval (PMI) calculation. The most dominant species present on a corpse are typically blowflies. However, several cases have been reported where access to a corpse has been restricted for blowflies (e.g., on a buried or wrapped cadavers) but species of the family Phoridae were abundant. It has also been reported that some phorid species that exploit human corpses may also feature in cases of myiasis acquired ante-mortem. In all these cases, they may provide decisive evidence. As for blowflies, the precise identification of a phorid species collected from a corpse is necessary when estimating the PMI. Since morphological determination is often hampered due to similar characteristics especially in the larval and pupal stage, we used DNA-based methods to identify six phorid species (Megaselia scalaris, Megaselia giraudii, Megaselia abdita, Megaselia rufipes, Conicera tibialis, and Puliciphora borinquenensis) on the molecular level. We focused on a 658-bp-long region of the cytochrome oxidase I gene (COI), the most common molecular marker in forensic entomology. The amplified fragment is also used in DNA barcode approaches and was found to be suitable for identification of a wide range of insect taxa. The present study demonstrates that this region is also sufficient to distinguish between several species of scuttle flies.

A review of termitophilous and other termite-associated scuttle flies worldwide (Diptera: Phoridae)

AbstractA review is provided of the morphological and behavioural observations known for the 190 recorded termitophilous and other termite-associated species of Phoridae (scuttle flies) known worldwide. A full list of these termite-associated phorids is provided, together with their recorded termite hosts, as an Appendix. The influence of batch size, egg size, developmental cycle, wing reduction and winglessness, egg-laying and morphological adaptations of a termite-associated lifestyle is discussed, based on differences observed among termite-associated phorids. A high number of termitophilous phorid species with batch sizes of four eggs or less are noted, probably reflecting the stable environment termitophilous phorids experience, and the high percentage of species with parasitoid or predatory larvae. Minimising the free-living larval stage by a reduction of the number of instars, by larval instar curtailment, or by endoparasitism is here hypothesised to be an advantageous life history strategy for many termite-associated phorids. Termite-associated phorids can be divided into four main types, according to their biology and morphology. The exploitive- and generalistic-types include both obligate and non-obligate termite associates that take advantage of the more vulnerable stages of the termites. The protective- and guest-types are obligate associates, spending full larval and pupal stages with their hosts. The guest-type is described as being socially integrated, communicating with the host and being involved in worker/nymph interactions.

Survey of Neodohrniphora spp. (Diptera: Phoridae) at colonies of Atta sexdens rubropilosa (FOREL) and specificity of attack behaviour in relation to their hosts

Atta sexdens rubropilosa is a leaf-cutting ant that is a significant agricultural and forestry pest in the Neotropical region. This ant is parasitized by flies from the genera Neodohrniphora spp., Apocephalus spp. and Myrmosicarius spp. This study was carried out to determine which species of Neodohrniphora spp. are found near foraging trails of Atta sexdens rubropilosa and to evaluate the specificity of attack behaviour of these parasitoids. From May 2002 to April 2004, we sampled Neodohrniphora spp. hovering over foraging trails of Atta sexdens rubropilosa between 8:00 and 11:00 h and between 15:00 and 18:00 h. To investigate the attacking behaviour against the ants, flies were released individually inside an observation chamber containing a single leaf-cutting ant worker. Each parasitoid was confronted successively with a worker ant of A. sexdens rubropilosa, Atta laevigata Smith, Acromyrmex crassispinus Forel and Acromyrmex subterraneus molestans Santschi. Phorids of three species were identified: Neodohrniphora elongata Brown, Neodohrniphora declinata Borgmeier and Neodohrniphora tonhascai Brown. The three phorid species were active throughout the year and often along the same foraging trails, but N. elongata was the most frequent species. In the laboratory assay, N. elongata, N. declinata and N. tonhascai attacked workers of A. sexdens rubropilosa, A. laevigata and A. crassispinus, but not of A. subterraneus molestans.

Some Scuttle Flies (Diptera: Phoridae) of the Galápagos Islands

The first scuttle fly (Diptera: Phoridae) recorded from the Galapagos Archipelago (Megaselia scalaris (Loew, 1866)) was collected during the Williams Expedition (1923) (Johnson 1924) and a second species (Dohrniphora cornuta (Bigot, 1857)) was collected during the Norwegian Zoological Expedition (1925) (Curran 1932). Additional material of the latter species was collected on the Templeton Crocker Expedition of 1932 (Van Duzee 1933; Curran 1934). In 1985, Stewart Peck (Carleton University, Ottawa) started the first of five collecting expeditions to the Galapagos, with the aim of generating an invertebrate inventory of the island fauna. There is little doubt that these surveys have had a tremendous impact on the knowledge of the terrestrial invertebrates, producing numerous publications in many and several major monographs (Peck 2001, 2006). BJS participated in the second Peck expedition of 1989. Vast numbers of specimens were collected on these two surveys, which resulted in the listing of four phorid species, all classified as introduced invasive species (Causton et al. 2006). We report here primarily on the collections of scuttle flies made by S. & J. Peck and BJS and identified by RHLD.

Discovery of Plethysmochaeta nobilis Schmitz (Diptera: Phoridae) from Japan, which has been known from Java

Plethysmochaeta nobilis hitherto known from Java was discovered in Fukuoka and Tokorozawa, Japan. Morphological characters of the specimens obtained in Japan are briefly described, and a key to morphologically similar phorid species in the lowland of Japan is given. In Fukuoka, P. nobilis was caught by sweeping at a park where thousands of crows gathered and the ground was covered with their droppings. In Tokorozawa, it was collected by traps baited with decaying meat. The genus Plethysmochaeta is saprophagous in the larval stage and has been known from Africa and Southeast Asia. It is possible that P. nobilis was transported to Japan by human activity, judging from its food preference and known locality of the genus. It is also possible that P. nobilis is native to Japan at least in the southern region, and the lack of its distribution record in the past is due to limited investigation on the phorids in Japan.

Ocorrência e características biológicas de forídeos parasitóides (Diptera: Phoridae) da saúva Atta laevigata (Smith) (Hymenoptera: Formicidae) em Porto Nacional, TO

The purpose of this study was to verify the occurrence of parasitism in Atta laevigata (Smith) by phorids in Porto Nacional, Tocantins, Brazil and to evaluate some biological characteristics of those flies. From October/2002 to September/2003, at 15-day intervals, 22 samplings were carried out (149.5 +/- 82.9 workers each) comprising 3,704 ants. In the laboratory, the ants were distributed in groups of five individuals per petri dish and maintained at temperature of 25 +/- 1 masculineC and 80 +/- 5% of RH. They were fed daily with a 50% honey solution until death. The total of 106 workers (2.8%), collected with or without load (plant fragment), were parasitized by phorids: 72 workers (68%) were parasitized by Apocephalus vicosae Disney, 28 individuals (26.4%) by Neodohrniphora erthali Brown, and six (5.6%) by Apocephalus attophilus Borgmeier. The higher parasitism rates by A. vicosae (3.9-5.4%) were observed during the dry season (June-August), while the parasitism by N. erthali was lower than 2.3% throughout the year. The bigger workers were parasitized by bigger parasitoid N. erthali or by parasitoid with larger number of larvae A. attophilus. The occurrence of three phorid species in Tocantins broadens the distribution of these flies in Brazil. The development of A. vicosae larva within the thorax of the host as well as the rupture between the ant pronotum and propleuron so that the emergence of the fly can take place are characteristics not yet described on parasitism of leaf-cutting ants by phorids.

Scuttle flies (Diptera: Phoridae) of saline habitats of the Gulf of Gdańsk, Poland

Results ofa survey ofthe scuttle flies (Diptera: Phoridae) of saline habitats ofthe Gulf of Gdańsk are reported. Within three study seasons (1999—2001), at ten 10 localities representing coastal brackish and maritime habitats, 39 phorid species were collected. Among these, 36 were new to these areas, and Xenotriphleba dentistylata Buck was the first record for Poland. The dominance structure, phenology and abundance ofphorids of saline habitats are described.

Testing for population-level impacts of introduced Pseudacteon tricuspis flies, phorid parasitoids of Solenopsis invicta fire ants

Abstract Parasitoid phorid flies in the genus Pseudacteon are potential biocontrol agents of invasive Solenopsis fire ants in the US. One Pseudacteon species, P. tricuspis Borgmeier, has been released and is now established over a large region of north central Florida. We conducted a multi-year, large-scale field experiment to investigate potential population-level impacts on host Solenopsis invicta Buren fire ants and associated arthropods. We established and monitored 67 field sites over a 3.5 year period, documenting S. invicta density and activity by three complementary sampling methods: (1) mound counts and measurements, (2) attraction to baits, and (3) pitfall trap catches. P. tricuspis abundance was determined by censusing flies at disturbed S. invicta mounds. P. tricuspis populations increased in abundance over the first two years following colonization and then oscillated seasonally, reaching higher abundances in the fall than in the preceding spring. S. invicta populations varied greatly over time, and repeated-measures ANCOVA revealed no effect of phorid parasitism pressure on S. invicta density or activity. P. tricuspis likely has a relatively small effect on S. invicta populations, which may not be consistent over space and time and is difficult to document against the background of high variability in fire ant populations due to various environmental factors (i.e., rainfall, disturbance). P. tricuspis parasitism pressure (averaged over the course of the experiment) was positively associated with changes in S. invicta density. Additionally, P. tricuspis abundance was positively correlated with S. invicta density after P. tricuspis populations had been established for >1 year. Introduced phorid populations may require many years before a measurable impact is apparent. Alternatively, parasitism pressure of a single phorid species may not be a major factor regulating fire ant populations.

Seasonal patterns of activity among species of black fire ant parasitoid flies (Pseudacteon: Phoridae) in Argentina explained by analysis of climatic variables

Abstract We monitored weekly relative abundances of adult female Pseudacteon (Diptera: Phoridae) species between February 1998 and May 2000 in Argentina. Fire ant-phorids were active around mounds of Solenopsis richteri Forel throughout the year. Phorid species richness ranged from six species during the summer-fall, to a single, large species during the winter. Species were classified as winter, summer, or fall-spring species, depending on times of peak mean abundance. We used descriptive multivariate techniques to analyze phorid phenological data (correspondence analysis), climatic data (principal component analysis), and their relationships (canonical correspondence analysis=CCA) at three temporal scales. The long-term mean temperatures, the mean and minimum sampling-time temperature, and the cumulative number of days without rain from the two months preceding each sampling day explained >90% of the variance when the data for sampling dates were averaged across the same months over the two years. Pseudacteon borgmeieri Schmitz, the winter dominant, was associated with lower temperatures and rainfall, whereas Pseudacteon curvatus Borgmeier, the summer dominant, showed the opposite pattern. Among the fall-spring species, Pseudacteon comatus Borgmeier was associated with months of higher maximum temperatures, longer photoperiods, and lower relative humidity. Pseudacteon nudicornis Borgmeier, in contrast, showed the opposite pattern. Pseudacteon tricuspis Borgmeier, was associated with months, typically in fall, having greater rainfall and fewer days with frosts. Implications of these patterns for the process of selecting particular species of S. richteri-attacking Pseudacteon for use in biological control introductions against imported fire ants are discussed in relation to climates of source and release areas.

First record of Phorid Parasitoids (Diptera: Phoridae) of the leaf-cutting ant Atta bisphaerica Forel (Hymenoptera: Formicidae)

Phoridae flies parasitize several ant species, including many Atta leaf-cutting ants. In this note, the attacks of three coexisting phorid species (Myrmosicarius grandicornis Borgmeier, Apocephalus attophilus Borgmeier and Neodorhniphora bragancai Brown) against Atta bisphaerica Forel workers in a pasture located in Viçosa County, Minas Gerais State, Brazil, are reported. The first two species of phorids are known to parasitize other leaf-cutting ants. N. bragancai, however, has been found only around A. bisphaerica nests. Each of these phorid species selects ants engaged in different tasks and oviposits in specific sites of the ant body.

Developmental rates and host specificity for Pseudacteon parasitoids (Diptera: Phoridae) of fire ants (Hymenoptera: Formicidae) in Argentina.

This study extends our comparative knowledge of Pseudacteon interactions with Solenopsis fire ant workers. Reported in this work are development times for seven Argentinean parasitoid species reared on two hosts, Solenopsis richteri Forel and Solenopsis invicta Buren, under laboratory temperature regimes comparable with those of the climatic zones occupied by these host species. Developmental times spanned 31-66 d across phorid species, and in general did not differ between genders or host species, but were longer at lower temperatures. The size distribution of flies reared was bimodal, with a group of large (Pseudacteon borgmeieri, Pseudacteon nocens, Pseudacteon obtusus and Pseudacteon tricuspis) and small (Pseudacteon cultellatus, Pseudacteon curvatus, and Pseudacteon nudicornis) species. P. borgmeieri was exceptional with respect to length of developmental time. Also reported are results of initial oviposition and developmental studies of some of these phorid species on other Argentinean Solenopsis ant species; P. curvatus was the only species able to complete its development on nonhost fire ants. These results support the concept of incorporating several complementary species of Pseudacteon in the biological control of pest fire ants.

Parasitism characteristics of two phorid fly species in relation to their host, the leaf-cutting ant Atta laevigata (Smith) (Hymenoptera: Formicidae)

The leaf-cutting ants Atta sexdens (L.) and Atta laevigata (Smith) constitute serious pests of agriculture and forestry in Brazil. These ants are parasitized by the phorids Neodohrniphora tonhascai Brown and Neodohrniphora erthali Brown (Diptera: Phoridae), respectively. The parasitic potential of N. tonhascai against its host has been previously investigated, but no equivalent information is available for N. erthali. The objectives of this study were to evaluate the oviposition behavior and some biological characteristics of N. erthali in relation to its host and to determine the parasitic potential of N. tonhascai against A. laevigata, considering that in many parts of southeastern Brazil nests of A. sexdens and A. laevigata are found in close proximity of each other. These data were obtained from female N. erthali and N. tonhascai collected in the field in Viçosa (Minas Gerais State) and released singly in an observation chamber placed between a laboratory nest of A. laevigata and its foraging arena. Neodohrniphora tonhascai took less time selecting its hosts, attacked more ants and had greater rate of parasitism in relation to N. erthali. We could not establish whether A. laevigata is parasitized by N. tonhascai in the field, but the reproductive success of N. tonhascai in the laboratory demonstrated that A. laevigata is a suitable host to this parasitoid. The types of defense displayed by A. laevigata against both phorid species were markedly different, and these results suggest that foragers take specific defensive steps in order to reduce the possibility of parasitism by phorid flies.

Phorid Fly (Diptera: Phoridae) Oviposition Behavior and Fire Ant (Hymenoptera: Formicidae) Reaction to Attack Differ According to Phorid Species

Phorid flies in the genus Pseudacteon affect the foraging and defensive behaviors of their host, the red imported fire ant, Solenopsis invicta Buren. Field observations of Pseudacteon species indicated interspecific variation in attack behavior. Here, we assess whether differences in attack behavior and ant response might assist in prioritizing species for biocontrol. We studied the oviposition behavior of eight phorid fly species and determined how attack by each influenced the normal behavior of the red imported fire ant. The fly species tested were: Pseudacteon borgmeieri Schmitz, P. curvatus Borgmeier, P. nudicornis Borgmeier, P. obtusus Borgmeier, P. solenopsidis (Schmitz), P. tricuspis Borgmeier, P. litoralis Borgmeier, and P. wasmanni (Schmitz). Of these, P. borgmeieri attack interfered with normal red imported fire ant worker behavior the most, whereas P. curvatus had the least effect. Because the supposed effectiveness of phorids as biocontrol agents depend on their ability to interfere with normal fire ant behavior, these results suggest that some species of phorids would be better candidates for biocontrol than others. Our results combined with results from other studies examining host specificity of phorids suggest that P. tricuspis and P. obtusus are excellent candidates for biocontrol of the red imported fire ant in geographical areas where polygyne colonies dominate, such as Texas. Conversely, where monogyne colonies dominate, such as Florida, P. litoralis should be considered.