Philornis Species Research Articles

Hospederos y patrones de prevalencia de parásitos aviares Philornis (Diptera: muscidae) en la costa de Ecuador

ABSTRACT Most of the species of the genus Philornis are obligate parasites of birds’ nests, especially affecting small populations. However, research on factors influencing its distribution is scarce. This study focuses on analyzing some elements that facilitate the parasitism of this genus on several species of birds in continental Ecuador. From a sample obtained over two years (2019-2020) in five different locations on the country’s coast, 693 nests of land birds and raptors were analyzed. Of these, 13% were parasitized. Two Philornis species already reported for Ecuador (Philornis downsi, P. niger) and two morphotypes not previously registered in the country were recorded, preliminarily classified as P. sp. nr. bellus and P. sp. nr. falsificus. The species with the highest proportion was P. downsi, both in terms of nest prevalence and intensity. Each species of the parasite showed an affinity for one or more families of birds and it was evidenced that the shape of the nest facilitates the prevalence of Philornis. The prevalence of Philornis decreases in higher places in the dry coastal forests. The probability of infection was also influenced by habitat alteration: nests from disturbed sites have a higher prevalence of parasites than nests with natural forest (P = 0.002). The present study strengthens the existing knowledge about different environmental factors that influence Philornis parasitism birds of continental Ecuador.

Specificity within bird–parasite–parasitoid food webs: A novel approach for evaluating potential biological control agents of the avian vampire fly

Abstract Quantitative food web analyses can provide insights into the specificity of consumers such as herbivores, parasites and parasitoids. Understanding such patterns can be useful in forecasting the potential benefits and risks of biological control agents being considered for introduction against invasive species. The avian vampire fly, Philornis downsi (Diptera: Muscidae), is a neotropical bird parasite that is invasive in the Galapagos Islands, where it is causing substantial mortality of endemic bird species. We used a novel in‐field experimental food web approach within the native range of P. downsi in Ecuador to test the hypotheses that pupal parasitoids known to attack P. downsi specialize on members of the genus Philornis, which occur only in bird nests. We deployed pupae of non‐Philornis fly species adjacent to bird nests to assess specificity of the parasitoids and used two indices to assess specificity: Resource Range (RR), which evaluates the breadth of host use, and Pair Difference Index (PDI), which evaluates interaction strength. The results revealed very strong compartmentalization within the guild of pupal fly parasitoids, with four species attacking only Philornis spp. Both specificity indices indicated significant levels of specificity towards the genus Philornis for two of these species: Conura annulifera and Trichopria sp. novus. We also assessed the specificity of the two dominant Philornis species attacking 11 bird species and preference of the two dominant parasitoid species for bird species. Although there was some significant preference for particular bird species by the Philornis spp., there was no indication that this drove specificity patterns by the parasitoids. Policy implications. Our results confirm previous laboratory studies indicating specificity by C. annulifera and support the hypothesis that this species would produce few, if any, nontarget impacts if released into Galapagos to suppress populations of the P. downsi. These results can inform an environmental risk assessment framework to guide governmental agencies in deliberation on potential field releases of parasitoids in the Galapagos Islands.

Taxonomy and observations of three species of Brazilian Philornis Meinert (Diptera, Muscidae) and two new host species of cavity-nesting birds

The mostly neotropical genus Philornis Meinert is associated with a variety of birds, where larvae can be free-living coprophagous, free-living semi-hematophagous, or subcutaneous hematophagous. The genus is taxonomically complicated because characters of some species are variable while others are more constant. Although most described Philornis species are taxonomically well known, larval biology and ecological associations with birds are less so. Here, during a study of cavity-nesting birds, we removed and collected subcutaneous larvae from young birds and pupae from nesting material in the nest boxes, that were then reared in the lab, from which we describe the adult male, larva, and puparium of Philornis obscurinervis Couri, 1984 and the puparium of Philornis diminutus Couri, 1984, and some associations of P. diminutus, Philornis falsificus Dodge & Aitken, 1968, and P. obscurinervis.

Survey of Philornis (Diptera: Muscidae) larvae in adult birds from central Argentina.

The majority of known Philornis species (Diptera: Muscidae) cause subcutaneous myiasis in Neotropical altricial and semi-altricial nestlings. Generating information about these parasites is of relevance as they are a threat for the conservation of some wild bird species and also because they are an excellent model to study the ecology of host-parasite interactions. Although there are records of this parasitism in adult birds, the parasitic larvae are primarily associated with nestlings. However, systematic surveys including active search for larvae in older birds have been very scarce. Here we present results from a survey conducted along 6years and encompassing a sample of 3029 subadult and adult birds in Santa Fe province, Argentina, where broods are frequently parasitised by the Philornis torquans complex. We found only one dipteran larva parasitising a greater thornbird. This larva was morphologically compatible with Philornis. Given the extremely low estimated prevalence (1/3029 = 0.03%), we conclude that the presence of larvae in subadult and adult birds is an extremely rare event in the studied bird community and that the species belonging to the P. torquans complex present in central Argentina are almost exclusively parasites of nestlings.

Genetic diversity and geographic distribution of parasitic flies of the Philornis torquans complex in Argentina.

Philornis Meinert 1890 (Diptera: Muscidae) is a genus of flies that parasitize birds in the Neotropical region. The characteristics of the host-parasite interactions and its consequences may depend on the Philornis species involved, and thus precise identification of these parasites is crucial for the interpretation of ecological and epidemiological studies. However, morphological identification of Argentine Philornis species is elusive while molecular evidence points towards the existence of a complex of cryptic species or lineages undergoing a speciation process, which were named the 'Philornis torquans complex'. Herein the authors extended the current knowledge on the systematics and biogeography of parasitic Philornis flies from Argentina, analysing samples collected in several ecoregions, including the Atlantic Forest, Iberá Wetlands, Open Fields and Grasslands, Espinal, Pampa, Dry Chaco, Humid Chaco, Delta and Paraná River Islands, Monte of Plains and Plateaus. The results of the present study strengthen the evidence on previously described Philornis genotypes using four genetic markers (ITS2, COI, ND6, 12S rRNA). The authors report new patterns of occurrence and describe the presence of a novel genotype of subcutaneous Philornis. In addition, the present study unveils ecological niche differences among genotypes of the Philornis torquans complex in southern South America.

Trypanosomatids Detected in the Invasive Avian Parasite Philornis downsi (Diptera: Muscidae) in the Galapagos Islands.

Alien insect species may present a multifaceted threat to ecosystems into which they are introduced. In addition to the direct damage they may cause, they may also bring novel diseases and parasites and/or have the capacity to vector microorganisms that are already established in the ecosystem and are causing harm. Damage caused by ectoparasitic larvae of the invasive fly, Philornis downsi (Dodge and Aitken) to nestlings of endemic birds in the Galapagos Islands is well documented, but nothing is known about whether this fly is itself associated with parasites or pathogens. In this study, diagnostic molecular methods indicated the presence of insect trypanosomatids in P. downsi; to our knowledge, this is the first record of insect trypanosomatids associated with Philornis species. Phylogenetic estimates and evolutionary distances indicate these species are most closely related to the Crithidia and Blastocrithidia genera, which are not currently reported in the Galapagos Islands. The prevalence of trypanosomatids indicates either P. downsi arrived with its own parasites or that it is a highly suitable host for trypanosomatids already found in the Galapagos Islands, or both. We recommend further studies to determine the origin of the trypanosomatid infections to better evaluate threats to endemic fauna of the Galapagos Islands.

More than just nestlings: incidence of subcutaneous Philornis (Diptera: Muscidae) nest flies in adult birds

Philornis flies Meinert (Diptera: Muscidae) have been documented parasitizing over 250 bird species, some of which are endemic species threatened with extinction. Philornis parasitism is hypothesized to affect nestlings disproportionately more than adult birds because limited mobility and exposed skin of nestlings increase their vulnerability to parasitism. We used a comprehensive literature review and our recent fieldwork in the Dominican Republic, Puerto Rico, and Grenada to challenge the idea that parasitism by subcutaneous Philornis species is a phenomenon primarily found in nestlings, a fact that has not been quantified to date. Of the 265 reviewed publications, 125 (49%) reported incidences of parasitism by subcutaneous Philornis, but only 12 included the sampling of adult breeding birds. Nine of these publications (75%) reported Philornis parasitism in adults of ten bird species. During fieldwork in the Dominican Republic, Puerto Rico, and Grenada, we documented 14 instances of parasitism of adult birds of seven avian species. From literature review and fieldwork, adults of at least fifteen bird species across 12 families and four orders of birds were parasitized by at least five Philornis species. In both the published literature and fieldwork, incidences of parasitism of adult birds occurred predominantly in females and was frequently associated with incubation. Although our findings indicate that Philornis parasitism of adult birds is more common than widely presumed, parasite prevalence is still greater in nestlings. In the future, we recommend surveys of adult birds to better understand host-Philornis relationships across life stages. This information may be essential for the development of effective control measures of Philornis to ensure the long-term protection of bird species of conservation concern.

A new host for Philornis torquans (Diptera, Muscidae) from the Brazilian Cerrado

Philornis larvae and pupae were collected in nestlings of Neothraupis fasciata (Lichtenstein), the White-banded Tanager (Passeriformes, Thraupidae), in three breeding seasons, between October and November 2003‑2005 in a reserve in central Brazil. Here, we present biological data, diagnosis to the recognition of the species and a key to the segregation of species occurring in the Cerrado. The larvae were intradermic in the nestlings and the pupae were collected in the nests after the birds have abandoned them. The immatures collected were taken to the laboratory and reared under laboratory conditions, until emergence. The species identified as Philornis torquans (Nielsen), is here firstly recorded from the Brazilian Cerrado, and firstly recorded its association with N. fasciata. With this record, the number of Philornis species occurring in the Cerrado rises to three.

Aspects of the life cycle of the avian parasitePhilornis torquans(Diptera: Muscidae) under laboratory rearing conditions

AbstractThe life cycle of the avian parasitic fliesPhilornisMeinert (Diptera: Muscidae) is poorly known, limiting the understanding of the ecology of these flies, including interactions with their hosts. We provide data on length and survival of pupal and adult stages and the duration of the pre-oviposition period ofPhilornis torquansNielsen. Specimens were collected at larval and pupal stages from infested broods. The pupal stage lasted on average 10.5 days and adults lived up to 100 days in the laboratory. At least 90.2% of larvae pupated and 85.7% of the latter emerged as adults. For individuals collected as larvae, pupal mortality was 3.5 times higher than for those collected as pupae. Females laid from 1–8 clutches in their lifetime and deposited, on average, 41 eggs per female (range: 1–148). Females collected as pupae were larger and had shorter pre-oviposition periods and lifespans than females collected as larvae, but there were no differences in the total eggs laid by these females. This is the first information on reproductive parameters of a subcutaneous species ofPhilornis, and forms the basis for studies on conditions required for reproduction of this species in captivity.

Alien Invasion: Biology of Philornis Flies Highlighting Philornis downsi, an Introduced Parasite of Galápagos Birds.

The muscid genus Philornis comprises approximately 50 described species of flies, nearly all of which are obligate parasites of nestling birds. Philornis species are native to the Neotropics and widely distributed from Florida to Argentina. Most research on this group has focused on P. downsi, which was introduced to the Galápagos Islands in the late twentieth century. Although Philornis parasitism kills nestlings in several native host species, nowhere do the effects seem more severe than in P. downsi in the Galápagos. Here, we review studies of native and introduced Philornis in an attempt to identify factors that may influence virulence and consider implications for the conservation of hosts in the Galápagos.

Description of Brachymeria philornisae sp. n. (Hymenoptera: Chalcididae),a parasitoid of the bird parasite Philornis trinitensis (Diptera: Muscidae) in Tobago, with a review of the sibling species.

In this paper, we describe and illustrate a new species of parasitoid wasp as Brachymeria philornisae Delvare, sp. nov. The new species was reared from Philornis trinitensis Dodge & Aitken (Diptera: Muscidae) puparia that were found in the nests of the bird species Mimus gilvus (Vieillot) (Mimidae) and Tiaris bicolor (L.) (Thraupidae) in Tobago. The new species is of particular interest as it may be considered a potential biological control agent in locations where Philornis species are invasive, such as the Galapagos Islands. Closely related Brachymeria species had taxonomically ambiguous relationship in the past and are compared and reviewed. The species have been classified in the subgenus Pseudobrachymeria, but are here treated within the newly defined subconica species-group of Brachymeria as part of a sibling species complex designated as the subrugosa complex. Species assigned to the subconica species-group are listed and five, one unnamed, are assigned to the subrugosa complex and their females keyed. Species are separated by qualitative characters and morphometry using distance measurements. Trigonura annulipes Costa Lima is renamed as Brachymeria costalimai Delvare nom. nov. because of secondary homonymy.

Life Cycle and Host Specificity of the Parasitoid Conura annulifera (Hymenoptera: Chalcididae), a Potential Biological Control Agent of Philornis downsi (Diptera: Muscidae) in the Galápagos Islands

The neotropical parasitoid Conura annulifera (Walker) (Hymenoptera: Chalcididae) is known to parasitize bird-parasitic flies in the genus Philornis (Diptera: Muscidae) including P. downsi (Dodge and Aitken), a species that has invaded the Galapagos islands and is negatively impacting populations of Darwin's finches. We report here some aspects of the life history, field ecology, and host specificity of C. annulifera. We collected puparia of four Philornis species in 13 bird nests during 2015 and 2016 in western mainland Ecuador and found that C. annulifera and three other parasitoid species emerged from those puparia. This is the first record of C. annulifera in Ecuador. Rearing records and dissections of parasitized puparia revealed that C. annulifera is a solitary pupal ectoparasitoid, placing its eggs in the gap between host pupa and puparium. Laboratory studies of host specificity involving P. downsi and pupae from five other dipteran, three lepidopteran, and one hymenopteran species found that C. annulifera only produced progeny when presented with P. downsi pupae. Pupae of P. downsi that had been exposed to C. annulifera also failed to emerge more often than expected by chance compared with no-parasitoid controls, suggesting that the parasitoids can cause developmental mortality through means other than successful parasitism. These studies constitute the first steps in evaluating C. annulifera as a potential biological control agent of P. downsi in the Galapagos Islands.

Tri‐trophic ecology of native parasitic nest flies of birds in Tobago

AbstractIntroduced parasites threaten host populations around the world. For example, introduced parasitic nest flies (Philornis downsi) have contributed to the decline of several species of Darwin's finches in the Galápagos Islands. Introduced parasites are thought to have severe effects on native hosts because the hosts do not have effective defenses against such parasites and/or because introduced parasites have escaped the native enemies that keep their own populations in check. Studying effects of parasites on native hosts is an essential step in testing these causal hypotheses. We conducted a field experiment to assess the virulence of a native species of Philornis (Philornis trinitensis), which parasitizes birds on the island of Tobago. We manipulated flies in nests of black‐faced grassquits (Tiaris bicolor), a close relative of Darwin's finches, as well as tropical mockingbirds (Mimus gilvus), a congener of the Galápagos mockingbird (Mimus parvulus). We predicted that P. trinitensis would be relatively avirulent because its native hosts in Tobago have had time to evolve effective defenses against it. We also noted the presence of parasitoids and other enemies of Philornis in Tobago nests. Surprisingly, effects of native P. trinitensis on Tobago birds were similar to the effects of introduced P. downsi on birds in the Galápagos. Flies reduced the reproductive success of grassquits, but not mockingbirds, which are also relatively unaffected by Philornis in the Galapagos. Thus, native Philornis flies are not less virulent than introduced flies. The prevalence of Philornis in Tobago was lower than the prevalence of Philornis in the Galápagos. Presumed enemies of Philornis (parasitoid wasps and ants) were relatively common in nests of birds in Tobago, but largely absent from nests in the Galápagos. We suggest that introduced P. downsi in the Galápagos is widespread, not because hosts lack defenses, but because it has left its enemies behind.

Host range and community structure of avian nest parasites in the genus Philornis (Diptera: Muscidae) on the island of Trinidad.

Parasite host range can be influenced by physiological, behavioral, and ecological factors. Combining data sets on host–parasite associations with phylogenetic information of the hosts and the parasites involved can generate evolutionary hypotheses about the selective forces shaping host range. Here, we analyzed associations between the nest-parasitic flies in the genus Philornis and their host birds on Trinidad. Four of ten Philornis species were only reared from one species of bird. Of the parasite species with more than one host bird species, P. falsificus was the least specific and P. deceptivus the most specific attacking only Passeriformes. Philornis flies in Trinidad thus include both specialists and generalists, with varying degrees of specificity within the generalists. We used three quantities to more formally compare the host range of Philornis flies: the number of bird species attacked by each species of Philornis, a phylogenetically informed host specificity index (Poulin and Mouillot's STD), and a branch length-based STD. We then assessed the phylogenetic signal of these measures of host range for 29 bird species. None of these measures showed significant phylogenetic signal, suggesting that clades of Philornis did not differ significantly in their ability to exploit hosts. We also calculated two quantities of parasite species load for the birds – the parasite species richness, and a variant of the STD index based on nodes rather than on taxonomic levels – and assessed the signal of these measures on the bird phylogeny. We did not find significant phylogenetic signal for the parasite species load or the node-based STD index. Finally, we calculated the parasite associations for all bird pairs using the Jaccard index and regressed these similarity values against the number of nodes in the phylogeny separating bird pairs. This analysis showed that Philornis on Trinidad tend to feed on closely related bird species more often than expected by chance.

Insects found in birds' nests from Argentina. Pseudoseisura lophotes Reichenbach, 1853 and Anumbius annumbi (Vieillot, 1817) (Aves: Furnariidae), hosts of Triatoma platensis Neiva, 1913 (Hemiptera: Reduviidae: Triatominae).

The insect fauna of the nests of Pseudoseisura lophotes (Reichenbach, 1853) (Aves: Furnariidae) from Argentina was investigated. A total of 110 species (68 identified to species, 22 identified to genus, 20 identified to family) in 40 families of 10 orders of insects was found in these nests. Triatoma platensis Neiva, 1913 (Hemiptera: Reduviidae) was found again in nests of P. lophotes, corroborating after 73 years the first observations made by Mazza in 1936. The occurrence of the insects in nests of P. lophotes is compared with the previously known insect fauna in nests of A. annumbi, Furnarius rufus (Furnariidae), and Myiopsitta monachus (Psittacidae). The insect fauna in additional nests of Anumbius annumbi from the same and/or different localities is given, and used in comparisons. The first occurrence of Cuterebridae (Diptera) in birds' nests, their pupae as the overwintering stage, and the second simultaneous infestation by two species of Philornis (Diptera: Muscidae) on the same nestlings are presented. Other simultaneous infestations of different hematophagous arthropods (Hemiptera: Cimidae; Reduviidae: Triatominae, and Acari: Argasidae) are remarked and discussed.

Myiasis by Philornis spp. (Diptera: Muscidae) in Dendroica castanea (Aves: Parulidae) in Panama

We report the parasitism of an unidentified species of Philornis, extracted from juvenile Dendroica castanea that was collected from Pipeline Road of the Soberania National Park of Panama. This finding is unusual, because Philornis spp. Parasitizes nested chicks, not birds with flight capacity. In the other hand, it would be the first report of this kind of parasitism in D. castanea.

Myiasis by Philornis spp. (Diptera: Muscidae) in Dendroica castanea (Aves: Parulidae) in Panama

We report the parasitism of an unidentified species of Philornis , extracted from juvenile Dendroica castanea that was collected from Pipeline Road of the Soberania National Park of Panama. This finding is unusual, because Philornis spp. Parasitizes nested chicks, not birds with flight capacity. In the other hand, it would be the first report of this kind of parasitism in D. castanea .

First record of the avian ectoparasite Philornis downsi Dodge & Aitken, 1968 (Diptera: Muscidae) in Argentina

Species of Philornis Meinert, 1890 (Diptera, Muscidae) are Neotropical dipterans that include species with parasitic larvae which feed on nestling birds. To date, all Philornis species that have been recorded from Argentina have parasitic subcutaneous larvae. Here, for the first time for Argentina, we report the finding of Philornis downsi Dodge & Aitken, 1968, a fly with a nest-dwelling, semi-haematophagous larva. This record, from the humid Chaco ecoregion of Argentina in the nest of a saffron finch Sicalis flaveola pelzelni Sclater, substantially extends the known distribution of this species. We also report the consensus sequences of the internal transcribed spacer 1 (ITS1) and ITS2 regions of three of the specimens for future reference and comparison. Further investigation is needed to determine whether Argentina is part of the historical range of P. downsi or, alternatively, represents a recent expansion of its range, perhaps due to climatic changes or other factors of global environmental variation.

Phylogeny of Philornis Meinert species (Diptera: Muscidae)

This study presents a cladistic analysis of the Neotropical Philornis species based on morphological characters of adults and larvae, as well as biological data on larvae. Forty-one species of Philornis were used in the analysis, which was based on a total of 64 characters and included six outgroup taxa, half of which belong to Passeromyia Rodhain & Villeneuve, an Old World genus that shows the same variety of associations with birds as Philornis. Four most parsimonious cladograms (242 steps in length; ci=30; ri=69) were produced. According to the analysis, the genus Philornis is supported by the following synapomorphies (adults): only the pre-scutellar pair of acrostichal postsutural setae developed and setulae on anepimeron present. The resulting phylogenetic hypothesis (strict consensus) shows a basal polytomy that includes the species that traditionally correspond to the “aitkeni-group”. This group is mainly defined by male characters, which are known for only about half of these species. The next clade is divided into two others, the first one supported by the homoplasies: cheek hairs yellow; setulae on anepimeron black on upper half and yellow on lower half and proepimeral hairs yellow. This group traditionally corresponds to the “falsificus-group” and more data on the biology of the species will certainly clarify and/or confirm their relationships. Philornis downsi Dodge & Aitken is the sister group of all the remaining Philornis species. This third clade corresponds to the “angustifrons-group”, defined in this analysis by the following synapomorphies: concave shape of posterior end of puparium and the median width of female frons. These “traditional” groups, the relationships among the species and their evolutionary trends are discussed.

Parasitoidism of Chalcidid wasps (Hymenoptera, Chalcididae) on Philornis sp. (Diptera, Muscidae)

Philornis Meinert larvae are known as parasites of birds, with coprophagous, semi-hematophagous or hematophagous habits. Biological data of the larvae of the fifty described species are still scarcely known. Here we describe some aspects of the parasitism of a species of Philornis on Thalurania glaucopis Gmelin (Trochilidae) and record two species of Chalcididae (Hymenoptera) parasitoids, Conura annulifera (Walker, 1864) and Brachymeria podagrica (Fabricius, 1787), reared from Philornis puparia.