Sonia Kleindorfer

The life-cycle of Philornis downsi (Diptera : Muscidae) parasitizing Darwin's finches and its impacts on nestling survival

The fly, Philornis downsi Dodge & Aitken, was first collected in 1964 on the Galápagos Islands and is now widespread across the archipelago. Virtually nothing is known about the behaviour and ecology of the fly as well as for the genus in general. Here, we describe all larval instars for the first time, and discuss infection intensity and impacts of parasitism on nestling survival of Darwins finches. Adult P. downsi are non-parasitic free-living flies, whereas the larvae are obligate blood-feeding parasites on nestling birds. The larvae show a marked shift in their host site specificity--a novel finding for the genus Philornis: the first and early second larval instars live as agents of myiasis in finch nostrils and other tissues, while the older second and third instar larvae reside in the nest material and feed externally on the blood of nestlings, leading to blood losses in nestlings of 18-55%. Pupation occurs in the bottom layer of the nest. The combined effects of tissue damage by the endoparasitic instar larvae and anaemia by nest-dwelling haematophagous instar larvae account for the high nestling mortality (76%) due to Philornis parasitism. This represents the highest mortality by Philornis reported in the literature and emphasizes the extremely serious threat this parasite poses for the endemic passerine fauna of the Galápagos Islands.

Effects of the parasitic flies of the genus Philornis (Diptera:Muscidae) on birds

Abstract Little is known about the genus Philornis (comprising ~50 species), a group of muscid flies that parasitise birds and may be highly detrimental to host nestlings. Philornis species affect at least 115 species of bird, particularly in the Neotropics. The main distribution of Philornis is in Central and South America, extending to the southern United States. Larvae of the genus Philornis reside in bird nests and may feed on either nestling faeces (coprophagous scavengers), the blood of nestlings (semi-haematophagous parasites), or on nestling tissue and fluid (subcutaneous parasites). Depending on the species of Philornis, larval development can occur in bird faeces, in nesting material or inside nestlings. Nestling mortality depends on the species of Philornis, the intensity of infestation and nestling susceptibility, which in turn depends on the nestling species, age, brood size, body condition and the anatomical site of infestation. Consequently, variable effects of Philornis parasitism are observed in relation to nestling growth, development and fledging success. The impetus for this review is the recent discovery of Philornis downsi on the Galapagos Archipelago, combined with high Philornis-induced mortality in Darwins finches. The potential for ectoparasites such as Philornis to compromise the viability of small, isolated bird populations is highlighted by this recently documented parasite invasion.

Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper)

Darwin’s medium tree finch (Camarhynchus pauper) meets the 2009 International Union for Conservation of Nature Red List criteria for a critically endangered species because it has “a very small range on a single island” and is “declining rapidly owing to the effects of the parasite Philornis downsi”, habitat degradation, and introduced predators. The medium tree finch is only found in patches of remnant highland forest on Floreana Island, where it co-exists with breeding populations of small and large tree finches (C. parvulus and C. psittacula). Here, we examine the intensity of P. downsi in nests of small, medium, and large tree finches on Floreana. We expected that parasite intensity would increase with finch body size, and with greater rainfall, and would also correlate with increased nestling mortality. We found a trend in the expected direction for parasite intensity and rainfall. Combined meta-analytically with data from a previous study, the overall trend for the two studies was significant. We also found a significant linear trend in parasite intensity with finch body size. In addition, the medium tree finch exhibited a somewhat higher parasite intensity than would be expected based on body mass alone. Of 63 active medium tree finch nests, 17 nests had nestlings: all of which were infested with P. downsi. Only 25% of medium tree finch nestlings fledged, 28% were depredated, 41% died due to P. downsi parasitism, and 6% died for other reasons.

Species collapse via hybridization in Darwin's tree finches.

Species hybridization can lead to fitness costs, species collapse, and novel evolutionary trajectories in changing environments. Hybridization is predicted to be more common when environmental conditions change rapidly. Here, we test patterns of hybridization in three sympatric tree finch species (small tree finch Camarhynchus parvulus, medium tree finch Camarhynchus pauper, and large tree finch: Camarhynchus psittacula) that are currently recognized on Floreana Island, Galápagos Archipelago. Genetic analysis of microsatellite data from contemporary samples showed two genetic populations and one hybrid cluster in both 2005 and 2010; hybrid individuals were derived from genetic population 1 (small morph) and genetic population 2 (large morph). Females of the large and rare species were more likely to pair with males of the small common species. Finch populations differed in morphology in 1852–1906 compared with 2005/2010. An unsupervised clustering method showed (a) support for three morphological clusters in the historical tree finch sample (1852–1906), which is consistent with current species recognition; (b) support for two or three morphological clusters in 2005 with some (19%) hybridization; and (c) support for just two morphological clusters in 2010 with frequent (41%) hybridization. We discuss these findings in relation to species demarcations of Camarhynchus tree finches on Floreana Island.

Alarm calls and chick reactions in the moustached warbler,Acrocephalus melanopogon

As in many altricial species, adult moustached warblers alarm call more at the nest as the breeding season progresses. This study used the experimental human approach method as well as two predator types (plastic snake and taxidermic raptor) placed at the nest to test the anti-predator responses of chicks to parental alarm calls. The probability of chicks making anti-predator responses (ducking and jumping) was strongly correlated with the probability of adults giving alarm calls. Furthermore, chicks reacted selectively to different predator types, tending to remain in the nest in response to aerial predators and to jump from the nest in response to ground predators. A conceptual framework is presented identifying the age of chicks when alarm calls are first given for the brood value, vulnerability and chick reaction hypotheses. These were tested by comparing the intercept of the regression line for alarm calls with those predicted by each hypothesis. The results suggest that the anti-predator response of chicks is the proximate cue for adult alarm calls.

Video analysis of host-parasite interactions in nests of Darwin's finches.

Parasites place their hosts under strong selection for adaptive traits that increase parasite resistance. The initial impact of invasive parasites has rarely been observed and can be particularly strong on naive hosts with limited prior exposure to parasites. Philornis downsi is an introduced fly to the Galapagos Islands whose parasitic larvae cause high mortality in nestlings of Darwins finches. We used a within-nest camera system and nest monitoring data to examine this new host–parasite interaction in the wild. Many P. downsi flies entered finch nests with incubated eggs or nestlings but only when parent finches were not present. Parasitic P. downsi larvae were observed to emerge from the nest base at night to feed both internally and externally on nestlings. Adult and nestling Darwin’s finches exhibit grooming and avoidance behaviours in the presence of P. downsi parasites. Specifically, in nests with high parasite intensity, nestlings increased self-preening behaviour, ate larvae and stood on top of one another. Female finches probed into their nestling’s nares (first instar larvae reside in the nares) and probed into the nest base (second and third larvae reside in the nest base during the day). These findings shed light on the emergence of anti-parasite behaviour as well as host–parasite relationships after recent parasitism in a naive host.

Love thy neighbour? Social nesting pattern, host mass and nest size affect ectoparasite intensity in Darwin’s tree finches

Social nesting behaviour is commonly associated with high prevalence and intensity of parasites in intraspecific comparisons. Little is known about the effects of interspecific host breeding density for parasite intensity in generalist host–parasite systems. Darwin’s small tree finch (Camarhynchus parvulus) on Santa Cruz Island, Galápagos Islands, nests in both heterospecific aggregations and at solitary sites. All Darwin finch species on Santa Cruz Island are infested with larvae of the invasive blood-sucking fly Philornis downsi. In this study, we test the prediction that total P. downsi intensity (the number of parasites per nest) is higher for nests in heterospecific aggregations than at solitary nests. We also examine variation in P. downsi intensity in relation to three predictor variables: (1) nest size, (2) nest bottom thickness and (3) host adult body mass, both within and across finch species. The results show that (1) total P. downsi intensity was significantly higher for small tree finch nests with many close neighbours; (2) finches with increased adult body mass built larger nests (inter- and intraspecific comparison); (3) parasite intensity increased significantly with nest size across species and in the small tree finch alone; and (4) nest bottom thickness did not vary with nest size or parasite intensity. These results provide evidence for an interaction between social nesting behaviour, nest characteristics and host mass that influences the distribution and potential impact of mobile ectoparasites in birds.

More is not always better: male incubation in two Acrocephalus warblers

This study investigates male and female incubation ability in two monogamous Acrocephalus warblers with overlapping, equally sized territories and similar prey abundance. Given the longer breeding time window of the moustached warbler (A. melanopogon) compared with the reed warbler (A. scirpaceus), the trade-off between the need for biparental care and the cost of inefficient incubation is discussed. Hourly protocols and egg temperature measurements were analyzed with regard to four primary questions: male and female incubation ability, the role of environmental parameters, hatching success and the influence of male incubation on female time allocation. In both species, males increase egg temperature per minute at a slower rate than do females. There is no species difference in the percentage of incubation per hour for males (20%) or females (50%). Ambient temperature influences male incubation only in the moustached warbler during the early season (April) when male incubation correlates with hatching success. The male reed warbler shows daily temporal selectivity throughout the breeding season, increased incubation during rainfall, and no correlation with hatching success. In both species, females receive direct benefits of increased foraging time through male incubation. However, only the female reed warbler adjusts her incubation duration to previous male incubation. Thus, female reed warblers maximise the male component and thereby reduce the total incubation phase with high male effort whereas the incubation phase is increased with above average male effort in the moustached warbler.

Distribution and abundance of Darwin's finches and other land birds on Santa Cruz Island, Galápagos: evidence for declining populations.

Population monitoring is a vital tool for conservation management and for testing hypotheses about population trends in changing environments. Darwin’s finches on Santa Cruz Island in the Galapagos archipelago have experienced habitat alteration because of human activity, introduced predators, parasites and disease. We used point counts to conduct systematic quantitative surveys of Darwin’s finches and other land birds between 1997 and 2010. The temporal analysis revealed that six of the nine species investigated declined significantly and that this decline was most pronounced at higher elevations in humid native forest and agricultural areas; the highland areas have been most affected by introduced species or direct human impact. Five of the six declining species are insectivorous, which suggests that changes in insect abundance or insect availability are a critical factor in the declines. Further study is required to test this idea. Other factors including habitat alteration and introduced parasites or pathogens may be contributing to the observed declines.

Genetic variation in the invasive avian parasite, Philornis downsi (Diptera, Muscidae) on the Galápagos archipelago

BackgroundUnderstanding the dispersal and genetic structure of invasive insects across islands is important for designing management plans that are appropriate at spatial and temporal scales. For invasive parasites, population dynamics are largely determined by the distribution and density of their host species. The introduced parasitic fly, Philornis downsi, parasitises nestlings of endemic birds on all major islands of the Galápagos archipelago. The flys high mortality and fitness impacts are of conservation concern for vulnerable and declining species of Darwins finches. Using microsatellite data in Bayesian clustering and landscape genetic analyses, we examine gene flow and dispersal in P. downsi between three islands and across habitats (highlands, lowlands) and examine for the presence of population bottlenecks. We also examine variation at the mitochondrial gene CO1 across islands to establish if cryptic species were present.ResultsBoth the mitochondrial and microsatellite data were consistent with there being a single species across islands. We found low genetic differentiation between islands and strong evidence for inter-island gene flow, or shared recent ancestry among individuals. Landscape genetic analysis identified two genetic clusters: one encompassing Santa Cruz and Isabela, and one on Floreana Island. There was no evidence of genetic differentiation between habitats and molecular variance was mainly attributable to within individuals. The combined P. downsi population was found to have undergone a population bottleneck.ConclusionPhilornis downsi populations have high connectivity within and between islands, with low levels of genetic differentiation between Floreana and the other two islands examined. The genetic bottleneck found across islands suggests there was a small founding population or few introduction events of P. downsi. The high dispersal capacity and wide habitat use of P. downsi highlights the significant threat that this parasite poses to the Galápagos avifauna. Our findings are relevant for assessing the viability of methods to control P. downsi on Galápagos, such as the sterile insect technique.