Native parasitic nest fly impacts reproductive success of an island‐endemic host (original) (raw)

Persistence of the invasive bird-parasitic fly Philornis downsi over the host interbreeding period in the Galapagos Islands

Scientific Reports

Many parasites of seasonally available hosts must persist through times of the year when hosts are unavailable. In tropical environments, host availability is often linked to rainfall, and adaptations of parasites to dry periods remain understudied. The bird-parasitic fly Philornis downsi has invaded the Galapagos Islands and is causing high mortality of Darwin’s finches and other bird species, and the mechanisms by which it was able to invade the islands are of great interest to conservationists. In the dry lowlands, this fly persists over a seven-month cool season when availability of hosts is very limited. We tested the hypothesis that adult flies could survive from one bird-breeding season until the next by using a pterin-based age-grading method to estimate the age of P. downsi captured during and between bird-breeding seasons. This study showed that significantly older flies were present towards the end of the cool season, with ~ 5% of captured females exhibiting estimated age...

Evidence for tolerance of parasitism in a tropical cavity-nesting bird, planalto woodcreeper (< i> Dendrocolaptes platyrostris), in northern Argentina

Journal of Tropical …, 2010

Avian hosts may either resist the negative effects of nestling ectoparasites by minimizing the number of parasites, or tolerate parasitism by increasing their fecundity via the reproductive compensation hypothesis. Little is known about the interactions between ectoparasites and their avian hosts in the tropics. We (1) examined nestling development rates, and tested whether (2) parasitism by a subcutaneous ectoparasitic botfly (Philornis sp.) had negative effects on the condition of nestlings, and (3) these negative effects were minimized in larger broods in a tropical cavitynesting bird, the planalto woodcreeper (Dendrocolaptes platyrostris), in primary and secondary Atlantic forests in the northern province of Misiones, Argentina. Nestling mass and ectoparasite load per nestling reached maxima when nestlings (n = 50) were between 10 and 14 d old. General linear mixed models predicted that mass at fledging declined with increasing nestling parasite load, suggesting that botflies had a negative influence on fledging condition. Parasite load per nestling declined with increasing brood size indicating that woodcreepers that increase their reproductive output minimize the negative effects of parasitism. Overall we found evidence to support the tolerance via reproductive compensation hypothesis. Future tests of the reproductive compensation hypothesis may help determine the underlying mechanism of the observed negative correlation between parasite load of nestlings and brood size.

Invasion of an Avian Nest Parasite, Philornis downsi, to the Galapagos Islands: Colonization History, Adaptations to Novel Ecosystems, and Conservation Challenges

Social and ecological interactions in the Galapagos Islands, 2017

This chapter discusses the invasion of an avian nest fly, Philornis downsi, to the Galapagos Islands, its interactions with novel bird hosts, and the strategies that are being implemented to protect threatened, endemic bird species. Philornis downsi was first recorded in the Galapagos less than 60 years ago and is the first bird parasite with parasitic larval stages and non-parasitic adults to reach the islands. Since its introduction, it has successfully spread to most islands and habitats in the archipelago and is associated with a wide range of bird hosts. The consequences of its feeding habits on naive birds have been deleterious to a large number of species, many of which are in decline. An international research group, coordinated by the Charles Darwin Foundation and Galapagos National Park Directorate, is studying various aspects of the biology of P. downsi and its impacts on selected bird species with the aim of fully understanding the complex interactions between flies and birds. The ultimate aim of these investigations is the development of effective management tools.

Evidence for tolerance of parasitism in a tropical cavity-nesting bird, planalto woodcreeper ( Dendrocolaptes platyrostris), in northern Argentina

Journal of Tropical Ecology, 2010

Avian hosts may either resist the negative effects of nestling ectoparasites by minimizing the number of parasites, or tolerate parasitism by increasing their fecundity via the reproductive compensation hypothesis. Little is known about the interactions between ectoparasites and their avian hosts in the tropics. We (1) examined nestling development rates, and tested whether (2) parasitism by a subcutaneous ectoparasitic botfly (Philornis sp.) had negative effects on the condition of nestlings, and (3) these negative effects were minimized in larger broods in a tropical cavitynesting bird, the planalto woodcreeper (Dendrocolaptes platyrostris), in primary and secondary Atlantic forests in the northern province of Misiones, Argentina. Nestling mass and ectoparasite load per nestling reached maxima when nestlings (n = 50) were between 10 and 14 d old. General linear mixed models predicted that mass at fledging declined with increasing nestling parasite load, suggesting that botflies had a negative influence on fledging condition. Parasite load per nestling declined with increasing brood size indicating that woodcreepers that increase their reproductive output minimize the negative effects of parasitism. Overall we found evidence to support the tolerance via reproductive compensation hypothesis. Future tests of the reproductive compensation hypothesis may help determine the underlying mechanism of the observed negative correlation between parasite load of nestlings and brood size.

Parental food provisioning and nestling growth under Philornis downsi parasitism in the Galapagos Green Warbler-Finch, classified as ‘vulnerable’ by the IUCN

Journal of ornithology, 2023

In the Galapagos Islands, many endemic landbird populations are declining due to habitat degradation, food availability, introduced species and other factors. Given nestlings typically lack efficient defense mechanisms against parasites, hematophagous ectoparasites such as the larvae of the introduced Avian Vampire Fly, Philornis downsi, can impose high brood mortality and cause threatening population declines in Darwin finches and other landbirds. Here, we assess whether the food compensation hypothesis (i.e., the parents' potential to compensate for deleterious parasite effects via increased food provisioning) applies to the Green Warbler-Finch. We differentiated nests with low or high infestation levels by P. downsi and quantified food provisioning rates of male and female parents, time females spent brooding nestlings, and nestling growth. Male provisioning rates, total provisioning rates and female brooding time did not significantly vary in relation to infestation levels, nor by the number of nestlings. Opposed to the predictions of the food compensation hypothesis, females showed significantly reduced provisioning rates at high infestation levels. Nestling body mass was significantly lower and there was a reduction of skeletal growth, although not significantly, in highly infested nests. The females' response to high infestation may be due to parasites directly attacking and weakening brooding females, or else that females actively reduce current reproductive effort in favor of future reproduction. This life-history trade-off may be typical for Darwin finches and many tropical birds with long lifespans and therefore high residual reproductive value. Conservation strategies may not build on the potential for parental food compensation by this species. Keywords Nest parasite • Parental care • Nestling growth • Host defense • Galapagos Islands • Philornis downsi Zusammenfassung Elterliche Nahrungsversorgung und Nestlingswachstum beim durch die IUCN als "gefährdet " eingestuften Waldsänger-Darwinfink bei Befall durch die parasitische invasive Vampirfliege Philornis downsi Auf den Galapagos-Inseln sind auf Grund von Habitatstörungen, eingeschleppten und invasiven Organismen und anderen Faktoren viele Vogelarten und Populationen in ihrer Existenz bedroht. Beispielsweise führen die hämatophagen Larven der eingeführten Vampirfliege Philornis downsi zu einer hohen Brutsterblichkeit unter den endemischen Darwinfinken, insbesondere da bei Nestlingen die Immunabwehr noch schwach und unvollständig ausgeprägt ist. Hier wird untersucht, ob brütende Waldsänger-Darwinfinken Certhidea olivacea in der Lage sind, die für das Nestlingswachstum schädlichen Communicated by F. Bairlein. Heinz Richner and Sabine Tebbich: Shared last authorship.

Population dynamics of an invasive bird parasite, Philornis downsi (Diptera: Muscidae), in the Galapagos Islands

PLOS ONE

The invasive parasitic fly, Philornis downsi (Muscidae), is one of the greatest threats to the avifauna of the Galapagos Islands. The larvae of this fly feed on the blood and tissues of developing nestlings of at least 18 endemic and native birds. The aim of the current study was to investigate biotic and abiotic factors that may influence the population dynamics of this invasive parasite. To study the influence of vegetation zone and related climatic factors on fly numbers, a biweekly monitoring program using papaya-baited traps was carried out at a dry, lowland site and at a humid, highland site on Santa Cruz Island between 2012-2014. Female flies, a large proportion of which were inseminated and gravid, were collected throughout the year at both sites, indicating females were active during and between the bird breeding seasons. This is the first evidence that female flies are able to persist even when hosts are scarce. On the other hand, catch rates of male flies declined between bird breeding seasons. Overall, catch rates of P. downsi were higher in the drier, lowland habitat, which may be a consequence of host or resource availability. Time was a stronger predictor of adult fly numbers than climate, further suggesting that P. downsi does not appear to be limited by its environment, but rather by host availability. Seasonal catch rates suggested that populations in both habitats were continuous and multivoltine. Numbers of adult female flies appeared to be regulated chiefly by simple direct density dependence, and may be governed by availability of bird nests with nestlings. Nevertheless, confounding factors such as the existence of reservoir hosts that perpetuate fly populations and changes in behavior of P. downsi may increase the vulnerability of bird hosts that are already IUCN red-listed or in decline.

Offspring genetic structure reveals mating and nest infestation behaviour of an invasive parasitic fly ( Philornis downsi ) of Galápagos birds

Biological Invasions, 2010

The natural reproductive behaviour of invasive insects is pivotal knowledge for managing species of ecological or economic concern. We use microsatellites to examine female multiple mating and multiple nest infestations in the introduced parasitic fly, Philornis downsi, which causes high mortality in endemic birds on the Galápagos Islands. We analyse larvae and pupae within 57 nests from Santa Cruz and Floreana Islands in both the highland and lowland habitats. Sib-ship reconstructions of offspring revealed that up to five females may infest a single nest, while multiple mating in females was frequent (65% of reconstructed maternal genotypes), with an average of 1.91 (±0.06 SE) males per female. Genetic relatedness (R) of offspring within nests was generally low, though lowland nests on Floreana had higher R than highland nests. Knowledge of the reproductive behaviour of P. downsi is necessary for modelling appropriate management strategies, in particular, the sterile insect technique, for which success is greatly influenced by female multiple mating.

Behavior of the Avian Parasite Philornis downsi (Diptera: Muscidae) in and Near Host Nests in the Galapagos Islands

Journal of Insect Behavior

The Avian Vampire Fly, Philornis downsi, has invaded the Galapagos Islands, where it causes high mortality of endemic and native landbird species, including most species of Darwin’s finches. Control methods are under development, but key information is missing about the reproductive biology of P. downsi and the behavior of flies in and near nests of their hosts. We used external and internal nest cameras to record the behavior of P. downsi adults within and outside nests of the Galapagos Flycatcher, Myiarchus magnirostris, throughout all stages of the nesting cycle. These recordings showed that P. downsi visited flycatcher nests throughout the day with higher fly activity during the nestling phase during vespertine hours. The observations also revealed that multiple P. downsi individuals can visit nests concurrently, and that there are some interactions among these flies within the nest. Fly visitation to nests occurred significantly more often while parent birds were away from the ...

The invasive parasitic fly Philornis downsi is threatening Little Vermilion Flycatchers on the Galápagos Islands

Avian Conservation and Ecology, 2022

Populations of several species of birds endemic to the Galápagos Islands have declined during recent decades, including endemic Little Vermilion Flycatchers (Pyrocephalus nanus). Understanding the reasons for the low breeding success of this species is a prerequisite for developing efficient conservation strategies. Studies of sympatric Darwin's finches suggest two potential reasons: parasitism by the invasive parasitic fly Philornis downsi and extreme climatic events. We investigated the role of each in the breeding success of Little Vermilion Flycatchers during three breeding seasons in the agricultural zone of Isabela Island. We found that Little Vermilion Flycatchers were severely affected by P. downsi, depending on the time of breeding. Nest success was high early in the breeding season (60% were successful) when rates of P. downsi prevalence and intensity were low, but nest success was zero and all nests were infested later in the breeding season. Philornis downsi prevalence and intensity increased with increasing temperature. Both low and high levels of rainfall had a negative effect on nest survival. A parasite removal experiment using insecticide confirmed the detrimental effect of the invasive parasite; nests infested with P. downsi had significantly lower nest success than treated nests. Injection of insecticide into nest bases can be an efficient short-term way to increase the nesting success of Little Vermilion Flycatchers, but finding long-term measures to control the P. downsi population is of utmost importance. La mouche vampire aviaire Philornis downsi menace la moucherolle des Galápagos RÉSUMÉ. Les populations de plusieurs espèces d'oiseaux endémiques des îles Galápagos ont décliné depuis quelques décennies, y compris celle des moucherolles des Galápagos (Pyrocephalus nanus). Il est essentiel de comprendre les raisons du faible taux de reproduction de cette espèce pour développer des stratégies de conservation efficaces. Des études menées sur les pinsons de Darwin sympatriques suggèrent deux raisons possibles : le parasitisme lié à la mouche vampire aviaire Philornis downsi et les événements climatiques extrêmes. Nous avons enquêté sur le rôle de chaque succès de reproduction des moucherolles des Galápagos au cours de trois saisons de reproduction dans la zone agricole de l'île d'Isabela. Nous avons constaté que les moucherolles des Galápagos étaient très affectées par la P. downsi, selon le moment de la période de reproduction. Le succès des nids était élevé au début de la saison de reproduction (60 % d'entre eux réussissaient) lorsque la prévalence et l'intensité des taux de P. downsi étaient faibles, alors que le succès des nids était nul et que tous les nids étaient infestés plus tard au cours de la saison de reproduction. La prévalence et l'intensité des populations de Philornis downsi augmentait avec la hausse des températures. Les niveaux de pluviosité faibles ou élevés entraînaient des effets négatifs sur la survie des nids. Une expérience d'élimination des parasites à l'aide d'insecticide a confirmé les effets délétères des parasites invasifs ; les nids infestés de P. downsi présentaient un taux de succès des nids nettement inférieur par rapport aux nids traités. L'injection d'insecticide dans les bases des nids peut constituer un moyen efficace à court terme pour augmenter le succès de la nidification des moucherolles des Galápagos, mais il est indispensable de trouver des mesures à long terme pour contrôler la population de P. downsi.

Dry year does not reduce invasive parasitic fly prevalence or abundance in Darwin's finch nests

Reports in Parasitology, 2013

The recent introduction of the parasitic nest fly Philornis downsi (Diptera: Muscidae) to the Galápagos Islands poses a serious threat to the bird species it infests, including Darwin's finches. Variation in climatic conditions, such as rainfall or drought, may influence fly populations and their effect on birds. We monitored the abundance of P. downsi in an extremely dry year in nests of the medium ground finch (Geospiza fortis). We fumigated nests to compare the reproductive success of birds in nests with and without flies. Neither the prevalence nor the abundance of P. downsi decreased significantly in the dry year compared with an earlier wet year for which we have already published data. Very few birds bred successfully under the dry conditions, independent of parasite prevalence and abundance. The low reproductive success of the finches presumably reflected limited food resources rather than parasites. Our sample sizes were low because few birds attempted to breed in the dry year. Nevertheless, our data indicate that P. downsi is capable of withstanding the extreme climatic fluctuations characteristic of the Galápagos Islands, which may contribute to the invasiveness of this parasite.