Co-parasitism in the face of predation: Effects of natural enemies on a neotropical mockingbird.

Co-parasitism is ubiquitous and has important consequences for the ecology and evolution of wild host populations. Studies of parasite co-infections remain limited in scope, with few experimental tests of the fitness consequences of multiple parasites, especially in natural populations. We measured the separate and combined effects of Philornis seguyi nest flies and shiny cowbirds Molothrus bonariensis on the fitness of a shared host, the chalk-browed mockingbird (Mimus saturninus) in Argentina. Using a two-factor experimental approach, we manipulated the presence of nest flies and cowbirds in mockingbird nests and assessed their effects on mockingbird haemoglobin levels, begging and provisioning rates, body size, and fledging success. We also monitored rates of nest predation in relation to parasitism by flies and cowbirds. Nest flies reduced the haemoglobin concentration, body size, and fledging success of mockingbirds, likely because mockingbirds did not compensate for parasitism by begging more or feeding their nestlings more. Cowbirds also reduced the fledging success of mockingbirds, even though they had no detectable effect on haemoglobin or body size. Nests with cowbirds, which beg more than mockingbirds, attracted more nest predators. There was no significant interaction between the effects of flies and cowbirds on any component of mockingbird fitness. The combined effects of nest flies and cowbirds were strictly additive. In summary, we show that nest flies and cowbirds both reduce host fitness, but do not have interactive effects in co-parasitized nests. Our results further suggest that predators exacerbate the effects of nest flies and cowbirds on their hosts. Our study shows that the fitness consequences of co-parasitism are complex, especially in the context of community-level interactions.

El co-parasitismo es ubicuo y tiene consecuencias importantes para la ecología y la evolución de las poblaciones de hospedadores silvestres. Los estudios de coinfecciones por parásitos poseen un alcance limitado, con pocos trabajos experimentales que analicen las consecuencias del parasitismo múltiple sobre la eficacia biológica, especialmente en poblaciones naturales. Medimos los efectos separados y combinados de las moscas de los nidos Philornis seguyi y el tordo renegrido (Molothrus bonariensis) sobre la eficacia biológica de un hospedador compartido, la calandria grande (Mimus saturninus) en Argentina. Utilizando un enfoque experimental de dos factores, manipulamos la presencia de moscas de nido y tordos en los nidos de calandrias y evaluamos sus efectos sobre los niveles de hemoglobina, las tasas de solicitud de alimento y aprovisionamiento, el tamaño corporal y el éxito de supervivencia de los pichones de calandria. También monitoreamos las tasas de depredación de nidos en relación con el parasitismo de moscas y tordos. Las moscas de los nidos redujeron la concentración de hemoglobina, el tamaño corporal y el éxito de supervivencia de los pichones de calandrias, probablemente porque las calandrias no compensaron el parasitismo solicitando más alimento o alimentando más a sus pichones. Los tordos también redujeron el éxito de supervivencia de las calandrias, aunque no tuvieron un efecto detectable sobre la hemoglobina o el tamaño corporal. Los nidos con tordos, quienes solicitaron más alimento más que las calandrias, atrajeron a más depredadores de nidos. El aumento de la depredación de nidos asociado a la alta intensidad de solicitud de alimento puede explicar por qué las calandrias en Argentina no solicitan más alimento en respuesta al parasitismo de las moscas. No hubo una interacción significativa entre los efectos de las moscas y los tordos en ningún componente de la eficacia biológica de las calandrias. Los efectos combinados de las moscas de los nidos y los tordos fueron estrictamente aditivos. En resumen, mostramos que las moscas de los nidos y los tordos reducen la eficacia biológica del hospedador, pero no tienen efectos interactivos en los nidos co-parasitados. Nuestros resultados sugieren además que los depredadores exacerban los efectos de las moscas de los nidos y los tordos sobre sus hospedadores. Nuestro estudio muestra que las consecuencias del co-parasitismo sobre la eficacia biológica son complejas, especialmente en el contexto de las interacciones a nivel comunitario.

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

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.

Temporal and spatial variation in sex-specific abundance of the avian vampire fly (Philornis downsi).

Understanding the range and behaviour of an invasive species is critical to identify key habitat areas to focus control efforts. Patterns of range use in parasites can differ temporally, across life stages and between sexes. The invasive avian vampire fly, Philornis downsi, spends the larval stage of its life within bird nests, feeding on developing nestlings and causing high levels of mortality and deformation. However, little is known of the ecology and behaviour of the non-parasitic adult fly life stage. Here, we document sex-specific temporal and spatial patterns of abundance of adult avian vampire flies during a single Darwin's finch breeding season. We analyse fly trapping data collected across 7 weeks in the highlands (N = 405 flies) and lowlands (N = 12 flies) of Floreana Island (Galápagos). Lowland catches occurred later in the season, which supports the hypothesis that flies may migrate from the food-rich highlands to the food-poor lowlands once host breeding has commenced. Fly abundance was not correlated with host nesting density (oviposition site) but was correlated with distance to the agricultural zone (feeding site). We consistently caught more males closer to the agricultural zone and more females further away from the agricultural zone. These sex differences suggest that males may be defending or lekking at feeding sites in the agricultural zone for mating. This temporal and sex-specific habitat use of the avian vampire fly is relevant for developing targeted control methods and provides insight into the behavioural ecology of this introduced parasite on the Galápagos Archipelago.

Female in-nest attendance predicts the number of ectoparasites in Darwin's finch species.

Selection should act on parental care and favour parental investment decisions that optimize the number of offspring produced. Such predictions have been robustly tested in predation risk contexts, but less is known about alternative functions of parental care under conditions of parasitism. The avian vampire fly (Philornis downsi) is a myasis-causing ectoparasite accidentally introduced to the Galápagos Islands, and one of the major mortality causes in Darwin's finch nests. With an 11-year dataset spanning 21 years, we examine the relationship between parental care behaviours and number of fly larvae and pupae in Darwin's finch nests. We do so across three host species (Camarhynchus parvulus, C. pauper, Geospiza fuliginosa) and one hybrid Camarhynchus group. Nests with longer female brooding duration (minutes per hour spent sitting on hatchlings to provide warmth) had fewer parasites, and this effect depended on male food delivery to chicks. Neither male age nor number of nest provisioning visits were directly associated with number of parasites. While the causal mechanisms remain unknown, we provide the first empirical study showing that female brooding duration is negatively related to the number of ectoparasites in nests. We predict selection for coordinated host male and female behaviour to reduce gaps in nest attendance, especially under conditions of novel and introduced ectoparasites.

Is the grass always greener on the other side? Weak relationships between vegetation cover and parasitic fly infestations.

Understanding parasite-host ecology is increasingly important for conservation efforts in a changing world. Parasitic nest flies in the genus Philornis (Diptera: Muscidae) have been implicated in the decline of endemic island species and are also known to negatively impact breeding success of the critically endangered Ridgway's hawk (B. ridgwayi) on the island of Hispaniola. Despite the importance of these effects on hosts, and extensive research of Philornis downsi in the Galápagos, the ecology of most species of philornid nest flies is poorly understood. We examined biotic factors related to Philornis pici infestations of nestling Ridgway's hawks in the Dominican Republic, where both fly and hawk are native. We found grass-cover was negatively associated with P. pici infestations, while coverage and height of other vegetation classes (tree, shrub, herbaceous, and bare ground) had no association, which is interesting considering recent landscape-level changes to Ridgway's hawk habitat. Anthropogenic activities in Los Haitises National Park, the last strong-hold of Ridgway's hawk, have shifted the landscape from primary forest to a fragmented secondary forest with smallholder or subsistence farms and grassy patches. New information on the ecology of nest flies in their native habitat can inform conservation efforts and allow us to make recommendations for future research.

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.

Epigenetic effects of parasites and pesticides on captive and wild nestling birds.

Anthropogenic changes to the environment challenge animal populations to adapt to new conditions and unique threats. While the study of adaptation has focused on genetic variation, epigenetic mechanisms may also be important. DNA methylation is sensitive to environmental stressors, such as parasites and pesticides, which may affect gene expression and phenotype. We studied the effects of an invasive ectoparasite, Philornis downsi, on DNA methylation of Galápagos mockingbirds (Mimus parvulus). We used the insecticide permethrin to manipulate P. downsi presence in nests of free-living mockingbirds and tested for effects of parasitism on nestling mockingbirds using epiGBS, a reduced-representation bisulfite sequencing (RRBS) approach. To distinguish the confounding effects of insecticide exposure, we conducted a matching experiment exposing captive nestling zebra finches (Taeniopygia guttata) to permethrin. We used zebra finches because they were the closest model organism to mockingbirds that we could breed in controlled conditions. We identified a limited number of differentially methylated cytosines (DMCs) in parasitized versus nonparasitized mockingbirds, but the number was not more than expected by chance. In contrast, we saw clear effects of permethrin on methylation in captive zebra finches. DMCs in zebra finches paralleled documented effects of permethrin exposure on vertebrate cellular signaling and endocrine function. Our results from captive birds indicate a role for epigenetic processes in mediating sublethal nontarget effects of pyrethroid exposure in vertebrates. Environmental conditions in the field were more variable than the laboratory, which may have made effects of both parasitism and permethrin harder to detect in mockingbirds. RRBS approaches such as epiGBS may be a cost-effective way to characterize genome-wide methylation profiles. However, our results indicate that ecological epigenetic studies in natural populations should consider the number of cytosines interrogated and the depth of sequencing in order to have adequate power to detect small and variable effects.

Specialist by preference, generalist by need: availability of quality hosts drives parasite choice in a natural multihost-parasite system.

Encountering suitable hosts is key for parasite success. A general assumption for disease transmission is that the contact of a parasite with a potential host is driven by the density or relative frequency of hosts. That assumption ignores the potential role of differential host attractiveness for parasites that can drive the encounter of hosts. It has been posited that hosts may be chosen by parasites as a function of their suitability, but the existing literature addressing that hypothesis is still very scarce. In a natural system involving a parasitic Philornis botfly and its multiple bird hosts, there are profound differences in host quality. The Great Kiskadee tolerates and does not invest in resisting the infection, which makes it an optimal host. Alternative hosts are frequently used, but whilst some of them may be good options, others are bad alternatives. Here we examined the host selection processes that drive parasite dynamics in this system with 8 years of data from a longitudinal study under natural conditions. We found that the use of an alternative host was not driven by its density or relative frequency, but instead selection of these hosts was strongly dependent on availability of more suitable hosts. When optimal hosts are plentiful, the parasite tends to ignore alternative ones. As broods of optimal hosts become limited, good alternative hosts are targeted. The parasite chooses bad alternative hosts only when better alternatives are not sufficiently available. These results add evidence from a natural system that some parasites choose their hosts as a function of their profitability, and show that host selection by this parasite is plastic and context-dependent. Such findings could have important implications for the epidemiology of some parasitic and vector-borne infections which should be considered when modelling and managing those diseases. The facultative host selection observed here can be of high relevance for public health, animal husbandry, and biodiversity conservation, because reductions in the richness of hosts might cause humans, domestic animals, or endangered species to become increasingly targeted by parasites that can drive the encounter of hosts.

Environmental variables determining the distribution of an avian parasite: the case of the Philornis torquans complex in South America.

Philornis flies are the major cause of myiasis in nestlings of Neotropical birds, being of major concern in geographically-restricted and endangered bird species. Despite its relevance for the conservation of birds, there is little information about the environmental dimensions determining Philornis spp. geographical range. By using maximum entropy, we identified for the first time the macro-environmental variables constraining the abiotic niche of the P. torquans complex in South America, and provided a model map of its potential distribution based on environmental suitability. We identified the minimum temperature of the coldest month as the most relevant variable, associated with the largest decrease in habitat suitability in Brazil and northern South America. Furthermore, the mean temperature of the warmest quarter limited suitability mostly along with the Andean range. In addition, humidity and moisture are influential factors in most of Argentina, northern Chile, and coastal Peru. The geographical projection suggests that environments in most of central-eastern Argentina, and in a broad area in central Chile, are suitable for the presence of the P. torquans complex. Besides providing information about the ecology of Philornis spp., this study represents a tool for bird conservation and a reference for future work on the distribution of this genus.

Timing of infestation influences virulence and parasite success in a dynamic multi-host-parasite interaction between the invasive parasite, Philornis downsi, and Darwin's finches.

Recently commenced host-parasite interactions provide an excellent opportunity to study co-evolutionary processes. Multi-host systems are especially informative because variation in virulence between hosts and temporal changes provides insight into evolutionary dynamics. However, empirical data under natural conditions are scarce. In the present study, we investigated the interaction between Darwin's finches and the invasive fly Philornis downsi whose larvae feed on the blood of nestlings. Recently, however, the fly has changed its behavior and now also attacks incubating females. Two sympatric hosts are affected differently by the parasite and parasite load has changed over time. Our study observed a reversal of trends described two decades ago: while, currently, small tree finches (Camarhynchus parvulus) experience significantly higher parasite load than warbler finches (Certhidea olivacea), this was the opposite two decades ago. Currently, fledging success is higher in warbler finches compared to small tree finches. Our data indicate that not only intensity but also timing of infestation influences hosts' reproductive success and parasite fitness. During incubation, prevalence was higher in warbler finches, but once chicks had hatched, prevalence was 100% in both species and parasite load was higher in small tree finches. Furthermore, our results suggest faster development and higher reproductive success of P. downsi in small tree finch nests. A change in host preference driven by larvae competition could have led to the reversal in parasite load.

Parental care in the Small Tree Finch Camarhynchus parvulus in relation to parasitism and environmental factors.

The parental food compensation hypothesis suggests that parents may compensate for the negative effects of parasites on chicks by increased food provisioning. However, this ability differs widely among host species and may also depend on ecological factors such as adverse weather conditions and habitat quality. Although weed management can improve habitat quality, management measures can bring about a temporary decrease in food availability and thus may reduce parents' ability to provide their nestlings with enough energy. In our study we investigated the interaction of parasitism and weed management, and the influence of climate on feeding rates in a Darwin's tree finch species, which is negatively impacted by two invasive species. The larvae of the invasive parasitic fly Philornis downsi ingest the blood and body tissues of tree finch nestlings, and the invasive Blackberry Rubus niveus affects one of the main habitats of Darwin's tree finches. We compared parental food provisioning of the Small Tree Finch Camarhynchus parvulus in parasitized and parasite-free nests in three different areas, which differed in invasive weed management (no management, short-term and long-term management). In a parasite reduction experiment, we investigated whether the Small Tree Finch increases food provisioning rates to nestlings when parasitized and whether this ability depends on weed management conditions and precipitation. Our results provide no evidence that Small Tree Finches can compensate with additional food provisioning when parasitized with P. downsi. However, we found an increase in male effort in the short-term management area, which might indicate that males compensate for lower food quality with increased provisioning effort. Furthermore, parental food provisioning was lower during rainfall, which provides an explanation for the negative influence of rain on breeding success found in earlier studies. Like other Darwin's finches, the Small Tree Finch seems to lack the ability to compensate for the negative effects of P. downsi parasitism, which is one explanation for why this invasive parasite has such a devastating effect on this host species.

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.

Parasitism by an invasive nest fly reduces future reproduction in Galápagos mockingbirds.

Organisms allocate limited resources to competing activities such as reproduction, growth, and defense against parasites and predators. The introduction of a novel parasite may create new life history trade-offs. As hosts increase their investment in self-maintenance or defense, the cost of parasitism may carry over to other aspects of host biology. Here, in an experimental field study, we document delayed effects of an introduced nest parasite, Philornis downsi, on reproduction of Galápagos mockingbirds (Mimus parvulus). Parasitism of first nests reduced both the number and size of chicks that parents hatched when they re-nested several weeks later. The delayed effect of P. downsi on future reproduction may have been mediated by behavioral shifts by the parents to avoid or resist parasitism. Our results demonstrate that effects of parasitism can persist even after immediate exposure ends. We draw attention to the potential implications that introduced parasites have for host reproductive strategies.

Behavioral Responses of the Invasive Fly Philornis downsi to Stimuli from Bacteria and Yeast in the Laboratory and the Field in the Galapagos Islands.

Philornis downsi Dodge and Aitken (Diptera: Muscidae) is an avian parasitic fly that has invaded the Galapagos archipelago and exerts an onerous burden on populations of endemic land birds. As part of an ongoing effort to develop tools for the integrated management of this fly, our objective was to determine its long- and short-range responses to bacterial and fungal cues associated with adult P. downsi. We hypothesized that the bacterial and fungal communities would elicit attraction at distance through volatiles, and appetitive responses upon contact. Accordingly, we amplified bacteria from guts of adult field-caught flies and from bird feces, and yeasts from fermenting papaya juice (a known attractant of P. downsi), on selective growth media, and assayed the response of flies to these microbes or their exudates. In the field, we baited traps with bacteria or yeast and monitored adult fly attraction. In the laboratory, we used the proboscis extension response (PER) to determine the sensitivity of males and females to tarsal contact with bacteria or yeast. Long range trapping efforts yielded two female flies over 112 trap-nights (attracted by bacteria from bird feces and from the gut of adult flies). In the laboratory, tarsal contact with stimuli from gut bacteria elicited significantly more responses than did yeast stimuli. We discuss the significance of these findings in context with other studies in the field and identify targets for future work.

Genetic admixture predicts parasite intensity: evidence for increased hybrid performance in Darwin's tree finches.

Hybridization can increase adaptive potential when enhanced genetic diversity or novel genetic combinations confer a fitness advantage, such as in the evolution of anti-parasitic mechanisms. Island systems are especially susceptible to invasive parasites due to the lack of defence mechanisms that usually coevolve in long-standing host-parasite relationships. We test if host genetic admixture affects parasite numbers in a novel host-parasite association on the Galápagos Islands. Specifically, we compare the number of Philornis downsi in nests with offspring sired by Darwin's small tree finch (Camarhynchus parvulus), Darwin's medium tree finch (C. pauper) and hybrids of these two species. The number of P. downsi decreased with an increasing genetic admixture of the attending male, and nests of hybrid males had approximately 50% fewer parasites than C. parvulus nests, and approximately 60% fewer parasites than C. pauper nests. This finding indicates that hybridization in this system could be favoured by selection and reveal a mechanism to combat an invasive parasite.

Annual environmental variation influences host tolerance to parasites.

When confronted with a parasite or pathogen, hosts can defend themselves by resisting or tolerating the attack. While resistance can be diminished when resources are limited, it is unclear how robust tolerance is to changes in environmental conditions. Here, we investigate the sensitivity of tolerance in a single host population living in a highly variable environment. We manipulated the abundance of an invasive parasitic fly, Philornis downsi, in nests of Galápagos mockingbirds ( Mimus parvulus) over four field seasons and measured host fitness in response to parasitism. Mockingbird tolerance to P. downsi varied significantly among years and decreased when rainfall was limited. Video observations indicate that parental provisioning of nestlings appears key to tolerance: in drought years, mockingbirds likely do not have sufficient resources to compensate for the effects of P. downsi. These results indicate that host tolerance is a labile trait and suggest that environmental variation plays a major role in mediating the consequences of host-parasite interactions.

Host-specific associations affect the microbiome of Philornis downsi, an introduced parasite to the Galápagos Islands.

The composition and diversity of bacteria forming the microbiome of parasitic organisms have implications for differential host pathogenicity and host-parasite co-evolutionary interactions. The microbiome of pathogens can therefore have consequences that are relevant for managing disease prevalence and impact on affected hosts. Here, we investigate the microbiome of an invasive parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, where it poses extinction threat to Darwin's finches and other land birds. Larvae infest nests of Darwin's finches and consume blood and tissue of developing nestlings, and have severe mortality impacts. Using 16s rRNA sequencing data, we characterize the bacterial microbiota associated with P. downsi adults and larvae sourced from four finch host species, inhabiting two islands and representing two ecologically distinct groups. We show that larval and adult microbiomes are dominated by the phyla Proteobacteria and Firmicutes, which significantly differ between life stages in their distributions. Additionally, bacterial community structure significantly differed between larvae retrieved from strictly insectivorous warbler finches (Certhidea olivacea) and those parasitizing hosts with broader dietary preferences (ground and tree finches, Geospiza and Camarhynchus spp., respectively). Finally, we found no spatial effects on the larval microbiome, as larvae feeding on the same host (ground finches) harboured similar microbiomes across islands. Our results suggest that the microbiome of P. downsi changes during its development, according to dietary composition or nutritional needs, and is significantly affected by host-related factors during the larval stage. Unravelling the ecological significance of bacteria for this parasite will contribute to the development of novel, effective control strategies.

Identification and Optimization of Microbial Attractants for Philornis downsi, an Invasive Fly Parasitic on Galapagos Birds.

We investigated the role of olfactory cues from actively fermenting yeast (Saccharomyces cerevisiae) in attraction of adult Philornis downsi and identified two synergistically attractive yeast volatiles. Larvae of this invasive fly parasitize the hatchlings of passerines and threaten the Galapagos avifauna. Gas chromatography coupled with electroantennographic detection (GC-EAD), coupled gas chromatography-mass spectrometry (GC-MS), and field trapping experiments were used to identify volatile compounds from a yeast-sugar solution. EAD responses were consistently elicited by 14 yeast volatiles. In a series of field trapping experiments, a mixture of the 14 EAD-active compounds was similarly attractive to P. downsi when compared to the yeast-sugar solution, and we found that acetic acid and ethanol were essential for attraction. A mixture of 0.03 % acetic acid and 3 % ethanol was as attractive as the 14-component blend, but was not as attractive as the yeast-sugar solution. Philornis downsi showed positive and negative dose-responses to acetic acid in the ranges of 0.01 ~ 0.3 % and 0.3 ~ 9 %, respectively. Further optimization showed that the mixture of 1 % acetic acid and 3 % ethanol was as attractive as the yeast-sugar solution. Both mixtures of acetic acid and ethanol were more selective than the yeast-sugar solution in terms of non-target moths and Polistes versicolor wasps captured. These results indicate that acetic acid and ethanol produced by yeasts are crucial for P. downsi attraction to fermented materials on which they feed as adults and can be used to manage this invasive fly in Galapagos.

An introduced parasitic fly may lead to local extinction of Darwin's finch populations.

Introduced pathogens and other parasites are often implicated in host population level declines and extinctions. However, such claims are rarely supported by rigorous real-time data. Indeed, the threat of introduced parasites often goes unnoticed until after host populations have declined severely. The recent introduction of the parasitic nest fly, Philornis downsi, to the Galápagos Islands provides an opportunity to monitor the current impact of an invasive parasite on endemic land bird populations, including Darwin's finches.In this paper we present a population viability model to explore the potential long-term effect of P. downsi on Darwin's finch populations. The goal of our study was to determine whether P. downsi has the potential to drive host populations to extinction and whether management efforts are likely to be effective.Our model is based on data from five years of experimental field work documenting the effect of P. downsi on the reproductive success of medium ground finch Geospiza fortis populations on Santa Cruz Island. Under two of the three scenarios tested, the model predicted medium ground finches are at risk of extinction within the next century.However, sensitivity analyses reveal that even a modest reduction in the prevalence of the parasite could improve the stability of finch populations. We discuss the practicality of several management options aimed at achieving this goal.Synthesis and applications. Our study demonstrates the predicted high risk of local extinction of an abundant host species, the medium ground finch Geospiza fortis due to an introduced parasite, Philornis downsi. However, our study further suggests that careful management practices aimed at reducing parasite prevalence have the potential to significantly lower the risk of host species extinction.

Galápagos mockingbirds tolerate introduced parasites that affect Darwin's finches.

Introduced parasites threaten native host species that lack effective defenses. Such parasites increase the risk of extinction, particularly in small host populations like those on islands. If some host species are tolerant to introduced parasites, this could amplify the risk of the parasite to vulnerable host species. Recently, the introduced parasitic nest fly Philornis downsi has been implicated in the decline of Darwin's finch populations in the Galápagos Islands. In some years, 100% of finch nests fail due to P. downsi; however, other common host species nesting near Darwin's finches, such as the endemic Galápagos mockingbird (Mimus parvulus), appear to be less affected by P. downsi. We compared effects of P. downsi on mockingbirds and medium ground finches (Geospiza fortis) on Santa Cruz Island in the Galápagos. We experimentally manipulated the abundance of P. downsi in nests of mockingbirds and finches to measure the direct effect of the parasite on the reproductive success of each species of host. We also compared immunological and behavioral responses by each species of host to the fly. Although nests of the two host species had similar parasite densities, flies decreased the fitness of finches but not mockingbirds. Neither host species had a significant antibody-mediated immune response to P. downsi. Moreover, finches showed no significant increase in begging, parental provisioning, or plasma glucose levels in response to the flies. In contrast, parasitized mockingbird nestlings begged more than nonparasitized mockingbird nestlings. Greater begging was correlated with increased parental provisioning behavior, which appeared to compensate for parasite damage. The results of our study suggest that finches are negatively affected by P. downsi because they do not have such behavioral mechanisms for energy compensation. In contrast, mockingbirds are capable of compensation, making them tolerant hosts, and a possible indirect threat to Darwin's finches.