Plant invasion causes alterations in Darwin's finch feeding patterns in Galápagos cloud forests.

Invasive species pose a major threat to forest biodiversity, particularly on islands such as the Galapágos. Here, invasive plants are threatening the remnants of the unique cloud forest and its iconic Darwin's finches. We posit that food web disturbances caused by invasive Rubus niveus (blackberry), have contributed to the rapid decline of the insectivourous green warbler finch (Certhidae olivacea). We compared the birds' dietary changes in long-term management, short-term management and unmanaged areas. We measured C:N ratios, and δ15N­nitrogen and δ13C­carbon values in both consumer tissues (bird-blood) and food sources (arthropods), as indicators of resource use change, and collected mass abundance, and arthropod diversity data. We characterised the birds' diets using isotope mixing models. The results revealed that finches in (blackberry-invaded) unmanaged areas foraged more on abundant, yet lower quality, arthropods present in the invaded understory. This suggests that blackberry encroachment leads to a decrease in food source quality with physiological consequences for green warbler finch chicks. Results also implied that blackberry control has a short-term impact on food source quantity, which led to a decrease in chick recruitment that we observed in our previous studies; despite this, in the long-term, these managed systems show signs of recovery within three years of restoration.

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.

Under adverse conditions, older small tree finch males (Camarhynchus parvulus) produce more offspring than younger males.

Females of many bird species prefer mating with older males, presumably because they provide superior parental care and possibly superior genes. A previous study found that female small tree finches (Camarhynchus parvulus) preferred pairing with old males and had a higher breeding success when paired with old males because their nests were more concealed, higher up in the canopy and therefore less likely to be depredated. However, causes for brood loss have changed over the last decade: predation of small tree finch nests has decreased, whereas brood losses due to parasitism by the invasive parasitic fly Philornis downsi have increased. In the present study, we investigated (a) how the change in predation and parasitism by P. downsi influenced the breeding success of small tree finches, (b) whether there were still differences in breeding success between young and old males, (c) whether P. downsi infestation had a differential effect on nests of young and old males and (d) whether young and old males differed in foraging success. During 2012-2016, we found an overall low influence of predation and a high influence of P. downsi, but neither differed between nests of young and old males. Nests of old males had more fledglings than those of young males. However, the difference in breeding success disappeared when P. downsi numbers were experimentally reduced by injecting an insecticide into nests. This indicates that older males were able to compensate for the detrimental effects of parasitism.

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

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 bi-weekly 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.

The impact of invasive plant management on the foraging ecology of the Warbler Finch (Certhidea olivacea) and the Small Tree Finch (Camarhynchus parvulus) on Galápagos.

In recent decades, arboreal Darwin's Finches have suffered from a dramatic population decline, which has been attributed to parasitism by the invasive botfly Philornis downsi. However, changes to their primary habitat caused by invasive plant species may have additionally contributed to the observed population decline. The humid cloud forest on Santa Cruz Island is a stronghold of arboreal Darwin's Finches but has been invaded by blackberry (Rubus niveus). In some areas, manual control and herbicide application are used to combat this invasion, both causing a temporary removal of the entire understory. We hypothesized that the removal of the understory reduces the availability of arthropods, which are a main food source during chick rearing. We compared the foraging behaviour of Warbler Finches (Certhidea olivacea) and Small Tree Finches (Camarhynchus parvulus) at three study sites that varied in the degree of R. niveus invasion and the length of time since the last herbicide application. We used prey attack rate and foraging success as an index for food availability and predicted a lower attack rate and foraging success in areas that had recently been sprayed with herbicides. We found that both the invasion and the management of R. niveus influenced microhabitat use, foraging substrate and prey choice in both species. Contrary to our hypothesis, we did not find a lower attack rate or foraging success in the area with recent herbicide application. This may be explained by the finding that both species mainly foraged in the canopy but also used dead plant structures of the understory of the recently controlled area that resulted from the invasive plant management.

Darwin's finches treat their feathers with a natural repellent.

Darwin's finches are highly innovative. Recently we recorded for the first time a behavioural innovation in Darwin's finches outside the foraging context: individuals of four species rubbed leaves of the endemic tree Psidium galapageium on their feathers. We hypothesised that this behaviour serves to repel ectoparasites and tested the repellency of P. galapageium leaf extracts against parasites that negatively affect the fitness of Darwin's finches, namely mosquitoes and the invasive hematophagous fly Philornis downsi. Mosquitoes transmit pathogens which have recently been introduced by humans and the larvae of the fly suck blood from nestlings and incubating females. Our experimental evidence demonstrates that P. galapageium leaf extracts repel both mosquitoes and adult P. downsi and also inhibit the growth of P. downsi larvae. It is therefore possible that finches use this plant to repel ectopoarasites.

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.

Invasive parasites, habitat change and heavy rainfall reduce breeding success in Darwin's finches.

Invasive alien parasites and pathogens are a growing threat to biodiversity worldwide, which can contribute to the extinction of endemic species. On the Galápagos Islands, the invasive parasitic fly Philornis downsi poses a major threat to the endemic avifauna. Here, we investigated the influence of this parasite on the breeding success of two Darwin's finch species, the warbler finch (Certhidea olivacea) and the sympatric small tree finch (Camarhynchus parvulus), on Santa Cruz Island in 2010 and 2012. While the population of the small tree finch appeared to be stable, the warbler finch has experienced a dramatic decline in population size on Santa Cruz Island since 1997. We aimed to identify whether warbler finches are particularly vulnerable during different stages of the breeding cycle. Contrary to our prediction, breeding success was lower in the small tree finch than in the warbler finch. In both species P. downsi had a strong negative impact on breeding success and our data suggest that heavy rain events also lowered the fledging success. On the one hand parents might be less efficient in compensating their chicks' energy loss due to parasitism as they might be less efficient in foraging on days of heavy rain. On the other hand, intense rainfalls might lead to increased humidity and more rapid cooling of the nests. In the case of the warbler finch we found that the control of invasive plant species with herbicides had a significant additive negative impact on the breeding success. It is very likely that the availability of insects (i.e. food abundance)is lower in such controlled areas, as herbicide usage led to the removal of the entire understory. Predation seems to be a minor factor in brood loss.