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Abstract Human activity changes multiple factors in the environment, which can have positive or negative synergistic effects on organisms. However, few studies have explored the causal effects of multiple anthropogenic factors, such as urbanization and invasive species, on animals and the mechanisms that mediate these interactions. This study examines the influence of urbanization on the detrimental effect of invasive avian vampire flies (Philornis downsi) on endemic Darwin's finches in the Galápagos Islands. We experimentally manipulated nest fly abundance in urban and non‐urban locations and then characterized nestling health, fledging success, diet, and gene expression patterns related to host defense. Fledging success of non‐parasitized nestlings from urban (79%) and non‐urban (75%) nests did not differ significantly. However, parasitized, non‐urban nestlings lost more blood, and fewer nestlings survived (8%) compared to urban nestlings (50%). Stable isotopic values (δ¹⁵N) from urban nestling feces were higher than those from non‐urban nestlings, suggesting that urban nestlings are consuming more protein. δ¹⁵N values correlated negatively with parasite abundance, which suggests that diet might influence host defenses (e.g., tolerance and resistance). Parasitized, urban nestlings differentially expressed genes within pathways associated with red blood cell production (tolerance) and pro‐inflammatory response (innate immunological resistance), compared to parasitized, non‐urban nestlings. In contrast, parasitized non‐urban nestlings differentially expressed genes within pathways associated with immunoglobulin production (adaptive immunological resistance). Our results suggest that urban nestlings are investing more in pro‐inflammatory responses to resist parasites but also recovering more blood cells to tolerate blood loss. Although non‐urban nestlings are mounting an adaptive immune response, it is likely a last effort by the immune system rather than an effective defense against avian vampire flies since few nestlings survived. 

Abstract Host‐associated microbiota can be affected by factors related to environmental change, such as urbanization and invasive species. For example, urban areas often affect food availability for animals, which can change their gut microbiota. Invasive parasites can also influence microbiota through competition or indirectly through a change in the host immune response. These interacting factors can have complex effects on host fitness, but few studies have disentangled the relationship between urbanization and parasitism on an organism's gut microbiota. To address this gap in knowledge, we investigated the effects of urbanization and parasitism by the invasive avian vampire fly (Philornis downsi) on the gut microbiota of nestling small ground finches (Geospiza fuliginosa) on San Cristóbal Island, Galápagos. We conducted a factorial study in which we experimentally manipulated parasite presence in an urban and nonurban area. Faeces were then collected from nestlings to characterize the gut microbiota (i.e. bacterial diversity and community composition). Although we did not find an interactive effect of urbanization and parasitism on the microbiota, we did find main effects of each variable. We found that urban nestlings had lower bacterial diversity and different relative abundances of taxa compared to nonurban nestlings, which could be mediated by introduction of the microbiota of the food items or changes in host physiology. Additionally, parasitized nestlings had lower bacterial richness than nonparasitized nestlings, which could be mediated by a change in the immune system. Overall, this study advances our understanding of the complex effects of anthropogenic stressors on the gut microbiota of birds. 

Invasive parasites are a major threat to biodiversity worldwide, so understanding the factors that control them is necessary to improve the health of affected host species. In the Galápagos Islands, the invasive nest ectoparasite, the avian vampire fly (Philornis downsi), is causing up to 100% mortality in nestling Darwin’s finches. However, urban finch nests have fewer flies than non-urban finch nests. One explanation is that finches incorporate cigarette butts into their nests, which can decrease nest parasite abundance for other bird species. For our study, we exposed larval flies to cigarette tobacco-treated (concentrated or diluted) or untreated cotton, then characterized pupation success, pupal deformities and success, and adult fly eclosure success and size. The influence of moisture on the effect of tobacco treatment on fly health was also determined. Flies reared in the tobacco treatments as larvae had lower pupation success, larger pupal volume, and a higher prevalence of pupal deformities compared to control flies, regardless of moisture treatment. Furthermore, we found that tobacco-treated flies had lower eclosure success. In fact, very few tobacco-treated flies survived to adulthood. We also collected finch nests and quantified the prevalence and mass of cigarette butts and abundance of flies in the nests. Although most urban finch nests contain cigarette butts (73%), the mass of cigarette butts was very low and did not correlate with fly abundance. Compared to past studies, finch nests require ten times as many cigarette butts to affect fly survival. Although tobacco can negatively affect vampire flies, finches likely do not incorporate enough cigarette butts to affect fly fitness. 

Urbanization can influence many environmental factors that can affect the condition, immunity, and gut microbiota of birds. Over the past several decades, the Galápagos Islands of Ecuador have experienced increasing human activity, which has led to recent changes in the morphology, gut microbiota, and immunity of Darwin’s finches. However, these traits have not been characterized before the exponential growth of human population size and tourist visitation rates, i.e., before 2009. The goal of this study was to determine the effect of land use on the fecal microbiota, immune response, and body measurements of Darwin’s finches in 2008, at a time of rapidly increasing human activity on the islands. Specifically, we compared fecal microbiota (bacterial diversity, community structure and membership, and relative abundance of bacterial taxa), proxies of immunity (lysozyme activity and haptoglobin, complement antibody, and natural antibody levels), and body measurements (body mass and condition, tarsus length) across undeveloped, agricultural, and urban areas for medium ground finches (Geospiza fortis) and small ground finches (G. fuliginosa). Lysozyme activity was lower and observed bacterial species richness was higher in urban areas compared to non-urban areas across both finch species. In medium ground finches, four genera (Methylobacterium-Methylorubrum, Escherichia-Shigella, Brucella, and Citrobacter spp.) were higher in urban areas compared to undeveloped areas. In small ground finches, Paucibacter, Achromobacter, Delftia, Stenotrophomonas, and Brucella spp. had higher relative abundances in undeveloped and agricultural areas whereas the genus Cutibacterium was more abundant in finches from urban and agricultural areas than in finches from undeveloped areas. Medium ground finches were smaller in undeveloped areas compared to the other two areas, but body mass of small ground finches did not differ across areas. Our results suggest that human activity can have an impact on immune measures and gut microbiota of Darwin’s finches.