Title: Host avian species and environmental conditions influence the microbial ecology of brood parasitic brown‐headed cowbird nestlings: What rules the roost?
Abstract The role of species interactions, as well as genetic and environmental factors, all likely contribute to the composition and structure of the gut microbiome; however, disentangling these independent factors under field conditions represents a challenge for a functional understanding of gut microbial ecology. Avian brood parasites provide unique opportunities to investigate these questions, as brood parasitism results in parasite and host nestlings being raised in the same nest, by the same parents. Here we utilized obligate brood parasite brown‐headed cowbird nestlings (BHCO;Molothrus ater) raised by several different host passerine species to better understand, via 16S rRNA sequencing, the microbial ecology of brood parasitism. First, we compared faecal microbial communities of prothonotary warbler nestlings (PROW;Protonotaria citrea) that were either parasitized or non‐parasitized by BHCO and communities among BHCO nestlings from PROW nests. We found that parasitism by BHCO significantly altered both the community membership and community structure of the PROW nestling microbiota, perhaps due to the stressful nest environment generated by brood parasitism. In a second dataset, we compared faecal microbiotas from BHCO nestlings raised by six different host passerine species. Here, we found that the microbiota of BHCO nestlings was significantly influenced by the parental host species and the presence of an inter‐specific nestmate. Thus, early rearing environment is important in determining the microbiota of brood parasite nestlings and their companion nestlings. Future work may aim to understand the functional effects of this microbiota variability on nestling performance and fitness.  more » « less
Award ID(s):
2305848 2026836
PAR ID:
10501898
Author(s) / Creator(s):
; ; ; ; ; ;
Publisher / Repository:
Wiley Publishing
Date Published:
Journal Name:
Molecular Ecology
Volume:
33
Issue:
6
ISSN:
0962-1083
Subject(s) / Keyword(s):
bacteria birds brood parasitism community ecology host–parasite interactions microbiome
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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. 
    more » « less
  2. Abstract BackgroundSpecies host diverse microbial communities that can impact their digestion and health, which has led to much interest in understanding the factors that influence their microbiota. We studied the developmental, environmental, and social factors that influence the microbiota of nestling barn owls (Tyto alba) through a partial cross-fostering experiment that manipulated the social and nest environment of the nestlings. We then examined the nestling microbiota before and three weeks after the exchange of nestlings between nests, along with the microbiota of the adults at the nest and nestlings in unmanipulated nests. ResultsWe found that nestlings had higher bacterial diversity and different bacterial communities than adults. The microbiota of nestlings was more like that of their mothers than their fathers, but the similarity to the father tended to increase with the amount of time the father was in close proximity to the nest, as measured from movement data. Cross-fostered offspring had higher bacterial diversity and greater changes in bacterial community composition over time than control offspring. Cross-fostering led the microbiota of the nestlings in the experiment to converge on similar bacterial communities. The microbiota of nestling owls therefore rapidly changed along with alterations to their social and nest environments. ConclusionsThese results highlight the dynamic nature of the microbiota during early development and that social interactions can shape microbial communities. 
    more » « less
  3. Urbanization reflects a major form of environmental change impacting wild birds globally. Whereas urban habitats may provide increased availability of water, some food items, and reduced predation levels compared to rural, they can also present novel stressors including increased light at night, ambient noise, and reduced nutrient availability. Urbanization can also alter levels of brood parasitism, with some host species experiencing elevated levels of brood parasitism in urban areas compared to rural areas. Though the demographic and behavioral consequences of urbanization and brood parasitism have received considerable attention, their consequences for cellular‐level processes are less understood. Telomeres provide an opportunity to understand the cellular consequences of different environments as they are a well‐established metric of biological state that can be associated with residual lifespan, disease risk, and behavior, and are known to be sensitive to environmental conditions. Here we examine the relationships between urbanization, brood parasitism, and blood telomere lengths in adult and nestling song sparrowsMelospiza melodia. Song sparrows are a North American songbird found in both urban and rural habitats that experience high rates of brood parasitism by brown‐headed cowbirdsMolothrus aterin the urban, but not the rural, sites in our study system. Among adults and nestlings from non‐parasitized nests, we found no differences in relative telomere lengths between urban and rural habitats. However, among urban nestlings, the presence of a brood parasite in the nest was associated with significantly shorter relative telomere lengths compared to when a brood parasite was absent. Our results suggest a novel, indirect, impact of urbanization on nestling songbirds through the physiological impacts of brood parasitism. 
    more » « less
  4. 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. 
    more » « less
  5. Urbanization is projected to grow rapidly in the coming decades. Several consequences of this form of anthropogenic change for ecosystems and individuals are described by the fields of urban ecology and urban ecophysiology, respectively. Of the environmental variables that could pose challenges for urban-living animals, energy limitations may be especially important, particularly for animals with critical periods of growth, such as nestling songbirds. Many studies document reduced arthropod prey availability for songbirds living in urban habitats, which can compromise the growth and condition of nestlings, possibly because of protein limitation. In our study system of replicate urban and rural song sparrow (Melospiza melodia) populations, there is lower arthropod biomass in urban habitats, as well as higher rates of brood parasitism by brown-headed cowbirds (Molothrus ater), which can cause additional nutritional limitation. Therefore, we hypothesized that urban nestling song sparrows may be protein-limited and experience compromised growth and body condition relative to rural nestlings. We tested this hypothesis with two studies. First, we took body measurements during the first 10 days of development from rural nestlings, urban nestlings without brood parasites, and urban nestlings with brood parasites to see if groups differed in growth (n = 348 nestlings over 6 years). Second, we collected nestling plasma samples (n = 43) from a subset of the birds measured in the first study and then used liquid chromatography-mass spectrometry (LC-MS) to determine concentrations of free amino acids. We found rural nestlings had greater change over time in body mass and tarsus length compared to both urban groups. However, we found no differences in amino acid concentrations across these nestling groups. Thus, urbanization appears to affect growth rates in song sparrows, especially when brood parasites are present in a nest, but we found no evidence supporting amino acids as the mechanistic link for these differences in our system. 
    more » « less