HEALTH MONITORING: BIRDS
Grant D., Todd P. A., Pennycott, T. (2007). Monitoring wild greenfinch (Carduelis chloris) for Salmonella enterica typhimurium. Ecological Research 22: 571-574.
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The identification and monitoring of emerging infectious diseases in free living wild birds is a challenge to wildlife biologists. In this study, a non-invasive methodology for identifying salmonellosis in wild garden birds was developed. We focussed on greenfinch, Carduelis chloris, which were found to have a seasonal pattern in the occurrence of Salmonella Typhimurium DT 56(v). Principal components analysis of biometric data indicated that low fat and low weight could be useful indicators of Salmonella positive greenfinch. A combination of biometrics taken from live birds, faecal analysis, and behavioural observations provide an effective and efficient system for identifying the presence of salmonellosis within greenfinch.
Honma H., Suyama Y., Nakai Y. (2011): Detection of parasitizing coccidia and determination of host crane species, sex and genotype by faecal DNA analysis. Molecular Ecology Resources 11: 1033-1044.
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In Japan, the three main crane species are the endangered red-crowned crane (Grus japonensis) inhabiting Hokkaido, the northernmost island of Japan; the vulnerable hooded crane (Grus monacha); and the vulnerable white-naped crane (Grus vipio). Both the hooded and white-naped cranes migrate in winter to Izumi in Kyushu, the southern island of Japan. In this study, we investigated the cranes and their coccidian parasites, through a targeted molecular approach using faecal DNA to develop a noninvasive method for infectious disease research. To determine the origin of noninvasively collected faecal samples, host species were identified by sequencing a region of approximately 470 bp of the mitochondrial 16S ribosomal RNA gene in the faecal DNA. Furthermore, to avoid sample redundancy, individual determination was performed by fragment analysis using microsatellite and sex-linked markers. For microsatellite genotyping, previously reported markers and markers isolated in this study were examined, and seven loci for red-crowned cranes, eight for hooded cranes and six for white-naped cranes displayed polymorphisms. A low error rate was demonstrated by comparing microsatellite data generated from faecal DNA samples with that generated from feather DNA samples, indicating a high reliability. Polymerase chain reaction–based capillary electrophoresis (PCR-CE), employing genetic markers in the second internal transcribed spacer (ITS2) of nuclear ribosomal DNA, was employed to detect crane coccidia. The sensitivity of detection of PCR-CE using faecal DNA was inferior to that with traditional microscopy; however, our results suggest that PCR-CE can depict crane coccidia diversity with higher resolution and it is a useful tool to characterize community composition of coccidia in detail.
Bandelj P., Trilar T., Vengust M., Rataj A. V. (2015): Influence of phylogeny, migration and type of diet on the presence of intestinal parasites in the faeces of European passerine birds (Passeriformes). Wildlife Biology 21: 227-233.
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Migratory and non-migratory passerine birds can carry several pathogens, including parasites, which may cause significant diseases in birds, other animal species and humans. Parasites have been shown to negatively impact many populations of wildlife, and this may become more significant with global temperature changes. This study was performed to investigate the prevalence of intestinal parasites in faecal samples of European passerines. Intestinal parasites identified were statistically associated with passerines phylogenetic classification, migratory habits (migratory, non-migratory) and the type of diet (omnivorous, insectivorous and granivorous). A total of 385 passerines of 42 species were captured and their droppings collected. The prevalence of parasites in faecal samples of passerines was 15.6%. Intestinal parasites were identified in 50/309 (16.2%) migratory passerines and 10/76 (13.2%) non-migratory passerines using the faecal flotation method. Coccidia were most often identified parasites; they were more likely to be present in an omnivorous bird species (p = 0.02). Syngamus spp. was more likely to be detected in omnivorous passerines (p = 0.04). Tits (p = 0.01) and finches (p = 0.006) were less likely to have intestinal parasites present in their faecal samples than passerines classified in other phylogenetic clades. Tits (p = 0.02) and finches (p = 0.008) were also less likely to have coccidia present in their faecal samples. Phylogeny was associated with the presence of parasites in faecal samples of passerines (p = 0.03). The prevalence of parasites, however, was not associated with the migration habit of passerines, but to the type of diet (p = 0.04). Our analysis suggests that the diversity of feeding sources of omnivore passerines exposes them to infection with intestinal parasites to a greater extent than granivore or insectivore passerines.
Dipineto L., Bossa L. M. D. L., Pace A., Russo T. P., Gargiulo A., Ciccarelli F., Raia P., Caputo V., Fioretti A. (2015): Microbiological survey of birds of prey pellets. Comparative Immunology, Microbiology and Infectious Diseases 41: 49-53.
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A microbiological survey of 73 pellets collected from different birds of prey species housed at the Wildlife Rescue and Rehabilitation Center of Napoli (southern Italy) was performed. Pellets were analyzed by culture and biochemical methods as well as by serotyping and polymerase chain reaction. We isolated a wide range of bacteria some of them also pathogens for humans (i.e. Salmonella enterica serotype Typhimurium, Campylobacter coli, Escherichia coli O serogroups). This study highlights the potential role of birds of prey as asymptomatic carriers of pathogenic bacteria which could be disseminated in the environment not only through the birds of prey feces but also through their pellets.
Kropáčková L., Pechmanová H., Vinkler M., Svobodová J., Velová H., Těšičký M., Martin J. F., Kreisinger J. (2017): Variation between the oral and faecal microbiota in a free-living passerine bird, the great tit (Parus major). Plos One 12: e0179945.
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The gastrointestinal tract of vertebrates is inhabited by diverse bacterial communities that induce marked effects on the host physiology and health status. The composition of the gastrointestinal microbiota is characterized by pronounced taxonomic and functional variability among different regions of the vertebrate gastrointestinal tract. Despite the relatively solid knowledge on the among-region variations of the gastrointestinal microbiota in model mammalian species, there are only a few studies concerning among-region variations of the gastrointestinal microbiota in free-living non-mammalian vertebrate taxa. We used Illumina MiSeq sequencing of bacterial 16S rRNA amplicons to compare the diversity as well as taxonomic composition of bacterial communities in proximal vs. distal parts of the gastrointestinal tract (represented by oral swabs and faecal samples, respectively) in a wild passerine bird, the great tit (Parus major). The diversity of the oral microbiota was significantly higher compared to the faecal microbiota, whereas interindividual variation was higher in faecal than in oral samples. We also observed a pronounced difference in taxonomic content between the oral and faecal microbiota. Bacteria belonging to the phyla Proteobacteria, Firmicutes and Actinobacteria typically dominated in both oral and faecal samples. A high abundance of bacteria belonging to Tenericutes was observed only in faecal samples. Surprisingly, we found only a slight correlation between the faecal and oral microbiota at the within-individual level, suggesting that the microbial composition in these body sites is shaped by independent regulatory processes. Given the independence of these two communities at the individual level, we propose that simultaneous sampling of the faecal and oral microbiota will extend our understanding of host vs. microbiota interactions in wild populations.
Knutie S. A., Gotanda K. M. (2018): A non-invasive method to collect fecal samples from wild birds for microbiome studies. Microbial Ecology 76: 851-855.
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Over the past few decades, studies have demonstrated that the gut microbiota strongly influences the physiology, behavior, and fitness of its host. Such studies have been conducted primarily in humans and model organisms under controlled laboratory conditions. More recently, researchers have realized the importance of placing host-associated microbiota studies into a more ecological context; however, few non-destructive methods have been established to collect fecal samples from wild birds. Here, we present an inexpensive and easy-to-use kit for the non-invasive collection of feces from small birds. The portability of the collection kit makes this method amenable to field studies, especially those in remote areas. The main components of the collection kit include a flat-bottomed paper bag, a large modified weigh boat (tray), vinyl-coated hardware cloth fencing (grate), a clothespin, and a 10% bleach solution (to sterilize the tray and grate). In the paper bag, a sterile tray is placed under a small grate, which prevents the birds from contacting the feces and reduces the risk of contamination. After capture, the bird is placed in the bag for 3–5 min until it defecates. After the bird is removed from the bag, the tray is extracted and the fecal sample is moved to a collection tube and frozen or preserved. We believe that our method is an affordable and easy option for researchers studying the gut microbiota of wild birds.
Videvall E., Strandh M., Engelbrecht A., Cloete S., Cornwallis C. K. (2018): Measuring the gut microbiome in birds: comparison of faecal and cloacal sampling. Molecular Ecology Resources 18: 424-434.
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The gut microbiomes of birds and other animals are increasingly being studied in ecological and evolutionary contexts. Numerous studies on birds and reptiles have made inferences about gut microbiota using cloacal sampling; however, it is not known whether the bacterial community of the cloaca provides an accurate representation of the gut microbiome. We examined the accuracy with which cloacal swabs and faecal samples measure the microbiota in three different parts of the gastrointestinal tract (ileum, caecum, and colon) using a case study on juvenile ostriches, Struthio camelus, and high-throughput 16S rRNA sequencing. We found that faeces were significantly better than cloacal swabs in representing the bacterial community of the colon. Cloacal samples had a higher abundance of Gammaproteobacteria and fewer Clostridia relative to the gut and faecal samples. However, both faecal and cloacal samples were poor representatives of the microbial communities in the caecum and ileum. Furthermore, the accuracy of each sampling method in measuring the abundance of different bacterial taxa was highly variable: Bacteroidetes was the most highly correlated phylum between all three gut sections and both methods, whereas Actinobacteria, for example, was only strongly correlated between faecal and colon samples. Based on our results, we recommend sampling faeces, whenever possible, as this sample type provides the most accurate assessment of the colon microbiome. The fact that neither sampling technique accurately portrayed the bacterial community of the ileum nor the caecum illustrates the difficulty in noninvasively monitoring gut bacteria located further up in the gastrointestinal tract. These results have important implications for the interpretation of avian gut microbiome studies.
Mukai Y., Tomita Y., Kryukov K., Nakagawa S., Ozawa M., Matsui T., Tomonaga K., Imanishi T., Kawaoka Y., Watanabe T., Horie M. (2019): Identification of a distinct lineage of aviadenovirus from crane feces. Virus Genes 55: 815-824.
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Viruses are believed to be ubiquitous; however, the diversity of viruses is largely unknown because of the bias of previous research toward pathogenic viruses. Deep sequencing is a promising and unbiased approach to detect viruses from animal-derived materials. Although cranes are known to be infected by several viruses such as influenza A viruses, previous studies targeted limited species of viruses, and thus viruses that infect cranes have not been extensively studied. In this study, we collected crane fecal samples in the Izumi plain in Japan, which is an overwintering site for cranes, and performed metagenomic shotgun sequencing analyses. We detected aviadenovirus-like sequences in the fecal samples and tentatively named the discovered virus crane-associated adenovirus 1 (CrAdV-1). We determined that our sequence accounted for approximately three-fourths of the estimated CrAdV-1 genome size (33,245 bp). The GC content of CrAdV-1 genome is 34.1%, which is considerably lower than that of other aviadenoviruses. Phylogenetic analyses revealed that CrAdV-1 clusters with members of the genus Aviadenovirus, but is distantly related to the previously identified aviadenoviruses. The protein sequence divergence between the DNA polymerase of CrAdV-1 and those of other aviadenoviruses is 45.2–46.8%. Based on these results and the species demarcation for the family Adenoviridae, we propose that CrAdV-1 be classified as a new species in the genus Aviadenovirus. Results of this study contribute to a deeper understanding of the diversity and evolution of viruses and provide additional information on viruses that infect cranes, which might lead to protection of the endangered species of cranes.
Borrelli L., Minichino A., Pace A., Dipineto L., Fioretti A. (2020): Fecal sample collection method for wild birds-associated microbiome research: perspectives for wildlife studies. Animals 10: 1349.
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Gut microbial communities play important roles in host health, modulating development, nutrient acquisition, immune and metabolic regulation, behavior and diseases. Wildlife microbiome studies and host–microbe interaction and exploration might be an important goal for evolutionary biology, conservation, and ecology. Therefore, collection and sampling methods must be considered before choosing a microbiome-based research plan. Since the fecal microbial community reflects the true gut community better than that of cloacal swab samples and only few nondestructive methods have been described, we propose an easy-to-build box for a noninvasive fecal collection method. The main components of the collection box include a plastic storage box, a plastic tray, a vinyl-coated hardware cloth, and a 10% bleach solution. In the plastic box, the tray is positioned under the raised grate, where the bird is placed, to reduce the risk of contamination of the fecal samples. This procedure could simplify handling and processing phases in wild birds or other animals. It might represent a cheap and useful method for research studies, wildlife rescue center activities, veterinary practices, and conservation practitioners.
Kaszab E., Lengyel G., Marton S., Dán Á., Bányai K., Fehér E. (2020): Occurrence and genetic diversity of CRESS DNA viruses in wild birds: A Hungarian study. Scientific Reports 10: 7036.
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Circoviruses, cycloviruses and other circular, replication-associated protein-encoding single stranded (CRESS) DNA viruses have been detected in a variety of animal taxa. In this study, cloacal swab samples (n = 90) were examined for CRESS DNA viruses from 31 wild bird species living at various aquatic sites in Hungary to identify possible reservoirs of viruses pathogenic to domestic poultry. A total of 30 (33.3%) specimens tested positive with pan-CRESS DNA virus specific PCR. Goose circovirus (GoCV), Duck associated cyclovirus 1 (DuACyV-1) and Garrulus glandarius associated circular virus 1 (GgaCV-1) were detected in nine, three and two different bird species, respectively. Selected specimens were subjected to whole genome sequencing. The obtained sequence data revealed conserved gene structure within the identified virus species and detected homologous (within GoCV) and possible heterologous recombination (within DuACyV-1) events. Results presented here provide new information on the genomic diversity and evolution of selected CRESS DNA viruses.
Martens J. M., Stokes H. S., Berg M. L., Walder K., Raidal S.R., Magrath M. J., Bennett A. T. (2020): A non-invasive method to assess environmental contamination with avian pathogens: beak and feather disease virus (BFDV) detection in nest boxes. PeerJ 8: e9211.
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Indirect transmission of pathogens can pose major risks to wildlife, yet the presence and persistence of wildlife pathogens in the environment has been little studied. Beak and feather disease virus (BFDV) is of global conservation concern: it can infect all members of the Psittaciformes, one of the most threatened bird orders, with infection often being lethal. Indirect transmission of BFDV through contaminated nest hollows has been proposed as a major infection source. However, data on whether and for how long nest sites in the wild remain contaminated have been absent. We determined the BFDV status of birds (parents and nestlings) for 82 nests of Crimson Rosellas, Platycercus elegans and Eastern Rosellas, Platycercus eximius. In 11 of these nests (13.4%, 95% confidence interval 6.9–22.7), we found an infected parent or nestling. Using nest swabs, we then compared BFDV presence at three points in time (before, during and after breeding) in three groups of nest boxes. These were nest boxes occupied by infected birds, and two control groups (nest boxes occupied by uninfected birds, and unoccupied nest boxes). Detection of BFDV on nest swabs was strongly associated with the infection status of parents in each nest box and with the timing of breeding. During breeding, boxes occupied by BFDV-positive birds were significantly more likely to have BFDV-positive nest swabs than boxes occupied by BFDV-negative birds; nest swabs tested BFDV-positive in 80% (28.4–99.5) of nests with parental antigen excretion, 66.7% (9.4–99.2) of nests occupied by parents with BFDV-positive cloacal swabs and 66.7% (22.3–95.7) of nests occupied by parents with BFDV–positive blood. 0% (0–52.2) of nests with BFDV–positive nestlings had BFDV–positive nest swabs. Across all boxes occupied by BFDV-positive birds (parents or nestlings), no nest swabs were BFDV–positive before breeding, 36.4% (95% CI 10.9–69.2) were positive during breeding and 9.1% (0.2–41.3) remained positive after breeding. BFDV was present on nest swabs for up to 3.7 months. Our study provides novel insights into the potential role of nest cavities and other fomites in indirect transmission of BFDV, and possibly other pathogens, and offers a non-invasive method for surveillance of pathogens in wild bird populations.
Oliveira B., Murray M., Tseng F., Widmer G. (2020): The fecal microbiota of wild and captive raptors. Animal Microbiome 2: 15.
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The microorganisms populating the gastro-intestinal tract of vertebrates, collectively known as “microbiota”, play an essential role in digestion and are important in regulating the immune response. Whereas the intestinal microbiota in humans and model organisms has been studied for many years, much less is known about the microbiota populating the intestinal tract of wild animals. The relatively large number of raptors admitted to the Tufts Wildlife Clinic on the Cummings School of Veterinary Medicine at Tufts University campus provided a unique opportunity to investigate the bacterial microbiota in these birds. Opportunistic collection of fecal samples from raptors of 7 different species in the orders Strigiformes, Accipitriformes, and Falconiformes with different medical histories generated a collection of 46 microbiota samples. Based on 16S amplicon sequencing of fecal DNA, large β-diversity values were observed. Many comparisons exceeded weighted UniFrac distances of 0.9. Microbiota diversity did not segregate with the taxonomy of the host; no significant difference between microbiota from Strigiformes and from Accipitriformes/Falconiformes were observed. In contrast, in a sample of 22 birds admitted for rehabilitation, a significant effect of captivity was found. The change in microbiota profile was driven by an expansion of the proportion of Actinobacteria. Based on a small number of raptors treated with anti-microbials, no significant effect of these treatments on microbiota α-diversity was observed. The concept of “meta-organism conservation”, i.e., conservation efforts focused on the host and its intestinal microbiome has recently been proposed. The observed effect of captivity on the fecal microbiota is relevant to understanding the response of wildlife to captivity and optimizing wildlife rehabilitation and conservation efforts.
Briscoe A. G., Nichols S., Hartikainen H., Knipe H., Foster R., Green A. J., Okamura B., Bass D. (2021): High‐Throughput Sequencing of faeces provides evidence for dispersal of parasites and pathogens by migratory waterbirds. Molecular Ecology Resources 22: 1303-1318.
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Examination of faecal material has demonstrated how a broad range of organisms are distributed by bird movements. Such research has largely focused on dispersal of plant seeds by frugivores and of freshwater organisms by waterbirds. However, with few exceptions (e.g. avian influenza, Ebola virus), there is a dearth of evidence for transport of parasites and pathogens. High-throughput sequencing methods now provide a powerful means of addressing this knowledge gap by elucidating faecal contents in unprecedented detail. We collected faeces excreted by a range of migratory waterbirds in south-west Spain and pooled faecal DNA to create libraries reflective of feeding behavior. We created sets of libraries using high-throughput metagenomic and amplicon sequencing. For the latter we employed two sets of primers to broadly target the V4 region of the 18S rRNA gene (one set amplifying the region across all eukaryotes, the other excluding amplification of metazoans). Libraries revealed a wide diversity of eukaryotes, including parasites of the faecal producers themselves, parasites of food items, or those incidentally ingested. We also detected novel microbial eukaryotic taxa and found that parasite assemblage profiles were relatively distinct. Comparing the performance of the methods used supports their joint use for future studies of diversity and abundance. Because viable stages of many parasites are likely to be present in faeces, our results suggest significant levels of bird-mediated dispersal of parasites (both from avian and other hosts). Our methods revealed much hidden biodiversity, and allowed identification of the individuals who produced the faecal samples to species level, facilitating the study of interaction networks.
Choi O. N., Corl A., Wolfenden A., Lublin A., Ishaq S. L., Turjeman S., Nathan R., Getz W. M., Bowie R. C., Kamath P. L. (2021): High-throughput sequencing for examining Salmonella prevalence and pathogen-microbiota relationships in barn swallows. Frontiers in Ecology and Evolution 9: 683183.
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Studies in both humans and model organisms suggest that the microbiome may play a significant role in host health, including digestion and immune function. Microbiota can offer protection from exogenous pathogens through colonization resistance, but microbial dysbiosis in the gastrointestinal tract can decrease resistance and is associated with pathogenesis. Little is known about the effects of potential pathogens, such as Salmonella, on the microbiome in wildlife, which are known to play an important role in disease transmission to humans. Culturing techniques have traditionally been used to detect pathogens, but recent studies have utilized high throughput sequencing of the 16S rRNA gene to characterize host-associated microbial communities (i.e., the microbiome) and to detect specific bacteria. Building upon this work, we evaluated the utility of high throughput 16S rRNA gene sequencing for potential bacterial pathogen detection in barn swallows (Hirundo rustica) and used these data to explore relationships between potential pathogens and microbiota. To accomplish this, we first compared the detection of Salmonella spp. in swallows using 16S rRNA data with standard culture techniques. Second, we examined the prevalence of Salmonella using 16S rRNA data and examined the relationship between Salmonella-presence or -absence and individual host factors. Lastly, we evaluated host-associated bacterial diversity and community composition in Salmonella-present vs. -absent birds. Out of 108 samples, we detected Salmonella in six (5.6%) samples based on culture, 25 (23.1%) samples with unrarefied 16S rRNA gene sequencing data, and three (2.8%) samples with both techniques. We found that sex, migratory status, and weight were correlated with Salmonella presence in swallows. In addition, bacterial community composition and diversity differed between birds based on Salmonella status. This study highlights the value of 16S rRNA gene sequencing data for monitoring pathogens in wild birds and investigating the ecology of host microbe-pathogen relationships, data which are important for prediction and mitigation of disease spillover into domestic animals and humans.
Lobos-Ovalle D., Navarrete C., Navedo J. G., Peña-Espinoza M., Verdugo C. (2021): Improving the sensitivity of gastrointestinal helminth detection using the Mini-FLOTAC technique in wild birds. Parasitology Research 120: 3319-3324.
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High-performance–validated tests are essential for successful epidemiological monitoring, surveillance of parasitic infections, and comparative studies in wildlife populations. The Mini-FLOTAC is a novel flotation–based technique for the sensitive detection and quantification of gastrointestinal parasites that is recently being explored for use in wildlife. A limitation of any flotation-based copromicroscopic method is the selection of the flotation solution (FS), which might influence the performance of the test. However, no study has compared the influence of using different FS in the Mini-FLOTAC technique for parasite detection in wild birds. Here, we evaluated the diagnostic performance of the Mini-FLOTAC in three waterbird host species using two widely used FS: saturated salt (NaCl; specific gravity 1.20) and saturated zinc sulfate (ZnSO4; specific gravity 1.35). One hundred fresh fecal samples were analyzed for parasite fecal egg counts (FEC). Regardless of the host species, fecal samples evaluated with the Mini-FLOTAC method using ZnSO4 resulted in a significantly higher detection rate and higher FEC of strongylid, capillarid, cestode, and trematode parasites, than samples analyzed with the NaCl solution. Our concise study demonstrated the importance of using an appropriate FS for the identification of parasite eggs in wildlife species, especially in hosts with an expected aggregated distribution and low parasite load such as waterbird hosts. The higher analytical sensitivity of the Mini-FLOTAC technique achieved with ZnSO4, and its applicability to fieldwork, highlights this method as a promising tool for the quantitative surveillance of parasite infections in wild bird populations.
Pekarsky S., Corl A., Turjeman S., Kamath P. L., Getz W. M., Bowie R. C., Markin Y., Nathan R. (2021): Drivers of change and stability in the gut microbiota of an omnivorous avian migrant exposed to artificial food supplementation. Molecular Ecology 30: 4723-4739.
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Human activities shape resources available to wild animals, impacting diet and probably altering their microbiota and overall health. We examined drivers shaping microbiota profiles of common cranes (Grus grus) in agricultural habitats by comparing gut microbiota and crane movement patterns (GPS-tracking) over three periods of their migratory cycle, and by analysing the effect of artificially supplemented food provided as part of a crane-agriculture management programme. We sampled faecal droppings in Russia (nonsupplemented, premigration) and in Israel in late autumn (nonsupplemented, postmigration) and winter (supplemented and nonsupplemented, wintering). As supplemented food is typically homogenous, we predicted lower microbiota diversity and different composition in birds relying on supplementary feeding. We did not observe changes in microbial diversity with food supplementation, as diversity differed only in samples from nonsupplemented wintering sites. However, both food supplementation and season affected bacterial community composition and led to increased abundance of specific genera (mostly Firmicutes). Cranes from the nonsupplemented groups spent most of their time in agricultural fields, probably feeding on residual grain when available, while food-supplemented cranes spent most of their time at the feeding station. Thus, nonsupplemented and food-supplemented diets probably diverge only in winter, when crop rotation and depletion of anthropogenic resources may lead to a more variable diet in nonsupplemented sites. Our results support the role of diet in structuring bacterial communities and show that they undergo both seasonal and human-induced shifts. Movement analyses provide important clues regarding host diet and behaviour towards understanding how human-induced changes shape the gut microbiota in wild animals.
Custer J. M., White R., Taylor H., Schmidlin K., Fontenele R. S., Stainton D., Kraberger S., Briskie J. V., Varsani A. (2022): Diverse single-stranded DNA viruses identified in New Zealand (Aotearoa) South Island robin (Petroica australis) fecal samples. Virology 565: 38-51.
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The South Island robin (Petroica australis) is a small passerine bird endemic to New Zealand (Aotearoa). Although its population has declined recently and it is considered ‘at risk,’ little research has been done to identify viruses in this species. This study aimed to survey the diversity of single-stranded DNA viruses associated with South Island robins in a small, isolated population on Nukuwaiata Island. In total, 108 DNA viruses were identified from pooled fecal samples collected from 38 individual robins sampled. These viruses belong to the Circoviridae (n = 10), Genomoviridae (n = 12), and Microviridae (n = 73) families. A number of genomes that belong to the phylum Cressdnaviricota but are otherwise unclassified (n = 13) were also identified. These results greatly expand the known viral diversity associated with South Island robins, and we identify a novel group of viruses most closely related genomoviruses.
Goossens E., Boonyarittichaikij R., Dekeukeleire D., Hertzog L., Van Praet S., Pasmans F., Bonte D., Verheyen K., Lens L., Martel A., Verbrugghe E. (2022): Tree species diversity and forest edge density jointly shape the gut microbiota composition in juvenile great tits (Parus major). Frontiers in Microbiology 13: 790189.
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Despite the microbiome’s key role in health and fitness, little is known about the environmental factors shaping the gut microbiome of wild birds. With habitat fragmentation being recognised as a major threat to biological diversity, we here determined how forest structure influences the bacterial species richness and diversity of wild great tit nestlings (Parus major). Using an Illumina metabarcoding approach which amplifies the 16S bacterial ribosomal RNA gene, we measured gut microbiota diversity and composition from 49 great tit nestlings, originating from 23 different nests that were located in 22 different study plots across a gradient of forest fragmentation and tree species diversity. Per nest, an average microbiome was determined on which the influence of tree species (composition and richness) and forest fragmentation (fragment area and edge density) was examined and whether this was linked to host characteristics (body condition and fledging success). We found an interaction effect of edge density with tree species richness or composition on both the microbial richness (alpha diversity: Chao1 and Shannon) and community structure (beta diversity: weighted and unweighted UniFrac). No significant short-term impact was observed of the overall faecal microbiome on host characteristics, but rather an adverse effect of specific bacterial genera on fledging success. These results highlight the influence of environmental factors on the microbial richness as well as the phylogenetic diversity during a life stage where the birds’ microbiota is shaped, which could lead to long-term consequences for host fitness.
Turjeman S., Pekarsky S., Corl A., Kamath P. L., Getz W. M., Bowie R. C., Markin Y., Nathan R. (2022): Comparing invasive and noninvasive fecal sampling in wildlife microbiome studies: A case study on wild common cranes. Molecular Ecology Resources 23: 359-367.
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In ecological and conservation studies, responsible researchers strive to obtain rich data while minimizing disturbance to wildlife and ecosystems. We assessed if samples collected noninvasively can be used for faecal microbiome research, comparing microbiota of noninvasively collected faecal samples to those collected from trapped common cranes at the same sites over the same periods. We found significant differences in faecal microbial composition (alpha and beta diversity), which likely did not result from noninvasive sample exposure to soil contaminants, as assessed by comparing bacterial oxygen use profiles. Differences might result from trapped birds’ exposure to sedatives or stress. We conclude that if all samples are collected in the same manner, comparative analyses are valid, and noninvasive sampling may better represent host faecal microbiota because there are no trapping effects. Experiments with fresh and delayed sample collection can elucidate effects of environmental exposures on microbiota. Further, controlled tests of stressing or sedation may unravel how trapping affects wildlife microbiota.
Rohrer S. D., Jiménez-Uzcátegui G., Parker P. G., Chubiz L. M. (2023): Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen. Scientific Reports 13: 5358.
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Microbial colonization plays a direct role in host health. Understanding the ecology of the resident microbial community for a given host species is thus an important step for detecting population vulnerabilities like disease. However, the idea of integrating microbiome research into conservation is still relatively new, and wild birds have received less attention in this field than mammals or domesticated animals. Here we examine the composition and function of the gut microbiome of the endangered Galapagos penguin (Spheniscus mendiculus) with the goals of characterizing the normal microbial community and resistome, identifying likely pathogens, and testing hypotheses of structuring forces for this community based on demographics, location, and infection status. We collected fecal samples from wild penguins in 2018 and performed 16S rRNA gene sequencing and whole genome sequencing (WGS) on extracted DNA. 16S sequencing revealed that the bacterial phyla Fusobacteria, Epsilonbacteraeota, Firmicutes, and Proteobacteria dominate the community. Functional pathways were computed from WGS data, showing genetic functional potential primarily focused on metabolism—amino acid metabolism, carbohydrate metabolism, and energy metabolism are the most well-represented functional groups. WGS samples were each screened for antimicrobial resistance, characterizing a resistome made up of nine antibiotic resistance genes. Samples were screened for potential enteric pathogens using virulence factors as indicators; Clostridium perfringens was revealed as a likely pathogen. Overall, three factors appear to be shaping the alpha and beta diversity of the microbial community: penguin developmental stage, sampling location, and C. perfringens. We found that juvenile penguins have significantly lower alpha diversity than adults based on three metrics, as well as significantly different beta diversity. Location effects are minimal, but one site has significantly lower Shannon diversity than the other primary sites. Finally, when samples were grouped by C. perfringens virulence factors, we found dramatic changes in beta diversity based on operational taxonomic units, protein families, and functional pathways. This study provides a baseline microbiome for an endangered species, implicates both penguin age and the presence of a potential bacterial pathogen as primary factors associated with microbial community variance, and reveals widespread antibiotic resistance genes across the population.