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Meals & nutrition

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Roman Young
Roman Young

New World Vulture

Order:CathartiformesFamily:Cathartidae Species on page - 6 out of 7 species in 5 out of 5 genera depicted Turkey vulture (Cathartes aura) Lesser yellow-headed vulture (Cathartes burrovianus) Black vulture (Coragyps atratus) California condor (Gymnogyps californianus) King vulture (Sarcoramphus papa) Andean condor (Vultur gryphus)Old World Vultures - Order: Accipitriformes

new world vulture

Vultures are scavengers that fill a key ecosystem niche, in which they have evolved a remarkable tolerance to bacterial toxins in decaying meat. Here we report the first deep metagenomic analysis of the vulture microbiome. Through face and gut comparisons of 50 vultures representing two species, we demonstrate a remarkably conserved low diversity of gut microbial flora. The gut samples contained an average of 76 operational taxonomic units (OTUs) per specimen, compared with 528 OTUs on the facial skin. Clostridia and Fusobacteria, widely pathogenic to other vertebrates, dominate the vulture's gut microbiota. We reveal a likely faecal-oral-gut route for their origin. DNA of prey species detectable on facial swabs was completely degraded in the gut samples from most vultures, suggesting that the gastrointestinal tracts of vultures are extremely selective. Our findings show a strong adaption of vultures and their bacteria to their food source, exemplifying a specialized host-microbial alliance.

The microbiota of vertebrates rapidly begin to decompose their hosts after death1. During the subsequent breakdown of tissue, these microorganisms excrete toxic metabolites, rapidly rendering the carcass a hazardous food source for most carnivorous and omnivorous animals2. Some scavengers such as vultures, however, are able to consume carrion without suffering any apparent ill-effects. Indeed, vultures may have to wait for decay to occur before they are able to scavenge carcasses with tough skins, thus substantially increasing the risk of exposure to toxins3. Furthermore, to obtain access to the inside of such carcasses, they often insert their heads directly in the body cavities of decaying prey, thereby exposing their head and neck to pathogenic bacteria3. Although the majority of the ingested bacteria will not survive the acidic gastric passage before hindgut colonization, toxins such as botulinum survive the passage into the hindgut, possibly seriously compromising the health of the consumer4. Furthermore the pioneering feeding experiments of Houston and Cooper revealed that spore forming pathogens such as Bacillus anthracis can be recovered from vulture faeces5.

To investigate how vultures are able to tolerate this challenging dietary niche, here we characterize the functional microbiome of the facial skin and the hindgut (large intestine) of the two most widespread species of vultures in the New World (Coragyps atratus (black vulture) n=26; Cathartes aura (turkey vulture) n=24; both collected in Nashville, USA). We show that the acidic gastrointestinal tract of vultures is a strong filter of the microbiota ingested from decaying carcasses resulting in a significantly less diverse hindgut flora dominated by Clostridia and Fusobacteria, which are pathogenic to most vertebrates.

There was no significant difference in the percentage of Clostridia on facial swabs from black vultures (min=7% and max=40%, ) and turkey vultures (min=8% and max=68%, ; Wilcoxon, P>0.05). Percentages of Fusobacteria were similar on the facial skin of black vultures (0% and max=31%, ) and turkey vultures (min=0.2% and max=23%, , Wilcoxon, P>0.05) as shown in Fig. 2a and Supplementary Table 2 (see also observed genera in Supplementary Table 3). Although no comparable studies of facial skin microbiomes are available for comparison, these observations are unusual with regard to available vertebrate facial microbiomes, such as those of human (predominantly Actinobacteria), frogs (predominately Actinobacteria and Betaproteobacteria) and salamander (predominately Betaproteobacteria)11,12. Fusobacteria have not been reported on human skin. Clostridia on the other hand have been found to colonize parts of the human skin with lowered oxygen availability, for example the buttocks, but not the face12,13.

(a) Mean bacterial class distribution found on facial skin and in the hindgut of black and turkey vultures (see details in Supplementary Notes 1 and 2). (b) Comparison of microbial communities of zoo bird faeces and vulture hindguts (UPGMA tree based on Unifrac metric). The hawk, owl and vultures in the zoo received fresh meat. (Microbial composition of zoo bird faeces is given in Supplementary Note 3). *Clades collapsed.

To explore which components of the hindgut microbiome are unique to vultures, we generated additional avian metagenomic data using faecal samples obtained from several other species from a single location (Copenhagen Zoo). Samples included two captive-bred turkey vultures, three predatory species (red-tailed hawk (Buteo jamaicensis), African spotted owl (Bubo africanus), and red-legged seriema (Cariama cristata)), a non-predatory Amazon parrot (Amazona sp.) and the American flamingo (Phoenicopterus ruber). Recent studies of human gut dynamics have demonstrated that the gut microbiome can rapidly adjust to dietary modifications15. In addition, the gut microbiota of alligators has been observed to vary seasonally with diet16. It is notable that despite having similar diets in the zoo, the faecal microbiome of the zoo-kept turkey vultures was considerably different from those of the hawk and owl (Fig. 2b, Supplementary Tables 5 and 6), but remarkably similar to the hindgut microbiome of the wild sampled vultures. This indicates that phylogenetic differences in the digestive physiology of vultures override the importance of diet in the assembly of the hindgut microbiota.

The frequency of Clostridia and Fusobacteria (Fig. 3a) in the hindgut raises the question of whether these bacteria simply outcompete other bacterial groups or if their presence is actually promoted for the physiological benefit of the vultures. The former option suggests that vultures are passive hosts that tolerate the bacteria and their toxins without receiving benefit, whereas the latter posits that the relationship is more mutualistic in that bacteria receive a predictable flow of protein-rich food in an anaerobic environment and the vultures obtain nutrients provided by bacterial degradation of carrion. Indeed we observed genes that encode tissue-degrading enzymes and toxins associated with Clostridium perfringens in the metagenome of the turkey vulture hindgut with shotgun sequencing (Supplementary Table 7).

Curiously, more than 90% of all microbial interactions in the hindguts of both vulture species (Fig. 3b,c) were of a positive nature. However, all negative co-occurrence interactions were assigned to either Clostridia and/or Fusobacteria, suggesting their competitive nature.

Therefore, the most likely scenario is that Clostridia and Fusobacteria outcompete other bacterial groups in the anaerobic hindgut, and that vultures benefit from the bacterial breakdown of carrion while tolerating bacterial toxins. Some scavenging birds are known to harbour antibodies against toxins such as botulinum24 and we speculate that vultures are unusually tolerant of toxins.

In summary, our findings demonstrate that wild vultures host a similar but very unique gut microbiome that is dominated by two major groups of bacteria that likely originate from their food sources. To determine essential functions of vulture homeostasis contributed by the gut microbiota, germ-free vultures will need to be experimentally exposed to the microbes observed in this study, using mammalian investigations as a model25.

We thank Brian Schmidt and Christina Gebhard (both Smithsonian Institution) for necropsying vultures; Blaine Hyle, Talon Redding, William Simmons and J.D. Freye (all USDA) for collecting vultures; and Keith Wehner, Blaine Hyle and Brett Dunlap (all USDA) for providing critical logistic support in Nashville. The Alexander Wetmore Fund of the Smithsonian Institution provided funding for fieldwork. G.R.G. thanks the Smoketree Trust for support. M.R. acknowledges the financial support of a PhD scholarship from the Center for Environmental and Agricultural Microbiology (CREAM) in Copenhagen, Denmark. L.H.H. thanks the Lundbeck grant no. R44-A4384. M.T.P.G. acknowledges the Lundbeck grant no. R52-A5062. Furthermore, we thank Nina Christiansen and Lillian Anne Petersen, from the Danish National High-Throughput DNA Sequencing Centre, who constructed the 16S rRNA gene amplicon and the shotgun metagenomic libraries. We also thank Gisle Vestergaard (Section for microbiology, University of Copenhagen) and Shaun Nielsen (UNSW, Sydney, Australia) for analytical support. Last but not least, we thank Jessica Metcalf, Tony Walters and Juan Manuel Peralta Sanchez from the Rob Knight lab for helpful discussion.

M.R. and L.H.H. analysed the microbial survey and are the main authors of this manuscript. M.R., L.H.H. and M.T.P.G. generated the microbial data. I.B.S., and M.T.P.G. profiled the mammalian dietary composition. N.B., J.B. and T.S.P. did the metagenomic analysis. The sampling was performed by G.R.G. (wild vultures) and M.F.B. (zoo samples). S.J.S. helped interpret the data. This project was conceived and designed by G.R.G., M.T.P.G. and L.H.H. All the authors have read and understood the manuscript.

All vultures have a wide wingspan, which allows them to soar for long periods of time without flapping so much as a feather while looking for carrion to eat. They all have a sharp, hooked beak for ripping apart meat. Vultures are large compared to other birds. Their bald head and neck serve a useful purpose, allowing vultures to steer clear of infection and tangled feathers when eating decaying meat. A strong immune system allows vultures to eat rotting and possibly infected meat without getting sick. 041b061a72

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