Introduction
Pigeon, the coarse diagnose for birds of the taxonomic family Columbidae and the arrange Columbiformes, is an all-important economic animal that provides kernel and eggs for humans. After fertilized eggs are incubated for 28 days, the squab hatch. Pigeons are altricial, meaning that newly-hatched squabs are ineffective to feed independently ; they must be fed “ pigeon milk ” ( PM ) in a mouth-to-mouth manner to survive. For most domestic fowl, the crop plays the role of impermanent food storage, but in pigeons, the crop acts as an organ that produces pigeon milk for squab, in addition to storing food ( Gillespie et al., 2011 ). fair as mammals lactate for their young, parent pigeons regurgitate pigeon milk from their crops to feed the squab ( Luo et al., 2017 ). Unlike mammals, both male and female pigeons produce pigeon milk ( Gillespie et al., 2012 ). Pigeon milk contains protein ( 60 % ), fat ( 32–36 % ), carbohydrate ( 1–3 % ), minerals ( calcium, potassium, sodium, and morning star ), and antibodies ( Davies, 1939 ; Kocianova et al., 1993 ). Up to 7 days of old age, squabs chiefly trust on pigeon milk to obtain nutrients, while between 8 and 14 days of senesce, the pigeon milk includes a large sum of food initially digested by their parents ( Horseman and Buntin, 1995 ). Because of this special prey convention, the act of pigeon ’ mho offspring and their survival rate are very low, which makes it difficult for the pigeon industry to achieve intensifier reproduction. Although researchers want to improve the industrialization of pigeons by producing artificial pigeon milk, the components and values of artificial pigeon milk are silent limited because most of the studies merely focused on the nutrition and immune officiate of pigeon milk ( Goudswaard et al., 1979 ; Shetty et al., 1994 ). consequently, the efficiency of the pigeon breeding industry remains low due to poor people understand of pigeon milk constitution, particularly regarding the microbiota in pigeon milk ( Shetty et al., 1990 ) .
There is a symbiotic relationship between microbiota and their hosts ( Rees et al., 2018 ; Dietz et al., 2019 ). The independent profit of microbe was to obtain a relatively stable habitat and adequate food source ( Kohl, 2012 ; McFall-Ngai et al., 2013 ). meanwhile, microbes play an authoritative character in many aspects of host physiology, including nutrition, metabolism, and intestinal homeostasis ( Walker et al., 2017 ). early colonization of microbiota can have long-standing consequences on server such as determining the production of necessity metabolites which facilitate postnatal development and enhance immune function ( Lee and Mazmanian, 2010 ; Funkhouser and Bordenstein, 2013 ; Gensollen et al., 2016 ; Stinson et al., 2017 ). Neonates of mammals can acquire enate microbiota through the placenta, amniotic fluent, vagina, and front milk ( DiGiulio et al., 2008 ; Satokari et al., 2009 ; Albesharat et al., 2011 ; Stout et al., 2013 ; Aagaard et al., 2014 ). The prenatal exposure is an important step in modulating the embryonic growth and the growth of immune system ( Nylund et al., 2014 ). Fetuses are highly susceptible to disease infections, not lone because their green immune system is less adequate to of generating adaptive immune effectors, such as antibodies, but besides because they lack divers commensalmicrobiota that can antagonize pathogens independently of host responses ( Basha et al., 2014 ; Simon et al., 2015 ; Zheng et al., 2020 ). Although the chicken embryo is isolated from the mother, the effect microbial colonizers of enate hens can be transmitted to the embryo in the serve of fertilization and egg formation in the fallopian tube ( Ding et al., 2017 ). Likewise, prenatal bacteria transfer may occur in other birds. The relatively senior high school percentage of shared operational taxonomic units ( OTUs ) between neonates and females is a solid indication that neonates of rock pigeons obtain bacteria through prenatal transfer ( Dietz et al., 2019 ). Research has shown that lactobacillus is important in maintaining a goodly microbial counterweight in the chicken crop ( Fuller, 1977 ), but american samoa regard to crop secretions, it is not known the pigeonmilkmicrobial typography and affair, and whether these microbes can be transmitted from rear pigeons to squabs .
In this sketch, we adopted new generation high throughput sequencing engineering to analyze the composition and serve of microbiota in pigeon milk and pigeon intestines at unlike developmental stages.
Reading: The Composition and Function of Pigeon Milk Microbiota Transmitted From Parent Pigeons to Squabs
Materials and Methods
Animal and Sample Collection
The pigeons to be sampled were selected from the Shanghai Xinrong Big Emperor Pigeon Breeding Professional Cooperative. A sum of 24 pigeons were selected, including 12 parent pigeons who were 2 years old and having similar burden and size, and 12 squabs of different ages [ 4 each at 1-day ( D1 ), 5-day ( D5 ), and 10-day ( D10 ) of historic period ; Figure 1A and Supplementary Figure 1A ]. Samples of parent and squab pigeons were collected on the lapp day ( Figure 1B and Supplementary Figure 1B ). In holy order to reduce the impact of environmental factors and verify its potency, we conducted effective experimental controls on the management and run of the pigeons, as manifested by the fact that all individuals were kept under the same ceiling, the rear pigeons are raised in the lapp cage with their offspring, and the feed recipe of the parent pigeons was coherent. routine feed procedures were followed for feeding management, and the subjects had unblock access to food and body of water. none of the selected pigeons had been exposed to antibiotics within a month. All experiments on these animals were conducted in accordance with the animal benefit protection provisions of the Shanghai Jiao Tong University. We collected 48 samples in sum, which consisted of 12 rear pigeon milk samples and 12 intestine content ( PG ) samples from rear pigeons, 12 crop capacity samples [ referred to as “ squab milk ” ( SM ) ] and 12 intestine content ( SG ) samples from squab. Pigeon milk and gut capacity were collected individually with sterile tweezers and were placed into aseptic centrifuge tube. The procedures of sample distribution collection and subsequent operation were carried out on a houseclean terrace under aseptic conditions. The samples were immediately stored at −80°C after collection .
FIGURE 1 
Figure 1. Aggregate squab milk microbiota composing and function. (A) The squab at 1-day ( D1 ), 5-day ( D5 ), and 10-day ( D10 ). (B) Morphology of squab milk at different developmental stages. (C) distribution of the squab milk microbiota among different developmental stages at the genus level. only major taxonomic groups are shown. (D) Dynamic distribution of squab milk microbiota at unlike developmental stages shown by principal component analysis ( PCA ) plot. (E) The running pathways of squab milk microbiota. only major pathways are shown.
DNA Extraction and 16S rRNA Gene Sequencing
The TIANGEN DNA stool mini kit out ( TIANGEN, kat # DP328 ) was used for microbial genome DNA extraction from pigeon milk and intestine subject samples, following the manufacturer ’ second instructions. The DNA quantity and quality were assessed by a Nanodrop spectrophotometer ( Thermo scientific, United States ). The V3–V4 hypervariable area of the 16S rRNA gene was amplified by PCR using sample-specific sequence barcoded fusion primers : ahead primer 338F ( 5′-ACTCCTACGGGAGGCAGCA-3 ‘ ), and reverse fuse 806R ( 5’‐ GGACTACHVGGGTWTCTAAT-3 ‘ ). The PCR reaction conditions and product refining were performed as former publication ( Zhao et al., 2013 ). 16S rRNA gene sequence of 48 samples was carried out using Illumina MiSeq ( Illumina, United States ) by the Shanghai Personal Biotechnology Limited Company, Shanghai, China. Our sequence reads quality control criteria were as follows : the reads with mean quality higher than 30, no ambiguous bases, sequence duration longer than 150 bp, no chimera, no adapter contaminations, and no master of ceremonies corrupting. The genome was assembled by the trickle sequences according to the overlap longer than 10 bp between read 1 and read 2 and without mismatches. Trimmed sequences were upload to QIIME for promote analysis. The deoxyribonucleic acid sequences are publicly available in Metagenome Rapid Annotation using Subsystem Technology ( MG-RAST ) under the stick out diagnose “ pigeon-milk-microbiota ” .
Taxonomy Classification and Statistical Analysis
Using QIIME V.1.9.1, we merged, apply quality master, and clustered the 16S rRNA gene reads into OTUs. Taxonomic groups were based on the GreenGene Database V.13_8 using closed references to perform reference-based OTU cluster ( Edgar, 2010 ; McDonald et al., 2012 ). OTUs that were present in at least 12 samples were used for the adjacent tone. The OTU abundance counts were log2 transformed and normalized by subtracting the mean of all transformed values and separate by the standard deviation of all log-transformed values for the given sample. In the end, the abundance profiles for 48 samples exhibited a mean of 0 and a standard deviation of 1. Normalized abundance was used to perform statistical analyses. Values employed for alpha diversity ( Chao1 index, Shannon index, and Simpson index ) and beta diverseness [ non-metric multidimensional scaling ( NMDS ; weighted UniFrac outdistance metrics ) and principle component analysis ( PCA ) ] were generated by QIIME V.1.9.1 The Venn diagrams were generated using mothur ( Schloss et al., 2009 ). Box plots and banish charts were created by SigmaPlot ( Kornbrot, 2000 ). Two-side Welch ’ s t -test and multiple comparisons were applied to identify different taxa microbes among groups. All values of p were adjusted using the Benjamini–Hochberg method. In the figures and tables, p < 0.05 indicates statistical meaning ( * p < 0.05, * * p < 0.01 ; Benjamini and Hochberg, 1995 ). statistical analyses and data visual image were performed using R V.3.5.0 ( under RStudio V.1.1.453 ; Dessau and Pipper, 2008 ) and STAMP ( Parks and Beiko, 2010 ). microbial functions were predicted using 16S rRNA gene sequence data by PICRUSt ( Langille et al., 2013 ). The OTUs were mapped to gg13.5 database at 97 % similarity by QIIME ’ randomness command “ pick_closed_otus. ” The OTUs abundance was normalized automatically using 16S rRNA gene transcript numbers from known bacterial genomes in integrate microbial genomes. The predict genes and their functions were aligned to the Kyoto Encyclopedia of Genes and Genomes ( KEGG ) database, and differences among groups were compared through software STAMP .
Results
The Squab Milk Microbial Characteristics and Dynamic Distribution at Different Developmental Stages
Twelve squab milk samples from the craw content of squabs were collected. As in former studies ( Horseman and Buntin, 1995 ), we besides found that the early milk of squab is bum, and late milk contains undigested food from their parents ( Figure 1B and Supplementary Figure 1 ). A full of 550,696 high quality reads were yielded from 12 squab milk samples by 16S rRNA gene sequencing. On average, 45,891 reads per sample distribution were classified into unlike taxonomies and diversity analyses. Based on the results of OTUs, 8 phylum, 96 genus, and 114 species of microbiota were recorded. The most abundant phylum was Firmicutes ( 67 % ), followed by Actinobacteria ( 27 % ), Bacteroidetes ( 4 % ), and Cyanobacteria ( 2 % ) in squab milk ( auxiliary Figure 2A ). Correspondingly, the dominant allele microbial genus were Lactobacillus, Bifidobacterium, Aeriscardovia, and Veillonella ( Figure 1C ). Beta diverseness suggested the active changes of these microbes in the squab milk at different developmental stages ( D1, D5, and D10 ; Figure 1D ). PCA showed that the microbiota were clustered at similar developmental stages. The phylogenetic distance of the first gear sidereal day microbiota significantly diverged from the 10-day in squab milk, and the 5-day microbial phylogenetic distance was associated with both ( Figure 1D ). At the genus degree, the microbial writing differed among the different developmental stages. As the squab ’ randomness development with meter, we observed that the proportions of the genus changed. Among the 96 genus, statistical analysis found that 38 of them were prominently different with time ( p < 0.05 ; Supplementary Table 1 ). The most abundant genus carried by squab milk was Lactobacillus, which showed a significantly increasing vogue according to developmental stages ( p < 0.01 ). At D1, the percentage of Lactobacillus was 33 %, which increased to 68 % at D5 and to 87 % at D10 ( Figure 1C ). Unclassified_Streptophyta besides perceptibly raised from 0.05 % ( D1 ) to 3.42 % ( D10 ) ( p < 0.01 ; supplementary Figure 2B ). In contrast, Bifidobacterium, Veillonella, and Prevotella diminished with emergence. Bifidobacterium decreased from 30 % ( D1 ) to 14 % ( D5 ) and to 3 % ( D10 ; Figure 1C ). Veillonella and Prevotella were besides markedly ranged between different developmental stages ( p < 0.01 ; Supplementary Table 1 ). The rate at which the genus increased from D1 to D5, and then had decreased at D10, corresponded with the proportion of Aeriscardovia ( 7, 15, and 9 % ; Figure 1C ). To promote investigate the functions of squab milk microbiota, we used PICRUSt to produce predict microbial functional pathways from 16S rRNA gene sequence data ( Figure 1E ). From this analysis, we observed that most of the squab milk microbes are involved in the pathways of membrane ecstasy, rejoinder and compensate, carbohydrate metamorphosis, amino acerb metabolism, and energy metabolism, which are authoritative to emergence and development of the organism ( Figure 1E and Supplementary Table 2 ) .
Microbiota Can Be Transmitted From Parents to Squabs by Pigeon Milk
To explore the origin of pigeon milk microbiota, we surveyed milk microbial musical composition and diversity between rear pigeon milk and squab milk ( Figure 2 ). Five phylum – Firmicutes, Actinobacteria, Proteobacteria, Bacteroidetes, and Cyanobacteria – were salute as major components in pigeon milk ( Figure 2A ). The pigeon milk genus in parent pigeons were dominated by Lactobacillus, Enterococcus, Veillonella, and Bifidobacterium ( 42, 9, 9, and 8 %, respectively ; Figure 2A ). analysis of squab milk showed that Lactobacillus besides accounted for a considerable proportion, 61 %, followed by Bifidobacterium, Aeriscardovia, and Veillonella, at 15, 10, and 4 %, respectively ( Figure 2A ). The increasing drift of Lactobacillus
FIGURE 2
Figure 2. Comparison and statistical psychoanalysis of microbiota between parent pigeon milk ( PM ) and squab milk ( SM ). (A) The distribution of the microbiota for PM and SM. (B) non-metric multidimensional scale ( NMDS ; weighted UniFrac distance ) plot. (C) Alpha diversity analysis by Shannon exponent.
table 1
Table 1. significant differences of pigeon milk microbial genus abundance between PM and SM ( p < 0.05 ).
Gut Microbial Characteristics of Parent Pigeons and Squabs
similar to pigeon milk, the dominant phylum of pigeon gut microbiota were Firmicutes ( 71 % ), Actinobacteria ( 12 % ), and Proteobacteria ( 12 % ; Supplementary Figure 4 ). We besides studied the bearing of gut microbiota between parent pigeons ( PG ) and squabs ( SG ) at the genus level. The catgut communities of rear pigeons were largely dominated by Turicibacter, Lactobacillus, and Enterococcus ( Figure 3A ). As expected, other bacteria made up a relatively little fraction of the overall community, with Lactobacillus ( 47 % ) and Bifidobacterium ( 10 % ) being the prevailing beneficial bacteria in squab ’ catgut ( Figure 3A ). NMDS based on leaden UniFrac distance revealed a significant separation of samples, indicating that the gut microbial communities of parent pigeons and squabs are different ( Figure 3B ). The intestine community diversity was reflected by a reduction of the Simpson index from rear pigeons to squabs ( Figure 3C ). The significant differences in residential district structure were besides apparent from the proportional proportion of unlike taxonomic group across the groups ( p < 0.05 ; Supplementary Table 3 ). Eight genus showed markedly unlike between the gut microbiota of rear pigeons and squabs, with a clean increase in the proportional abundance of Lactobacillus and Bifidobacterium, and a decrease in Turicibacter and Enterococcus in squab, proportional to parent pigeons ( Figure 3D ). The significant difference of gut microbiota between parent pigeons and squabs may be demonstrated that the intestinal microbial structure of squab was affected by the squab milk microbiota .
FIGURE 3 
Figure 3. Pigeon intestine microbial characteristics and distribution. (A) Parent pigeon intestine ( PG ) and squab gut ( SG ) microbiota constitution at the genus level. (B) Gut microbial beta diversity of pigeons with a NMDS plot. (C) Simpson calculator to exhibit the different community diversities in PG and SG. (D) significantly unlike gut microbes between PG and SG.
The Comparison of Microbial Composition and Function Between Parent Pigeon Milk and Gut
In club to investigate which microbe of rear pigeons will be transmitted to their offspring, we compared the gut microbiota ( PG ) and the milk microbiota ( PM ) in parent pigeons. The phylum of Firmicutes, Proteobacteria, and Actinobacteria were common in PG and PM ( supplementary Figure 5 ). But the Bacteroidetes and Cyanobacteria are bountiful in pigeon milk, and Tenericutes was the dominant allele microbial phylum of the pigeon gut. At the genus floor, 12 bacteria genus showed a significant deviation between the pigeon milk microbiota and intestine microbiota ( p < 0.05 ; Supplementary Table 4 and Figure 4A ). The overriding genus in pigeon milk were Lactobacillus ( 42 % ), Enterococcus ( 9 % ), Veillonella ( 9 % ), and Bifidobacterium ( 8 % ), while the pigeon gut was dominated by Turicibacter ( 20 % ), Lactobacillus ( 13 % ), Unclassified_Clostridiaceae ( 12 % ), Enterococcus ( 12 % ), and Unclassified_Mollicates ( 9 % ; Supplementary Figure 6 ). The abundances of Gallibacterium, Veillonella, and Lactobacillus in pigeon milk were about seven-, four-, and double higher than that in pigeon intestine, respectively ( Supplementary Table 4 ). however, some bacteria associated with inflammation, such as Turicibacter and Clostridium unusually enriched in pigeon gut microbiota ( Supplementary Table 4 ). Faced with a complex microbial structure, parent pigeons may select some beneficial and valuable microbes to transfer to the squab. furthermore, based on the psychoanalysis of the microbial 16S rRNA gene sequencing data, we discovered that the abundant microbes in pigeon milk were frequently involved in the functional pathways of energy metabolism, digestive system, metamorphosis of cofactors and vitamins, glycan biosynthesis and metamorphosis, nucleotide metamorphosis, and so on ( Figure 4B ). Compared with pigeon milk, the microbial pathways of immune system, environmental adaptation, and neurodegenerative diseases were abundant in the pigeon gut ( Figure 4B ) .
FIGURE 4 
Figure 4. The analysis of the catgut microbiota ( PG ) and the milk microbiota ( PM ) in parent pigeons. (A) Heatmap of hierarchy cluster results for the microbiota of PG and PM at the genus degree. (B) meaning differences of microbial metabolic pathways for PG and PM.
Discussion
pigeon is one of the few birds adequate to of regurgitating pigeon milk to nourish young squab, which can not eat independently like other poultry due to their belated maturity. similar to mammalian breast milk ( Boix-Amorós et al., 2016 ), pigeon milk is highly alimentary, consisting of protein, fat, carbohydrates, and minerals ( Xie et al., 2019 ). interestingly, we found a mass of microbiota in pigeon milk in this learn ( Figure 2A ). furthermore, the pigeon milk microbiota can be transmitted from parents to squabs. It implies that pigeons not only transfer nutrients, but besides microbiota to squabs by pigeon milk to help them cope with the building complex live environment. Analyzing the microbial KEGG pathway suggested that galactose, starch, and sucrose metamorphosis belonging to carbohydrate metabolism were perceptibly higher in squab milk than in parent pigeon milk ( Supplementary Table 5 ). Galactose is a key informant of energy and peculiarly crucial for early homo development ( Coelho et al., 2015 ). The galactose and sucrose metamorphosis present in milk is a determinant factor in neonatal horde defense and incendiary processes due to their prebiotic effect and is an crucial source of energy in infants ( Mills et al., 2011 ). Genomic psychoanalysis of probiotics from infants besides has revealed specific familial venue related to milk oligosaccharide import and process, suggesting coevolution between the human host, milk oligosaccharide, and the microbes they enrich ( Chichlowski et al., 2011 ). We besides found bountiful probiotics in squab milk ( Figure 1C ), which are able to consume human milk oligosaccharides ( Ward et al., 2006 ; Thongaram et al., 2017 ). consequently, the high abundance of carbohydrate metabolism in squab milk echoed with the presence of electric potential probiotics, and besides implied that the universe of milk microbiota could assist the host by metabolizing nutrients ( Ballini et al., 2019 ). Taken together, our studies suggested that rear pigeons help their offspring grow by transferring the microbiota via pigeon milk .
There were abundant Lactobacillus and Bifidobacterium in squab milk ( Figure 1C ), which implied that they could be crucial probiotics associated with growth and development of individuals of squab. In animals, oral presidency of Bifidobacterium or Lactobacillus has had useful effects in newborn calves and piglets, including improved body weight profit, tip conversion, and faecal condition ( Abe et al., 1995 ). Lactobacillus and Bifidobacteria can be detected in breast milk after oral supplement in the mother and in about all infants after oral supplementation during the first class of biography, vitamin a well as occasionally in many untreated infants ( Abrahamsson et al., 2009 ; Fernandez et al., 2013 ). When the squab grow older, pigeon milk is mix with grains soaked in the crop of the parents and is gradually replaced by grains only ( Vandeputte-Poma, 1980 ). The universe of Lactobacillus and Bifidobacteria may be related to the changes of pigeon milk musical composition thus as to protect gastrointestinal tract health of squab ( Figure 2A ). It has been discovered that live Lactobacillus strains could enhance the barrier serve of naïve epithelial cells which are not exposed to any pathogen and alleviate the diarrhea in mouse ( Resta-Lenert and Barrett, 2003 ; Wang et al., 2019 ). notably, we besides detected bountiful functional pathways, including butirosin and neomycin biosynthesis, biosynthesis of vancomycin group antibiotics, dioxin degradation, and xylene abasement in squab milk ( Supplementary Table 5 ). This may indicate that the milk microbiota were involved in the immune system of squab. Immune-modulating research has suggested that Lactobacillus and Bifidobacterium show a genus-specific ability to modulate in vitro unconditioned unsusceptibility, antimicrobial bodily process against gut pathogens, and reducing colitis and ignition ( Liévin-Le and Servin, 2014 ; Luongo et al., 2017 ; Inchingolo et al., 2019 ). Moderate prenatal stress was sufficient to decrease the numbers of Lactobacillus and Bifidobacterium in neonate baby monkey. This change could result in heighten susceptibility to infection and suggest a mechanism for some effects of maternal pregnancy conditions on baby health ( Bailey et al., 2004 ). Since a mass of antibiotics biosynthesis pathways was discovered in squab milk ( Supplementary Table 5 ), in agreement with the fact that probiotics are involved in immune system to prevent disease infections ( Rosenberg et al., 2016 ). According to previous report, squabs are easily died or fail to thrive if they fed a nutritional substitute of pigeon milk ( Guareschi, 1936 ). consequently, it is reasonable to presume that the probiotics was an all-important factor in the growth and development of squab. During pigeon engender, adding probiotics and changing the proportion of probiotics in artificial pigeon milk with the development stages may improve the survival rate of squab and promote the production performance of pigeon .
Conclusion
This sketch investigates the microbial composition and function in pigeon milk and pigeon intestines. We found abundant microbiota in pigeon milk, which are dominated by the phylum of Firmicutes and the genus of Lactobacillus and Bifidobacterium. The squab milk microbial abundance changes dynamically with emergence and exploitation stages, and besides related to the changes of microbiota in rear pigeons among different developmental stages. furthermore, microbiota can be transmitted from parents to squabs by pigeon milk. The overriding genus of parent pigeon milk, such as Lactobacillus, are besides accounted for a considerable proportion in squab milk. In addition, the intestinal microbial social organization of pigeon was affected by the pigeon milk microbiota. Our results indicates that microbiota play an important function in squabs and can be transmitted from rear pigeons to squabs by pigeon milk, and besides remind us to consider adding probiotics to the artificial pigeon milk to promote the exploitation of the pigeon industry .
Data Availability Statement
The datasets presented in this study can be found in on-line repositories. The names of the repository/repositories and accession number ( second ) can be found at : hypertext transfer protocol : //www.mg-rast.org/mgmain.html ? mgpage=project & project=mgp93364, pigeon-milk-microbiota ( mgp93364 ) .
Ethics Statement
The animal study was reviewed and approved by The Institute for Laboratory Animal Research ( ILAR ) Guide for Care and Use of Laboratory Animals in Shanghai Jiao Tong University .
Author Contributions
JD wrote the manuscript. JD, NL, and HM conceived and designed the experimental procedure. JD, NL, YZ, and LY collected samples and extracted DNA. JD performed statistical analysis and data march. HZ, KX, CH, CQ, CT, and LW coordinated sample solicitation and supervised the sketch. All authors read, comment and approved the final manuscript .
Funding
This research was funded by the National key Research and Development Program of China, concede act 2017YFD0500506, and the National Science Foundation of China, concede number 31572384 .
Conflict of Interest
CT was employed by Shanghai Xinrong Big Emperor Pigeon Breeding Professional Cooperation .
The remaining authors declare that the research was conducted in the absence of any commercial or fiscal relationships that could be construed as a electric potential conflict of matter to .
Supplementary Material
The Supplementary Material for this article can be found on-line at : hypertext transfer protocol : //unianimal.com/articles/10.3389/fmicb.2020.01789/full # supplementary-material.
Footnotes
References
Abe, F., Ishibashi, N., and Shimamura, S. ( 1995 ). Effect of government of bifidobacteria and lactic acid bacteria to newborn calves and piglets. J. Dairy Sci. 78, 2838–2846. department of the interior : 10.3168/jds.S0022-0302 ( 95 ) 76914-4
PubMed Abstract | CrossRef Full Text | Google Scholar Abrahamsson, T. R., Sinkiewicz, G., Jakobsson, T., Fredrikson, M., and Bjorksten, B. ( 2009 ). probiotic lactobacillus in breast milk and baby stool in relation to oral inhalation during the inaugural year of life. J. Pediatr. Gastroenterol. Nutr. 49, 349–354. department of the interior : 10.1097/MPG.0b013e31818f091b
PubMed Abstract | CrossRef Full Text | Google Scholar Albesharat, R., Ehrmann, M. A., Korakli, M., Yazaji, S., and Vogel, R. F. ( 2011 ). Phenotypic and genotypical analyses of lactic acid bacteria in local fermented food, breast milk and faeces of mothers and their babies. Syst. Appl. Microbiol. 34, 148–155. department of the interior : 10.1016/j.syapm.2010.12.001
PubMed Abstract | CrossRef Full Text | Google Scholar Ballini, A., Gnoni, A., De Vito, D., Dipalma, G., Cantore, S., Gargiulo Isacco, C., et aluminum. ( 2019 ). effect of probiotics on the occurrence of nutriment absorption capacities in healthy children : a randomized double-blinded placebo-controlled pilot burner study. Eur. Rev. Med. Pharmacol. Sci. 23, 8645–8657. department of the interior : 10.26355/eurrev_201910_19182
PubMed Abstract | CrossRef Full Text | Google Scholar Benjamini, Y., and Hochberg, Y. ( 1995 ). Controlling the faithlessly discovery rate : a virtual and potent overture to multiple testing. J. R. Stat. Soc. Ser. B. 57, 289–300. department of the interior : 10.1111/j.2517-6161.1995.tb02031.x
CrossRef Full Text | Google Scholar Digiulio, D. B., Romero, R., Amogan, H. P., Kusanovic, J. P., Bik, E. M., Gotsch, F., et alabama. ( 2008 ). microbial preponderance, diversity and abundance in amniotic fluid during preterm labor : a molecular and culture-based probe. PLoS One 3 : e3056. department of the interior : 10.1371/journal.pone.0003056
PubMed Abstract | CrossRef Full Text | Google Scholar Gillespie, M. J., Stanley, D., Chen, H., Donald, J. A., Nicholas, K. R., Moore, R. J., et aluminum. ( 2012 ). functional similarities between pigeon ‘ milk ’ and mammal milk : initiation of immune gene expression and modification of the microbiota. PLoS One 7 : e48363. department of the interior : 10.1371/journal.pone.0048363
PubMed Abstract | CrossRef Full Text | Google Scholar Goudswaard, J., van five hundred Donk, J. A., van five hundred Gaag, I., and Noordzij, A. ( 1979 ). Peculiar IgA transfer in the pigeon from mother to squab. Dev. Comp. Immunol. 3, 307–319. department of the interior : 10.1016/S0145-305X ( 79 ) 80027-0
PubMed Abstract | CrossRef Full Text | Google Scholar Guareschi, C. ( 1936 ). The necessity of maternal alimentary factors in the emergence of youthful pigeons. Boll. Soc. Ital. Biol. Sper. 11, 411–412 .
Google Scholar Kocianova, E., Rehacek, J., and Lisak, V. ( 1993 ). transmission of antibodies to Chlamydia psittaci and Coxiella burnetii through eggs and “ craw milk ” in pigeons. Eur. J. Epidemiol. 9, 209–212. department of the interior : 10.1007/BF00158794
PubMed Abstract | CrossRef Full Text | Google Scholar Lee, Y. K., and Mazmanian, S. K. ( 2010 ). Has the microbiota played a critical function in the development of the adaptive immune organization ? Science 330, 1768–1773. department of the interior : 10.1126/science.1195568
PubMed Abstract | CrossRef Full Text | Google Scholar Liévin-Le, M. V., and Servin, A. L. ( 2014 ). Anti-infective activities of Lactobacillus strains in the homo intestinal microbiota : from probiotics to gastrointestinal anti-infectious biotherapeutic agents. Clin. Microbiol. Rev. 27, 167–199. department of the interior : 10.1128/CMR.00080-13
PubMed Abstract | CrossRef Full Text | Google Scholar Luo, Y., Wang, X., Ma, Y., and Li, X. K. ( 2017 ). The biological function of pigeon crop milk and the regulation of its production. Yi Chuan 39, 1158–1167. department of the interior : 10.16288/j.yczz.17-132
PubMed Abstract | CrossRef Full Text | Google Scholar Luongo, D., Treppiccione, L., Sorrentino, A., Ferrocino, I., Turroni, S., Gatti, M., et aluminum. ( 2017 ). Immune-modulating effects in mouse dendritic cells of lactobacillus and bifidobacteria isolated from individuals following omnivorous, vegetarian and vegan diets. Cytokine 97, 141–148. department of the interior : 10.1016/j.cyto.2017.06.007
PubMed Abstract | CrossRef Full Text | Google Scholar McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., et aluminum. ( 2012 ). An better Greengenes taxonomy with denotative ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610–618. department of the interior : 10.1038/ismej.2011.139
PubMed Abstract | CrossRef Full Text | Google Scholar Mills, S., Ross, R. P., Hill, C., Fitzgerald, G. F., and Stanton, C. ( 2011 ). milk intelligence : mining milk for bioactive substances associated with human health. Int. Dairy J. 21, 377–401. department of the interior : 10.1016/j.idairyj.2010.12.011
CrossRef Full Text | Google Scholar Resta-Lenert, S., and Barrett, K. E. ( 2003 ). know probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive Escherichia coli ( EIEC ). Gut 52, 988–997. department of the interior : 10.1136/gut.52.7.988
PubMed Abstract | CrossRef Full Text | Google Scholar Vandeputte-Poma, J. ( 1980 ). Feeding, increase and metamorphosis of the pigeon, Columba livia domestica : duration and function of crop milk feeding. J. Comp. Physiol. B. 135, 97–99. department of the interior : 10.1007/BF00691198
CrossRef Full Text | Google Scholar Wang, Y., Li, A., Zhang, L., Waqas, M., Mehmood, K., Iqbal, M., et alabama. ( 2019 ). probiotic likely of Lactobacillus on the intestinal microflora against Escherichia coli induce mouse model through high-throughput sequence. Microb. Pathog. 137:103760. department of the interior : 10.1016/j.micpath.2019.103760
PubMed Abstract | CrossRef Full Text | Google Scholar Ward, R. E., Niñonuevo, M., Mills, D. A., Lebrilla, C. B., and German, J. B. ( 2006 ). In vitro zymosis of summit milk oligosaccharides by Bifidobacterium infantis and Lactobacillus gasseri. Appl. Environ. Microbiol. 72, 4497–4499. department of the interior : 10.1128/AEM.02515-05
PubMed Abstract | CrossRef Full Text | Google Scholar Xie, W. Y., Fu, Z., Pan, N. X., Yan, H. C., Wang, X. Q., and Gao, C. Q. ( 2019 ). Leucine promotes the growth of squab by increasing crop milk protein synthesis through the TOR signaling nerve pathway in the domestic pigeon ( Columba livia ). Poult. Sci. 98, 5514–5524. department of the interior : 10.3382/ps/pez296
PubMed Abstract | CrossRef Full Text | Google Scholar Zhao, L., Wang, G., Siegel, P., He, C., Wang, H., Zhao, W., et aluminum. ( 2013 ). quantitative genetic background of the server influences gut microbiomes in chickens. Sci. Rep. 3:1163. department of the interior : 10.1038/srep01163
CrossRef Full Text | Google Scholar
I am broadly interested in how human activities influence the ability of wildlife to persist in the modified environments that we create.
Specifically, my research investigates how the configuration and composition of landscapes influence the movement and population dynamics of forest birds. Both natural and human-derived fragmenting of habitat can influence where birds settle, how they access the resources they need to survive and reproduce, and these factors in turn affect population demographics. Most recently, I have been studying the ability of individuals to move through and utilize forested areas which have been modified through timber harvest as they seek out resources for the breeding and postfledging phases. As well I am working in collaboration with Parks Canada scientists to examine in the influence of high density moose populations on forest bird communities in Gros Morne National Park. Many of my projects are conducted in collaboration or consultation with representatives of industry and government agencies, seeking to improve the management and sustainability of natural resource extraction.
