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Manuel Martín-vivaldi - One of the best experts on this subject based on the ideXlab platform.
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Autoclaving Nest-Material Remains Influences the Probability of Ectoparasitism of Nestling Hoopoes (Upupa epops).
Biology, 2020Co-Authors: Mónica Mazorra-alonso, Manuel Martín-vivaldi, Juan Manuel Peralta-sánchez, Juan José SolerAbstract:Nest bacterial environment influences avian reproduction directly because it might include pathogenic- or antibiotic-producing bacteria or indirectly because predators or ectoparasites can use volatile compounds from nest bacterial metabolism to detect nests of their avian hosts. Hoopoes (Upupa epops) do not build nests. They rather reuse holes or nest-boxes that contain remains of nest-materials from previous breeding seasons. Interestingly, it has been recently described that the nest’s bacterial environment partly affects the uropygial gland microbiota of Hoopoe females and eggshells. Blood-sucking ectoparasites use chemical cues to find host nests, so we experimentally tested the hypothetical effects of microorganisms inhabiting nest-material remains before reproduction regarding the intensity of ectoparasitism suffered by 8-day-old nestling Hoopoes. In accordance with the hypothesis, nestlings hatched in nest-boxes with autoclaved nest-material remains from the previous reproductive seasons suffered less from ectoparasites than those hatched in the control nest-boxes with nonautoclaved nest-material. Moreover, we found a positive association between the bacterial density of nest-material during the nestling phase and ectoparasitism intensity that was only apparent in nest-boxes with autoclaved nest-material. However, contrary to our expectations, nest bacterial load was positively associated with fledgling success. These results suggest a link between the community of microorganisms of nest-material remains and the intensity of ectoparasitism, and, on the other hand, that the nest bacterial environment during reproduction is related to fledging success. Here, we discuss possible mechanisms explaining the experimental and correlative results, including the possibility that the experimental autoclaving of nest material affected the microbiota of females and nestlings’ secretion and/or nest volatiles that attracted ectoparasites, therefore indirectly affecting both the nest bacterial environment at the nestling stage and fledging success.
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Seasonal and Sexual Differences in the Microbiota of the Hoopoe Uropygial Secretion
Genes, 2018Co-Authors: Sonia M. Rodríguez-ruano, Manuel Martín-vivaldi, Juan Manuel Peralta-sánchez, Juan José Soler, Eva Valdivia, Ana B. García-martín, Ángela Martínez-garcía, Manuel Martínez-buenoAbstract:The uropygial gland of Hoopoe nestlings and nesting females hosts bacterial symbionts that cause changes in the characteristics of its secretion, including an increase of its antimicrobial activity. These changes occur only in nesting individuals during the breeding season, possibly associated with the high infection risk experienced during the stay in the hole-nests. However, the knowledge on Hoopoes uropygial gland microbial community dynamics is quite limited and based so far on culture-dependent and molecular fingerprinting studies. In this work, we sampled wild and captive Hoopoes of different sex, age, and reproductive status, and studied their microbiota using quantitative polymerase chain reaction (qPCR), fluorescence in situ hybridization (FISH) and pyrosequencing. Surprisingly, we found a complex bacterial community in all individuals (including non-nesting ones) during the breeding season. Nevertheless, dark secretions from nesting Hoopoes harbored significantly higher bacterial density than white secretions from breeding males and both sexes in winter. We hypothesize that bacterial proliferation may be host-regulated in phases of high infection risk (i.e., nesting). We also highlight the importance of specific antimicrobial-producing bacteria present only in dark secretions that may be key in this defensive symbiosis. Finally, we discuss the possible role of environmental conditions in shaping the uropygial microbiota, based on differences found between wild and captive Hoopoes.
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Acquisition of Uropygial Gland Microbiome by Hoopoe Nestlings.
Microbial Ecology, 2017Co-Authors: Manuel Martín-vivaldi, Magdalena Ruiz-rodríguez, Juan José Soler, Ángela Martínez-garcía, Laura Arco, Natalia Juárez-garcía-pelayo, Manuel Martínez-buenoAbstract:Mutualistic symbioses between animals and bacteria depend on acquisition of appropriate symbionts while avoiding exploitation by non-beneficial microbes. The mode of acquisition of symbionts would determine, not only the probability of encountering but also evolutionary outcomes of mutualistic counterparts. The microbiome inhabiting the uropygial gland of the European Hoopoe (Upupa epops) includes a variety of bacterial strains, some of them providing antimicrobial benefits. Here, the mode of acquisition and stability of this microbiome is analyzed by means of Automated rRNA Intergenic Spacer Analysis and two different experiments. The first experiment impeded mothers' access to their glands, thus avoiding direct transmission of microorganisms from female to offspring secretions. The second experiment explored the stability of the microbiomes by inoculating glands with secretions from alien nests. The first experiment provoked a reduction in similarity of microbiomes of mother and nestlings. Interestingly, some bacterial strains were more often detected when females had not access to their glands, suggesting antagonistic effects among bacteria from different sources. The second experiment caused an increase in richness of the microbiome of receivers in terms of prevalence of Operational Taxonomic Units (OTUs) that reduced differences in microbiomes of donors and receivers. That occurred because OTUs that were present in donors but not in receivers incorporated to the microbiome of the latter, which provoked that cross-inoculated nestlings got similar final microbiomes that included the most prevalent OTUs. The results are therefore consistent with a central role of vertical transmission in bacterial acquisition by nestling Hoopoes and support the idea that the typical composition of the Hoopoe gland microbiome is reached by the incorporation of some bacteria during the nestling period. This scenario suggests the existence of a coevolved core microbiome composed by a mix of specialized vertically transmitted strains and facultative symbionts able to coexist with them. The implications of this mixed mode of transmission for the evolution of the mutualism are discussed.
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Multi‐functional crest display in Hoopoes Upupa epops
Journal of Avian Biology, 2017Co-Authors: Magdalena Ruiz-rodríguez, Manuel Martín-vivaldi, Jesús M. AvilésAbstract:Animals can engage in visual displays, which may target conspecifics, heterospecifics or both. Here we studied the function of the flamboyant crest-raising display of Hoopoes Upupa epops in experiments performed with males in captivity. Males were exposed to sounds of a conspecific (male Hoopoe song), a potential predator (human voice), and two controls (the song of a blackbird Turdus merula, and background noise). These stimuli were presented to males in the presence and absence of females. Males raised the crest with a significantly higher probability when confronted with stimuli indicating potential threats (rival mate or predator) than with controls. The crest display was frequent when confronted with both kinds of threats independently of the presence of a female, suggesting that it was directed to the predator and the rival male. The probability of raising the crest was not related to body condition, and there was a marginally but not significant negative relationship between probability of raising the crest and the number of black spots on the crest feathers, which may suggest that crest display could be informing about male quality. Therefore, male Hoopoes display the crest in a heterospecific context in response to detection of potential threats, which could be a deceptive or pursuit-deterrent signal. The results also support a role of the crest in sexual selection, suggesting that crest display in male Hoopoes may serve multiple functions.
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Nestedness of Hoopoes' bacterial communities: symbionts from the uropygial gland to the eggshell
Biological Journal of the Linnean Society, 2016Co-Authors: Juan José Soler, Sonia M. Rodríguez-ruano, Antonio M. Martín-platero, Juan Manuel Peralta-sánchez, Manuel Martínez-bueno, Ángela Martínez-garcía, Manuel Martín-vivaldiAbstract:How microbial symbionts are established and maintain on their hosts is a leading question with important consequences for the understanding of the evolution and functioning of mutualistic relationships. The acquisition by hosts of mutualistic microbial symbionts can be considered as colonization processes of environments (i.e., host) by symbionts. Colonization processes can be explored by characterizing the nestedness of communities, but this approach has rarely been applied to communities of microbial symbionts. We used this approach here, and estimated the nestedness of bacterial communities of Hoopoes (Upupa epops), a species with symbiotic bacteria in their uropygial gland that are expected to colonize eggshells where they protect embryos from pathogens. Bacterial communities were characterized by ARISA (Automated rRNA Intergenetic Spacer Region) and studied the nestedness characteristics of bacterial communities living in the uropygial secretion, bill, belly and eggshells of each sampled female Hoopoes. We detected a consistent nested pattern of bacterial communities of Hoopoes; from the uropygial gland to the eggshell. We also found evidence of study year and reproductive events influencing the level of nestedness of bacterial communities of Hoopoes. These results indicate that bacterial communities of eggshells and body parts of female Hoopoes are at least partially conditioned by the symbiotic community in the uropygial gland. We discuss the importance of these results for understanding this host–microbial mutualism functioning and evolution.
Juan José Soler - One of the best experts on this subject based on the ideXlab platform.
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Autoclaving Nest-Material Remains Influences the Probability of Ectoparasitism of Nestling Hoopoes (Upupa epops).
Biology, 2020Co-Authors: Mónica Mazorra-alonso, Manuel Martín-vivaldi, Juan Manuel Peralta-sánchez, Juan José SolerAbstract:Nest bacterial environment influences avian reproduction directly because it might include pathogenic- or antibiotic-producing bacteria or indirectly because predators or ectoparasites can use volatile compounds from nest bacterial metabolism to detect nests of their avian hosts. Hoopoes (Upupa epops) do not build nests. They rather reuse holes or nest-boxes that contain remains of nest-materials from previous breeding seasons. Interestingly, it has been recently described that the nest’s bacterial environment partly affects the uropygial gland microbiota of Hoopoe females and eggshells. Blood-sucking ectoparasites use chemical cues to find host nests, so we experimentally tested the hypothetical effects of microorganisms inhabiting nest-material remains before reproduction regarding the intensity of ectoparasitism suffered by 8-day-old nestling Hoopoes. In accordance with the hypothesis, nestlings hatched in nest-boxes with autoclaved nest-material remains from the previous reproductive seasons suffered less from ectoparasites than those hatched in the control nest-boxes with nonautoclaved nest-material. Moreover, we found a positive association between the bacterial density of nest-material during the nestling phase and ectoparasitism intensity that was only apparent in nest-boxes with autoclaved nest-material. However, contrary to our expectations, nest bacterial load was positively associated with fledgling success. These results suggest a link between the community of microorganisms of nest-material remains and the intensity of ectoparasitism, and, on the other hand, that the nest bacterial environment during reproduction is related to fledging success. Here, we discuss possible mechanisms explaining the experimental and correlative results, including the possibility that the experimental autoclaving of nest material affected the microbiota of females and nestlings’ secretion and/or nest volatiles that attracted ectoparasites, therefore indirectly affecting both the nest bacterial environment at the nestling stage and fledging success.
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Seasonal and Sexual Differences in the Microbiota of the Hoopoe Uropygial Secretion
Genes, 2018Co-Authors: Sonia M. Rodríguez-ruano, Manuel Martín-vivaldi, Juan Manuel Peralta-sánchez, Juan José Soler, Eva Valdivia, Ana B. García-martín, Ángela Martínez-garcía, Manuel Martínez-buenoAbstract:The uropygial gland of Hoopoe nestlings and nesting females hosts bacterial symbionts that cause changes in the characteristics of its secretion, including an increase of its antimicrobial activity. These changes occur only in nesting individuals during the breeding season, possibly associated with the high infection risk experienced during the stay in the hole-nests. However, the knowledge on Hoopoes uropygial gland microbial community dynamics is quite limited and based so far on culture-dependent and molecular fingerprinting studies. In this work, we sampled wild and captive Hoopoes of different sex, age, and reproductive status, and studied their microbiota using quantitative polymerase chain reaction (qPCR), fluorescence in situ hybridization (FISH) and pyrosequencing. Surprisingly, we found a complex bacterial community in all individuals (including non-nesting ones) during the breeding season. Nevertheless, dark secretions from nesting Hoopoes harbored significantly higher bacterial density than white secretions from breeding males and both sexes in winter. We hypothesize that bacterial proliferation may be host-regulated in phases of high infection risk (i.e., nesting). We also highlight the importance of specific antimicrobial-producing bacteria present only in dark secretions that may be key in this defensive symbiosis. Finally, we discuss the possible role of environmental conditions in shaping the uropygial microbiota, based on differences found between wild and captive Hoopoes.
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Acquisition of Uropygial Gland Microbiome by Hoopoe Nestlings.
Microbial Ecology, 2017Co-Authors: Manuel Martín-vivaldi, Magdalena Ruiz-rodríguez, Juan José Soler, Ángela Martínez-garcía, Laura Arco, Natalia Juárez-garcía-pelayo, Manuel Martínez-buenoAbstract:Mutualistic symbioses between animals and bacteria depend on acquisition of appropriate symbionts while avoiding exploitation by non-beneficial microbes. The mode of acquisition of symbionts would determine, not only the probability of encountering but also evolutionary outcomes of mutualistic counterparts. The microbiome inhabiting the uropygial gland of the European Hoopoe (Upupa epops) includes a variety of bacterial strains, some of them providing antimicrobial benefits. Here, the mode of acquisition and stability of this microbiome is analyzed by means of Automated rRNA Intergenic Spacer Analysis and two different experiments. The first experiment impeded mothers' access to their glands, thus avoiding direct transmission of microorganisms from female to offspring secretions. The second experiment explored the stability of the microbiomes by inoculating glands with secretions from alien nests. The first experiment provoked a reduction in similarity of microbiomes of mother and nestlings. Interestingly, some bacterial strains were more often detected when females had not access to their glands, suggesting antagonistic effects among bacteria from different sources. The second experiment caused an increase in richness of the microbiome of receivers in terms of prevalence of Operational Taxonomic Units (OTUs) that reduced differences in microbiomes of donors and receivers. That occurred because OTUs that were present in donors but not in receivers incorporated to the microbiome of the latter, which provoked that cross-inoculated nestlings got similar final microbiomes that included the most prevalent OTUs. The results are therefore consistent with a central role of vertical transmission in bacterial acquisition by nestling Hoopoes and support the idea that the typical composition of the Hoopoe gland microbiome is reached by the incorporation of some bacteria during the nestling period. This scenario suggests the existence of a coevolved core microbiome composed by a mix of specialized vertically transmitted strains and facultative symbionts able to coexist with them. The implications of this mixed mode of transmission for the evolution of the mutualism are discussed.
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Nestedness of Hoopoes' bacterial communities: symbionts from the uropygial gland to the eggshell
Biological Journal of the Linnean Society, 2016Co-Authors: Juan José Soler, Sonia M. Rodríguez-ruano, Antonio M. Martín-platero, Juan Manuel Peralta-sánchez, Manuel Martínez-bueno, Ángela Martínez-garcía, Manuel Martín-vivaldiAbstract:How microbial symbionts are established and maintain on their hosts is a leading question with important consequences for the understanding of the evolution and functioning of mutualistic relationships. The acquisition by hosts of mutualistic microbial symbionts can be considered as colonization processes of environments (i.e., host) by symbionts. Colonization processes can be explored by characterizing the nestedness of communities, but this approach has rarely been applied to communities of microbial symbionts. We used this approach here, and estimated the nestedness of bacterial communities of Hoopoes (Upupa epops), a species with symbiotic bacteria in their uropygial gland that are expected to colonize eggshells where they protect embryos from pathogens. Bacterial communities were characterized by ARISA (Automated rRNA Intergenetic Spacer Region) and studied the nestedness characteristics of bacterial communities living in the uropygial secretion, bill, belly and eggshells of each sampled female Hoopoes. We detected a consistent nested pattern of bacterial communities of Hoopoes; from the uropygial gland to the eggshell. We also found evidence of study year and reproductive events influencing the level of nestedness of bacterial communities of Hoopoes. These results indicate that bacterial communities of eggshells and body parts of female Hoopoes are at least partially conditioned by the symbiotic community in the uropygial gland. We discuss the importance of these results for understanding this host–microbial mutualism functioning and evolution.
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The Hoopoe's Uropygial Gland Hosts a Bacterial Community Influenced by the Living Conditions of the Bird
PLOS ONE, 2015Co-Authors: Sonia M. Rodríguez-ruano, Manuel Martín-vivaldi, Antonio M. Martín-platero, J. Pablo López-lópez, Juan Manuel Peralta-sánchez, Magdalena Ruiz-rodríguez, Juan José Soler, Eva Valdivia, Manuel Martínez-buenoAbstract:Molecular methods have revealed that symbiotic systems involving bacteria are mostly based on whole bacterial communities. Bacterial diversity in Hoopoe uropygial gland secretion is known to be mainly composed of certain strains of enterococci, but this conclusion is based solely on culture-dependent techniques. This study, by using culture-independent techniques (based on the 16S rDNA and the ribosomal intergenic spacer region) shows that the bacterial community in the uropygial gland secretion is more complex than previously thought and its composition is affected by the living conditions of the bird. Besides the known enterococci, the uropygial gland hosts other facultative anaerobic species and several obligated anaerobic species (mostly clostridia). The bacterial assemblage of this community was largely invariable among study individuals, although differences were detected between captive and wild female Hoopoes, with some strains showing significantly higher prevalence in wild birds. These results alter previous views on the Hoopoe-bacteria symbiosis and open a new window to further explore this system, delving into the possible sources of symbiotic bacteria (e.g. nest environments, digestive tract, winter quarters) or the possible functions of different bacterial groups in different contexts of parasitism or predation of their Hoopoe host.
Manuel Martinvivaldi - One of the best experts on this subject based on the ideXlab platform.
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preening as a vehicle for key bacteria in Hoopoes
Microbial Ecology, 2015Co-Authors: Angela Martinezgarcia, Juan José Soler, Sonia M Rodriguezruano, Manuel Martinezbueno, Antonio M Martinplatero, Natalia Juarezgarcia, Manuel MartinvivaldiAbstract:Oily secretions produced in the uropygial gland of incubating female Hoopoes contain antimicrobial-producing bacteria that prevent feathers from degradation and eggs from pathogenic infection. Using the beak, females collect the uropygial gland secretion and smear it directly on the eggshells and brood patch. Thus, some bacterial strains detected in the secretion should also be present on the eggshell, beak, and brood patch. To characterize these bacterial communities, we used Automatic Ribosomal Intergenic Spacer Analysis (ARISA), which distinguishes between taxonomically different bacterial strains (i.e. different operational taxonomic units [OTUs]) by the size of the sequence amplified. We identified a total of 146 different OTUs with sizes between 139 and 999 bp. Of these OTUs, 124 were detected in the uropygial oil, 106 on the beak surface, 97 on the brood patch, and 98 on the eggshell. The highest richness of OTUs appeared in the uropygial oil samples. Moreover, the detection of some OTUs on the beak, brood patch, and eggshells of particular nests depended on these OTUs being present in the uropygial oil of the female. These results agree with the hypothesis that symbiotic bacteria are transmitted from the uropygial gland to beak, brood patch, and eggshell surfaces, opening the possibility that the bacterial community of the secretion plays a central role in determining the communities of special Hoopoe eggshell structures (i.e., crypts) that, soon after hatching, are filled with uropygial oil, thereby protecting embryos from pathogens.
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special structures of Hoopoe eggshells enhance the adhesion of symbiont carrying uropygial secretion that increase hatching success
Journal of Animal Ecology, 2014Co-Authors: Manuel Martinvivaldi, Juan José Soler, Laura Arco, Manuel Martinezbueno, Antonio M Martinplatero, Juan Manuel Peraltasanchez, Magdalena Ruizrodriguez, Eva ValdiviaAbstract:This is the pre-peer-reviewed version of the following article: Martin-Vivaldi, M.; et al. Special structures of Hoopoe eggshells enhance the adhesion of symbionts-carrying uropygial secretion to prevent embryo infection. Journal of Animal Ecology, (2014). which has been published in final form at: http://onlinelibrary.wiley.com/doi/10.1111/1365-2656.12243/abstract
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song strophe length and reproductive success in a non passerine bird the Hoopoe upupa epops
Ibis, 2008Co-Authors: Manuel Martinvivaldi, José Javier Palomino, Manuel Soler, Juan Gabriel MartínezAbstract:Hoopoe Upupa epops males produce a very simple song, with a repertoire size of one, in which the main difference between different strophes of a male and between the songs of different males is the number of elements they include (strophe-length). In several passerine species it has been shown that strophe-length is a sexually selected trait that reflects male quality and correlates with reproductive success. Here we analyse whether in a non-passerine, the Hoopoe, strophe-length of males is correlated with several variables of their reproductive success. Females paired with males singing long strophes laid their first clutch earlier, produced larger first clutches and laid second clutches after a successful first one more frequently than those paired with males singing short strophes. Moreover, males with long strophes produced more fledglings in their first clutches and in the whole season, partly because they brought more food for the brood than males with short strophes. The relationships found are not mediated by age effects. Previously we have shown that Hoopoe females in the early spring are attracted preferentially to songs with long strophes. Here we show that males singing long strophes also obtain postpairing benefits in terms of reproductive success, and that females paired with these males obtain direct benefits because these males provide greater feeding effort in the second half of the nestling period. These findings support the hypothesis that in the Hoopoe, strophe-length is a sexually selected cue under direct selection.
Eva Valdivia - One of the best experts on this subject based on the ideXlab platform.
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Seasonal and Sexual Differences in the Microbiota of the Hoopoe Uropygial Secretion
Genes, 2018Co-Authors: Sonia M. Rodríguez-ruano, Manuel Martín-vivaldi, Juan Manuel Peralta-sánchez, Juan José Soler, Eva Valdivia, Ana B. García-martín, Ángela Martínez-garcía, Manuel Martínez-buenoAbstract:The uropygial gland of Hoopoe nestlings and nesting females hosts bacterial symbionts that cause changes in the characteristics of its secretion, including an increase of its antimicrobial activity. These changes occur only in nesting individuals during the breeding season, possibly associated with the high infection risk experienced during the stay in the hole-nests. However, the knowledge on Hoopoes uropygial gland microbial community dynamics is quite limited and based so far on culture-dependent and molecular fingerprinting studies. In this work, we sampled wild and captive Hoopoes of different sex, age, and reproductive status, and studied their microbiota using quantitative polymerase chain reaction (qPCR), fluorescence in situ hybridization (FISH) and pyrosequencing. Surprisingly, we found a complex bacterial community in all individuals (including non-nesting ones) during the breeding season. Nevertheless, dark secretions from nesting Hoopoes harbored significantly higher bacterial density than white secretions from breeding males and both sexes in winter. We hypothesize that bacterial proliferation may be host-regulated in phases of high infection risk (i.e., nesting). We also highlight the importance of specific antimicrobial-producing bacteria present only in dark secretions that may be key in this defensive symbiosis. Finally, we discuss the possible role of environmental conditions in shaping the uropygial microbiota, based on differences found between wild and captive Hoopoes.
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SEE PROFILE
2016Co-Authors: Antonio Martin-platero, Magdalena Ruiz-rodríguez, Eva Valdivia, Manuel Martínez-bueno, See Profile, Antonio M. Martín-plateroAbstract:Special structures of Hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching succes
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Similarity among bacterial communities of eggshells depending on type of nest material.
2016Co-Authors: Ángela Martínez-garcía, Manuel Martín-vivaldi, Sonia M. Rodríguez-ruano, Juan Manuel Peralta-sánchez, Eva Valdivia, Juan J. SolerAbstract:Multidimensional space representation (PCoA) based on similarities of the composition of bacterial communities harbored on Hoopoe eggshells in nests with control (CN) and experimental (EN) materials. Variance captured by each of the three axes is shown within the axis legends in parenthesis.
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Similarities of bacterial communities in control nests.
2016Co-Authors: Ángela Martínez-garcía, Manuel Martín-vivaldi, Sonia M. Rodríguez-ruano, Juan Manuel Peralta-sánchez, Eva Valdivia, Juan J. SolerAbstract:Multidimensional space representation (PCoA) based on similarities of communities harbored in female Hoopoe uropygial gland, cloaca, eggshells and nest material of control nests. Variance captured by each axe is shown within the axis legends in parenthesis. The analysis was performed including only the OTUs present in uropygial secretion that were detected in at least 4 samples of any of the bacterial communities considered.
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The Hoopoe's Uropygial Gland Hosts a Bacterial Community Influenced by the Living Conditions of the Bird
PLOS ONE, 2015Co-Authors: Sonia M. Rodríguez-ruano, Manuel Martín-vivaldi, Antonio M. Martín-platero, J. Pablo López-lópez, Juan Manuel Peralta-sánchez, Magdalena Ruiz-rodríguez, Juan José Soler, Eva Valdivia, Manuel Martínez-buenoAbstract:Molecular methods have revealed that symbiotic systems involving bacteria are mostly based on whole bacterial communities. Bacterial diversity in Hoopoe uropygial gland secretion is known to be mainly composed of certain strains of enterococci, but this conclusion is based solely on culture-dependent techniques. This study, by using culture-independent techniques (based on the 16S rDNA and the ribosomal intergenic spacer region) shows that the bacterial community in the uropygial gland secretion is more complex than previously thought and its composition is affected by the living conditions of the bird. Besides the known enterococci, the uropygial gland hosts other facultative anaerobic species and several obligated anaerobic species (mostly clostridia). The bacterial assemblage of this community was largely invariable among study individuals, although differences were detected between captive and wild female Hoopoes, with some strains showing significantly higher prevalence in wild birds. These results alter previous views on the Hoopoe-bacteria symbiosis and open a new window to further explore this system, delving into the possible sources of symbiotic bacteria (e.g. nest environments, digestive tract, winter quarters) or the possible functions of different bacterial groups in different contexts of parasitism or predation of their Hoopoe host.
Manuel Martínez-bueno - One of the best experts on this subject based on the ideXlab platform.
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Seasonal and Sexual Differences in the Microbiota of the Hoopoe Uropygial Secretion
Genes, 2018Co-Authors: Sonia M. Rodríguez-ruano, Manuel Martín-vivaldi, Juan Manuel Peralta-sánchez, Juan José Soler, Eva Valdivia, Ana B. García-martín, Ángela Martínez-garcía, Manuel Martínez-buenoAbstract:The uropygial gland of Hoopoe nestlings and nesting females hosts bacterial symbionts that cause changes in the characteristics of its secretion, including an increase of its antimicrobial activity. These changes occur only in nesting individuals during the breeding season, possibly associated with the high infection risk experienced during the stay in the hole-nests. However, the knowledge on Hoopoes uropygial gland microbial community dynamics is quite limited and based so far on culture-dependent and molecular fingerprinting studies. In this work, we sampled wild and captive Hoopoes of different sex, age, and reproductive status, and studied their microbiota using quantitative polymerase chain reaction (qPCR), fluorescence in situ hybridization (FISH) and pyrosequencing. Surprisingly, we found a complex bacterial community in all individuals (including non-nesting ones) during the breeding season. Nevertheless, dark secretions from nesting Hoopoes harbored significantly higher bacterial density than white secretions from breeding males and both sexes in winter. We hypothesize that bacterial proliferation may be host-regulated in phases of high infection risk (i.e., nesting). We also highlight the importance of specific antimicrobial-producing bacteria present only in dark secretions that may be key in this defensive symbiosis. Finally, we discuss the possible role of environmental conditions in shaping the uropygial microbiota, based on differences found between wild and captive Hoopoes.
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Acquisition of Uropygial Gland Microbiome by Hoopoe Nestlings.
Microbial Ecology, 2017Co-Authors: Manuel Martín-vivaldi, Magdalena Ruiz-rodríguez, Juan José Soler, Ángela Martínez-garcía, Laura Arco, Natalia Juárez-garcía-pelayo, Manuel Martínez-buenoAbstract:Mutualistic symbioses between animals and bacteria depend on acquisition of appropriate symbionts while avoiding exploitation by non-beneficial microbes. The mode of acquisition of symbionts would determine, not only the probability of encountering but also evolutionary outcomes of mutualistic counterparts. The microbiome inhabiting the uropygial gland of the European Hoopoe (Upupa epops) includes a variety of bacterial strains, some of them providing antimicrobial benefits. Here, the mode of acquisition and stability of this microbiome is analyzed by means of Automated rRNA Intergenic Spacer Analysis and two different experiments. The first experiment impeded mothers' access to their glands, thus avoiding direct transmission of microorganisms from female to offspring secretions. The second experiment explored the stability of the microbiomes by inoculating glands with secretions from alien nests. The first experiment provoked a reduction in similarity of microbiomes of mother and nestlings. Interestingly, some bacterial strains were more often detected when females had not access to their glands, suggesting antagonistic effects among bacteria from different sources. The second experiment caused an increase in richness of the microbiome of receivers in terms of prevalence of Operational Taxonomic Units (OTUs) that reduced differences in microbiomes of donors and receivers. That occurred because OTUs that were present in donors but not in receivers incorporated to the microbiome of the latter, which provoked that cross-inoculated nestlings got similar final microbiomes that included the most prevalent OTUs. The results are therefore consistent with a central role of vertical transmission in bacterial acquisition by nestling Hoopoes and support the idea that the typical composition of the Hoopoe gland microbiome is reached by the incorporation of some bacteria during the nestling period. This scenario suggests the existence of a coevolved core microbiome composed by a mix of specialized vertically transmitted strains and facultative symbionts able to coexist with them. The implications of this mixed mode of transmission for the evolution of the mutualism are discussed.
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SEE PROFILE
2016Co-Authors: Antonio Martin-platero, Magdalena Ruiz-rodríguez, Eva Valdivia, Manuel Martínez-bueno, See Profile, Antonio M. Martín-plateroAbstract:Special structures of Hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching succes
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Nestedness of Hoopoes' bacterial communities: symbionts from the uropygial gland to the eggshell
Biological Journal of the Linnean Society, 2016Co-Authors: Juan José Soler, Sonia M. Rodríguez-ruano, Antonio M. Martín-platero, Juan Manuel Peralta-sánchez, Manuel Martínez-bueno, Ángela Martínez-garcía, Manuel Martín-vivaldiAbstract:How microbial symbionts are established and maintain on their hosts is a leading question with important consequences for the understanding of the evolution and functioning of mutualistic relationships. The acquisition by hosts of mutualistic microbial symbionts can be considered as colonization processes of environments (i.e., host) by symbionts. Colonization processes can be explored by characterizing the nestedness of communities, but this approach has rarely been applied to communities of microbial symbionts. We used this approach here, and estimated the nestedness of bacterial communities of Hoopoes (Upupa epops), a species with symbiotic bacteria in their uropygial gland that are expected to colonize eggshells where they protect embryos from pathogens. Bacterial communities were characterized by ARISA (Automated rRNA Intergenetic Spacer Region) and studied the nestedness characteristics of bacterial communities living in the uropygial secretion, bill, belly and eggshells of each sampled female Hoopoes. We detected a consistent nested pattern of bacterial communities of Hoopoes; from the uropygial gland to the eggshell. We also found evidence of study year and reproductive events influencing the level of nestedness of bacterial communities of Hoopoes. These results indicate that bacterial communities of eggshells and body parts of female Hoopoes are at least partially conditioned by the symbiotic community in the uropygial gland. We discuss the importance of these results for understanding this host–microbial mutualism functioning and evolution.
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The Hoopoe's Uropygial Gland Hosts a Bacterial Community Influenced by the Living Conditions of the Bird
PLOS ONE, 2015Co-Authors: Sonia M. Rodríguez-ruano, Manuel Martín-vivaldi, Antonio M. Martín-platero, J. Pablo López-lópez, Juan Manuel Peralta-sánchez, Magdalena Ruiz-rodríguez, Juan José Soler, Eva Valdivia, Manuel Martínez-buenoAbstract:Molecular methods have revealed that symbiotic systems involving bacteria are mostly based on whole bacterial communities. Bacterial diversity in Hoopoe uropygial gland secretion is known to be mainly composed of certain strains of enterococci, but this conclusion is based solely on culture-dependent techniques. This study, by using culture-independent techniques (based on the 16S rDNA and the ribosomal intergenic spacer region) shows that the bacterial community in the uropygial gland secretion is more complex than previously thought and its composition is affected by the living conditions of the bird. Besides the known enterococci, the uropygial gland hosts other facultative anaerobic species and several obligated anaerobic species (mostly clostridia). The bacterial assemblage of this community was largely invariable among study individuals, although differences were detected between captive and wild female Hoopoes, with some strains showing significantly higher prevalence in wild birds. These results alter previous views on the Hoopoe-bacteria symbiosis and open a new window to further explore this system, delving into the possible sources of symbiotic bacteria (e.g. nest environments, digestive tract, winter quarters) or the possible functions of different bacterial groups in different contexts of parasitism or predation of their Hoopoe host.