Abstract
Microbiomes have emerged as a key component essential for maintaining the health of an organism. Additionally, the roles of microbiomes are multifaceted, some unique to specific body areas and organs while others, particularly the gut microbiome, having broader effects on the entire organism. Comparative literature is emerging that compares microbiomes across mammals and birds. Domestic poultry have been the most extensively studied relative to their role in production agriculture. These data have provided a great deal of information about the effects of diet and nutritional requirements relative to the gut microbiome, productivity, and resilience to diseases. Conversely, limited research has been conducted on wild birds, despite them inhabiting a broad array of ecological niches and environments, providing a rich diversity in their adaptations to different habitats. Migratory birds and raptors are of particular interest. Migratory birds encounter a range of ecosystems and provide a link between allopatric populations. Raptors occupy high positions in the food chain, with potential exposure to biomagnification of environmental contaminants and pathogens. This review overviews our current understanding of the structure and function of avian microbiomes as related to avian health and reproduction in domestic and wild birds, highlighting knowledge gaps in need of further investigation for more effective conservation of rapidly declining avian populations.
Lay summary
Birds are among the most endangered organisms on the planet, vulnerable to many environmental challenges, including disease, loss of habitat, shortage of food resources, and climate-related change. They need to adapt to these challenges to survive and flourish. While the links between the gut microbiome, diet, resistance to infection, and behavior have been well studied in humans, laboratory animals, and domestic or captive birds, comparatively little is known about these associations in wildlife, where diet is expected to be more varied and seasonal. This is especially true for wild bird species. We review the information that is available on the microbiomes of both domestic and wild birds, highlighting knowledge gaps in our understanding of the health and reproduction of wild birds, toward furthering their conservation.
Introduction
A sharp decline in avian populations over the past century has been linked to anthropogenic factors originating from industry, urbanization, changing land use, habitat loss, pollution, emerging diseases, and climate change. These integrating factors exert increasing stress, leading to diminished metabolic, immune, and reproductive functions, contributing to deteriorating overall health and reduced longevity (Ottinger & Geiselman 2023). This drastic loss of avian species underscores the critical need for methods to evaluate health in field populations (Ottinger et al. 2019). In particular, research is needed to understand the dynamic interrelationship of environmental stressors, health, and the role of the microbiome in maintaining the health of individuals and populations (Hird et al. 2015, Grond et al. 2018, Song et al. 2022). Key questions include the following: Are there environmental factors that contribute to the host-associated microbiome alterations; Is the microbiome the first line of immune defense; Dow do the multiple functions of the microbiome contribute to the overall health, productivity, and longevity of an individual; What are the dynamics of microbiome composition and diversity over the reproductive lifespan? Investigations into the microbiome as a key component in individual health and pathogen resilience will provide important insights into adaptive strategies across avian species related to environmental stressors, and thereby facilitate and strengthen management strategies and conservation efforts for these species.
Microbiomes residing in the gut, skin, and other organs are increasingly recognized as critical to the overall health of an individual, including wildlife (Comizzoli et al. 2021). Research in domesticated livestock and in laboratory models has provided a great deal of fundamental information about the critical role of the microbiome in health and immune resilience (Trevelline et al. 2019). Wildlife studies have found associations between gut health and diet (red squirrels – Ren et al. 2017, African buffalo – Couch et al. 2021, great apes – Hicks et al. 2018), parasite burden (gorilla – Vičková et al. 2018), captivity (black rhinoceros – Gibson et al. 2019), and anthropogenic changes (Amato et al. 2013). The conserved mechanisms necessary for the health of the individual are now expanding to include microbiomes in wildlife studies with a linkage to the reproductive biology of wild animals (Comizzoli et al. 2021). The role of microbiomes has become exceedingly complex as more insights are gained into the importance of the microbial makeup of our environment as well as the role of an individual’s microbiome in promoting health and homeostasis. This broadened view of the scale and diversity of microbiomes and their influence on living organisms is giving rise to exciting emerging research.
Birds are the focus of this review, specifically the role of the gut and other microbiomes in domestic and wild species. There is tremendous diversity in both domestic and wild birds in their diet, habitat, and life history, which can affect the gut microbiota (Waite & Taylor 2015, Grond et al. 2018). In addition, there are clear interactive physiological systems that are proving to be reliant on the microbiome, including immune, metabolic, and reproductive systems, especially in wild birds (Grond et al. 2019, 2017, Matheen et al. 2022). Given that studies of the microbiome are accelerating with the availability of powerful sequencing technologies, more studies can directly address the role of the microbial populations in the gut and other organs in wild birds (Hird 2017, Aruwa et al. 2021, Bodawatta et al. 2020a,b, 2021). Moreover, there is a rich literature for domestic poultry relating the effects of diet, health, and life stages to microbiomes (Proszkowiec-Weglarz et al. 2023). Further, many species of birds that migrate have high-energy consumption demands that are reliant on the available resources during migration, fluctuations in which are reflected in the gut microbiome (Song et al. 2022) and immune functions (Eikenar et al. 2020). Because there is such diversity across wild birds in their life history, habitat, migratory patterns, and lifespan, there is tremendous variation in the microbiota constituting an individual’s microbiome. As such, this review is not an exhaustive discussion of all aspects of available information about avian microbiomes. Rather, we seek to provide basic information about the role of the microbiome in avian health, longevity, and lifetime productivity in domestic and wild birds. Finally, owing to the greater risk that avian species higher on the food chain have exposure to contaminants because of anthropogenic changes to the environment, we are including the biomagnification of toxins and the example of African vultures, many of which are critically endangered. As obligate scavengers, these species provide a unique ecosystem sanitation service. Studies of vultures will be discussed from the perspective of potential differences in the microbiomes of scavengers and other raptors as indices of health.
Microbiome structure and composition in birds
Studies on microbiomes in birds span the past two decades, with foundational work conducted in domestic poultry, and later being applied to wild birds. There has been an exponential increase in the number of studies of the avian microbiome from 2006 to 2022 that include domestic and captive birds, as well as wild birds that have been opportunistically sampled (Fig. 1; Sun et al. 2022). It is critical to have information from agriculturally relevant domestic species and birds kept as pets or for aviculture to provide a basic understanding of the biological function of the microbiome across avian species as well as insights into the effects of predictable diets and life stages. This information can then provide the basis for studies on wild birds maintained in captivity, either in zoological and conservation facilities or in rehabilitation centers with the aim of eventual release. Together, these data can then be compared to studies on free-living wild birds to gain an understanding of microbiome composition differences associated with clade, habitat, and alterations/adaptations related to migration. As mentioned earlier, the concern about the spread of pathogens has given rise to recent investigations of antimicrobial resistance and the potential for resistant pathogens and genes being carried by migratory birds. As shown in Fig. 1, the range of topical areas in which microbiomes have been studied is vast in birds, again more so in domestic birds as opposed to wild species. Fortunately, there are some extensive reviews from within the last decade that begin to synthesize the available literature for birds.
Disciplinary areas encompassed by publications from 2006 to 2022 (from Sun et al. 2022, available from Creative Commons Attribution License ICC BY).
Citation: Reproduction and Fertility 5, 3; 10.1530/RAF-23-0076
Detailed studies on the effects of diet and nutrition in domestic poultry have provided the cornerstone for integrating the role of the gut microbiome in optimizing health and productivity (Ashayerizadeh et al. 2009, Aruwa et al. 2021, Yaqoob et al. 2021, Lee et al. 2022). There is a growing number of studies across wild birds, with the objective of discerning species characteristics and the effects of environment, migration, and habitat. Of particular interest to our group is studying the role of the microbiome in maintaining the health of raptors and avian scavengers, specifically African vultures. They have remarkable resistance to potentially extremely pathogenic microbes that they ingest yet exhibit vulnerabilities to environmental chemical contaminants. These studies are necessarily multidimensional and must consider the biological/microbiological makeup, habitat, diet, and environmental stressors such as chemical contaminants and human–wildlife conflict.
Much attention has been on the gut microbiome and its relationship to immune function, physiological homeostasis, endocrine and behavioral components of reproduction, and metabolism. Birds have unique characteristics compared to mammals, including higher body temperature and metabolism, which affect the acquisition and composition of their gut microbiomes. As described by Hird (2015, 2017), host genetics, resource availability, and environmental conditions contribute to variations in the gut microbiota in birds. Interestingly, the egg is exposed to the rich microbial populations from the incubating parents and the surrounding nesting material, some of which can have antimicrobial properties. As will be discussed next, the cloacal, gut, and preen gland microbiomes vary with species and environment and are often altered by disease (Hird et al. 2018). Accordingly, there is wide variation in the microbiota that constitute the microbiomes across wild birds and other wildlife (Handy et al. 2023).
Bacterial composition of the avian microbiome
Rapid advances have occurred in bioinformatics and the analytical capabilities needed for investigating microbial populations in birds. These advances in our understanding of the role and importance of the gut microbiome have been facilitated by direct sequencing of 16S rRNA genes, metagenomics, and metaproteomics, among other approaches, which have provided extensive data and improved methods of analysis. Importantly, the capability of discerning differences in the bacterial populations according to site (gastrointestinal and other organs) provides additional insight into the functional roles of each. One of the factors involved in determining the bacterial makeup of a particular microbiome is the methods available for sampling. In domestic poultry and laboratory studies, it is possible to take invasive samples that can discern not only the microbiome of the cecum, skin, oral cavity, and preen gland but also the variations of the microbial populations along the segments of the intestinal tract. Additionally, the administration of pre- and probiotics and fecal transplants has provided some direct evidence for the potential beneficial effects of the microbiome on the health and productivity of an individual (Fig. 2). In a detailed review of microbiomes in domestic chickens, Yeoman et al. (2012) highlighted how microbial communities along the length of the gastrointestinal tract showed spatial variation in composition. Variations in microbial makeup in organs and various birds are discussed in more detail further next.
Cecal microbiome composition can influence poultry performance as evidenced in studies supplementing broiler chickens with prebiotics (Ricke et al. 2020, Yaqoob et al. 2021), laying hens with probiotics (Xiang et al. 2019) and in experiments relating to egg yields from laying hens (Cao et al. 2023).
Citation: Reproduction and Fertility 5, 3; 10.1530/RAF-23-0076
Sampling in wild birds presents a greater challenge. Many ongoing monitoring studies are now incorporating a health check, using primarily non- or minimally invasive methods (Ottinger et al. 2019). For instances, where wild birds are being handled for banding, movement studies, or other reasons for capture, the sampling of various microbiomes is possible with the use of swabs. Swabs have been used to obtain microbiome samples from different regions: buccal, skin, cloacal, as well as from feces and preen gland secretions relatively efficiently. However, it is important to note that some wild bird studies have found feces to be more representative of the gut microbiome than cloacal samples, possibly owing to the dual nature of this orifice, being for excretion and reproduction. Notably, cloacal microbiome samples have shown differences related to breeding season (Escallón et al. 2019) and reproductive activity itself; e.g., females that mated with more males had a higher diversity of cloacal microbiota. As such, one would expect that the degree of representation of gut bacteria within the cloacal sample will vary. Despite this, cloacal samples are a relatively non-invasive means of obtaining some indication of gut bacteria presence in the absence of an available fecal sample. Moreover, the fact that the cloaca contains a mix of gut and reproductive bacteria could be seen as an advantage should the researcher wish to determine health correlates during the breeding and non-breeding seasons. Interestingly, 16S rRNA sequencing and compositional analyses of great tit (Parus major) gut and cloacal microbiome communities, obtained from dissected digestive tracts and cloacal swabs respectively, demonstrated variations in the alpha and beta diversities of microbial communities of the gut regions and cloacal swabs (Bodawatta et al. 2020a,b). While there were no significant differences in alpha diversities of microbial communities between the gut and cloaca, significant differences were evident in beta diversity and community composition in the cloacal swab samples compared to the gut. Despite these differences at the microbial community level, cloacal swab samples were able to qualitatively capture most of the bacterial diversity of the gut (Bodawatta et al. 2020a, b). Thus, the minimally invasive cloacal sampling may be an ideal sampling method to qualitatively depict the gut microbiota from endangered species for the study of the host microbiomes.
Not surprisingly, the characteristics of the avian microbiome vary with the anatomical site and physiological function of that organ (Fig. 3). For example, the gut, skin, cloacal, preen gland, and feather microbiomes all differ from one another. In addition, over the lifespan of the individual, migration, and habitat also influence the microbiota (Waite & Taylor 2015, Grond et al. 2018, Jacob et al. 2018, Bodawatta et al. 2020a,b, Cao et al. 2020, Song et al. 2022, Proszkowiec-Weglarz et al. 2023). Because the gut microbiome has received the most attention, we will go into more detail about that research in sections III-V, with the acknowledgment that understanding the dynamic interrelationships of all microbiotas in an individual is important and will require further investigation. For example, the maintenance of feathers is essential for flight, thermoregulation, and mate attraction, with the preen gland and preen oil playing a critical role (Kolattukudy 1981). This unique feature of birds is a fascinating example of an adaptation important in maintaining health and productivity.
Composition of the microbiomes of domestic and wild birds at different body sites. Data were compiled from Andreani et al. 2020, Zepeda Mendoza et al. 2018, Meng et al. 2017, Roggenbuck et al. 2014, Qu et al. 2008, Hird et al. 2015 & Escallón et al. 2019.
Citation: Reproduction and Fertility 5, 3; 10.1530/RAF-23-0076
Role of the preen gland and its microbiome
The preen or uropygial gland plays a crucial role in avian health. Secretions of this gland have been characterized in detail in poultry and consist of 34 fatty acids and 77 volatile organic compounds (VOCs) (Gvoždíková Javůrková et al. 2023). Interestingly, this study also demonstrated strain differences in VOCs, with the meat-type Ross 308 preen secretions being higher in VOCs, hypothesized to possibly increase susceptibility to ectoparasites. This study captures the multifaceted function of the preen gland in maintaining health through feather integrity and the antimicrobial and antiparasitic effects of the oils, along with chemical communication.
Studies in wild birds have also shown strong evidence for the essential role of the preen gland secretions (Moreno-Rueda 2017). Hoopoes (Upupa epops; Phoeniculus purpureus) have documented changes in their preen gland secretions, with nestlings producing secretions that differ from those analyzed from adults (Martin-Vivaldi et al. 2010). Both types of secretions have strong antimicrobial properties, suggesting the presence of symbiotic bacteria that comprise the microbiome of the preen gland.
Evidence for protective functions of the preen gland secretions has also been reported in wild great tits (Parus major), which, like poultry, contain lipids that provide a protective coating and non-lipid volatile compounds that appear to be involved in olfactory communication, with potential antimicrobial properties (Bodawatta et al. 2020a,b). Characterization of the microbiota also revealed a diversity of roles in the preen gland microbiome that is important for feather and skin health and disease resistance. In addition, these preen gland secretions help to maintain an antimicrobial defense mechanism against microbes that may damage feather integrity and health (Jacob et al. 2018). Relationships were observed between the major histocompatibility complex (MHC) and microbial taxa in the preen oil and between microbes and preen oil chemicals in the song sparrow (Melospiza melodia; Grieves et al. 2021a,b). Studies by Whittaker and colleagues (2013, 2016, 2019) also demonstrated the importance of preen gland secretions in reproduction of the dark-eyed junco (Junco hyemalis), finding associations of the volatile compounds produced with odor and reproductive success, hinting at the potential links between uropygial gland microbial communities and behavioral communication. These sociobiological aspects of the role of preen gland secretions are important for the health and productivity of an individual.
Drivers of variation in microbiome structure and composition
Insights from domestic poultry: sex, age, and reproduction
One of the challenges in developing an understanding of microbiomes in birds is the tremendous variation in the environment in which they live. Even domesticated birds encompass a wide array of species, including those grown for agricultural food production and pets. The domestic chicken has been extensively studied, including genomics, metabolomics, characterization of bacterial populations, effects of probiotics, and association of microbiome function with health and has the advantage of consistency in genetics and housing/environment (for reviews, see Oakley et al. 2014, Aruwa et al. 2021). For this reason, we begin with information obtained in poultry and then move on to examples and data collected in wild birds living in a variety of habitats.
The beneficial and critical role of the gut microbiome has been incorporated into dietary ingredients for poultry to promote beneficial gut bacteria populations, including Lactobacillus and bifidobacteria (Yaqoob et al. 2021). Active populations of these and other bacteria promote a host of functional benefits, including boosting immune function and reducing pathogenic disease as well as enhancing reproductive function. Pre- and probiotics have also been shown to promote gut health and may synergize with other dietary supplements to optimize overall host health (Shehata et al. 2022). In laying hens, probiotic supplementation has resulted in improved productivity, egg quality, and eggshell strength (Xiang et al. 2019). Broiler flock performance also improved with enriched beneficial gut microorganisms (Ashayerizadeh et al. 2009). Similarly, prebiotics were shown to boost gut microbiomes in poultry by enhancing the proliferation of beneficial bacterial populations (Fig. 2; Ricke et al. 2020, Yaqoob et al. 2021).
Further direct evidence for the positive effects of the microbiome on poultry production is observed with fecal microbiota transplantation (FMT) from high-laying hens to those with lower productivity. Low-producing hens receiving FMT had higher laying rates, with increased estradiol levels and anti-Mullerian hormone, decreased proinflammatory cytokine concentrations, and physical improvement in the intestinal lining (Cao et al. 2023). Moreover, reproductive performance-related genes were expressed in greater abundance with FMT from high-producing hens to low-producing hens, indicating beneficial effects, presumably from the bacterial populations in the high-producing hens (Cao et al. 2023). There are several targets of the microbiota, including their secretions, which engage molecular mechanisms (Fig. 4). Taken together, there is growing evidence for the influence of the microbiome on multiple physiological functions and the adaptive changes that can occur in the microbial composition associated with FMT.
Cecal microbiomes of breeders with high egg-laying performance have more diverse activities, which may be related to the metabolism and health of the host; and FMT from high-yield donors can increase the microbiota diversity and enrichment of Butyricicoccus, Enterococcus, Lactobacillus, jejunum health, and ovarian function to improve egg-laying performance. The SIRT1-related apoptosis and cytokine signaling pathway were involved in this process (from Cao et al. 2023, Creative Commons license – Elsevier Press).
Citation: Reproduction and Fertility 5, 3; 10.1530/RAF-23-0076
As more data are collected on domesticated birds, it is becoming increasingly clear that the gut microbiome, diet, nutrient absorption, and even the age of the individual are closely linked to overall health (Shang et al. 2018). Interestingly, there is an intriguing suggestion that behavior, such as dominance hierarchy in roosters, may relate to the production of metabolites and gut microbial composition (Chen et al. 2022). This potential correlation of social dominance, gut microbiome, and production of metabolites has implications for a brain–behavior–microbiome relationship that could affect productivity and overall health. Further, stressors such as extreme heat can promote inflammation and other deleterious physiological responses and conditions that adversely affect the health and function of the microbiome (Kikusato & Toyomizu 2023). Notably, the effects of stressors engage all aspects of an individual’s physiological homeostasis, making its functional responses extremely complex. However, some clear responses to stressors, especially those that are chronic, include adrenal activation with elevated stress hormones, reduced resistance to disease, impaired reproductive function, and disrupted nutrient uptake. Accordingly, stressors also have functional effects on the microbiome and intestinal mucosa that further contribute to the dysfunction and adverse effects on the health of the individual (Kikusato & Toyomizu 2023).
What is known about microbiomes in wild birds?
Studies in wild birds in field environment habitats fall into two categories: those that have the benefit of an experimental design, and more frequently the somewhat opportunistic sampling to understand species differences and effects of environment, migration, seasonal resources, and life stage. Opportunistic sampling has yielded important information and insights into the complexities of the interactions of individuals with their environment, responses that vary with life history, and reproductive strategies. Studies in great tits revealed age-dependent variation in gut microbiota associated with life history, productivity, and environmental factors related to habitat and site (Somers et al. 2023). Interestingly, nestlings were greatly affected by environmental factors. Studies on arctic shorebirds showed evidence for an exponential increase in gut microbial populations post hatching, with both diet and nesting materials contributing to the intestinal flora (Grond et al. 2017). In numerous neotropical birds, intestinal microbial populations were found to be highly variable in terms of taxon as well as influenced by habitat and diet (Hird et al. 2015). Samples taken from three colonies of Galapagos penguins (Spheniscus mendiculus) showed variations with developmental stage, with juveniles having reduced microbial alpha and beta diversity (Rohrer et al. 2023). Moreover, although not a strong trend, each colony had a characteristic overall microbial diversity, possibly owing to the specific diet at different sites or exposure to different environmental microbes.
Migratory birds have the added stress of long flights and seasonal changes in habitat and diet. Not surprisingly, there are changes in the microbiome of migratory birds at their wintering grounds, with a ‘habitat filter’ that allows the gut microbial population to adapt to changing resources (for reviews, see Song et al. 2022, Wang et al. 2022). Thus, it appears that phylogeny and local resources combine to promote adaptive changes in the gut microbial population, which could be a potential mechanism to ensure individual resilience to environmental stressors. There are multiple factors and environmental stressors that can affect the microbiome (Fig. 5), which taken together could affect individual health and that of populations (for review, see Sun et al. 2022).
Factors influencing microbiome composition at different body sites in birds (diagram modified from Sun et al. 2022).
Citation: Reproduction and Fertility 5, 3; 10.1530/RAF-23-0076
Influence of microbiome on immunity, reproduction, behavior, and antibiotic resistance
Immune system resilience and antibiotic resistance
The importance of a highly functional immune system is becoming more essential with climate change and other environmental stressors, such as habitat and resource loss. In addition, climate changes and increased human–wildlife conflict may amplify the risk of exposure to additional pathogens and their transmission. There is a potentially intriguing role for the microbiome as a complement to the immune system. Evidence for active communication between the intestinal tract and immune response is complex, with organized lymphoid structures (Peyer’s patches), lymphoid follicles, and mucosa-specific cells producing leukocytes (Kogut et al. 2020).
Most avian research has focused on the interaction of the microbiome with disease resistance and the potential threat, especially from migratory birds, of the spread of antibiotic-resistant microbes. This concern has been crystalized in studies that track the path of migratory species, their potential interaction with domestic fowl, and the likelihood of spreading pathogens (Prosser et al. 2013, 2016). As may be predicted, a comprehensive review of gut microbiomes found in migratory birds revealed variations in microbiome structure and function; however, the metabolic and functional characteristics were similar (Cao et al. 2020). More concerning was that migratory birds were found to have antimicrobial-resistant genes in their gut that could contribute to the spread of pathogens. In addition, cloacal viral populations (viromes) were found to be highly diverse, both in samples taken from wild birds and in birds housed in captivity or rehabilitation facilities (Shan et al. 2022). Similarly, the cloacal microbiota varied across species of wild ducks, with additional effects from influenza A viral infection (Hird et al. 2018). Although most studies measure either gut or cloacal microbiomes, it is important to recognize that consistent analysis of a consistent area (gut vs cloacal) will yield insights into the response of the individual to stressors and environmental factors. The gut microbiome is responsive to pathogenic bacteria and viruses, perhaps acting as part of an individual’s immune defenses. This conclusion is supported by findings in the domestic chicken in which the gut microbiome contains specific bacteria that participate in the immune response against pathogenic viruses (for review, see Abaidullah et al. 2019).
Interactions between the microbiome and pathogens; antimicrobials in the microbiome
As discussed previously, there are a multitude of cells in the intestinal lining that produce factors and immunoglobulins that reduce the risk of pathogenic infections. In addition, the intestinal mucosa has rich supplies of proteins active in the digestive process as well as inactivating deleterious products. All these functional contributions are critical to the overall health of the individual. Most intriguing is the role of the preen or uropygial gland, as discussed next. Importantly, the secretions of the preen gland are spread throughout the wings and body feathers, with the presence of products from antimicrobial and symbiotic biota providing essential benefits for the health and integrity of both the feathers and skin.
Linking reproduction and the avian microbiome
The microbiome underpins the health and function of physiological systems critical to successful reproduction. Unsurprisingly, some of the most compelling and complete information comes from studies conducted in domestic poultry. These data relate nutrition, growth, and productivity to characteristics of gut microbial communities. For example, highly productive laying hen flocks had shifting bacterial communities over the production lifespan that were observed both in the gut and in the respiratory tract (Ngunjiri et al. 2019). Similarly, tree swallows (Tachycineta bicolor) showed increased cloacal microbiome diversity in females that had increased sexual activity in response to exogenous estradiol (Hernandez et al. 2021). The latter study’s authors also observed age-related differences in cloacal microbial communities, suggesting that there are potentially direct linkages in breeding individuals and in successful breeding individuals over their reproductive lifespan. Similarly, there were alterations in gut microbiomes with sex and season in murres (Uria lomvia) (Góngora et al. 2021). An interesting observation is that made by Velando and colleagues (2021), who found a correlation of telomere length with the microbiota, with greater commensal bacterial populations related to longer telomere length, and possibly offspring health and survival, in hatchling yellow-legged gulls (Larus michahellis). This is an interesting observation that may indicate lifelong health effects from early microbiome constitution.
Behavioral linkages to the gut microbiome
Behavioral linkages to the microbiome in birds are still rather nebulous. There are reports of increased exploratory behavior correlating with higher microbiome alpha diversity in wild house sparrows (Passer domesticus) (Florkowski & Yorzinski 2023). This study is particularly notable because of the relationship between increased diversity in the gut microbial composition (alpha diversity) and increased exploratory behavior, suggesting that exploration and perhaps greater exposure to other individuals, novel dietary resources, and environments may be beneficial for individual health. Avian species also exhibit behavioral changes during the breeding season, which could be associated with microbiome composition changes. The breeding season has been shown to relate to changes in the cloacal microbiome in rufous-collared sparrows (Zonatrichia capensis), with greater diversity in males at the start of the breeding season (Escallón et al. 2019). Because cloacal contact in birds is the primary form of fertilization, there is a high probability of transfer of microbes between pairs, which could potentially increase the female’s cloacal microbial diversity. Interestingly, the cloacal microbiome beta diversity composition of male rufous-collared sparrows increased when they transitioned into breeding condition and then similarly decreased when reverting to non-breeding status. Further, a trend was noted between circulating testosterone levels and greater cloacal microbiome diversity.
Is there a link between circulating hormones and the microbiome of an individual?
The relationship of circulating hormones to the status of the microbiome has also been considered relative to the role of stressors in potentially influencing the microbial populations. As shown by Noguera et al. (2018), corticosterone treatments to simulate glucocorticoid secretion by the adrenal in response to stress suppressed several microbial taxa in the yellow-legged gull. Compelling supporting evidence gained from studies in captive house sparrows demonstrated that gut microbiomes in stressed birds had a relative increase in bacteria associated with inflammatory responses and a loss of taxa associated with beneficial effects (Madden et al. 2022). Domestic chickens (Gallus gallus) exhibiting dysfunctional behaviors, including feather pecking, also had altered gut microbiome composition, suggesting an intestinal alteration in serotonin synthesis (Jadhav et al. 2022). Furthermore, for wild birds, proximity to urban environments may act as a stressor affecting health and survival. In American white ibises (Eudocimus albus)in south Florida, birds with greater contact with urban environments exhibited altered gut microbiota (Murray et al. 2020). Similar observations have been found for mourning doves (Zenaida macroura) living in urban areas (Mohr et al. 2022). Additionally, these urban-related shifts in the microbial composition may encourage the promotion of pathogens (Murray et al. 2020). The question is if these changes in the microbiome composition of birds are directly influenced by the urbanization of their habitat or whether there are other influencing factors, such as pollutants and changes in the individuals’ diet due to the availability of anthropogenic food sources and waste.
Impacts of global environmental changes and pollutants on avian microbiomes
Effects of environmental chemicals
Relatively little information is available about the direct effects of environmental pollutants and toxicants on the microbiome in wildlife, including birds (for review, see Handy et al. 2023). In poultry, fungal contaminants, such as zearalenone, produce a metabolite with well-documented adverse effects on health and productivity (Yuan et al. 2022). In laying hens, contamination by zearalenone resulted in impaired production accompanied by significant inhibition of reproductive hormones and altered composition and functional changes in the microbiome (Yuan et al. 2022). Interestingly, this study also revealed reduced overall bacterial diversity, with altered abundance in some genera making up the microbiota. Similarly, there were documented effects of glyphosate herbicides on lifetime reproductive traits but not productivity in Japanese quail (Coturnix japonica), despite altered gut microbiome composition in an age- and gender-related manner (Ruuskanen et al. 2020). Studies that consider both environmental chemicals and effects on the microbiome in wild birds are less available. Exposure to microplastics is an emerging ubiquitous contaminant, especially for seabirds. Fackelmann et al. (2023) reported that wild northern fulmars (Fulmarus glacialis) and Cory’s shearwaters (Calonectris borealis) had altered gut microbial diversity that correlated with gut microplastics. More compelling, this study documented increased pathogenic, antibiotic-resistant, and plastic-degrading microbes. Studies that integrate environmental chemical stressors with microbiota populations and health will provide important insights into the drivers of healthy wild avian populations.
Habitat, resources, and conservation: a focus on raptors and specific scavengers
In addition to increasing adverse effects from exposure to environmental chemicals, wild birds are subjected to other stressors, including loss of habitat, altered resource availability, and other anthropogenic effects associated with human communities. Few studies have reported the relationship of microbiomes to health and reproduction in raptors. One study in barn owls (Tyto alba) documented the relationship of sex differences in the diversity of bacterial populations (Corl et al. 2020). Additionally, those individuals that showed greater movement behavior had greater diversity in their microbiome, possibly owing to their exposure to a wider variety of habitats. We could expect to see similar patterns in other wide-ranging species, such as African vultures. The current vulture crisis in Africa is just one example of the collision of environmental stressors, human anthropogenic damage, and the loss of vibrant and healthy bird populations worldwide. Figure 6 illustrates the position of raptors and in particular obligate scavengers such as vultures in the ecosystem, illustrating a key question: How do scavengers resist exposure to and infection from a wide variety of highly pathogenic bacteria and viruses? Raptors are at higher levels of the food chain, given that they feed on other vertebrates, and therefore would be exposed to a range of pathogens and bioaccumulation of chemical contaminants and toxins. Moreover, vultures and other scavengers play an essential role in the ecosystem as the cleanup crew for anthrax and other pathogenic bacteria and viruses (van den Heever et al. 2021).
Top predators and scavengers, such as the vulture, are subjected to a host of bacteria, many of which are highly pathogenic. Microbiomes in birds, and particularly in scavengers, may be a key component in maintaining health and immune function in these species (from Krüger et al. 2022).
Citation: Reproduction and Fertility 5, 3; 10.1530/RAF-23-0076
Conclusion and future perspectives
There are large gaps in our understanding of the role and function of microbiomes in birds. Domestic poultry have exquisitely defined genetic, nutritional, and production characteristics that provide the basis for studies on the role of the gut microbiome. The current advances in molecular techniques, allowing for the rapid cataloging of taxa, have led to an increase in the number of studies focusing on the microbial makeup of different body sites and within and between species. Our review highlights microbiomes as an integral part of all aspects of avian biology. We include studies reporting associations with gut microbiomes and reproductive health, breeding status, and productivity (including egg-laying potential and offspring survival). In addition, studies on domesticated birds are extremely useful in gaining an understanding and characterizing the microbiomes of wild species.
Technical advances now allow for the rapid cataloging of taxa that make up the microbiome. Accumulation of data from a diversity of bird species across a variety of environmental conditions will move the field forward from basic association descriptions to a greater understanding of the impact of different microbes on the health and behavior of birds. An important aspect of avian microbiomes that needs further study relates to the interplay between disease and microbiome composition, particularly relating to vultures and other avian scavengers.
Raptors, and in particular vultures, appear to have unique adaptations pertaining to the functional role of their microbiome. Utilizing a comparative approach is important to gain an understanding of nutritional processes across a range of species and food resource utilization (Bodawatta et al. 2022; Martinez-Hernandez et al. 2023). In the case of obligate scavengers, such as vultures, there are important questions pertinent to humans and wildlife. Given that these scavengers provide protection from pathogens, they are essential to the resilience of the ecosystem. But how do scavengers neutralize these pathogens so that they don’t suffer ill effects? Is there something specific in their microbial composition and function that allows them to feed on these pathogen-laden carcasses? Furthermore, can information about the microbiome in the gut be used to develop treatment strategies for humans to combat pathogens and a range of infectious agents? Questions about specific microbiomes in glands, such as the preen gland, are also of interest because of the evidence for antimicrobial actions by the secretory products.
With further recognition of the close interrelationship between wildlife and humans, and the deleterious anthropogenic effects associated with human populations, it is important to develop strategies to conserve wildlife health and ecosystem resilience, such as through a One Health conceptual framework. Future research should focus on monitoring microbial changes with species movements to track the spread of pathogens and antimicrobial-resistant microbes. Collecting monitoring data for wildlife species, including migratory birds, along with associated metadata, will help define the environmental stressors and conditions that are essential for wildlife health. These data will inform conservation efforts and enable managers of protected areas to assess wildlife health and evaluate the efficacy of management and remediation programs.
Declaration of interest
The authors declared that there is no conflict of interest that could be perceived as prejudicing the impartiality of this review.
Funding
Some of the initial work was supported by our National Socio-Environmental Synthesis Center (SESYNC) ‘Saving African Vultures’ project. This review was supported in part by the SESYNC under funding received from the National Science Foundation DBI-1052875. Otherwise, this article did not receive any specific grant from any funding agency in the public, commercial, or not-for-profit sector.
Author contribution statement
MAO wrote the initial draft of the review; all coauthors provided edits to the subsequent versions of the draft manuscript and approved the final submission; MAO and SM conceived the study in vultures; SM, SWM, and LC provided technical capabilities and insight into microbiome research; SK and BC are critical as field biologists, collaborators, and for providing their extensive experiences and capabilities in conducting the field research.
Acknowledgements
We are grateful to the African Birds of Prey Sanctuary for allowing us to sample captive vultures, to Ben Hoffman from Raptor Rescue for allowing us to sample rehab birds, and to the staff from Wildlife ACT and Ezemvelo KZN Wildlife who assisted with the capture of wild birds.
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