Avian Reproduction Research Articles

Increased Reproductive Output and Telomere Shortening Following Calcium Supplementation in a Wild Songbird.

Life history theory predicts increased parental investment comes with fitness costs, often expressed as negative effects on survival and future reproduction. To better understand the costs of reproduction and life history trade-offs, we evaluated calcium supplementation at a high-elevation site in Colorado as a novel approach to experimentally alter reproductive investment in nesting female Tachycineta bicolor (tree swallow). Calcium is a nutrient critical to avian reproduction as the intake of natural calcium is essential for egg production, embryo development, and nestling growth. Altering calcium availability exclusively during the breeding season allowed examination of individual biological responses to experimental modification of reproduction, as well as the reproductive costs associated with egg production and laying an entire clutch. As a functional endpoint and proxy for fitness and longevity, telomere length was measured at the beginning and end of each breeding season. Telomeres-protective "caps" at the ends of chromosomes-have been shown to shorten with aging and a variety of stressors, including higher reproductive output. Results demonstrate that tree swallow mothers supplemented with calcium during the breeding season experience higher reproductive output and produce offspring with longer telomeres, which came at the cost of relatively shorter telomeres during the reproductive season. These findings provide additional support for reproductive trade-offs, and also challenge previous calcium supplementation studies that suggest excess calcium reduces the cost of reproduction.

Integrating adverse effects of triazole fungicides on reproduction and physiology of farmland birds

The extensive use of pesticides has been recognized as one of the major factors negatively impacting birds in agricultural habitats. One of the pesticide groups most used worldwide are triazole fungicides due to their effectiveness in controlling phytopathogenic fungi in cereals, vineyards and orchards. In the last decades, different experimental studies have reported important negative effects on the health and fitness of birds after exposure to triazoles. Birds can be exposed throughout the year through different routes, including oral uptake, dermal contact with treated surfaces and inhalation by overspray. Yet, the ingestion of treated or sprayed material is the principal route. The most alarming effect of triazoles, which can even occur several months after cessation of the exposure, is the decreasing reproductive outputs of birds, including delay in the onset of laying dates, reduced clutch size and hatching rate, and increased mortality of chicks. In order to synthesize the data and knowledge about the toxic effects of triazoles at different levels of biological organization, here we propose an dverse outcome pathway (AOP) on the mechanisms by which triazoles can affect avian reproduction and physiology. The reported effects highlight that the current risk assessment needs some improvements to avoid undesired effects on birds, especially long‐term effects that can influence stability and viability of avian populations from agricultural habitats.

Integrating Genomics and Transcriptomics to Identify Candidate Genes for Egg Production in Taihe Black-Bone Silky Fowls (Gallus gallus domesticus Brisson).

The Taihe Black-Bone Silky Fowl (Gallus gallus domesticus Brisson) possesses significant value in terms of consumption, medicinal applications, and ornamental appeal, representing a precious genetic resource and traditional Chinese medicinal material. However, considerable variation exists within populations regarding egg-laying performance. This study integrates a whole-genome selection signal analysis (SSA) with a transcriptome analysis to identify genes associated with egg-laying traits in Taihe Black-Bone Silky Fowls. We identified 31 candidate genes under selection from the high-yield chicken (HC) and low-yield chicken (LC) groups. Additionally, through RNA-seq analysis, 257 common differentially expressed genes (DEGs) were identified from four comparative groups. Two overlapping genes-LPL and SETBP1-were found in both the selected gene and DEG lists. These selected genes and DEGs were enriched in pathways related to ovarian development, including the lysosome pathway, the ECM-receptor interaction pathway, the TGF-beta signaling pathway, the Wnt signaling pathway, the PPAR signaling pathway, and the glycerolipid metabolism pathway. These research findings contribute to the breeding of Taihe Black-Bone Silky Fowls with high egg production traits and provide a theoretical foundation for exploring the regulatory mechanisms of avian reproduction.

Microbiomes in Birds: A Review of Links to Health and Reproduction.

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 such 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.

The role of climatic variables on nest evolution in tanagers.

Avian nests are fundamental structures in avian reproduction and face strong selective forces. Climatic conditions are likely to have shaped the evolution of specific nest traits, but evidence is scarce at a macroevolutionary level. The Thraupidae family (commonly known as tanagers) is an ideal clade to understand the link between nest architecture and climate because it presents wide variation in nest traits. To understand whether climatic variables have played a role in the diversification of nest traits among species in this family, we measured nests from 49 species using museum collections. We observed that dome-nesting species are present in dryer and hotter environments, in line with previous findings suggesting that domed nests are a specialisation for arid conditions. We also found evidence that nests with thicker walls are present in locations with lower precipitation and that solar radiation can influence the shape of domed nests; birds tend to build shorter and narrower domes in areas with high levels of solar radiation. Open nest architecture is also potentially influenced by wind speed, with longer and deeper nests in areas characterised by strong winds. Our results support the hypothesis that different climatic variables can drive the evolution of specific aspects of nest architecture and contribute to the diversity of nest shapes we currently observe. However, climatic variables account only for a small fraction of the observed structural variation, leaving a significant portion still unexplained.

Effects of the temperature during embryonic development on adult reproduction and the phenotype of the second generation in zebra finches

Across taxa, the temperature experienced by individuals early in life can have large effects on their development. However, comparatively little is known about whether the effects of this thermal developmental environment can be long-lasting or transgenerational. In birds, one important aspect of the developmental environment is incubation and, in general, eggs incubated at low temperatures produce offspring with smaller morphology, suboptimal physiology, and even lower long-term survival. Yet, little is known about whether incubation temperature may affect avian reproduction in adulthood, and nothing is known about whether the effects of avian incubation temperature may be transgenerational. To investigate this, we incubated zebra finch (Taeniopygia guttata) eggs at two different temperatures: 37.5 °C (‘control’) and 36.3 °C (‘low’), raised nestlings until adulthood, and allowed same-temperature treatment pairs to reproduce. We found that F1 individuals incubated at the low temperature had shorter beaks at the start of reproduction than those incubated at the control temperature. Further, compared to those from control parents, F2 offspring from parents incubated at the low temperature had lighter body masses at 5 days-old and had shorter beaks at 30 days-old. However, we found little evidence that incubation temperature affected other aspects of reproduction, with no effect on latency to lay, clutch size, egg mass, incubation period, hatching success/asynchrony, fledging, or the number of offspring that ultimately survived until independence. Overall, we found some evidence that a difference in the early thermal developmental environment can have lasting morphological effects into the next generation. However, future work is needed to determine whether the incubation temperature that birds experience as embryos may influence parental care behaviors or lifetime reproductive success.

Attaching organic fibers to mineral: The case of the avian eggshell

Bird eggs possess a mineralized eggshell with a soft underlying fibrous membrane. These dissimilar material layers successfully evolved a structural attachment to each other as a conserved avian reproduction strategy essential to avian embryonic development, growth, and hatching of the chick. To understand how organic membrane fibers attach to shell mineral (calcite), 3D multiscale imaging including X-ray and electron tomography coupled with deep learning-based feature segmentation was used to show how membrane fibers are organized and anchored into shell mineral. Whole fibers embed into mineral across the microscale, while fine mineral projections (granules/spikes) insert into fiber surfaces at the nanoscale, all of which provides considerable surface area and multiscale anchorage at the organic-inorganic interface between the fibrous membrane and the shell. Such a reciprocal anchorage system occurring at two different length scales between organic fibers and inorganic mineral provides a secure attachment mechanism for avian eggshell integrity across two dissimilar materials.

Agriculture and hot temperatures interactively erode the nest success of habitat generalist birds across the United States.

Habitat conversion and climate change are fundamental drivers of biodiversity loss worldwide but are often analyzed in isolation. We used a continental-scale, decades-long database of more than 150,000 bird nesting attempts to explore how extreme heat affects avian reproduction in forests, grasslands, and agricultural and developed areas across the US. We found that in forests, extreme heat increased nest success, but birds nesting in agricultural settings were much less likely to successfully fledge young when temperatures reached anomalously high levels. Species that build exposed cup nests and species of higher conservation concern were particularly vulnerable to maximum temperature anomalies in agricultural settings. Finally, future projections suggested that ongoing climate change may exacerbate the negative effects of habitat conversion on avian nesting success, thereby compromising conservation efforts in human-dominated landscapes.

Nestling growth rate and food consumption increases under experimentally prolonged daylength in a New World sparrow

When evaluating avian reproduction, life history theory examines the trade‐offs between parental effort, the number and size of offspring, and the rate of nestling development. The growth rates and body sizes of developing birds vary geographically and can diverge with both latitude and migratory strategy. In terms of offspring size, growth rate can deviate in nestlings of the same or similar species due to the correlated influences of weather events, predation pressure, food availability, number of nestmates and parental provisioning. Furthermore, a longer photoperiod for species nesting at higher latitudes increases the duration over which a nestling can be fed each day, and increased nestling provisioning has been positively correlated with growth rate. Whether the amount of time a bird is fed during development drives this variation in growth rate and morphology is unknown. By removing supplemental environmental stressors (e.g. weather, predation) and standardizing feeding rate and environment, we explored the influence of daily duration of nestling provisioning on dark‐eyed junco Junco hyemalis nestlings. We hand‐reared 65 chicks of a sedentary junco subspecies J. h. carolinensis under both their natural photoperiod and the longer photoperiod of a closely related migratory subspecies J. h. hyemalis and compared growth rate, mass, morphology and the amount of food consumed. Average growth rate, fasted mass, wing length and total daily food consumption were all greater in birds hand‐reared under the longer, more northern photoperiod treatment. These findings suggest that increased daily photoperiod at higher latitudes may allow for greater total food provisioning and thus may play a role in the ability of parents in compressed breeding seasons to produce high quality offspring. This points to a trade‐off between provisioning effort and nestling growth rate in lower latitude (shorter photoperiod) populations and points to an important role of developmental plasticity on growth rate and morphology.

Physiological impacts of chronic and experimental Plasmodium infection on breeding-condition male songbirds

While Plasmodium parasitism is common in songbirds, its impact on avian reproduction is unclear owing to conflicting reports in the existing literature. Particularly understudied is the impact of phase of infection on variation in host reproductive physiology in wild, breeding-condition birds. However, assessing the full impact of Plasmodium on reproductive success in the wild can be difficult because individuals experiencing severe effects of parasitism may not enter the breeding population and may be less likely to be captured during field studies. To address these factors, we quantified metrics of health and reproductive physiology in wild-caught, breeding-condition male dark-eyed juncos (Junco hyemalis hyemalis) before and after experimental Plasmodium inoculation in a captive setting. Metrics of health and reproductive physiology included activity rate, hematocrit, scaled body mass, testosterone and sperm production. Individuals already infected at capture (i.e., chronically infected) had higher levels of hematocrit than males without chronic infections. Experimentally infected males showed a larger reduction in hematocrit and activity rate as compared to controls. However, chronic infection status did not influence the extent of metric decline. Testosterone production did not vary by treatment and most birds produced sperm following inoculation. Broadly, our results suggest that male juncos exposed to Plasmodium during the breeding season likely experience declines in general health, but Plasmodium infections do not negatively impact reproductive physiology. We conclude that physiological tradeoffs in males may favor maintenance of reproductive function despite infection.

Complex relationships between climate and reproduction in a resident montane bird.

Animals use climate-related environmental cues to fine-tune breeding timing and investment to match peak food availability. In birds, spring temperature is a commonly documented cue used to initiate breeding, but with global climate change, organisms are experiencing both directional changes in ambient temperatures and extreme year-to-year precipitation fluctuations. Montane environments exhibit complex climate patterns where temperatures and precipitation change along elevational gradients, and where exacerbated annual variation in precipitation has resulted in extreme swings between heavy snow and drought. We used 10 years of data to investigate how annual variation in climatic conditions is associated with differences in breeding phenology and reproductive performance in resident mountain chickadees (Poecile gambeli) at two elevations in the northern Sierra Nevada mountains, USA. Variation in spring temperature was not associated with differences in breeding phenology across elevations in our system. Greater snow accumulation was associated with later breeding initiation at high, but not low, elevation. Brood size was reduced under drought, but only at low elevation. Our data suggest complex relationships between climate and avian reproduction and point to autumn climate as important for reproductive performance, likely via its effect on phenology and abundance of invertebrates.

Camelthorn and blackthorn trees provide important resources for Southern Pied Babblers (Turdoides bicolor) in the Kalahari

In the southern Kalahari Desert, cooperatively breeding Southern Pied Babblers Turdoides bicolor frequently build their nests and forage in camelthorn trees Vachellia erioloba, a keystone species in the region, and blackthorn trees Senegalia mellifera, a widespread early successional shrub. Using Ivlev's electivity indices (Ei), we show that Southern Pied Babblers preferentially nest in camelthorn trees and preferentially forage in or under camelthorn and blackthorn trees. Southern Pied Babblers primarily forage on the ground; however, they will make use of arboreal resources when these are available. We observed the birds spending the highest proportion of foraging time off the ground during October, when breeding is also most common, compared with all other months within the austral summer breeding season. They are most likely to be observed foraging in camelthorn trees earlier in the breeding season and blackthorn trees later in the breeding season. We demonstrate that Southern Pied Babblers have a strong relationship with camelthorn trees, in which they prefer to both nest and forage. We highlight the importance of protecting camelthorn trees, a keystone species in the region, as part of the conservation and management of endemic Kalahari fauna such as the Southern Pied Babbler. In addition to contributing to the literature on keystone species, our observations raise questions about the ways in which avian reproduction in the arid zone could be decoupled from rainfall via the phenology of deep‐rooted tree species.

Gradual changes in model shape affect egg-directed behaviours by parasitic shiny cowbirds Molothrus bonariensis in captivity.

Eggs are critically important for avian reproduction as all birds are oviparous. Accordingly, the recognition and care of own eggs represent the cornerstones of avian breeding, whereas the elimination of foreign objects, including brood-parasitic eggs and non-egg items from the nest are known to also increase fitness by refocusing incubation effort on the parents' own eggs. But egg recognition also plays a role in some avian obligate brood parasites' reproductive strategy through the pecking of already present eggs in the hosts' clutch to reduce nestmate competition with the parasite's own hatchling. Here we tested egg shape recognition in this parasitic egg-pecking context by exposing two different series of 3D printed models to captive obligate brood-parasitic shiny cowbirds (Molothrus bonariensis) in artificial nests. Natural egg-shaped models were pecked more often compared with increasingly thinner models, but there was no effect of increasing angularity on pecking rates, implying that a natural, rather than an artificial, range of variability elicited adaptive responses from parasitic cowbirds.

Patterns in avian reproduction in the Prudhoe Bay Oilfield, Alaska, 2003–2019

The Arctic Coastal Plain is one of the most important avian breeding grounds in the world; however, many species are in decline. Arctic‐breeding birds contend with short breeding seasons, harsh climatic conditions, and now, rapidly changing, variable, and unpredictable environmental conditions caused by climate change. Additionally, those breeding in industrial areas may be impacted by human activities. It is difficult to separate the impacts of industrial development and climate change; however, long‐term datasets can help show patterns over time. We evaluated factors influencing reproductive parameters of breeding birds at Prudhoe Bay, Alaska, 2003–2019, by monitoring 1265 shorebird nests, 378 passerine nests, and 231 waterfowl nests. We found that nest survival decreased significantly nearer high‐use infrastructure for all guilds. Temporally, passerine nest survival declined across the 17 years of the study, while there was no significant evidence of change in their nest density. Shorebird nest survival did not vary significantly across years, nor did nest density. Waterfowl nest density increased over the course of the study, but we could not estimate nest survival in all years. Egg predator populations varied across time; numbers of gulls and ravens increased in the oilfields 2003–2019, while Arctic fox decreased, and jaeger numbers did not vary significantly. Long‐term datasets are rare in the Arctic, but they are crucial for understanding impacts to breeding birds from both climate change and increasing anthropogenic activities. We show that nest survival was lower for birds nesting closer to high‐use infrastructure in Arctic Alaska, which was not detected in earlier, shorter‐term studies. Additionally, we show that Lapland longspur nest survival decreased across time, in concert with continent‐wide declines in many passerine species. The urgency to understand these relationships cannot be expressed strongly enough, given change is continuing to happen and the potential impacts are large.

Development of a mechanistic model for analyzing avian reproduction data for pesticide risk assessment

Mechanistic effect models are increasingly recommended as tools for refining evaluations of risk from exposure to pesticides. In the context of bird and mammal risk assessments, DEB-TKTD models have been recommended for characterizing sublethal effects at lower tiers. However, there are currently no such models. Currently, chronic, multi-generational studies are performed to characterize potential effects of pesticides on avian reproduction, but it is has not been established to what extent results from these studies can inform effect models. Here, a standard Dynamic Energy Budget (DEB) model was extended to account for the avian toxicity endpoints observed in regulatory studies. We linked this new implementation to a toxicological module to capture observed pesticide effects on reproduction via a decreased efficiency of egg production. We analysed ten reproduction studies with five different pesticides conducted with the mallard (Anas platyrhynchos) and the northern bobwhite (Colinus virginianus). The new model implementation accurately distinguished between effects on egg production from direct mechanism of toxicity and from food avoidance. Due to the specific nature of regulatory studies, model applicability for risk refinement is currently limited. We provide suggestions for next steps in model development.

Overwinter users of nest cavities affect breeding birds via nest‐dwelling ectoparasites

AbstractCavities used for avian reproduction in spring often host other organisms for roosting during winter, which should affect their microclimatic conditions and, then, the patterns of emergence of nest‐dwelling ectoparasites of birds and successful parasitism. To prove these cascade effects, we experimentally blocked the entrance of half of nest boxes previously used for reproduction by hoopoes (Upupa epops), recorded temperature and humidity during the fall–winter period, and evaluated abundance, emergence of ectoparasitic flies (Carnus hemapterus), and intensity of parasitism in hoopoe nestlings growing in open and blocked nest boxes the next spring. As expected, experimental treatment as well as the occupancy of open nest boxes by rodents (i.e., mainly dormice [Eliomys quercinus]) affected temperature and humidity, but did not predict the onset or duration of Carnus emergence. Moreover, flies were more abundant in open nest boxes and, among them, those occupied by dormice showed the lowest abundance. Finally, hoopoe nestlings developing in nest boxes blocked during winter experienced lower intensity of ectoparasitism than those in open nest boxes. These hitherto undescribed cryptic effects of overwinter occupants of nest cavities on subsequent emergence and viability of nest‐dwelling ectoparasites would profoundly impact on the interaction with their avian hosts.

Ground nesting in passerine birds: evolution, biogeography and life history correlates

Nest location is one of the key components of avian reproduction and sharp transitions between different nest location strategies may have profound ecological and evolutionary consequences. Here, we used a phylogenetically‐informed comparative framework to reconstruct the evolution of ground nesting behaviour in passerine birds, quantify its biogeographical and habitat variation, and test for its associations with life history traits. Our dataset comprised over 1600 species distributed worldwide and representing ca 90% of all extant passerine families. Our analyses revealed a scattered phylogenetic distribution and moderate phylogenetic signal in the occurrence of ground nesting in passerines. We also found relatively high forward and backward transitions rates between character states of ground and non‐ground nesting, indicating strong evolutionary lability. Non‐ground nesting was identified as a likely ancestral state at the root of passerine phylogeny. Occurrence of ground nesting was clearly associated with habitat variation, as open habitats generally supported greater proportion of ground nesting species than non‐open habitats (forests). Within the major habitat categories we found greater proportion of ground nesters in boreal and temperate than subtropical and tropical zones. This reflected a general latitudinal gradient in the occurrence of ground nesting, with higher proportion of ground nesting species at higher latitudes (especially at the northern hemisphere). Ground nesting was also associated with fast life histories, as ground nesters had larger clutches, shorter incubation periods and faster chick development rates than non‐ground nesters. This variation was possibly driven by higher predation rates on nestlings and adult birds in ground nesting species. Our study lays a foundation for a comprehensive understanding of mechanisms and processes that have driven macroevolution of ground nesting behaviour in the most species‐rich extant avian lineage.

Molecular characterisation and expression profile of the PRLR gene during goose ovarian follicle development

ABSTRACT 1. Although PRL-PRLR signalling plays important roles in regulating avian reproduction, there is a paucity of information regarding the functional significance of PRLR in goose ovarian follicle development. 2. The full-length 2,496 bp coding sequence of PRLR was obtained from Sichuan White goose (Anser cygnoides) for the first time and was seen to encode a polypeptide containing 831 amino acids. Goose PRLR shares similar sequence characteristics and conserved functional domains to other avian species and was phylogenetically clustered into the avian clade. 3. The qPCR results suggested that the mRNA levels of PRLR significantly increased in primary follicles during weeks 3 to 4 of age and were higher in secondary- than in primordial follicles at week 5 post-hatching, which suggested that the PRLR-mediated signalling could be involved in regulation of early folliculogenesis. 4. The PRLR mRNA was expressed at the highest levels in the prehierarchical 8–10 mm granulosa layers throughout goose ovarian follicle development, indicating a role for PRLR in the process of follicle selection. 5. PRLR mRNA was differentially expressed in the three cohorts of in vitro cultured granulosa cells harvested from different sized goose ovarian follicles, which suggested that PRLR was involved in regulating granulosa cell functions depending on the stage of follicle development. These data provide novel insights into the role of PRLR during goose ovarian follicle development, although the underlying mechanisms await further investigations.

Symbiotic microbes play a role more important than preen gland in avian pheromone production––A review

The uropygial gland or preen gland is a complex holocrine structure present only in birds, and plays an important role in avian communication and reproduction. This gland produces preen oil, which helps birds maintain intact plumage, plumage colorage, but also possesses antibacterial and anti-predator properties, and the evidence for these claims is still in infancy. Preen gland harbour a large number of microbiota among which as many as 110 are bacterial genera dominated by Firmicutes, Proteobacteria, Bacteroidetes, etc., families, and the roles of these microbes are largely unknown. However, these microbes are believed to maintain symbiotic relationship with the host and exert positive effects in the host’s physiology and behaviour. Many studies have proven that these microbes produce chemical cues as metabolic by-products that modulate the host’s behavior. In birds, these symbiotic microbes are needed for normal growth, development and even reproduction. Earlier findings about preen gland microbiota of birds connect it to good feather condition, recent evidences connect it to antifungal and antimicrobial activities. Although preen gland plays a major role in bird’s development, symbiotic microbes of preen gland seem to play a crucial role in reproduction and pheromonal communication. Here, we review the role of microbes present in avian preen gland in production of chemical signals and document the relationship between the microbes and preen gland in chemical communication.

Predicting the probability of avian reproductive success and its components at a nesting site

Avian reproduction has four prime components: nesting, mating, hatching, and fledging. Predicting the probability of individual components helps in identifying the period of reproduction that would benefit from an increased conservation effort. Identification of biotic, abiotic, and sociological variables of the nesting sites is essential to calculate the component-wise success probabilities. There is no standard methodology to estimate these probability values separately. This study proposes a methodology to estimate the success probability of each component, identifies correlated environmental predictors, and provides a modelling framework to accurately predict the nesting success probabilities using Merops philippinus as a model species. Primary surveillance data and the proposed methodology indicate that the time window between the bird's nesting and mating is most vulnerable to environmental fluctuations. Both biotic and abiotic factors are crucial determinants of nesting success. Sociological factors also play a crucial role in determining the probabilities of these successes. Mating, hatching, and fledging success depend more on biotic factors than abiotic ones. Linear modelling frameworks are helpful in exploring which types of environments are better determinants of the success of a reproductive component. Artificial neural networks are useful in predicting mating, nesting, and overall reproductive success probabilities. Though the models in this study are developed using Merops philippinus data, the proposed methodology and modelling framework is also applicable for other bird species.