SnapShot: Branching Morphogenesis.

Ectodermal appendages such as feathers, hair, mammary glands, salivary glands, and sweat glands form branches, allowing much-increased surface for functional differentiation and secretion. Here, the principles of branching morphogenesis are exemplified by the mammary gland and feathers.

Observed declines in body size have differential effects on survival and recruitment, but no effect on population growth in tropical birds.

Declines in body size can be an advantageous physiological response to warming temperatures, or a result of physiological and nutritional stress. Either way, studies often assume that these climate-induced trait changes have important implications for fitness and demography. We leveraged almost three decades of capture-mark-recapture data of 51 bird species in Panama to examine if body size has changed through time, how sensitive body size is to changes in weather, and if body size impacts population demography. We evaluated two metrics of body size, structural size (wing length), and body condition (residual body mass). Over the study, wing length changed in varying directions for 88% of species (23 decrease, 22 increase), but the effects were weak, and change was only significant for two species. Conversely, body condition declined for 88% of species (45), effects were stronger, and that change was significant for 22% of species (11). This suggests that nutritional stress is likely the cause of changes in body size, not an adaptive response to warming. Precipitation metrics impacted body condition across three of our four feeding guilds, while wing length was only impacted by weather metrics for two guilds. This suggests that body condition is more sensitive to change in weather metrics compared to wing length. Lastly, we found that the impact of changes in body size on survival and recruitment was variable across species, but these relationships were in the opposite direction, ultimately resulting in no change in population growth for all but one species. Thus, while different stages (adult survival and recruitment) of populations may be impacted by body size, populations appear to be buffered from changes. The lack of an effect on population growth rate suggests that populations may be more resilient to changes in body size, with implications for population persistence under expected climate change.

Early-life environmental effects on birds: epigenetics and microbiome as mechanisms underlying long-lasting phenotypic changes.

Although the long-lasting effects of variation in early-life environment have been well documented across organisms, the underlying causal mechanisms are only recently starting to be unraveled. Yet understanding the underlying mechanisms of long-lasting effects can help us predict how organisms will respond to changing environments. Birds offer a great system in which to study developmental plasticity and its underlying mechanisms owing to the production of large external eggs and variation in developmental trajectories, combined with a long tradition of applied, physiological, ecological and evolutionary research. Epigenetic changes (such as DNA methylation) have been suggested to be a key mechanism mediating long-lasting effects of the early-life environment across taxa. More recently, changes in the early-life gut microbiome have been identified as another potential mediator of developmental plasticity. As a first step in understanding whether these mechanisms contribute to developmental plasticity in birds, this Review summarizes how changes in early-life environment (both prenatal and postnatal) influence epigenetic markers and the gut microbiome. The literature shows how both early-life biotic (such as resources and social environment) and abiotic (thermal environment and various anthropogenic stressors) factors modify epigenetic markers and the gut microbiome in birds, yet data concerning many other environmental factors are limited. The causal links of these modifications to lasting phenotypic changes are still scarce, but changes in the hypothalamic-pituitary-adrenal axis have been identified as one putative pathway. This Review identifies several knowledge gaps, including data on the long-term effects, stability of the molecular changes, and lack of diversity in the systems studied, and provides directions for future research.

Self-assembly of biological networks via adaptive patterning revealed by avian intradermal muscle network formation.

Networked structures integrate numerous elements into one functional unit, while providing a balance between efficiency, robustness, and flexibility. Understanding how biological networks self-assemble will provide insights into how these features arise. Here, we demonstrate how nature forms exquisite muscle networks that can repair, regenerate, and adapt to external perturbations using the feather muscle network in chicken embryos as a paradigm. The self-assembled muscle networks arise through the implementation of a few simple rules. Muscle fibers extend outward from feather buds in every direction, but only those muscle fibers able to connect to neighboring buds are eventually stabilized. After forming such a nearest-neighbor configuration, the network can be reconfigured, adapting to perturbed bud arrangement or mechanical cues. Our computational model provides a bioinspired algorithm for network self-assembly, with intrinsic or extrinsic cues necessary and sufficient to guide the formation of these regenerative networks. These robust principles may serve as a useful guide for assembling adaptive networks in other contexts.

An Overview of the Current Known and Unknown Roles of Vitamin D3 in the Female Reproductive System: Lessons from Farm Animals, Birds, and Fish.

Recent studies have clearly shown that vitamin D3 is a crucial regulator of the female reproductive process in humans and animals. Knowledge of the expression of vitamin D3 receptors and related molecules in the female reproductive organs such as ovaries, uterus, oviduct, or placenta under physiological and pathological conditions highlights its contribution to the proper function of the reproductive system in females. Furthermore, vitamin D3 deficiency leads to serious reproductive disturbances and pathologies including ovarian cysts. Although the influence of vitamin D3 on the reproductive processes of humans and rodents has been extensively described, the association between vitamin D3 and female reproductive function in farm animals, birds, and fish has rarely been summarized. In this review, we provide an overview of the role of vitamin D3 in the reproductive system of those animals, with special attention paid to the expression of vitamin D3 receptors and its metabolic molecules. This updated information could be essential for better understanding animal physiology and overcoming the incidence of infertility, which is crucial for optimizing reproductive outcomes in female livestock.

Development and evolution of the notarium in Pterosauria.

The notarium is the structure formed by fusion of the dorsal vertebrae which occurred independently in pterosaurs and birds. This ankylosis usually involves two to six elements and in many cases, also includes the last cervical vertebra. Fusion can occur in different degrees, uniting the vertebral centra, the neural spines, the transverse processes, the ventral processes, or a combination of these sites. A detailed assessment of the fusion process of pterosaur dorsal vertebrae is still lacking. Here we identify the fusion sequence of pterosaur notarial elements, demonstrating the order of ossification in vertebral bodies and neural spines based on fossils and extant birds. In both Pterosauria and Aves, the notarium generally develops in a antero-posterior direction, but the actual order of each fusion locus may present slight variations. Based on our data, we were able to identify seven developmental stages in the notarium formation, with broad implications for the prediction of ontogenetic stages for the Pterosauria. In addition, we report the occurrence of a notarium in Ardeadactylus longicollum (Kimmeridgian, Southern Germany), the oldest occurrence of this structure in pterosaurs.

Developmental origins of mosaic evolution in the avian cranium.

Mosaic evolution, which results from multiple influences shaping morphological traits and can lead to the presence of a mixture of ancestral and derived characteristics, has been frequently invoked in describing evolutionary patterns in birds. Mosaicism implies the hierarchical organization of organismal traits into semiautonomous subsets, or modules, which reflect differential genetic and developmental origins. Here, we analyze mosaic evolution in the avian skull using high-dimensional 3D surface morphometric data across a broad phylogenetic sample encompassing nearly all extant families. We find that the avian cranium is highly modular, consisting of seven independently evolving anatomical regions. The face and cranial vault evolve faster than other regions, showing several bursts of rapid evolution. Other modules evolve more slowly following an early burst. Both the evolutionary rate and disparity of skull modules are associated with their developmental origin, with regions derived from the anterior mandibular-stream cranial neural crest or from multiple embryonic cell populations evolving most quickly and into a greater variety of forms. Strong integration of traits is also associated with low evolutionary rate and low disparity. Individual clades are characterized by disparate evolutionary rates among cranial regions. For example, Psittaciformes (parrots) exhibit high evolutionary rates throughout the skull, but their close relatives, Falconiformes, exhibit rapid evolution in only the rostrum. Our dense sampling of cranial shape variation demonstrates that the bird skull has evolved in a mosaic fashion reflecting the developmental origins of cranial regions, with a semi-independent tempo and mode of evolution across phenotypic modules facilitating this hyperdiverse evolutionary radiation.

Climate-driven declines in arthropod abundance restructure a rainforest food web.

A number of studies indicate that tropical arthropods should be particularly vulnerable to climate warming. If these predictions are realized, climate warming may have a more profound impact on the functioning and diversity of tropical forests than currently anticipated. Although arthropods comprise over two-thirds of terrestrial species, information on their abundance and extinction rates in tropical habitats is severely limited. Here we analyze data on arthropod and insectivore abundances taken between 1976 and 2012 at two midelevation habitats in Puerto Rico's Luquillo rainforest. During this time, mean maximum temperatures have risen by 2.0 °C. Using the same study area and methods employed by Lister in the 1970s, we discovered that the dry weight biomass of arthropods captured in sweep samples had declined 4 to 8 times, and 30 to 60 times in sticky traps. Analysis of long-term data on canopy arthropods and walking sticks taken as part of the Luquillo Long-Term Ecological Research program revealed sustained declines in abundance over two decades, as well as negative regressions of abundance on mean maximum temperatures. We also document parallel decreases in Luquillo's insectivorous lizards, frogs, and birds. While El Niño/Southern Oscillation influences the abundance of forest arthropods, climate warming is the major driver of reductions in arthropod abundance, indirectly precipitating a bottom-up trophic cascade and consequent collapse of the forest food web.

The old and new faces of morphology: the legacy of D'Arcy Thompson's 'theory of transformations' and 'laws of growth'.

In 1917, the publication of On Growth and Form by D'Arcy Wentworth Thompson challenged both mathematicians and naturalists to think about biological shapes and diversity as more than a confusion of chaotic forms generated at random, but rather as geometric shapes that could be described by principles of physics and mathematics. Thompson's work was based on the ideas of Galileo and Goethe on morphology and of Russell on functionalism, but he was first to postulate that physical forces and internal growth parameters regulate biological forms and could be revealed via geometric transformations in morphological space. Such precise mathematical structure suggested a unifying generative process, as reflected in the title of the book. To Thompson it was growth that could explain the generation of any particular biological form, and changes in ontogeny, rather than natural selection, could then explain the diversity of biological shapes. Whereas adaptationism, widely accepted in evolutionary biology, gives primacy to extrinsic factors in producing morphological variation, Thompson's 'laws of growth' provide intrinsic directives and constraints for the generation of individual shapes, helping to explain the 'profusion of forms, colours, and other modifications' observed in the living world.

Daily energy expenditure in white storks is lower after fledging than in the nest.

Many juvenile birds turn into long-distance migrants within weeks of fledging. This transition involves upheavals in their energy management as major changes in growth and activity occur. Understanding such ontogenetic transitions in energy allocation has been difficult because collecting continuous data on energy costs in wild developing birds was previously largely impossible. Here, we continuously measured heart rate and fine-scale movements of 20 free-living juvenile white storks (Ciconia ciconia) using on-board bio-loggers to explore individual and environmental factors relating to daily mean heart rate. In addition, we explored which specific energy management strategy storks use during these crucial early life stages. We found that daily mean heart rate increased with overall movement activity, and increasing body temperature, but that it decreased with age. Further, we found that during the nestling period, when growth costs are high, activity costs are low, and post-fledging that activity costs are increased while maintenance costs are low, indicating a constraint on overall energy use in both phases. Our observations are consistent with the hypothesis that individuals invested more energy per unit time while still in the nest than after fledging despite the high costs of flight.

Strengthening protected areas for biodiversity and ecosystem services in China.

Recent expansion of the scale of human activities poses severe threats to Earth's life-support systems. Increasingly, protected areas (PAs) are expected to serve dual goals: protect biodiversity and secure ecosystem services. We report a nationwide assessment for China, quantifying the provision of threatened species habitat and four key regulating services-water retention, soil retention, sandstorm prevention, and carbon sequestration-in nature reserves (the primary category of PAs in China). We find that China's nature reserves serve moderately well for mammals and birds, but not for other major taxa, nor for these key regulating ecosystem services. China's nature reserves encompass 15.1% of the country's land surface. They capture 17.9% and 16.4% of the entire habitat area for threatened mammals and birds, but only 13.1% for plants, 10.0% for amphibians, and 8.5% for reptiles. Nature reserves encompass only 10.2-12.5% of the source areas for the four key regulating services. They are concentrated in western China, whereas much threatened species' habitat and regulating service source areas occur in eastern provinces. Our analysis illuminates a strategy for greatly strengthening PAs, through creating the first comprehensive national park system of China. This would encompass both nature reserves, in which human activities are highly restricted, and a new category of PAs for ecosystem services, in which human activities not impacting key services are permitted. This could close the gap in a politically feasible way. We also propose a new category of PAs globally, for sustaining the provision of ecosystems services and achieving sustainable development goals.

Organochlorine Pesticide Residues Among Colonial Nesting Birds in Tamil Nadu, India: A Maiden Assessment from Their Breeding Grounds.

Use of pesticides continues to be indiscriminate, and birds are one of the worst affected non-targeted organisms. Information on the ill effects of pesticides on birds far from desired in India. Despite the presence of a wide variety and number of birds, there is exceedingly little data on organochlorine pesticide (OCP) residues in colonial nesting birds in sanctuaries of India. A total of 76 individuals belonging to 14 species of birds found dead between March 2008 and March 2010 were analyzed for pesticide residues in various tissues. Of all the OCPs analyzed, concentration of HCH was found to be the highest. Magnitude of contamination varied widely among species. Accumulation pattern of OCPs in colonial nesting birds was in the order ∑HCH > ∑endosulfan > ∑DDT > heptachlor epoxide > dieldrin. Pesticides, namely p,p-DDE and ß-HCH contributed most towards the total OCPs. Concentrations of DDT and its metabolites, HCH and isomers, dieldrin, and heptachlor epoxide were lower than the concentrations reported for various species of birds elsewhere in India. Although the sanctuaries presently studied have official boundaries, physical demarcations are missing and there are no proper earthen dykes particularly in Vedanthangal and Koonthankulam Bird Sanctuaries. During monsoon, runoff not only floods the Sanctuaries but also the cultivated areas nearby. Run off brings in residues of pesticides and fertilizers from the agricultural lands into the sanctuaries. Although OCP results in this study were below threshold limits, it may be noted that the long duration exposure even to low levels of pesticides could create a significant impact at population level. Hence, earthen dykes need to be built to avoid agricultural runoff entering the Sanctuary and also help to hold sufficient amount of water for breeding birds.

Higher Nest Predation Favors Rapid Fledging at the Cost of Plumage Quality in Nestling Birds.

High predation risk can favor rapid offspring development at the expense of offspring quality. Impacts of rapid development on phenotypic quality should be most readily expressed in traits that minimize fitness costs. We hypothesize that ephemeral traits that are replaced or repaired after a short period of life might express trade-offs in quality as a result of rapid development more strongly than traits used throughout life. We explored this idea for plumage quality in nestling body feathers, an ephemeral trait. We found a strong trade-off whereby nestlings that spend less time in the nest produced lower-quality plumage with less dense barbs relative to adults across 123 temperate and tropical species. For a subset of these species ( n=67 ), we found that variation in the risk of nest predation explained additional variation in plumage quality beyond development time. Ultimately, the fitness costs of a poor-quality ephemeral trait, such as nestling body feathers, may be outweighed by the fitness benefits of shorter development times that reduce predation risk. At the same time, reduced resource allocation to traits with small fitness costs, such as ephemeral traits, may ameliorate resource constraints from rapid development on traits with larger fitness impacts.

The effect of insularity on avian growth rates and implications for insular body size evolution.

Island populations often differ in consistent ways from their mainland counterparts with respect to their ecology, behaviour, morphology, demography and life-history characteristics; a set of changes referred to as the 'island syndrome'. To understand the ecological and evolutionary drivers of the island syndrome requires characterization of suites of interacting traits. While patterns in some types of traits, e.g. body size, are well characterized across a range of taxa, key gaps remain. Growth rate is one such trait, being an important determinant of both increases and decreases in body size, and can vary with changes in predation pressure and food limitation; two factors that are known to differ between mainland and island environments. Using a phylogenetic meta-analytic approach, we characterize differences in growth rates among mainland and island altricial bird populations, controlling for environmental factors. We found a trend towards slower growth on islands in small-bodied (less than 1 kg) bird species. This is consistent with the idea that the pattern of body size increases in small-bodied island colonists is associated with the evolution of slower growth combined with shifts in age and size at maturity in relaxed predation regimes.

Adaptive responses of the embryos of birds and reptiles to spatial and temporal variations in nest temperatures.

Natural nests of egg-laying birds and reptiles exhibit substantial thermal variation, at a range of spatial and temporal scales. Rates and trajectories of embryonic development are highly sensitive to temperature, favouring an ability of embryos to respond adaptively (i.e. match their developmental biology to local thermal regimes). Spatially, thermal variation can be significant within a single nest (top to bottom), among adjacent nests (as a function of shading, nest depth etc.), across populations that inhabit areas with different weather conditions, and across species that differ in climates occupied and/or nest characteristics. Thermal regimes also vary temporally, in ways that generate differences among nests within a single population (e.g. due to seasonal timing of laying), among populations and across species. Anthropogenic activities (e.g. habitat clearing, climate change) add to this spatial and temporal diversity in thermal regimes. We review published literature on embryonic adaptations to spatio-temporal heterogeneity in nest temperatures. Although relatively few taxa have been studied in detail, and proximate mechanisms remain unclear, our review identifies many cases in which natural selection appears to have fine-tuned embryogenesis to match local thermal regimes. Developmental rates have been reported to differ between uppermost versus lower eggs within a single nest, between eggs laid early versus late in the season, and between populations from cooler versus warmer climates. We identify gaps in our understanding of thermal adaptations of early (embryonic) phases of the life history, and suggest fruitful opportunities for future research.

Early-life telomere length predicts lifespan and lifetime reproductive success in a wild bird.

Poor conditions during early development can initiate trade-offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life-history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early-life conditions to lifespan and fitness. In wild purple-crowned fairy-wrens, we combined measurements of nestling telomere length (TL) with detailed life-history data to investigate whether early-life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age-dependent with early-life TL having a positive effect on lifespan only among individuals that survived their first year. Early-life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early-life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early-life TL, which reflects growth, accumulated early-life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early-life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early- and late-life performance and trade-offs across a lifetime.

Exposure to artificial light at night increases innate immune activity during development in a precocial bird.

Humans have greatly altered Earth's night-time photic environment via the production of artificial light at night (ALAN; e.g. street lights, car traffic, billboards, lit buildings). ALAN is a problem of growing importance because it may significantly disrupt the seasonal and daily physiological rhythms and behaviors of animals. There has been considerable interest in the impacts of ALAN on health of humans and other animals, but most of this work has centered on adults and we know comparatively little about effects on young animals. We exposed 3-week-old king quail (Excalfactoria chinensis) to a constant overnight blue-light regime for 6 weeks and assessed weekly bactericidal activity of plasma against Escherichia coli - a commonly employed metric of innate immunity in animals. We found that chronic ALAN exposure significantly increased bactericidal activity and that this elevation in immune performance manifested at different developmental time points in males and females. Whether this short-term increase in immune activity can be extended to wild animals, and whether ALAN-mediated increases in immune activity have positive or negative fitness effects, are unknown and will provide interesting avenues for future studies.

Persistent Organic Pollutants in Livers and Hg in Feathers of Neotropic Cormorants (Phalacrocorax brasilianus) from the Trinity River Watershed (Texas, USA).

The Trinity River (Texas, USA) has been historically known as a polluted river because of its proximity to the Dallas-Fort Worth area and because of known discharges of sewage and agricultural irrigation waters to the river. Surprisingly, there are no studies regarding the presence of legacy contaminants in the river and their impacts to wildlife. The objectives of this study were to determine accumulation and potential impacts of persistent organic pollutants, such as organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs), on Neotropic cormorants (Phalacrocorax brasilianus) nesting along the Trinity River. Adult and first-year cormorants were collected from two sites on the Trinity River Watershed during 2014 and 2015. Tissue sections from liver, spleen, kidneys, and gonads were used for histopathology analysis, and a portion of the liver was analyzed for OCPs, PCBs, and PBDEs. Breast feathers were analyzed for Hg. Surprisingly, all the contaminants were present at low concentrations, p,p'-DDE (2-724 ng/g ww), PCBs (28-851 ng/g ww), PBDEs (1-85 ng/g ww), Hg (1.9-3.4 µg/g dw), and below those that could be associated with adverse effects. Also, histological analysis of liver and kidney samples did not reveal morphologic changes consistent with acute or chronic toxicosis. The majority of the histologic changes were inflammatory and were related to parasitic infestation. Our results suggest that aquatic birds using the Trinity River watershed are not at risk for adverse effects due to the contaminants studied. These results should be useful to wildlife managers regarding concerns over contaminant impacts on wildlife of the Trinity River.

Convergence of biannual moulting strategies across birds and mammals.

Birds and mammals have developed numerous strategies for replacing worn feathers and hair. Moulting usually occurs on an annual basis; however, moults that take place twice per year (biannual moults) also occur. Here, we review the forces driving the evolution of various moult strategies, focusing on the special case of the complete biannual moult as a convergence of selection pressures across birds and mammals. Current evidence suggests that harsh environmental conditions or seasonality (e.g. larger variation in temperatures) drive evolution of a biannual moult. In turn, the biannual moult can respond to secondary selection that results in phenotypic alteration such as colour changes for mate choice dynamics (sexual selection) or camouflage requirements (natural selection). We discuss the contributions of natural and sexual selection to the evolution of biannual moulting strategies in the contexts of energetics, niche selection, functionality and physiological mechanisms. Finally, we suggest that moult strategies are directly related to species niche because environmental attributes drive the utility (e.g. thermoregulation, camouflage, social dynamics) of the hair or feathers. Functional efficiency of moult may be undermined if the pace of evolution fails to match that of the changing climate. Thus, future research should seek to understand the plasticity of moult duration and phenology, especially in the context of annual cycles.

Increased sea ice concentration worsens fledging condition and juvenile survival in a pagophilic seabird, the snow petrel.

Polar sea ice is changing rapidly, threatening many taxa in the Arctic and the Antarctic. Little is known about the effects of sea ice on early life-history traits of sea ice specialist species, although juvenile stages are a critical component of population dynamics and recruitment. We examined how annual variation in sea ice concentration (SIC) affects juvenile survival and body condition at fledging in the snow petrel Pagodroma nivea using long-term datasets encompassing 22 years for body condition and 37 years for juvenile survival. We show that SIC and southern annular mode (SAM), the principal mode of variability of the atmospheric circulation in the Southern Hemisphere, have strong nonlinear effects on juvenile survival and body condition. Below ca 20-30% SIC, body condition remained stable, but decreased almost linearly for higher SIC. Juvenile survival was negatively related to SIC and to SAM during the chick rearing period. We suggest that the base of the sea ice food web would be directly affected by sea ice conditions, thus acting locally on the abundance and structure of prey communities.