Community-Level Physiological Profiles of Cloacal Microbes in Songbirds (Order: Passeriformes): Variation Due to Host Species, Host Diet, and Habitat

The relationship between microorganisms and birds has received increased attention recently. The state of knowledge of this relationship, however, is based largely on examination of sick or dead birds, and knowledge of the prevalence and community structure and function of microbes in healthy wild populations is limited. Using carbon substrate utilization profiles, microbial communities were examined in 91 cloacal samples from 14 species within apparently healthy summer and winter passerine populations. Within each season, gradient lengths and eigenvalues from ordination analyses suggested that many samples differed in their carbon substrate utilization and several had very different communities. Cloacal microbe carbon utilization profiles were distinguishable among host species, season-specific diet, and study site in the ordination analyses. However, these patterns were only observed for the analysis of the summer data set. The results of this study support the idea that the avian host’s microbial community, relative to carbon substrate utilization, is related to host diet. Previously, this pattern had only been reported for potential pathogens isolated from the avian cloaca. Study site–specific patterns in the ordination analysis suggest that environmental conditions at a particular study site may influence cloacal microbial communities in birds. Results of this study indicate that examination of community-level physiological profiles may be a useful technique for distinguishing among avian cloacal samples, similar to that already established for discriminating aqueous and soil samples. Future studies that correlate microbe physiological profiles to condition-based indices of avian hosts may be most useful for eventually using the profile as an indicator of environmental conditions experienced by hosts.     

A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences

A phylogeny of haemosporidian parasites (phylum Apicomplexa, family Plasmodiidae) was recovered using mitochondrial cytochrome b gene sequences from 52 species in 4 genera (Plasmodium, Hepatocystis, Haemoproteus, and Leucocytozoon), including parasite species infecting mammals, birds, and reptiles from over a wide geographic range. Leucocytozoon species emerged as an appropriate out-group for the other malarial parasites. Both parsimony and maximum-likelihood analyses produced similar phylogenetic trees. Life-history traits and parasite morphology, traditionally used as taxonomic characters, are largely phylogenetically uninformative. The Plasmodium and Hepatocystis species of mammalian hosts form 1 well-supported clade, and the Plasmodium and Haemoproteus species of birds and lizards form a second. Within this second clade, the relationships between taxa are more complex. Although jackknife support is weak, the Plasmodium of birds may form 1 clade and the Haemoproteus of birds another clade, but the parasites of lizards fall into several clusters, suggesting a more ancient and complex evolutionary history. The parasites currently placed within the genus Haemoproteus may not be monophyletic. Plasmodium falciparum of humans was not derived from an avian malarial ancestor and, except for its close sister species, P. reichenowi, is only distantly related to haemospordian parasites of all other mammals. Plasmodium is paraphyletic with respect to 2 other genera of malarial parasites, Haemoproteus and Hepatocystis. Explicit hypothesis testing supported these conclusions.     

Are seals frequently infected with avian influenza viruses?

Influenza A virus isolates of the H4N5 subtype (which has previously been detected only in birds) were recovered from harbor seals dying of viral pneumonia on the New England coast from June 1982 through March 1983. When these isolates were compared with other mammalian and avian viruses in serological assays and RNA-RNA competitive hybridization, it was found that the seal viruses were most closely related antigenically and genetically to recent avian virus strains and were readily distinguishable from mammalian viruses, including H7N7 isolates recovered from seals in 1980. Unlike any previous isolates from mammals, these recent seal viruses replicate in the intestinal tracts of ducks, a characteristic of avian viruses. The association of avian viruses with influenza outbreaks in seals suggests that transmission of avian viruses to seals is occurring in nature. Potentially, this may be an example of the adaptation of avian viruses to mammals, which would represent an intermediate step in the evolution of new mammalian strains.     

Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines

Ultraviolet (UV) light-transmitted signals play a major role in avian foraging and communication, subserving functional roles in feeding, mate choice, egg recognition, and nestling discrimination. Sequencing functionally relevant regions of the short wavelength sensitive type 1 (SWS1) opsin gene that is responsible for modulating the extent of SWS1 UV sensitivity in birds allows predictions to be made about the visual system's UV sensitivity in species where direct physiological or behavioral measures would be impractical or unethical. Here, we present SWS1 segment sequence data from representative species of three avian lineages for which visually based cues for foraging and communication have been investigated to varying extents. We also present a preliminary phylogenetic analysis and ancestral character state reconstructions of key spectral tuning sites along the SWS1 opsin based on our sequence data. The results suggest ubiquitous ultraviolet SWS1 sensitivity (UVS) in both paleognaths, including extinct moa (Emeidae), and parrots, including the nocturnal and flightless kakapo (Strigops habroptilus), and in most, but not all, songbird (oscine) lineages, and confirmed violet sensitivity (VS) in two suboscine families. Passerine hosts of avian brood parasites were included both UVS and VS taxa, but sensitivity did not co-vary with egg rejection behaviors. The results should stimulate future research into the functional parallels between the roles of visual signals and the genetic basis of visual sensitivity in birds and other taxa.     

Prevalence and host-parasite list of some nasal mites from birds (Acarina: Rhinonyssidae, Speleognathidae)

A survey of nasal mites, primarily from birds in Texas, was reported and comparisons with the other major studies were made. Of 103 host species examined, 40 were parasitized, and of 502 individual birds examined, 87 were parasitized (17% prevalence). It was shown that the prevalence of infection was significantly dependent on the bird taxa examined, which indicates that the evolution of the hosts has affected the nasal mites' ability to parasitize their avian hosts. It was also shown that the prevalence of rhinonyssid nasal mites in their hosts seems to differ significantly between geographic regions.     

不同食性野生鸟类肠道微生物研究进展

肠道微生物是庞大而多样的微生物群落,通过促进营养摄取、宿主防御、免疫调节等,在维持机体健康方面起着至关重要的作用。宿主外部或内部环境的任何变化都会影响肠道微生物的组成,鸟类具有复杂的生活史和多样化的食性,飞翔生活使它们的生理活动面临更大的选择性压力,导致肠道微生物菌群的变化更加复杂。近年来,随着基因测序技术的发展以及对鸟类肠道微生物研究的日益重视,导致了鸟类肠道微生物研究呈指数增长。但目前的研究主要以家禽为主,野生鸟类肠道微生物报道则相对较少。野生鸟类肠道微生物结构变化及其维持机制等的研究仍处于起步阶段,有较大的研究空间。从植食性、肉食性、杂食性三种食性的鸟类肠道微生物组成及特点、影响因素等方面对前人的文献进行了全面梳理,以期为野生鸟类肠道微生物研究提供参考。总的来说,植食性鸟类肠道微生物多样性最低,以高丰度的变形菌门（Proteobacteria）、厚壁菌门（Firmicutes）为主;而杂食性鸟类肠道微生物多样性最高。遗传、生活史特征、人类活动、城市化、圈养行为等对鸟类肠道微生物的组成具有显著性的影响。     

Avian louse phylogeny (Phthiraptera: Ischnocera): a cladistic study based on morphology

The louse suborder Ischnocera (Phthiraptera) contains 3060 currently described species from over 150 genera. These lice are permanent obligatory ectoparasites of a diverse selection of birds and mammals with a worldwide distribution. Historically, they have played a major role in the development of our ideas on coevolution, and species hosted by mammals have been used extensively as model organisms for the study of cospeciation. In contrast, avian taxa comprising 90% of ischnoceran species have been neglected due to a lack of data on their wider systematics. A comparative study based on the adult and nymphal instar morphology of avian lice yielded 138 characters from 56 species (51 genera), all of which are illustrated or discussed here for the first time. A further five outgroup taxa were examined from the mammalian ischnoceran family Trichodectidae. Phylogenetic analyses of these data produced three most parsimonious cladograms, the strict consensus of which is highly resolved and broadly consistent with previous classifications. Morphological character variation is extensive, and nymphal character traits are useful in identifying instances of convergent evolution in adult morphology. The role of ontogeny in the development of the major character complexes of the head and abdomen is discussed, and its implications for further work on the phylogeny of avian Ischnocera is considered. Comparison with host taxonomy reveals a series of complex host-parasite associations that do not support a hypothesis of strict one to one cospeciation. However, extrapolation of these associations is compromised by the low sample size. The role of niche specialization to explain the presence of multiple unrelated lineages on the same host taxon is considered.     

The gut microflora and intestinal epithelial cells: a continuing dialogue

The mammalian intestinal epithelium effectively performs its physiological functions in a microbe-rich environment, while the prokaryotic population thrives amidst efficient cellular defenses. Recent delineation of the mechanisms by which bacteria communicate with their eukaryotic hosts and the cellular sites that microbial signals act in may shed light on these complex interactions.     

Evolution and distribution of class II-related endogenous retroviruses

Endogenous retroviruses (ERVs) are widespread in vertebrate genomes and have been loosely grouped into "classes" on the basis of their phylogenetic relatedness to the established genera of exogenous retroviruses. Four of these genera-the lentiviruses, alpharetroviruses, betaretroviruses, and deltaretroviruses-form a well-supported clade in retroviral phylogenies, and ERVs that group with these genera have been termed class II ERVs. We used PCR amplification and sequencing of retroviral fragments from more than 130 vertebrate taxa to investigate the evolution of the class II retroviruses in detail. We confirm that class II retroviruses are largely confined to mammalian and avian hosts and provide evidence for a major novel group of avian retroviruses, and we identify additional members of both the alpha- and the betaretrovirus genera. Phylogenetic analyses demonstrated that the avian and mammalian viruses form distinct monophyletic groups, implying that interclass transmission has occurred only rarely during the evolution of the class II retroviruses. In contrast to previous reports, the lentiviruses clustered as sister taxa to several endogenous retroviruses derived from rodents and insectivores. This topology was further supported by the shared loss of both the class II PR-Pol frameshift site and the class II retrovirus G-patch domain.     

Emergence of influenza A viruses.

Pandemic influenza in humans is a zoonotic disease caused by the transfer of influenza A viruses or virus gene segments from animal reservoirs. Influenza A viruses have been isolated from avian and mammalian hosts, although the primary reservoirs are the aquatic bird populations of the world. In the aquatic birds, influenza is asymptomatic, and the viruses are in evolutionary stasis. The aquatic bird viruses do not replicate well in humans, and these viruses need to reassort or adapt in an intermediate host before they emerge in human populations. Pigs can serve as a host for avian and human viruses and are logical candidates for the role of intermediate host. The transmission of avian H5N1 and H9N2 viruses directly to humans during the late 1990s showed that land-based poultry also can serve between aquatic birds and humans as intermediate hosts of influenza viruses. That these transmission events took place in Hong Kong and China adds further support to the hypothesis that Asia is an epicentre for influenza and stresses the importance of surveillance of pigs and live-bird markets in this area.     

Individual patterns of habitat and nest-site use by hosts promote transgenerational transmission of avian brood parasitism status

Brood parasitic birds impose variable fitness costs upon their hosts by causing the partial or complete loss of the hosts' own brood. Growing evidence from multiple avian host-parasite taxa indicates that exposure of individual hosts to parasitism is not necessarily random and varies with habitat use, nest-site selection, age or other phenotypic attributes. For instance, nonrandom patterns of brood parasitism had similar evolutionary consequences to those of limited horizontal transmission of parasites and pathogens across space and time and altered the dynamics of both population productivity and co-evolutionary interactions of hosts and parasites. We report that brood parasitism status of hosts of brown-headed cowbirds Molothrus ater is also transmitted across generations in individually colour-banded female prothonotary warblers Protonotaria citrea. Warbler daughters were more likely to share their mothers' parasitism status when showing natal philopatry at the scale of habitat patch. Females never bred in their natal nestboxes but daughters of parasitized mothers had shorter natal dispersal distances than daughters of nonparasitized mothers. Daughters of parasitized mothers were more likely to use nestboxes that had been parasitized by cowbirds in both the previous and current years. Although difficult to document in avian systems, different propensities of vertical transmission of parasitism status within host lineages will have critical implications both for the evolution of parasite tolerance in hosts and, if found to be mediated by lineages of parasites themselves, for the difference in virulence between such extremes as the nestmate-tolerant and nestmate-eliminator strategies of different avian brood parasite species.     

Using non-mammalian hosts to study fungal virulence and host defense

Non-mammalian hosts have been used to study host-fungal interactions. Hosts such as Drosophila melanogaster, Caenorhabditis elegans, Acathamoeba castellanii, Dictyostelium discoideum, and Galleria mellonella have provided means to examine the physical barriers, cellular mechanisms and molecular elements of the host response. The Drosophila host-response to fungi is mediated through the Toll pathway, whereas in C. elegans the host-response is TIR-1-dependent. Virulence traits that are involved in mammalian infection are important for the interaction of fungi with these hosts. Screening of fungal virulence traits using mutagenized fungi to determine changes in fungal infectivity of non-mammalian hosts has been used to identify novel virulence proteins used to infect C. elegans such as Kin1 (a serine/threonine protein kinase) and Rom2 (a Rho1 guanyl-nucleotide exchange factor) from Cryptococcus neoformans. These heterologous non-mammalian hosts highlight the similarities and differences between different hosts in fungal pathogenesis and they complement studies in mammalian systems and those using other genetic approaches.     

Evolving nonapeptide mechanisms of gregariousness and social diversity in birds

Of the major vertebrate taxa, Class Aves is the most extensively studied in relation to the evolution of social systems and behavior, largely because birds exhibit an incomparable balance of tractability, diversity, and cognitive complexity. In addition, like humans, most bird species are socially monogamous, exhibit biparental care, and conduct most of their social interactions through auditory and visual modalities. These qualities make birds attractive as research subjects, and also make them valuable for comparative studies of neuroendocrine mechanisms. This value has become increasingly apparent as more and more evidence shows that social behavior circuits of the basal forebrain and midbrain are deeply conserved (from an evolutionary perspective), and particularly similar in birds and mammals. Among the strongest similarities are the basic structures and functions of avian and mammalian nonapeptide systems, which include mesotocin (MT) and arginine vasotocin (VT) systems in birds, and the homologous oxytocin (OT) and vasopressin (VP) systems, respectively, in mammals. We here summarize these basic properties, and then describe a research program that has leveraged the social diversity of estrildid finches to gain insights into the nonapeptide mechanisms of grouping, a behavioral dimension that is not experimentally tractable in most other taxa. These studies have used five monogamous, biparental finch species that exhibit group sizes ranging from territorial male-female pairs to large flocks containing hundreds or thousands of birds. The results provide novel insights into the history of nonapeptide functions in amniote vertebrates, and yield remarkable clarity on the nonapeptide biology of dinosaurs and ancient mammals. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism

Understanding of the conditions encouraging the evolution of kleptoparasitism has been limited by the preponderance of attention focused on a limited number of taxa (predominantly birds). However, most animal taxa contain kleptoparasitic members. In many ways, adult birds are aberrant because most are acrobatic, capable of three-dimensional movement, and steal from hosts that are capable of similar feats. The mobility of kleptoparasites and their hosts falls along a continuum, with the acrobatic birds at one end and sessile hosts and kleptoparasites at the other. Considering sedentary systems requires amendments to the criteria previously outlined as necessary for kleptoparasitism. Kleptoparasitic interactions between agile participants are ephemeral, involve numerous hosts over the lifetime of the kleptoparasite, and usually rely on vision. Large concentrations of hosts and large, high-quality food items are important in mobile systems. By contrast, the long-term, intimate associations of sedentary interactions demand that the host not consume the kleptoparasite's offspring and that the host must either have a longer life cycle than the kleptoparasite or be located in aggregations that have staggered life cycles (so the kleptoparasite can move to a new host when the original host dies). Expanding studies of kleptoparasitism to other taxa will differentiate between the selective pressures and evolutionary responses that are universal among kleptoparasitic symbioses and those that are restricted to certain groups.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 745–762.     

Characterization of the first growth hormone gene sequence for a passerine bird--the pied flycatcher (Ficedula hypoleuca).

While the growth hormone (GH) gene has been characterized in a broad range of vertebrates, surprisingly little is known about this gene in birds. In order to extend knowledge of the GH gene in avian species and non-domestic species, the pied flycatcher (Ficedula hypoleuca) GH gene has been sequenced in this study. The overall average pairwise sequence divergence level was 0.08 among all available avian sequences and 0.27 among other taxa. However, the overall genetic organization of the gene is quite conserved. The similarity of the GH gene sequence of pied flycatchers with those of chicken and duck suggests that the rapid bursts of molecular evolution observed in mammalian and fish GH have not occurred during the divergence of passerine and non-passerine birds.     

Ecoimmunology and microbial ecology: Contributions to avian behavior,physiology, and life history

Bacteria have had a fundamental impact on vertebrate evolution not only by affecting the evolution of the immune system, but also generating complex interactions with behavior and physiology. Advances in molecular techniques have started to reveal the intricate ways in which bacteria and vertebrates have coevolved. Here, we focus on birds as an example system for understanding the fundamental impact bacteria have had on the evolution of avian immune defenses, behavior, physiology, reproduction and life histories. The avian egg has multiple characteristics that have evolved to enable effective defense against pathogenic attack. Microbial risk of pathogenic infection is hypothesized to vary with life stage, with early life risk being maximal at either hatching or fledging. For adult birds, microbial infection risk is also proposed to vary with habitat and life stage, with molt inducing a period of increased vulnerability. Bacteria not only play an important role in shaping the immune system as well as trade-offs with other physiological systems, but also for determining digestive efficiency and nutrient uptake. The relevance of avian microbiomes for avian ecology, physiology and behavior is highly topical and will likely impact on our understanding of avian welfare, conservation, captive breeding as well as for our understanding of the nature of host-microbe coevolution.     

Interspecific variation in dietary carotenoid assimilation in birds: links to phylogeny and color ornamentation

Many birds use carotenoid pigments to acquire rich red, orange, and yellow coloration in feathers and bare parts that is used as a signal of mate quality. Because carotenoids are derived from foods, much attention has been paid to the role of diet in generating color variation both within and among avian species. Less consideration has been given to physiological underpinnings of color variability, especially among species. Here, I surveyed published literature (e.g. captive feeding studies) on carotenoid assimilation in six bird species and completed additional controlled carotenoid-supplementation experiments in two others to consider the ability of different taxa to extract carotenoids from the diet in relation to phylogeny and coloration. I found that, for a given level of carotenoids in the diet, passerine birds (zebra finch, Taeniopygia guttata; house finch, Carpodacus mexicanus; American goldfinch, Carduelis tristis; society finch, Lonchura domestica) exhibit higher levels of carotenoids in circulation than non-passerines like gamebirds (domestic chicken, Gallus domesticus; red junglefowl, Gallus gallus; Japanese quail, Coturnix coturnix; red-legged partridge, Alectoris rufa). This difference in carotenoid accumulation is likely due to interspecific variation in micelle, chylomicron, or lipoprotein concentrations or affinities for xanthophyll carotenoids. Passerine birds more commonly develop carotenoid-based colors than do birds from ancient avian lineages such as Galliformes, and the physiological differences I uncover may explain why songbirds especially capitalize on carotenoid pigments for color production. Ultimately, because we can deconstruct color traits into component biochemical, physical, and physiological parts, avian color signals may serve as a valuable model for illuminating the proximate mechanisms behind interspecific variation in signal use in animals.     

Nest predators and the evolution of avian reproductive strategies: a comparison of Australian and New Zealand birds

Summary Nest predation has been considered an important factor in the evolution of avian life histories: smaller clutches and shorter incubation and nestling periods are expected where nest predation has significant effects on reproductive success. Unlike the Australian avifauna, terrestrial New Zealand birds have evolved in the absence of reptilian and mammalian predators. Here we compare the reproductive strategies of terrestrial native New Zealand birds with those of their Australian sister taxa. In 11 of 14 comparisons, New Zealand birds were larger than their Australian relatives, but we did not find any significant differences in reproductive tactics between the two regions, a result inconsistent with the nest predation hypothesis. We discuss several reasons why this may be so. One possibility is that selection imposed on avian life history tactics by mammalian predators following the arrival of humans in New Zealand has led to strategies similar to those adopted in Australia.     

A dead giveaway: Foraging vultures and other avian scavengers respond to auditory cues

Carrion represents an unpredictable and widely distributed primary food source for vultures and other avian scavengers. Avian scavengers in African savanna ecosystems are reported to rely exclusively on visual stimuli to locate carcasses. However, carnivores’ predation of large mammalian herbivores and subsequent competition for access to the carcass can result in considerable noise, often audible over long distances and for prolonged periods. Vultures and other avian scavengers may therefore detect and respond to these auditory cues, as do the mammalian carnivores alongside which vultures have coevolved, but this has not been investigated to date. Working in the Serengeti ecosystem, Tanzania, we used diurnal auditory broadcasts to simulate predation and competitive carnivore feeding interactions. Based on the current understanding of avian scavenger ecology, we hypothesized that avian responses to call‐in stations would be evoked exclusively by visual, rather than auditory, cues. We therefore predicted that (a) the arrival of avian scavengers at call‐in stations should be preceded and facilitated by mammalian carnivores and that (b) the arrival of avian scavengers would be positively correlated with the number of mammalian scavengers present, which would increase detectability. We recorded 482 birds during 122 separate playback events. In 22% of these instances, avian scavengers arrived first, ruling out responses based exclusively on visual observations of mammalian carnivores, thereby contradicting our first prediction. Furthermore, the first avian arrivals at survey sessions were inversely related to the number of hyenas and jackals present, contradicting our second prediction. Since no bait or carcasses were used during the experiments, these responses are indicative of the birds’ ability to detect and respond to audio stimuli. Our findings challenge the current consensus of sensory perception and foraging in these species and provide evidence that avian scavengers have the ability to use sound to locate food resources.     

Recent developments in our understanding of the avian melanocortin system: its involvement in the regulation of pigmentation and energy homeostasis

The mammalian melanocortin system has been established as a crucial regulatory component in an extraordinarily diverse number of physiological functions. In contrast, comparatively little is known about the avian melanocortin system: interest in the physiological role of alpha-MSH in birds has been limited by the fact that birds lack the intermediate lobe of the pituitary, the main source of circulating alpha-MSH in most vertebrates. Recently, however, the main avian melanocortin system genes, including POMC, AGRP, and all the melanocortin receptors, have been cloned and their physiological roles are the beginning to be elucidated. This review outlines our improved understanding of the avian melanocortin system, particularly in relation to two of the most widely studied physiological functions of the melanocortin system in mammals, the regulation of pigmentation and energy homeostasis. The data reviewed here indicate that the melanocortin system has been strongly conserved during vertebrate evolution and that alpha-MSH is produced locally in birds to act as an autocrine/paracrine hormone.