Adult Finches Research Articles

Mercury causes degradation of spatial cognition in a model songbird species

Mercury is a widespread pollutant of increasing global concern that exhibits a broad range of deleterious effects on organisms, including birds. Because the developing brain is well-known to be particularly vulnerable to the neurotoxic insults of mercury, many studies have focused on developmental effects such as on the embryonic brain and resulting behavioral impairment in adults. It is not well understood how the timing of exposure, for example exclusively in ovo versus throughout life, influences the impact of mercury. Using dietary exposure to environmentally relevant methylmercury concentrations, we examined the role that timing and duration of exposure play on spatial learning and memory in a model songbird species, the domesticated zebra finch (Taeniopygia guttata castanotis). We hypothesized that developmental exposure was both necessary and sufficient to disrupt spatial memory in adult finches. We documented profound disruption of memory for locations of hidden food at two spatial scales, cage- and room-sized enclosures, but found that both developmental and ongoing adult exposure were required to exhibit this behavioral impairment. Methylmercury-exposed birds made more mistakes before mastering the spatial task, because they revisited unrewarded locations repeatedly even after discovering the rewarded location. Contrary to our prediction, hippocampal volume was not affected in birds exposed to methylmercury over their lifetimes. The disruption of spatial cognition that we detected is severe and would likely have implications for survival and reproduction in wild birds; however, it appears that individuals that disperse or migrate from a contaminated site might recover later in life if no longer exposed to the toxicant.

Development of a Vitamin A Deficient (VAD) Songbird

Vitamin A deficiency (VAD) is a global health problem with effects on brain function through altered retinoic acid signaling. However, the specific effect of VAD on speech and vocal‐motor learning has not been studied. Songbirds possess a cortical brain circuit for vocal learning that relies on retinoic acid signaling during the critical period of vocal learning. To study VAD in a vocal learner we developed a special diet from white rice and sunflower seed, two grains that are naturally low in vitamin A and carotenoids, with other essential vitamins and minerals added back. This diet was fed to zebra finch family groups during chick rearing to evaluate the ability of parents to feed the diet to their chicks and the effects of a VAD diet on serum and brain retinol, chick growth and development. We found that adult birds readily consumed the rice/sunflower seed diet and fed it to their nestlings. Adults that consumed the diet maintained the same caloric intakes compared to when fed a regular seed diet and although these birds showed some decline in body mass, it remained within a normal range. Surprisingly, we detected a 28% decline in serum retinol at three weeks on the VAD diet in adult finches, a response that makes songbirds a highly useful model to study VAD. Juveniles that were fed the diet by the adults beginning at hatch also were able to consume and thrive. Compared to controls, chicks on the VAD diet showed no effects on growth rate between 10‐65 days, but the chick survival rate was 63% lower than that of controls with no chicks surviving beyond 65 days old. Chicks that were on the VAD diet did not exhibit sub‐song behavior between 35‐50 days (72 total hours of monitoring), whereas chicks that were on a seed diet or a rice/sunflower seed control diet (with retinol added back) showed song development. We also note that VAD affected eye shape and appearance, consistent with what is found during VAD in non‐avian models. Serum retinol of chicks on the VAD diet showed a 57% decline compared to controls. Further development of this model will require titration of the VAD to moderate levels that allow for song development and high chick survival. This study lays the groundwork for the use of modified diets in the songbird model to examine how VAD or other micronutrients may modulate neural development in the vocal circuit of a vocal learner, as well as open the door for the use of the model in high‐fat diet nutrition experiments and lipid transport studies.

Male zebra finches exposed to lead (Pb) during development have reduced volume of song nuclei, altered sexual traits, and received less attention from females as adults

Lead (Pb) is a pervasive global contaminant that interferes with sensitive windows for neurological development and causes oxidative damage to tissues. The effects of moderate and high exposure to Pb have been well-studied in birds, but whether low-level early-life exposure to Pb influences adult phenotype remains unclear. Female songbirds use a male's song and coloration to discriminate between high- and low-quality males. Therefore, if early-life exposure to Pb disrupts song learning ability or shifts the allocation of antioxidant pigments away from colorful secondary sexual traits, male birds exposed to Pb may be less attractive to females. We exposed developing zebra finches (Taeniopygia guttata) to Pb-contaminated drinking water (100 or 1000 parts per billion [ppb]) after hatching (days 0–100). Once male finches reached adulthood (120–150 days post hatch), we measured song learning ability, coloration of bill and cheek patches, and volume of song nuclei in the brain. We also measured female preference for Pb-exposed males relative to control males. Finally, we measured motoric and spatial cognitive performance in male and female finches to assess whether cognitive traits differed in their sensitivity to Pb exposure. Male zebra finches exposed to 1000 ppb Pb had impaired song learning ability, reduced volume of song nuclei, bills with less redness and received less attention from females. Additionally, Pb exposure impaired motoric performance in both male and female finches but did not affect performance in a spatial cognitive task. Adult finches exposed to Pb-contaminated water had higher blood-Pb levels, though in all cases blood-Pb levels were below 7.0 µg dL−1. This study suggests that low-level exposure to Pb contributes to cognitive deficits that persist into adulthood and may indirectly influence fitness by altering secondary sexual traits and reducing male attractiveness.

Impact of nest sanitation on the immune system of parents and nestlings in a passerine bird.

Bacterial communities are thought to have fundamental effects on the growth and development of nestling birds. The antigen exposure hypothesis suggests that, for both nestlings and adult birds, exposure to a diverse range of bacteria would select for stronger immune defences. However, there are relatively few studies that have tested the immune/bacterial relationships outside of domestic poultry. We therefore sought to examine indices of immunity (microbial killing ability in naive birds, which is a measure of innate immunity, and the antibody response to sheep red blood cells, which measures adaptive immunity) in both adult and nestling zebra finches (Taeniopygia guttata). We did this throughout breeding and between reproductive attempts in nests that were experimentally manipulated to change the intensity of bacterial exposure. Our results suggest that nest sanitation and bacterial load affected measures of the adaptive immune system, but not the innate immune parameters tested. Adult finches breeding in clean nests had a lower primary antibody response to sheep red blood cells, particularly males, and a greater difference between primary and secondary responses. Adult microbial killing of Escherichia coli decreased as parents moved from incubation to nestling rearing for both nest treatments; however, killing of Candida albicans remained consistent throughout. In nestlings, both innate microbial killing and the adaptive antibody response did not differ between nest environments. Together, these results suggest that exposure to microorganisms in the environment affects the adaptive immune system in nesting birds, with exposure upregulating the antibody response in adult birds.

The influence of nest-site choice and predator sensory cues on nesting success in the Crimson Finch (Neochmia phaeton)

The attributes of a nest-site that a bird selects may be influenced by the potential predator species present, as different types of predator use different foraging strategies and sensory cues to locate nests. However, in many studies of avian nesting, the identity of the main nest predators and their foraging strategies are not known, limiting our interpretation and understanding of how choice of nest-site and nesting success might be linked. We investigated nest-site choice, nest survival and the nest predators in a population of Crimson Finch (Neochmia phaeton) in tropical Australia. Crimson Finches preferred to nest among foliage of the crowns of Pandanus on stems with aquatic barriers, and near old nests of conspecifics. However, none of these or any other attributes of nest-sites that we recorded significantly affected nest survival. Moreover, neither visual nor olfactory cues influenced nesting success in field experiments with quail eggs. Similar rates of predation of natural and experimental nests, coupled with similar rates of daily predation of eggs and nestlings suggest that predators were not using nest-attendance behaviour of the adult Finches as a cue to find active nests. Identified nest predators were reptiles; our study suggests that Crimson Finches may not be able to choose nest-sites that reduce the ability of these olfactory-driven predators.

Oxidative stress in songbirds exposed to dietary methylmercury.

Long-term, sublethal methylmercury exposure can cause reproductive depression, immune suppression, endocrine disruption and other problems in birds. We used two biomarkers to detect oxidative stress in livers of zebra finches (Taeniopygia guttata) developmentally exposed to sublethal levels of dietary methylmercury (0.0, 0.3, 0.6, 1.2, or 2.4μg/g wet weight in diet). Our findings indicate that young adult finches exposed to environmentally relevant concentrations of mercury in ovo and through their diets, exhibited oxidative stress in their livers. We measured the ratio of the antioxidant glutathione in its reduced form (GSH) versus its oxidized form (GSSG) and the activity of the superoxide dismutase (SOD) enzyme suite. Blood total mercury served as a proxy for liver mercury concentration, and was on average 8.4 times the dietary dose (e.g., birds consuming 0.6μg/g had blood mercury levels of ~5μg/g on a wet weight basis). Consistent with what is known from large, aquatic bird species, there was a significant, negative relationship between GSH/GSSG ratios and tissue mercury concentrations, which is indicative of oxidative stress. This relationship was driven by a significant increase in the oxidized glutathione in the livers of birds with higher blood mercury levels. SOD activity was also found to have a significant, negative relationship with blood mercury.

Discovery of a novel functional leptin protein (LEP) in zebra finches: evidence for the existence of an authentic avian leptin gene predominantly expressed in the brain and pituitary.

Leptin (LEP) is reported to play important roles in controlling energy balance in vertebrates, including birds. However, it remains an open question whether an authentic "LEP gene" exists and functions in birds. Here, we identified and characterized a LEP gene (zebra finch LEP [zbLEP]) encoding a 172-amino acid precursor in zebra finches. Despite zbLEP showing limited amino acid sequence identity (26%-29%) to human and mouse LEPs, synteny analysis proved that zbLEP is orthologous to mammalian LEP. Using a pAH32 luciferase reporter system and Western blot analysis, we demonstrated that the recombinant zbLEP protein could potently activate finch and chicken LEP receptors (zbLEPR; cLEPR) expressed in human embryonic kidney 293 cells and enhance signal transducer and activator of transcription 3 phosphorylation, further indicating that zbLEP is a functional ligand for avian LEPRs. Interestingly, quantitative real-time RT-PCR revealed that zbLEP mRNA is expressed nearly exclusively in the pituitary and various brain regions but undetectable in adipose tissue and liver, whereas zbLEPR mRNA is widely expressed in adult finch tissues examined with abundant expression noted in pituitary, implying that unlike mammalian LEP, finch LEP may not act as an adipocyte-derived signal to control energy balance. As in finches, a LEP highly homologous to zbLEP was also identified in budgerigar genome. Strikingly, finch and budgerigar LEPs show little homology with chicken LEP (cLEP) previously reported, suggesting that the so-called cLEP is incorrect. Collectively, our data provide convincing evidence for the existence of an authentic functional LEP in avian species and suggest an important role of brain- and pituitary-derived LEP played in vertebrates.

Naris and beak malformation caused by the parasitic fly, Philornis downsi (Diptera: Muscidae), in Darwin's small ground finch, Geospiza fuliginosa (Passeriformes: Emberizidae)

Parasites induce phenotypic modifications in their hosts, which can compromise host fitness. For example, the parasitic fly Philornis downsi, which was recently introduced to the Galapagos Islands, causes severe naris and beak malformation in Darwin's finches. The fly larvae feed on tissues from the nares of developing finch nestlings, thereby altering the size and shape of the nares and beak. Although the parasitism is age-specific (adult finches are not parasitized), naris and beak malformations persist into adulthood as parasite-induced malformations. We systematically examined adult populations of Darwin's small ground finch, Geospiza fuliginosa, on the islands of Santa Cruz for P. downsi-induced malformation. We found that malformed birds had significantly longer nares, and shorter, shallower beaks, than birds considered to be normal (i.e. with no nares or beak malformation). In addition, normal birds showed an isometry between naris length and beak dimensions (beak length feather and beak depth), which was not found in malformed birds. These differences suggest that beak morphology was influenced by P. downsi parasitism. Interestingly, we did not find any evidence of developmental impairment (smaller body size) or reduced foraging efficiency (lower body condition) between normal and malformed birds. Our findings of P. downsi-induced malformation raise new questions about the evolutionary trajectory and conservation status for this group of birds. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 577–585.

Genomic organization of zebra finch alpha and beta globin genes and their expression in primitive and definitive blood in comparison with globins in chicken

How alpha and beta globin genes are organized and expressed in amniotes is of interest to researchers in a wide variety of fields. Data regarding this from avian species have been scarce. Using genomic and proteomic approaches, we present here our analysis of alpha and beta globins of zebra finch, a passerine bird. We show that finch alpha globin gene cluster has three genes (alphas 1-3), each orthologous to its chicken counterpart. Finch beta globin gene cluster has three genes (betas 1-3), with an additional pseudogene at the 3' end. Finch beta3 is orthologous to chicken betaA, but the orthology of beta1 and beta2 to chicken counterparts is less clear. All six finch globins are confirmed to encode functional proteins. Gene expression in both globin gene clusters is regulated developmentally. Adult finch blood has a globin profile similar to that of adult chicken, with high levels of beta3 and alpha3 and moderate levels of alpha2. Finch embryonic primitive blood exhibits a globin profile very different from that of equivalent stage chick embryos, with all six globins expressed at high levels. Overall, our data provide a valuable resource for future studies in avian globin gene evolution and globin switching during erythropoietic development.

Individual variation in the basal metabolism of Zebra finches Taeniopygia guttata: no effect of food quality during early development

We investigated the physiological background to individual variation in basal metabolic rate (BMR) in a laboratory population of a small passerine bird, the Zebra finch, Taeniopygia guttata. We especially explored whether food-quality during early development influenced the BMR later in life. Zebra finches were raised on two different food regimes; one (‘low quality’) involving only mixed seed diet, while the other (‘high quality’) in addition including a protein supplement and daily fresh hard-boiled eggs. The different diets were administrated to the birds only during the first 6 weeks of life. At an age of 1.5 to 2 years, and after a breeding period of their own, BMR was measured in all individuals. Food quality had a significant effect on body mass. Adult finches raised on high-quality protein-rich food were significantly heavier (2.2 g for males and 1.9 g for females) than their counterparts raised on low-quality food. Despite this, the BMR of the adult birds did not differ beyond that expected based on variation in body mass alone. Hence, the early feeding regimes, which induced a non-genetic phenotypic variability in body mass, did apparently not induce any long-term changes in body composition or in organ metabolic intensity.

Rapidly learned song-discrimination without behavioral reinforcement in adult male zebra finches ( Taeniopygia guttata)

Zebra finches communicate via several distinct vocalizations, of which song is the most studied. Behavioral observations indicate that adults are able to discriminate among the songs of different conspecific individuals. In the wild, zebra finches live in structured but mobile colonies, and encounter new individuals on a frequent basis. Thus it seems plausible that adult finches might have the capacity to recognize and remember new songs they encounter on a single day, but this has never been directly tested. Here we devised a simple observational assay to determine whether adult male zebra finches show recognition of a song they have heard repeatedly from taped playbacks, over a single three hour period the day before. We quantified the rate of production of six discrete behaviors (short calls, contact calls, singing, short hops, long hops, and beak swipes) made by adult male zebra finches as they listened to the playbacks. At the onset of song playback, all birds suspended these behaviors and sat silently—occasionally moving their heads. Then, after a measurable period (“response latency”), the birds resumed these activities. We observed that the response latency was long (∼10 min) when birds were hearing a particular song for the first time. The response latency was much shorter (∼1–2 min) when the birds had heard the same song the day before. Thus, functional song memories must result from as little as 3 h of passive song-exposure. These results suggest that ongoing song learning may play a natural role in the daily life of adult zebra finches, and provide a behavioral reference point for studies of molecular and physiological plasticity in the adult auditory system.

Thymoma in a Finch

An adult finch was presented with a 1-cm mass near the thoracic inlet. Histologically, the mass was diagnosed as a thymoma of lymphocytic type. The clinical signs and histologic findings related to the thymoma are presented. The similarities and differences between thymomas in birds and mammals are discussed briefly.

Estrogen Promotes the Initial Migration and Inception of NgCAM-Dependent Calcium-Signaling by New Neurons of the Adult Songbird Brain

The adult avian forebrain continues to generate neurons from ventricular zone (VZ) precursor cells, whose neuronal progeny then migrate into the brain parenchyma. Migrating neurons respond to the Ig-family adhesion molecule NgCAM with increments in cytosolic calcium, and migration is disrupted by anti-NgCAM Ig. The calcium response to NgCAM is developmentally restricted to bipolar migrants during a period spanning 6 to 9 DIV. This period corresponds to the postmitotic age at which new neurons leave the adult VZ to traverse a subjacent layer of estrogen-receptive “gatekeeper” neurons. Since neuronal passage through this layer occurs concurrently with the onset of NgCAM-dependent calcium signaling, we asked whether acquisition of the calcium response to NgCAM required estrogen exposure. Among neurons arising from explants of the adult finch neostriatal VZ, only those supplemented with estrogen developed calcium responses to NgCAM; neither explants raised in the absence of estrogen, nor those supplemented with testosterone, did so. Neurons in all three groups expressed NgCAM, had equivalent baseline calcium levels, and responded identically to K+-depolarization. Nonetheless, many more neurons migrated from explants of both finch and canary VZ raised in estrogen-supplemented media than from their estrogen-deprived counterparts, even though no effect of estrogen on neuronal survival per se was noted. These findings suggest that estrogen encourages the initial departure and assumption of signal competence by neurons arising from the adult avian VZ, thereby promoting their parenchymal recruitment and migration success.

Insulin-like growth factor-1 is a radial cell-associated neurotrophin that promotes neuronal recruitment from the adult songbird edpendyma/subependyma.

In the adult songbird forebrain, neurons continue to be produced from precursor cells in the forebrain ependymal/subependymal zone (SZ), from which they migrate upon radial guide fibers. The new neurons and their radial cell partners may coderive from a common SZ progenitor, which may be the radial cell itself. On this basis, we asked whether radial cells might provide trophic support for the migration or survival of newly generated neurons. We focused upon the insulin-like growth factors (IGFs) IGF-1 and IGF-2, which have previously been shown to support the survival and differentiation of neural progenitor cells. We found that IGF-1 immunoreactivity was expressed heavily by adult zebra finch radial cells and their fibers, with little expression otherwise. IGF-2, in contrast, was expressed by parenchymal astrocytes and exhibited little radial cell expression. Despite their distinct distributions, IGF-1 and IGF-2 exerted similar trophic effects on finch SZ cells in vitro; both greatly increased the number of neurons migrating from explants of the adult finch SZ, relative to explants raised in low-insulin, IGF-1-deficient media. However, neither factor extended neuronal survival. These results suggest that in neurogenic regions of the adult avian forebrain, IGF-1 acts as a radial cell-associated neuronal differentiation and/or departure factor, which may serve to regulate neuronal recruitment into the adult brain.

Adult bengalese finches (Lonchura striata var.domestica) require real-time auditory feedback to produce normal song syntax

Songbirds develop their songs by imitating songs of adults. For song learning to proceed normally, the bird's hearing must remain intact throughout the song development process. In many species, song learning takes place during one period early in life, and no more new song elements are learned thereafter. In these so-called close-ended learners, it has long been assumed that once song development is complete, audition is no longer necessary to maintain the motor patterns of full song. However, many of these close-ended learners maintain plasticity in overall song organization; the number and the sequence of song elements included in a song of an individual vary from one utterance to another, although no new song elements are added or lost in adulthood. It is conceivable that these species rely on continued auditory feedback to produce normal song syntax. The Bengalese finch is a close-ended learner that produces considerably variable songs as an adult. In the present study, we found that Bengalese finches require real-time auditory feedback for motor control even after song learning is complete; deafening adult finches resulted in development of abnormal song syntax in as little as 5 days. We also found that there was considerable individual variation in the degree of song deterioration after deafening. The neural mechanisms underlying adult song production in different species of songbirds may be more diverse than has been traditionally considered.

Cochlosoma infections in finches.

To survey finches in pet shops for Cochlosoma infection and evaluate the efficacy of antiprotozoal therapy with metronidazole or ronidazole. A survey of pet shop finches and drug efficacy trials. Finches in pet shops were randomly selected and their faeces examined microscopically for motile Cochlosoma sp trophozoites. Drug trials were carried out on 60 adult finches with naturally occurring infections. Body weight was measured and the faeces of each bird was examined for trophozoites at the beginning and 7 days after the end of treatment. In some birds, additional daily faecal examinations were done until three consecutive negative results were obtained. Metronidazole was administered at various dose rates by crop gavage or in drinking water to eight groups of five to ten finches each. Ronidazole was given in water for 7 days to ten finches. In addition, six finches whose faeces tested positive were necropsied and their tissues collected for histological examination. Motile flagellates in the faeces were identified as C anatis-like protozoa. Red-headed parrot-finches, Bengalese and Lady Gould finches were found to be most commonly infected. Cochlosoma sp was also found in the blue-faced parrot-finch, zebra finch, painted finch, nutmeg mannikin and double-barred finch. Metronidazole and ronidazole were found to be effective against Cochlosoma sp. Histological findings on infected adult finches were normal, except for the presence of numerous flagellates between the colorectal villi and cloacal mucosal folds. Cochlosoma anatis-like organisms can infect several species of finches and in adult finches are confined to the colorectum and cloaca. Infection in adult finches was mostly subclinical and could be treated effectively with metronidazole or ronidazole.

Ontogenetic modification of the hypercapnic ventilatory response in the zebra finch

We investigated the effect of exposure to CO 2 during development on the adult ventilatory response to CO 2 of zebra finches. Developing zebra finches were exposed to chronic hypercapnic respiratory environments as embryos, as nestlings or during both developmental periods. Their responsiveness to CO 2 was then measured following a 125–135 day post-fledging deacclimation period. At a Fl CO 2 of 0.06, mean ventilation of adult finches in the three groups was 74.8, 61.3 and 65.8%, respectively, of that of finches reared under normocapnic conditions. These data indicate that adult acute ventilatory responsiveness to CO 2 in birds may be in part determined by CO 2 exposure during early development and may help explain the observation that fossorial and semifossorial species of birds and mammals, that naturally encounter high CO 2 conditions in their burrows, have a blunted hypercapnic ventilatory response.

Parasitism of wild Gouldian finches (Erythrura gouldiae) by the air-sac mite Sternostoma tracheacolum.

Sixty-two percent of 26 wild caught Gouldian finches (Erythrura gouldiae) were infected with Sternostoma tracheacolum, a parasitic rhinonyssid mite. The intensity of infection was higher in adult finches than juveniles, and higher in juvenile females than juvenile males. Histopathological investigation of wild Gouldian Finches revealed bronchopneumonia and air sacculitis associated with mite infection. Although this mite may not have contributed to the decline of Gouldian finch populations in the wild during the past 20 yr, it may be suppressing the return of the finch to its former status.

Choanotaeniaspp. infestation of Australian finches (Estrildidae)

Mortality of 2 to 5% was reported in young adult finches (Emblema, Poephila, Neochmia and Chloebia spp.) from aviaries in Victoria, Australia. Affected birds were depressed and had severe diarrhoea for 2 to 4 days before death. Lesions found on gross postmortem examination were marked distension of the duodenum by 20 to 40 cestodes (Choanotaenia spp.) and fluid-filled distal intestines. Histological examination of the duodenum revealed enteritis. The heavy cestode infection was considered the cause of the diarrhoea and deaths. Oral treatment of remaining finches in two aviaries with praziquantel was associated with cessation of mortality. Specific identification of the cestodes was not possible due to the condition of the specimens and the confused taxonomy of some Australian species of the genus. Control of the internal parasites, and of intermediate hosts in the environment, is important in captive finch management.

Acuaris skrjabini Infection of the Gizzard of Finches

Adult finches from aviaries in Victoria, Australia, were reported to experience a 4 to 5% mortality rate. Affected birds were lethargic and inappetant and had mild diarrhea for 1 to 2 days before death. Lesions found on post-mortem examination were gizzard mucosal necrosis, with an associated 30 to 60 Acuaria skrjabini spiruroids in each bird and surrounding inflammation. Treatment of remaining finches in the aviaries with either 80 mg of levamisole or 50 mg of fenbendazole per liter of drinking water for 3 days prevented further cases. Acuaria sp. infection can be an important predisposing factor in the mortality of aviary finches.