Ontogeny of the adrenocortical response in an extremely altricial bird.

Life history theory predicts that physiological and behavioral responsiveness to stress should be delayed in development until the benefits of heightened reactivity outweigh the costs of potentially chronic glucocorticoid levels. Birds often acquire stress-responsiveness at locomotor independence, however, both stress-responsiveness and locomotor ability are delayed in birds with altricial developmental strategies. Parrots (Psittacidae) are extremely altricial, but it is not known whether they also postpone physiological responsiveness to stress until locomotor independence. We quantified individual variation in baseline and stress-induced plasma corticosterone (CORT) concentrations, the main avian glucocorticoid, in wild green-rumped parrotlets (Forpus passerinus) of Venezuela at four stages of nestling development. Parrotlet neonates are very underdeveloped and compete for parental care among extreme sibling size hierarchies, a competitive scenario that might benefit from early hypothalamic-pituitary-adrenal (HPA) functionality. Nestlings that underwent a standardized restraint stress-treatment showed higher average CORT concentrations compared to baseline in all age groups sampled, and exhibited no evidence of age-related changes in the stress response. This is 2 weeks before locomotor independence and earlier than previously documented for altricial species. Results suggest that precocity of HPA function may be advantageous to growth and survivorship in extremely altricial birds.

Influence of hand rearing and bird age on the fecal microbiota of the critically endangered kakapo.

The critically endangered New Zealand parrot, the kakapo, is subject to an intensive management regime aiming to maintain bird health and boost population size. Newly hatched kakapo chicks are subjected to human intervention and are frequently placed in captivity throughout their formative months. Hand rearing greatly reduces mortality among juveniles, but the potential long-term impact on the kakapo gut microbiota is uncertain. To track development of the kakapo gut microbiota, fecal samples from healthy, prefledged juvenile kakapos, as well as from unrelated adults, were analyzed by using 16S rRNA gene amplicon pyrosequencing. Following the original sampling, juvenile kakapos underwent a period of captivity, so further sampling during and after captivity aimed to elucidate the impact of captivity on the juvenile gut microbiota. Variation in the fecal microbiota over a year was also investigated, with resampling of the original juvenile population. Amplicon pyrosequencing revealed a juvenile fecal microbiota enriched with particular lactic acid bacteria compared to the microbiota of adults, although the overall community structure did not differ significantly among kakapos of different ages. The abundance of key operational taxonomic units (OTUs) was correlated with antibiotic treatment and captivity, although the importance of these factors could not be proven unequivocally within the bounds of this study. Finally, the microbial community structure of juvenile and adult kakapos changed over time, reinforcing the need for continual monitoring of the microbiota as part of regular health screening.

Theoretical morphology and development of flight feather vane asymmetry with experimental tests in parrots.

Asymmetry in flight feather vane width is a major functional innovation associated with the evolution of flight in the ancestors of birds. However, the developmental and morphological basis of feather shape is not simple, and the developmental processes involved in vane width asymmetry are poorly understood. We present a theoretical model of feather morphology and development that describes the possible ways to modify feather development and produce vane asymmetry. Our model finds that the theoretical morphospace of feather shape is redundant, and that many different combinations of parameters could be responsible for vane asymmetry in a given feather. Next, we empirically measured morphological and developmental model parameters in asymmetric and symmetric feathers from two species of parrots to identify which combinations of parameters create vane asymmetry in real feathers. We found that both longer barbs, and larger barb angles in the relatively wider trailing vane drove asymmetry in tail feathers. Developmentally, longer barbs were the result of an offset of the radial position of the new barb locus, whereas larger barb angles were produced by differential expansion of barbs as the feather unfurls from the tubular feather germ. In contrast, the helical angle of barb ridge development did not contribute to vane asymmetry and could be indicative of a constraint. This research provides the first comprehensive description of both the morphological and developmental modifications responsible for vane asymmetry within real feathers, and identifies key steps that must have occurred during the evolution of vane asymmetry.

Factors shaping the ontogeny of vocal signals in a wild parrot.

Parrots rely heavily on vocal signals to maintain their social and mobile lifestyles. We studied vocal ontogeny in nests of wild green-rumped parrotlets (Forpus passerinus) in Venezuela. We identified three successive phases of vocal signaling that corresponded closely to three independently derived phases of physiological development. For each ontogenetic phase, we characterized the relative importance of anatomical constraints, motor skills necessary for responding to specific contexts of the immediate environment, and the learning of signals that are necessary for adult forms of communication. We observed shifts in the relative importance of these three factors as individuals progressed from one stage to the next; there was no single fixed ratio of factors that applied across the entire ontogenetic sequence. The earliest vocalizations were short in duration, as predicted from physical constraints and under-developed motor control. Calls became longer and frequency modulated during intermediate nestling ages in line with motor skills required for competitive begging. In the week before fledging, calls drastically shortened in accordance with the flight-constrained short durations of adult contact calls. The latter constraints were made evident by the demonstrated links between wing-assisted incline running, a widespread prelude to avian flight, just before the shift from long-duration begging calls to short-duration contact calls. At least in this species, the shifting emphases of factors at different ontogenetic stages precluded the morphing of intermediate-stage begging calls into adult contact calls; as shown previously, the latter are influenced by sample templates provided by parents.

Vertical transmission of learned signatures in a wild parrot.

Learned birdsong is a widely used animal model for understanding the acquisition of human speech. Male songbirds often learn songs from adult males during sensitive periods early in life, and sing to attract mates and defend territories. In presumably all of the 350+ parrot species, individuals of both sexes commonly learn vocal signals throughout life to satisfy a wide variety of social functions. Despite intriguing parallels with humans, there have been no experimental studies demonstrating learned vocal production in wild parrots. We studied contact call learning in video-rigged nests of a well-known marked population of green-rumped parrotlets (Forpus passerinus) in Venezuela. Both sexes of naive nestlings developed individually unique contact calls in the nest, and we demonstrate experimentally that signature attributes are learned from both primary care-givers. This represents the first experimental evidence for the mechanisms underlying the transmission of a socially acquired trait in a wild parrot population.

Predation and infanticide influence ideal free choice by a parrot occupying heterogeneous tropical habitats.

The ideal free distribution (IFD) predicts that organisms will disperse to sites that maximize their fitness based on availability of resources. Habitat heterogeneity underlies resource variation and influences spatial variation in demography and the distribution of populations. We relate nest site productivity at multiple scales measured over a decade to habitat quality in a box-nesting population of Forpus passerinus (green-rumped parrotlets) in Venezuela to examine critical IFD assumptions. Variation in reproductive success at the local population and neighborhood scales had a much larger influence on productivity (fledglings per nest box per year) than nest site or female identity. Habitat features were reliable cues of nest site quality. Nest sites with less vegetative cover produced greater numbers of fledglings than sites with more cover. However, there was also a competitive cost to nesting in high-quality, low-vegetative cover nest boxes, as these sites experienced the most infanticide events. In the lowland local population, water depth and cover surrounding nest sites were related with F. passerinus productivity. Low vegetative cover and deeper water were associated with lower predation rates, suggesting that predation could be a primary factor driving habitat selection patterns. Parrotlets also demonstrated directional dispersal. Pairs that changed nest sites were more likely to disperse from poor-quality nest sites to high-quality nest sites rather than vice versa, and juveniles were more likely to disperse to, or remain in, the more productive of the two local populations. Parrotlets exhibited three characteristics fundamental to the IFD: habitat heterogeneity within and between local populations, reliable habitat cues to productivity, and active dispersal to sites of higher fitness.

Comparison of the nutrient analysis and caloric density of 30 commercial seed mixtures (in toto and dehulled) with 27 commercial diets for parrots.

In this paper, an overview is given of the composition of 30 commercially available parrot seed mixtures. As parrots dehull the seeds, the analysis of the total seed mixture tends to differ from that of the ingested feed. Statistical evaluation and comparison of the dehulled seeds vs. the whole seeds indicates that most parrot species are fed a diet rich in fat (31.7 +/- 13.1% crude fat) and energy (22.4 +/- 2.9 MJ ME/kg). As the analysis of the total seed mixtures underestimates fat and energy content of the ingested feed, it is suggested that researchers, bird nutritionists and bird food producers should calculate diets based on the analysis of the dehulled seeds. Finally, the calculated data were compared with the composition of formulated pelleted/extruded diets on the market. These data indicate that the energy density of most diets (15.6 +/- 1.4 MJ ME/kg) is far below the energy density of common seed mixtures.

Differential expression of glutamate receptors in avian neural pathways for learned vocalization.

Learned vocalization, the substrate for human language, is a rare trait. It is found in three distantly related groups of birds-parrots, hummingbirds, and songbirds. These three groups contain cerebral vocal nuclei for learned vocalization not found in their more closely related vocal nonlearning relatives. Here, we cloned 21 receptor subunits/subtypes of all four glutamate receptor families (AMPA, kainate, NMDA, and metabotropic) and examined their expression in vocal nuclei of songbirds. We also examined expression of a subset of these receptors in vocal nuclei of hummingbirds and parrots, as well as in the brains of dove species as examples of close vocal nonlearning relatives. Among the 21 subunits/subtypes, 19 showed higher and/or lower prominent differential expression in songbird vocal nuclei relative to the surrounding brain subdivisions in which the vocal nuclei are located. This included relatively lower levels of all four AMPA subunits in lMAN, strikingly higher levels of the kainite subunit GluR5 in the robust nucleus of the arcopallium (RA), higher and lower levels respectively of the NMDA subunits NR2A and NR2B in most vocal nuclei and lower levels of the metabotropic group I subtypes (mGluR1 and -5) in most vocal nuclei and the group II subtype (mGluR2), showing a unique expression pattern of very low levels in RA and very high levels in HVC. The splice variants of AMPA subunits showed further differential expression in vocal nuclei. Some of the receptor subunits/subtypes also showed differential expression in hummingbird and parrot vocal nuclei. The magnitude of differential expression in vocal nuclei of all three vocal learners was unique compared with the smaller magnitude of differences found for nonvocal areas of vocal learners and vocal nonlearners. Our results suggest that evolution of vocal learning was accompanied by differential expression of a conserved gene family for synaptic transmission and plasticity in vocal nuclei. They also suggest that neural activity and signal transduction in vocal nuclei of vocal learners will be different relative to the surrounding brain areas.

Development of the skeleton and feathers of dusky parrots (Pionus fuscus) in relation to their behaviour.

A clutch of five dusky parrots (Pionus fuscus) was observed from hatching to fully grown. They were examined radiographically from 16 to 45 days of age, a few days before the cessation of bone growth, and the development of their feathers and their behaviour were also studied. It was observed that when growing birds were removed from the nest and placed singly on a flat surface they would stand up and walk about until restrained; normally these birds would move very little and lie in an intertwined huddle that supported their relatively weak growing skeletons. At 50 days old they would climb to the nest entrance, retreating if scared. From day 51 the parrots flapped their wings vigorously inside the nest box, and they emerged at 53 days old when nearly all their large feathers had finished growing. These findings may help to explain the high rate of juvenile osteodystrophy in hand-reared parrots; premature exercise could lead to pathological deformity of the long bones, especially the major weight-bearing bone, the tibiotarsus.

Morphogenesis of parrot jaw muscles: understanding the development of an evolutionary novelty.

Parrots have developed novel head structures in their evolutionary history. The appearance of two new muscles for strong jaw adduction is especially fascinating in developmental and evolutionary contexts. However, jaw muscle development of parrots has not been described, despite its uniqueness. This report first presents the normal developmental stages of the cockatiel (Nymphicus hollandicus), comparable to that of the chick. Next, the peculiar skeletal myogenesis in the first visceral arch of parrots is described, mainly focusing on the development of two new jaw muscles. One of the parrot-specific muscles, M. ethmomandibularis, was initially detected at Nymphicus Stage 28 (N28) as the rostral budding of M. pterygoideus. After N32, the muscle significantly elongates rostrodorsally toward the interorbital septum, following a course lateral to the palatine bone. Another parrot-specific muscle, M. pseudomasseter, was first recognized at N36. The muscle branches off from the posteromedial M. adductor mandibulae externus and grows in a dorsolateral direction, almost covering the lateral surface of the jugal bar. The upper tip of the muscle is accompanied by condensed mesenchyme, which seems to be derived from cephalic neural crest cells.

Investigations on feathering, feather growth and potential influences of nutrient supply on feathers' regrowth in small pet birds (canaries, budgerigars and lovebirds).

The aim of this study was to quantitate feathering in several companion birds. Besides the ratio of feathers to whole body mass, feather length as well as feather weight were of interest. Furthermore, data on feather loss and growth rates were estimated. In general, it could be observed that the proportion of feathers relative to body mass varied between 14 (canaries) and 7.4% (lovebirds). Feather losses (outside the moult period) amounted to an average of 6.65 (canaries), 8.98 (budgerigars), and 8.43 (lovebirds) mg/bird/day respectively or 37 (canaries), 20 (budgerigars), and 17 (lovebirds) mg/100 g body weight/day (values of interest in calculating of protein requirements for maintenance). In canaries, the average growth rate of the developing feathers amounted to 2 mm/day. In contrast to the onset of feather regeneration, the growth rate of new feathers leaving the follicle was not influenced by the supplements used here. The regeneration period (first measurable feather growth) of a plucked pinion can be used as an indicator and objective parameter to test potential nutritional influences. Parallel to the improvement of nutrient supply the rates of feather losses and also replacement increased, whereas the rates decreased when seed mixtures without any addition of minerals, sulphurous amino acids, and vitamins were fed.

The skull development of parrots with special reference to the emergence of a morphologically unique cranio-facial hinge.

The order Psittaciformes (parrots) has unique morphological features in the head that are evolutionarily novel. To better understand the unique evolution of the head in parrots, the developmental pattern of the skull of the budgerigar (Melopsittacus undulatus) was initially described on the basis of transparent skeletal specimens. Although the fundamental pattern of the skull development of birds is conserved in parrots, some differences were observed between parrots and other groups of birds. In parrots, the vacuity in the interorbital septum did not emerge throughout ontogeny, in contrast to other lineages of birds, for example Galliformes and Coliiformes. This feature seems to be concerned with the attachment of the unique jaw muscle of parrots, M. ethmomandibularis, to the interorbital septum. In spite of a prokinetic skull, the cranio-facial hinge of parrots was brought about by secondary transformation of dermal bones unlike that of birds with a standard prokinetic skull (e.g. Corvus) in which the nasal-frontal suture directly becomes a hinge of bending. To further understand the evolution of "pseudoprokinesis" in parrots, the construction of a robust avian phylogeny is desired. The parrot-specific suborbital arch and cranio-facial hinge are not seen until birds leave the nest and can feed themselves. In conclusion, these structures are considered to be essential for eating hard and/or large meals.

Effect of age on seed digestion in parrots (Amazona aestiva).

The objective of this study was to compare the capacity of adult (more than 3 yr old) and young (less than 1 yr old) true parrots to digest seeds that are normally included in their diet in captivity, particularly soybean, sunflower, and corn. All the seeds were offered for 5 d with an interval of 15 d between different diets. The seeds of soybean and corn were boiled for 15 min and soaked in water at ambient temperature for 12 h before being fed to the birds. There were no differences in the digestibilities of crude protein and fats (ether extract) among animals, but the digestibilities of dry matter and crude fiber by the adult animals were higher than those of the young ones. The digestibility of carbohydrate (nitrogen-free extract) by adult birds was higher only for sunflower seeds. It is concluded that the capacity of parrots to digest fiber may change according to the age of the animal. Since the digestion of fiber depends on the action of microorganisms, these results suggest that the colonization of the gastrointestinal tract is delayed or very slow in young parrots.

Simultaneous development of vocal and physical object combinations by a Grey parrot (Psittacus erithacus): bottle caps, lids, and labels.

On the basis of primarily behavioral data, researchers (e.g., P. M. Greenfield, 1991) have argued (a) that parallel development of communicative and physical object (manual) combinatorial abilities exists in young children; (b) that these abilities initially have a common neural substrate; (c) that a homologous substrate in great apes allows for similar, if limited, parallel development of these 2 abilities; and (d) that such abilities thus may indicate a shared evolutionary history for both communicative and physical behavior (J. Johnson-Pynn, D. M. Fragaszy, E. M. Hirsh, K. E. Brakke, & P. M. Greenfield, 1999). The authors of the present study found a comparable, if limited, parallel combinatorial development in a Grey parrot (Psittacus erithacus). Given the evolutionary distance between parrots and primates, the authors suggest that the search for and arguments concerning responsible substrates and common behavior should be approached with care and should not be restricted to the primate line.

Development of thermoregulation and posthatching growth in the altricial cockatiel Nymphicus hollandicus.

The development of thermoregulation and growth during the nestling period of cockatiel Nymphicus hollandicus were examined in this study. It was hypothesised that, in comparison to other altricial species of similar body mass, cockatiel chicks develop endothermy earlier and consequently have less energy available for growth, resulting in reduced growth rates. While poorly insulated and blind at hatching, cockatiel developed endothermic responses in their first week, and were individually effectively homeothermic (with 75% of adult ability to maintain body temperature during exposure to 20 degrees-25 degrees C), by maintaining high metabolic rates (at all ambient temperatures tested) above the predicted resting rates of an adult of similar body mass before parental brooding ceased (12-13 d). Mass-independent metabolic rates were equivalent to those of fledglings at only 20% of the nestling period (37 d), well before adequate insulation was obtained. The Gompertz growth constants of cockatiel were significantly lower than those of other altricial land birds, which supports the hypothesis of this study.

The nutrition of the budgerigar (Melopsittacus undulatus).

Growing interest in the nutrition of the budgerigar (Melopsittacus undulatus) has highlighted the paucity of knowledge in this area. The aims of this study were to review the available literature on their individual nutrient requirements and relate this to the nutrient content of their predominantly seed-based diet and to investigate the effect of the bird's daily energy requirement on the fluctuations in body weight. Studies were conducted at the Waltham Centre to measure the relationship between daily metabolizable energy intake (kJ/kg BW) and body weight change (g/d) for groups of adult budgerigars. The birds were found to require daily 48-128 kJ/bird depending on their body mass (birds in our colony typically weigh 30-80 g). During a series of breeding trials the daily energy intake for a breeding pair plus their three chicks, at peak energy intake, was found to be 483-505 kJ (at pairing, the mean daily energy intake of the breeding pairs was 231 kJ). Apparent metabolizability of the major nutrients from a seed diet were generally found to be greater than 80%, which allows these birds to assimilate the high levels of energy needed for their basal metabolism. In summary, the nutrient requirements of the budgerigar (where known) were found to be similar to those of other avian species, however, further work is needed, especially in the area of availability of key nutrients. Further developments in the dietary management of these birds will only be possible if researchers can overcome the birds' poor acceptance of novel foods and satisfy their high basal energy requirements before establishing their requirements for individual nutrients.