The uropygial gland of the monk parakeet Myiopsitta monachus: Histology, morphogenesis, and evolution within Psittaciformes (Aves).

We describe the morphology, histology, and histochemical characteristics of the uropygial gland (UG) of the monk parakeet Myiopsitta monachus. The UG has a heart-shape external appearance and adenomers extensively branched with a convoluted path, covered by a stratified epithelium formed by different cellular strata and divided into three zones (based on the epithelial height and lumen width), a cylindrical papilla with an internal structure of delicate type and two excretory pores surrounded by a feather tuft. Histochemical and lectin-histochemical techniques performed showed positivity against PAS, AB pH 2.5, AB-PAS, and some lectines, likely related to the granivorous feeding habits. Also, we describe the morphogenesis of the UG of the monk parakeet, which appears at embryological stage 34 as a pair of ectodermal invaginations. Heterochronic events in the onset development of the UG when compared with other birds could be recognized. Finally, to examine the phylogenetic occurrence of the UG within the Psittaciformes and infer its evolutionary history, we mapped its presence/absence over a molecular phylogeny. The reconstruction of the characters states at ancestral nodes revealed that the presence of the UG was the plesiomorphic feature for Psittaciformes and its loss evolved independently more than once.

Quantitative genetics in the monk parakeet (Myiopsitta monachus) from central Argentina: Estimation of heritability and maternal effects on external morphological traits.

The monk parakeet (Myiopsitta monachus) is a South American species unique among parrots; it builds communal stick nests that allow independence from tree or cliff cavities required by most parrots. As a very successful invasive species, it has expanded into several countries around the world. Questions remain around the factors that allowed this species to be such a successful invader in its native range as in other countries, and particularly the extent that evolutionary processes may be involved in adapting to new areas. Along with this line of analysis, we focused on assessing whether morphological characteristics are sufficiently heritable, and therefore responsive to selection. As the first step in this direction, we have estimated heritability of monk parakeet in six external morphological traits considered of potential adaptability value. Samples were obtained in the province of Córdoba in central Argentina. Data from seven microsatellites were used to determine the familial relationships among individuals. Heritabilities and genetic correlations were estimated by means of animal models. We found evidence for significant heritability in the six traits measured, particularly in weight, tarsus length and bill width. We also found evidence of maternal effects on morphological traits, particularly in the traits with lower heritability: wing length, bill length and tail length. Genetic correlations between traits were significant and associated with phenotypic correlations, suggesting that these traits are constrained in terms of evolutionary potential, whereas the amount of additive genetic variance in weight, tarsus length and bill width indicate that these traits could be responsive to selection.

The identity of the mysterious "Azara's Parakeet" Sittace flaviventris Wagler, 1832.

Sittace flaviventris Wagler, 1832 was the name given to Azara's No. 276 "Maracaná cabeza y encuentro roxos", but since then the identity of the species has remained a mystery. Based on a tail-less domestic individual, it has most often been attributed to an aberrant Aratinga parakeet, and is currently considered a doubtful taxon. In this note the identity of "Azara's Parakeet" is confirmed as Red-spectacled Amazon Amazona pretrei (Temminck, 1830), a species that still occurs today in the region from where Azara described it. Sittace flaviventris is thus a junior synonym of Amazona pretrei.

Computed tomographic anatomy of the heads of blue-and-gold macaws (Ara ararauna), African grey parrots (Psittacus erithacus), and monk parakeets (Myiopsitta monachus).

OBJECTIVE To create an atlas of the normal CT anatomy of the head of blue-and-gold macaws (Ara ararauna), African grey parrots (Psittacus erithacus), and monk parakeets (Myiopsitta monachus). ANIMALS 3 blue-and-gold macaws, 5 African grey parrots, and 6 monk parakeets and cadavers of 4 adult blue-and-gold macaws, 4 adult African grey parrots, and 7 monk parakeets. PROCEDURES Contrast-enhanced CT imaging of the head of the live birds was performed with a 4-multidetector-row CT scanner. Cadaveric specimens were stored at -20°C until completely frozen, and each head was then sliced at 5-mm intervals to create reference cross sections. Frozen cross sections were cleaned with water and photographed on both sides. Anatomic structures within each head were identified with the aid of the available literature, labeled first on anatomic photographs, and then matched to and labeled on corresponding CT images. The best CT reconstruction filter, window width, and window level for obtaining diagnostic images of each structure were also identified. RESULTS Most of the clinically relevant structures of the head were identified in both the cross-sectional photographs and corresponding CT images. Optimal visibility of the bony structures was achieved via CT with a standard soft tissue filter and pulmonary window. The use of contrast medium allowed a thorough evaluation of the soft tissues. CONCLUSIONS AND CLINICAL RELEVANCE The labeled CT images and photographs of anatomic structures of the heads of common pet parrot species created in this study may be useful as an atlas to aid interpretation of images obtained with any imaging modality.

Development of the Superaltricial Monk Parakeet (Aves, Psittaciformes): Embryo Staging, Growth, and Heterochronies.

Knowledge about the embryonic stages of birds is important in answering many questions about development and evolution. We give the first description of 41 embryological stages of the monk parakeet (Myiopsitta monachus) on the basis of external morphology and comparison with the chicken. We also provide measurements of some external morphological characters (i.e. body mass, crown-rump, beak, forelimb, and third toe lengths) and perform comparisons with other precocial and altricial birds with the aim of identifying heterochronous developmental features. The following differences in the development of characters in the monk parakeet when compared with other birds were found: (1) delay of the feathers primordia, (2) wing buds initially greater than leg buds, (3) forelimbs and hindlimbs with similar relative size, (4) retroversion of the toe IV, (5) ventral curvature of the upper jaw, (6) positive regressions between stages and beak length with acceleration and higher values and III toe lengths with deceleration and lower values in the monk parakeet compared to the chicken. The growth pattern of the monk paraket Myiopsitta monachus could be influenced by some heterochronic processes like post-displacement, acceleration and/or deceleration. Results of this research allow the standard identification of stages in different species of parrots, recognize similarities and differences between precocial (the chicken) and altricial species (Myiopsitta), and provide planning data for future studies.

Jaw myology and bite force of the monk parakeet (Aves, Psittaciformes).

Psittaciform birds exhibit novelties in jaw bone structure and musculature that are associated with strong bite forces. These features include an ossified arcus suborbitalis and the muscles ethmomandibularis and pseudomasseter. We analyse the jaw musculature of the monk parakeet (Myiopsitta monachus) to enable future studies aimed at understanding craniofacial development, morphology, function and evolution. We estimate bite force based on muscle dissections, physiological cross-sectional area and skull biomechanical modelling. We also compare our results with available data for other birds and traced the evolutionary origin of the three novel diagnostic traits. Our results indicate that, in Myiopsitta, (i) the arcus suborbitalis is absent and the orbit is ventrally closed by an elongate processus orbitalis and a short ligamentum suborbitale; (ii) the ethmomandibularis muscle is a conspicuous muscle with two bellies, with its origin on the anterior portion of the septum interorbitale and insertion on the medial aspect of the mandible; (iii) the pseudomasseter muscle consists of some fibers arising from the m. adductor mandibulae externus superficialis, covering the lateral surface of the arcus jugalis and attaches by an aponeurotic sheet on the processus orbitalis; (iv) a well-developed adductor mandibulae complex is present; (v) the bite force estimation relative to body mass is higher than that calculated for other non-psittaciform species; and (vi) character evolution analysis revealed that the absence of the arcus suborbitalis and the presence of the m. pseudomassseter are the ancestral conditions, and mapping is inconclusive about presence of one or two bellies of the m. ethmomandibularis.

Hindlimb myology of the monk parakeet (Aves, Psittaciformes).

We studied the hindlimb myology of the monk parakeet (Myiopsitta monachus). Like all parrots, it has zygodactyl feet enabling perching, climbing, hanging, moving easily among trees, and handling food. Muscles were described and weighed, and physiological cross-sectional area (PCSA) of four flexors and one extensor was calculated. In comparison to other muscles, the M. tibialis cranialis and the M. fibularis brevis show increased development and high PCSA values, and therefore, large potential force production. Also, a large proportion of muscle mass was involved in flexing the digits. We hypothesize that these muscle traits are associated with the arboreal locomotion and food manipulation habits. In the monk parakeet, the M. extensor digitorum longus sends a branch to the hallux, and the connection between the M. flexor digitorum longus and the M. flexor hallucis longus is type I (Gadow's classification). We reaffirm the presence of the M. ambiens as a plesiomorphic condition that disappears in most members of the order. Among Psittaciformes, the M. fibularis brevis is stronger and the M. fibularis weaker in arboreal species than in basal terrestrial ones (e.g., Strigops).

Vocal tract articulation revisited: the case of the monk parakeet.

Birdsong and human speech share many features with respect to vocal learning and development. However, the vocal production mechanisms have long been considered to be distinct. The vocal organ of songbirds is more complex than the human larynx, leading to the hypothesis that vocal variation in birdsong originates mainly at the sound source, while in humans it is primarily due to vocal tract filtering. However, several recent studies have indicated the importance of vocal tract articulators such as the beak and oropharyngeal-esophageal cavity. In contrast to most other bird groups, parrots have a prominent tongue, raising the possibility that tongue movements may also be of significant importance in vocal production in parrots, but evidence is rare and observations often anecdotal. In the current study we used X-ray cinematographic imaging of naturally vocalizing monk parakeets (Myiopsitta monachus) to assess which articulators are possibly involved in vocal tract filtering in this species. We observed prominent tongue height changes, beak opening movements and tracheal length changes, which suggests that all of these components play an important role in modulating vocal tract resonance. Moreover, the observation of tracheal shortening as a vocal articulator in live birds has to our knowledge not been described before. We also found strong positive correlations between beak opening and amplitude as well as changes in tongue height and amplitude in several types of vocalization. Our results suggest considerable differences between parrot and songbird vocal production while at the same time the parrot's vocal articulation might more closely resemble human speech production in the sense that both make extensive use of the tongue as a vocal articulator.

Species differences in early patterning of the avian brain.

The telencephalon is proportionately larger in parrots than in galliformes (chicken-like birds), whereas the midbrain tectum is proportionately smaller. We here test the hypothesis that the adult species difference in midbrain proportion is due to an evolutionary change in early brain patterning. In particular, we compare the size of the early embryonic midbrain between parakeets (Melopsittacus undulatus) and bobwhite quail (Colinus virgianus) by examining the expression domains of transcription factors Pax6 and Gbx2, which are expressed in the forebrain and hindbrain, respectively. Because these expression domains form rostral and caudal borders with the presumptive midbrain when this region is specified (Hamburger-Hamilton stages 9-11), they allow us to measure and compare the sizes of a molecularly defined presumptive midbrain in the two species. Based on published data from older embryos, we predicted that the molecularly defined midbrain territory is significantly larger in quail than parakeets. Indeed, our data show that normalized midbrain length is 33% greater in quail and that the midbrain to forebrain ratio is 28% greater. This is strong evidence of a significant species difference in early brain patterning.

Digit ratio in birds.

The Homeobox (Hox) genes direct the development of tetrapod digits. The expression of Hox genes may be influenced by endogenous sex steroids during development. Manning (Digit ratio. New Brunswick, NJ: Rutgers University Press, 2002) predicted that the ratio between the lengths of digits 2 (2D) and 4 (4D) should be sexually dimorphic because prenatal exposure to estrogens and androgens positively influence the lengths of 2D and 4D, respectively. We measured digits and other morphological traits of birds from three orders (Passeriformes, house sparrow, Passer domesticus; tree swallow, Tachycineta bicolor; Pscittaciformes, budgerigar, Melopsittacus undulates; Galliformes, chicken, Gallus domesticus) to test this prediction. None were sexually dimorphic for 2D:4D and there were no associations between 2D:4D and other sexually dimorphic traits. When we pooled data from all four species after we averaged right and left side digits from each individual and z-transformed the resulting digit ratios, we found that males had significantly larger 2D:4D than did females. Tetrapods appear to be sexually dimorphic for 2D:4D with 2D:4D larger in males as in some birds and reptiles and 2D:4D smaller in males as in some mammals. The differences between the reptile and mammal lineages in the directionality of 2D:4D may be related to the differences between them in chromosomal sex determination. We suggest that (a) natural selection for a perching foot in the first birds may have overridden the effects of hormones on the development of digit ratio in this group of vertebrates and (b) caution be used in making inferences about prenatal exposure to hormones and digit ratio in birds.

Developmental origins of species differences in telencephalon and tectum size: morphometric comparisons between a parakeet (Melopsittacus undulatus) and a quail (Colinus virgianus).

Parrots, including parakeets, evolved significantly larger brains than other birds, relative to their body size, and they possess a proportionately larger telencephalon. For example, the telencephalon occupies approximately 68% of the brain in parakeets but only 52% in bobwhite quail. The present study was designed to determine when and how this difference in brain region proportions arises during development. To that end, we present volumetric data on the major brain regions in parakeets and bobwhite quail at several stages of embryogenesis, at hatching and, for the parakeets, 1 week after hatching. We also report on the proportional sizes of each region's proliferative and postproliferative zones. One major finding is that parakeets develop a proportionately larger telencephalon relatively late in development and that this late increase correlates with a delay in telencephalic neurogenesis. The most prominent aspect of this delayed telencephalic development is a tremendous expansion of the proliferative subventricular zone in the telencephalon of late embryonic and posthatching parakeets. The second major finding is that the tectum is much smaller in parakeets than in quail at all developmental stages examined, suggesting that the tectum's reduced size is due to an evolutionary change in how much tissue was allocated to become tectum at the time of brain regionalization. Collectively these findings indicate that evolutionary changes in brain region proportions are caused not by a single type of change but by several distinct developmental mechanisms, including changes in brain regionalization and neurogenesis timing.

Molecular phylogeny and morphological change in the Psittacula parakeets.

We reconstruct a phylogeny of the African and Asian Psittacula parakeets using approximately 800bp of mitochondrial cytochrome b sequence to examine their evolutionary relationships in reference to their head plumage and major morphological tail innovations. Our phylogeny identifies three groups, whose distinctiveness is also apparent from their possession of three different head plumage characters: a neck ring, a distinctive colouration of the head, and a 'moustache'-shaped pattern that extends from the chin to the cheek. We examine the extent of sexual dimorphism in tail length across the phylogeny and reveal large differences between closely related forms. We apply a range of published avian cytochrome b substitution rates to our data, as an alternative to internal calibration of a molecular clock arising from incomplete paleontological information. An ancestral Psittacula form appears to have evolved during the late Miocene-early Pliocene (3.4-9.7MYA), a time when regional geological processes on the Asian continent may have promoted subsequent diversity at the species level, and many forms diverged relatively early on in the evolutionary history of Psittacula (between 2.5 and 7.7MYA). However, others, such as the derbyan and moustached parakeets, diverged as recently as 0.2MYA. Our phylogeny also suggests that the echo parakeet from Mauritius diverged from the Indian ringneck parakeet as opposed to the African ringneck, and may have done so relatively recently. The molecular results indicate support for a southwards radiation from India across the Indian Ocean to Mauritius, where the arrival-date of the echo parakeet appears consistent with the island's volcanic formation.

Molecular mapping of brain areas involved in parrot vocal communication.

Auditory and vocal regulation of gene expression occurs in separate discrete regions of the songbird brain. Here we demonstrate that regulated gene expression also occurs during vocal communication in a parrot, belonging to an order whose ability to learn vocalizations is thought to have evolved independently of songbirds. Adult male budgerigars (Melopsittacus undulatus) were stimulated to vocalize with playbacks of conspecific vocalizations (warbles), and their brains were analyzed for expression of the transcriptional regulator ZENK. The results showed that there was distinct separation of brain areas that had hearing- or vocalizing-induced ZENK expression. Hearing warbles resulted in ZENK induction in large parts of the caudal medial forebrain and in 1 midbrain region, with a pattern highly reminiscent of that observed in songbirds. Vocalizing resulted in ZENK induction in nine brain structures, seven restricted to the lateral and anterior telencephalon, one in the thalamus, and one in the midbrain, with a pattern partially reminiscent of that observed in songbirds. Five of the telencephalic structures had been previously described as part of the budgerigar vocal control pathway. However, functional boundaries defined by the gene expression patterns for some of these structures were much larger and different in shape than previously reported anatomical boundaries. Our results provide the first functional demonstration of brain areas involved in vocalizing and auditory processing of conspecific sounds in budgerigars. They also indicate that, whether or not vocal learning evolved independently, some of the gene regulatory mechanisms that accompany learned vocal communication are similar in songbirds and parrots.

Vocal control pathways through the anterior forebrain of a parrot (Melopsittacus undulatus).

A feature of the telencephalic vocal control system in the budgerigar (Melopsittacus undulatus) that has been hypothesized to represent a profound difference in organization from the oscine vocal system is its reported lack of an inherent circuit through the anterior forebrain. The present study reports anatomical connections that indicate the existence of an anterior forebrain circuit comparable in important ways to the "recursive" pathway of oscine songbirds. Results from anterograde and retrograde tracing experiments with biocytin and fluorescently labeled dextran amines indicate that the central nucleus of the anterior archistriatum (AAc) is the source of ascending projections upon the oval nuclei of the anterior neostriatum and ventral hyperstriatum (NAo and HVo, respectively). Efferent projections from the latter nuclei terminate in the lateral neostriatum afferent to AAc, thereby forming a short recurrent pathway through the pallium. Previously reported projections from HVo and NAo upon the magnocellular nucleus of the lobus parolfactorius (LPOm), and after LPOm onto the magnocellular nucleus of the dorsal thalamus (DMm; G.F. Striedter [1994] J. Comp. Neurol. 343:35-56), are confirmed. A specific projection from DMm onto NAom is also demonstrated; therefore, a recurrent pathway through the basal forebrain also exists in the budgerigar vocal system that is similar to the anterior forebrain circuit of oscine songbirds. Parallels between these circuits and mammalian basal ganglia-thalamo-cortical circuits are discussed. It is hypothesized that vocal control nuclei of the avian anterior neostriatum may perform a function similar to the primate supplemental motor area.

The vocal control pathways in budgerigars differ from those in songbirds.

Previous studies concluded that parrots and oscine songbirds, two taxa that have independently evolved the ability to learn vocalizations, possess similar neural circuits for vocal control. These investigations suggested, however, that the vocal control systems of parrots and songbirds may also differ in several respects. Most importantly, auditory inputs to the vocal control system derive from Field L in songbirds, but this area does not appear to project to the vocal control system in parrots. The principal aims in the present study were, therefore, to determine 1) exactly how similar the vocal control system in budgerigars is to that in songbirds and 2) whether the vocal control system in budgerigars receives auditory inputs from areas other than Field L. Biotinylated and fluorescently labeled dextrans were injected into five telencephalic nuclei of the vocal control system in budgerigars and into the physiologically identified auditory portions of the frontal neostriatum and nucleus basalis. The results indicate that the forebrain vocal control system in budgerigars is only superficially similar to that in songbirds. Many of the vocal control nuclei differ between the two taxa in both cytoarchitecture and connections. The nuclei in budgerigars that are comparable to those of the accessory loop of the vocal control system in songbirds, for example, do not form an accessory loop in budgerigars. The vocal control systems in the two taxa differ most significantly in the source of their auditory inputs. In songbirds, auditory information is conveyed to the vocal control system via Field L, whereas, in budgerigars, the auditory inputs to the vocal control system derive from nucleus basalis and the frontal neostriatum. A phylogenetic analysis suggests that the midbrain and medullary vocal control pathways are homologous across all birds, but that most of the vocal control circuits in the forebrain have probably evolved independently in parrots and songbirds.

Ultrastructure and secretory nature of the seminal glomus in budgerigars (Melopsittacus undulatus).

The seminal glomera from captive budgerigars were dissected and prepared for ultrastructural and histochemical studies of the lining epithelia. The general structure suggested that they are formed by convolutions of the terminal portions of the ductus deferens which appear as a network of tubules. The epithelium lining the tubules was identified as pseudostratified ciliated and non-ciliated columnar epithelium. With the electron microscope it was possible to identify two different cell types in the epithelium: type 1, ciliated cells and type 2, non-ciliated epithelial cells. Light microscopy revealed periodic acid Schiff (PAS) positive material, resistant to diastase digestion in the distal parts of some of the epithelial cells, indicating its glycoprotein nature. Alcian blue/PAS staining showed mixed acidic and neutral glycoproteins. Alcian blue staining at different hydrogen ion concentrations (pH) showed that the acidic glycoprotein was of the weakly sulphated type. Periodic acid thiocarbohydrazide silver proteinase staining, at the ultrastructural level, confirmed the presence of an intracellular glycoprotein.

Anatomical study of the parrakeet (Aratinga canalicularis)

De estudios recientes sobre la organización del telencéfalo de las aves se sabe que esta estructura tiene muchas similitudes cocn el cerebro de los mamíferos. Tambíen se conoce que la porción del hiperestriado dorsal conocida como la wulst así cocmo la porción lateral, identificada como el lado ventricular dorsal, tiene un papel importante en la integración sensorial, el aprendizaje y la producción del canto en las aves. Aunque ambas estructuras no poseen laminación como la de la neocorteza de los mamíferos, sin embargp, ciertas aves como el búho muestran una clara pseudolaminación. En la literatura no hay descripciones anatómicas de la wulst en preicos, por lo que el objetivo del presente trabajo fue estudiar esta estructura en la ewpecie. Aratinga canicularis. Se identificaron tres tipos celulares y, mediante métodos morfométricos efectuados en un total de 240 células por cada estrato, se midieron 10 parámetros distintos y se distinguieron tres estratos, a los que se les denominó dorsal, medial y ventral. Cada uno de los tres tipos celulares presentaron características específicas. Las células multipolares y triangulares mostraron un patrón dendrítico ramificado y abundantes espinas dendríticas. Las triangulares difieron en cuanto a la extensión de sus dendritas y la ramificación de su axón en ángulos rectos dirigidos hacia el estrato suprayacente. Las células ovoides fueron las mas pequeñas con pocas ramas y espinas. Estas células son similares a las del hiperestriatum accesorio del buho, las que a su vez son análogas a las células granulares de la corteza visual de los mamíferos