Social Feedback and the Emergence of Rank in Animal Society.

Dominance hierarchies are group-level properties that emerge from the aggression of individuals. Although individuals can gain critical benefits from their position in a hierarchy, we do not understand how real-world hierarchies form. Nor do we understand what signals and decision-rules individuals use to construct and maintain hierarchies in the absence of simple cues such as size or spatial location. A study of conflict in two groups of captive monk parakeets (Myiopsitta monachus) found that a transition to large-scale order in aggression occurred in newly-formed groups after one week, with individuals thereafter preferring to direct aggression more frequently against those nearby in rank. We consider two cognitive mechanisms underlying the emergence of this order: inference based on overall levels of aggression, or on subsets of the aggression network. Both mechanisms were predictive of individual decisions to aggress, but observed patterns were better explained by rank inference through subsets of the aggression network. Based on these results, we present a new theory, of a feedback loop between knowledge of rank and consequent behavior. This loop explains the transition to strategic aggression and the formation and persistence of dominance hierarchies in groups capable of both social memory and inference.

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.

[Endocrinologic studies of male psittacine birds for the evaluation of their reproductive status]. / Endokrinologische Untersuchung männlicher Papageienvögel zur Beurteilung ihres Reproduktionsstatus.

OBJECTIVE: Evaluating methods of hormone measurement in different specimens of male parrots in order to assess their reproductive status and stress axis. MATERIAL AND METHODS: Cockatiels and rose-ringed parakeets were chosen as psittaciforme representatives and their endocrine profiles were examined. In various pre-experiments, suitable techniques for the determination of testosterone in plasma, saliva and faeces of male parrots were established. Before analysing the samples by enzyme immunoassay, blood and faeces were extracted using diethyl ether, while saliva could be tested without extraction. Based on the excretion of mainly conjugated testosterone metabolites, parrots' faecal samples were also hydrolysed with ß-glucuronidase/arylsulfatase before extraction. In addition, the levels of the stress hormone corticosterone were determined by radioimmunoassay in order to assess possible relationships between stress and the secretion of testosterone. RESULTS: The examined psittacine species displayed different seasonal secretion patterns for both testosterone and corticosterone. Cockatiels had maximum plasma testosterone levels in February, in contrast, rose-ringed parakeets showed highest concentrations in November. As a consequence of cumulative excretion, both species showed much higher faecal than plasma testosterone concentrations. In rose-ringed parakeets, the levels of corticosterone in plasma were exceptionally high compared to the cockatiels. CONCLUSION: According to this study, we have been able to establish suitable methods for testosterone analysis in blood and faeces of cockatiels and rose-ringed parakeets, supporting the assessment of their reproductive status. At present saliva does not appear to be an ideal medium for reliable hormone level measurement, thus further investigations are required concerning this subject. CLINICAL RELEVANCE: By means of process analysis, it will be possible to detect increasing testosterone levels and/or pathological alterations, which could be considered in breeding programmes.

Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet.

As the only endemic neotropical parrot to have recently lived in the northern hemisphere, the Carolina parakeet (Conuropsis carolinensis) was an iconic North American bird. The last surviving specimen died in the Cincinnati Zoo in 1918 [1]. The cause of its extinction remains contentious: besides excessive mortality associated to habitat destruction and active hunting, their survival could have been negatively affected by its range having become increasingly patchy [2] or by the exposure to poultry pathogens [3, 4]. In addition, the Carolina parakeet showed a predilection for cockleburs, an herbaceous plant that contains a powerful toxin, carboxyatractyloside, or CAT [5], which did not seem to affect them but made the birds notoriously toxic to most predators [3]. To explore the demographic history of this bird, we generated the complete genomic sequence of a preserved specimen held in a private collection in Espinelves (Girona, Spain), as well as of a close extant relative, Aratinga solstitialis. We identified two non-synonymous genetic changes in two highly conserved proteins known to interact with CAT that could underlie a specific dietary adaptation to this toxin. Our genomic analyses did not reveal evidence of a dramatic past demographic decline in the Carolina parakeet; also, its genome did not exhibit the long runs of homozygosity that are signals of recent inbreeding and are typically found in endangered species. As such, our results suggest its extinction was an abrupt process and thus likely solely attributable to human causes.

Effect of photoperiod on the adrenal activities of male rose ringed parakeet, Psittacala krameri.

Adult male rose ringed parakeets were exposed to very long photoperiod (22 hr L: 2 hr D) and very short photoperiod (2 hr L: 22 hr D) daily for 60 days during different phases of the annual testicular cycle. Adrenal activities of the experimental birds were compared with that of parallel held natural photoperiodic birds. Marked atrophy of adrenocortical cells was noted in the glands of long photoperiod (22 hr L:2 hr D) during different phases, i.e., post-breeding, quiescent and pre-breeding phases of annual gonadal cycle. The atrophied cells were not uniformly distributed in different groups of long photoperiod responsive birds. During pre-breeding, post-breeding and quiescent phases marked atrophy of the adrenocortical cells were restricted to the sub capsular zone of the gland. The cytometric and karyometric studies also revealed significant decrease in the cortical cord width and diameter of nuclei in the cortical cells in either subcapsular zone in the gland of long photoperiodic birds considered for treatment during pre-breeding, post-breeding and quiescent phase or in both the sub capsular zone and the inner zone. The cytometric and karyometric values did not show any change from control birds.

Vocal-tract filtering by lingual articulation in a parrot.

Human speech and bird vocalization are complex communicative behaviors with notable similarities in development and underlying mechanisms. However, there is an important difference between humans and birds in the way vocal complexity is generally produced. Human speech originates from independent modulatory actions of a sound source, e.g., the vibrating vocal folds, and an acoustic filter, formed by the resonances of the vocal tract (formants). Modulation in bird vocalization, in contrast, is thought to originate predominantly from the sound source, whereas the role of the resonance filter is only subsidiary in emphasizing the complex time-frequency patterns of the source (e.g., but see ). However, it has been suggested that, analogous to human speech production, tongue movements observed in parrot vocalizations modulate formant characteristics independently from the vocal source. As yet, direct evidence of such a causal relationship is lacking. In five Monk parakeets, Myiopsitta monachus, we replaced the vocal source, the syrinx, with a small speaker that generated a broad-band sound, and we measured the effects of tongue placement on the sound emitted from the beak. The results show that tongue movements cause significant frequency changes in two formants and cause amplitude changes in all four formants present between 0.5 and 10 kHz. We suggest that lingual articulation may thus in part explain the well-known ability of parrots to mimic human speech, and, even more intriguingly, may also underlie a speech-like formant system in natural parrot vocalizations.

Feeding ecology of the Green-cheeked parakeet (Pyrrhura molinae) in dry forests in western Brazil.

The genus Pyrrhura includes small to medium-sized parakeets, which inhabit both low and dry alongside tall rainforests, mainly in South America. Pyrrhura molinae is still common, year round, in the markedly seasonal forests of western Brazil. This parakeet, as well as most Neotropical parrots, continues to be poorly understood. Hence, in the present study I examined their foraging ecology both in a highly deciduous and in a semi-deciduous forest in western Brazil. In addition, I assessed the relationship between food resource production (flowers and fruits), and the diet of this parakeet. Pyrrhura molinae exhibited a flexible diet consisting of 16 tree species, from which it consumed flowers (three species), seeds (three species), fruit pulp or aril (four species), and both pulp and seeds (six species). Parakeets consumed a wide array of fleshy fruits in the semi-deciduous forest, especially Cecropia pachystachya catkins. Conversely, in the highly deciduous forest they extensively foraged for figs (70% of the diet), in addition to nectar and seeds from dry fruits. Ficus calyptroceras, besides being abundant, bore fruits year round, and was substantially used by parakeets every month. Potentially, by exploiting a diverse set of plant food resources, and particularly due to the substantial use of figs, asynchronously produced, Pyrrhura molinae persists during the long dry season in the markedly seasonal forests of western Brazil.

History of nonnative Monk Parakeets in Mexico.

Nonnative Monk Parakeets have been reported in increasing numbers across many cities in Mexico, and were formally classified as an invasive species in Mexico in late 2016. However, there has not been a large-scale attempt to determine how international pet trade and national and international governmental regulations have played a part in colonization, and when the species appeared in different areas. We describe the changes in regulations that led the international pet trade market to shift to Mexico, then used international trade data to determine how many parakeets were commercially imported each year and where those individuals originated. We also quantified the recent increases in Monk Parakeet (Myiopsitta monachus) sightings in Mexico in both the scientific literature and in citizen science reports. We describe the timeline of increased reports to understand the history of nonnative Monk Parakeets in Mexico. As in other areas where the species has colonized, the main mode of transport is through the international pet trade. Over half a million Monk Parakeets were commercially imported to Mexico during 2000-2015, with the majority of importation (90%) occurring in 2008-2014, and almost all (98%) were imported from Uruguay. The earliest record of a free-flying Monk Parakeet was observed during 1994-1995 in Mexico City, but sightings of the parakeets did not become geographically widespread in either the scientific literature or citizen science databases until 2012-2015. By 2015, parakeets had been reported in 97 cities in Mexico. Mexico City has consistently seen steep increases in reporting since this species was first reported in Mexico. Here we find that both national and international legal regulations and health concerns drove a rise and fall in Monk Parakeet pet trade importations, shortly followed by widespread sightings of feral parakeets across Mexico. Further monitoring of introduced Monk Parakeet populations in Mexico is needed to understand the establishment, growth and spread of introduced populations.

Sedative effects of midazolam and xylazine with or without ketamine and detomidine alone following intranasal administration in Ring-necked Parakeets.

OBJECTIVE: To evaluate the effects of intranasal administration of midazolam and xylazine (with or without ketamine) and detomidine and their specific antagonists in parakeets. DESIGN: Prospective study. ANIMALS: 17 healthy adult Ring-necked Parakeets (Psittacula krameri) of both sexes (mean weight, 128.83+/-10.46 g [0.28+/-0.02 lb]). PROCEDURE: The dose of each drug or ketamine-drug combination administered intranasally that resulted in adequate sedation (ie, unrestrained dorsal recumbency maintained for >or=5 minutes) was determined; the onset of action, duration of dorsal recumbency, and duration of sedation associated with these treatments were evaluated. The efficacy of the reversal agents flumazenil, yohimbine, and atipamezole was also evaluated. RESULTS: In parakeets, intranasal administration of midazolam (7.3 mg/kg [3.32 mg/lb]) or detomidine (12 mg/kg [5.45 mg/lb]) caused adequate sedation within 2.7 and 3.5 minutes, respectively. Combinations of midazolam (3.65 mg/kg [1.66 mg/lb]) and xylazine (10 mg/kg [4.55 mg/lb]) with ketamine (40 to 50 mg/kg [18.2 to 22.7 mg/lb]) also achieved adequate sedation. Compared with detomidine, duration of dorsal recumbency was significantly longer with midazolam. Intranasal administration of flumazenil (0.13 mg/kg [0.06 mg/lb]) significantly decreased midazolam-associated recumbency time. Compared with the xylazineketamine combination, duration of dorsal recumbency was longer after midazolam-ketamine administration. Intranasal administration of flumazenil, yohimbine, or atipamezole significantly decreased the duration of sedation induced by midazolam, xylazine, or detomidine, respectively. CONCLUSIONS AND CLINICAL RELEVANCE: Intranasal administration of sedative drugs appears to be an acceptable method of drug delivery in Ring-necked Parakeets. Reversal agents are also effective when administered via this route.

Limited Dispersal and Significant Fine - Scale Genetic Structure in a Tropical Montane Parrot Species.

Tropical montane ecosystems are biodiversity hotspots harbouring many endemics that are confined to specific habitat types within narrow altitudinal ranges. While deforestation put these ecosystems under threat, we still lack knowledge about how heterogeneous environments like the montane tropics promote population connectivity and persistence. We investigated the fine-scale genetic structure of the two largest subpopulations of the endangered El Oro parakeet (Pyrrhura orcesi) endemic to the Ecuadorian Andes. Specifically, we assessed the genetic divergence between three sites separated by small geographic distances but characterized by a heterogeneous habitat structure. Although geographical distances between sites are small (3-17 km), we found genetic differentiation between all sites. Even though dispersal capacity is generally high in parrots, our findings indicate that dispersal is limited even on this small geographic scale. Individual genotype assignment revealed similar genetic divergence across a valley (~ 3 km distance) compared to a continuous mountain range (~ 13 km distance). Our findings suggest that geographic barriers promote genetic divergence even on small spatial scales in this endangered endemic species. These results may have important implications for many other threatened and endemic species, particularly given the upslope shift of species predicted from climate change.

Jaw myogenesis in the monk parakeet: evidence of developmental reprogramming in the emergence of novel muscles in Psittaciformes (Aves).

Psittaciformes have apomorphies in the muscles of the jaw that include both the adductors m. ethmomandibularis (EM) and m. pseudomasseter (PM), which are responsible for the generation of strong bite forces. While the EM is present in all Psittaciformes, the PM can be absent or present, and even underdeveloped or well-developed. The aim of this study is to identify developmental reprogramming processes by comparing the myogenesis of the jaw of the monk parakeet Myiopsitta monachus with the information available about other species of Psittaciformes. Seventeen specimens including embryos at different developmental stages, and nestlings of different ages were studied through the analysis of serial histological sections. At embryonic stage 24 (S24) the muscle precursor was observed in the first pharyngeal arch. At S27 the muscle precursor was found to be divided into lateral, intermediate and medial portions. At S31 the independent development of the EM as a rostro-dorsal projection of the mm. pterygoidei could be observed. At S36 the individualization of all muscles was complete. Finally, the PM was detected two days after hatching as an aponeurotic dorsal projection of the m. adductor mandibulae externus superficialis, located lateral to the arcus jugalis. Our results suggest that in M. monachus the muscles EM and PM emerge as a result of a process of heterotipy, and variations in the degree of development of the PM are associated to a heterochronic process of post-displacement, with M. monachus having an underdeveloped PM with respect to basal Psittaciformes.

Extensive consumption of Tabebuia aurea (Manso) Benth. & Hook. (Bignoniaceae) nectar by parrots in a Tecoma savanna in the southern Pantanal (Brazil).

Neotropical parrots forage for various food items such as seeds, fruit pulp, flowers, young leaves, and even arthropods. While foraging, many species wander over large areas that include both open and closed habitats. In this study, I examined parrot foraging activity during a brief synchronous and massive flowering in August 1998 in a tecoma savanna (dominated by Tabebuia aurea) in the southern Pantanal. Six parrot species, ranging from the small Brotogeris chiriri to the large Amazona aestiva, foraged for T. aurea nectar, but Nandayus nenday was by far the major nectar consumer, and the results of each of their visits, like those of the other species, was damage of a substantial proportion of the existing flower crop. Parrots foraged mostly during the afternoon, when nectar concentration tended to be higher. Nevertheless, compared to bird-pollinated flowers, which produce copious nectar, T. aurea had a smaller mean nectar volume per flower. Hence, presumably the amount of damage wreaked by these parrots resulted from their efforts to obtain part of their daily energy and water requirements. Thus, the synchronous and massive flowering occurring in such a brief period in the dry season may be related to, among other factors, the necessity of satiating predators such as parrots, which are still abundant in the Pantanal.

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.

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.

H2O2 production of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involved.

Birds have a maximum longevity (MLSP) much higher than mammals of similar body size in spite of their high metabolic rates. In this study, State 4 and State 3 rates of H2O2 production were lower in canary (MLSP = 24 years) and parakeet (MLSP = 21 years) than in mouse (MLSP = 3.5 years) heart mitochondria. Studies using specific inhibitors of the respiratory chain indicate that free radical generation sites at Complexes I and III are responsible for these differences. Main mechanisms lowering H2O2 production in these birds are a low rate of mitochondrial oxygen consumption in the parakeet and a low mitochondrial free radical leak in the canary. Strong increases in H2O2 production during active respiration (State 3) released by addition of ADP to pyruvate/malate-supplemented mitochondria are avoided in three species because the free radical leak decreases during the transition from State 4 to State 3 respiration. These results, together with those previously obtained in pigeons and in various mammalian species, suggest that the rate of mitochondrial free radical production correlates better with the rate of aging and the MLSP than the metabolic rate. They also suggest that a low rate of mitochondrial H2O2 production is a general characteristic of birds, animals showing very slow aging rates.

Reciprocal connections between primary and secondary auditory pathways in the telencephalon of the budgerigar (Melopsittacus undulatus).

Among avian species that learn their vocalizations, budgerigars have been thought to be unusual in receiving auditory input to the vocal control circuitry of the telencephalon via an auditory component of nucleus basalis (NB), rather than via Field L2, the end station of the classical thalamofugal pathway. In the present study, however, the application of neural tracing techniques showed the two auditory pathways to be reciprocally connected within the telencephalon. The implication is, therefore, that auditory information essential for vocal learning and vocal production in the budgerigar is derived from the primary as well as the secondary auditory pathway.

A comparative study of the beta-adrenoceptors in higher song nuclei of birds.

The present study analyses the presence of beta-adrenoceptors in the main telencephalic song nuclei of the goldfinch and parakeet, species belonging to the two most important groups of birds that reproduce learned songs: oscine songbirds and parrots, respectively. Brains of both species sectioned at appropriate levels were used to perform autoradiographic saturation studies using [3H]CGP 12177 as a radioligand. The results show similar K(D)values for both species (0.1-0.3 nM) and striking differences in Bmax. Thus, beta-adrenoceptors are abundant in the telencephalic vocal control nuclei of the parakeet but not of the goldfinch. The predominance of the beta2 subtype in the song nuclei of both species is also confirmed. We conclude that these receptors could be involved in functions unique to the parakeet and therefore may contribute to the greater flexibility of the vocal system of this species. Our findings also support the possible involvement of beta-adrenoceptors in the evolution of the avian brain.