Developmental basis for telencephalon expansion in waterfowl: enlargement prior to neurogenesis

Some altricial and some precocial species of birds have evolved enlarged telencephalons compared with other birds. Previous work has shown that finches and parakeets, two species that hatch in an immature (i.e. altricial) state, enlarged their telencephalon by delaying telencephalic neurogenesis. To determine whether species that hatch in a relatively mature (i.e. precocial) state also enlarged their telencephalon by delaying telencephalic neurogenesis, we examined brain development in geese, ducks, turkeys and chickens, which are all precocial. Whereas the telencephalon occupies less than 55 per cent of the brain in chickens and turkeys, it occupies more than 65 per cent in ducks and geese. To determine how these species differences in adult brain region proportions arise during development, we examined brain maturation (i.e. neurogenesis timing) and estimated telencephalon, tectum and medulla volumes from serial Nissl-stained sections in the four species. We found that incubation time predicts the timing of neurogenesis in all major brain regions and that the telencephalon is proportionally larger in ducks and geese before telencephalic neurogenesis begins. These findings demonstrate that the expansion of the telencephalon in ducks and geese is achieved by altering development prior to neurogenesis onset. Thus, precocial and altricial species evolved different developmental strategies to expand their telencephalon.     

Monoamine containing neurons in the pigeon brain stem and their terminal fields in the telencephalon

Cellular localization of monoamines in the upper brain stem and distribution of their telencephalic terminal fields were studied in pigeons by fluorescence histochemistry. Two distinct cellular types were identified: one containing primary catecholamines (NE or DA), the other, 5-HT. In the telencephalon numerous DA axons were identified in the paleostriatum augmentatum and in the lobus paraolfactorius. The noradrenergic fibers were mainly concentrated in the Wulst regions which receive visual afferents from the dorsolateral thalamus.     

Interspecies avian brain chimeras reveal that large brain size differences are influenced by cell-interdependent processes

Like humans, birds that exhibit vocal learning have relatively delayed telencephalon maturation, resulting in a disproportionately smaller brain prenatally but enlarged telencephalon in adulthood relative to vocal non-learning birds. To determine if this size difference results from evolutionary changes in cell-autonomous or cell-interdependent developmental processes, we transplanted telencephala from zebra finch donors (a vocal-learning species) into Japanese quail hosts (a vocal non-learning species) during the early neural tube stage (day 2 of incubation), and harvested the chimeras at later embryonic stages (between 9-12 days of incubation). The donor and host tissues fused well with each other, with known major fiber pathways connecting the zebra finch and quail parts of the brain. However, the overall sizes of chimeric finch telencephala were larger than non-transplanted finch telencephala at the same developmental stages, even though the proportional sizes of telencephalic subregions and fiber tracts were similar to normal finches. There were no significant changes in the size of chimeric quail host midbrains, even though they were innervated by the physically smaller zebra finch brain, including the smaller retinae of the finch eyes. Chimeric zebra finch telencephala had a decreased cell density relative to normal finches. However, cell nucleus size differences between each species were maintained as in normal birds. These results suggest that telencephalic size development is partially cell-interdependent, and that the mechanisms controlling the size of different brain regions may be functionally independent.     

Phylogenetic relationships of the paraphyletic ‘caprimulgiform’ birds (nightjars and allies)

In the past years, paraphyly of the traditional ‘Caprimulgiformes’ (nightjars and allies) with respect to Apodiformes (swifts and hummingbirds) has been well established, but the relationships between the five ‘caprimulgiform’ family‐level taxa remain controversial. These crepuscular or nocturnal birds differ in numerous anatomical features, and here an analysis of 69 morphological characters is performed. Except for the position of the Nyctibiidae (potoos), the topology of the single most‐parsimonious tree agrees with the results of a recently published large‐scale ‘phylogenomic’ study. Whereas molecular data support a clade including Nyctibiidae and the Steatornithidae (oilbird), potoos were shown to be the sister taxon of Caprimulgidae (nightjars) in the present analysis. A sister group relationship between Nyctibiidae and Caprimulgidae is strongly supported, both in terms of bootstrap robustness and the number of synapomorphies, and it is detailed that the morphological data are more likely to reflect the true relationships of these birds. A classification is proposed, and the term Strisores is introduced for a clade including all ‘Caprimulgiformes’ and Apodiformes. It is most parsimonious to assume a single origin of dark activity in the stem lineage of Strisores and a reversal to diurnal activity in Apodiformes. However, a fourfold origin of dark‐activity in the stem lineages of Steatornithidae, Podargidae, Aegothelidae and the Caprimulgidae/Nyctibiidae cannot be conclusively excluded with the data at hand.     

Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds

In mammals, species with more frontally oriented orbits have broader binocular visual fields and relatively larger visual regions in the brain. Here, we test whether a similar pattern of correlated evolution is present in birds. Using both conventional statistics and modern comparative methods, we tested whether the relative size of the Wulst and optic tectum (TeO) were significantly correlated with orbit orientation, binocular visual field width and eye size in birds using a large, multi-species data set. In addition, we tested whether relative Wulst and TeO volumes were correlated with axial length of the eye. The relative size of the Wulst was significantly correlated with orbit orientation and the width of the binocular field such that species with more frontal orbits and broader binocular fields have relatively large Wulst volumes. Relative TeO volume, however, was not significant correlated with either variable. In addition, both relative Wulst and TeO volume were weakly correlated with relative axial length of the eye, but these were not corroborated by independent contrasts. Overall, our results indicate that relative Wulst volume reflects orbit orientation and possibly binocular visual field, but not eye size.     

Old growth and secondary forest site occupancy by nocturnal birds in a neotropical landscape

High rates of old growth (OG) forest destruction and difficult farming conditions result in increasing cover of secondary forests (SF) in the Amazon. In this setting, it is opportune to ask which animals use newly available SF and which stay restricted to OG. This study presents a comparison of SF and OG site occupancy by nocturnal birds in terra firme forests of the Amazon Guianan shield, north of Manaus, Brazil. We tested species-specific occupancy predictions for two owls ( Lophostrix cristata/Glaucidium hardyi ), two potoos ( Nyctibius leucopterus/Nyctibius griseus ) and two nightjars ( Caprimulgus nigrescens/Nyctidromus albicollis ). For each pair, we predicted that one species would have higher occupancy in OG while the other would either be indifferent to forest type or favor SF sites. Data were collected in 30 OG and 24 SF sites with monthly samples from December 2007 to December 2008. Our analytic approach accounts for the possibility of detection failure and for spatial autocorrelation in occupancy, thus leading to strong inferences about changes in occupancy between forest types and between species. Nocturnal bird richness and community composition were indistinguishable between OG and SF sites. Owls were relatively indifferent to forest type. Potoos followed the a priori predictions, and one of the nightjars ( C. nigrescens ) favored SF instead of OG as predicted. Only one species, Nyctib. leucopterus , clearly favored OG. The landscape context of our SF study sites, surrounded by a vast expanse of continuous OG forest, partially explains the resemblance between SF and OG fauna but leaves unexplained the higher occupancy for SF than OG sites for several study species. The causal explanation of high SF occupancy remains an open question, but the result itself motivates further comparisons for other groups, as well as recognition of the conservation potential of SF.     

Elasmobranch Central Nervous System Organization and Its Possible Evolutionary Significance

Examination of shark brain:body ratios reveals that these taxapossess relative brain volumes in a range overlapping thoseof bony fish as well as birds and mammals. Much of the variationis due to relative development of the telencephalon and cerebellum.Telencephalic weights vary from 24% in Squalus to 52% in Sphyrna.Analysis of the cytoarchitectonics of the shark brains revealsat least two patterns of development. Squalomorph sharks possesslow brain:body ratios, and the telencephalon of these taxa possesswell developed lateral ventricles and poorly developed pallialareas. The diencephalon is characterized by prominent periventricularlaminae, and the cerebellum lacks foliation. The lamniform andcarcharhiniform sharks are characterized by high brain: bodyratios, and there is marked hypertrophy of the telencephalon.The roof (pallial) regions, as well as the diencephalon, arecharacterized by extensive cellular migrations. The cerebellaof these forms possess extensive complex foliation. These brain patterns are compared with the brain organizationof Holocephali, and I conclude that the holocephalans are asister radiation of the elasmobranchs. Comparisons with bonyfish and land vertebrates suggest that elasmobranchs have independentlydeveloped complex pallial fields and cerebellar foliation asa result of parallel evolutionary trends.     

Some introductory notes on the organization of the forebrain in tetrapods.

As an introduction to the main theme of this conference an overview of the organization of the tetrapod forebrain is presented with emphasis on the telencephalic representation of sensory and motor functions. In all classes of tetrapods, olfactory, visual, octavolateral, somatosensory and gustatory information reaches the telencephalon. Major differences exist in the telencephalic targets of sensory information between amphibians and amniotes. In amphibians, three targets are found: the lateral pallium for olfactory input, the medial pallium for visual and multisensory input, and the lateral subpallium for visual, octavolateral and somatosensory information. The forebrains of reptiles and mammals are similar in that the dorsal surface of their cerebral hemisphere is formed by a pallium with three major segments: (a) an olfactory, lateral cortex; (b) a 'limbic' cortex that forms the dorsomedial wall of the hemisphere, and (c) an intermediate cortex that is composed entirely of isocortex in mammals, but in reptiles (and birds) consists of at least part of the dorsal cortex (in birds the Wulst) and a large intraventricular protrusion, i.e. the dorsal ventricular ridge. In birds, the entire lateral wall of the hemisphere is involved in this expansion. The intermediate pallial segment receives sensory projections from the thalamus and contains modality-specific sensory areas in reptiles, birds and mammals. The most important differences between the intermediate pallial segment of amniotes concern motor systems.     

Anatomical specializations for nocturnality in a critically endangered parrot, the Kakapo (Strigops habroptilus)

The shift from a diurnal to nocturnal lifestyle in vertebrates is generally associated with either enhanced visual sensitivity or a decreased reliance on vision. Within birds, most studies have focused on differences in the visual system across all birds with respect to nocturnality-diurnality. The critically endangered Kakapo (Strigops habroptilus), a parrot endemic to New Zealand, is an example of a species that has evolved a nocturnal lifestyle in an otherwise diurnal lineage, but nothing is known about its' visual system. Here, we provide a detailed morphological analysis of the orbits, brain, eye, and retina of the Kakapo and comparisons with other birds. Morphometric analyses revealed that the Kakapo's orbits are significantly more convergent than other parrots, suggesting an increased binocular overlap in the visual field. The Kakapo exhibits an eye shape that is consistent with other nocturnal birds, including owls and nightjars, but is also within the range of the diurnal parrots. With respect to the brain, the Kakapo has a significantly smaller optic nerve and tectofugal visual pathway. Specifically, the optic tectum, nucleus rotundus and entopallium were significantly reduced in relative size compared to other parrots. There was no apparent reduction to the thalamofugal visual pathway. Finally, the retinal morphology of the Kakapo is similar to that of both diurnal and nocturnal birds, suggesting a retina that is specialised for a crepuscular niche. Overall, this suggests that the Kakapo has enhanced light sensitivity, poor visual acuity and a larger binocular field than other parrots. We conclude that the Kakapo possesses a visual system unlike that of either strictly nocturnal or diurnal birds and therefore does not adhere to the traditional view of the evolution of nocturnality in birds.     

The hyperstriatum and nesting behaviour in the domestic hen

Bilateral ablation of the ventral hyperstriatum resulted in hens ceasing to use trap-nests which they had formerly used. The appetitive component of their pre-laying behaviour was normal in form but was not directed towards the trap-nests, as it was in control birds. In the absence of trap-nests in a pen control birds laid in corners and were conservative in choice of site but both these characteristics were abolished by these ablations. Other bilateral ablations involving the Wulst had less drastic effects on pre-laying behaviour while bilateral ablations in the posterior telencephalon had no effect on this behaviour pattern.     

The evolution of complex brains and behaviors in African cichlid fishes

In this review, I explore the effects of both social organization and the physical environment, specifically habitat complexity, on the brains and behavior of highly visual African cichlid fishes, drawing on examples from primates and birds where appropriate. In closely related fishes from the monophyletic Ectodinii clade of Lake Tanganyika, both forces influence cichlid brains and behavior. Considering social influences first, visual acuity differs with respect to social organization (monogamy versus polygyny). Both the telencephalon and amygdalar homologue, area Dm, are larger in monogamous species. Monogamous species are found to have more vasotocin-immunoreactive cells in the preoptic area of the brain. Habitat complexity also influences brain and behavior in these fishes. Total brain size, telencephalic and cerebellar size are positively correlated with habitat complexity. Visual acuity and spatial memory are enhanced in cichlids living in more complex environments. However habitat complexity and social forces affect cichlid brains differently. Taken together, our field data and plasticity data suggest that some of the species-specific neural effects of habitat complexity could be the consequence of the corresponding social correlates. Environmental forces, however, exert a broader effect on brain structures than social ones do, suggesting allometric expansion of the brain structures in concert with brain size and/or co-evolution of these structures [Current Zoology 56 (1): 144-156 2010].     

Annual cycle of the black-capped chickadee: seasonality of singing rates and vocal-control brain regions

Black-capped chickadees have a rich vocal repertoire including learned calls and the learned fee-bee song. However, the neural regions underlying these vocalizations, such as HVC, area X, and RA (robust nucleus of arcopallium), remain understudied. Here, we document seasonal changes in fee-bee song production and show a marked peak in singing rate during March through May. Despite this, we found only minimal seasonal plasticity in vocal control regions of the brain in males. There was no significant effect of time of year on the size of HVC, X, or RA in birds collected in January, April, July, and October. We then pooled birds into two groups, those with large testes (breeding condition) and those with small testes (nonbreeding), regardless of time of year. Breeding birds had slightly larger RA, but not HVC or X, than nonbreeding birds. Breeding birds had slightly larger HVC and RA, but not X, as a proportion of telencephalon volume than did nonbreeding birds. Birds collected in July had heavier brains than birds at other times of year, and had the greatest loss in brain mass during cryoprotection. The absence of any overall seasonal change in the vocal-control regions of chickadees likely results from a combination of individual differences in the timing of breeding phenology and demands on the vocal-control regions to produce learned calls year-round.     

Annual cycle of the black‐capped chickadee: Seasonality of singing rates and vocal‐control brain regions

Black‐capped chickadees have a rich vocal repertoire including learned calls and the learned fee‐bee song. However, the neural regions underlying these vocalizations, such as HVC, area X, and RA (robust nucleus of arcopallium), remain understudied. Here, we document seasonal changes in fee‐bee song production and show a marked peak in singing rate during March through May. Despite this, we found only minimal seasonal plasticity in vocal control regions of the brain in males. There was no significant effect of time of year on the size of HVC, X, or RA in birds collected in January, April, July, and October. We then pooled birds into two groups, those with large testes (breeding condition) and those with small testes (nonbreeding), regardless of time of year. Breeding birds had slightly larger RA, but not HVC or X, than nonbreeding birds. Breeding birds had slightly larger HVC and RA, but not X, as a proportion of telencephalon volume than did nonbreeding birds. Birds collected in July had heavier brains than birds at other times of year, and had the greatest loss in brain mass during cryoprotection. The absence of any overall seasonal change in the vocal‐control regions of chickadees likely results from a combination of individual differences in the timing of breeding phenology and demands on the vocal‐control regions to produce learned calls year‐round. © 2006 Wiley Periodicals, Inc. J Neurobiol, 2006     

Higher-level phylogeny of trogoniformes

Phylogenetic relationships between Trogoniformes and several other putative closely related groups of birds, based on complete cytochrome b and nearly complete 12S ribosomal RNA sequences, were studied. The taxa included trogons, owls, cuckoos, parrots, nightjars, hummingbirds, kingfishers, motmots, rollers, mousebirds, and woodpeckers. The group most commonly suggested as the nearest relative to trogons had been the coraciiforms (kingfishers, rollers, and allies) but this hypothesis was not supported. It appeared that Trogons are more closely related to mousebirds, parrots, and perhaps cuckoos than to coraciiforms. Conflicting results, however, prevented precise determination of higher-level phylogenetic affinities of trogons. A saturation analysis showed evident saturation in cytochrome b third positions and 12S loops. After saturated partitions were removed, the phylogeny supported the mousebirds (Coliiformes) as the sister taxon to trogons. Phylogenetic inconsistencies appeared to be attributable to an imbalance between the lengths of terminal and internodal branches. Apparently, the limited number of characters supporting internodal branches exemplifies a relatively rapid cladogenesis at an early period in the evolutionary history of these birds.     

Arginine vasotocin neuronal phenotypes, telencephalic fiber varicosities, and social behavior in butterflyfishes (Chaetodontidae): potential similarities to birds and mammals

The neuropeptide arginine vasopressin (AVP) influences many social behaviors through its action in the forebrain of mammals. However, the function of the homologous arginine vasotocin (AVT) in the forebrain of fishes, specifically the telencephalon remains unresolved. We tested whether the density of AVT-immunoreactive (-ir) fiber varicosities, somata size or number of AVT-ir neuronal phenotypes within the forebrain were predictive of social behavior in reproductive males of seven species of butterflyfishes (family Chaetodontidae) in four phylogenetic clades. Similar to other fishes, the aggressive (often territorial) species in most cases had larger AVT-ir cells within the gigantocellular preoptic cell group. Linear discriminant function analyses demonstrated that the density of AVT-ir varicosities within homologous telencephalic nuclei to those important for social behavior in mammals and birds were predictive of aggressive behavior, social affiliations, and mating system. Of note, the density of AVT-ir varicosities within the ventral nucleus of the ventral telencephalon, thought to be homologous to the septum of other vertebrates, was the strongest predictor of aggressive behavior, social affiliation, and mating system. These results are consistent with the postulate that AVT within the telencephalon of fishes plays an important role in social behavior and may function in a similar manner to that of AVT / AVP in birds and mammals despite having cell populations solely within the preoptic area.     

An additional bone in the sclera of the eyes of owls and the common potoo (Nictibius griseus) and its role in the contraction of the nictitating membrane

Morphometric, anatomical and histological examinations were made in 10 species of owls of the families Tytonidae and Strigidae and compared with the eyes of other species of nocturnal birds including common potoo (Nictibiidae) and three species of nightjars (Caprimulgidae) and two diurnal species: the roadside hawk (Accipitridae) and the domestic duck (Anatidae). In owls and the common potoo the nictitating membrane is situated on the dorsal edge of the eye. In these birds, the scleral ring bears an additional, previously undescribed bone of various forms and dimensions (1.4-6.8 mm of length and 0.8-3.3 mm of width), located on the trajectory of the tendon of the pyramidal muscle which is attached to the nictitating membrane. This bone has a groove that encloses the tendon of the pyramidal muscle, preventing it from separating from the sclera during contraction, as well as diverting the trajectory of the tendon to impede it from projecting itself over the cornea. In the ferruginous pygmy owl, Nacunda nighthawk, Pauraque, scissor-tailed nightjar, roadside hawk and domestic duck the additional bone was not seen. Based on the morphofunctional characteristics of the bone, we suggest that this bone should be named the scleral sesamoid bone.     

Is Cooperative Breeding Associated With Bigger Brains? A Comparative Test in the Corvida (Passeriformes)

The cognitive demands of a social existence favour the evolution of relatively large brains and neocortices in primates. Comparable tests of sociality and brain size/structure in birds have not been performed, despite marked similarities in the social systems of birds and mammals. Here, we test whether one aspect of avian sociality, cooperative breeding, is associated with an increase in brain size across 155 species of the passeriform parvorder Corvida. Using conventional and phylogeny‐corrected statistics, we examined the correlated evolution of relative brain size and: the presence/absence of cooperative breeding, percentage of nests that are cooperative and cooperatively breeding group size. Most of the comparisons yielded non‐significant results, which suggests that cooperative breeding is not related to relative brain size in this parvorder. There are a number of potential explanations for our findings. First, changes in brain region size may be correlated with cooperative breeding without affecting overall brain size. Secondly, cooperatively breeding birds might not possess more complex social behaviour than non‐cooperatively breeding birds. Thirdly, relatively large brains might be ancestral in this parvorder. This may predispose them to evolve the range of complex behaviours found in this group, including extreme sociality. Finally, ecological and/or developmental factors might play a more significant role than social behaviour in the diversification of avian brain size. Assessing these alternatives requires more information on the neural and cognitive differences between bird species.     

ORDINAL AFFINITIES OF THE AEGIALORNITHIDAE

The Aegialornithidae of the Eocene-Oligocene, previously regarded as swifts, have been transferred by Brodkorb (1971) to the nightjar order Caprimulgiformes. The fossil forelimb bones representing this early family have now been compared with those of recent species of the true swifts and tree swifts (Apodi in Apodiformes) and with nightjars, Oilbirds and frogmouths (Caprimulgiformes). The corresponding bones in swifts differ consistently from those of nightjars in the greater development of various prominences for muscle attachment. In all critical characters the fossil bones resemble those of swifts, and it is concluded that the Aegialornithidae should be reinstated as a family of the Apodiformes.