Adaptations of the hoatzin (Opisthocomus hoazin) to leaf-eating. Morphological characteristics and functional features of its bill and hyoid apparatus

The hoatzin remains one of the most enigmatic birds. A morphofunctional analysis of its bill and hyoid apparatus throws new light on its feeding adaptation as well as on its systematic relationships. Bony and muscular skull, rhamphotheca, palate, and hyoid apparatus were described in details. Though keeping into the general organisation pattern found among Neognathae (except Galliformes), bill and hyoid apparatus of the hoatzin displays a series of species-specific features, some unique among birds. This species appears particularly well adapted to tear of leaves and process them inside the bill before ingestion. Because of very important anatomical and thence functional differences in bill and hyoid structure, any close relationship between the hoatzin and Galliformes cannot be envisioned. Such a hypothesis would implicate a counter-selective evolutionary reversion.     

Morphofunctional analysis and trophic adaptations: the case of bill apparatus of Old World flycatchers

A morphofunctional analysis of the bill apparatus was conducted on some African forest flycatchers (Muscicapidae, Platysteiridae, Monarchidae) in relation to detailed eco-ethological data available on these species. The aim was to evaluate relationships between anatomical structures and habitat constraints and also identify the most pertinent trophic adaptations. If forest Muscicapidae have essentially conserved the generalized passerine structures and occupy open-habitat niches in the forest, Platysteiridae and Monarchidae have adapted to forest conditions and show a key-adaptation based on specific changes in the structure of the bill apparatus in response to particular light patterns and habitat clogginess, constraints that require speed and precision for the capture of prey and protection of the skull against collisions.     

Phylogenetic relationships of turacos (Musophagidae; Cuculiformes) based on comparative chromosome banding analysis

Cladistic analysis of chromosome banding patterns in nine species of turacos (Musophagidae; Cuculiformes) revealed the existence of two clades, one comprised of species of the genera Tauraco, Gallirex (= Tauraco ) and Musophaga , and another of species of Corythaixoides. The results are consistent with the allocation of the former to a subfamily Tauracinae and the allocation of the latter to the subfamily Criniferinae which also includes Crinifer. Comparative C-banding suggests that the putatively polytypic Tauraco corythaix is occupied by more than one species; more such studies in this group may resolve other questionable cases of conspecificity. Comparison of our results to studies of Cuculidae suggest that they do not share with musophagids two major derived fissions that set musophagids apart from other avian orders. Detailed comparison of ancestral karyotypes from several groups (Galliformes, Cuculidae, Musophagidae and Opisthocomidae) may help to resolve their still unresolved phylogenetic relationships.
Our results confirm previous studies showing karyotypic uniformity within avian orders. The uniformity suggests a negligible role for chromosome rearrangement in speciation in this group, since several indisputably distinct species do not differ karyotypically in any significant fashion. Intraspecific uniformity is punctuated by the presence in Livingstone's turaco Tauraco corythaix livingstonii of inversion heteromorphism, the class of rearrangement encountered most frequently in other avian species.     

Morphofunctional study of the bill and hyoid apparatus of Momotus momota (Aves, Coraciiformes, Momotidae): implications for omnivorous feeding adaptation in motmots

The present study contrasts available biological data and results of morphofunctional analyses of the bill and hyoid apparatus in motmots. It shows that these omnivorous birds, which take relatively large food items, possess osteomuscular peculiarities that enable them to process these items as a whole in order to soften or cut them, and make them suited for easy ingestion. For that, they use the crenate edges of their rhamphotheca. Their jaws work as a highly mobile saw-like system. Their mutual movements, enhanced by the fact that particular dispositions of the hyoid apparatus rise the tongue and the supported items high up into buccal cavity, facilitate an effective clamping of items that can be moved along the jaws and be quite appropriately processed.     

Bill and hyoid apparatus of pigeons (Columbidae) and sandgrouse (Pteroclididae): a common adaptation to vegetarian feeding?

For the present study, 15 species of pigeons representing the 5 sub-families usually recognized, and 3 species of sandgrouse were examined. The skeleton and musculature of the bill and hyoid apparatus are described. Morpho-functional analyses show that from a key adaptation to the removal and deglutition (without processing) of attached plant items, pigeons would have followed two pathways, one based on the joint muscular control of the movement of the jaws (Columbinae, Treroninae, Gourinae), the other on the separate muscular control (Didunculinae, Otidiphabinae). Sandgrouse would have diverged from this latter, developing the ability to very selectively remove attached plant items as well as to peck particularly small seeds on the ground. Unexpected differences appeared between sandgrouse species which raise eco-ethological problems.     

The Long and the Short of It: No Dietary Specialisation between Male and Female Western Sandpipers Despite Strong Bill Size Dimorphism

Many bird species show spatial or habitat segregation of the sexes during the non-breeding season. One potential ecological explanation is that differences in bill morphology favour foraging niche specialisation and segregation. Western sandpipers Calidris mauri have pronounced bill size dimorphism, with female bills averaging 15% longer than those of males. The sexes differ in foraging behaviour and exhibit partial latitudinal segregation during the non-breeding season, with males predominant in the north and females in the south. Niche specialisation at a local scale might account for this broad geographic pattern, and we investigated whether longer-billed females and shorter-billed males occupy different foraging niches at 16 sites across the non-breeding range. We used stable-nitrogen (δ¹⁵N) isotope analysis of whole blood to test for dietary specialisation according to bill length and sex. Stable-nitrogen isotope ratios increase with trophic level. We predicted that δ¹⁵N values would increase with bill length and would be higher for females, which use a greater proportion of foraging behaviour that targets higher-trophic level prey. We used stable-carbon (δ¹³C) isotope analysis to test for habitat segregation according to bill length and sex. Stable-carbon isotope ratios vary between marine- and freshwater-influenced habitats. We predicted that δ¹³C values would differ between males and females if the sexes segregate between habitat types. Using a model selection approach, we found little support for a relationship between δ¹⁵N and either bill length or sex. There was some indication, however, that more marine δ¹³C values occur with shorter bill lengths. Our findings provide little evidence that male and female western sandpipers exhibit dietary specialisation as a function of their bill size, but indicate that the sexes may segregate in different habitats according to bill length at some non-breeding sites. Potential ecological factors underlying habitat segregation between sexes include differences in preferred habitat type and predation risk.     

Effects of thyroid hormone level alterations on the Weberian apparatus ontogeny of cyprinids (Cyprinidae; Teleostei)

Effects of thyroid hormone (TH) level alterations on the development and definitive morphology of the Weberian apparatus (WA, morphofunctional complex, providing transmission of sound signals from the gas bladder to the labyrinth of inner ear) were experimentally assessed in cyprinid fishes (Labeobarbus intermedius and Danio rerio). Alterations of TH-level were shown to lead to heterochronies, changes of timing and rates of ontogenetic events resulting in changes of definitive morphology of some structures as well as of the WA as a whole. Differences in reaction of WA structures to the TH-level alterations, and inter- and intraspecific variability of TH-responsiveness were revealed.     

Short-term exposure to testosterone propionate leads to rapid bill color and dominance changes in zebra finches

Testosterone (T) can influence both male-male competition and mate choice displays. In zebra finches, female mate choice is based in part on bill color, and bill color has been shown to be enhanced by long-term testosterone supplementation. However, it is not clear whether bill color plays a role in male-male interactions and how bill color responds to shorter-term changes in T. We tested whether a single injection of testosterone propionate (TP) would influence male-male dominance interactions and lead to rapid (over a three-day period) changes in bill color. In addition, we tested whether bill color predicted aggression and dominance. We allowed birds in triads to establish hierarchies and then injected either dominant or subordinate individuals with TP, in addition to establishing sham control triads. We found that red chroma, but not hue, predicted aggressiveness of males. Exposure to TP led both dominant and subordinate birds to increase dominance scores over three days, longer than the < 24 h period in which injected TP stays active. In addition, exposure to TP increased red chroma and hue in three days showing the dynamic nature of allocation of pigments to the bill. Our results suggest that zebra finches can modulate T and bill color levels over short time periods and these changes may occur through positive feedback between T-levels and dominance.     

Specific changes in the sodium chloride intake and activity of the taste receptor apparatus of rats administered the peptide litorin and its albumin conjugate

The role of bombesin-like peptide litorin in control of salt consumption was studied in rats. The influence of exogenous injection and binding of the endogenous litorin in the organism on the consumption of sodium chloride and sucrose solutions was analyzed in deprived rats in the process of 15-min. testing. It was found that intraperitoneal injection of 10(-6) - 10(-5) M of litorin led to an increase, and rats immunization by peptide conjugate with ox serum albumin--to a decrease of the consumption of salt solution, without changing the consumption of sucrose solution. Titres of antibodies to litorin in the plasma of rats immunized with the conjugate were higher than in the control. Intraperitoneal, subcutaneous or intranasal injections of 10(-5) M of litorin led to selective increase of gustatory responses (recorded from the chorda tympani) to tongue stimulation by salt and acid solutions not influencing the responses to quinine and sucrose in anesthetized rats. The study shows, that the peptide litorin selectively participates in the control of sodium chloride consumption. In the process of such control the increase of taste apparatus sensitivity to the sodium chloride is probably involved.     

Functional and evolutionary consequences of cranial fenestration in birds

Ostrich‐like birds (Palaeognathae) show very little taxonomic diversity while their sister taxon (Neognathae) contains roughly 10,000 species. The main anatomical differences between the two taxa are in the crania. Palaeognaths lack an element in the bill called the lateral bar that is present in both ancestral theropods and modern neognaths, and have thin zones in the bones of the bill, and robust bony elements on the ventral surface of their crania. Here we use a combination of modeling and developmental experiments to investigate the processes that might have led to these differences. Engineering‐based finite element analyses indicate that removing the lateral bars from a neognath increases mechanical stress in the upper bill and the ventral elements of the skull, regions that are either more robust or more flexible in palaeognaths. Surgically removing the lateral bar from neognath hatchlings led to similar changes. These results indicate that the lateral bar is load‐bearing and suggest that this function was transferred to other bony elements when it was lost in palaeognaths. It is possible that the loss of the load‐bearing lateral bar might have constrained diversification of skull morphology in palaeognaths and thus limited taxonomic diversity within the group.     

Avoiding Competition: the Ecological History of Late Cenozoic Metatherian Carnivores in South America

The ecological interaction between small and medium sized South American metatherian carnivores, from the Miocene to Recent, has been analyzed with the objective to understand the ecological interactions between the Hathliacynidae (Sparassodonta) and some Didelphoidea (Didelphimorphia). The species richness through time for these two groups, along with the body mass, diet, and several morphofunctional variables has been analyzed here. The results show a double-wedge geometry of the diversity curve. The climax of the Hathliacynidae took place during the Santacrucian mammal-age with a subsequent decline, in the species richness of this family, followed by the extinction of the family at the Barrancalobian subage. Carnivorous Didelphoidea show a first maximum species richness during the Chapadmalalan followed by a decline and a new rise during Recent times. The coexistence of these mentioned groups took place from the Chasicoan to the Chapadmalalan mammal-ages covering a time span of around 6,000,000 years. The multivariate and univariate analyses of morphofunctional variables suggest a restriction of the Hathliacynidae to hypercarnivory while the Didelphoidea occupied the niche of meso- and hypocarnivory. The body mass analyses show some overlap in small sizes but it is not correlated with any superposition in the morphospace of functional variables. In summary, any passive replacement or active displacement between the Hathliacynidae and carnivorous Didelphoidea are supported by the fossil record. In turn, a partition of the metatherian carnivorous guild seems to have occurred through to the Neogene. The extinction of the Hathliacynidae seems to be a result of environmental change.     

Partition of aminoacyl-tRNA synthetases in two different structural classes dating back to early metabolism: Implications for the origin of the genetic code and the nature of protein sequences

We describe, on the molecular level, a possible fuzzy and primordial translation apparatus capable of synthesizing polypeptides from nucleic acids in a world containing a mixture of coevolving molecules of RNA and proteins already arranged in metabolic cycles (including cofactors). Close attention is paid to template-free systems because they are believed to be the immediate ancestors of this primordial translation apparatus. The two classes of amnoacyl-tRNA synthetases (aaRSs), as seen today, are considered as the remnants of such a simple imprecise translation apparatus and are used as guidelines for the construction of the model. Earlier theoretical work by Bedian on a related system is invoked to show how specificity and stability could have been achieved automatically and rather quickly, starting from such an imprecise system, i.e., how the encoded synthesis of proteins could have appeared. Because of the binary nature of the underlying proto-code, the first genetically encoded proteins would then have been alternating copolymers with a high degree of degeneracy, but not random. Indeed, a clear signal for alternating hydrophobic and hydrophilic residues in present-day protein sequences can be detected. Later evolution of the genetic code would have proceeded along lines already discussed by Crick. However, in the initial stages, the translation apparatus proposed here is in fact very similar to the one postulated by Woese, only here it is given a molecular framework. This hypothesis departs from the paradigm of the RNA world in that it supposes that the origin of the genetic code occurred after the apparition of some functional (statistical) proteins first. Implications for protein design are also discussed.     

Distinctive morphofunctional features of the bill and hyoid apparatus of turacos (Aves, Musophagidae): relations with frugivory]

The present study points to morpho-anatomical features that allow vegetarian but mainly frugivorous turacos to fill at best their specific feeding requirements. Mechanisms are analysed which the bird can use to detach a fruit and avoid it rolls out of the bill. It is also examined how vegetable items can be processed particularly when they have to be cut, and what can facilitate their ingestion particularly when they are fruits that have to be swallowed entirely and are large and/or have dry or fibrous skin or flesh. The skeletal and muscular anatomy of the bill and hyoid apparatus is described in details and illustrated. The particularly short and stout bill coupled with a relatively simple system of aponevroses of the adductors reflects a trade-off between two important jaw functional requirements: huge efforts for clamping, and a wide opening for plucking, processing and swallowing relatively large fruit. The clearly oblique orientation of the modified outer adductor seems an adaptation to the detachment of fruits. The os uncinatum, particularly developed in this bird family, is interpreted as maintaining transversal stability, particularly when jaws act as a pair of scissors. Most food items being processed near the base of the bill, mechanisms have been developed which contribute to overcome the risk of breakage at the level of the prokinetic hinge because of a vertically oriented force there.     

Sesamoids and Morphological Variation: a Hypothesis on the Origin of Rod-like Skeletal Elements in Aerial Mammals

Enigmatic rod-like skeletal structures that support compliant membranes (patagia) in aerial mammals have been often considered as neomorphic elements or as evolutionary novelties, and their origin has remained poorly understood. A potential source of skeletal plasticity and, probably, of morphofunctional innovations are sesamoids, which were recently demonstrated to have a common cellular origin with bone eminences. In this review, I compile information regarding anatomy, evolution, and development of rod-like skeletal elements in extant gliding and flying mammals and propose a working hypothesis on the origin of these structures. Rod-like skeletal elements, namely, the calcar in bats (Chiroptera), the unciform element in Anomaluridae (Rodentia), and the styliform cartilage in Pteromyini (Rodentia: Sciuridae), would derive from sesamoids, which, in turn, would have the same origin as eminences of long bones (or bones with a long-bone-like growth), i.e., calcaneus, ulna, and pisiform, respectively. Rod-like skeletal elements exhibit several features of sesamoids. However, further developmental data are needed to confirm this hypothesis, particularly whether these structures share a cellular origin and molecular developmental pathways with sesamoids and bone eminences. If this hypothesis were supported, a new role for sesamoids in generating morphofunctional innovations in mammals and, potentially, in other aerial amniotes, would be recognized. Rod-like skeletal elements, which are key in the evolution of aerial locomotion, might constitute an example of pre-existing traits that acquire novel functions through relatively little developmental plasticity.

     

Study of axodendritic synapses of the hippocampal CA3 field in experimental uremia and administration of exogenous parathyroid hormone]

The effect of parathyroid hormone intraperitoneal injection at different stages of experimental uremia induced by subtotal nephrectomy on ultrastructural morphofunctional characteristics of hippocampus Ca3 field axospinal synapses was studied. A conclusion is made that the decrease of synaptic activity in the hippocampus field due to redistribution of calcium ions between spine cytoplasm and spine apparatus may take place after PTH injection and during uremia development.     

On the structural adaptations of the bill, skull-elements, tongue, and hyoid of some Indian insect-eating birds

The study of the functional morphology of the feeding apparatus of some Indian insect-eating birds reveals suitable adaptational changes in the structure of their bill, skull-elements, tongue, and byoid in different degrees, depending on the nature of their partial adaptation to secondary food-habits. The hooked tip of the upper beak in Muscicapa and Dicrurus, sharp tomial edges of both the beaks in Turdoides and the long, gradually curved bill in Merops are some of the suitable adaptations of the bill for food-getting. The dimensional variations of the skull and its kinetic elements may be correlated not only with the food-habits of birds studied, but also with the patterns of jaw and tongue muscles possessed by them. A comparatively greater width of the cranium and height of the lower jaw in Turdoides and Dicrurus provide wider areas for the origins and insertions of the adductor muscles. The skull in all the birds studied is pro-kinetic. The kinesis of the upper jaw, however, depends on several factors of which the angles of placement of the quadrate-pterygoid-palatine components, the nature of the naso-frontal hinge and the resultant "torques" produced by differential forces of muscles are very significant. The upper jaw kinesis is best developed in Merops and Orthotomus. The variations in the structure of the tongue and hyoid may also be correlated with various movements of the tongue in both primary and secondary food-adaptations.     

Vision, touch and object manipulation in Senegal parrots Poicephalus senegalus

Parrots are exceptional among birds for their high levels of exploratory behaviour and manipulatory abilities. It has been argued that foraging method is the prime determinant of a bird's visual field configuration. However, here we argue that the topography of visual fields in parrots is related to their playful dexterity, unique anatomy and particularly the tactile information that is gained through their bill tip organ during object manipulation. We measured the visual fields of Senegal parrots Poicephalus senegalus using the ophthalmoscopic reflex technique and also report some preliminary observations on the bill tip organ in this species. We found that the visual fields of Senegal parrots are unlike those described hitherto in any other bird species, with both a relatively broad frontal binocular field and a near comprehensive field of view around the head. The behavioural implications are discussed and we consider how extractive foraging and object exploration, mediated in part by tactile cues from the bill, has led to the absence of visual coverage of the region below the bill in favour of more comprehensive visual coverage above the head.     

Similarities between the faces of parents and offspring in Bewick's swan and the differences between mates

The faces of individual Bewick's swans ( Cygnus columbianus bewickii ) are highly distinctive. Similarities between the faces of parents and their offspring in 12 families living in the wild were examined using a code that gave a value to 29 features of each individual's face. The similarities between the faces of 22 wild–living mated pairs were also analyzed. The offspring resembled both their parents more closely than would have been expected on a chance basis. The similarities were particularly striking in the upper part of the bill. Mates, on the other hand, did not resemble each other and analysis of each character suggested that in some respects, they were less like each other than would have been expected on a chance basis. It is concluded that the facial appearance of Bewick's swans is inherited and that the swans may actively outbreed.     

Differences in foraging ecology determine variation in visual fields in ibises and spoonbills (Threskiornithidae)

Variations in visual field topography among birds have been interpreted as adaptations to the specific perceptual challenges posed by the species’ foraging ecology. To test this hypothesis we determined visual field topography in four bird species which have different foraging ecologies but are from the same family: Puna Ibis Plegadis ridgwayi (probes for prey in the soft substrates of marsh habitats), Northern Bald Ibis Geronticus eremita (surface pecks for prey in dry terrestrial habitats), African Spoonbill Platalea alba and Eurasian Spoonbill Platalea leucorodia (bill‐sweeps for prey in shallow turbid waters). All four species employ tactile cues provided by bill‐tip organs for prey detection. We predicted that the visual fields of these species would show general features similar to those found in other birds whose foraging is guided by tactile cues from the bill (i.e. bill falling outside the frontal binocular field and comprehensive visual coverage of the celestial hemisphere). However, the visual fields of all four species showed general features characteristic of birds that take food directly in the bill under visual guidance (i.e. a narrow and vertically long binocular field in which the projection of the bill tip is approximately central and with a blind area above and behind the head). Visual fields of the two spoonbills were very similar but differed from those of the ibises, which also differed between themselves. In the spoonbills, there was a blind area below the bill produced by the enlarged spatulate bill tip. We discuss how these differences in visual fields are related to the perceptual challenges of these birds’ different foraging ecologies, including the detection, identification and ingestion of prey. In particular we suggest that all species need to see binocularly around the bill and between the opened mandibles for the identification of caught prey items and its transport to the back of the mouth. Our findings support the hypothesis that sensory challenges associated with differences in foraging ecology, rather than shared ancestry or the control of locomotion, are the main determinants of variation in visual field topography in birds.     

Relations between the ectosomatic and the entosomatic organs

A.N. Severtsov, when introduced the concepts of ecto- and entosomatic organs, illustrated them by three examples of adaptations, namely by the blindness of some subterranean vertebrates, by the "suckers" on the geckos' fingers and toes, and by the flattened body shape of skates and rays. Morphology of the pterygoideus muscle in some song-birds, which is one of the most complicated jaw muscles, is considered here in the framework of those concepts. This muscle displays mosaic variation among bird taxa while the arrangement of skeletal and ligamentous components is rather monotonous. The ventromedial portion of the muscle predominates in the Vietnamese babblers (Garrulax leucolophus, Alcippe peracensis, and Yuhina zantholeuca; fam. Timaliidae), in the leafbird Aegithina lafresnayei (fam. Chloropsidae), and in the drongo Dicrurus aeneus (fam. Dicruridae). One part of this portion, m. retractor palatini, is relatively big in the starling, Gracula religiosa (fam. Sturnidae), and in the dipper, Cinclus cinclus (fam. Trogloditidae). Both muscular bulks (entosomatic organs after Severtsov) affect clearly and directly properties of the bill (ectosomatic organ) without any visible differences in its construction. They provide the upper jaw with additional force (directed downward while grasping a prey) and so fasten it against the passive deviation during tearing or pulling off the food item (the mandible does not accept those forces). These two versions of the muscle morphology are parallel in the functional sense and are independent in respect to their evolutionary origin. The ventromedial portion, judging by its attachment to the mandible close to the center of the quadrato-mandibular joint, is neutral in respect to its adduction, and the m. retractor palatini is not connected to it. Thus, muscular portions under consideration, in spite of their position deep in the feeding apparatus, behave as ectosomatic organs. Deviations in their morphology are not the answer to any antecedent modification of the bill shape or of arrangement of the skeleto-ligamentous apparatus components. Instead, they appear to be primary results due to immediate action of the natural selection to provide a direct functional effects.