Postnatal ontogeny, population structure, and extinction of the giant moa Dinornis

Recent reinterpretation of the giant moa Dinornis as consisting of two sexually dimorphic allospecies permits thorough site-by-site investigation of the ontogeny and population biology of this genus. Analysis of subadult skeletal material from natural swamp sites in the North and South Islands of New Zealand forms the basis for recognition of growth series for each long bone element, characterized by sequential formation of fossulae in the femur and fusion of bones in the tibiotarsus and tarsometatarsus. Femora reached progressive developmental stages more rapidly than the other long bones, but all three elements reached maturity at about the same time. Patterns of bone fusion in Dinornis are more similar to those in Apteryx than in Struthio, and kiwi are recognized as a suitable developmental analog for interpreting moa ontogeny. Samples from Bell Hill Vineyard Swamp (South Island) and Makirikiri swamp (North Island) are interpreted as representing autochthonous moa populations; comparison with stages of kiwi long bone development suggests that Dinornis at these sites had high adult survivorship in strongly K-selected populations, with 72.5-87.3% of individuals having achieved adult body mass, and 55.9-78.2% being sexually mature. The pattern of low fecundity and probable high longevity in both Dinornis species suggests that populations were vulnerable to loss of adults, primarily through hunting, rather than as a result of habitat destruction.     

Mathematical modeling of appendicular bone growth in glaucous‐winged gulls

Development of locomotor activity is crucial in tetrapods. In birds, this development leads to different functions for hindlimbs and forelimbs. The emergence of walking and flying as very different complex behavior patterns only weeks after hatching provides an interesting case study in animal development. We measured the diaphyseal lengths and midshaft diameters of three wing bones (humerus, ulna, and carpometacarpus) and three leg bones (femur, tibiotarsus, and tarsometatarsus) of 79 juvenile (ages 0–42 days) and 13 adult glaucous‐winged gulls (Larus glaucescens), a semiprecocial species. From a suite of nine alternative mathematical models, we used information‐theoretic criteria to determine the best model(s) for length and diameter of each bone as a function of age; that is, we determined the model(s) that obtained the best tradeoff between the minimized sum of squared residuals and the number of parameters used to fit the model. The Janoschek and Holling III models best described bone growth, with at least one of these models yielding an R² ≥ 0.94 for every dimension except tarsometatarsus diameter (R² = 0.87). We used the best growth models to construct accurate allometric comparisons of the bones. Early maximal absolute growth rates characterize the humerus, femur, and tarsometatarsus, bones that assume adult‐type support functions relatively early during juvenile development. Leg bone lengths exhibit more rapid but less sustained relative growth than wing bone lengths. Wing bone diameters are initially smaller than leg bone diameters, although this relationship is reversed by fledging. Wing bones and the femur approach adult length by fledging but continue to increase in diameter past fledging; the tibiotarsus and tarsometatarsus approach both adult length and diameter by fledging. In short, the pattern of bone growth in this semiprecocial species reflects the changing behavioral needs of the developing organism. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

中国中生代鸟类后肢骨骼的长度比例特征及栖息习性的分析

通过对18目59科137例现生不同栖息习性鸟类的后肢3块骨骼(股骨、胫跗骨和跗跖骨)长度比例的观察和特征分析,推断出鸟类的栖息习性与后肢3块骨骼中各骨骼长度所占总长度的比例存在密切的关系。即在所有鸟类的后肢骨骼中,胫跗骨的长度占3块骨骼的比例为最大;地栖鸟类后肢骨骼中股骨的长度要短于跗跖骨;树栖鸟类后肢骨骼中股骨的长度要长于跗跖骨。鸟类后肢3块骨骼的长度比例特征是鸟类长期对栖息等行为适应的结果。在此基础上,对中国中生代14例鸟类的栖息习性进行了分析,利用三元投影的统计方法,并以国内外新生代(古近纪和新近纪)21例鸟类标本作为对比参考,得出辽西中生代不同类型鸟类的栖息行为特征:基干鸟类以树栖为主要习性,其中个别鸟类还具有攀援的习性,而反鸟类则是典型的树栖鸟类,今鸟类兼有树、地栖的习性。研究表明,在现行的鸟类系统发育框架下,树栖适应(及攀援)代表了鸟类演化历史中最原始的生活方式。这一结论也支持鸟类飞行的树栖起源假说。中生代鸟类栖息习性分异的多样性反映了早期鸟类演化过程中自身以及与其他同期生物在生态空间和食物资源的竞争的加剧和对环境的不断适应。     

Primate limb bones and locomotor types in arboreal or terrestrial environments

Postcranial limb bones were compared among primates of different locomotor types. Seventy-one primate species, in which all families of primates were included, were grouped into nine locomotor types. Osteometrical data on long bones and data on the cross-sectional geometry of the humerus and the femur were studied by means of allometric analysis and principal component analysis. Relatively robust forelimb bones were observed in the primate group which adopted the relatively terrestrial locomotor type compared with the group that adopted the arboreal locomotor type. The difference resembled the previously reported comparison between terrestrial and arboreal groups among all quadrupedal mammals. The degree of arboreality in daily life is connected with the degree of hindlimb dominance, or the ratio of force applied to the fore- and hindlimb in positional behaviour and also with the shape, size and robusticity of limb bones.     

Allometry of the leg bones of moas (Dinornithes) and other birds

The body masses of various moas have been estimated, measurements have been made of their leg bones and allometric equations have been calculated. Corresponding equations have been calculated for various groups of living birds, using new data and data from the literature. The two families of moas are compared with each other, with modern ratites and with flying birds. Shortening of the tarsometatarsus in moas and narrowing of the pelvis in other ratites are interpreted as adaptations concerned with balancing the bird on its feet. following reduction of the wings.     

Microstructure and Cross-Sectional Shape of Limb Bones in Great Horned Owls and Red-Tailed Hawks: How Do These Features Relate to Differences in Flight and Hunting Behavior?

The Red-tailed Hawk and Great Horned Owl are two species of raptor that are similar in body size, diet, and habitat. Both species use their hindlimbs during hunting, but differ in foot morphology, how they approach and immobilize prey, and the average size of prey captured. They also differ in primary flight style: the Red-tailed Hawk uses static soaring and the Great Horned Owl uses flap-gliding. The objectives of this study were to characterize the microstructure and cross-sectional shape of limb bones of these species and examine the relationship with flight and hunting behaviors. The mid-shaft of six limb bones from six individuals of each species was sampled. The degree of bone laminarity (proportion of circular primary vascular canals) and cross-sectional geometric parameters were calculated. In both species, the humerus and femur exhibited features that suggest high resistance to torsional loading, whereas the tibiotarsus and phalanges had a shape more likely to resist compression and bending in a specific plane. The femur of the Red-tailed Hawk exhibited higher laminarity and larger polar moment of area than that of the Great Horned Owl. The tibiotarsus was more elliptical than that of the Great Horned Owl. The hawk approaches prey from a more horizontal axis, takes prey of greater mass, and is more likely to pursue prey on the ground, which could potentially be causing more torsional loads on the femur and bending loads on the tibiotarsus. In addition, differences in polar moment of area of the phalanges between the species could relate to differences in foot morphology or digit length. The humerus and ulna of the flap-gliding Great Horned Owl are more elliptical than the static soaring Red-tailed Hawk, a shape that may better resist the bending loads associated with a larger amount of flapping.     

Sagittal long bone curvature in birds

The maximum sagittal curvature of the long bones (humeras, radius, ulna, femur, tibiotarsus and tarsometatarsus) of 45 specimens of birds, belonging to 36 species, was measured and regressed to the corresponding body mass. Mathematical results show a tendency of curvature to scale with strong positive allometry. Within the species studied, those with more characteristic flapping flight tend to show relatively low values of curvature in the wing bones. To check the agreement of the present results with current hypotheses on the origin of long bone curvature, previous results on scaling of myological and cross-sectional parameters in birds are considered. Indirect evidence suggests that curvature tends to increase bone stresses. Hypotheses that consider curvature as a consequence of the mechanical action of muscle allocation and optimization of functional strains are discussed at length. The possible double genetic-epigenetic determinism of the curvature character is evoked.     

A new genus of crane (Aves: Gruiformes) from the Late Tertiary of the Balearic Islands, Western Mediterranean

A new genus and species of crane is described from Late Tertiary karstic deposits in Punta Nati-Cala's Pous, in the north-west of Menorca. The coracoid, the ends of the distal and proximal tibiotarsus, the proximal and distal ends of the tarsometatarsus (the latter is not well preserved) and the femur have been recovered, in what is one of the best osteological series of a crane pre-dating the Pleistocene. The morphology of the fossil is mainly coincident with the Gruinae, especially with recent Grus . However, its size and some symplesiomorphic features of the distal end of the tibiotarsus and of the coracoid are coincident with Balearica , and automorphic characters are also found mainly in the proximal end of the tibiotarsus. The combination of characters justifies the creation of a new genus that is considered basal in the Gruinae.     

Periosteal bone growth rates in extant ratites (ostriche and emu). Implications for assessing growth in dinosaurs

The first quantitative experimental data on growth dynamics of the primary cortical bone of young ratites demonstrate the following. 1) From hatching to 2 months of age, cortical thickness remains constant, thereby expressing equilibrium between periosteal bone deposition and an endosteal bone resorption. 2) Radial growth rates of the diaphyseal bone cortex are high (10-40 microns.day-1 on average--maximum 80 microns.day-1) in the hindlimb (femur, tibiotarsus and tarsometatarsus). Wing bones are smaller and later developed. They have lower rates of radial osteogenesis (2-14 microns.day-1). 3) High growth rates are linked to densely vascularized primary bone belonging to the reticular or laminar tissue types. Growth rates fall when bone vascular density decreases. These results emphasize the importance of examining a large number of skeletal elements in order to build a precise knowledge of the general relationship between bone growth rate and bone tissue type. They also stress the potential of bone growth rate quantification among extinct tetrapods, including non-avian dinosaurs.     

More than One Way of Being a Moa: Differences in Leg Bone Robustness Map Divergent Evolutionary Trajectories in Dinornithidae and Emeidae (Dinornithiformes)

The extinct moa of New Zealand included three families (Megalapterygidae; Dinornithidae; Emeidae) of flightless palaeognath bird, ranging in mass from <15 kg to >200 kg. They are perceived to have evolved extremely robust leg bones, yet current estimates of body mass have very wide confidence intervals. Without reliable estimators of mass, the extent to which dinornithid and emeid hindlimbs were more robust than modern species remains unclear. Using the convex hull volumetric-based method on CT-scanned skeletons, we estimate the mass of a female Dinornis robustus (Dinornithidae) at 196 kg (range 155–245 kg) and of a female Pachyornis australis (Emeidae) as 50 kg (range 33–68 kg). Finite element analysis of CT-scanned femora and tibiotarsi of two moa and six species of modern palaeognath showed that P. australis experienced the lowest values for stress under all loading conditions, confirming it to be highly robust. In contrast, stress values in the femur of D. robustus were similar to those of modern flightless birds, whereas the tibiotarsus experienced the highest level of stress of any palaeognath. We consider that these two families of Dinornithiformes diverged in their biomechanical responses to selection for robustness and mobility, and exaggerated hindlimb strength was not the only successful evolutionary pathway.     

Indices of Anseriform body shape based on the relative size of major skeletal elements and their relationship to reproductive effort

To assess whether relative clutch mass (RCM) in Anseriformes (wildfowl or waterfowl) is constrained by body shape, principal components (PCs) of size‐adjusted measurements of five major skeletal elements of adult males and females of 60 species of Anseriformes provided indices of body shape. PC1 accounted for 69.8% of the variance and contrasted anterior elements (cranium and sternum) to posterior elements (synsacrum, femur and tibiotarsus). PC1 scores were high in species with a ‘duck‐like’ body shape and low in those with a ‘goose‐like’ body shape. Over the phylogeny of Anseriformes, decreased PC1 scores were associated with feeding on land. PC2 accounted for 18.6% of the variance and contrasted core elements (sternum and synsacrum) with peripheral elements (cranium, femur and tibiotarsus). High PC2 scores were associated with dependence on animal food, particularly in diving species. PC3 accounted for 7.7% of the variance and reflected mainly the relative size of the femur, which was low in diving species. Controlling statistically for phylogenetically independent contrasts in female body shape, there was a significant positive partial correlation between RCM and PC1, suggesting that independent of body size, body shape imposes constraints on reproductive effort in Anseriformes. The results suggest that models of the evolution of reproductive effort in this order, and perhaps in other orders, of birds should control for the effects of body shape.     

Phenotypic Changes Across a Geographic Gradient: The Case of Three Sympatric Dolphin Species

Phenotypic changes in the mammalian mandible can occur at different spatial and temporal scales. We investigated mandibular size and shape variation in three extant closely related dolphins (Cetacea, Odontoceti): Tursiops truncatus, Stenella coeruleoalba and Delphinus delphis in order to test the hypothesis that similar phenotypic changes occur across the same geographical gradient. Our data included 219 specimens representative of the following geographic locations: the Mediterranean Sea, the eastern north Atlantic and the North Sea. Each mandibula was photographed laterally and spatial positioning of eight homologous 2D landmarks was recorded. After applying generalised Procrustes analysis (GPA), intraspecific variation was first investigated between sexes and among populations to allow further pooling of samples. Size and shape differences among populations and species were investigated through multivariate ordination techniques (PCA), Procrustes ANOVA and allometric analyses. In all three species, Mediterranean populations clearly differed in mandible shape from the extra-Mediterranean ones. Among the three, the direction of geographic phenotypic changes was significantly similar in the striped and common dolphin, while the bottlenose dolphin was the most divergent species, differing both in size and allometric trajectory. Shape variation of the two former species highlighted a morphological convergence in the Atlantic, and a phenotypic divergence in the Mediterranean. Shape differences among the three dolphin species were interpreted in the light of different prey preferences, feeding strategies and habitat partitioning to avoid direct competition.     

Intraspecific mating system evolution and its effect on complex male secondary sexual traits: Does male–male competition increase selection on size or shape?

Sexual selection is generally held responsible for the exceptional diversity in secondary sexual traits in animals. Mating system evolution is therefore expected to profoundly affect the covariation between secondary sexual traits and mating success. Whereas there is such evidence at the interspecific level, data within species remain scarce. We here investigate sexual selection acting on the exaggerated male fore femur and the male wing in the common and widespread dung flies Sepsis punctum and S. neocynipsea (Diptera: Sepsidae). Both species exhibit intraspecific differences in mating systems and variation in sexual size dimorphism (SSD) across continents that correlates with the extent of male–male competition. We predicted that populations subject to increased male–male competition will experience stronger directional selection on the sexually dimorphic male foreleg. Our results suggest that fore femur size, width and shape were indeed positively associated with mating success in populations with male‐biased SSD in both species, which was not evident in conspecific populations with female‐biased SSD. However, this was also the case for wing size and shape, a trait often assumed to be primarily under natural selection. After correcting for selection on overall body size by accounting for allometric scaling, we found little evidence for independent selection on any of these size or shape traits in legs or wings, irrespective of the mating system. Sexual dimorphism and (foreleg) trait exaggeration is therefore unlikely to be driven by direct precopulatory sexual selection, but more so by selection on overall size or possibly selection on allometric scaling.     

A small loon and a new species of large owl from the Rupelian of Belgium (Aves: Gaviiformes,Strigiformes)

The early Oligocene Boom Formation in Belgium yielded many avian remains from the Rupelian unit-stratotype, most of which have remained unstudied so far. Here, I describe a small loon (Gaviiformes) and a new species of large owl (Strigiformes) that are represented by associated bones of a single individual each. The loon, of which wing and pectoral girdle bones are preserved, is assigned to Colymboides (?) metzleri, a species previously known from a partial skeleton from the Rupelian of Germany. The owl is based on a tarsometatarsus and distal tibiotarsus and described as a new species, Selenornis steendorpensis. It constitutes the most substantial fossil record of the taxon Selenornis, which was before known from a distal tibiotarsus from an unknown horizon of the Quercy fissure fillings in southwestern France. It is detailed that there are differences in the higher level taxonomic composition of the known early Oligocene avifaunas of northern and southern Europe, which may reflect true zoogeographic facts owing to a different climate and vegetation.     

Radiographic analysis of the development of the pelvic limb of captive-reared cranes (Grus spp.)

For captive-reared cranes, pelvic limb abnormalities in chicks have been identified as significant morbidity/mortality factors. An important component of the diagnosis of limb abnormalities is the understanding of the normal limb. This study was undertaken to describe the normal, radiographic development of the femur, tibiotarsus, tarsometatarsus, and fibula of the whooping crane (Grus americana), Florida sandhill crane (Grus canadensis pratensis), and Siberian crane (Grus leucogeranus). Crane chicks were anesthetized and their pelvic limb bone development evaluated radiographically on a weekly to bimonthly basis from one to fourteen weeks of age. Body weight, bone length, diaphyseal width, and physeal development and closure were evaluated. Based on the radiographic analysis, the gross development of the long bones of the pelvic limb of whooping, Florida sandhill, and Siberian cranes was found to be similar among the three species, and not dissimilar from other avian species which have been studied. Repeated handling, anesthesia, and radiographic exposure did not produce any behavioral, developmental, or physical abnormalities in the studied cranes when compared to cranes of the same species raised using the same methods. This is the first work to describe pelvic limb bone development in these species. © 1996 Wiley-Liss, Inc.     

The first Cenozoic fossil bird from Venezuela

The first Cenozoic avian remains from Venezuela are described. The material comprises an associated right tarsometatarsus and tibiotarsus from the earliest Pliocene of the Codore Formation, northwestern Venezuela. The fossil-bearing horizon represents a deltaic paleoenvironment. The elements are long and narrow, and the presence of a circular incisura intercondylaris bordered proximally by a prominent and centrally-situated tuberculum m. tibialis anticus on the tibiotarsus, allows confident referral to the Ciconiidae (storks). The elements are a close match in morphology and size to the extantJabiru mycteria (Jabiru Stork), although the presence on the distal tibiotarsus of a well-defined caudal sulcus, a narrower sulcus extensorius and shallower angled pons supratendineus, and on the tarsometatarsus of a narrower and deeper sulcus on the plantar surface and a less prominent ridge laterally bordering the fossa supratrochlearis plantaris indicate that this is a new species,Jabiru codorensis n. sp.Jabiru mycteria, the only living species, still occurs in Venezuela, where it is found mostly in grassy wetlands. These specimens represent the first fossil record ofJabiru, as well as the first pre-Pleistocene record of fossil birds from Venezuela.      

Locomotion in the quail (Coturnix japonica): the kinematics of walking and increasing speed

Hindlimb segmental kinematics and stride characteristics are quantified in several quail locomoting on a treadmill over a six-fold increase in speed. These data are used to describe the kinematics of a walking stride and to identify which limb elements are used to change stride features as speed increases. In quail, the femur does not move during locomotion and the tarsometatarsus-phalangeal joint is a major moving joint; thus, quail have lost the most proximal moving joint and added one distally. The tibiotarsus and tarsometatarsus act together as a fixed strut swinging from the knee during stance phase (the ankle angle remains constant at a given speed) and the tarsometatarsus-phalangeal joint appears to have a major role in increasing limb length during the propulsive phase of the stride. Speed is increased with greater knee extension and by lengthening the tibiotarsus/tarsometatarsus via increased ankle extension at greater speeds. Because the femur is not moved and three distal elements are, quail move the limb segments through a stride and increase speed in a way fundamentally different from other nonavian vertebrates. However, the three moving joints in quail (the knee, ankle, and tarsometatarsophangeal joint) have strikingly similar kinematics to the analogous moving joints (the hip, knee, and ankle) in other vertebrates. Comparisons to other vertebrates indicate that birds appear to have two modes of limb function (three- and four-segment modes) that vary with speed and locomotory habits.     

Functional correlation between habitat use and leg morphology in birds (Aves)

Many of the morphological features of animals are considered to be adaptations to the habitat that the animals utilize. The habitats utilized by birds vary, perhaps more than for any other group of vertebrates. Here, we study possible adaptations in the morphology of the skeletal elements of the hind limbs to the habitat of birds. Measurements of the lengths of the femur, tibiotarsus and tarsometatarsus of 323 bird species from 74 families are used together with body mass data, taken from the literature. The species are separated into six habitat groups on the basis of literature data on leg use. A discriminant analysis of the groups based on leg morphology shows that swimming birds, wading birds and ground living species are more easily identified than other birds. Furthermore, functional predictions are made for each group based on ecological and mechanical considerations. The groups were tested for deviation from the norm for all birds for three indices of size- and leg-length-independent measures of the bones and for a size-independent-index of leg length. Several of the groups deviate significantly from the norm for one or more of the indices used, suggesting habitat-related adaptations in the leg morphology of birds. The results indicate that stability is an important factor affecting the leg morphology of primarily long-legged birds. The femur seems to be more important than previously thought because several of the groups have high femur indices, suggesting a positive selection pressure on this bone. On a general basis, the results suggest that the effect of leg length should be taken into consideration when discussing adaptations of mass-independent lengths of the long bones of the legs of birds.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79, 461–484.     

Rejection of non-adaptive hypotheses for intraspecific variation in trophic morphology in gape-limited predators

Recent studies have interpreted intraspecific divergence in relative head sizes in snakes as evidence for adaptation of the trophic apparatus in gape-limited predators to local prey size. However, such variation might also arise from non-adaptive processes (such as allometry, correlated response, genetic drift, or non-adaptive phenotypic plasticity). We test predictions from these alternative hypotheses using data on the allometric relationship between head size and body size in two wide-ranging snake species: eight populations of adders ( Vipera berus ) and 30 populations of common gartersnakes ( Thamnophis sirtalis ). Our data enable strong rejection of the alternative (non-adaptive) hypotheses, because the relationship between head and body size differed significantly among populations, the geographic distance separating pairs of populations explained less than 1.5% of their divergence in allometric coefficients, and the within-population allometric coefficients were higher than the among-population coefficients in each species. In addition, the geographical variability of allometric coefficients in females did not parallel that in males, suggesting that allometric coefficients have evolved independently in the two sexes. Phenotypic plasticity also cannot explain the data, because laboratory studies show that the allometric relationship between head size and body size is relatively insensitive to differing growth rates. We conclude that the intraspecific head size divergence in these snakes is better explained by spatially heterogeneous selection to optimize prey handling ability, than by non-adaptive processes.