The origin and early evolution of birds: discoveries,disputes, and perspectives from fossil evidence

The study of the origin and early evolution of birds has never produced as much excitement and public attention as in the past decade. Well preserved and abundant new fossils of birds and dinosaurs have provided unprecedented new evidence on the dinosaurian origin of birds, the arboreal origin of avian flight, and the origin of feathers prior to flapping flight. The Mesozoic avian assemblage mainly comprises two major lineages: the prevalent extinct group Enantiornithes, and the Ornithurae, which gave rise to all modern birds, as well as several more basal taxa. Cretaceous birds radiated into various paleoecological niches that included fish- and seed-eating. Significant size and morphological differences and variation in flight capabilities, ranging from gliding to powerful flight among early birds, highlight the diversification of birds in the Early Cretaceous. There is little evidence, however, to support a Mesozoic origin of modern avian groups. Controversy and debate, nevertheless, surround many of these findings, and more details are needed to give a better appreciation of the significance of these new discoveries.     

A drowned Mesozoic bird breeding colony from the Late Cretaceous of Transylvania

Despite a rapidly improving fossil record, the reproductive biology of Mesozoic birds remains poorly known: only a handful of undisputed, isolated Cretaceous eggs (some containing embryonic remains) are known. We report here the first fossil evidence for a breeding colony of Mesozoic birds, preserved at the Late Cretaceous (Maastrichtian) Oarda de Jos (Od) site in the Sebe? area of Transylvania, Romania. A lens of calcareous mudstone with minimum dimensions of 80?cm length, 50?cm width and 20?cm depth contains thousands of tightly packed, morphologically homogenous eggshell fragments, seven near-complete eggs and neonatal and adult avialan skeletal elements. Eggshell forms 70–80?% of the matrix, and other fossils are entirely absent. The bones exhibit clear characters of the Cretaceous avialan clade Enantiornithes, and the eggshell morphology is also consistent with this identification. Both taphonomy and lithology show that the components of this lens were deposited in a single flood event, and we conclude that it represents the drowned remains of a larger enantiornithine breeding colony, swamped by rising water, washed a short distance and deposited in a shallow, low-energy pond. The same fate often befalls modern bird colonies. Such a large concentration of breeding birds suggests aquatic feeding in this species, augments our understanding of enantiornithine biology and shows that colonial nesting was not unique to crown birds.     

Postnatal nutrition influences male attractiveness and promotes plasticity in male mating preferences

The fossil record of Late Cretaceous–Paleogene modern birds in the Southern Hemisphere includes the Maastrichtian Neogaeornis wetzeli from Chile, Polarornis gregorii and Vegavis iaai from Antarctica, and Australornis lovei from the Paleogene of New Zealand. The recent finding of a new and nearly complete Vegavis skeleton constitutes the most informative source for anatomical comparisons among Australornis, Polarornis, and Vegavis. The present contribution includes, for the first time, Vegavis, Polarornis, and Australornis in a comprehensive phylogenetic analysis. This analysis resulted in the recognition of these taxa as a clade of basal Anseriformes that we call Vegaviidae. Vegaviids share a combination of characters related to diving adaptations, including compact and thickened cortex of hindlimb bones, femur with anteroposteriorly compressed and bowed shaft, deep and wide popliteal fossa delimited by a medial ridge, tibiotarsus showing notably proximally expanded cnemial crests, expanded fibular crest, anteroposterior compression of the tibial shaft, and a tarsometatarsus with a strong transverse compression of the shaft. Isolated bones coming from the Cretaceous and Paleogene of South America, Antarctica, and New Zealand are also referred to here to Vegaviidae and support the view that these basal anseriforms were abundant and diverse at high southern latitudes. Moreover, vegaviids represent the first avian lineage to have definitely crossed the K–Pg boundary, supporting the idea that some avian clades were not affected by the end Mesozoic mass extinction event, countering previous interpretations. Recognition of Vegaviidae indicates that modern birds were diversified in southern continents by the Cretaceous and reinforces the hypothesis indicating the important role of Gondwana for the evolutionary history of Anseriformes and Neornithes as a whole.

     

Direct evidence of hybodont shark predation on Late Jurassic ammonites

Sharks are known to have been ammonoid predators, as indicated by analysis of bite marks or coprolite contents. However, body fossil associations attesting to this predator–prey relationship have never been described so far. Here, I report a unique finding from the Late Jurassic of western France: a complete specimen of the Kimmeridgian ammonite Orthaspidoceras bearing one tooth of the hybodont shark Planohybodus. Some possible tooth puncture marks are also observed. This is the first direct evidence of such a trophic link between these two major Mesozoic groups, allowing an accurate identification of both organisms. Although Planohybodus displays a tearing-type dentition generally assumed to have been especially adapted for large unshelled prey, our discovery clearly shows that this shark was also able to attack robust ammonites such as aspidoceratids. The direct evidence presented here provides new insights into the Mesozoic marine ecosystem food webs.     

Individual differences and repeatability in vocal production: stress-induced calling exposes a songbird's personality

Recent research in songbirds has demonstrated that male singing behavior varies systematically with personality traits such as exploration and risk taking. Here we examine whether the production of bird calls, in addition to bird songs, is repeatable and related to exploratory behavior, using the black-capped chickadee (Poecile atricapillus) as a model. We assessed the exploratory behavior of individual birds in a novel environment task. We then recorded the vocalizations and accompanying motor behavior of both male and female chickadees, over the course of several days, in two different contexts: a control condition with no playback and a stressful condition where chick-a-dee mobbing calls were played to individual birds. We found that several vocalizations and behaviors were repeatable within both a control and a stressful context, and across contexts. While there was no relationship between vocal output and exploratory behavior in the control context, production of alarm and chick-a-dee calls in the stressful condition was positively associated with exploratory behavior. These findings are important because they show that bird calls, in addition to bird song, are an aspect of personality, in that calls are consistent both within and across contexts, and covary with other personality measures (exploration).     

Hyperdisease in the late Pleistocene: validation of an early 20th century hypothesis

The hypothesis of disease-related large mammal extinction has new support. A unique pathologic zone of resorption was first noticed in a Hiscock Mammut americanum metacarpal. The pathognomonic zone of resorption was present in fifty-nine (52%) of 113 skeletons with feet available for examination. Metacarpals and metatarsals were most commonly affected. Associated rib periosteal reaction is highly suggestive of tuberculosis and the foot lesions were identical to that documented in Bison as pathognomonic for tuberculosis. Recognizing that only a portion of animals infected by infectious tuberculosis develop bone involvement, the high frequency of the pathology in M. americanum suggests that tuberculosis was not simply endemic, but actually pandemic, a hyperdisease. Pandemic tuberculosis was one of several probable factors contributing to mastodon extinction.     

Food remains in Confuciusornis sanctus suggest a fish diet

Despite hundreds of excellent fossils of Confuciusornis, the most abundant group of birds in the Early Cretaceous, ‘Jehol Biota’ in China, there is yet no indication of the food choice of these birds. Here, we describe fish remains preserved in the alimentary system of a specimen of Confuciusornis sanctus from the Jiufotang Formation. This find is about five million years younger than all previously published confuciusornithid birds from the Yixian Formation. Although it is unknown how common fish was in the diet of Confuciusornis, the find does not support previous hypotheses that it fed on plants or grain.     

<Emphasis Type="Italic">Jeholornis</Emphasis> compared to<Emphasis Type="Italic"> Archaeopteryx</Emphasis>, with a new understanding of the earliest avian evolution

The recently reported Jeholornis represents the only known bird with a complete long skeletal tail except for Archaeopteryx. Two newly discovered specimens referable to Jeholornis provide some important new information about its anatomy. The tail of Jeholornis is much longer than that of Archaeopteryx and comprises a maximum of 27 caudal vertebrae compared with only 23 in Archaeopteryx. More interestingly, the tail feathers are shaped more like those of dromaeosaurs than those of Archaeopteryx. We conclude that the common ancestor of birds must have a more primitive tail than that in Archaeopteryx, confirming the side branch position of Archaeopteryx in the early avian evolution. The synsacrum is composed of six sacrals, representing a transitional stage between Archaeopteryx and more advanced birds. The scapula of Jeholornis has a dorso-laterally exposed glenoid facet, and the coracoid has a supracoracoid foramen. The presence of a pair of fenestrae in the sternum of Jeholornis has further implications for the air-sac system in early birds. Electronic Supplementary Material  The online version of this article (doi: contains supplementary material, which is available to authorized users.     

A new clade of archaic large-bodied predatory dinosaurs (Theropoda: Allosauroidea) that survived to the latest Mesozoic

Non-avian theropod dinosaurs attained large body sizes, monopolising terrestrial apex predator niches in the Jurassic–Cretaceous. From the Middle Jurassic onwards, Allosauroidea and Megalosauroidea comprised almost all large-bodied predators for 85 million years. Despite their enormous success, however, they are usually considered absent from terminal Cretaceous ecosystems, replaced by tyrannosaurids and abelisaurids. We demonstrate that the problematic allosauroids Aerosteon, Australovenator, Fukuiraptor and Neovenator form a previously unrecognised but ecologically diverse and globally distributed clade (Neovenatoridae, new clade) with the hitherto enigmatic theropods Chilantaisaurus, Megaraptor and the Maastrichtian Orkoraptor. This refutes the notion that allosauroid extinction pre-dated the end of the Mesozoic. Neovenatoridae includes a derived group (Megaraptora, new clade) that developed long, raptorial forelimbs, cursorial hind limbs, appendicular pneumaticity and small size, features acquired convergently in bird-line theropods. Neovenatorids thus occupied a 14-fold adult size range from 175 kg (Fukuiraptor) to approximately 2,500 kg (Chilantaisaurus). Recognition of this major allosauroid radiation has implications for Gondwanan paleobiogeography: The distribution of early Cretaceous allosauroids does not strongly support the vicariant hypothesis of southern dinosaur evolution or any particular continental breakup sequence or dispersal scenario. Instead, clades were nearly cosmopolitan in their early history, and later distributions are explained by sampling failure or local extinction.     

Does leaf flushing in the dry season affect leaf traits and herbivory in a tropical dry forest?

We report a small hawk-like diurnal bird from the early Oligocene (30–31 million years ago) of Poland. Aviraptor longicrus, n. gen. et sp. is of a size comparable with the smallest extant Accipitridae. The new species is characterized by very long legs, which, together with the small size, suggest an avivorous (bird-eating) feeding behavior. Overall, the new species resembles extant sparrowhawks (Accipiter spp.) in the length proportions of the major limb bones, even though some features indicate that it convergently acquired an Accipiter-like morphology. Most specialized avivores amongst extant accipitrids belong to the taxon Accipiter and predominantly predate small forest passerines; the smallest Accipiter species also hunts hummingbirds. Occurrence of a possibly avivorous raptor in the early Oligocene of Europe is particularly notable because A. longicrus coexisted with the earliest Northern Hemispheric passerines and modern-type hummingbirds. We therefore hypothesize that the diversification of these birds towards the early Oligocene may have triggered the evolution of small-sized avivorous raptors, and the new fossil may exemplify one of the earliest examples of avian predator/prey coevolution.

     

Do birds sleep in flight?

The following review examines the evidence for sleep in flying birds. The daily need to sleep in most animals has led to the common belief that birds, such as the common swift (Apus apus), which spend the night on the wing, sleep in flight. The electroencephalogram (EEG) recordings required to detect sleep in flight have not been performed, however, rendering the evidence for sleep in flight circumstantial. The neurophysiology of sleep and flight suggests that some types of sleep might be compatible with flight. As in mammals, birds exhibit two types of sleep, slow-wave sleep (SWS) and rapid eye-movement (REM) sleep. Whereas, SWS can occur in one or both brain hemispheres at a time, REM sleep only occurs bihemispherically. During unihemispheric SWS, the eye connected to the awake hemisphere remains open, a state that may allow birds to visually navigate during sleep in flight. Bihemispheric SWS may also be possible during flight when constant visual monitoring of the environment is unnecessary. Nevertheless, the reduction in muscle tone that usually accompanies REM sleep makes it unlikely that birds enter this state in flight. Upon landing, birds may need to recover the components of sleep that are incompatible with flight. Periods of undisturbed postflight recovery sleep may be essential for maintaining adaptive brain function during wakefulness. The recent miniaturization of EEG recording devices now makes it possible to measure brain activity in flight. Determining if and how birds sleep in flight will contribute to our understanding of a largely unexplored aspect of avian behavior and may also provide insight into the function of sleep.     

Carotenoids,immune response and the expression of sexual ornaments in male greenfinches (<Emphasis Type="Italic">Carduelis chloris</Emphasis>)

Allocation trade-offs of carotenoids between their use in the immune system and production of sexual ornaments have been suggested as a proximate mechanism maintaining honesty of sexual signals. To test this idea, we experimentally examined whether carotenoid availability in the diet was related to variation in antibody response to novel antigens in male greenfinches (Carduelis chloris aurantiiventris), a species with extensive carotenoid-dependent plumage colouration. We also measured the cost of mounting a humoral response in terms of circulating carotenoids. Finally, we examined the relationship between plumage colour, immune response and circulating carotenoids. We found that males with carotenoid-supplemented diets showed stronger antibody response than non-supplemented birds. We also found that activation of the immune system significantly reduced circulating carotenoids (24.9% lower in immune-challenged birds than in control birds). Finally, intensity (chroma) of ventral plumage colouration of males, a character directly related to concentration of total carotenoids in feathers, was negatively correlated with the immune response and circulating carotenoids in winter. These results support the idea that carotenoids are a limiting resource and that males trade ornamental colouration against immune response.     

Scale-dependent habitat selection in migratory frugivorous passerines

Frugivorous migrants may select fruit-rich habitats en route to attain high food rewards, yet their stopover behavior may also be shaped by other considerations, such as predation risk. During 1996–2001 we investigated autumn stopover habitat use of three Sylvia warblers (sylviids; S. hortensis, S. atricapilla and S. curruca) and three Turdidae chats (turdids; Cercotrichas galactotes, Oenanthe hispanica and Phoenicurus phoenicurus) in planted groves of the fruiting tree Pistacia atlantica in Lahav Forest, Israel, which is located at the edge of a desert. We used fecal analysis, a constant-effort trapping scheme and field observations to estimate the extent of frugivory, and bird habitat and microhabitat selection with regard to natural fruit and foliage densities. We also measured bird microhabitat selection in a set of fruit-manipulated trees. We trapped a total of 2,357 birds during the course of the study. Although sylviids exhibited higher frugivory level than turdids, both species groups exhibited a similar significantly positive correlation between bird and fruit densities at the habitat scale. However, at the microhabitat scale, sylviids selected densely foliated trees, whilst turdids were randomly distributed among trees. Our findings suggest that both species groups selected fruit-rich stopover habitats to take advantage of the high food availability before the demanding migration journey. No other mechanism except predation avoidance can explain the sylviids microhabitat selection; the migrants used foliage cover to reduce bird detectability by raptors. We conclude that en route passerines may use staging habitats in a sophisticated manner, by adopting scale-related behavior with regard to the availability of food and refuge cover.     

Gastroliths in<Emphasis Type="Italic"> Yanornis</Emphasis>: an indication of the earliest radical diet-switching and gizzard plasticity in the lineage leading to living birds?

Yanornis martini is an Early Cretaceous basal ornithurine bird. Its fish-eating diet was previously recognized from a discrete mass of disarticulated fish remains discovered in its abdominal region. A new complete and articulated specimen of Yanornis martini preserves abundant in-situ gastroliths such as have been associated with a herbivorous diet. We suggest that the occurrence of gastroliths in this specimen, fish remains in a second, and the lack of gastroliths in three others, is consistent with diet-switching in Yanornis martini. Incompatibility of the preserved data with explanations of the grit as an artifact of preservation or result of accidental ingestion is discussed. This discovery indicates the earliest presence of intermittent diet change (and associated gizzard plasticity) observed in extant birds seasonally and in response to changes in available food sources.     

Out of Africa: Fossils shed light on the origin of the hoatzin,an iconic Neotropic bird

We describe the earliest fossils of the enigmatic avian taxon Opisthocomiformes (hoatzins) from the Oligo-Miocene (22–24 mya) of Brazil. The bones, a humerus, scapula and coracoid, closely resemble those of the extant hoatzin, Opisthocomus hoazin. The very similar osteology of the pectoral girdle in the new Brazilian fossil compared to the extant O. hoazin, in which it reflects peculiar feeding adaptations, may indicate that hoatzins had already evolved their highly specialized feeding behavior by the mid-Cenozoic. We further show that Namibiavis senutae from the early Miocene of Namibia is another, previously misclassified representative of Opisthocomiformes, which documents that the extant Neotropic distribution of hoatzins is relictual. Because of the weak flight capabilities of hoatzins, their occurrence on both sides of the South Atlantic is of particular biogeographic interest. We detail that this distribution pattern is best explained by dispersal from Africa to South America, and that Opisthocomiformes provide the first example of transatlantic rafting among birds.     

Avian phenotypic traits related to feeding preferences in two <Emphasis Type="Italic">Culex</Emphasis> mosquitoes

Host choice by mosquitoes affects the transmission dynamics of vector-borne infectious diseases. Although asymmetries in mosquito attraction to vertebrate species have been reported, the relative importance of host characteristics in mosquito blood-feeding behavior is still poorly studied. Here, we investigate the relationship between avian phenotypic traits—in particular, morphometry, plumage coloration, and nesting and roosting behavior—and the blood-feeding patterns in two common Culex mosquito species on a North American avian community. Forage ratios of the mosquito species were unrelated to the phylogenetic relationships among bird species. Culex pipiens fed preferably on birds with lighter-colored plumage and longer tarsi; furthermore, solitary roosting avian species were both bitten by Cx. pipiens and Cx. restuans more often than expected. These associations may be explained by greater mosquito attraction towards larger birds with a greater color contrast against the background. Although communally roosting birds may release more cues and attract more mosquitoes, individuals may in fact receive fewer bites due to the encounter-dilution effect. Mosquito feeding behavior is a highly complex phenomenon, and our results may improve understanding of the non-random interaction between birds and mosquitoes in natural communities.     

Vegaviidae,a new clade of southern diving birds that survived the K/T boundary

The fossil record of Late Cretaceous–Paleogene modern birds in the Southern Hemisphere includes the Maastrichtian Neogaeornis wetzeli from Chile, Polarornis gregorii and Vegavis iaai from Antarctica, and Australornis lovei from the Paleogene of New Zealand. The recent finding of a new and nearly complete Vegavis skeleton constitutes the most informative source for anatomical comparisons among Australornis, Polarornis, and Vegavis. The present contribution includes, for the first time, Vegavis, Polarornis, and Australornis in a comprehensive phylogenetic analysis. This analysis resulted in the recognition of these taxa as a clade of basal Anseriformes that we call Vegaviidae. Vegaviids share a combination of characters related to diving adaptations, including compact and thickened cortex of hindlimb bones, femur with anteroposteriorly compressed and bowed shaft, deep and wide popliteal fossa delimited by a medial ridge, tibiotarsus showing notably proximally expanded cnemial crests, expanded fibular crest, anteroposterior compression of the tibial shaft, and a tarsometatarsus with a strong transverse compression of the shaft. Isolated bones coming from the Cretaceous and Paleogene of South America, Antarctica, and New Zealand are also referred to here to Vegaviidae and support the view that these basal anseriforms were abundant and diverse at high southern latitudes. Moreover, vegaviids represent the first avian lineage to have definitely crossed the K–Pg boundary, supporting the idea that some avian clades were not affected by the end Mesozoic mass extinction event, countering previous interpretations. Recognition of Vegaviidae indicates that modern birds were diversified in southern continents by the Cretaceous and reinforces the hypothesis indicating the important role of Gondwana for the evolutionary history of Anseriformes and Neornithes as a whole.     

A juvenile coelurosaurian theropod from China indicates arboreal habits

Here we report an unequivocal arboreal coelurosaur, Epidendrosaurus ningchengensis gen. et sp. nov. This juvenile coelurosaur's third manual digit is extremely elongated, distinctively different from that of other known dinosaurs and birds. It represents certainly a type of adaptation previously unreported from the Mesozoic although the exact function of the third manual digit is unclear. The relatively long forelimb, penultimate phalanx of manual digit II, and pedal penultimate phalanges, are interpreted as evidence for the arboreal habit of Epidendrosaurus. Because Epidendrosaurus is more similar to advanced birds in some arboreal features than to Archaeopteryx, we suggest that the initial appearance of tree-adaptation in theropods was probably not directly related to flight but to other functions, such as seeking food or escaping from predators. Electronic Supplementary Material is available if you access this article at http://dx.doi.org/10.1007/s00114-002-0353-8. On that page (frame on the left side), a link takes you directly to the supplementary material.     

Largest bird from the Early Cretaceous and its implications for the earliest avian ecological diversification

With only one known exception, early Cretaceous birds were smaller than their closest theropod dinosaur relatives. Here we report on a new bird from the Early Cretaceous feathered-dinosaur-bearing continental deposits of Liaoning, northeast China, which is not only larger than Archaeopteryx but is nearly twice as large as the basal dromaeosaur Microraptor. The new taxon, Sapeornis chaoyangensis gen. et sp. nov., has a more basal phylogenetic position than all other birds except for Archaeopteryx. Its exceptionally long forelimbs, well-developed deltoid crest of the humerus, proximally fused metacarpals, relatively short hindlimbs and short pygostyle indicate powerful soaring capability and further suggest that by the Early Cretaceous ecological diversification of early birds was greater than previously assumed. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00114-001-0276-9.     

Bird pollination of Canary Island endemic plants

The Canary Islands are home to a guild of endemic, threatened bird-pollinated plants. Previous work has suggested that these plants evolved floral traits as adaptations to pollination by flower specialist sunbirds, but subsequently, they appear to have co-opted generalist passerine birds as sub-optimal pollinators. To test this idea, we carried out a quantitative study of the pollination biology of three of the bird-pollinated plants, Canarina canariensis (Campanulaceae), Isoplexis canariensis (Veronicaceae) and Lotus berthelotii (Fabaceae), on the island of Tenerife. Using colour vision models, we predicted the detectability of flowers to bird and bee pollinators. We measured pollinator visitation rates, nectar standing crops as well as seed-set and pollen removal and deposition. These data showed that the plants are effectively pollinated by non-flower specialist passerine birds that only occasionally visit flowers. The large nectar standing crops and extended flower longevities (>10 days) of Canarina and Isoplexis suggests that they have evolved a bird pollination system that effectively exploits these low frequency non-specialist pollen vectors and is in no way sub-optimal. Seed set in two of the three species was high and was significantly reduced or zero in flowers where pollinator access was restricted. In L. berthelotii, however, no fruit set was observed, probably because the plants were self-incompatible horticultural clones of a single genet. We also show that, while all three species are easily detectable for birds, the orange Canarina and the red Lotus (but less so the yellow-orange Isoplexis) should be difficult to detect for insect pollinators without specialised red receptors, such as bumblebees. Contrary to expectations if we accept that the flowers are primarily adapted to sunbird pollination, the chiffchaff (Phylloscopus canariensis) was an effective pollinator of these species.