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An Early Cretaceous bird from Spain and its implications for the evolution of avian flight
Abstract
AVIAN flight is one of the most remarkable achievements of vertebrate evolution, yet there is little evidence of its early phases. Specimens of Archaeopteryx shed important (albeit controversial) light on this evolutionary phenomenon, but the large morphological (and almost certainly functional) gap between Archaeopteryx and modern avians remained virtually empty until recently. Here we report a new, exquisitely preserved, bird from the Lower Cretaceous Konservat-Lagerstätte of Las Hoyas (Cuenca, Spain) which provides evidence for the oldest known alula (bastard wing). Crustacean remains found inside its belly also provide the oldest direct evidence of feeding habits in birds. The new specimen has numerous synapomorphies with the Enantiornithes, but its unique sternal morphology, along with other autopomorphies in the furcula and vertebral centra, support the recognition of a new enantiornithine taxon, Eoalulavishoyasi. The combination in Eoalulavis of a decisive aerodynamic feature, such as the alula, with the basic structures of the modern flight apparatus indicates that as early as 115 million years ago, birds had evolved a sophisticated structural system that enabled them to fly at low speeds and to attain high manoeuvrability.
... The mid-sized pterosaur Europejara, with an estimated wingspan of 3 -4 m, would presumably pertain to this level of herbivore The ecological link between water and land would be attributable to predators with amphibian lifestyle, including the small anurans (i.e., frogs and toads-Salientia), the small pseudosuchian and neosuchian crocodilians, and the large goniopholidid crocodiles, whose presence is only evidenced by several trackways (Moratalla et al., 1995). On the other hand, the Enantiornithine avians (Fig. 6) stand among the most abundant land tetrapods in Las Hoyas, with at least ten recognized specimens (Sanz et al. 1988, Sanz et al. 1996, Sanz and Buscalioni 1992, Sanz et al. 2001Cambra et al. 2006, Navalón et al. 2015 and a new specimen under study. Evidence of crustacean remains in the stomach of Eoalulavis indicated that they probably fed in the water column (Sanz et al. 1996). ...
... On the other hand, the Enantiornithine avians (Fig. 6) stand among the most abundant land tetrapods in Las Hoyas, with at least ten recognized specimens (Sanz et al. 1988, Sanz et al. 1996, Sanz and Buscalioni 1992, Sanz et al. 2001Cambra et al. 2006, Navalón et al. 2015 and a new specimen under study. Evidence of crustacean remains in the stomach of Eoalulavis indicated that they probably fed in the water column (Sanz et al. 1996). These large numbers, along with the diagnosis of Iberomesornis as a sub-adult (Sanz et al. 2002, Cubo et al. 2022, other young specimens in a possible pellet (Sanz et al. 2001) and the report of a hatchling (Knoll et al. 2018, Kaye et al. 2019Fig. ...
Las Hoyas (Cuenca, Spain) represents a unique Lower Cretaceous (Barremian) fossil biota of a wetland. The site has yielded a particularly diverse assemblage of more than twenty thousand plant and animal fossils, many of which present unprecedented soft-tissue preservation, including microstructural details. Among the most significant discoveries are the oldest angiosperms, the smallest species of chondrichtians and squamates, new theropod dinosaurs, including several enantiornithine birds, the first European tapejarid pterosaur and the most complete Eutriconodont mammal. Such discoveries have produced data on important aspects related to plant and animal evolution, such as the first steps in flower development by plants, insight on unknown anatomical and diet specializations in theropod dinosaurs, the development of flight maneuverability in early birds, the unexpected global distribution of tapejarid dinosaurs, and groundbreaking data on early mammalian hair development. There are many more discoveries to unveil and new research is now liking the immense wealth of paleobiological information with mathematical procedures to study the ecological structure of the wetland.
Supplementary material: https://doi.org/10.6084/m9.figshare.c.6336914
... Among Enantiornithes, the most diverse and widespread avialans in the Mesozoic, only Eoalulavis and Shenqiornis have good evidence (i.e. fossilised digestive tract contents or more than one line of quantitative proxy evidence) backing any particular diet [1,5] out of nearly 100 known species [6]. A more robust understanding of non-avian avialan diet will allow us to test key hypotheses in bird evolution, such as beak evolution allowing for extant bird dietary diversity [7,8], trophic level reduction driving powered flight development [9], and birds occupying a low-level consumer role in Mesozoic ecosystems [10]. ...
... [202], with scripts available from [203]. Additional files 2, 3,4,5,6,7,8,9,10,11,12,13,14 and 15 also include interactive HTML-based three-dimensional graphs of all multivariate analysis results and two-dimensional multivariate FEA graphs annotated with contour plots of each jaw. Both were made using a package from Plotly (Plotly, Canada) for R [204], version 4.9.4.1. ...
Background
Birds are key indicator species in extant ecosystems, and thus we would expect extinct birds to provide insights into the nature of ancient ecosystems. However, many aspects of extinct bird ecology, particularly their diet, remain obscure. One group of particular interest is the bizarre toothed and long-snouted longipterygid birds. Longipterygidae is the most well-understood family of enantiornithine birds, the dominant birds of the Cretaceous period. However, as with most Mesozoic birds, their diet remains entirely speculative.
Results
To improve our understanding of longipterygids, we investigated four proxies in extant birds to determine diagnostic traits for birds with a given diet: body mass, claw morphometrics, jaw mechanical advantage, and jaw strength via finite element analysis. Body mass of birds tended to correspond to the size of their main food source, with both carnivores and herbivores splitting into two subsets by mass: invertivores or vertivores for carnivores, and granivores + nectarivores or folivores + frugivores for herbivores. Using claw morphometrics, we successfully distinguished ground birds, non-raptorial perching birds, and raptorial birds from one another. We were unable to replicate past results isolating subtypes of raptorial behaviour. Mechanical advantage was able to distinguish herbivorous diets with particularly high values of functional indices, and so is useful for identifying these specific diets in fossil taxa, but overall did a poor job of reflecting diet. Finite element analysis effectively separated birds with hard and/or tough diets from those eating foods which are neither, though could not distinguish hard and tough diets from one another. We reconstructed each of these proxies in longipterygids as well, and after synthesising the four lines of evidence, we find all members of the family but Shengjingornis (whose diet remains inconclusive) most likely to be invertivores or generalist feeders, with raptorial behaviour likely in Longipteryx and Rapaxavis.
Conclusions
This study provides a 20% increase in quantitatively supported fossil bird diets, triples the number of diets reconstructed in enantiornithine species, and serves as an important first step in quantitatively investigating the origins of the trophic diversity of living birds. These findings are consistent with past hypotheses that Mesozoic birds occupied low trophic levels.
... There is some evidence suggesting that the enlarged size of extant avian endosseous labyrinths is related to enhanced visual acuity [34], and that its size and marked ventral deflection is associated with enhanced manoeuvrability in some crown birds [19], although other investigations [34,35] have failed to support this latter interpretation. The enhanced flight proficiency of enantiornithines has been supported by different lines of evidence [36][37][38][39], and it is possible (as mentioned above) that some aspects of inner ear morphology may reflect adaptations for such aerial prowess [19,34,35]. Nonetheless, we argue the possibility that the crown-like vestibular traits observed in MPM-334-1 constitute an epiphenomenon related to brain flexion and the resultant caudal repositioning of the optic tectum need to be given careful attention. ...
Among terrestrial vertebrates, only crown birds (Neornithes) rival mammals in terms of relative brain size and behavioural complexity. Relatedly, the anatomy of the avian central nervous system and associated sensory structures, such as the vestibular system of the inner ear, are highly modified with respect to those of other extant reptile lineages. However, a dearth of three-dimensional Mesozoic fossils has limited our knowledge of the origins of the distinctive endocranial structures of crown birds. Traits such as an expanded, flexed brain, a ventral connection between the brain and spinal column, and a modified vestibular system have been regarded as exclusive to Neornithes. Here, we demonstrate all of these 'advanced' traits in an undistorted braincase from an Upper Cretaceous enantiornithine bonebed in southeastern Brazil. Our discovery suggests that these crown bird-like endocranial traits may have originated prior to the split between Enantior-nithes and the more crownward portion of avian phylogeny over 140 Ma, while coexisting with a remarkably plesiomorphic cranial base and posterior palate region. Altogether, our results support the interpretation that the distinctive endocranial morphologies of crown birds and their Mesozoic relatives are affected by complex trade-offs between spatial constraints during development.
... Conversely, lines of fossil evidence suggest that some fish 34,35 , turtles 36 , and crocodiles 35 fed on molluscan invertebrates during the Early Cretaceous, and the Kitadani Freshwater Bivalves indeed occurs with abundant lepisosteiform scales, testudinate shells and crocodile teeth. Additionally, at least one Early Cretaceous avian species with crustacean gut contents can be attributed to the durophagous diet 37 , and the Kitadani Formation has yielded avialan skeletal remains 38 , and footprints 39,40 . Therefore, fish, turtles, crocodiles, and birds are likely candidates for visual predators of the Early Cretaceous freshwater bivalves, and have remained so until present. ...
The class Bivalvia (phylum Mollusca) is one of the most successful at survival groups of animals with diverse color patterns on their shells, and they are occasionally preserved in the fossil record as residual color patterns. However, the fossil record of the residual color patterns in freshwater bivalves could be traced only to the Miocene, greatly limiting color pattern evolution knowledge. We present the color patterns of the Cretaceous freshwater bivalves belonging to three extinct families of the order Trigoniida (hereinafter the Kitadani Freshwater Bivalves) from Japan, which is the oldest and the second fossil record of freshwater molluscan color patterns. The Kitadani Freshwater Bivalves consists of two types of color patterns: stripes along the growth lines and radial rays tapered toward the umbo, which resemble that of the colored bands of extant freshwater bivalves. This resemblance of the color patterns between the Kitadani Freshwater Bivalves and the extant species indicates that the color patterns of the freshwater bivalves represent the convergent evolution between Trigoniida and Unionida. To explain this convergent evolution, we advocate three conceivable factors: the phylogenetic constraints, monotonous habitats typical of freshwater ecosystems, and the predation pressure by visual predators in freshwater sediments.
... Trackmaker recognition of this abnormal and pathological trackway should be carefully considered. Small-to medium-sized avian and non-avian theropods that characterise the Las Hoyas diversity, such as the enantiornithes [69][70][71], and ornithomimosaur, Pelecanimimus polyodon [72] were discarded as putative producers due to their body size. The carcharodontosaurid, Concavenator corcovatus [73][74] was also discarded because it shows a pes of half the size of the magenta footprints with short and subequal toes. ...
We describe a trackway (LH-Mg-10-16) occurring in laminated carbonated limestones of the Las Hoyas locality, Serranía de Cuenca, Spain. It is unmistakably a large theropod dinosaur trackway encompassing two unusual aspects, namely, wide-steps, and a set of equally deformed left footprints (with a dislocated digit). The layer also preserves other vertebrate trails (fish Undichna ) and different impressions in the sediment. To address these complex settings, we devised a multidisciplinary approach, including the ichnological and taphonomical descriptions, characterisation of the rock lithofacies using thin-sections, 3D structured-light digitalisation with a high precision of 200–400 μm, and a geometric morphometric comparison with a large sample of bipedal dinosaur trackways. Sedimentary analyses showed that the trackway was produced in a humid, benthonic microbial mat, the consistency and plasticity of which enabled the preservation of the details of the movement of the animal. The results of the geometric analysis indicate that the “wide-steps” of the trackway is not unusual compared to other trackways, providing evidence that it was made by a single individual with an estimated hip height approximately 2 m. Analogous pathologies in extant archosaurs that yield the combination of wide steps and deformed digits in the same trackway were considered. All results mutually support the hypothesis that a large theropod dinosaur, with a pathological foot, generated the trackway as it crossed an area of shallow water while slowly walking towards the main water source, thus stepping steadily over the benthonic mat over which multiple fish were swimming.
The Longipterygidae are a unique clade among the enantiornithines in that they exhibit elongate rostra (≥60% total skull length) with dentition restricted to the distal tip of the rostrum, and pedal morphologies suited for an arboreal lifestyle (as in other enantiornithines). This suite of features has made interpretations of this group’s diet and ecology difficult to determine due to the lack of analogous taxa that exhibit similar morphologies together. Many extant bird groups exhibit rostral elongation, which is associated with several disparate ecologies and diets ( e.g ., aerial insectivory, piscivory, terrestrial carnivory). Thus, the presence of rostral elongation in the Longipterygidae only somewhat refines trophic predictions of this clade. Anatomical morphologies do not function singularly but as part of a whole and thus, any dietary or ecological hypothesis regarding this clade must also consider other features such as their unique dentition. The only extant group of dentulous volant tetrapods are the chiropterans, in which tooth morphology and enamel thickness vary depending upon food preference. Drawing inferences from both avian bill proportions and variations in the dental morphology of extinct and extant taxa, we provide quantitative data to support the hypothesis that the Longipterygidae were animalivorous, with greater support for insectivory.
An unabated surge of new and important discoveries continues to transform knowledge of pen-naraptoran biology and evolution amassed over the last 150+ years. This chapter summarizes progress made thus far in sampling the pennaraptoran fossil record of the Mesozoic and Paleocene and proposes priority areas of attention moving forward. Oviraptorosaurians are bizarre, nonparavian pennaraptorans first discovered in North America and Mongolia within Late Cretaceous rocks in the early 20th century. We now know that oviraptorosaurians also occupied the Early Cretaceous and their unquestionable fossil record is currently limited to Laurasia. Early Cretaceous material from China preserves feathers and other soft tissues and ingested remains including gastroliths and other stomach contents, while brooding specimens and age-structured, single-species accumulations from China and Mongolia provide spectacular behavioral insights. Less specialized early oviraptorosaurians like Incisivosaurus and Microvenator remain rare, and ancestral forms expected in the Late Jurassic are yet to be discovered, although some authors have suggested Epidexipteryx and possibly other scansoriopterygids may represent early-diverging oviraptorosaurians. Long-armed scansoriopterygids from the Middle-Late Jurassic of Laurasia are either early-diverging oviraptorosaurians or paravians, and some have considered them to be early-diverging avialans. Known from five (or possibly six) feathered specimens from China, only two mature individuals exist, representing these taxa. These taxa, Yi and Ambopteryx, preserve stylopod-supported wing membranes that are the only known alternative to the feathered, muscular wings that had been exclusively associated with dinosaurian flight. Thus, scansoriopterygid specimens-particularly those preserving soft tissue-remain a key priority for future specimen collection. Dromaeosaurids and troodontids were first discovered in North America and Mongolia in Late Cretaceous rocks. More recent discoveries show that these animals originated in the Late Jurassic, were strikingly feathered, lived across diverse climes and environments, and at least in the case of dromaeosaurids, attained a global distribution and the potential for aerial locomotion at small size.
The phylum Bivalvia is one of the most successful at survival groups of animals with diverse color patterns on their shells, and they are occasionally preserved in the fossil record as residual color patterns. However, the fossil record of the residual color patterns in freshwater bivalves could be traced only to the Miocene, greatly limiting color pattern evolution knowledge. We present the color patterns of the Cretaceous freshwater bivalves (hereinafter the Kitadani Freshwater Bivalves) from Japan, which is the oldest and the second fossil record of freshwater molluscan color patterns. The Kitadani Freshwater Bivalves consists of two types of color patterns: stripes along the growth lines and radial rays tapered toward the umbo, which resemble that of the colored bands of extant freshwater bivalves. This resemblance of the color patterns between the Kitadani Freshwater Bivalves and the extant species indicates that the color patterns of the freshwater bivalves have remained unchanged for approximately 120 million years, representing an extreme evolutionary conservatism. To explain this evolutionary conservatism, we advocate two conceivable factors: one is promoted by monotonous habitats typical of freshwater ecosystems, and the predation pressure by visual predators against such pressure for camouflaging in freshwater sediments.
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Our understanding of the early evolution of birds has advanced over the past 2 decades, thanks to an ever-improving fossil record. Extraordinary fossils have revealed new details about the evolution of the avian brain, respiratory system, digestive tract, and reproductive system. Many of the traits most strongly associated with birds first arose in nonavian theropod dinosaurs. Theropods evolved pennaceous feathers, incipient wings, and gliding flight long before modern birds appeared. Birds likewise inherited features such as an expanded forebrain, gizzard, dorsally immobile lung, pigmented eggs, and paternal brooding system from their theropod ancestors. Yet, the earliest birds also retained primitive traits such as teeth, clawed hands, long bony tails, partially buried nests, and slower growth. The evolution of birds was profoundly influence by the Cretaceous–Paleogene mass extinction, which wiped out the previously dominant Enantiornithines (“opposite birds”). This sets the stage for modern birds to radiate into the most diverse major clade of tetrapods.
The Neocomian Spanish outcrops of Montsec (province of Lérida) and the new one of Las Hoyas (province of Cuenca) have yielded several avian remains in the last few years. Several isolated feathers have been reported from Montsec, and a specimen of some feathered wing bones has recently been found. Las Hoyas has yielded an isolated feather and a nearly articulated small fossil bird that lacks the skull. This new specimen, reported here, presents a combination of derived (strut-like coracoids, pygostyle) and primitive (pelvic girdle, sacrum, hind limb) character states. If one considers Archaeopteryx, Ornithurae and the new Spanish fossil bird, it seems clear that the latter taxon is the sister group of Ornithurae (extant birds and all other fossil birds that are closer to recent forms than is Archaeopteryx).
More than half of the evolutionary history of birds is played out in the Mesozoic. A recent burst of fossil discoveries has documented a tremendous diversity of early avians. Clarification of the Phylogenetic structure of this diversity has provided clues for a better understanding of the evolution of functional, developmental and physiological characteristics of modern birds. Yet their long Mesozoic history is only beginning to be deciphered.
A new genus and species of Late Cretaceous (Coniancian–Santonian) birds, Neuquenornis volans, is described. This new taxon is known from a fairly complete, articulated specimen from the Río Colorado Formation of northwestern Patagonia. Synapomorphies of the humerus, radius, ulna, coracoid, femur, tibiotarsus, tarsometatarsus, and thoracic vertebrae, support its allocation to the Enantiornithes. The tarsometatarsal structure of Neuquenornis refers it to the Late Cretaceous family Avisauridae. The structure of the wing and pectoral girdle of Neuquenornis indicates that it was an active flyer, an aptitude also inferred for the El Brete enantiornithines from the Upper Cretaceous Lecho Formation of northwestern Argentina. The pedal structure of Neuquenornis and Soroavisaurus from El Brete, indicates that avisaurids were capable of perching in trees.
As the earliest birds known, the late Jurassic specimens of Archaeopteryx have been the object of great speculative interest. Ostrom1–3 has argued that Archaeopteryx was a terrestrial, cursorial predator that represents a preflight stage in the origin of birds in which the forelimbs were used as nets to trap insects. So far, this has been challenged mainly on the grounds that such activity would have caused excessive feather wear4. The principal evidence for regarding Archaeopteryx as flightless, or at best an inept non-flapping glider, has come from interpretations of the structure of the pectoral girdle. The absence of an ossified sternum for attachment of flight muscles has long been cited. More recently, it has been argued that the structure of the coracoid of Archaeopteryx would not have permitted the supracoracoideus muscle to function as a wing elevator2,5. Because the asymmetrical remiges of Archaeopteryx prove that the wing had an aerodynamic function6, we now hope to show that neither of the preceding points precludes a capacity for powered flight in Archaeopteryx.
ALBANERPETONTIDS are a group of enigmatic salamander-like fossil amphibians known from deposits of middle Jurassic to Miocene age across Euramerica and Central Asia. Throughout a long history they remained remarkably conservative but can be diagnosed by a suite of unique derived character states, including an anterior peg-and-socket joint between the mandibles, non-pedicellate tricuspate teeth, a distinctive polygonal dermal sculpture pattern, and a two-part craniovertebral joint analogous to that of amniotes. Previous interpretations have placed albanerpetontids within salamanders1, 2 or as a separate amphibian group3, 4. We report here on the recovery of the first complete albanerpetontid specimens (including traces of skin and possible male courtship glands) from the early Cretaceous of Spain. The new material supports the interpretation of albanerpetontids as predominantly terrestrial animals. Albanerpetontids resemble salamanders only in retaining an unspecialized tailed body form; cladistic analysis suggests they represent a distinct lissamphibian lineage.
Scanning electron microscopy of feathers has revealed evidence that a
bacterial glycocalyx (a network of exocellular polysaccharide fibers)
played a role in promoting their fossilization in some cases. This mode
of preservation has not been reported in other soft tissues. The
majority of fossil feathers are preserved as carbonized traces. More
rarely, bacteria on the surface are replicated by authigenic minerals
(bacterial autolithification). The feathers of Archaeopteryx are
preserved mainly by imprintation following early lithification of the
substrate and decay of the feather. Lacustrine settings provide the most
important taphonomic window for feather preservation. Preservation in
terrestrial and normal-marine settings involves very different processes
(in amber and in authigenically mineralized coprolites, respectively).
Therefore, there may be a significant bias in the avian fossil record in
favor of inland water habitats.
The avian wrist is extraordinarily adapted for flight. Its intricate osteology is constructed to perform four very different, but extremely important, flight-related functions. (1) Throughout the downstroke, the cuneiform transmits force from the carpometacarpus to the ulna and prevents the manus from hyperpronating. (2) While gliding or maneuvering, the scapholunar interlocks with the carpometacarpus and prevents the manus from supinating. By employing both carpal bones simultaneously birds can lock the manus into place during flight. (3) Throughout the downstroke-upstroke transition, the articular ridge on the distal extremity of the ulna, in conjuction with the cuneiform, guides the manus from the plane of the wing toward the body. (4) During take-off or landing, the upstroke of some heavy birds exhibits a pronounced flick of the manus. The backward component of this flick is produced by reversing the wrist mechanism that enables the manus to rotate toward the body during the early upstroke. The upward component of the flick is generated by mechanical interplay between the ventral ramus of the cuneiform, the ventral ridge of the carpometacarpus, and the ulnocarpo-metacarpal ligament.
Without the highly specialized osteology of the wrist it is doubtful that birds would be able to carry out successfully the wing motions associated with flapping flight. Yet in Archaeopteryx, the wrist displays a very different morphology that lacks all the key features found in the modern avian wrist. Therefore, Archaeopteryx was probably incapable of executing the kinematics of modern avian powered flight.