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Osteohistology of the Lower Cretaceous Yixian Formation ornithuromorph (Aves) Iteravis huchzermeyeri

Jingmai K. O'Connor, Min Wang, Shuang Zhou, and Zhonghe Zhou

Plain Language Abstract

We conduct histological analysis of the bone tissue of the first Early Cretaceous ornithuromorph, a member of the derived lineage of birds that includes all living species. Previous histological analyses of Cretaceous ornithuromorphs basal to Ichthyornis (a fairly derived ornithurine ornithuromorph) were conducted on specimens younger by approximately 50 million years; these specimens retain lines of arrested growth (LAGs) indicating that these birds, similar to non-avian dinosaurs, required more than one year to reach skeletal maturity. In contrast, Ichthyornis and most living birds complete their growth within a year. Iteravis comes from the 128 Ma Yixian Formation in northeastern China, the second oldest geologic unit that preserves members of the Ornithuromorpha. The bone preserves no signs of arrested growth suggesting it reached adult size within a year. This indicates that the derived growth strategy arose early in the evolution of Ornithuromorpha but that some primitive lineages retained slow growth throughout their evolutionary history into the Late Cretaceous.

Resumen en Español

Osteohistología de Iteravis huchzermeyeri (Aves: Ornithuromorpha) de la Formación Yixian del Cretácico Inferior

Se describe por primera vez la histología de un ave del clado Ornithuromorpha del Grupo Jehol del Cretácico Inferior, revelando la estructura ósea de uno de los miembros más antiguos de este clado derivado. La localidad Sihedang recién descubierta de la Formación Yixian en el noreste de China conserva la más antigua avifauna dominada por ejemplares del clado Ornithuromorpha, considerando que todas las aves encontradas se atribuyen a un solo taxón, Iteravis huchzermeyeri. Estos ejemplares están preservados en un relativamente mayor grado de tridimensionalidad en comparación con los ejemplares Jehol de otras localidades. Se han tomado muestras de un ejemplar de Iteravis con el fin de testar la hipótesis de que esta asociación de aves representa una colonia de cría. Aunque se sabe que el hueso medular puede estar ocasionalmente conservado en tres dimensiones, este tejido óseo no estaba presente en las muestras histológicas. El espécimen es casi adulto de acuerdo a la fusión observada en el esqueleto, y la histología indica que se produjo expansión medular y que una capa interna circunferencial ya se había formado. Sin embargo, las líneas de crecimiento detenido están ausentes. En general, la histología ósea es comparable a la de Ichthyornis; esto es consistente con el emplazamiento filogenético derivado que se ha inferido para este nuevo taxón en relación con taxones basales del clado Ornithuromorpha previamente muestreados (Patagopteryx, Hollanda), todos los cuales indican que se requiere más de un año para llegar a la edad adulta. Esto sugiere que la estrategia moderna de crecimiento aviar se desarrolló en el Cretácico Inferior en aves no pertenecientes al clado Ornithurae.

Palabras clave: Jehol; matriz ósea; Ornithuromorpha; crecimiento; Sihedang

Traducción: Enrique Peñalver

Résumé en Français

Histologie osseuse de l'ornithuromorphe (Aves) Iteravis huchzermeyeri du Crétacé inférieur de la formation de Yixian

Nous décrivons pour la première fois l'histologie d'un oiseau ornithuromorphe provenant du Crétacé inférieur du groupe du Jehol, révélant la structure osseuse de l'un des plus anciens membres de ce clade dérivé. La nouvelle localité de Sihedang dans la formation de Yixian, située dans le nord-est de la Chine, conserve la plus ancienne avifaune dominée par des ornithuromorphes, avec tous les oiseaux collectés attribuables à un taxon unique, Iteravis huchzermeyeri. Ces spécimens sont tous conservés dans un degré relativement élevé de tridimensionnalité par rapport aux spécimens des autres localités du Jehol. Nous avons échantillonné un spécimen d'Iteravis afin de tester l'hypothèse selon laquelle cette accumulation d'oiseaux représenterait une colonie de reproduction. Bien que l'os médullaire soit connu pour faciliter la conservation en trois dimensions, ce tissu osseux n'était pas présent dans les échantillons histologiques. D'après la fusion du squelette, le spécimen est presque adulte, et l'histologie indique qu'une croissance médullaire s'était produite et qu'un système fondamental interne s'était déjà formé. Cependant, les lignes d'arrêt de croissance sont absentes. Dans l'ensemble, l'histologie osseuse est comparable à celle d'Ichtyornis. Cela est cohérent avec le placement phylogénétique dérivé estimé pour ce nouveau taxon par rapport aux ornithuromorphes basaux précédemment échantillonnés (Patagopteryx, Hollanda), ce qui indique qu'il leur fallait tous plus d'une année pour atteindre l'âge adulte. Cela suggère que la stratégie de croissance des oiseaux modernes a évolué pendant le Crétacé ancien chez des oiseaux n'appartenant pas aux Ornithurae.

Mots-clés : Jehol ; matrice osseuse ; Ornithuromorpha ; croissance ; Sihedang

Translator: Antoine Souron

Deutsche Zusammenfassung

Osteohistologie des Ornithuromorphen (Aves) Iteravis huchzermeyeri aus der unterkretazischen Yixian Formation

Wir beschreiben zum ersten Mal die Histologie eines ornithuromorphen Vogels aus der unterkretazischen Jehol-Gruppe und zeigen damit die Knochenstruktur eines der ältsten Mitglieder dieser abgeleiteten Klade. Die kürzlich entdeckte Sihedang Lokalität der Yixian Formation in Nordost-China bewahrt die älteste mit Ornithuromorphen dominierte Avifauna in der alle gesammelten Vögel einem einzigen Taxon zugehören, Iteravis huchzermeyeri. Diese Stücke sind alle etwas besser dreidimensional erhalten im Vergleich zu Jehol Stücken aus anderen Lokalitäten. Wir beprobten ein Stück von Iteravis um die Hypothese zu testen, dass diese Vogelansammlung möglicherweise eine Brutkolonie repräsentiert. Obwohl bekannt ist, dass Knochenmark eine dreidimensionale Erhaltung vereinfachen würde, war dieses Knochengewebe nicht in den histologischen Proben enthalten. Hinsichtlich der Knochenverschmelzung war das Stück nahezu adult und die Histologie weist darauf hin, dass der Markkanal expandiert war und eine innere umlaufende Schicht schon gebildet war. Allerdings sind keine gehemmten Wachstumslinien sichtbar. Allgemein ist die Knochenhistologie mit Ichthyornis vergleichbar. Dies ist konsistent mit der abgeleiteten phylogenetischen Platzierung, die für dieses neue Taxon angenommen wird, relativ zu vorherigen beprobten basalen Ornithuromorphen (Patagopteryx, Hollanda), bei denen alles darauf hindeutet, dass sie mehr als ein Jahr benötigen um das Erwachsenenalter zu erreichen. Dies weist darauf hin, dass sich die moderne Wachstumsstrategie der Vögel unter nicht-ornithurinen Vögeln in der Frühen Kreide entwickelte.

Schlüsselwörter: Jehol; Knochenmatrix; Ornithuromorpha; Wachstum; Sihedang

Translator: Eva Gebauer

Arabic

520 arab

Translator: Ashraf M.T. Elewa

 

 

author1Jingmai K. O'Connor
Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy of Sciences
Institute of Vertebrate Paleontology and Paleoanthropology
Chinese Academy of Sciences
142 Xizhimenwai Dajie
Beijing 100044
P.R. China 
This email address is being protected from spambots. You need JavaScript enabled to view it.

Conducted her undergraduate research on Cenozoic mammals with Dr. Xiaoming Wang (LACM) and Dr. Donald Prothero at Occidental College. Received her Ph.D. from the University of Southern California where she studied Mesozoic birds with Dr. Luis Chiappe (LACM). Currently working with Dr. Zhonghe Zhou as an Associate Professor at the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences in Beijing. Research interests include nearly all aspects of Mesozoic paravian biology including feathers, diet, reproduction as well as taxonomy, phylogeny and morphology.

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Min Wang
author2Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy of Sciences
Institute of Vertebrate Paleontology and Paleoanthropology
Chinese Academy of Sciences
142 Xizhimenwai Dajie
Beijing 100044
P.R. China 
This email address is being protected from spambots. You need JavaScript enabled to view it.

Received his B.A. in Paleontology and Stratigraphy from the School of Earth Sciences and Engineering of Nanjing University; received his Ph.D. from the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences. Currently working as an Associate Professor at the IVPP. Research interests include morphology, ontogeny, and phylogeny of Mesozoic birds with also some interest in Cenozoic avian fossils.

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author3Shuang Zhou
Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy of Sciences
Institute of Vertebrate Paleontology and Paleoanthropology
Chinese Academy of Sciences
142 Xizhimenwai Dajie
Beijing 100044
P.R. China
This email address is being protected from spambots. You need JavaScript enabled to view it.

Received her B.A. at Nankai University; received her M.S. and Ph.D. from the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences. Research is primarily on ornithuromorph birds from the Jehol. Currently working as editor of Vertebrata Palasiatica.

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author4Zhonghe Zhou
Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy of Sciences
Institute of Vertebrate Paleontology and Paleoanthropology
Chinese Academy of Sciences
142 Xizhimenwai Dajie
Beijing 100044
P.R. China
This email address is being protected from spambots. You need JavaScript enabled to view it.

Received his Masters degree from the Department of Geological Sciences, Graduate School of the Chinese University of Science and Technology before doing his Ph.D. at the University of Kansas studying Mesozoic birds with Dr. Larry Martin. Currently serving as director of the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences. Member of the National Academy of Sciences, U.S.A. and the Chinese Academy of Sciences.

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FIGURE 1. Simplified cladogram depicting relationships between specimens of Mesozoic birds that have been histologically sampled (modified from Zhou et al., 2014). Red indicates lineages in which rapid growth evolved; the dashed line for Confuciusornis is to indicate that although growing relatively faster than other basal birds, this taxon did not achieve growth rates comparable to derived members of the ornithuromorph lineage. Stages 1-5 (grey numbers) refer to important evolutionary transitions in basal bird bone microstructure: 1, bone shows increased vascularity and a primarily woven matrix but growth is non-continuous; 2, the Confuciusornis lineage evolves at least a period of post-natal growth in which fibro-lamellar bone is formed and growth lines are only found in the outermost cortex indicating these birds approached adult size within the first year; 3, at least one lineage of Late Cretaceous enantiornithines evolves a slow and protracted growth strategy; 4, fibro-lamellar bone matrix indicative of more rapid growth appears in ornithuromorphs but growth lines persist; 5, derived ornithuromorphs evolve uninterrupted growth. Abbreviations: FLB, fibro-lamellar bone; LAG, line of arrested growth; PFB, parallel fibered bone; WB, woven bone.

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FIGURE 2. Photograph of the holotype of Iteravis huchzermeyeri IVPP V18958 after sampling (indicated by white boxes); scale bar equals 2 centimeters.

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FIGURE 3. Histological sections taken from Iteravis huchzermeyeri IVPP V18958: 1, ulna; 2, tibiotarsus; 3, close up of denoted area of the ulna ; 4, close up of the contact with the endosteal layer under cross polarized light showing presence of lamellae; 5, close up of denoted area of the tibiotarsus; 6, close up of the tibiotarsus under cross polarized light showing the endosteal layer is parallel fibered. Abbreviations: c, simple canal; icl, inner circumferential layer; po, primary osteon.

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