Histological evidence for a supraspinous ligament in sauropod dinosaurs

Supraspinous ossified rods have been reported in the sacra of some derived sauropod dinosaurs. Although different hypotheses have been proposed to explain the origin ofthis structure, histological evidence has never been provided to support or reject any of them. In order to establish its origin, we analyse and characterize the microstructure of thesupraspinous rod of two sauropod dinosaurs from the Upper Cretaceous of Argentina. The supraspinous ossified rod is almost entirely formed by dense Haversian bone. Remains ofprimary bone consist entirely of an avascular tissue composed of two types of fibre-like structures, which are coarse and longitudinally (parallel to the main axis of the element) oriented. These structures are differentiated on the basis of their optical properties under polarized light. Very thin fibrous strands are also observed in some regions. These small fibres are all oriented parallel to one another but perpendicular to the element main axis. Histological features of the primary bone tissue indicate that the sacral supraspinous rod corresponds to an ossified supraspinous ligament. The formation of this structure appears to have been a non-pathological metaplastic ossification, possibly induced by the continuous tensile forces applied to the element.Fil: Cerda, Ignacio Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigación en Paleobiología y Geología; Argentina. Universidad Nacional de Río Negro; ArgentinaFil: Casal, Gabriel. Universidad Nacional de la Patagonia; ArgentinaFil: Martínez, Rubén Darío. Universidad Nacional de la Patagonia ; ArgentinaFil: Ibiricu, Lucio Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentin

Bone histology sheds new light on the ecology of the dodo (Raphus cucullatus, Aves, Columbiformes)

Abstract The dodo, Raphus cucullatus, a flightless pigeon endemic to Mauritius, became extinct during the 17th century due to anthropogenic activities. Although it was contemporaneous with humans for almost a century, little was recorded about its ecology. Here we present new aspects of the life history of the dodo based on our analysis of its bone histology. We propose that the dodo bred around August and that the rapid growth of the chicks enabled them to reach a robust size before the austral summer or cyclone season. Histological evidence of molting suggests that after summer had passed, molt began in the adults that had just bred; the timing of molt derived from bone histology is also corroborated by historical descriptions of the dodo by mariners. This research represents the only bone histology analysis of the dodo and provides an unprecedented insight into the life history of this iconic bird

Bone remodeling in the longest living rodent, the naked mole-rat : interelement variation and the effects of reproduction

The pattern of bone remodeling of one of the most peculiar mammals in the world, the naked mole-rat (NMR), was assessed. NMRs are known for their long lifespans among rodents and for having low metabolic rates. We assessed long-term in vivo bone labeling of subordinate individuals, as well as the patterns of bone resorption and bone remodeling in a large sample including reproductive and non-reproductive individuals (n = 70). Over 268 undecalcified thin cross-sections from the midshaft of humerus, ulna, femur and tibia were analyzed with confocal fluorescence and polarized light microscopy. Fluorochrome analysis revealed low osteogenesis, scarce bone resorption and infrequent formation of secondary osteons (Haversian systems) (i.e., slow bone turnover), thus most likely reflecting the low metabolic rates of this species. Secondary osteons occurred regardless of reproductive status. However, considerable differences in the degree of bone remodeling were found between breeders and non-breeders. Pre-reproductive stages (subordinates) exhibited quite stable skeletal homeostasis and bone structure, although the attainment of sexual maturity and beginning of reproductive cycles in female breeders triggered a series of anabolic and catabolic processes that up-regulate bone turnover, most likely associated with the increased metabolic rates of reproduction. Furthermore, bone remodeling was more frequently found in stylopodial elements compared to zeugopodial elements. Despite the limited bone remodeling observed in NMRs, the variation in the pattern of skeletal homeostasis (interelement variation) reported here represents an important aspect to understand the skeletal dynamics of a small mammal with low metabolic rates. Given the relevance of the remodeling process among mammals, this study also permitted the comparison of such process with the well-documented histomorphology of extinct therapsids (i.e., mammalian precursors), thus evidencing that bone remodeling and its endocortical compartmentalization represent ancestral features among the lineage that gave rise to mammals. It is concluded that other factors associated with development (and not uniquely related to biomechanical loading) can also have an important role in the development of bone remodeling.CONICYT; National Research Foundation and DST-NRF.http://www.wileyonlinelibrary.com/journal/joahj2022Mammal Research InstituteZoology and Entomolog

Was Dinosaurian Physiology Inherited by Birds? Reconciling Slow Growth in Archaeopteryx

Archaeopteryx is the oldest and most primitive known bird (Avialae). It is believed that the growth and energetic physiology of basalmost birds such as Archaeopteryx were inherited in their entirety from non-avialan dinosaurs. This hypothesis predicts that the long bones in these birds formed using rapidly growing, well-vascularized woven tissue typical of non-avialan dinosaurs. We report that Archaeopteryx long bones are composed of nearly avascular parallel-fibered bone. This is among the slowest growing osseous tissues and is common in ectothermic reptiles. These findings dispute the hypothesis that non-avialan dinosaur growth and physiology were inherited in totality by the first birds. Examining these findings in a phylogenetic context required intensive sampling of outgroup dinosaurs and basalmost birds. Our results demonstrate the presence of a scale-dependent maniraptoran histological continuum that Archaeopteryx and other basalmost birds follow. Growth analysis for Archaeopteryx suggests that these animals showed exponential growth rates like non-avialan dinosaurs, three times slower than living precocial birds, but still within the lowermost range for all endothermic vertebrates. The unexpected histology of Archaeopteryx and other basalmost birds is actually consistent with retention of the phylogenetically earlier paravian dinosaur condition when size is considered. The first birds were simply feathered dinosaurs with respect to growth and energetic physiology. The evolution of the novel pattern in modern forms occurred later in the group's history

The Ontogenetic Osteohistology of Tenontosaurus tilletti

Tenontosaurus tilletti is an ornithopod dinosaur known from the Early Cretaceous (Aptian-Albian) Cloverly and Antlers formations of the Western United States. It is represented by a large number of specimens spanning a number of ontogenetic stages, and these specimens have been collected across a wide geographic range (from central Montana to southern Oklahoma). Here I describe the long bone histology of T. tilletti and discuss histological variation at the individual, ontogenetic and geographic levels. The ontogenetic pattern of bone histology in T. tilletti is similar to that of other dinosaurs, reflecting extremely rapid growth early in life, and sustained rapid growth through sub-adult ontogeny. But unlike other iguanodontians, this dinosaur shows an extended multi-year period of slow growth as skeletal maturity approached. Evidence of termination of growth (e.g., an external fundamental system) is observed in only the largest individuals, although other histological signals in only slightly smaller specimens suggest a substantial slowing of growth later in life. Histological differences in the amount of remodeling and the number of lines of arrested growth varied among elements within individuals, but bone histology was conservative across sampled individuals of the species, despite known paleoenvironmental differences between the Antlers and Cloverly formations. The bone histology of T. tilletti indicates a much slower growth trajectory than observed for other iguanodontians (e.g., hadrosaurids), suggesting that those taxa reached much larger sizes than Tenontosaurus in a shorter time

Breeding young as a survival strategy during earth’s greatest mass extinction

Studies of the effects of mass extinctions on ancient ecosystems have focused on changes in taxic diversity, morphological disparity, abundance, behaviour and resource availability as key determinants of group survival. Crucially, the contribution of life history traits to survival during terrestrial mass extinctions has not been investigated, despite the critical role of such traits for population viability. We use bone microstructure and body size data to investigate the palaeoecological implications of changes in life history strategies in the therapsid forerunners of mammals before and after the Permo-Triassic Mass Extinction (PTME), the most catastrophic crisis in Phanerozoic history. Our results are consistent with truncated development, shortened life expectancies, elevated mortality rates and higher extinction risks amongst post-extinction species. Various simulations of ecological dynamics indicate that an earlier onset of reproduction leading to shortened generation times could explain the persistence of therapsids in the unpredictable, resource-limited Early Triassic environments, and help explain observed body size distributions of some disaster taxa (e.g., Lystrosaurus). Our study accounts for differential survival in mammal ancestors after the PTME and provides a methodological framework for quantifying survival strategies in other vertebrates during major biotic crises

Unusually thick dinosaur eggshell fragments from the Spanish Late Cretaceous

[EN] Fieldwork carried out recently in the southeastern branch of the Iberian Range (Valencia Province, Spain) has led to the collection of a large volume of dinosaur eggshell fragments of unusual thickness. These specimens, up to 4.9 mm thick, were recovered from palustrine grey marls of the upper Campanian-lower Maastrichtian Sierra Perenchiza Formation, which comprises a wetland paleoenvironment deposit. These eggshell fragments have a characteristic compactituberculate ornamentation, dinosauroid-spherulitic organisation, and exhibit a complex canaliculate respiratory system. The external tuberculate surface of the shell as well as the internal microstructure enable referral to Megaloolithus aff. siruguei, the most common megaloolithid oospecies known from the Iberian Peninsula and southern France. The biostratigraphic range of M. siruguei matches the temporal distribution of titanosaurid dinosaurs across the Iberian Range, tentatively considered to be potential producers.This work was supported by the Ministerio de Economia y Competitividad of Spain [Secretaria de Estado de Investigacion, Desarrollo e Innovacion, projects CGL2013-47521-P and CGL2014-53548-P]Company Rodríguez, J. (2017). Unusually thick dinosaur eggshell fragments from the Spanish Late Cretaceous. Historical Biology (Online). 31(2):203-210. https://doi.org/10.1080/08912963.2017.1357717S203210312Allain, R., & Suberbiola, X. P. (2003). Dinosaurs of France. Comptes Rendus Palevol, 2(1), 27-44. doi:10.1016/s1631-0683(03)00002-2Bravo, A. M., & Gaete, R. (2014). Titanosaur eggshells from the Tremp Formation (Upper Cretaceous, Southern Pyrenees, Spain). Historical Biology, 27(8), 1079-1089. doi:10.1080/08912963.2014.934231Canudo, J. I., Oms, O., Vila, B., Galobart, À., Fondevilla, V., Puértolas-Pascual, E., … Blanco, A. (2016). The upper Maastrichtian dinosaur fossil record from the southern Pyrenees and its contribution to the topic of the Cretaceous–Palaeogene mass extinction event. Cretaceous Research, 57, 540-551. doi:10.1016/j.cretres.2015.06.013Cruzado-Caballero, P., Ruiz-Omeñaca, J. I., Gaete, R., Riera, V., Oms, O., & Canudo, J. I. (2013). A new hadrosaurid dentary from the latest Maastrichtian of the Pyrenees (north Spain) and the high diversity of the duck-billed dinosaurs of the Ibero-Armorican Realm at the very end of the Cretaceous. Historical Biology, 26(5), 619-630. doi:10.1080/08912963.2013.822867Chiappe, L. M., Coria, R. A., Dingus, L., Jackson, F., Chinsamy, A., & Fox, M. (1998). Sauropod dinosaur embryos from the Late Cretaceous of Patagonia. Nature, 396(6708), 258-261. doi:10.1038/24370Company J. 2004. Vertebrados continentales del Cretácico superior (Campaniense-Maastrichtiense) de Valencia [PhD dissertation]. Valencia: Universidad de Valencia.Company, J., & Szentesi, Z. (2012). Amphibians from the Late Cretaceous Sierra Perenchiza Formation of the Chera Basin, Valencia Province, Spain. Cretaceous Research, 37, 240-245. doi:10.1016/j.cretres.2012.04.003Csiki-Sava, Z., Buffetaut, E., Ősi, A., Pereda-Suberbiola, X., & Brusatte, S. L. (2015). Island life in the Cretaceous - faunal composition, biogeography, evolution, and extinction of land-living vertebrates on the Late Cretaceous European archipelago. ZooKeys, 469, 1-161. doi:10.3897/zookeys.469.8439Erben, H. K., Hoefs, J., & Wedepohl, K. H. (1979). Paleobiological and isotopic studies of eggshells from a declining dinosaur species. Paleobiology, 5(4), 380-414. doi:10.1017/s0094837300016900García, R. A. (2007). An «egg-tooth»–like structure in titanosaurian sauropod embryos. Journal of Vertebrate Paleontology, 27(1), 247-252. doi:10.1671/0272-4634(2007)27[247:aesits]2.0.co;2Garcia, G., & Vianey-Liaud, M. (2001). Dinosaur eggshells as biochronological markers in Upper Cretaceous continental deposits. Palaeogeography, Palaeoclimatology, Palaeoecology, 169(1-2), 153-164. doi:10.1016/s0031-0182(01)00215-2Grellet-Tinner, G., Chiappe, L. M., & Coria, R. (2004). Eggs of titanosaurid sauropods from the Upper Cretaceous of Auca Mahuevo (Argentina). Canadian Journal of Earth Sciences, 41(8), 949-960. doi:10.1139/e04-049Grigorescu, D., Garcia, G., Csiki, Z., Codrea, V., & Bojar, A.-V. (2010). Uppermost Cretaceous megaloolithid eggs from the Haţeg Basin, Romania, associated with hadrosaur hatchlings: Search for explanation. Palaeogeography, Palaeoclimatology, Palaeoecology, 293(3-4), 360-374. doi:10.1016/j.palaeo.2010.03.031Izquierdo LA, Montero D, Pérez G, Urién V, Meijide M. 2001. Macroestructura de huevos de dinosaurios en el Cretácico superior de “La Rosaca” (Burgos, España). Actas de las I Jornadas Internacionales Sobre Paleontología de Dinosaurios y su Entorno. Ed. Colectivo Arqueológico y Paleontológico de Salas. Salas de los Infantes. p. 389–395.Jackson FD. 2007. Titanosaur reproductive biology: comparison of the Auca Mahuevo Titanosaur nesting locality (Argentina), to the Pinyes Megaloolithus nesting locality (Spain) [PhD dissertation]. Bozeman (MT): Montana State University.Jackson, F. D., Garrido, A., Schmitt, J. G., Chiappe, L. M., Dingus, L., & Loope, D. B. (2004). Abnormal, multilayered titanosaur (Dinosauria: Sauropoda) eggs from in situ clutches at the Auca Mahuevo locality, Neuquen Province, Argentina. Journal of Vertebrate Paleontology, 24(4), 913-922. doi:10.1671/0272-4634(2004)024[0913:amtdse]2.0.co;2Jackson, F. D., Varricchio, D. J., Jackson, R. A., Vila, B., & Chiappe, L. M. (2008). Comparison of water vapor conductance in a titanosaur egg from the Upper Cretaceous of Argentina and a Megaloolithus siruguei egg from Spain. Paleobiology, 34(2), 229-246. doi:10.1666/0094-8373(2008)034[0229:cowvci]2.0.co;2López-Martı́nez, N., Moratalla, J. J., & Sanz, J. L. (2000). Dinosaurs nesting on tidal flats. Palaeogeography, Palaeoclimatology, Palaeoecology, 160(1-2), 153-163. doi:10.1016/s0031-0182(00)00063-8Mohabey, D. M. (1998). Systematics of Indian Upper Cretaceous dinosaur and chelonian eggshells. Journal of Vertebrate Paleontology, 18(2), 348-362. doi:10.1080/02724634.1998.10011063Moratalla JJ. 1993. Restos indirectos de dinosaurios del registro español: paleoicnología de la Cuenca de (Jurásico superior-Cretácico inferior) y paleoología del Cretácico superior [PhD dissertation]. Madrid: Universidad Autónoma de Madrid.Moreno-Azanza, M., Bauluz, B., Canudo, J. I., Gasca, J. M., & Torcida Fernández-Baldor, F. (2016). Combined Use of Electron and Light Microscopy Techniques Reveals False Secondary Shell Units in Megaloolithidae Eggshells. PLOS ONE, 11(5), e0153026. doi:10.1371/journal.pone.0153026Moreno-Azanza, M., Bauluz, B., Canudo, J. I., Puértolas-Pascual, E., & Sellés, A. G. (2013). A re-evaluation of aff. Megaloolithidae eggshell fragments from the uppermost Cretaceous of the Pyrenees and implications for crocodylomorph eggshell structure. Historical Biology, 26(2), 195-205. doi:10.1080/08912963.2013.786067Oms, O., Dinarès-Turell, J., Vicens, E., Estrada, R., Vila, B., Galobart, À., & Bravo, A. M. (2007). Integrated stratigraphy from the Vallcebre Basin (southeastern Pyrenees, Spain): New insights on the continental Cretaceous−Tertiary transition in southwest Europe. Palaeogeography, Palaeoclimatology, Palaeoecology, 255(1-2), 35-47. doi:10.1016/j.palaeo.2007.02.039Ortega, F., Bardet, N., Barroso-Barcenilla, F., Callapez, P. M., Cambra-Moo, O., Daviero- Gómez, V., … Sanz, J. L. (2015). 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First Evidence of Dinosaurian Secondary Cartilage in the Post-Hatching Skull of Hypacrosaurus stebingeri (Dinosauria, Ornithischia)

Bone and calcified cartilage can be fossilized and preserved for hundreds of millions of years. While primary cartilage is fairly well studied in extant and fossilized organisms, nothing is known about secondary cartilage in fossils. In extant birds, secondary cartilage arises after bone formation during embryonic life at articulations, sutures and muscular attachments in order to accommodate mechanical stress. Considering the phylogenetic inclusion of birds within the Dinosauria, we hypothesized a dinosaurian origin for this “avian” tissue. Therefore, histological thin sectioning was used to investigate secondary chondrogenesis in disarticulated craniofacial elements of several post-hatching specimens of the non-avian dinosaur Hypacrosaurus stebingeri (Ornithischia, Lambeosaurinae). Secondary cartilage was found on three membrane bones directly involved with masticatory function: (1) as nodules on the dorso-caudal face of a surangular; and (2) on the bucco-caudal face of a maxilla; and (3) between teeth as islets in the alveolar processes of a dentary. Secondary chondrogenesis at these sites is consistent with the locations of secondary cartilage in extant birds and with the induction of the cartilage by different mechanical factors - stress generated by the articulation of the quadrate, stress of a ligamentous or muscular insertion, and stress of tooth formation. Thus, our study reveals the first evidence of “avian” secondary cartilage in a non-avian dinosaur. It pushes the origin of this “avian” tissue deep into dinosaurian ancestry, suggesting the creation of the more appropriate term “dinosaurian” secondary cartilage