Life and reproduction of titanosaurians: Isotopic hallmark of mid-palaeolatitude eggshells and its significance for body temperature, diet, and nesting
“…In this sense, it has also been suggested that many titanosaurs required specific conditions for nesting (e.g., at Sanagasta nesting site 11 , 19 ) and would have migrated in search of these peculiar nesting areas. Philopatric behaviour, in addition to other specific intrinsic and extrinsic characteristics, further supports the idea that titanosaurs were breeding migrants 25 . Figure 6 Model of events of titanosaur egg laying in two levels (L1 and L2), preservation, and subsequent sedimentation in the Ponte Alta nesting site.…”
Section: Discussionsupporting
confidence: 58%
“…Thus, these pores increase the pore area and could be a physiological response in those cases of pores clogged by sand grains allowing a continuous exchange of gases and maintaining a high diffusion. Moreover, this suggests an adaptive response to reproduction under relatively arid environmental conditions, a very common behaviour in mid-palaeolatitude titanosaurs 25 .…”
Section: Discussionmentioning
confidence: 79%
“…There is no unambiguous taxonomic certainty for these embryonic eggs, but it is likely that they belong to one of the two major groups of Late Cretaceous titanosaurs, namely Saltasauridae and Colossosauria 2 . The combination of palaeontological and sedimentological data from Argentinean sites, mainly in Patagonia and La Rioja Province, has provided crucial information on their palaeobiology, life history, physiology and embryology, reproductive strategies and nesting behaviours, as well as taphonomic and diagenetic processes associated with dinosaur eggs 11 , 16 , 18 – 25 . These titanosaur egg-clutches of up to 30 spherical eggs, about 12–18 cm in diameter, display a monolayered shell traditionally classified within Megaloolithidae, a parataxonomic group without any modern biological and evolutionary principles 11 .…”
Titanosaurs were successful herbivorous dinosaurs widely distributed in all continents during the Cretaceous, with the major diversity in South America. The success of titanosaurs was probably due to several physiological and ecological factors, in addition to a series of morphological traits they achieved during their evolutionary history. However, the generalist nesting behaviour using different palaeoenvironments and strategies was key to accomplish that success. Titanosaur nesting sites have been found extensively around the world, with notable records in Spain, France, Romania, India, and, especially, Argentina. Here, we describe the first titanosaur nesting site from the Late Cretaceous of Brazil that represents the most boreal nesting site for South America. Several egg-clutches, partially preserved, isolated eggs and many eggshell fragments were discovered in an Inceptisol palaeosol profile of the mining Lafarge Quarry, at the Ponte Alta District (Uberaba Municipality, Minas Gerais State), corresponding to the Serra da Galga Formation (Bauru Group, Bauru Basin). Although classical mechanical preparation and CT scans have not revealed embryonic remains in ovo, the eggs and eggshell features match those eggs containing titanosaurian embryos found worldwide. The morphology of the egg-clutches and observations of the sedimentary characteristics bolster the hypothesis that these sauropods were burrow-nester dinosaurs, as was already suggested for the group based on other nesting sites. The egg-clutches distributed in two levels along the Lafarge outcrops, together with the geopalaeontological data collected, provide clear evidence for the first colonial nesting and breeding area of titanosaur dinosaurs in Brazil.
“…In this sense, it has also been suggested that many titanosaurs required specific conditions for nesting (e.g., at Sanagasta nesting site 11 , 19 ) and would have migrated in search of these peculiar nesting areas. Philopatric behaviour, in addition to other specific intrinsic and extrinsic characteristics, further supports the idea that titanosaurs were breeding migrants 25 . Figure 6 Model of events of titanosaur egg laying in two levels (L1 and L2), preservation, and subsequent sedimentation in the Ponte Alta nesting site.…”
Section: Discussionsupporting
confidence: 58%
“…Thus, these pores increase the pore area and could be a physiological response in those cases of pores clogged by sand grains allowing a continuous exchange of gases and maintaining a high diffusion. Moreover, this suggests an adaptive response to reproduction under relatively arid environmental conditions, a very common behaviour in mid-palaeolatitude titanosaurs 25 .…”
Section: Discussionmentioning
confidence: 79%
“…There is no unambiguous taxonomic certainty for these embryonic eggs, but it is likely that they belong to one of the two major groups of Late Cretaceous titanosaurs, namely Saltasauridae and Colossosauria 2 . The combination of palaeontological and sedimentological data from Argentinean sites, mainly in Patagonia and La Rioja Province, has provided crucial information on their palaeobiology, life history, physiology and embryology, reproductive strategies and nesting behaviours, as well as taphonomic and diagenetic processes associated with dinosaur eggs 11 , 16 , 18 – 25 . These titanosaur egg-clutches of up to 30 spherical eggs, about 12–18 cm in diameter, display a monolayered shell traditionally classified within Megaloolithidae, a parataxonomic group without any modern biological and evolutionary principles 11 .…”
Titanosaurs were successful herbivorous dinosaurs widely distributed in all continents during the Cretaceous, with the major diversity in South America. The success of titanosaurs was probably due to several physiological and ecological factors, in addition to a series of morphological traits they achieved during their evolutionary history. However, the generalist nesting behaviour using different palaeoenvironments and strategies was key to accomplish that success. Titanosaur nesting sites have been found extensively around the world, with notable records in Spain, France, Romania, India, and, especially, Argentina. Here, we describe the first titanosaur nesting site from the Late Cretaceous of Brazil that represents the most boreal nesting site for South America. Several egg-clutches, partially preserved, isolated eggs and many eggshell fragments were discovered in an Inceptisol palaeosol profile of the mining Lafarge Quarry, at the Ponte Alta District (Uberaba Municipality, Minas Gerais State), corresponding to the Serra da Galga Formation (Bauru Group, Bauru Basin). Although classical mechanical preparation and CT scans have not revealed embryonic remains in ovo, the eggs and eggshell features match those eggs containing titanosaurian embryos found worldwide. The morphology of the egg-clutches and observations of the sedimentary characteristics bolster the hypothesis that these sauropods were burrow-nester dinosaurs, as was already suggested for the group based on other nesting sites. The egg-clutches distributed in two levels along the Lafarge outcrops, together with the geopalaeontological data collected, provide clear evidence for the first colonial nesting and breeding area of titanosaur dinosaurs in Brazil.
“…Palaeoenvironmental information can be acquired from eggshells ( Stern et al, 1994 ; Angst et al, 2015 ; Montanari, 2018 ; Niespolo et al, 2020 ; Niespolo et al, 2021 ; Leuzinger et al, 2021 ). Because Cenozoic palaeoenvironmental or geological events that might have influenced the evolution of Palaeognathae are comparatively well understood ( Mitchell et al, 2014 ; Claramunt and Cracraft, 2015 ; Grealy et al, 2017 ; Yonezawa et al, 2017 ; Crouch and Clarke, 2019 ; Figure 13 ), further analytical investigation on Cenozoic palaeognath eggshells with proper geological and climatological contexts may shed light on the palaeoenvironmental settings of fossil localities and their effects in the evolution of Palaeognathae and its eggshells.…”
The avian palaeognath phylogeny has been recently revised significantly due to the advancement of genome-wide comparative analyses and provides the opportunity to trace the evolution of the microstructure and crystallography of modern dinosaur eggshells. Here, eggshells of all major clades of Palaeognathae (including extinct taxa) and selected eggshells of Neognathae and non-avian dinosaurs are analysed with electron backscatter diffraction. Our results show the detailed microstructures and crystallographies of (previously) loosely categorized ostrich-, rhea-, and tinamou-style morphotypes of palaeognath eggshells. All rhea-style eggshell appears homologous, while respective ostrich-style and tinamou-style morphotypes are best interpreted as homoplastic morphologies (independently acquired). Ancestral state reconstruction and parsimony analysis additionally show that rhea-style eggshell represents the ancestral state of palaeognath eggshells both in microstructure and crystallography. The ornithological and palaeontological implications of the current study are not only helpful for the understanding of evolution of modern and extinct dinosaur eggshells, but also aid other disciplines where palaeognath eggshells provide useful archive for comparative contrasts (e.g. palaeoenvironmental reconstructions, geochronology, and zooarchaeology).
“…With respect to thermophysiology, recent studies suggest the presence of high metabolic rates in most dinosaurs ( 18 , 30 ), but estimates of absolute body temperature are required to understand their thermoregulatory strategy. Clumped isotope thermometry (i.e., measurement of Δ 47 , which allows reconstruction of carbonate precipitation temperature without prior knowledge of the original fluid isotopic composition) has already been used to reconstruct dinosaur body temperatures ( 19 , 31 – 35 ). Specifically, studies on non-avian theropods indicate that some might have possessed body temperatures lower than modern birds but higher than ambient temperature, while others might have possessed body temperature very close to those of birds ( 19 , 31 , 34 ).…”
The dinosaur–bird transition involved several anatomical, biomechanical, and physiological modifications of the theropod bauplan. Non-avian maniraptoran theropods, such as
Troodon
, are key to better understand changes in thermophysiology and reproduction occurring during this transition. Here, we applied dual clumped isotope (Δ
47
and Δ
48
) thermometry, a technique that resolves mineralization temperature and other nonthermal information recorded in carbonates, to eggshells from
Troodon
, modern reptiles, and modern birds.
Troodon
eggshells show variable temperatures, namely 42 and 29 ± 2 °C, supporting the hypothesis of an endothermic thermophysiology with a heterothermic strategy for this extinct taxon. Dual clumped isotope data also reveal physiological differences in the reproductive systems between
Troodon
, reptiles, and birds.
Troodon
and modern reptiles mineralize their eggshells indistinguishable from dual clumped isotope equilibrium, while birds precipitate eggshells characterized by a positive disequilibrium offset in Δ
48
. Analyses of inorganic calcites suggest that the observed disequilibrium pattern in birds is linked to an amorphous calcium carbonate (ACC) precursor, a carbonate phase known to accelerate eggshell formation in birds. Lack of disequilibrium patterns in reptile and
Troodon
eggshells implies these vertebrates had not acquired the fast, ACC-based eggshell calcification process characteristic of birds. Observation that
Troodon
retained a slow reptile-like calcification suggests that it possessed two functional ovaries and was limited in the number of eggs it could produce; thus its large clutches would have been laid by several females. Dual clumped isotope analysis of eggshells of extinct vertebrates sheds light on physiological information otherwise inaccessible in the fossil record.
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