First evidence of reproductive adaptation to "Island effect" of a Dwarf Cretaceous Romanian titanosaur, with embryonic integument in Ovo

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Grellet Tinner, Gerald ^a,b,c   Codrea, Vlad ^d   Folie, Annelise ^e   Higa, Alessandra ^f   Smith, Thierry ^e  

^a FIELD MUSEUM OF NATURAL HISTORY   (United States)

^b The Journey Museum   (United States)

^c Centro Regional de Investigaciones Cientificas y Transferencia Tecnologia   (Argentina)

^d BABE BOLYAI UNIVERSITY   (Romania)

^e ROYAL BELGIAN INSTITUTE OF NATURAL SCIENCES   (Belgium)

^f Oglala Lakota College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOMINERALIZATION; BODY SIZE; CLUTCH SIZE; CONTROLLED STUDY; CRETACEOUS; EMBRYO DEVELOPMENT; EVOLUTIONARY ADAPTATION; INTEGUMENT; NESTING; NONHUMAN; ORGANOGENESIS; OSSIFICATION; PHILOPATRY; PHYLOGEOGRAPHY; SCANNING ELECTRON MICROSCOPY; SPECIES IDENTIFICATION; TAXONOMIC IDENTIFICATION; TISSUE PRESERVATION; TITANOSAUR; ADAPTATION; ANIMAL; DINOSAUR; EGG SHELL; FOSSIL; HISTOLOGY; PHYSIOLOGY; REPRODUCTION; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); DINOSAURIA; NEMEGTOSAURIDAE; SPONDIAS PURPUREA; VERTEBRATA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CLUTCH SIZE; DINOSAURS; EGG SHELL; FOSSILS; REPRODUCTION;

EID: 84857806165     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032051     Document Type: Article

References (82)

1. Csontos L, Vörös A, (2004) Mesozoic plate tectonic reconstruction of the Carpathian region. Palaeogeogr Palaeoclimateol Palaeoecol 210: 1-56.
2. Benton MJ, Csiki Z, Grigorescu D, Redelstorff R, Sander PM, et al. (2010) Dinosaurs and the island rule: The dwarfed dinosaurs from Haţeg Island. Palaeogeogr Palaeoclimateol Palaeoecol 293: 438-454.
3. Csiki Z, Vremir M, Brusatte SL, Norell MA, (2010) An aberrant island-dwelling theropod dinosaur from the Late Cretaceous of Romania. Proc Natl Acad Sci USA 107: 15357-15361.
4. Stein K, Csiki Z, Curry Rogers K, Weishampel DB, Redelstorff R, et al. (2010) Small body size and extreme cortical bone remodeling indicate phyletic dwarfism in Magyarosaurus dacus (Sauropoda: Titanosauria). Proc Natl Acad Sci USA 107: 9258-9263.
5. Csiki Z, Codrea V, Jipa-Murzea C, Godefroit P, (2010) A partial titanosaur (Sauropoda, Dinosauria) skeleton from the Maastrichtian of Nǎlaţ-Vad, Haţeg Basin, Romania. Neues Jahrb Geol Palaontol Abh 258: 297-324.
6. Nopcsa F, (1915) Die Dinosaurier der siebenbürgischen Landesteile Ungarns. Mitt Jahr Konig-Ungar Geol Reichs 23: 1-24.
7. Csiki Z, (1999) New evidence of armoured titanosaurids in the Late Cretaceous - Magyarosaurus dacus from the Haţeg Basin (Romania). Oryctos 2: 93-99.
8. Upchurch P, Barrett PM, Dodson P, (2004) Sauropoda. In: Weishampel DB, Dodson P, Osmólska H, editors. The Dinosauria, Second Edition Berkeley University of California Press pp. 259-322.
9. Grigorescu D, (2010) The Latest Cretaceous fauna with dinosaurs and mammals from the Haţeg Basin - A historical overview. Palaeogeogr Palaeoclimateol Palaeoecol 293: 271-282.
10. Zaher H, Pol D, Carvalho AB, Nascimento PM, Riccomini C, et al. (2011) A complete Skull of an Early Cretaceous sauropod and the evolution of advanced titanosaurians. PLoS ONE 6: e16663 doi:10.1371/journal.pone.0016663.
11. Grellet-Tinner G, Sim CM, Kim DH, Trimby P, Higa A, et al. (2011) Description of the first lithostrotian titanosaur embryo in ovo with Neutron characterization and implications for lithostrotian Aptian migration and dispersion. Gondwana Res 20: 621-629.
12. Grellet-Tinner G, Fiorelli LE, (2010) A new Argentinean nesting site showing neosauropod dinosaur reproduction in a Cretaceous hydrothermal environment. Nat Com 1: 32 doi:10.1038/ncomms1031.
13. Grigorescu D, (2010) The "Tustea Puzzle": Hadrosaurid (Dinosauria, Ornithopoda) hatchlings associated with Megaloolithidae eggs in the Maastrichtian of Hateg Basin (Romania). Ameghiniana 47: 89-97.
14. Grigorescu 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. Palaeogeogr Palaeoclimateol Palaeoecol 293: 360-374.
15. Grigorescu D, (2005) Rediscovery of a "forgotten land": The last three decades of research on the dinosaur-bearing deposits from the Haţeg Basin. Acta Paleontol Rom 5: 191-204.
16. Codrea V, Smith T, Dica P, Folie A, Garcia G, et al. (2002) Dinosaur egg nests, mammals and other vertebrates from a new Maastrichtian site of the Haţeg Basin (Romania). CR Palevol 1: 173-180.
17. Wilby PR, Briggs DEG, (1997) Taxonomic trends in the resolution of detail preserved in fossil phosphatized soft tissues. Geobios-Lyon 20: 493-502.
18. Briggs DEG, (2003) The role of decay and mineralization in the preservation of soft-bodied fossils. Annu Rev Earth Pl Sc 31: 275-301.
19. Gupta NS, Cambra-Moo O, Briggs DEG, Love GD, Fregenal-Martinez MA, et al. (2008) Molecular taphonomy of macrofossils from the Cretaceous Las Hoyas Formation, Spain. Cretaceous Res 29: 1-8.
20. Grellet-Tinner G, (2005) The membrana testacea of titanosaurid dinosaur eggs from Auca Mahuevo (Argentina): Implications for the exceptional preservation of soft tissue in Lagerstätten. J Vertebr Paleontol 25: 99-106.
21. Gheerbrant E, Rage J-C, (2006) Paleobiogeography of Africa: How distinct from Gondwana and Laurasia? Palaeogeogr Palaeoclimateol Palaeoecol 241: 224-246.
22. Van Itterbeeck J, Markevich VS, Codrea V, (2005) Palynostratigraphy of the Maastrichtian dinosaur- and mammal sites of the Râul Mare and Barbat Valleys (Haţeg Basin, Romania). Geol Carpath 56: 137-147.
23. Bojar A-V, Halas S, Bojar H-G, Grigorescu D, Vasile S, (2011) Upper Cretaceous volcanoclastic deposits from the Haţeg Basin, South Carpathians (Romania): K-Ar ages and intrabasinal correlation. Geochronometria 38: 182-188.
24. Van Itterbeeck J, Sǎsǎran E, Codrea V, Sǎsǎran L, Bultynck P, (2004) Sedimentology of the Upper Cretaceous mammal- and dinosaur-bearing sites along the Râul Mare and Barbat rivers, Haţeg Basin, Romania. Cretaceous Res 25: 517-530.
25. Smith T, Codrea V, Sǎsǎran E, Van Itterbeeck J, Bultynck P, et al. (2002) A new exceptional vertebrate site from the Late Cretaceous of the Haţeg Basin (Romania). Stud Univ Babes-Bolyai Geol, Special Issue 1: 321-330.
26. Grellet-Tinner G, Chiappe L, Coria R, (2004) Eggs of titanosaurid sauropods from the Upper Cretaceous of Auca Mahuevo (Argentina). Can J Earth Sci 41: 949-960.
27. Grellet-Tinner G, (2000) Phylogenetic interpretation of eggs and eggshells. In: Bravo AM, Reyes T, editors. First International Symposium on Dinosaur Eggs and Babies Spain Isona I Conca Dellà Catalonia pp. 61-75.
28. Grellet-Tinner G, (2006) Phylogenetic interpretation of eggs and eggshells: Implications for phylogeny of Paleognathae. Alcheringa 30: 141-182.
29. Grellet-Tinner G, Makovicky PJ, (2006) A possible egg of the dromaeosaur Deinonychus antirrhopus: Phylogenetic and biological implications. Can J Earth Sci 43: 705-719.
30. Grellet-Tinner G, Fiorelli LE, Salvador RB, (2012) Water vapor conductance of the Lower Cretaceous dinosaurian eggs from Sanagasta, La Rioja, Argentina: Paleobiological and paleoecological implications for South American faveoloolithid and megaloolithid eggs. Palaios 27: 35-47.
31. Brown G, (1984) Crystal structures of clay minerals and related phyllosilicates. Philos T Roy Soc A 311: 221-240.
32. Krekeler M, (2004) Polysome-width variation in palygorskite-sepiolite minerals: a TEM and AFM investigation of structural variations and transformations. Geol Soc Am Abstracts with Programs 36: 114.
33. Krekeler M, (2004) Improved constraints on sedimentary environments of palygorskite deposits of the Hawthorne Formation, southern Georgia, from a detailed study of a core. Clay Miner 52: 253-262.
34. Krekeler M, Guggenheim S, Rakovan J, (2004) A microtexture study of palygorskite-rich sediments from the Hawthorne Formation, southern Georgia, by transmission electron microscopy and atomic force microscopy. Clay Miner 52: 263-274.
35. Furbish WJ, Sando TW, (1976) Palygorskite by direct precipitation from a hydrothermal solution. Clay Miner 11: 147-152.
36. Garcia RA, Salgado L, Coria RA, Chiappe LM, (2010) Osteología embrionaria de saurópodos titanosaurios de Neuquén (Argentina): Aspectos ontogenéticos y evolutivos. Ameghiniana 47: 409-430.
37. Kurzanov SM, Bannikov AF, (1983) A new sauropod from the Upper Cretaceous of Mongolia. Paleontol Zh 2: 90-96 [in Russian].
38. Wilson JA, (2005) Redescription of the Mongolian sauropod Nemegtosaurus mongoliensis Nowinski (Dinosauria: Saurischia) and comments on Late Cretaceous sauropod diversity. J Syst Palaeontol 3: 283-318.
39. Curry RK, Forster CA, (2001) The last of the dinosaur titans: A new sauropod from Madagascar. Nature 412: 530-534.
40. Chiappe LM, Schmitt JG, Jackson FD, Garrido A, Dingus L, et al. (2004) Nest structure for sauropods: Sedimentary criteria for recognition of dinosaur nesting traces. Palaios 19: 89-95.
41. Deeming DC, (2006) Ultrastructural and functional morphology of eggshells supports the idea that dinosaur eggs were incubated buried in a substrate. Palaeontology 49: 171-185.
42. Shine R, Harlow PS, (1996) Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology 77: 1808-1817.
43. Kolbe JJ, Janzen FJ, (2002) Impact of nest-site selection on nest success and nest temperature in natural and disturbed habitats. Ecology 83: 269-281.
44. Kamel SJ, Mrosovsky N, (2005) Repeatability of nesting preferences in the Hawksbill Sea Turtle, Eretmochelys imbricata, and their fitness consequences. Anim Behav 70: 819-828.
45. Shine R, (2005) Life-history evolution in reptiles. Annu Rev Ecol Evol Syst 36: 23-46.
46. Göth A, Vogel U, (1997) Egg laying and incubation of the Polynesian Megapode. Annu Rev World Pheasant Assoc pp. 43-54.
47. Freedberg S, Wade MJ, (2001) Cultural inheritance as a mechanism for population sex-ratio bias in reptiles. Evolution 55: 1049-1055.
48. Brown G, Shine R, (2007) Like mother, like daughter: inheritance of nest-site location in snakes. Biol Lett 3: 131-133.
49. Werner DI, (1983) Reproduction in the iguana Conolophus subcristatus on Fernandina Island, Galapagos: Clutch size and migration costs. Am Nat 121: 757-775.
50. Chen T-C, Kam Y-C, Lin Y-S, (2001) Thermal physiology and reproductive phenology of Buergeria japonica (Rhacophoridae) breeding in a stream and a geothermal hotspring in Taiwan. Zool Sci 18: 591-596.
51. Wu C-S, Kam Y-C, (2005) Thermal tolerance and thermoregulation by Taiwanese rhacophorid tadpoles (Buergeria japonica) living in geothermal hot springs and streams. Herpetologica 61: 35-46.
52. Guo P, Liu S-Y, Feng J-C, He M, (2008) The description of a new species of Thermophis (Serpentes: Colubridae). Sichuan J Zool 27: 321.
53. Huang S, Liu S-Y, Guo P, Zhang Y-P, Zhao E-M, (2009) What are the closest relatives of the hot-spring snakes (Colubridae, Thermophis), the relict species endemic to the Tibetan Plateau? Mol Phylogenet Evol 51: 438-446.
54. Sas I, Antal C, Covaciu-Marcov SD, (2010) Tropics patch in the Holarctic: A new case of wintertime breeding of a Pelophylax ridibundus population in North-Western Romania. North-West J Zool 6: 128-133.
55. Eikenberg J, Vezzu G, Zumsteg I, Bajo S, Ruethi M, et al. (2001) Precise two chronometer dating of Pleistocene travertine: The 230Th/234U and 226Raex/226Ra(0) approach. Quaternary Sci Rev 20: 1935-1953.
56. Russo-Sändulescu D, Berza T, (1979) Banatites from the western part of the South Carpathians. Rev Roum Geol Geophys Geogr 23: 149-158.
57. Kräutner HG, Berza T, Dimitrescu R, (1986) K-Ar dating of the banatitic magmatites from the southern Poiana Ruscǎ Mountains (Rusca Montanǎ Sedimentary Basin). D.S Inst Geol Geof 70-71: 373-388.
58. Ştefan A, Lazǎr C, Berbeleac I, Udubaşa G, (1988) Evolution of banatitic magmatism in the Apuseni Mountains and associated metallogenesis. D.S. Inst Geol Geol 72-73: 195-213.
59. West JB, (1990) Respiratory physiology, the essentials fourth edition Baltimore Williams and Wilkins.
60. Kardong K, (2001) Vertebrates: Comparative anatomy, function, evolution, third edition Boston McGraw-Hill Science/Engineering/Math.
61. Spearman RIC, Riley PA, (1969) A comparison of the epidermis and pigment cells of the crocodile with those in two lizard species. Zool J Linn Soc 48: 453-466.
62. Wu P, Hou L, Plikus M, Hughes M, Scehnet J, et al. (2004) Evo-devo of amniote integuments and appendages. Int J Dev Biol 48: 249-270.
63. Alibardi L, Thompson MB, (2001) Fine structure of the developing epidermis in the embryo of the American alligator (Alligator mississippiensis, Crocodilia, Reptilia). J Anat 198: 265-282.
64. Vickaryous MK, Sire JY, (2009) The integumentary skeleton of tetrapods: Origin, evolution, and development. J Anat 214: 441-464.
65. Ferguson MWJ, (1985) Reproductive biology and embryology of the crocodilians. In: Gans C, Billett F, Maderson P, editors. Biology of the Reptilia New York John Wiley and Sons pp. 329-491.
66. Coria RA, Chiappe LM, (2007) Embryonic skin from Late Cretaceous sauropods (Dinosauria) of Auca Mahuevo, Patagonia, Argentina. J Paleontol 81: 1528-1532.
67. Chiappe LM, Coria RA, Dingus L, Jackson F, Chinsamy A, et al. (1998) Sauropod dinosaur embryos from the Late Cretaceous of Patagonia. Nature 396: 258-261.
68. Tazaki K, (2006) Clays, microorganisms, and biomineralization. In: Bergaya F, Theng BKG, Lagaly G, editors. Handbook of clay science, volume 1 (developments in clay science) Amsterdam Elsevier pp. 477-497.
69. Weishampel DB, Grigorescu D, Norman DB, (1991) The dinosaurs of Transylvania: Island biogeography in the Late Cretaceous. Natl Geogr Res 7: 68-87.
70. Weishampel DB, Csiki Z, Benton MJ, Grigorescu D, Codrea V, (2010) Palaeobiogeographic relationships of the Haţeg biota- Between isolation and innovation. Palaeogeogr, Palaeoclimateol, Palaeoecol 293: 419-437.
71. Ösi A, Apesteguía S, Kowalewski M, (2010) Non-avian theropod dinosaurs from the Early Late Cretaceous of central Europe. Cretaceous Res 31: 304-320.
72. Nowinski A, (1971) Nemegtosaurus mongoliensis n. gen., n. sp. (Sauropoda) from the Uppermost Cretaceous of Mongolia. Palaeont Pol 25: 57-81.
73. Wilson JA, Upchurch P, (2003) A revision of Titanosaurus Lydekker (Dinosauria-Sauropoda), the first dinosaur genus with a "Gondwanan" distribution. J Syst Palaeontol 1: 125-160.
74. Canudo JI, Barco JL, Pereda-Suberbiola X, Ruiz-Omeñaca JI, Salgado L, et al. (2009) What Iberian dinosaurs reveal about the bridge said to exist between Gondwana and Laurasia in the Early Cretaceous. B Soc Geol Fr 180: 5-11.
75. Dercourt J, Ricou LE, Vrielynck B, (1993) Atlas Tethys- palaeoenvironmental maps. CCGM/CGMW, Paris: Gauthier-Villars.
76. Dercourt J, Gaetani M, Vrielynck B, Barrier E, Biju-Duval B, et al. (2000) Atlas Peri-Tethys- palaeogeographical atlas Paris CCGM/CGMW.
77. Prieto-Marquez A, Wagner JR, (2009) Pararhabdodon isonensis and Tsintaosaurus spinorhinus: a new clade of lambeosaurine hadrosaurids from Eurasia. Cretaceous Res 30: 1238-1246.
78. Dalla Vecchia FM, (2009) Tethyshadros insularis, a new hadrosauroid dinosaur (Ornithischia) from the Upper Cretaceous of Italy. J Vertebr Paleontol 29: 1100-1116.
79. Ösi A, Butler RJ, Weishampel DB, (2010) A Late Cretaceous ceratopsian dinosaur from Europe with Asian affinities. Nature 465: 466-468.
80. Pereda-Suberbiola X, (2009) Biogeographical affinities of Late Cretaceous continental tetrapods of Europe. B Soc Geol Fr 180: 57-71.
81. Smith T, De Bast E, Sigé B, (2010) Euarchontan affinity of Palaeocene Afro-European adapisoriculid mammals and their origin in the late Cretaceous Deccan Traps of India. Naturwissenschaften 97: 417-422.
82. Brazaitis P, Watanabe ME, (2011) Crocodilian behaviour: A window to dinosaur behaviour? Hist Bio 23: 73-90.