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Porosity and water vapor conductance of two Troodon formosus eggs: an assessment of incubation strategy in a maniraptoran dinosaur

Published online by Cambridge University Press:  11 March 2013

David J. Varricchio ,
Frankie D. Jackson ,
Robert A. Jackson  and
Darla K. Zelenitsky
David J. Varricchio
Affiliation:
Department of Earth Sciences, Montana State University, Bozeman, Montana 59717, U.S.A. E-mail: djv@montana.edu
Frankie D. Jackson
Affiliation:
Department of Earth Sciences, Montana State University, Bozeman, Montana 59717, U.S.A. E-mail: djv@montana.edu
Robert A. Jackson
Affiliation:
Department of Earth Sciences, Montana State University, Bozeman, Montana 59717, U.S.A. E-mail: djv@montana.edu
Darla K. Zelenitsky
Affiliation:
Department of Geoscience, University of Calgary, Calgary, Alberta, Canada T2N 1N4
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Abstract

Using tangential thin sections, we examined variation in porosity and water vapor conductance across two eggs of Troodon formosus, a small (∼50 kg) theropod dinosaur from the North American Upper Cretaceous, testing two hypotheses of egg incubation: (1) full burial within sediments or vegetation and (2) partial burial with exposed upper egg portions. We divided and sampled the eggs in five zones, 1 through 5 from blunt top to more pointed bottom. A geometric model composed of a hemisphere, cone, and paraboloid was used to estimate total and zonal volumes and surface areas. The 138 × 67 mm idealized Troodon egg has a volume, surface area, and mass of 296.4 cm3, 239.23 cm2, and 314.2 g, respectively. Zonal surface areas and volumes highlight the strongly asymmetric and elongate form of the Troodon egg. Geometric modeling provides better estimates of volume and surface area where egg shape diverges markedly from that of a typical bird egg. Porosity varies significantly across both Troodon eggs, with zones 2 and 3 having the largest pores and a majority (70–78%) of total conductance, whereas zone 5 has very low conductance. Total water vapor conductance in the two eggs are 31.85 and 40.62 mg H2O day− Torr−, values 76% and 97% of those predicted for an avian egg of similar size. Low total conductance compares favorably to values in extant birds and non-avian reptiles that incubate in open nests, arguing against full burial incubation. Together with nesting site evidence, low conductance values favor partial burial and incubation by a Troodon adult. Asymmetric egg shape concentrates volume, surface area, and conductance near or at the point of subaerial exposure. Among non-avian dinosaurs, the eggs of Troodon and troodontids are most similar to those of modern birds in having an asymmetric shape, low porosity, no ornamentation, and three structural eggshell layers.

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Articles
Information
Paleobiology , Volume 39 , Issue 2 , Spring 2013 , pp. 278 - 296
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Ackerman, R. A. 1980. Physiological and ecological aspects of gas exchange by sea turtle eggs. American Zoologist 20:575–583.CrossRefGoogle Scholar
Ar, A., and Rahn, H. 1985. Pores in avian eggshells: gas conductance, gas exchange, and embryonic growth rate. Respiration Physiology 61:1–20.Google ScholarPubMed
Ar, A., Paganelli, C. V., Reeves, R. B., and Rahn, H. 1974. The avian egg: water vapor conductance, shell thickness, and functional pore area. Condor 76:153–158.CrossRefGoogle Scholar
Balkan, M., Karakas, R., and Biricik, M. 2006. Changes in eggshell thickness, shell conductance and pore density during incubation in the Peking Duck (Anas platyrhynchos f. dom.). Ornis Fennica 83:117–123.Google Scholar
Bates, R. L., and Jackson, J. A. 1984. Dictionary of geological terms. Random House, New York.Google Scholar
Bever, G. S., and Norell, M. A. 2009. The perinate skull of Byronosaurus (Troodontidae) with observations on the cranial ontogeny of paravian theropods. American Museum Novitates No. 3657.CrossRefGoogle Scholar
Booth, D. T., and Seymour, R. S. 1987. Effects of eggshell thinning on water vapor conductance of Malleefowl (Laipoa ocellata) eggs. Condor 89:453–459.CrossRefGoogle Scholar
Booth, D. T., and Thompson, M. B. 1991. A comparison of reptilian eggs with those of megapode birds. Pp. 325–344inDeeming, D. C. and Ferguson, M. W. J., eds. Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Brady, N. C., and Weil, R. R. 2002. The nature and properties of soils. Prentice Hall, Upper Saddle River, N.J.Google Scholar
Brown, S. G., and Duffy, P. K. 1992. The effects of egg-laying site, temperature, and salt water on incubation time and hatching success in the gecko Lepidodactylus lugubris. Journal of Herpetology 26:510–513.CrossRefGoogle Scholar
Carpenter, K. 1999. Eggs, nests, and baby dinosaurs: a look at dinosaur reproduction. Indiana University Press, Bloomington.Google Scholar
Chou, L. M. 1979. Eggs and incubation period of three gekkonid lizards. Copeia 1979:552–54.CrossRefGoogle Scholar
de Blij, H. J., Muller, P. O., and Williams, R. S. Jr. 2004. Physical geography: the global environment. Oxford University Press, New York.Google Scholar
Deeming, D. C. 2002. Importance and evolution of incubation in avian reproduction. Pp. 1–7inDeeming, D. C., ed. Avian incubation: behaviour, environment and evolution. Oxford University Press, Oxford.Google Scholar
Deeming, D. C. 2006. Ultrastructural and functional morphology of eggshells supports the idea that dinosaur eggs were incubated buried in a substrate. Palaeontology 49:171–185.CrossRefGoogle Scholar
Deeming, D. C., and Thompson, M. B. 1991. Gas exchange across reptilian eggshells. Pp. 277–284inDeeming, D. C. and Ferguson, M. W. J., eds. Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Donaire, M., and Lopéz-Martínez, N. 2009. Porosity of Late Paleocene Ornitholithus eggshells (Tremp Fm, south-central Pyrenees, Spain): palaeoclimatic implications. Palaeogeography, Palaeoclimatology, Palaeoecology 279:147–159CrossRefGoogle Scholar
Dunson, W. A. 1982. Low water vapor conductance of hard-shelled eggs of the gecko lizards Hemidactylus and Lepidodactylus. Journal of Experimental Zoology.219:377−379.CrossRefGoogle Scholar
Dunson, W. A., and Bramham, C. R. 1981. Evaporative water loss and oxygen consumption of three small lizards from the Florida Keys: Spanerodactylus cinereus, S. notatus, and Anolis sagrei. Physiological Zoology 54:253–259.CrossRefGoogle Scholar
Erickson, G. M., Curry Rogers, K., Varricchio, D. J., Norell, M. A., and Xu, X. 2007. Growth patterns in brooding dinosaurs reveals the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition. Biology Letters 3:558–561.CrossRefGoogle ScholarPubMed
Gao, C., Morschhauser, E. M., Varricchio, D. J., Liu, J., and Zhao, B. 2012. A second soundly sleeping dragon: new anatomical details of the Chinese troodontid Mei long with implications for phylogeny and taphonomy. PLoS ONE 7 (9): e45203 doi:10.1371/journal.pone.0045203.Google Scholar
Grellet-Tinner, G. 2006. Oology and the evolution of thermophysiology in saurischian dinosaurs: homeotherm and endotherm deinonychosaurians? Papéis Avulsos de Zoologia 46:1–10.CrossRefGoogle Scholar
Grellet-Tinner, G., and Chiappe, L. M. 2004. Dinosaur eggs and nesting: implications for understanding the origin of birds. Pp. 185–214inCurrie, P. J., Koppelhus, E. B., Shugar, M. A., and Wright, J. L., eds. Feathered dragons: studies on the transition from dinosaurs to birds. Indiana University Press, Bloomington.Google Scholar
Grellet-Tinner, G., and Makovicky, P. 2006. A possible egg of the dromaeosaur Deinonychus antirrhopus: phylogenetic and biological implications. Canadian Journal of Earth Sciences 43:705–719.CrossRefGoogle Scholar
Grellet-Tinner, G., Chiappe, L. M., Norell, M., and Bottjer, D. 2006. Dinosaur eggs and nesting ecology: a paleobiological investigation. Palaeogeography, Palaeoclimatology, Palaeoecology 232:294–321.CrossRefGoogle Scholar
Grellet-Tinner, G., Fiorelli, L. E., and Salvador, R. B. 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.CrossRefGoogle Scholar
Grigorescu, D., Weishampel, D.Norman, D., Seclamen, M., Rusu, M., Baltres, A., and Teodorescu, V. 1994. Late Maastrichtian dinosaur eggs from Hateg Basin (Romania). Pp. 75–87inCarpenter, K., Hirsch, K. F., and Horner, J. R., eds. Dinosaur eggs and babies. Cambridge University Press, Cambridge.Google Scholar
Harrison, T., and Msuya, C. P. 2005. Fossil struthionid eggshells from Laetoli, Tanzania: taxonomic and biostratigraphic significance. Journal of African Earth Sciences 4:303–315.CrossRefGoogle Scholar
Hirsch, K. F., and Quinn, B. 1990. Eggs and eggshell fragments from the Upper Cretaceous Two Medicine Formation of Montana. Journal of Vertebrate Paleontology 10:491–511.CrossRefGoogle Scholar
Horner, J. R. 1982. Evidence for colonial nesting and “site fidelity” in ornithischian dinosaurs. Nature 297:675–676.CrossRefGoogle Scholar
Horner, J. R. 1984. The nesting behavior of dinosaurs. Scientific American 250:130–137.CrossRefGoogle Scholar
Horner, J. R. 1987. Ecologic and behavioral implications derived from a dinosaur nesting site. Pp. 50–63inCzerkas, S. J. and Olson, E. C., eds. Dinosaurs past and present, Vol. II. Natural History Museum of Los Angeles County, Los Angeles.Google Scholar
Horner, J. R. 2000. Dinosaur reproduction and parenting. Annual Review of Earth and Planetary Sciences 28:19–45.CrossRefGoogle Scholar
Horner, J. R., Padian, K., and de Ricqlès, A. 2001. Comparative osteohistology of some embryonic and perinatal archosaurs: phylogenetic and behavioral implications for dinosaurs. Paleobiology 27:39–58.2.0.CO;2>CrossRefGoogle Scholar
Howell, T. R. 1979. Breeding biology of the Egyptian Plover, Pluvianus aegyptius. University of California Publications in Zoology 113:1–76.Google Scholar
Hoyt, D. F. 1979. Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73–77.Google Scholar
Jackson, F. D., Varricchio, D. J., Jackson, R., Vila, B., and Chiappe, L. 2008. Water vapor conductance of a titanosaur egg (Megaloolithus patagonicus) from Argentina: comparison with a Megaloolithus siruguei egg from Spain. Paleobiology 34:229–246.CrossRefGoogle Scholar
Jackson, F. D., Horner, J. R., and Varricchio, D. J. 2010. A study of a Troodon egg containing embryonic remains using epifluorescence microscopy and other techniques. Cretaceous Research 31:255–262.CrossRefGoogle Scholar
Jones, D. N., Dekker, R. W. R. J., and Roselaar, C. S. 1995. The megapodes, Megapodiidae. Oxford University Press, Oxford.Google Scholar
Kern, M. D., and Ferguson, M. W. 1997. Gas permeability of American alligator eggs and its anatomical basis. Physiological Zoology 70:530–546.CrossRefGoogle ScholarPubMed
Kolesnikov, C. M., and Sochava, A. V. 1972. A paleobiochemical study of Cretaceous dinosaur eggshell from the Gobi. Paleontological Journal 2:235–245.Google Scholar
Lide, D. R. 2009. CRC handbook of chemistry and physics 2009−2010. CRC Press, Boca Raton, Fla.Google Scholar
Lutz, P. L., and Dunbar-Cooper, A. 1984. The nest environment of the American crocodile (Crocodylus acutus). Copeia 1984:153–161.CrossRefGoogle Scholar
Maclean, G. L. 1996. Family Glareolidae: coursers and pratincoles. Pp. 364–383inJ. del Hoyo, A. Elliott, and Sargatal, J., eds. Handbook of birds of the world, Vol. 3. Hoatzin to auks. Lynx Edicions, Barcelona.Google Scholar
Mikhailov, K. E. 1997. Fossil and recent eggshell in amniotic vertebrates: fine structure, comparative morphology and classification. Special Papers in Palaeontology 56:1–80.Google Scholar
Packard, G. C., Taigen, T. L., Packard, M. J., and Shuman, R. D. 1979. Water-vapor conductance of testudinian and crocodilian eggs (Class Reptilia). Respiration Physiology 38:1–10.CrossRefGoogle ScholarPubMed
Paganelli, C. V. 1980. The physics of gas exchange across the avian eggshell. American Zoologist 20:329–338.CrossRefGoogle Scholar
Paganelli, C. V., Olszowka, A., and Ar, A. 1974. The avian egg: surface area, volume, and density. Condor 76:319–325.CrossRefGoogle Scholar
Paganelli, C. V., Ackerman, R. A., and Rahn, H. 1978. The avian egg: in vivo conductances to oxygen, carbon dioxide, and water vapor in late development. Pp. 212–218inPiiper, J., ed. Respiratory function in birds, adult and embryonic. Springer, Berlin.CrossRefGoogle Scholar
Rogers, R. R., Swisher, C. C. III, and Horner, J. R. 1993. 40Ar/39Ar age and correlation of the nonmarine Two Medicine Formation (Upper Cretaceous), northwestern Montana, U.S.A. Canadian Journal Earth Sciences 30:1066–1075.CrossRefGoogle Scholar
Rokitka, M. A., and Rahn, H. 1987. Regional differences in shell conductance and pore density of avian eggs. Respiration Physiology 68:371–376.CrossRefGoogle ScholarPubMed
Russell, D. A., and Dong, Z.-M. 1993. A nearly complete skeleton of a new troodontid dinosaur from the Early Cretaceous of the Ordos Basin, Inner Mongolia, People's Republic of China. Canadian Journal of Earth Sciences 30:2163–2173.CrossRefGoogle Scholar
Sabath, K. 1991. Upper Cretaceous amniotic eggs from the Gobi Desert. Acta Palaeontologica Polonica 36:151–192.Google Scholar
Sahni, A., Tandon, S. K., Jolly, A., Bajpai, S., Sood, A., and Srinivasan, S. 1994. Upper Cretaceous dinosaur eggs and nesting sites from the Deccan volcano-sedimentary province of peninsular India. Pp. 204–226inCarpenter, K., Hirsch, K. F., and Horner, J. R., eds. Dinosaur eggs and babies. Cambridge University Press, Cambridge.Google Scholar
Sereno, P. C. 1999. The evolution of dinosaurs. Science 284:2137–2147.CrossRefGoogle ScholarPubMed
Seymour, R. S. 1979. Dinosaur eggs: gas conductance through the shell, water loss during incubation and clutch size. Paleobiology 5:1–11.CrossRefGoogle Scholar
Seymour, R. S., and Ackerman, R. A. 1980. Adaptations to underground nesting in birds and reptiles. American Zoologist 20:437–447.CrossRefGoogle Scholar
Seymour, R. S., and Visschedijk, A. H. J. 1988. Effects of variation in total and regional shell conductance on air cell gas tensions and regional gas exchange in chicken eggs. Journal of Comparative Physiology B 158:229–236.CrossRefGoogle Scholar
Seymour, R. S., Vleck, D., and Vleck, C. 1986. Gas exchange in the incubation mounds of megapode birds. Journal of Comparative Physiology B 156:773–782.CrossRefGoogle Scholar
Shelton, J. A. 2007. Application of sequence stratigraphy to the nonmarine upper Cretaceous Two Medicine Formation, Willow Creek Anticline, northwestern Montana, Earth Sciences M.S. thesis. Montana State University, Bozeman.Google Scholar
Shott, A. R., and Preston, F. W. 1975. The surface area of an egg. Condor 77:103–104.CrossRefGoogle Scholar
Thompson, M. B. 1985. Functional significance of the opaque white patch in eggs of Emydura macquarii. Pp. 387–395inGrigg, G., Shine, R., and Ehmann, H., eds. Biology of Australian frogs and reptiles. Royal Zoological Society, Sydney.Google Scholar
Thompson, M. B., and Speake, B. K. 2004. Egg morphology and composition. Pp. 45–74inDeeming, D. C., ed. reptilian incubation, environment, evolution and behaviour. Nottingham University Press, Nottingham.Google Scholar
Varricchio, D. J. 1993a. Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 13:99–104.CrossRefGoogle Scholar
Varricchio, D. J. 1993b. Montana climatic changes associated with the Cretaceous Claggett and Bearpaw transgressions. Pp. 97–102inHunter, L. D. V., ed. Energy and mineral resources of central Montana: 1993 field conference guidebook. Montana Geological Society, Billings.Google Scholar
Varricchio, D. J. 1995. Taphonomy of Jack's Birthday Site, a diverse dinosaur bone bed from the Upper Cretaceous Two Medicine Formation of Montana. Palaeogeography, Palaeoclimatology, Palaeoecology 114:297–323.CrossRefGoogle Scholar
Varricchio, D. J., and Jackson, F. D. 2004a. Two eggs sunny-side up: reproductive physiology in the dinosaur Troodon formosus. Pp. 215–233inCurrie, P. J., Koppelhus, E. B., Shugar, M. A., and Wright, J. L., eds. Feathered dragons: studies on the transition from dinosaur to birds. Indiana University Press, Bloomington.Google Scholar
Varricchio, D. J., and Jackson, F. D. 2004b. Cladistic analysis of eggshell characters: a phylogenetic assessment of prismatic dinosaur eggs from the Cretaceous Two Medicine Formation of Montana. Journal of Vertebrate Paleontology 24:931–937.CrossRefGoogle Scholar
Varricchio, D. J., Jackson, F., Borkowski, J., and Horner, J. R. 1997. Nest and egg clutches of the dinosaur Troodon formosus and the evolution of avian reproductive traits. Nature 385:247–250.CrossRefGoogle Scholar
Varricchio, D. J., Jackson, F., and Truman, C. 1999. A nesting trace with eggs for the Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 19:91–100.CrossRefGoogle Scholar
Varricchio, D. J., Horner, J. R., and Jackson, F. 2002. Embryos and eggs for the Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 22:564–576.CrossRefGoogle Scholar
Varricchio, D. J., Moore, J. R., Erickson, G. M., Norell, M. A., Jackson, F. D., and Borkowski, J. J. 2008. Avian paternal care had dinosaur origin. Science 322:1826–1828.CrossRefGoogle ScholarPubMed
Varricchio, D. J., Koeberl, C., Raven, R. F., Wolbach, W., Elsik, W. C., and Miggins, D. P. 2010. Tracing the Manson impact event across the Western Interior Cretaceous Seaway. InGibson, R. L. and Reimold, W. U., eds. Large meteorite impacts and planetary evolution IV. Geological Society of America Special Paper 465:269–299.Google Scholar
Vleck, C. M., and Hoyt, D. F. 1991. Metabolism and energetics of reptilian and avian embryos. Pp. 285–306inDeeming, D. C. and Ferguson, M. W. J., eds. Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Webb, G. J. W. 1981. Nesting biology of Crocodylus johnstoni in the Northern Territory. Pp. 107inBanks, C. B. and Martin, A. A., eds. Proceedings of the Melbourne herpetological symposium. Dominion Press, Victoria, Australia.Google Scholar
Webb, G. J. W., Buckworth, R., and Manolis, S. C. 1983. Crocodylus johnstoni in the McKinlay River, N.T. VI. Nesting biology. Australian Wildlife Research 10:607–637.CrossRefGoogle Scholar
Weisstein, E. W. 2011a. “Sphere.” MathWorld—A Wolfram Web Resource. http://mathworld.wolfram.com/Sphere.html.Google Scholar
Weisstein, E. W. 2011b. “Spherical Segment.” MathWorld—A Wolfram Web Resource. http://mathworld.wolfram.com/SphericalSegment.html.Google Scholar
Weisstein, E. W. 2011c. “Cone.” MathWorld—A Wolfram Web Resource. http://mathworld.wolfram.com/Cone.html.Google Scholar
Weisstein, E. W. 2011d. “Paraboloid.” MathWorld—A Wolfram Web Resource. http://mathworld.wolfram.com/Paraboloid.html.Google Scholar
Williams, D.L.G., Seymour, R.S., and Kerourio, P. 1984. Structure of fossil dinosaur eggshell from the Aix Basin, France. Palaeogeography, Palaeoclimatology, Palaeoecology 45:23–37.CrossRefGoogle Scholar
Xu, X., and Norell, M. A. 2004. A new troodontid dinosaur from China with avian-like sleeping posture. Nature 431:838–841.CrossRefGoogle ScholarPubMed
Zelenitsky, D. K., and Hills, L. V. 1996. An egg clutch of Prismatoolithus levis oosp. nov. from the Oldman Formation (Upper Cretaceous), Devil's Coulee, southern Alberta. Canadian Journal of Earth Sciences 33:1127–1131.CrossRefGoogle Scholar
Zelenitsky, D. K., and Therrien, F. 2008. Phylogenetic analysis of reproductive traits of maniraptoran theropods and its implications for egg parataxonomy. Palaeontology 51:807–816.CrossRefGoogle Scholar
Zelenitsky, D. K., Modesto, S., and Currie, P. J. 2002. Bird-like characteristics of troodontid theropod eggshell. Cretaceous Research 23:297–305.CrossRefGoogle Scholar
Zhao, Z.-K. 2000. Nesting behavior of dinosaurs as interpreted from the Chinese Cretaceous dinosaur eggs. Paleontology Society of Korea Special Publication 4:115–126.Google Scholar
Zhao, Z.-K. 2003. The nesting behavior of troodontid dinosaurs. Vertebrata PalAsiatica 41:157–168.Google Scholar
Zhao, Z. K., and Li, R. 1993. First record of late Cretaceous hypsilophodontid eggs from Bayan Manduhu Inner Mongolia. Vertebrata PalAsiatica 31:77–84.Google Scholar