Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-17T23:28:47.573Z Has data issue: false hasContentIssue false
  • English
  • Français

Incubation time as an important influence on egg production and distribution into clutches for sauropod dinosaurs

Published online by Cambridge University Press:  08 April 2016

Graeme D. Ruxton ,
Geoffrey F. Birchard  and
D. Charles Deeming
Graeme D. Ruxton
Affiliation:
School of Biology, University of St. Andrews, St. Andrews KY16 9TH, U.K. E-mail: [email protected]
Geoffrey F. Birchard
Affiliation:
Department of Environmental Science and Policy, George Mason University, Fairfax, Virginia 22030, U.S.A.
D. Charles Deeming
Affiliation:
Department of Biological Sciences, University of Lincoln, Lincoln LN2 2LG, U.K.
Get access Rights & Permissions [Opens in a new window]

Abstract

Individual egg size and clutch size of the largest of the dinosaurs (the sauropods) are both smaller than might be expected for such large oviparous organisms. We suggest that these effects can be understood in the light of likely incubation times of sauropod eggs. Using allometric relationships from extant birds and crocodilians, we estimate that time from laying to hatching was likely to have been 65–82 days. If total predation risk varies with length of incubation time, there may be egg sizes above which the advantages of larger initial hatchling size are outweighed by the increased risk of predation during the egg stage. Also, in seasonal environments there will often be a finite limit to the period over which environmental temperatures are high enough for egg development. Thus incubation time may have been an important constraint explaining the small individual size of sauropod eggs. We further suggest that for sauropods spatial dispersal of eggs in small clutches was an adaptive strategy to mitigate this high predation risk associated with long time of exposure in the egg stage. Such a dispersive strategy brings several benefits. Thus, incubation time may also be key to explaining the surprisingly small clutch sizes.

Type
Featured Article
Information
Paleobiology , Volume 40 , Issue 3 , Summer 2014 , pp. 323 - 330
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Anderson, M., and Ahlund, M. 2012. Don't put all your eggs in one nest: spread them and cut time at risk. American Naturalist 180:354–363.Google Scholar
Bertram, B. C. R. 1992. The ostrich communal nesting system. Princeton University Press, Princeton, N.J.Google Scholar
Birchard, G. F., and Deeming, D. C. 2009. Scaling of avian eggshell thickness: implications for maximum body mass in birds. Journal of Zoology 279:95–101.Google Scholar
Booth, D. T., and Jones, D. N. 2002. Underground nesting in the megapodes. Pp. 192–206inDeeming, D. C.ed. Avian incubation: behaviour, environment and evolution. Oxford University Press, Oxford.Google Scholar
Chiappe, L. M., and Dingus, L. 2001. Walking on eggs. Scribner, New York.Google Scholar
Chiappe, L. M., Jackson, F. D., Coria, R. A., and Dingus, L. 2001. Nesting titanosaurs from Auca Maheuvo and adjacent sites. Pp. 285–302inCurry Rogers, K. A. and Wilson, J. A., eds. The sauropods: evolution and paleobiology. University of California Press, Berkeley.Google Scholar
Chiappe, L. M., Schmitt, J. G., Jackson, F. D., Garrido, A., Dingus, L., and Grellet-Tinner, G. 2004. Nest structure for sauropods: sedimentary criteria for recognition of dinosaur nesting traces. Palaios 19:89–95.Google Scholar
Dale, R. H. I. 2010. Birth statistics for African (Loxodonta Africana) and Asian (Elephas maximus) elephants in human care: history and implications for elephant welfare. Zoo Biology 29:87–103.Google Scholar
Davies, S. J. J. F. 2002. Ratites and tinamous: Tinamidae, Rheidae, Dromaiidae, Casuariidae, Apterygidae, Struthionidae. Oxford University Press, Oxford.Google Scholar
Deeming, D. C. 2006. Ultrastructural and functional morphology of eggshells supports idea that dinosaur eggs were incubated buried in a substrate. Paleontology 49:171–185.Google Scholar
Deeming, D. C. 2008. Avian brood patch temperature: relationships with female body size, incubation period, developmental maturity and phylogeny. Journal of Thermal Biology 33:345–354.Google Scholar
Deeming, D. C., and Ar, A. 1999. Factors affecting the success of commercial incubation. Pp. 159–190inDeeming, D. C.ed. The ostrich: biology, production and health. CAB International, Wallingford, U.K.Google Scholar
Deeming, D. C., Birchard, G. F., Crafer, R., and Eady, P. E. 2006. Egg mass and incubation period allometry in birds and reptiles: the effects of phylogeny. Journal of Zoology 270:209–218.CrossRefGoogle Scholar
Dinsmore, S. J., White, G. C., and Knopf, F. L. 2002. Advanced techniques for modelling avian nest survival. Ecology 83:3476–3488.Google Scholar
Ferguson, M. W. J. 1985. Reproductive biology and embryology of the crocodilians. Pp. 329–492inGans, C., Billett, F., and Maderson, P. F. A., eds. Biology of the Reptilia, Vol. 14. Development A. Wiley, New York.Google Scholar
Grant, T. A., Shaffer, T. L., Madden, E. M., and Pietz, P. J. 2005. Time-specific variation in passerine next survival: new insights into old questions. Auk 122:661–672.CrossRefGoogle Scholar
Grellet-Tinner, G., and Fiorelli, L. E. 2010. A new Argentinean nesting site showing neosauropod dinosaur reproduction in a Cretaceous hydrothermal environment. Nature Communications 1:32.Google Scholar
Hoyt, D. F. 1979. Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73–77.Google Scholar
Huchzermeyer, F. W. 2003. Crocodiles: biology, husbandry and diseases. CABI Publishing, Wallingford, U.K.Google Scholar
Jackson, F. D., Varricchio, D. J., Jackson, R. A., Vila, B., and 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 34:229–246.Google Scholar
Janis, C. M., and Carrano, M. 1992. Scaling of reproductive turnover in archosaurs and animals: why are large terrestrial mammals so rare? Annales Zoologici Fennici 28:201–216.Google Scholar
Kirkland, J. I. 1994. Predation of dinosaur nest by terrestrial crocodilians. Pp. 124–133inCarpenter, K., Hirsch, K. F., and Horner, J. R., eds. Dinosaur eggs and babies. Cambridge University Press, Cambridge.Google Scholar
Klein, N., Remes, K., Gee, C. T., and Sander, P. M. 2011. Compilation of published body mass data for a variety of basal sauropodomorphs and sauropods. Pp. 317–322inKlein, N., Remes, K., Gee, C. T., and Sander, P. M., eds. Biology of the sauropod dinosaurs: understanding the life of giants. Indiana University Press, Bloomington.Google Scholar
Magige, F. L., Stokke, B. A., Sortland, R., and Roskaft, E. 2009. Breeding biology of ostriches (Struthio camelus) in the Serengeti ecosystem, Tanzania. African Journal of Ecology 47:400–408.Google Scholar
Mohabey, D. M. 1996. A new oospecies, Megaloolithus matleyi, from the Lameta Formation (Upper Cretaceous) of Chandrapur district, Maharashatra, India, and general remarks on the palaeoenvironment and nesting behaviour of dinosaurs. Cretaceous Research 17:183–196.Google Scholar
Male, L. H., and Smulders, T. V. 2007. Hyperdispersed cache distributions reduce pilferage: a field study. Animal Behavior. 73:717–726.Google Scholar
Mrosovsky, N. 1983. Ecology and nest-site selection of leatherback turtles (Dermochelys coriacea). Biological Conservation 26:47–56.Google Scholar
Mueller-Töwe, I., Sander, P. M., Schüller, H., and Theis, D. 2002. Hatching and infilling of dinosaur eggs as revealed by computed tomography. Palaeontographica A 267:119–168.Google Scholar
Rahn, H., and Ar, A. 1974. The avian egg: incubation time and water loss. Condor 76:147–152.Google Scholar
Reisz, R. E., Scott, D., Sues, H.-D., Evans, D. C., and Raath, M. A. 2005. Embryos of an early Jurassic prosauropod dinosaur and their evolutionary significance. Science 309:761–764.Google Scholar
Reisz, R. E., Evans, D. C., Sues, H.-D., and Scott, D. 2010a. Embryonic skeletal anatomy of the sauropodomorph dinosaur Massospondylus from the lower Jurassic of South Africa. Journal of Vertebrate Paleontology 30:1653–1665.CrossRefGoogle Scholar
Reisz, R. E., Evans, D. C., Roberts, E. M., Sues, H.-D., and Yates, A. M. 2010b. Oldest known dinosaurian nesting site and reproductive biology of the early Jurassic sauropodomorph Massospondylus. Proceedings of the National Academy of Sciences USA 109:2428–2433.Google Scholar
Reisz, R. E., Huang, T. D., Roberts, E.M., Peng, S., Sullivan, C., Stein, K., LeBlanc, A. R. H., Shieh, D., Chang, R., Chiang, C., Yang, C., and Zhong, S. 2013. Embryology of Early Jurassic dinosaur from China with evidence of preserved organic remains. Nature 496:210–214.Google Scholar
Sander, P. M., Peitz, C., Gallemi, J., and Cousin, R. 1998. Dinosaurs nesting on a red beach? Comptes Rendus de l'Académie des Sciences, Paris, série IIA (Sciences de la Terre et des Planètes) 327:67–74.Google Scholar
Sander, P. M., Peitz, C., Jackson, F. D., and Chiappe, L. M. 2008. Upper Cretaceous titanosaur nesting sites and their implications for sauropod dinosaur reproductive biology. Palaeontographica A 284:69–107.Google Scholar
Sander, P. M., Christian, A., Clauss, M., Fechner, R., Gee, C. T., Griebeler, E.-M., Gunga, H.-C., Hummel, J., Mallison, H., Perry, S. F., Preuschoft, H., Rauhut, O. W. M., Remes, K., Tutken, T., Wings, O., and Witzel, U. 2011. Biology of the sauropod dinosaurs: the evolution of gigantism. Biological Reviews 86:117–155.Google Scholar
Sebei, S. K., Bergaoui, R., Hamouda, M. B., and Cooper, R. G. 2009. Wild ostrich (Struthio camelus australis) reproduction in Orbata, a nature reserve in Tunisia. Tropical Animal Health and Production 41:1427–1438.Google Scholar
Seymour, R. S. 1979. Dinosaur eggs: gas conductance through the shell, water loss during incubation, and clutch size. Paleobiology 5:1–11.Google Scholar
Simpson, E. L., Hilbert-Wolf, H. L., Wizevich, M. C., Tindall, S. E., Fasinski, B. R., Storm, L. P., and Needle, M. D. 2010. Predatory digging behaviour in dinosaurs. Geology 38:699–702.Google Scholar
Upchurch, P., Barrett, P. M., and Dodson, P. 2004. Sauropoda. Pp. 259–322inWeishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria, 2nd ed. University of California Press, Berkeley.Google Scholar
Vanderwall, S. B. 1990. Food hoarding in animals. University of Chicago Press, Chicago.Google Scholar
Vila, B., Jackson, F. D., Fortuny, J., Sellés, A. G. and Galobart, A. 2010. 3-D modelling of megaloolithid clutches: insights about nest construction and dinosaur behaviour. PLoS ONE 5 (5):e10362. doi: 10.1371/journal.pone.0010362.Google Scholar
Werner, J., and Griebeler, E. M. 2011. Reproductive biology and its impact on body size: comparative analysis of mammalian, avian and dinosaurian reproduction. PLoS ONE 6 (12):e28442. doi: 10.1371/journal.pone.0028442.Google Scholar
Werner, J., and Griebeler, E. M. 2013. New insights into non-avian dinosaur reproduction and their evolutionary and ecological implications: linking fossil evidence to allometries of extant close relatives. PLoS ONE 8 (8):e72862. doi: 10.1371/journal.pone.0072862.Google Scholar
Wilson, J. A., Mohabey, D. M., Peters, S. E., and Head, J. J. 2010. Predation upon hatchling dinosaurs by a new snake from the Late Cretaceous of India. PLoS Biology 8 (3):e1000322. doi: 10.1371/journal.pbio.1000322.Google Scholar