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Czech Geological Survey,
W. Bohemia Museum Pilsen
ISSN: 1802-8225 (online),
Environmental impact on ectocochleate cephalopod reproductive strategies and the evolutionary significance of cephalopod egg size
Published in: Bulletin of Geosciences, volume 88, issue 1; pages: 83 - 94; Received 2 February 2012; Accepted in revised form 19 June 2012; Online 28 November 2012
Keywords: Ammonoidea, Nautiloidea, reproductive strategy, mass extinction, climate change, egg,
Compilation of embryonic shell measurements of Paleozoic and Mesozoic ammonoid taxa, geographic areas and inferred climate.
Compilation of embryonic shell measurements of Paleozoic–recent coiled nautiloids, geographic areas and inferred climate.
References for Nautiloidea and Ammonoidea
AbstractPublished data on initial chamber (protoconch) diameter in 507 species, and embryonic shell (ammonitella) diameter in 231 species of Ammonoidea, and embryonic shell (nauta) diameters for 132 species of coiled Nautiloidea, were used to examine evolutionary change in ectocochleate cephalopod reproductive strategies. Palaeotemperatures were found to be a key factor influencing historical changes in the evolution of egg size in ammonoids and nautiloids. A negative relationship was found between egg size and warming of the Earth’s climate. Factors related to habitat were also important; in general egg size was larger in cold-water cephalopods. Egg size in Lytoceratina and Phylloceratina in the deep waters of the upper continental slope was much larger than in epipelagic Scaphitidae, as in modern fish and squids. Small eggs and high evolutionary rates helped ammonoids to colonise new habitats and develop high biological diversity, but involved them in planktonic food webs making them more vulnerable to abiotic variability (e.g., climatic changes), ultimately leading to their extinction. Large eggs helped nautiloids to persist through geological history, but at the cost of lower biological diversity, lower evolutionary rates and restricted options for colonising new habitats. Large-egged species such as nautiloids are more vulnerable to ecological, biotic disasters such as the appearance of new predators, including modern fishery. Independence from the planktonic food web is likely to be very important for a taxon’s long-term survival over evolutionary history, as demonstrated also by Coelacanthiformes and Elasmobranchia.
Arkhipkin, A. & Laptikhovsky, V. 2012. Impact of oceanic acidification on plankton larvae as cause of mass extinctions in ammonites and belemnites. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 266/1, 39–50.
Baranov, V.N. 1985. Ob ostatkah ikry v zhilyh kamerah pozdnevolzhskih ammonitov. Bulletin Moskovskogo Obshchestva Ispytatelei Prirody, Otdel Geologicheskii 60, 89–91.
Barash, M.S. 2008. Development of Mesozoic ocean biota under influence of abiotic factors. Okeanologiya 48, 583–599.
Brayard, A., Escarguelez, J., Bucher, H., Monnet, C., Briihwiler, T., Goudernand, N., Galfetti, T. & Guexs, J. 2009. Good Genes and Good Luck: Ammonoid Diversity and the End-Permian Mass Extinction. Science 235, 1118–1121.
Chirat, R. 2001. Anomalies in embryonic shell growth in post-Triassic Nautilida. Paleobiology 27, 485–499.
Cichowolski, M., Ambrosio, A. & Concheiro, A. 2005. Nautilids from the Upper Cretaceous of the James Ross Basin, Antarctic Peninsula. Antarctic Science 17, 267–280.
Cushing, D.H. 1974. The possible density dependence of larval mortality in fishes, 103–111. In Blaxter, J.H.S. (ed.) The Early Life History of Fish. Springer-Verlag, New York.
De Baets, K., Klug, C., Korn, D. & Landman, N.H. 2012. Early evolutionary trends in Ammonoid embryonic development. Evolution 66, 1788–1806.
Dera, G., Neige, P., Dommergues, J.-L. & Brayard, A. 2011. Ammonite paleobiogeography during the Pliensbachian–Toarcian crisis (Early Jurassic) reflecting paleoclimate, eustasy, and extinctions. Global and Planetary Change 78, 92–105.
Donnadieu, Y., Pierrehumbert, R., Jacob, R. & Fluteau, F. 2006. Modelling the primary control of paleogeography on Cretaceous climate. Earth and Planetary Science Letters 248, 426–437.
Drushchits, V.V. & Doguzhaeva, L.A. 1981. Ammonity pod elektronnym mikroskopom. 240 pp. Moscow University Press, Moscow.
Emeis, K.-C., Brüchert, V., Currie, B., Endler, R., Ferdelman, T., Kiessling, A., Leipe, T., Noli-Peard, K., Struck, U. & Vogt, T. 2004. Shallow gas in shelf sediments of the Namibian coastal upwelling ecosystem. Continental Shelf Research 24, 627–642.
Etches, S., Clarke, J. & Callomon, J. 2009. Ammonite eggs and ammonitellae from the Kimmeridge Clay Formation (Upper Jurassic) of Dorset, England. Lethaia 42, 204–217.
Föllmi, K.B. 2012. Early Cretaceous life, climate and anoxia. Cretaceous Research 35, 230–257.
Frank, S.A. & Slatkin,M. 1990. Evolution in a variable environment. American Naturalist 136, 244–260.
Friedman, M. 2009. Ecomorphological selectivity among marine teleost fishes during the end-Cretaceous extinction. Proceeding of National Academy of Sciences (PNAS) 106, 5218–5223.
Golonka, J. 2007. Late Triassic and Early Jurassic palaeogeography of the world. Palaeogeography, Palaeoclimatology, Palaeoecology 244, 297–307.
Gradstein, F.M., Ogg, J.G. & Kranendonk, M. van 2008. On the Geologic Time Scale. Newsletters on Stratigraphy 43, 5–13.
Guex, J., Schoene, B., Bartolini, A., Spangenberg, J., Schaltegger, U., O’Dogherty, L., Taylor, D., Bucher, H. & Atudorei, V. 2012. Geochronological constraints on post-extinction recovery of the ammonoids and carbon cycle perturbations during the Early Jurassic. Palaeogeography, Palaeoclimatology, Palaeoecology 346–347, 1–11.
House, M.R. 1996. Juvenile goniatite survival strategies following Devonian extinction events, 163–185. In Hart, M.B. (ed.) Biotic Recovery from Mass Extinction Events. Geological Society of London, Special Publication 102.
Jaeckle, W.B. 2001. Variation in the egg size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development, 49–77. In McEdward, L. (ed.) Ecology of marine invertebrate larvae. CRC Press, London.
Joachimski, M.M., Breisig, S., Buggisch, W., Talent, J.A., Mawson, R., Gereke, M.,Morrow, J.R., Day, J. & Weddige, K. 2009. Devonian climate and reef evolution: Insights from oxygen isotopes in apatite. Earth and Planetary Science Letters 284, 599–609.
Kasyanov, V.L. 1999. Reproductive Strategy in Marine Bivalves and Echinoderms. 229 pp. Oxonian Press, New Delhi.
Klinberg, C.P. 1998. Heterochroby and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews 73, 79–123.
Klug, C. 2001. Life-cycles of some Devonian ammonoids. Lethaia 34, 215–233.
Klug, C., Kröger, B., Kiessling, W.,Mullins, G.L., Servais, T., Frýda, J., Korn, D. & Turner, S. 2010. The Devonian nekton revolution. Lethaia 43, 465–477.
Kurushin, N.I. & Zakharov, V.A. 1995. Triassic climate in the North Siberia. Bulletin of Moscow Society of Naturalists, Geological series 70, 55–60. [in Russian]
Landman, N.H. 1988. Early ontogeny of Mesozoic ammonites and nautilids, 215–228. In Wiedmann, J. & Kullmann, J. (eds) Cephalopods – Present and Past. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart.
Landman, N.H., Cobban, W.A. & Larson, N.L. 2012. Mode of life and habitat of scaphitid ammonites. Geobios 45, 87–98.
Landman, N.H. & Geyssant, J.R. 1993. Heterochrony and ecology in Jurassic and Cretaceous ammonites. Geobios 26, Supplement 1, 247–255.
Landman, N.H., Tanabe, K. & Shigeta,Y. 1996. Ammonoid embryonic development, 343–405. In Landman, N., Tanabe, K. & Davies, R.A. (eds) Topics in Geobiology Volume 13. Ammonoid Paleobiology. Plenum Press, New York.
Laptikhovsky, V.V. 1990. Vidovoy sostav i raspredelenie golovonogih na shelfe i materikovom sklone Namibii. MS stored in VNIERKH 26.01.90 1084-rh90, 20 pp.
Laptikhovsky, V. 1998. Differentiation of reproductive strategies within a taxon, as exemplified by octopods. Ruthenica 8, 77–80.
Laptikhovsky, V. 2006. Latitudinal and bathymetric trends in egg size variation: a new look at Thorson’s and Rass’s rules. Marine Ecology 27, 7–14.
Laptikhovsky, V.V., Arkhipkin, A.I. & Golub, A.A. 1993. Larval age, growth and mortality in the oceanic squid Sthenoteuthis pteropus (Cephalopoda, Ommastrephidae) from the eastern tropical Atlantic. Journal of Plankton Research 15, 375–384.
Laptikhovsky, V., Rogov, M., Nikolaeva, S. & Arkhipkin, A. 2010. Evolutionary significance of cephalopod egg size during mass extinctions, 66. 8th International Symposium, Cephalopods – Present and Past, University of Burgundy & CNRS Dijon – France, August 30–September 3, 2010.
MacArthur, R.H. & Wilson, E.O. 1967. The theory of island biogeography. 203 pp. Princeton University Press, Princeton, New Jersey.
Manda, Š. 2008. Palaeoecology and palaeogeographic relations of the Silurian phragmoceratids (Nautiloidea, Cephalopoda) of the Prague Basin (Bohemia). Bulletin of Geosciences 83, 39–62.
Manda, Š & Frýda, J. 2010. Silurian-Devonian boundary events and their influence on cephalopod evolution: evolutionary significance of cephalopod egg size during the mass extinctions. Bulletin of Geosciences 85, 513–540.
Manda, Š. & Turek, V. 2011. Late Emsian Rutoceratoidea (Nautiloidea) from the Prague Basin, Czech Republic: morphology, diversity and palaecology. Palaeontology 54, 999–1024.
Mapes, R.H. & Nützel, A. 2009. Late Palaeozoic mollusc reproduction: cephalopod egg-laying behavior and gastropod larval palaeobiology. Lethaia 42, 341–356.
Marshall, N.B. 1953. Egg size in Arctic, Antarctic, and deep-sea fishes. Evolution 7, 328–341.
McGowan, A.J. 2004. The effect of the Permo-Triassic bottleneck on Triassic ammonoid morphological evolution. Paleobiology 30, 369–395.
Minelli, A. 2003. The development of animal form: ontogeny, morphology, and evolution. 342 pp. Cambridge University Press.
Moriya, K., Nishi, H., Kawahata, H., Tanabe, K. & Takayanagi, Y. 2003. Demersal habitat of Late Cretaceous ammonoids: Evidence from oxygen isotopes for the Campanian (Late Cretaceous) northwestern Pacific thermal structure. Geology 31, 167–170.
Mutterlose, J., Bornemann, A. & Herrle, J. 2009. The Aptian–Albian cold snap: Evidence for “mid” Cretaceous icehouse interludes. Neues Jahrbuch für Geologie und Paläontologie 252, 217–225.
Nesis, K.N. 1985. Oceanic cephalopod molluscs: distribution, life forms and evolution. 285 pp. Nauka Press, Moscow.
Nesis, K.N. 1995. Mating, spawning and death in oceanic cephalopods: a review. Ruthenica 6, 23–64.
Nigmatullin, C.M. & Laptikhovsky, V.V. 1994. Reproductive strategies in the squid of the family Ommastrephidae (preliminary report). Ruthenica 4, 79–82.
North, A.W. 2001. Early life history strategies of notothenoids at South Georgia. Journal of Fish Biology 58, 496–505.
Pianka, E.R. 1970. On r- and K-selection. American Naturalist 104, 592–597.
Rass, T.S. 1935. Geographische Gesetzmässigkeiten im Bau der Fischeier und Larven. Zoogeographica 3, 90–95.
Riegraf, W. & Shmidt-Riegraf, C. 1995. Mandibula fossiles ammonitorum et nautilorum (Rhyncholithi et rhynchoteuthes, excl. aptychi et anaptychi). In Westphal, E. (ed.) Fossilium Catalogus. I: Animalia. Pars 134. 219 pp. Kugler, Amsterdam.
Ross, C.A., Moore, G.T. & Hayashida, D.N. 1992. Late Jurassic paleoclimate simulation – paleoecological implications for Ammonoid provinciality. Palaios 7, 487–507.
Schlögl, J., Chirat, R., Balter, V., Joachimski, M., Hudáčková, N. & Quillévéré, F. 2011. Aturia from the Miocene Paratethys: an exceptional window on nautilid habitat and lifestyle. Palaeogeography, Palaeoclimatology, Palaeoecology 308, 330–338.
Seilacher, A. & Labarbera, M. 1995. Ammonites as Cartesian divers. Palaios 10, 493–506.
Sewell, M.A. & Young, C.M. 1997. Are echinoderm egg size distribution bimodal? Biological Bulletin 193, 297–305.
Shigeta, Y. 1993. Post-hatching early life history of Cretaceous Ammonoidea. Lethaia 26, 133–145.
Shimanski, V.N. 1975. Melovye Nautiloidei [Cretaceous Nautiloids]. Paleontologicheskii Institut, Trudy 150, 1–208.
Slatkin, M. 1974. Hedging ones evolutionary bets. Nature 250, 704–705.
Stearns, S.C. 1992. The evolution of life histories. 249 pp. Oxford University Press, Oxford.
Stephen, D.A. & Stanton, R.J. Jr. 2002. Impact of reproductive strategy on cephalopod evolution. Abhandlungen der Geologischen Bundesanstalt 57, 151–155.
Sweeney, M.J., Roper, C.F.E.,Mangold, K.M., Clarke, M.R. & Boletzky, S.V. 1992. “Larval” and juvenile cephalopods: A manual for their identification. Smithsonian Contributions to Zoology 513, 1–282.
Tajika, A. & Wani, R. 2011. Intraspecific variation of hatchling size in Late Cretaceous ammonoids from Hokkaido, Japan: implication for planktic duration at early ontogenetic stage. Lethaia 44, 287–298.
Takashima, R., Nishi, H., Huber, B.T. & Leckie, M.R. 2006. Greenhouse world and Mesozoic ocean. Oceanography 19, 82–92.
Teichert, C. 1967. Major features of cephalopod evolution, 162–210. In Teichert, C. & Yochelson, E.L. (eds) Essays in Paleontology and Stratigraphy. Department of Geology, University of Kansas, Special Publication 2.
Thorson, G. 1950. Reproductive and larval ecology of marine invertebrates. Biological Reviews 25, 1–45.
Uchiyama, K. & Tanabe, K. 1999. Hatching experiment of Nautilus macromphalus in the Toba Aquarium, Japan, 13–16. In Oloriz, F. & Tover, F. (eds) Cephalopods – Present and Past. Kluwer Academic/Plenum Pub., New York.
Vance, R.R. 1973a. On reproductive strategies in marine benthic invertebrates. American Naturalist 107, 339–352.
Vance, R.R. 1973b. More on reproductive strategies in marine benthic invertebrates. American Naturalist 107, 353–361.
Wani, R., Kurihara, K. & Ayyasami, K. 2011. The large hatchling size in Cretaceous nautiloids persists across the end-Cretaceous mass extinction: new data on Hercoglossidae hatchlings. Cretaceous Research 32, 618–622.
Ward, P. 1980. Comparative shell shape distributions in Jurassic-Cretaceous ammonites and Jurassic-Tertiary nautilids. Paleobiology 6, 32–43.
Ward, P.D. 1996. Ammonoid extinction, 815–824. In Landman, N.H., Tanabe, K. & Davis, R.A. (eds) Topics in Geobiology. Vol. 13, Ammonoid Paleobiology. Plenum Press, New York.
Ward, P.D. & Bandel, K. 1987. Life history strategies in fossil cephalopods, 329–350. In Boyle, P.R. (ed.) Cephalopod life cycles, Vol. 2. Comparative Reviews. Academic Press, London.
Ward, P.D. & Signor, P.W. 1983. Evolutionary tempo in Jurassic and Cretaceous ammonites. Paleobiology 9, 183–198.
Westermann, G.E.G. 1996. Ammonoid life and habitat, 607–707. In Landman, N., Tanabe, K. & Davies, R.A. (eds) Topics in Geobiology. Vol. 13, Ammonoid Paleobiology. Plenum Press, New York.
Westermann, G.E.G. & Tsujita, C.J. 1999. Life habits of ammonoids, 299–325. In Savazzi, E. (ed.) Functional morphology of invertebrate skeleton. John Wiley & Sons Ltd.
Wierzbowski, H. & Rogov, M. 2011. Reconstructing the palaeoenvironment of the Middle Russian Sea during the Middle–Late Jurassic transition using stable isotope ratios of cephalopod shells and variations in faunal assemblages. Palaeogeography, Palaeoclimatology, Palaeoecology 299, 250–264.
Zakharov, Y.D., Boriskina, N.G., Ignatyev, A.V., Tanabe, K., Shigeta, Y., Popov, A.M., Afanasyeva, T.B. & Maeda, H. 1999. Palaeotemperature curve for the Late Cretaceous of the northwestern circum-Pacific. Cretaceous Research 20, 685–697.