Skip to main content

Intraspecific variation in cephalopod conchs changes during ontogeny: perspectives from three-dimensional morphometry of Nautilus pompilius

  • Amane Tajika (a1), Naoki Morimoto (a2), Ryoji Wani (a3) and Christian Klug (a1)

Intraspecific variation of organisms is of great importance to correctly carry out taxonomic work, which is a prerequisite for key disciplines in paleontology such as community paleoecology, biostratigraphy, and biogeography. However, intraspecific variation is rarely studied in ectocochleate cephalopods (ammonoids and nautiloids), for which an excessive number of taxa was established during the past centuries. Because intraspecific variation of fossilized organisms suffers from various biases (time averaging and taphonomy), an extant example is needed for actualistic comparison. We applied 3D morphometry to 93 specimens of Nautilus pompilius from three different geographic populations. This data set was used to examine the intraspecific variation throughout ontogeny in detail. Although there are slight differences between the populations as well as some measurement biases, a common pattern of intraspecific variation appears to be present. High variation in morphometric variables appears early in ontogeny and then decreases gradually in the following ontogenetic stages. Subsequently, the variation shows an increase again before maturity until a sharp increase or decrease occurs toward the end of ontogeny. Comparison with intraspecific variation of ammonoids and belemnites illustrated that some groups have ontogenetic patterns of intraspecific variation that are similar to that of N. pompilius. This implies that the abovementioned ontogenetic pattern of intraspecific variation might be common in some major cephalopod clades.

Hide All
Arnold J. M., Landman N. H., and Mutvei H.. 1987. Development of the embryonic shell of Nautilus . Pp. 373400. in W. B. Saunders, and N. H. Landman, eds. Nautilus: the biology and paleobiology of a living fossil. Springer, New York.
Bert D. 2014. Factors of intraspecific variability in ammonites, the example of Gassendiceras alpinum (d’Orbigny, 1850) (Hemihoplitidae, Upper Barremian). Annales de Paléontologie 100:217236.
Bonnaud L., Ozouf-Costaz C., and Boucher-Rodoni R.. 2004. A molecular and karyological approach to the taxonomy of Nautilus . Comptes Rendus Biologies 327:133138.
Bush A. M., and Bambach R. K.. 2015. Sustained Mesozoic–Cenozoic diversification of marine Metazoa: a consistent signal from the fossil record. Geology 43:979982.
Courville P., and Crônier C.. 2005. Diversity or disparity in the Jurassic (Upper Callovian) genus Kosmoceras (Ammonitina): a morphometric approach. Journal of Paleontology 79:944953.
Crick R. E. 1978. Morphological variations in the ammonite Scaphites of the Blue Hill member, Carlile Shale, upper Cretaceous, Kansas. University of Kansas Paleontological Contributions, Paper 88.
Dagys A., and Wetschat W.. 1993. Extensive intraspecific variation in a Triassic ammonoid from Siberia. Lethaia 26:113121.
De Baets K., Klug C., and Monnet C.. 2013. Intraspecific variability through ontogeny in early ammonoids. Paleobiology 39:7594.
De Baets K., Bert D., Hoffmann R., Monnet C., Yacobucci M. M., and Klug C.. 2015. Ammonoid intraspecific variability. Pp. 359426. in C. Klug, D. Korn, K. De Baets, I. Kruta, and R. H. Mapes, eds. Ammonoid paleobiology: from anatomy to ecology. Springer, New York.
Dzik J. 1984. Phylogeny of the Nautiloidea. Palaeontologia Polonica 45:1319.
Dzik J. 1985. Typologic versus population concepts of chronospecies: implications for ammonite biostratigraphy. Acta Palaeontologica Polonica 30:12.
Dzik J. 1990. The concept of chronospecies in ammonites. Pp. 2530. in F. Cecca, S. Cresta, G. Pallini, and M. Santantonio, eds. Atti del Secondo Convegno Internazionale Fossili. Evoluzione, Ambiente, Pergola.
Haas O. 1946. Intraspecific variation in, and ontogeny of, Prionotropis woollgari and Prionocyclus wyomingensis . Bulletin of the American Museum of Natural History 86:141224.
Hoffmann R., Schultz J. A., Schellhorn R., Rybacki E., Keupp H., Gerden S. R., Lemanis R., and Zachow S.. 2014. Non-invasive imaging methods applied to neo- and paleo-ontological cephalopod research. Biogeosciences 11:27212739.
Hohenegger J., and Tatzreiter F.. 1992. Morphometric methods in determination of ammonite species, exemplified through Balatonites shells (Middle Triassic). Journal of Paleontology 66:801816.
House M. 1981. Early ammonoids in space and time. In M. House, and J. Senior, eds. The Ammonoidea: the evolution, classification, mode of life and geological usefulness of a major fossil group. Systematics Association Special Volume 18:359367. Academic, London.
House M. 1985. The ammonoid time-scale and ammonoid evolution. Geological Society of London Memoir 10:273283.
House M., and Kerr W.. 1989. Ammonoid extinction events [and discussion]. Philosophical Transactions of the Royal Society of London B 325:307326.
Hughes N. C., and Labandeira C. C.. 1995. The stability of species in taxonomy. Paleobiology 21:401403.
Jacobs D. K., and Landman N. H.. 1993. Nautilus—a poor model for the function and behavior of ammonoids? Lethaia 26:101111.
Jattiot R., Bucher H., Brayard A., Monnet C., Jenks J. F., and Hautmann M.. 2015. Revision of the genus Anasibirites Mojsisovics (Ammonoidea): an iconic and cosmopolitan taxon of the late Smithian (Early Triassic) extinction. Papers in Palaeontology 2:155158.
Kennedy W. J. 1977. Ammonite evolution. Pp. 251304. in A. Hallam, ed. Patterns of evolution. Elsevier, Amsterdam.
Kennedy W. J. 1989. Thoughts on the evolution and extinction of Cretaceous ammonites. Proceedings of the Geologists’ Association 100:251279.
Kennedy W. J., and Cobban W.. 1976. Aspects of ammonite biology, biogeography, and biostratigraphy. Special Papers in Paleontology 17:194.
Kennedy W. J., and Wright C.. 1985. Evolutionary patterns in Late Cretaceous ammonites. Special Papers in. Palaeontology 33:131143.
Kidwell S. M. 2002. Time-averaged molluscan death assemblages: palimpsests of richness, snapshots of abundance. Geology 30:803806.
Klug C. 2001. Life-cycle of Emsian and Eifelian ammonoids (Devonian). Lethaia 34:215233.
Klug C. 2004. Mature modifications, the black band, the black aperture, the black stripe, and the periostracum in cephalopods from the Upper Muschelkalk (Middle Triassic, Germany). Mitteilungen aus dem Geologisch-Paläontologischen Institut der Universität Hamburg 88:6378.
Klug C., Korn D., Landman N. H., Tanabe K., De Baets K., and Naglik C.. 2015a. Describing ammonoid conchs. Pp. 324. in C. Klug, D. Korn, K. De Baets, I. Kruta, and R. H. Mapes, eds. Ammonoid paleobiology: From anatomy to ecology. Topics in geobiology, 43. Springer, Dordrecht, Netherlands.
Klug C., Zatoń M., Parent H., Hostettler B., and Tajika A.. 2015b. Mature modifications and sexual dimorphism. Pp. 261328. in C. Klug, D. Korn, K. De Baets, I. Kruta, and R. H. Mapes, eds. Ammonoid paleobiology: From anatomy to ecology. Topics in geobiology, 43. Springer, Dordrecht, Netherlands.
Korn D. 2017. Goniatites sphaericus (Sowerby, 1814), the archetype of Palaeozoic ammonoids: a case of decreasing phenotypic variation through ontogeny. Paläontologische Zeitschrift 91:337352.
Korn D., and Klug C.. 2007. Conch form analysis, variability, morphological disparity, and mode of life of the Frasnian (Late Devonian) ammonoid Manticoceras from Coumiac (Montagne Noire, France). Pp. 5785. in N. H. Landman, R. A. Davis, and R. H. Mapes, eds. Cephalopods present and past: new insights and fresh perspectives. Springer, Dordrecht, Netherlands.
Korn D., Klug C., and Walton S. A.. 2015. Taxonomic diversity and morphological disparity of Paleozoic ammonoids. Pp. 431464. in C. Klug, D. Korn, K. De Baets, I. Kruta, and R. H. Mapes, eds. Ammonoid paleobiology: From macroevolution to paleogeography. Topics in geobiology, 44. Springer, Dordrecht, Netherlands.
Monnet C., Bucher H., Wasmer M., and Guex J.. 2010. Revision of the genus Acrochordiceras Hyatt, 1877 (Ammonoidea, Middle Triassic): morphology, biometry, biostratigraphy and intra-specific variability. Palaeontology 53:961996.
Naglik C., Monnet C., Goetz S., Kolb C., De Baets K., Tajika A., and Klug C.. 2015. Growth trajectories of some major ammonoid sub-clades revealed by serial grinding tomography data. Lethaia 48:2946.
Nardin E., Rouget I., and Neige P.. 2005. Tendencies in paleontological practice when defining species, and consequences on biodiversity studies. Geology 33:969972.
Palframan D. 1966. Variation and ontogeny of some Oxfordian ammonites: Taramelliceras richei (de Loriol) and Creniceras renggeri (Oppel), from Woodham, Buckinghamshire. Palaeontology 9:290311.
Saunders W. B. 1987. The species of Nautilus . Pp. 3552. in W. B. Saunders, and N. H. Landman, eds. Nautilus: the biology and paleobiology of a living fossil. Springer, New York.
Saunders W. B., and Spinosa C.. 1978. Sexual dimorphism in Nautilus from Palau. Paleobiology 4:349358.
Sepkoski J. J., Bambach R. K., Raup D. M., and Valentine J. W.. 1981. Phanerozoic marine diversity and the fossil record. Nature 293:435437.
Sinclair B., Briskey L., Aspden W., and Pegg G.. 2007. Genetic diversity of isolated populations of Nautilus pompilius (Mollusca, Cephalopoda) in the Great Barrier Reef and Coral Sea. Reviews in Fish Biology and Fisheries 17:223235.
Stevens S. S. 1946. On the theory of scales of measurement. Science 103:677680.
Swan A. R., and Saunders W. B.. 1987. Morphological variation in Nautilus from Papua New Guinea. Pp. 85103. in W. B. Saunders, and N. H. Landman, eds. Nautilus. Plenum, New York.
Tajika A., Morimoto N., Wani R., Naglik C., and Klug C.. 2015. Intraspecific variation of phragmocone chamber volumes throughout ontogeny in the modern nautilid Nautilus and the Jurassic ammonite Normannites . PeerJ 3:e1306.
Tajika A., Kürsteiner P., Pictet A., Lehmann J., Tschanz K., Jattiot R., and Klug C.. 2017. Cephalopod associations and palaeoecology of the Cretaceous (Barremian–Cenomanian) succession of the Alpstein, northeastern Switzerland. Cretaceous Research 70:1554.
Tanabe K., and Shigeta Y.. 1987. Ontogenetic shell variation and streamlining of some Cretaceous ammonites. Transactions and Proceedings of the Paleontological Society of Japan, new series 1987:165179.
Tanabe K., and Tsukahara J.. 1995. Morphological analysis of living Nautilus from Palau. Kagoshima University Research Center for the South Pacific, Occasional Papers 27:41–55.
Tanabe K., Hayasaka S., Saisho T., Shinomiya A., and Aoki K.. 1983. Morphologic variation of Nautilus pompilius from the Philippines and Fiji islands. Kagoshima University Research Center for the South Pacific, Occasional Papers 1:9–21.
Tanabe K., Hayasaka S., and Tsukahara J.. 1985. Morphological analysis of Nautilus pompilius. Kagoshima University Research Center for the South Pacific, Occasional Papers 4:38–49.
Tanabe K., Tsukahara J., and Hayasaka S.. 1990. Comparative morphology of living Nautilus (Cephalopoda) from the Philippines, Fiji and Palau. Malacologia 31:297312.
Vandepas L. E., Dooley F. D., Barord G. J., Swalla B. J., and Ward P. D.. 2016. A revisited phylogeography of Nautilus pompilius . Ecology and Evolution 6:49244935.
Wani R., and Ayyasami K.. 2009. Ontogenetic change and intra-specific variation of shell morphology in the Cretaceous nautiloid (Cephalopoda, Mollusca) Eutrephoceras clementinum (d’Orbigny, 1840) from the Ariyalur area, southern India. Journal of Paleontology 83:365378.
Wani R., Tajika A., Ikuno K., and Iwasaki T.. 2018. Ontogenetic trajectories of septal spacing in early Jurassic belemnites from Germany and France, and their Paleobiological implications. Palaeontology 61:7788.
Ward P. D. 1987. The natural history of. Nautilus . Allen and Unwin, Boston.
Westermann G. E. G. 1996. Ammonoid life and habitat. Pp. 607707. in N. H. Landman, K. Tanabe, and R. A. Davis, eds. Ammonoid paleobiology. Plenum, New York.
Wray C. G., Landman N. H., Saunders W. B., and Bonacum J.. 1995. Genetic divergence and geographic diversification in Nautilus . Paleobiology 21:220228.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0094-8373
  • EISSN: 1938-5331
  • URL: /core/journals/paleobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score

Full text views

Total number of HTML views: 5
Total number of PDF views: 31 *
Loading metrics...

Abstract views

Total abstract views: 220 *
Loading metrics...

* Views captured on Cambridge Core between 24th January 2018 - 22nd February 2018. This data will be updated every 24 hours.