Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-17T23:08:42.269Z Has data issue: false hasContentIssue false

Development and growth in skulls of three Otariidae species: a comparative morphometric study

Published online by Cambridge University Press:  03 August 2017

Daniela Sanfelice*
Affiliation:
Animal Biology Graduate Program, IB/UFRGS, Building 43435, CEP 91501-970, Porto Alegre, RS, Brazil Instituto Federal de Educação, Ciência e Tecnologia do Rio Grande do Sul- Campus Restinga, Rua Alberto Hoffman, 285 Bairro Restinga CEP: 91791-508 Porto Alegre/RS, Brazil
Daniza Molina-Schiller
Affiliation:
Ecology Graduate Program, IB/UFRGS, Av. Bento Gonçalves, 9500, Bloc IV, Cx. Postal 15007, CEP: 91540-000, Porto Alegre, RS, Brazil
Thales R. O. De Freitas
Affiliation:
Animal Biology Graduate Program, IB/UFRGS, Building 43435, CEP 91501-970, Porto Alegre, RS, Brazil Ecology Graduate Program, IB/UFRGS, Av. Bento Gonçalves, 9500, Bloc IV, Cx. Postal 15007, CEP: 91540-000, Porto Alegre, RS, Brazil Genetics Department, IB/UFRGS, Av. Bento Gonçalves 9500, Cx. Postal 15053, Porto Alegre, RS, Brazil
*
Correspondence should be addressed to: D. Sanfelice, Instituto Federal de Educacão,Ciência e Tecnologia do Rio Grande do Sul- Campus Restinga, Rua Alberto Hoffman, 285 Bairro Restinga CEP: 91791-508 Porto Alegre/RS, Brazil email: daniela.sanfelice@gmail.com

Abstract

We examined the skulls of Arctocephalus australis, Callorhinus ursinus and Otaria byronia with the objectives of (1) estimating the development and growth rates and comparing these parameters among the species; (2) describing the development for each linear measure, for each species and sex; (3) determining which variables are best correlated with age; (4) determining age of physical maturity. We employed traditional and geometric morphometric techniques to study the skulls. In A. australis and C. ursinus, skulls of females mature at about 6 years of age, and those of males at about 8 years. Otaria byronia matures later, at about 9 years. Using geometric morphometric data sets, the rate and constant of growth in A. australis did not differ between the sexes. Callorhinus ursinus and O. byronia showed rates significantly different between sexes concerning growth (and in the constant as well), but only O. byronia differed between sexes in both developmental model parameters (rates and constant). Comparisons between the growth and developmental models showed significant differences in slope and constant. In both treatments employed, a relationship between size and shape dimorphism could be inferred for the skulls of all three species. We conclude that rates or timing of growth and development evolves within a conserved spatiotemporal organization of morphogenesis.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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.)

Footnotes

Current address: casilla 215, Quilpué, Valparaiso, 2430000, Chile.

References

REFERENCES

Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716723.Google Scholar
Alberch, P. (1980) Ontogenesis and morphological diversification. American Zoologist 20, 653667.Google Scholar
Arthur, W. (2002) Mechanisms of morphological evolution. New York, NY: Wiley.Google Scholar
Barreto, A.S. (2000) Variação craniana e genética de Tursiops truncatus (Delphinidae, Cetácea) (Montagu, 1821) na costa Atlântica da América do Sul. PhD thesis. Fundação Universidade Federal do Rio Grande (FURG), Rio Grande, Brazil.Google Scholar
Berta, A. and Churchill, M. (2012) Pinniped taxonomy: review of currently recognized species and subspecies, and evidence used for their description. Mammal Review 42, 207234.Google Scholar
Berta, A. and Sumich, J.L. (1999) Marine mammals – evolutionary biology. New York, NY: Academic Press.Google Scholar
Boness, D.J., Bowen, W.D. and Iverson, S.J. (1985) Does male harassment of females contribute to reproductive synchrony in the grey seal by affecting maternal performance? Behavioral and Ecological Sociobiology 36, 110.Google Scholar
Bookstein, F.L. (1989) Principal warps: thin-plate splines and the decomposition of deformations. I.E.E.E. Transactions on Pattern Analysis and Machine Intelligence 11, 567585.Google Scholar
Bookstein, F.L. (1991) Morphometric tools for landmark data: geometry and biology. New York, NY: Cambridge University Press.Google Scholar
Bookstein, F.L. (1996) Combining the tools of geometric morphometrics. In Marcus, L.F., Corti, M., Loy, A., Nayulor, G.J.P. and Slice, D.E. (eds) Advances in morphometrics. New York, NY: Plenum Press, pp. 131151.Google Scholar
Brunner, S. (2000) Cranial morphometric of fur seals and sea lions (family: Otariidae) – systematics, geographic variation and growth. PhD thesis. University of Sydney, New South Wales, Australia.Google Scholar
Brunner, S. (2004) Cranial ontogeny of otariid seals. Systematics and Biodiversity 1, 339439.Google Scholar
Brunner, S., Bryden, M.M. and Shaughnessy, P.D. (2003) Cranial ontogeny of otariid seals. Systematics and Biodiversity 2, 83110.Google Scholar
Burns, J.J., Fay, F.H. and Fedoseev, G.A. (1984) Craniological analysis of harbor and spotted seals of the North Pacific region. In Fay, F.H. and Fedoseev, G.A. (eds) Soviet-American cooperative research on marine mammals. Volume 1 – pinnipeds. Nagaevskaya: National Oceanic and Atmospheric Administration, U. S. Department of Commerce, pp. 516.Google Scholar
Cappozzo, H.L., Campagna, C. and Monserrat, J. (1991) Sexual dimorphism in newborn southern sea lions. Marine Mammals Science 7, 385394. doi: 10.1111/j.1748-7692.1991.tb00113.x.Google Scholar
Cheverud, J. (1983) Phenotypic, genetic, and environmental integration in the cranium. Evolution 36, 499516.Google Scholar
Committee on Marine Mammals (1967) Standard measurements of seals. Journal of Mammalogy 48, 459462.Google Scholar
Corcuera, J. (1989) Análisis preliminar de la biología reproductiva del lobo marino de dos pelos, Arctocephalus australis (Zimmermann, 1783) (Carnivora, Otariidae). Argentina: Seminario de Licenciatura del Departamento de Ciencias Biológicas, Facultad de Ciências, Universidad de Buenos Aires.Google Scholar
Costa, D.P. and Gentry, R.L. (1986) Free-ranging energetics of northern fur seal. In Gentry, R.L. and Kooyman, G.L. (eds) Fur seals: maternal strategies on land and at sea. Princeton, NJ: Princeton University Press, pp. 70101.Google Scholar
Creighton, G.K. and Strauss, R.E. (1986) Comparative patterns of growth and development in cricetine rodents and the evolution of ontogeny. Evolution 40, 94106.Google Scholar
Dans, S. (1993) Análisis preliminar de la biología reproductiva de algunas especies de mamíferos marinos en el litoral norpatagónico. Argentina: Seminario de Licenciatura en Ciencias Biológicas, Universidade Nacional de Patagonia.Google Scholar
del Castillo, D., Segura, V., Flores, D. and Cappozzo, L. (2016) Cranial development and directional asymmetry in Commerson's dolphin, Cephallorhynchus commersonii: 3D geometric morphometric approach. Journal of Mammalogy 97, 13451354. doi: 10.1093/jmammal/gyw101.Google Scholar
Doidge, D.W., Croxall, J.P. and Ricketts, C. (1984) Growth rates of Antarctic fur seal Arctocephalus gazella at South Georgia. Journal of Zoology 203, 8793.Google Scholar
Drehmer, C.J. and Ferigolo, J. (1997) Osteologia craniana comparada entre Arctocephalus australis e Arctocephalus tropicalis (Pinnipedia, Otariidae). Iheringia, Série Zoologia 83, 137149.Google Scholar
Fedoseev, G.A. (1984) Use of nonmetrical characters of skulls of Bering Sea seals in a study of the phenotypic structure of their populations. In Fay, F.H. and Fedoseev, G.A. (eds) Soviet-American cooperative research on marine mammals. Volume 1 – pinnipeds. Nagaevskaya: National Oceanic and Atmospheric Administration, U. S. Department of Commerce, pp. 4954.Google Scholar
Fiorello, C.V. and German, R.Z. (1997) Heterochrony within species: craniofacial growth in giant, standard, and dwarf rabbits. Evolution 51, 250261.Google Scholar
Gaillard, J.M., Pontier, D., Allaine, D., Lison, A., Herve, J.C. and Heizmann, A. (1997) Variation in growth form and precocity at birth in eutherian mammals. Proceedings of the Royal Society of London B 264, 859868.Google Scholar
Garlich-Miller, J.L. and Stewart, R.E.A. (1998) Growth and sexual dimorphism of Atlantic walruses (Odobenus rosmarus rosmarus) in Foxe Basin, Northwest Territories, Canada. Marine Mammal Science 14, 803818.Google Scholar
Glantz, S.A. (1992) Primer of bio-statistics. New York, NY: McGraw-Hill.Google Scholar
Herring, S.W. (1993) Formation of the vertebrate face: epigenetic and functional influences. American Zoologist 33, 472483.Google Scholar
Higgins, L.V., Costa, D.P., Huntley, A.C. and Le Boeuf, B.J. (1988) Behavior and physiological measurements of the maternal investment in the Steller sea lion, Eumetopias jubatus. Marine Mammal Science 4, 4458.Google Scholar
Hue, E. (1907) MuséeOstéologique. Paris: Librairie C. Reinwald.Google Scholar
Innes, S., Steward, R.E.A. and Lavigne, D.M. (1981) Growth in Northwest Atlantic harp seals, Phoca groenlandica. Journal of Zoology 194, 1124.Google Scholar
Kerley, G.I.H. and Robinson, T.J. (1987) Skull morphometrics of male Antarctic fur seals, Arctocephalus gazella and Arctocephalus tropicalis, and their interspecific hybrids. National Oceanic Atmospheric Administration, Techniques Report National Marine Fisheries Service 51, 121131.Google Scholar
Kingsley, M.C.S. (1979) Fitting the von Bertalanffy growth equation to polar bear age-weight data. Canadian Journal of Zoology 57, 10201025.Google Scholar
Klingenberg, C.P. (1996) Individual variation of ontogenies: a longitudinal study of growth and timing. Evolution 50, 24122428.Google Scholar
Knutsen, L.Ø. and Born, E.W. (1991) Growth body composition and insulative characteristics of Atlantic walruses. Greenland Fisheries Research Institute Manuscript Report 135, 117.Google Scholar
Kovacs, K.M. and Lavigne, D.M. (1986) Maternal investment and neonatal growth in phocid seals. Journal of Animal Ecology 55, 10351051.Google Scholar
Lander, R.H. (1981) A life table and biomass estimate for northern fur seals. Fisheries Research 1, 5570.Google Scholar
Leigh, S.R. (1995) Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates. American Journal of Physical Anthropology 97, 39356.Google Scholar
Leutenegger, W. and Larson, S. (1985) Sexual dimorphism in the postcranial skeleton of New World primates. Folia Primatologica 44, 8295.Google Scholar
Leutenegger, W. and Masterson, T.J. (1989) The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus). Zeitschrift für Morphologie und Anthropologie 78, 1524.Google Scholar
Lima, M. and Páez, E. (1995) Growth and reproductive patterns in the South American fur seal. Journal of Mammalogy 76, 12491255.Google Scholar
Lindenfors, P., Tulberg, B.S. and Biuw, M. (2002) Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behavior and Ecology in Sociobiology 52, 188193.Google Scholar
Mansfield, A.W. (1958) The biology of the Atlantic walrus, Odobenus rosmarus rosmarus (Linnaeus) in the eastern Canadian Arctic. Canadian Fisheries Research Board. Manuscript Report Series (Biology) 653, 13.Google Scholar
Mattlin, R.H. (1981) Pup growth of the New Zealand fur seal, Arctocephalus forsteri on the Open Bay Islands, New Zealand. Journal of Zoology 193, 305314.Google Scholar
Maynard Smith, F.R.S. (1980) Models of evolution. Proceedings of the Royal Society of London B 219, 315325.Google Scholar
McKinney, M.L. and McNamara, K. (1991) Heterochrony – the evolution of ontogeny. New York, NY: Plenum Press.Google Scholar
McLaren, I.A. (1993) Growth in pinnipeds. Biological Review 68, 179.Google Scholar
Misra, R.K. (1986) Fitting and comparing several growth curves of the generalized Von Bertalanffy type. Canadian Journal of Fisheries and Aquatic Sciences 43, 16561659.Google Scholar
Molina-Schiller, D.M.M. (2000) Idade e desenvolvimento craniano do lobo-marinho-do-sul, Arctocephalus australis (Zimmermann, 1783) (Carnivora: Otariidae), no litoral do Rio Grande do Sul, Brasil. Master's thesis. Fundação Universidade Federal do Rio Grande (FURG), Rio Grande, Brazil.Google Scholar
Molina-Schiller, D.M.M. and Pinedo, M.C. (2004a) Using canine teeth for sex determination of the South American fur seal, Arctocephalus australis. Latin American Journal of Aquatic Mammals 3, 1924.Google Scholar
Molina-Schiller, D.M.M. and Pinedo, M.C. (2004b) Growth and skull development in the South American fur seal, Arctocephalus australis (Zimmermann, 1783) (Carnivora: Otariidae), from Rio Grande do Sul coast, Brazil. Latin American Journal of Aquatic Mammals 3, 95105.Google Scholar
Oliveira, L.R., Hingst-Zaher, E. and Morgante, J.S. (2005) Size and shape sexual dimorphism in the skull of the South American fur seal, Arctocephalus australis (Zimmermann, 1783) (Carnivora: Otariidae). Latin American Journal of Aquatic Mammals 4, 2740.Google Scholar
Parsons, K.J., Robinson, B.W. and Hrbek, T. (2003) Getting into shape: an empirical comparison of traditional truss-based morphometric methods with a newer geometric method applied to new world cichlids. Environmental Biology of Fishes 67, 417. doi: 10.1023/A:1025895317253.Google Scholar
Perrin, W.F. and Myrick, A.C. Jr (1980) Age determination of toothed whales and sirenians. Cambridge: International Whaling Commission.Google Scholar
Pierce, K.V. and Kajimura, H. (1980) Acid etching and highlighting for defining growth layers in cetacean teeth. In Perrin, W.F. and Myrick, A.C. Jr (eds) Age determination of toothed whales and sirenians. Cambridge: International Whaling Commission, pp. 99103.Google Scholar
Press, W.H., Teukolsky, S.A., Etterling, W.T. and Flannery, B.P. (1992) Numerical recipes. The art of scientific computing. New York, NY: Cambridge University Press.Google Scholar
Ramos, R.M.A., Di Beneditto, A.P., Siciliano, S., Santos, M.C.O., Zerbini, A.N., Bertozzi, C., Vicente, A.F.C., Zampirolli, E., Alvarenga, F.S. and Lima, N.R.W. (2002) Morphology of the Franciscana (Pontoporia blainvillei) off southeastern Brazil: sexual dimorphism, growth and geographic variation. Latin American Journal of Aquatic Mammals 1, 129144.Google Scholar
Richtsmeier, J.T., Corner, B.D., Grausz, H.M., Cheverud, J.M. and Danahey, S.E. (1993) The role of postnatal growth pattern in the production of facial morphology. Systematic Biology 42, 307330.Google Scholar
Riedman, M. (1990) The pinnipeds: seals, sea lions and walruses. Berkeley, CA: University of California Press.Google Scholar
Rosas, F.C.W. (1989) Aspectos da dinâmica populacional e interações com a pesca, do leão marinho do sul, Otária flavescens (Shaw, 1800) (Pinnipedia, Otariidae), no litoral sul do Rio Grande do Sul, Brasil. Master's thesis. Fundação Universidade Federal do Rio Grande (FURG), Rio Grande, Brazil.Google Scholar
Rosas, F.C.W. and Barreto, A. (2003) Age and growth of the estuarine dolphin (Sotalia guianensis) (Cetacea, Delphinidae) on the Paraná coast, southern Brazil. Fishery Bulletin 101, 377383.Google Scholar
Rosas, F.C.W., Haimovici, M. and Pinedo, M.C. (1993) Age and growth of the South American sea lion, Otaria flavescens (Shaw, 1800), in southern Brazil. Journal of Mammalogy 74, 141147.Google Scholar
Sanfelice, D. and de Freitas, T.R.O. (2008) A comparative description of dimorphism in skull ontogeny of Arctocephalus australis, Callorhinus ursinus, and Otaria byronia (Carnivora: Otariidae). Journal of Mammalogy 89, 336346.Google Scholar
Schiavini, A.C., Lima, M.M. and Batallés, L.M. (1992) Growth structures of maxillary canines of the Southern fur seal (Arctocephalus australis). Marine Mammals Science 8, 8993.Google Scholar
Shea, B.T. (1986) Ontogenetic approaches to sexual dimorphism in anthropoids. Human Evolution 1, 97110.Google Scholar
Sheets, D.H. (2000) Integrated morphometric softwares (IMP) – mathworks, MATLAB6. Natick, MA: The Mathworks.Google Scholar
Stewart, R.E.A. (1994) Size-at-age relationships as discrimination of white whale (Delphinateus leucas Pallas 1776) stocks in the eastern Canadian Arctic. Bioscience 39, 217226.Google Scholar
Stuart, L.J. and Morejohn, G.V. (1980) Developmental patterns in osteology and external morphology in Phocoena phocoena. Reports of the International Whaling Commission Special Issue 3, 133142.Google Scholar
Tanner, J.M. (1963) Regulation of growth in size in mammals. Nature 199, 845850.Google Scholar
Tarnawski, B.A., Cassini, G.H. and Flores, D.A. (2013) Skull allometry and sexual dimorphism in the ontogeny of the southern elephant seal (Mirounga leonina). Canadian Journal of Zoology 92, 1931.Google Scholar
Tarnawski, B.A., Cassini, G.A. and Flores, D.A. (2014) Allometry of the postnatal cranial ontogeny and sexual dimorphism in Otaria byronia (Otariidae). Acta Theriologica 58, 8197. doi: 10.1007/s13364-012-0124-7.Google Scholar
Trillmich, F. (1996) Parental investment in pinnipeds. In Rosenblatt, J.S. and Snowdon, C.T. (eds) Parental care: evolution, mechanisms, and adaptive significance. San Diego, CA: Academic Press, pp. 533577.Google Scholar
Vaz-Ferreira, R. and Ponce De Léon, A. (1987) South American fur seal, Arctocephalus australis, in Uruguay. In Croxall, J. and Gentry, R.L. (eds) Status, biology and ecology of fur seals. Proceedings of an international symposium and workshop, Cambridge, UK, 23–27 April 1984. NOAA Technical Reports. NMFS 51, pp. 165168.Google Scholar
Wiig, O. and Lie, R.W. (1984) An analysis of the morphological relationships between the hooded seals (Cystophora cristata) of Newfoundland, the Denmark Strait, and Jan Mayen. Zoological Society of London B 203, 227240.Google Scholar
Wyss, A.R. (1987) The walrus auditory region and the monophyly of the pinnipeds. American Museum Novitates 2871, 131.Google Scholar
Ximénez, I., Lima, M., Ponce de León, A., Batallés, L.M. and Malek, A. (1984) Estudio estadístico de relaciones craneales en el ‘lobo fino’ sudamericano, Arctocephalus australis (Zimmermann, 1783). Anales de la Industria lobera y pesquera (ILPE) 1, 133.Google Scholar
Zelditch, M.L., Fink, W.L. and Swiderski, D.L. (2001) The spatial complexity and evolutionary dynamics of growth. In Zelditch, M.L. (ed.) Beyond heterochrony: the evolution of development. New York, NY: Wiley, pp. 145194.Google Scholar
Zelditch, M.L., Lundrigan, B.L., Sheets, D.H. and Theodore, G. Jr (2003) Do precocial mammals develop at a faster rate? A comparison of rates of skull development in Sigmodon fulviventer and Mus musculus domesticus. Journal of Evolutionary Biology 16, 708720.Google Scholar
Zelditch, M.L., Swiderski, D.L., Sheets, H.D. and Fink, W.L. (2004) Geometric morphometrics for biologists: a primer. New York, NY: Elsevier Academic Press.Google Scholar
Zullinger, E.M., Ricklefs, R.E., Redford, K.H. and Mace, G.M. (1984) Fitting sigmoidal equations to mammalian growth curves. Journal of Mammalogy 65, 607636.Google Scholar