Abstract
Ontogenetic changes in the skull of Lycalopex culpaeus were studied in relation to feeding function and performance at different age classes. Most cranial changes occurred in the orbitotemporal region and consisted of the visible appearance of structures that were later found to be absent in juveniles. These changes were related to the development of the adult skull in order to capture, kill, and process prey. In general, fusion occurred earlier in neurocranial sutures than in the splachnocranium, although rostral sutures never became fused. The cranial sutures of culpeo are conservative, displaying few changes in suture type but some in suture fusion sequence. These modifications occur during the first year, from the late juvenile stages, when individuals are similar to adults in general appearance and body size as well as in skull size. However, it was noted that basicranial synchondroses became fused in the adult stages, indicating that longitudinal growth could extend until this latter time. This could be indicative not only of size change in adult specimens but also of shape change.
I thank David Flores for the permission to study the material under his care; Francisco Prevosti and David Flores for their critical revision of the manuscript and two anonymous reviewers who provided comments and suggestions that greatly improved this article; and Cecilia Morgan and Cynthia Kemp for their revision of the English grammar. I am also grateful to CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas) PIP 01054 and ANPCyT (PICT 2008-1798) for partially funding this research.
Appendix
Appendix 1
Specimens of Lycalopex culpaeus of MACN used in this study.
15022; 15024; 15025; 15028; 15033; 15037; 15040; 15044; 15045; 15049; 15050; 15055; 15062; 15063; 15064; 15073; 15078; 15081; 15082; 15083; 15089; 15093; 15096; 15101; 15106; 15112; 15119; 15121; 15122; 15123; 15124; 15127; 15129; 15130; 15131; 15132; 15133; 15138; 15140; 15149; 15151; 15154; 15158; 15163; 15168; 15172; 15173; 15177; 15180; 15181; 15182; 15190; 15194; 15196; 15197; 15199; 15200; 15201; 15202; 15203; 15208; 15212; 15220; 15223; 15224; 15226; 15227; 15228; 15229; 15232; 15233; 15240; 15243; 15246; 15248; 15258; 15259; 15260; 15261; 15266; 15267; 15268; 23072; 23076; 23077; 23093; 23095; 23098; 23099; 23100; 23101; 23102; 23103; 23104; 23108; 23119; 23123; 23125; 23143; 23148; 23152.
References
Abdala, F., D.A. Flores and N.P. Giannini. 2001. Postweaning ontogeny of the skull of Didelphis albiventris. J. Mammal. 82: 190–200.10.1093/jmammal/82.1.190Search in Google Scholar
Antón, M., M.J. Salesa, J.F. Pastor, I.M. Sánchez, S. Fraile and J. Morales. 2004. Implications of the mastoid anatomy of larger extant felids for the evolution and predatory behaviour of sabretoothed cats (Mammalia, Carnivora, Felidae). Zool. J. Linn. Soc. 140: 207–221.10.1111/j.1096-3642.2003.00093.xSearch in Google Scholar
Biknevicius, A.R. and B. Van Valkenburgh. 1996. Design for killing: craniodental adaptations of predators. In: (J.L. Gittleman, ed.) Carnivore behavior, ecology, and evolution. Cornell University Press, New York. pp. 393–428.Search in Google Scholar
Binder, W.J. and B. Van Valkenburgh. 2000. Development of bite strength and feeding behavior in juvenile spotted hyenas (Crocuta crocuta). J. Zool. 252: 273–283.10.1111/j.1469-7998.2000.tb00622.xSearch in Google Scholar
Crespo, J.A. and J.M. De Carlo. 1963. Estudio ecológico de una población de zorros colorados Dusicyon culpaeus. Rev. Mus. Argent. Cienc. Nat. 1: 1–55.Search in Google Scholar
Drake, A.G. 2011. Dispelling dog dogma: an investigation of heterochrony in dogs using 3D geometric morphometric analysis of skull shape. Evol. Dev. 13: 204–213.10.1111/j.1525-142X.2011.00470.xSearch in Google Scholar
Duckler, G.L. 1998. An unusual osteological formation in the posterior skulls of captive tigers (Panthera tigris). Zoo Biol. 17: 135–142.10.1002/(SICI)1098-2361(1998)17:2<135::AID-ZOO8>3.0.CO;2-ASearch in Google Scholar
Evans, H.E. 1993. Miller’s anatomy of the dog, 3rd edition. W.B. Saunders Company, Philadelphia, PA. pp. 1113.Search in Google Scholar
Ewer, R. 1973. The carnivores. Cornell University Press, Ithaca, NY. pp. 500.Search in Google Scholar
Flores, D.A. and L. Barone. 2012. Cranio-facial sutures of the black-capped squirrel monkey Saimiri boliviensis (Primates: Cebidae): gross morphology and postnatal ontogeny. Mammalia 76: 91–98.10.1515/mamm.2011.103Search in Google Scholar
Flores, D.A., N.P. Giannini and F. Abdala. 2006. Comparative postnatal ontogeny of the skull in an Australidelphian Metatherian Dasyurus albopunctatus (Marsupialia: Dasyuromorpha: Dasyuridae). J. Morphol. 267: 426–440.10.1002/jmor.10420Search in Google Scholar
Flores, D.A., N.P. Giannini and F. Abdala. 2010. Cranial ontogeny of Caluromys philander (Didelphidae: Caluromyinae): a qualitative and quantitative approach. J. Mammal. 91: 539–550.10.1644/09-MAMM-A-291.1Search in Google Scholar
García-Perea, R. 1996. Patterns of postnatal development in skull of lynxes, genus Lynx (Mammalia: Carnivora). J. Morphol. 229: 241–254.Search in Google Scholar
Giannini, N.P., J.R. Wible and N.B. Simmons. 2006. On the cranial osteology of Chiroptera. I. Pteropus (Megachiroptera: Pteropodidae). Bull. Am. Mus. Nat. Hist. 295: 1–134.10.1206/0003-0090(2006)295[0001:OTCOOC]2.0.CO;2Search in Google Scholar
Gilbert, S.G. 1997. Pictorial anatomy of the cat. University of Washington Press, Seattle, WA. pp. 120.Search in Google Scholar
Henderson, J.H., L.Y. Chang, H.M. Song, M.T. Longaker and D.R. Carter. 2005. Age-dependent properties and quasi-static strain in the rat sagittal suture. J. Biomech. 38: 2294–2301.10.1016/j.jbiomech.2004.07.037Search in Google Scholar
Herring, S.W. and S. Teng. 2000. Strain in the braincase and its sutures during function. Am. J. Phys. Anthrop. 112: 575–593.10.1002/1096-8644(200008)112:4<575::AID-AJPA10>3.0.CO;2-0Search in Google Scholar
Herring, S.W., S. Teng, X. Huang, R.J. Mucci and J. Freeman. 1996. Patterns of bone strain in the zygomatic arch. Anat. Rec. 246: 446–457.10.1002/(SICI)1097-0185(199612)246:4<446::AID-AR4>3.0.CO;2-TSearch in Google Scholar
Herring, S.W., K.L. Rafferty, Z J. Liu and C.D. Marshall. 2001. Jaw muscles and the skull in mammals: the biomechanics of mastication. Comp. Biochem. Physiol. 131: 207–219.10.1016/S1095-6433(01)00472-XSearch in Google Scholar
Holton, N.E., R.G. Franciscus, M.A. Nieves, S.D. Marshall, S.B. Reimer, T.E. Southard, J.C. Keller and S.D. Maddux. 2010. Sutural growth restriction and modern human facial evolution: an experimental study in a pig model. J. Anat. 216: 48–61.10.1111/j.1469-7580.2009.01162.xSearch in Google Scholar
Jasinoski, S.C., B.D. Reddy, K.K Louw and A. Chinsamy. 2010. Mechanics of cranial sutures using the finite element method. J. Biomech. 43: 3104–3111.10.1016/j.jbiomech.2010.08.007Search in Google Scholar
Jaslow, C.R. 1990. Mechanical properties of cranial sutures. J. Biomech. 23: 313–321.10.1016/0021-9290(90)90059-CSearch in Google Scholar
Jiménez, J.E. and A.J. Novaro. 2004. Pseudalopex culpaeus (Molina, 1782). In: (C. Sillero-Zubiri, M. Hoffmann and D.W. Macdonald, eds.) Canids: foxes, wolves, jackals and dogs. Status Survey and Conservation Action Plan, IUCN/SSC Canid Specialist Group, Gland, Switzerland. pp. 44–49.Search in Google Scholar
Johnson, W.E. and W.L. Franklin. 1994. Role of body size in the diets of sympatric gray and culpeo foxes. J. Mammal. 75: 163–174.10.2307/1382248Search in Google Scholar
La Croix, S., K.E. Holekamp, J.A. Shivik, B.L. Lundrigan and M.L. Zelditch. 2011a. Ontogenetic relationships between cranium and mandible in coyotes and hyenas. J. Morphol. 272: 662–674.10.1002/jmor.10934Search in Google Scholar
La Croix, S., M.L. Zelditch, J.A. Shivik, B.L. Lundrigan and K.E. Holekamp. 2011b. Ontogeny of feeding performance and biomechanics in coyotes. J. Zool. 285: 301–315.10.1111/j.1469-7998.2011.00847.xSearch in Google Scholar
Leyhausen, P. 1979. Cat behaviour: the predatory and social behaviour of domestic and wild cats. Garland STPM Press, New York. pp. 340.Search in Google Scholar
Mao, J.J. 2002. Mechanobiology of craniofacial sutures. J. Dent. Res. 81: 810–816.10.1177/154405910208101203Search in Google Scholar
Mao, J.J. and H.D. Nah. 2004. Growth and development: hereditary and mechanical modulations. Am. J. Orthod. Dentofac. 125: 676–89.10.1016/j.ajodo.2003.08.024Search in Google Scholar PubMed
Moore, W.J. 1981. The mammalian skull. Cambridge University Press, Cambridge, UK. pp. 369.Search in Google Scholar
Novaro, A.J. 1997. Pseudalopex culpaeus. Mamm. Species 558: 1–8.10.2307/3504483Search in Google Scholar
Rice, D.P. 2008. Craniofacial sutures: development, disease, and treatment. Frontiers of oral biology. Karger, London. pp. 236.Search in Google Scholar
Richmond, F.J.R., D. Thomson and G. Loeb. 1992. Electromyographic studies of neck muscles in the intact cat. Exp. Brain Res. 88: 41–58.10.1007/BF02259127Search in Google Scholar PubMed
Segura, V. and D. Flores. 2009. Aproximación cualitativa y aspectos funcionales en la ontogenia craneana de Puma concolor (felidae). Mastozool. Neotrop. 16: 169–182.Search in Google Scholar
Segura, V. and F. Prevosti. 2012. A quantitative approach to the cranial ontogeny of Lycalopex culpaeus (Carnivora: Canidae). Zoomorphology 131: 79–92.10.1007/s00435-012-0145-4Search in Google Scholar
Slater, G.J., E. Dumont and B. Van Valkenburgh. 2009. Implications of predatory specialization for cranial form and function in canids. J. Zool. 278: 181–188.10.1111/j.1469-7998.2009.00567.xSearch in Google Scholar
Tanner, J.B., M.L. Zelditch, B.L. Lundrigan, K.E. Holekamp. 2010. Ontogenetic change in skull morphology and mechanical advantage in the spotted hyena (Crocuta crocuta). J. Morphol. 271: 353–365.10.1002/jmor.10802Search in Google Scholar PubMed
Travaini, A., J. Juste, A. Novaro and A. Capurro. 2000. Sexual dimorphism and sex identification in the South American culpeo fox, Pseudalopex culpaeus (Carnivora: Canidae). Wildl. Res. 27: 669–674.Search in Google Scholar
Tseng, Z.J. 2009. Cranial function in a late Miocene Dinocrocuta gigantea (Mammalia: Carnivora) revealed by comparative finite element analysis. Biol. J. Linn. Soc. 96: 51–67.10.1111/j.1095-8312.2008.01095.xSearch in Google Scholar
Tseng, Z.J. and X. Wang. 2010. Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia). J. Morphol. 271: 1386–1398.10.1002/jmor.10881Search in Google Scholar PubMed
Van Valkenburgh, B.1991. Iterative evolution of hypercarnivory in canids (Mammalia: Carnivora): evolutionary interactions among sympatric predators. Paleobiology 17: 340–362.10.1017/S0094837300010691Search in Google Scholar
Van Valkenburgh, B. 2007. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integr. Comp. Biol. 47: 147–163.10.1093/icb/icm016Search in Google Scholar PubMed
Van Valkenburgh, B. and K.P. Koepfli. 1993. Cranial and dental adaptations to predation in canids. Symp. Zool. Soc. Lond. 65: 15–37.Search in Google Scholar
Wagemans, P.A., J. Van de Velde, and A. Kuijpers-Jagtman. 1988. Sutures and forces: a review. Am. J. Orthod. Dentofac. 94: 129–141.10.1016/0889-5406(88)90361-7Search in Google Scholar
Wayne, R.K. 1986. Cranial morphology of domestic and wild canids: the influence of development on morphological change. Evolution 40: 243–261.10.1111/j.1558-5646.1986.tb00467.xSearch in Google Scholar PubMed
Wickland, C.R., J. Baker and B. Paterson. 1991. Torque vectors of neck muscles in the cat. Exp. Brain Res. 84: 64–659.10.1007/BF00230978Search in Google Scholar PubMed
Zapata, S.C., M. Funes, A. Novaro. 1997. Estimación de la edad en el zorro colorado patagónico (Pseudalopex culpaeus). Mastozool. Neotrop. 4: 145–150.Search in Google Scholar
©2013 by Walter de Gruyter Berlin Boston
